Encyclopedia of Entomology

Encyclopedia of Entomology

Edited by
John L. Capinera
University of Florida

Second Edition

Volume 4
SZ
Professor John L. Capinera
Dept. Entomology and Nematology
University of Florida
Gainesville FL 326110620
USA

Library of Congress Control Number: 2008930112

ISBN: 978-1-4020-6242-1
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Editorial Board
Cyrus Abivardi Eugene J. Gerberg
Swiss Federal Institute of Technnoloy University of Florida
Donald R. Barnard Donald W. Hall
United States Department of Agriculture University of Florida
Jean-Luc Boev Marjorie A. Hoy
Royal Belgian Institute of Natural Sciences University of Florida
Drion Boucias John B. Heppner
University of Florida Florida State Collection of Arthropods
Paul. M. Choate Pauline O. Lawrence
University of Florida University of Florida
Whitney Cranshaw Heather J. McAuslane
Colorado State University University of Florida
Thomas C. Emmel James L. Nation
University of Florida University of Florida
J. Howard Frank Herb Oberlander
University of Florida United States Department of Agriculture
Severiano F. Gayubo Frank B. Peairs
Universidad de Salamanca Colorado State University
Acknowledgments
This project is the labor of many people, including some who labored diligently behind the scenes.
Among those to whom I am greatly indebted for their behind-the-scenes assistance are Pam Howell and
Carole Girimont (first edition) and Pam Howell (second edition) for document processing and editing
assistance; Mike Sanford, Pat Hope, and Jane Medley (first edition) and Hope Johnson (second edition)
for assistance with the images, and Marsha Capinera for compiling the list of contributors. Ron Cave,
Andrei Sourakov, and Lyle Buss helped greatly by supplying numerous photographs for the second
edition.
Howard Frank deserves special mention for his editing acumen and assistance. Drion Boucias con-
tributed the lengthy unattributed sections on insect pathology. The unattributed biographic sketches
with last names beginning with A to J were contributed by Howard Frank. All other unattributed
sections were contributed by John Capinera.
Preface
Some biologists have called this the Age of Insects. Among animals, certainly the diversity of insects is
unrivaled. Nearly one million species have been described to date, and some entomologists estimate that
as the tropics are fully explored, we will find that there are actually more than three million insect spe-
cies. The large number of insects is often attributed to the divergence of plants (angiosperms), which
provide numerous hosts and places to feed, but if plant feeders are excluded from the tabulation the
biodiversity of insects remains unrivaled. Virtually every environment has been exploited by these resil-
ient organisms. Even if one dislikes insects, they are impossible to ignore, and a little knowledge about
them could be indispensable should one have a close encounter of an unpleasant kind.
Insects are remarkable biological organisms. They are small enough to escape the detailed scrutiny
of most people, but I have yet to meet anyone whom, once provided the opportunity to examine insects
closely (through a microscope) is not completely amazed by the detail and complexity of these exqui-
sitely designed (by natural selection) beasties. They are fascinating in function as well as form. Insects are
the only invertebrates to fly, they are disproportionately strong, and their ecological adaptability defies
belief. For example, some insects produce their own version of anti-freeze, which allows them to be fro-
zen solid yet to regain normal function upon thawing. Their sensory abilities are beyond human com-
prehension; a male insect can sometimes locate a female by her perfume (pheromone) from several
kilometers distance. Although not normally considered intelligent, insects display surprisingly complex
behaviors, and altruistic social systems that could well serve as models for human societies.
Insects and their close relatives are important for many reasons besides their sheer diversity. Their
effect on humans is profound. Insects are our chief competitor for food and fiber resources throughout
the world. Annual crop losses of 10 to 15% are attributed to insects, with both pre-harvest and post-
harvest losses considerably more at times. Insects also are the principal vector of many human, animal,
and plant diseases, including viruses, mollicutes, bacteria, fungi, and nematodes. The ability to transmit
diseases magnifies their effect, and makes it more difficult to manage injury. Over the course of human
history, insect-transmitted disease has caused untold human suffering. For example, introduction of
flea-transmitted bubonic plague to Europe centuries ago killed millions of people and caused severe
disruption to western civilization. Though less dramatic, mosquito-transmitted malaria kills thousands
annually throughout the world, and unlike plague, which is now mostly a historical footnote, the toll
continues to mount.
Advances in technology, particularly the introduction of chemical insecticides, have done much to
remove the threat of insect-related damage from the consciousness of most humans. Insecticides are
applied preventatively to avoid pre- and post-harvest damage to crops, to our dwellings, and to our land-
scape. This is an oft-overlooked but remarkable achievement that has increased stability in the supply
and price of resources, and in the lives of resource producers. No longer are people faced with starvation
or economic ruin due to the ravages of insects; in almost all parts of the world, the ready availability of
insecticides can be used to prevent massive insect population outbreaks. However, we realize increas-
ingly that this approach is not without its own set of health, environmental and economic costs, and
alleviating dependency on insecticides, or making alternatives to insecticides more readily available, has
assumed greater priority.
x
Preface

We are faced with an interesting dichotomy. There is a wealth of information about insects, but it is
known mostly to insect scientists (entomologists). The public (non-entomologists or 99.99% of all peo-
ple) has little knowledge about insects, and poor access to vital information about these important
organisms. So this encyclopedia is presented to bridge the gap to better enable those with a need to
know to find fundamental information provided by more than 450 experts in the field of entomology.
We provide a broad overview of insects and their close relatives, including taxonomy, behavior, ecology,
physiology, history, and management. Importantly, we provide critical links to the entomological litera-
ture, much of which presently is unavailable for search electronically. The contributors are distinguished
entomologists from around the world. They hope that the availability of this encyclopedia will help oth-
ers to reap the benefits of centuries of discovery, and to discover the wonders that make the study of
insects so compelling. It was constructed with college and university students in mind, but others may
find it a handy reference.

John L. Capinera, Gainesville (Florida) April, 2008

Highlights of the Encyclopedia of
Entomology
Major Taxa of Insects and Their Stoneflies (Plecoptera)
Near Relatives Stylopids (Strepsiptera)
Symphylans (Symphyla)
Alderflies and Dobsonflies (Megaloptera) Termites (Isoptera)
Angel Insects (Zoraptera) Thrips (Thysanoptera)
Bark-Lice, Book-Lice, or Psocids (Psocoptera) Ticks (Ixodida)
Beetles (Coleoptera) Wasps, Ants, Bees, and Sawflies (Hymenoptera)
Bristletails (Archeognatha) Webspinners (Embiidina)
Bugs (Hemiptera)
Butterflies and Moths (Lepidoptera)
Caddisflies (Trichoptera) Other Groups
Centipedes (Chilopoda)
Chewing and Sucking Lice (Phthiraptera) Anagrus Fairyflies (Hymenoptera: Mymaridae)
Cockroaches (Blattodea) Ants (Hymenoptera: Formicidae)
Diplurans (Diplura) Aphids (Hemiptera: Aphididae)
Dragonflies and Damselflies (Odonata) Apoid Wasps (Hymenoptera: Apoidea:
Earwigs (Dermaptera) Spheciformes)
Fleas (Siphonaptera) Argasid (Soft) Ticks (Acari: Ixodida: Argasidae)
Flies (Diptera) Assassin Bugs, Kissing Bugs and Others
Gladiators (Mantophasmatodea) (Hemiptera: Reduviidae)
Grasshoppers, Katydids, and Crickets Bark Beetles, Dendroctonus spp. (Coleoptera:
(Orthoptera) Curculionidae: Scolytinae)
Lacewings, Antlions, and Mantispids Bees (Hymenoptera: Apoidea: Apiformes)
(Neuroptera) Bess Beetles (Coleoptera: Passalidae)
Mayflies (Ephemeroptera) Biting Midges, Culicoides (Diptera:
Millipedes (Diplopoda) Ceratopogonidae)
Mites (Acari) Black Flies (Diptera: Simuliidae)
Pillbugs and Sowbugs, or Woodlice (Isopoda) Blister Beetles (Coleoptera: Meloidae)
Praying Mantids (Mantodea) Bulb Mites, Rhizoglyphus (Acari: Acaridae)
Proturans (Protura) Burnet Moth Biology (Lepidoptera:
Rock Crawlers (Grylloblattodea) Zygaenidae)
Scorpionflies (Mecoptera) Brush-Footed Butterflies (Lepidoptera:
Scorpions (Scorpiones) Nymphalidae)
Sea Spiders (Pycnogonida) Butterflies (Lepidoptera: Rhopalocera)
Silverfish (Zygentoma) Carpenter Bees (Hymenoptera: Apidae:
Snakeflies (Raphidioptera) Xylocopinae)
Spiders (Araneae) Carrion Beetles (Coleoptera: Silphidae)
Springtails (Collembola) Cicadas (Hemiptera: Cicadoidea)
Stick and Leaf Insects (Phasmida) Clearwing Moths (Lepidoptera: Sesiidae)
xii
Highlights of the Encyclopedia of Entomology

Coreid Bugs and Relatives: Coreidae, Marine Insects and the Sea-Skater Halobates
Stenocepahidae, Alydidae, Rhopalidae, and (Hemiptera: Gerridae)
Hyocephalidae (Hemiptera: Coreoidea) Metalmark Butterflies (Lepidoptera: Riodinidae)
Crane Flies (Diptera: Tipulidae and Others) Microdon spp. (Diptera: Syrphidae)
Dance Flies, Balloon Flies, Predaceous Flies Minute Pirate Bugs (Hemiptera: Anthocoridae)
(Diptera: Empidoidea, exclusive of Mosquitoes (Diptera: Culicidae)
Dolichopodidae) Moths (Lepidoptera: Heterocera)
Darkling Beetles (Coleoptera: Tenebrionidae) Nuttalliellidae (Acari)
Earwigflies (Mecoptera: Meropeidae) Orchid Bees (Hymenoptera: Apidae)
Fairyflies (Hymenoptera: Mymaridae) Parasitic Hymenoptera (Hymenoptera: Parasitica)
Fireflies (Coleoptera: Lampyridae) Paederus Fabricius (Coleoptera: Staphylinidae:
Flea Beetles (Coleoptera: Chrysomelidae: Paederinae)
Alticinae) Pelecinid Wasps (Hymenoptera: Pelecinidae)
Four-Legged Mites (Eriophyoidea or Tetrapodili) Periodical Cicadas, Magicicada spp. (Hemiptera:
Fruit Flies (Diptera: Tephritidae) Cicadidae)
Fungus Gnats (Diptera: Mycetophilidae and Phytoseiid Mites (Acari: Phytoseiidae)
Others) Powderpost Beetles (Coleoptera: Bostrichidae:
Gall Midges (Diptera: Cecidomyiidae) Lyctinae)
Gall Wasps (Hymenoptera: Cynipidae) Pine Tip Moths, Rhyacionia spp. (Lepidoptera:
Giant Water Bugs (Hemiptera: Belostomatidae) Tortricidae)
Greater Fritillaries or Silverspots, Speyeria [= Plant Bugs (Hemiptera: Miridae)
Argynnis] (Lepidoptera: Nymphalidae) Planthoppers (Hemiptera: Fulgoroidea)
Ground Beetles (Coleoptera: Carabidae): Plume Moths (Lepidoptera: Pterophoridae)
Taxonomy Powderpost Beetles (Coleoptera: Bostrichidae:
Harvester Ants, Pogonomyrmex (Hymenoptera: Lyctinae)
Formicidae) Predatory Stink Bugs (Hemiptera: Pentatomidae:
Horse Flies and Deer Flies (Diptera: Tabanidae) Asopinae)
Jerusalem Crickets (Orthoptera: Riffle Beetles (Coleoptera: Elmidae)
Stenopelmatidae) Robber Flies (Diptera: Asilidae)
Jumping Spiders (Arachnida: Araneae: Salticidae) Rove Beetles (Coleoptera: Staphylinidae)
June Beetles, Phyllophaga spp. (Coleoptera: Sac Spiders (Arachnida: Araneae: Tengellidae,
Scarabaeidae: Melolothinae: Melolothini) Zorocratidae, Miturgidae, Anyphaenidae,
Katydids (Orthoptera: Tettigoniidae) Clubionidae, Liocranidae, and Corinnidae)
Kissing Bugs (Hemiptera: Reduviidae: Triatominae) Sap Beetles (Coleoptera: Nitidulidae)
Lace Bugs (Hemiptera: Tingidae) Sawflies (Hymenoptera: Symphyta)
Ladybird Beetles (Coccinellidae: Coleoptera) Sawflies (Hymenoptera: Tenthredinidae)
Leaf Beetles (Coleoptera: Chrysomelidae) Scale Insects and Mealybugs (Hemiptera:
Leaf-Cutting Ants (Formicidae: Myrmicinae: Coccoidea)
Attini) Scarab Beetles (Coleoptera: Scarabaeoidea)
Leaf-Miner Flies (Diptera: Agromyzidae) Skin-Piercing and Blood-Feeding Moths, Calyptra
Leafhoppers (Hemiptera: Cicadellidae) spp. (Lepidoptera: Noctuidae: Calpinae)
Longicorn, Longhorned, or Round-Headed Soil Mites (Acari: Oribatida and Others)
Beetles (Coleoptera: Cerambycidae) Spittlebugs (Hemiptera: Cercopoidea)
Long-Legged Flies (Diptera: Dolichopodidae) Spongillaflies (Neuroptera: Sisyridae)
Mantidflies (Neuroptera: Mantispidae) Stilt Bugs (Hemiptera: Berytidae)
 Highlights of the Encyclopedia of Entomology
xiii

Stink Bugs (Hemiptera: Pentatomidae), Alarm Pheromones

Emphasizing Economic Importance Alary Muscles
Tachinid Flies (Diptera: Tachinidae) Alimentary Canal and Digestion
Tent Caterpillars, Malacosoma spp. (Lepidoptera: Biological Clock of the German Cockroach,
Lasiocampidae) Blattella germanica (L.)
Tiger Beetles (Coleoptera: Carabidae: Collyrinae Chordotonal Sensory Organs
and Cicindelinae) Corazonin
Termites (Isoptera) in South America Cryptobiosis
Tiphiid Wasps (Hymenoptera: Tiphiidae) Diapause
Treehoppers (Hemiptera: Membracidae) Dorsal Vessel: Heart and Aorta
Underwing Moths Catocala (Lepidoptera: Ecdysone Agonists, a Novel Group of Insect
Noctuidae) Growth Regulators
Velvet Ants (Hymenoptera: Mutillidae) Ecdysteroids
Water Penny Beetles (Coleoptera: Psephenidae) Embryogenesis
Weevils, Billbugs, Bark Beetles, and Others Endocrine Regulation of Insect Reproduction
(Coleoptera: Curculionoidea) Eyes and Vision
Weta (Orthoptera: Anostostomatidae, Fatty Acid Binding Proteins
Rhaphidophoridae) Fireflies: Control of Flashing
Whiteflies (Hemiptera: Aleyrodidae) Hemocytes in Insects: Their Morphology and
Function
H-Organ
Morphology and Anatomy Immunity
Integument: Structure and Function
Abdomen of Hexapods Entomopathogenic Fungi and Their Host Cuticle
Antennae of Hexapods Juvenile Hormone
Head of Hexapods Learning in Insects: Neurochemistry and
Internal Anatomy of Insects Localization of Brain Function
Alimentary Canal and Digestion Locomotion and Muscles
Legs of Hexapods Metamorphosis
Mouthparts of Hexapods Midgut and Insect Pathogens
Thorax of Hexapods Multifunctional Semiochemicals
Wings of Insects Nervous System
Eggs of Insects Neurological Effects of Insecticides and the Insect
Nervous System Nervous System
Eyes and Vision Nutrition in Insects
Integument: Structure and Function Oogenesis
Nygma Pheromones
Wing Coupling Polyphenism in Insects and Juvenile Hormone
(JH)
Prothoracicotropic Hormone
Physiology Reflex Bleeding
Regulation of Sex Pheromone Production in
Accessory Pulsatile Hearts Moths
Adipokinetic and Hypertrehalosemic Reproduction
Neurohormones Reselin
xiv
Highlights of the Encyclopedia of Entomology

Sex Attractant Pheromones Arthropod-Associated Plant Effectors (AAPEs):

Social Insect Pheromones Elicitors and Suppressors of Crop Defense
Sound Production in the Cicadoidea Attraction of Insects to Organic Sulfur
Storage Proteins Compounds in Plants
Storage Protein Receptors Blister Beetle Antennal Twisting Behavior
Stress-Induced Host Plant Free Amino Acids and Construction Behavior of Insects
Insects Crypsis
Taste and Contact Chemoreception Cycloalexy
Tracheal System and Respiratory Gas Exchange Deflection Marks
Ultrastructure of Insect Sensilla Deimatic Behavior
Venoms and Toxins in Insects Drumming Communication and Intersexual
Venoms of Ectoparasitic Wasps Searching Behavior of Stoneflies
Venoms of Endoparasitic Wasps (Plecoptera)
Vitellogenesis Environmental Influences on Behavioral
Water Balance Development in Insects
Facultative Predators
Flash Colors
Genetics Glowworms
Gregarious Behavior in Insects
Bacteriophage WO Hilltopping
Behavior of Insects: Genetic Analysis by Crossing Host Location in Parasitic Wasps
and Selection Host Plant Selection by Insects
Behavior: Molecular Genetic Analyses Inverted Copulation
Genetic Modification of Drosophila By P Learning in Insects
Elements Marking Insects for Studying Ecology and
Genetic Sexing Behavior
Genetic Transformation Mosquito Oviposition
Genomes of Insects Multifunctional Semiochemicals
Homeotic Genes in Coleoptera Myrmecomorphy
Honey Bee Sexuality: A Historical Perspective Myrmecophiles
Meiotic Drive in Insects Parental Care in Heteroptera (Hemiptera:
Molecular Diagnosis Heteroptera)
Polytene Chromosomes Puddling Behavior in Butterflies
Sex Ratio Modification by Cytoplasmic Agents Red Imported Fire Ant Territorial Behavior
Sibling Species Reflex Bleeding
Transgenic Arthropods for Pest Management Sociality of Insects
Programs Sound Production in the Cicadoidea
RNA Interference Sphragis
Spider Behavior and Value in Agricultural
Landscapes
Behavior Thermoregulation in Insects
Vibrational Communication
Acoustic Communication in Insects Visual Mating Signals
Acoustical Communication in Heteroptera Walking Stick Defensive Behavior and
(Hemiptera: Heteroptera) Regeneration of Appendages
 Highlights of the Encyclopedia of Entomology
xv

Ecology and Evolution Insectivorous Plants

Life Tables
Mimicry
Adaptation of Indigenous Insects to Introduced Mosquito Larval Feeding Ecology
Crops Mosquito Overwintering Ecology
Allelochemicals Natural Enemy Attraction to Plant
Ant-Plant Interactions Volatiles
Aposematism Night Blooming Plants and Their Insect
Arthropod-Associated Plant Effectors Pollinators
(AAPEs): Elicitors and Suppressors of Nutrient Content of Insects
Crop Defense Outbreaks of Insects
Bioclimatic Models in Entomology Overwintering in Insects
Biogeography Phase Polymorphism in Locusts
Brachelytry Phylogenetics
Bromeliad Fauna Phytotelmata
Cannibalism Plant Extrafloral Nectaries
Carnivorous Plants Plant Secondary Compounds and Phytophagous
Carnivory and Symbiosis in the Purple Insects
PitcherPlant Pollination and Flower Visitation
Castes Pollination by Osmia Bees (Hymenoptera:
Cave Adapted Insects Megachilidae)
Cave Habitat Colonization Pollination by Yucca Moths
Chemical Ecology of Insects Pollution and Terrestrial Arthropods
Cold Tolerance in Insects Polyphenism
Conservation of Insects Polyacetylenes and Their Thiophene
Cryptobiosis Derivatives
Decomposer Insects Predation: The Role of Generalist Predators
Diapause inBiodiversity and Biological
Eggs of Insects Control
Endophytic Fungi and Grass-Feeding Pyrophilous Insects
Insects Pyrrolizidine Alkaloids and Tiger Moths
Food Habits of Insects (Lepidoptera: Arctiidae)
Fossil Record of Insects Retournement and Deversement of the
Furanocoumarins Aedeagusin Coleoptera
Gall Formation Rhythms of Insects
Galpagos Islands Insects: Colonization, Seed Predation by Insects
Structure, and Evolution Sexual Selection
Geological Time Sociality of Insects
Glowworms Species Concepts
Gregarious Behavior in Insects Speciation Processes Among Insects
Ground Beetle (Coleoptera: Carabidae) Symbiosis Between Planthoppers and
FeedingEcology Microorganisms
Hypertely Trichomes and Insects
Hypericin Tritrophic Interactions
Inquilines and Cleptoparasites Water Pollution and Insects
xvi
Highlights of the Encyclopedia of Entomology

Microbiology and Pathology Nosema disease

Nomuraea
Microbial Control of Insects Orcytes virus and other Nudiviruses
Microbial Control of Medically Important Paecilomyces
Insects Paenibacillus
Symbionts of Insects Parvoviruses
Symbiosis Between Planthoppers and Polydnaviruses
Microorganisms Reoviruses
Symbiotic Viruses of Parasitic Wasps Rhabdoviruses
Fungal Pathogens in Insects Septobasidium
Entomopathogenic Fungi and Their Host Cuticle Serratia entomophila
Midgut and Insect Pathogens Small RNA viruses of invertebrates
Immunity Sorosporella
Pathogens of Whiteflies (Hemiptera: Trichomycetes
Aleyrodidae)
Diseases Of Grasshoppers and Locusts
Nematode Parasites of Insects Humans and Insects
Nematomorphs (Nematomorpha)
Entomopathogenic Nematodes and Insect Apiculture (Beekeeping)
Management Aquatic Entomology and Flyfishing
Thrips-Parasitic Nematodes Butterfly Counts
American Foulbrood Butterfly Gardening
Amoebae Careers in Entomology
Ascosphaera apis Collecting and Preserving Insects
Ascoviruses Common (Vernacular) Names of Insects
Bacillus sphaericus Conservation of Insects
Bacillus thuringiensis Costs and Benefits of Insects
Baculoviruses Cultural Entomology
Beauveria Entomodeltiology
Birnaviruses Entomophagy: Human Consumption of Insects
Cestodes Forensic Entomology
Coelomomyces History and Insects
Culicinomyces Honeybee Sexuality: An Historical Perspective
Entomophthorales Identification of Insects
Entomopoxviruses (Poxviruses) Insects as Aphrodisiacs
Granulovirus Invasive Species
Helicosporium Lacquers and Dyes From Insects
Hirsutella Literature and Insects
Iridoviruses Maggot Therapy
Laboulbeniales Marking Insects for Studying Ecology and
Lagenidium giganteum Behavior
Lecanicillium Midges as Human Food
Metarhizium Mythology and Insects
Microsporidia (Phylum Microsporidia) Native American Culture and Insects
Nosema locustae (Protozoa: Microsporidia) Popularity of Insects
 Highlights of the Encyclopedia of Entomology
xvii

Pronunciation of Scientific Names and Terms Bokor, Elemr

Psychiatry And Insects: Phobias and Delusions of Bonnet, Charles
Insect Infestations in Humans Borgmeier, Thomas
Rearing of Insects Bving, Adam Giede
Scientific Names and Other Words From Latin Brauer, Friedrich Moritz
and Greek Broun, Thomas
Sericulture Bruch, Carlos
Silk Brues, II, Charles Thomas
Teaching and Training in Entomology: Institu- Brull, Gaspard Auguste
tional Models Brunner von Wattenwyl, Carl
Teaching Entomology: A Review of Techniques Buffon, Georges Louis Leclerc (Comte de)
Burgess, Albert Franklin
Burmeister, Carl Hermann Conrad
Notable and Pioneer Buxton, Patrick Alfred
Entomologists Calvert, Philip Powell
Cameron, Malcolm
Abafi-Aigner, Lajos (Ludwig Aigner) Candze, Ernest Charles Auguste
Abbott, John Carpenter, Frank Morton
Agassiz, Jean Louis Rodolphe Carter, Herbert James
Aldrovandi, Ulisse (Ulysse, Ulysses) Casey, Thomas Lincoln
Alexander, Charles Paul Caudell, Andrew Nelson
Amerasinghe, Felix P. Chagas, Carlos Justiniano Ribeiro
Andrewartha, Herbert George Chaudoir, Maximilien Stanislavovitch de
Arnett, Jr., Ross Harold Champion, George Charles
Audinet-Serville, Jean-Guillaume Chapman, Reginald Frederick
Audouin, Jean-Victor Chevrolat, Louis Alexandre Auguste
Barber, Herbert Spencer Chiang, Huai C.
Bates, Henry Walter China, William Edward
Bates, Marston Chittenden, Frank Hurlbut
Beck, Stanley Dwight Christophers, (Sir) Samuel Rickard
Beklemishev, Vladimir NikolayevicH Cockerell, Theodor Dru Alison
Bell, William J. Comstock, John Henry
Becquaert, Joseph Charles Coquillett, Daniel William
Berlese, Antonio Craw, Alexander
Bernhauer, Max Cresson, Ezra Townsend
Bertram, Douglas Somerville Criddle, Norman
Br, Lajos Crotch, George Robert
Blackburn, Thomas Crowson, Roy Albert
Blackwelder, Richard Elliot Csiki, Erno (Ernst Dietl)
Blaisdell, Frank Ellsworth Curran, Charles Howard
Blatchley, Willis Stanley Curtis, John
Bodenheimer, Friedrich (Frederick) Simon Cushman, Robert Asa
Bohart, Richard M. Cuvier, (Baron) Georges Lopold Chretien
Boheman, Carl Heinrich Frdric Dagobert
Boisduval, Jean-Baptiste Alphonse Dechauffour Dahlbom, Anders Gustav
xviii
Highlights of the Encyclopedia of Entomology

Darlington, Jr., Philip J. Frivaldszky, Jnos

Darwin, Charles Froggatt, Walter Wilson
Davis, William Thompson Gahan, Arthur Burton
Debach, Paul Ganglbauer, Ludwig
Degeer, Carl (Carolus, Karl, Charles) Germar, Ernst Friedrich
Dejean, Pierre Franois Marie Auguste Ghilarov, Mercury Sergeevich
Dethier, Vincent Gaston Girault, Alexandre Arsne
Dobzhansky, Theodosius Grigorievich Glover, Townend
Donisthorpe, Horace St. John Kelly Gmelin, Johann Friedrich
Douglas, John William Goeldi, Emil (Emilio) August
Drake, Carl John Gorgas, William Crawford
Dudich, Endre Graham, Marcus William Robert de Vere
Dufour, Lon Jean Marie Grassi, Giovanni Battista
Duponchel, Philogne August-Joseph Gravenhorst, Johan Ludwig Christian
Dyar, Harrison Grey Gressitt, Judson Linsley
Edwards, William Henry Grote, Augustus Radcliffe
Eickwort, George C. Guene, Achille
Emerson, Alfred Edwards Gurin-Mneville, Flix Edouard
Endrdi, Seb (Sebastian Endrdi) Gundlach, Johannes (Juan) Christopher
Endrdy-Younga, Sebastian (Sebestyn Gyllenhal, Leonhard
Endrdy-Younga, Sebestyn Endrdy) Haddow, Alexander John
Erichson, Wilhelm Ferdinand Hagen, Hermann August
Esaki, Teiso Hagen, Kenneth Sverre
Evans, Howard Ensign Hahn, Carl Wilhelm
Fabre, Jean-Henri Casimir Hale Carpenter, Geoffrey Douglas
Fabricius, Johann Christian Haliday, Alexander Henry
Fairchild, Alexander Graham Bell Handlirsch, Anton
Fairmaire, Lon Hansen, Viktor
Fall, Henry Clinton Harris, Thaddeus William
Fauvel, Charles Adolphe Albert Hatch, Melville Harrison
Felt, Ephraim Porter Heer, Oswald
Fenichel, Smuel Henneguy, Louis Flix
Fennah, Ronald Gordon Hennig, Willi
Fernald, Charles Henry Herman, Ott
Ferris, Gordon Floyd Herrich-Schffer, Gottlieb August
Fischer Von Waldheim, Gotthelf Hewitt, Charles Gordon
Fitch, Asa Hinton, Howard Everest
Fletcher, James Hobby, Bertram Maurice
Foote, Richard H. Hocking, Brian
Forbes, Stephen Alfred Hogstraal, Harry O.
Ford, Edmund Brisco Holland, William Jacob
Forel, Auguste Henri Hope, Frederick William
Fourcroy, Antoine-Franois (Comte de) Hopkins, Andrew Delmar
Frisch, K. von Horn, George Henry
Frivaldszky, Imre Horn, Hermann Wilhelm Walther
 Highlights of the Encyclopedia of Entomology
xix

Horsfall, William R. Maskell, William Miles

Howard, Leland Ossian Masters, George
Hbner, Jacob Matheson, Robert
Huffaker, Carl Barton Matsumura, Shonen
Hungerford, Herbert Barker Mcdunnough, James Halliday
Ihering, Hermann Von Mcglashan, Charles Fayette
Imms, Augustus Daniel Meigen, Johann Wilhelm
Jacquelin du Val, Pierre Nicolas Camille Mellanby, Kenneth
Jeannel, Ren Melander, Axel Leonard
Johannsen, Oskar Augustus Melsheimer, Frederick Valentine
Jordan, Heinrich Ernst Karl Mntris, Edouard
Kaszab, Zoltn Metcalf, Clell Lee
Kellogg, Vernon Lyman Metcalf, Zeno Payne
Kennedy, John S. Meyrick, Edward
Kershaw, John Crampton Wilkinson Miller, David
Kevan, Douglas Keith McEwan Mlachlan, Robert
Kiesenwetter, Ernst August Hellmuth von Morgan, Thomas Hunt
Kirby, William Morrison, Herbert Knowles
Klee, Waldemar G. Morse, Albert Pitts
Knipling, Edward Fred Motschulsky, Victor Ivanovich
Koebele, Albert Mller, Johann Friedrich Theodor
Kraatz, Ernst Gustav Mller, Josef
Kring, James Burton Mulsant, Etienne
Lamarck, Jean-Baptiste Needham, James George
Latreille, Pierre Andr Newell, Wilmon
Lea, Arthur Mills Newman, Edward.
Lea, H. Arnold Newsom, Leo Dale
LeConte, John Lawrence Olivier, Guillaume Antoine
Leech, Hugh Bosdin Ormerod, Eleanor Anne
Lefroy, Harold Maxwell Osborn, Herbert
Leng, Charles William Osten Sacken, C.R.
Lepeletier, Amde Louis Michel Packard, Alpheus Spring
Lindroth, Carl H. Painter, Reginald Henry
Linnaeus, Carolus (Linn, Carl von) Palm, Thure
Linsley, Earle Gorton Pass, Bobby Clifton
Loew, Hermann Patch, Edith Marion
Lorguin, Pierre Joseph Michel Paykull, Gustaf
Lugger, Otto Peairs, Leonard Marion
Macleay (Sir) William John Peck, William Dandridge
Macquart, Pierre Justin Marie Petrunkevitch, Alexander
Mallis, Arnold Pickett, Allison Deforest
Mann, William M. Pomerantsev, Boris Ivanovich
Mannerheim, Carl Gustav von Potter, Charles
Marlatt, Charles Lester Prokopy, Ronald J.
Marx, George Provancher, (labb) Lon
xx
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Putzeys, Jules Antoine Adolphe Henri Stern, Vernon M.

Rabb, Robert Lamar Swammerdam, Jan
Radoshkowsky, Octavius John Swezey, Otto Herman
de Raumur, Ren Antoine Ferchault Szent-Ivny, Jzsef Gyula Hubertus
Redi, Francesco Thomas, Cyrus
Redtenbacher, Ludwig Thomson, Carl Gustav
Reed, Walter. Thunberg, Carl Peter
Rehn, James Abram Garfield Tillyard, Robin John
Reitter, Edmund Torre-Bueno, Jos Rollin De La
Remington, Charles Lee Townes, Jr., Henry K.
Rey, Claudius Treherne, John E
Richards, Owain Westmacott Uhler, Philip Reese
Riley, Charles Valentine Usinger, Robert Leslie
Robineau-Desvoidy, Jean Baptiste Uvarov, (Sir) Boris Petrovich
Rondani, Camillo Van Den Bosch, Robert
Rosen, David Van Duzee, Edward Payson
Ross, Herbert Holdsworth Varley, George C
Rothschild, Miriam Viereck, Henry Lorenz
Roubal, Jan Walker, Francis
Sabrosky, Curtis Waloff, Nadejda
Sahlberg, Carl Reinhold Walsh, Benjamin Dann
Sailer, Reece I. Walsingham, (Lord) Thomas de Gray
Sanderson, Dwight Wasmann, Erich
Saunders, William Wesmael, Constantin
Saussure, Henri Louis Frederic de Westwood, John Obadiah
Say, Thomas Wheeler, William Morton
Scheerpeltz, Otto Wiedemann, Christian Rudolph Wilhelm
Schneiderman, Howard Allen Wigglesworth, (Sir) Vincent Brian
Schwarz, Eugene Amandus Williams, Carroll Milton
Scudder, Samuel Hubbard Williston, Samuel Wendell
Selys-Longchamps, Michel Edmond de Wirth, Willis Wagner
Sharp, David Wolcott, George N.
Shelford, Victor Ernest Wollaston, Thomas Vernon
Signoret, Victor Antoine Young, Jr., David A
Silvestri, Filippo Zeller, Philipp Christoph
Sylveira Caldeira, Joo da Zetterstedt, Johann Wilhelm
Smirnoff, Vladimir A. Zachvatkin (Jasykov), Aleksei Alekseevich
Smith, John Bernhardt
Smith, Harry Scott
Smith, Ray F. Pest Management
Snodgrass, Robert Evans
Snow, Francis Huntington Integrated Pest Management (IPM)
Spielman, Andrew Economic Injury Level (EIL) and Economic
Stl, Carl Threshold (ET) Concepts in Pest
Steinhaus, Edward Arthur Management
 Highlights of the Encyclopedia of Entomology
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Costs and Benefits of Insects Augmentative Biological Control

Methods for Measuring Crop Losses by Insects Classical Biological Control
Sampling Arthropods Conservation Biological Control
Traps for Capturing Insects Natural Enemies Important in Biological Control
Scale and Hierarchy in Integrated Pest Mass Rearing of Natural Enemies
Management Culture of Natural Enemies on Factitious Foods
Phenology Models for Pest Management and Artificial Diets
Agroecology Classical Biological Control of Chestnut Gall
Organic Agriculture Wasp in Japan
Regulatory Entomology Conservation of Ground Beetles in
Regulations Affecting the Implementation of Annual Crops
Regulatory Entomology Practices Filth Fly Parasitoids (Hymenoptera:
Invasive Species Pteromalidae) in North America
Pest Risk Analysis Carabid Beetles (Coleoptera: Carabidae) as
Mechanical Protection of Humans from Parasitoids
Arthropod Attacks and Bites History of Biological Control of Wheat Stem
Repellents of Biting Flies Sawflies (Hymenoptera: Cephidae)
Physical Management of Insect Pests Parasitism of Lepidoptera Defoliators in
Kaolin-Based Particle Films for Arthropod Sunflower and Legume Crops, and A djacent
Control Vegetation in the Pampas of Argentina
Controlled Atmosphere Technologies for Insect Transmission of Plant Diseases by Insects
Control Plant Viruses and Insects
Cultural Control of Insects Management of Insect-Vectored Pathogens of
Plant Resistance to Insects Plants
Resistance of Solanaceous Vegetables to Insects Transmission of Xylella fastidiosa Bacteria by
Cover, Border and Trap Crops for Pest and Xylem-Feeding Insects
Disease Management Vectors of Phytoplasmas
Polyculture
Microbial Control of Insects
Visual Attractants and Repellents in IPM Pesticides and Pesticide
Push-Pull Strategy for Insect Pest Management Application
Area-Wide Insect Pest Management
Sterile Insect Technique Acaricides or Miticides
Filter Rearing System for Sterile Insect Boric Acid
Technology DDT
Weeds in Crop Systems for Pest Suppression Insecticides
Biological Control of Weeds Insecticide Application: The Dose Transfer
Weed Biological Control in Australia Process
Biological Control of Invasive Plants in Latin Food-Based Poisoned Baits for Insect Control
America Soil Fumigation
Host Specificity of Weed-Feeding Insects Structural Fumigation
Foreign Exploration for Insects that Feed on Insecticide Bioassay
Weeds Insecticide Formulation
Flower Strips as Conservation Areas for Pest Insecticide Resistance
Management Insecticide Toxicity
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Pesticide Hormoligosis Maize (Corn) Pests and Their Management

Synergism Mite Pests of Crops in Asia
Chronotoxicology Musk Thistle Suppression Using Weevils For
Detoxification Mechanisms in Insects Biological Control
Enhanced Biodegradation of Soil-Applied Palm Insects
Pesticides Pests and Their Natural Enemies (Parasitoids
Pesticide Resistance Management and/or Predators) in The Middle East
Natural Products Used for Insect Control Potato Pests and Their Management
Botanical Insecticides School IPM, or Pest Management on School
Chinaberry, Melia azedarach, a Biopesticidal Tree Grounds
Pyrethrum and Persian Insect Powder Shade Tree Arthropods and Their Management
Neem Small Fruit Pests and Their Management
Horticultural Oils Stored Grain and Flour Insects and Their
Soaps as Insecticides Management
Diatomaceous Earth Sugarcane Pests and Their Management
Photodynamic Action in Pest Control and Sweetpotato Weevils and Their Eradication
Medicine Programs in Japan
Neurological Effects of Insecticides and the Insect Tropical Fruit Pests and Their Management
Nervous System Turfgrass Insects of the United States and Their
Regulations Affecting Use of Pesticides Management
Urban Entomology
Vegetable Pests and Their Management
Pests Groups and Their Veterinary Pests and Their Management
Management Wheat Pests and Their Management
Whitefly Bioecology and Management in Latin
Agricultural Crop Pests in Southeast Asia America
Including South China Wood-Attacking Insects
Alfalfa (Lucerne) Pests and Their Management
Apple Pests and Their Management
Banana Pests and Their Management Medical and Veterinary
Bark Beetles in The Genus Dendroctonus Entomology
Cassava Pests and Their Management
Citrus Pests and Their Management African Horse Sickness Viruses
Coffee Pests and Their Management Argasid (Soft) Ticks (Acari: Ixodida: Argasidae)
Crucifer Pests and Their Management Avian (Bird) Malaria
Desert Locust, Schistocerca gregaria Forskl Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)
(Orthoptera: Acrididae) Plagues Biting Midges, Culicoides spp. (Diptera:
Grasshoppers and Locusts as Agricultural Pests Ceratopogonidae)
Grasshoppers of the Argentine Pampas Black Flies Attacking Livestock: Simulium
Grasshopper and Locust Pests in Africa arcticum Malloch and Simulium luggeri
Grasshopper and Locust Pests in Australia Nicholson & Mickel (Diptera: Simuliidae)
Grasshopper Pests in North America Bluetongue Disease
Gramineous Lepidopteran Stem Borders in Bovine Hypodermosis: Phenology in Europe
Africa Brown Dog Tick, Rhipicephalus sanguineus
Mahogany Pests and Their Management (Latreille) (Acari: Ixodida: Ixodidae)
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Cat Flea, Ctenocephalides felis felis Bouch Rocky Mountain Wood Tick, Dermacentor
(Siphonaptera: Pulicidae) andersoni Stiles (Acari: Ixodidae)
Chagas, Carlos Justiniano Ribeiro Rodent Trypanosomiasis: A Comparison
Chagas Disease or American Trypanosomiasis Between Trypanosoma lewisi and
Chagas Disease: Biochemistry of the Vector Trypanosoma musculi
Chikungunya Simulium spp. Vectors of Onchocerca volvulus
Chironomids as a Nuisance and of Medical Skin-Piercing and Blood-Feeding Moths,
Importance Calyptra spp. (Lepidoptera: Noctuidae:
Cockroaches and Disease Calpinae)
Dermatitis Linearis Sleeping Sickness or African Trypanosomiasis
Dengue St. Louis Encephalitis
Dirofilariasis Sugar-Feeding in Blood-Feeding Flies
Eastern Equine Encephalitis Taiga Tick, Ixodes persulcatus Schulze (Acari:
Horse Flies and Deer flies Ixodida: Ixodidae)
House Fly, Musca domestica L. (Diptera: Tick Paralysis
Muscidae) Ticks (Ixodida)
Human Botfly, Dermatobia hominis (Linneaus, Ticks as Vectors of Pathogens
Jr.) (Diptera: Oestridae) Trypanosomes
Human Lice Tsetse Flies, Glossina spp. (Diptera: Glossinidae)
Human Lymphatic Filariasis (Elephantiasis) Types of Pathogen Transmission by Arthropods
Human Scabies Vector Capability of Blood-Sucking Arthropods:
Hypodermosis in Deer A Forecasting Matrix
Japanese Encephalitis Venoms And Toxins in Insects
La Crosse Encephalitis West Nile Fever
Leishmaniasis Yellow Fever
Lyme Borreliosis
Maggot Therapy
Malaria Arthropods of Economic
Mechanical Protection of Humans from Arthro- Importance
pod Attacks and Bites
Microbial Control of Medically African Armyworm, Spodoptera exempta
Important Insects (Lepidoptera: Noctuidae)
Mites (Acari) African Honey Bee, Africanized Honey Bee, or
Mosquitoes (Diptera: Culicidae) Killer Bee, Apis mellifera scutellata Lepeletier
Mosquitoes as Vectors of Viral Pathogens (Hymenoptera: Apidae)
Mosquito Oviposition African Mahogany-Feeding Caterpillar,
Myiasis Heteronygmia dissimilis Aurivillius
Onchocerciasis (Lepidoptera: Lymantriidae)
Paederina African Pine-Feeding Grasshopper, Plagiotriptus
Pederin pinivorus (Descamps) (Orthoptera:
Pathogen Transmission by Arthropods Eumastacidae)
Piroplasmosis: Babesia and Theileria Alfalfa Leafcutting Bee, Megachile rotundata
Reed, Walter Fabricius (Hymenoptera: Megachilidae)
Repellents of Biting Flies Allegheny Mound Ant, Formica exsectoides Foretl
Rocky Mountain Spotted Fever (Hymenoptera: Formicidae)
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American Grasshopper, Schistocerca americana Cabbage Looper, Trichoplusia ni (Hbner)

(Drury) (Orthoptera: Acrididae) (Lepidoptera Noctuidae)
Almond Seed Wasp, Eurytoma amygdali Cabbageworm, Pieris rapae (Linnaeus)
Enderlein (Hymenoptera: Eurytomidae) (Lepidoptera: Pieridae)
American Serpentine Leafminer, Liriomyza Cactus Moth, Cactoblastis cactorum (Berg)
trifolii (Burgess) (Diptera: Agromyzidae) (Lepidoptera: Pyralidae)
Argentine Ant, Linepithema humile (Mayr), Cape Honey Bees, Apis mellifera capensis Escholtz
(Hymenoptera: Formicidae: Cassava Mealybug, Phenacoccus manihoti
Dolichoderinae) Matile-Ferrero (Hemiptera:
Army Cutworm, Euxoa auxiliaris (Grote) Pseudococcidae)
(Lepidoptera: Noctuidae) Chilli Thrips, Scirtothrips dorsalis Hood
Armyworm, Pseudaletia unipuncta (Haworth) (Thysanoptera: Thripidae)
(Lepidoptera: Noctuidae) Chinch Bug, Blissus leucopterus (Say) (Hemiptera:
Asian Citrus Psyllid, Diaphorina citri Kuwayama Blissidae)
(Hemiptera: Psyllidae) Cluster Fly, Pollenia rudis (Fabricius) and
Asparagus Aphid, Brachycorynella asparagi P.pseudorudis Rognes (Diptera:
(Mordvilko) (Hemiptera: Aphididae) Calliphoridae)
Aster Leafhopper, Macrosteles quadrilineatus Coconut Mite, Aceria guerreronis (Acari:
Forbes (Hemiptera: Cicadellidae) Eriophyidae)
Australian Sheep Blowfly, Lucilia cuprina Coffee Berry Borer, Hypthenemus hampei
Wiedemann (Diptera: Calliphoridae) (Ferrari) (Coleoptera: Curculionidae:
Banana Weevil, Cosmopolites sordidus (Germar) Scolytinae)
(Coleoptera: Curculionidae) Colorado Potato Beetle, Leptinotarsa
Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) decemlineata (Say) (Coleoptera:
Bee Louse, Bee Fly, or Braulid, Braula coeca Chrysomelidae)
Nitzsch (Diptera: Braulidae) Corn Delphacid, Peregrinus maidis (Ashmead)
Beet Armyworm, Spodoptera exigua (Hbner) (Hemiptera: Delphacidae)
(Lepidoptera: Noctuidae) Corn Earworm, Helicoverpa zea (Boddie)
Bertha Armyworm, Mamestra configurata Walker (Lepidoptera: Noctuidae)
(Lepidoptera: Noctuidae) Corn Leaf Aphid, Rhopalosiphum maidis (Fitch)
Black Cutworm, Agrotis ipsilon (Hufnagel) (Hemiptera: Aphididae)
(Lepidoptera: Noctuidae) Corn Leafhopper, Dalbulus maidis (Delong And
Black Fig Fly, Silba adipata McAlpine (Diptera: Wolcott) (Hemiptera: Cicadellidae)
Lonchaeidae) Cotton Leafworm, Spodoptera littoralis
Bogong moth, Agrotis infusa (Boisduval) (Boisduval)
(Lepidoptera: Noctuidae) Crapemyrtle Aphid Sarucallis kahawaluokalani
Boll Weevil, Anthonomus grandis Boheman (Kirkaldy) (Hemiptera: Aphididae)
(Coleoptera: Curculionidae) Date Palm Stem Borer, Pseudophilus testaceus
Brown Citrus Aphid, Toxoptera citricida Gah. (= Jebusea hammershmidti Reiche)
(Kirkaldy) (Hemiptera: Aphididae) (Coleoptera: Cerambycidae)
Cabbage Aphid, Brevicoryne brassicae (L.) Diamondback Moth, Plutella xylostella
(Hemiptera: Aphididae) (Linnaeus) (Lepidoptera: Plutellidae)
Cabbage Maggot or Cabbage Root Fly, Delia radi- Diaprepes Root Weevil, Diaprepes abbreviatus
cum (Linnaeus) (Diptera: Anthomyiidae) (L.) (Coleoptera: Curculionidae)
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Differential Grasshopper, Melanoplus differentialis Greater Date Moth, Arenipses sabella Hmps
(Thomas) (Orthoptera: Acrididae) (Lepidoptera: Pyralidae)
Douglas-Fir Beetle, Dendroctonus pseudotsugae Greenhouse Whitefly, Trialeurodes vaporariorum
pseudotsugae Hopkins (Coleoptera: (Westwood) (Hemiptera: Aleyrodidae)
Curculionidae, Scolytinae) Green Peach Aphid, Myzus persicae (Sulzer)
Driver Ants (Dorylus Subgenus Anomma) (Hemiptera: Aphididae)
(Hymenoptera: Formicidae) Gypsy Moth, Lymantria dispar Linnaeus
Dubas Bug (Old World Date Bug), Ommatissus (Lepidoptera: Lymantriidae)
binotatus (Hemiptera: Tropiduchidae) Harlequin Bug, Murgantia histrionica (Hahn)
Eastern Lubber Grasshopper, Romalea microptera (Hemiptera: Pentatomidae)
(Beauvois) (Orthoptera: Acrididae) Hazelnut and Walnut Twig Borer, Oberea
Elm Leaf Beetle, Xanthogaleruca (= Pyrrhalta) linearis Linnaeus (Coleoptera:
luteola (Mller) (Coleoptera: Cerambycidae)
Chrysomelidae) Hessian Fly, Mayetiola destructor (Say) (Diptera:
Eri Silkworm, Philosamia ricini (Lepidoptera: Cecidomyiidae)
Saturniidae) Honey Bee, Apis mellifera Linnaeus
Eurasian Spruce Bark Beetle, Ips typographus (Hymenoptera: Apidae)
Linnaeus (Coleoptera: Curculionidae, Horn Fly, Haematobia irritans (L.) (Diptera:
Scolytinae) Muscidae)
European Cherry Fruit Fly Rhagoletis cerasi House Fly, Musca domestica L. (Diptera:
(Linnaeus) (Diptera: Tephritidae) Muscidae)
European Corn Borer, Ostrinia nubilalis (Hbner) Human Botfly, Dermatobia hominis (Linneaus,
(Lepidoptera: Pyralidae) Jr.) (Diptera: Oestridae)
European Earwig, Forficula auricularia Linnaeus Japanese Beetle, Popillia japonica Newman
(Dermaptera: Forficulidae) (Coleoptera: Scarabaeidae)
Face Fly, Musca autumnalis De Geer (Diptera: Jewel Wasp, Nasonia vitripennis (Walker)
Muscidae) (Hymenoptera: Pteromalidae)
Fall Armyworm, Spodoptera frugiperda (J.E. Khapra Beetle, Trogoderma granarium Everts
Smith) (Lepidoptera: Noctuidae) (Coleoptera: Dermestidae)
Formosan Subterranean Termite, Coptotermes Large Milkweed Bug, Oncopeltus fasciatus
formosanus Shiraki (Isoptera: (Dallas) (Hemiptera: Lygaeidae)
Rhinotermitidae) Large Cabbage White Butterfly,
Fruit Stalk Borer, Oryectes elegans Prell Pieris brassicae (Linnaeus) (Lepidoptera:
(Coleoptera: Scarabaeidae) Pieridae)
Gamagrass Leafhopper Dalbulus quinquenotatus Larger Grain Borer, Prostephanus truncatus
Delong & Nault (Hemiptera: (Horn) (Coleoptera: Bostrichidae)
Cicadellidae) Leaf-Cutting Ants (Formicidae: Myrmicinae:
Glassy-Winged Sharpshooter, Homalodisca Attini)
vitripennis (Hemiptera: Cicadellidae) Lesser Date Moth, Batrachedra amydraula
Grape Phylloxera, Daktulosphaira vitifoliae Meyrick (Lepidoptera: Cosmopterygidae)
(Fitch) (Hemiptera: Aphidoidea: Lettuce Root Aphid, Pemphigus bursarius
Phylloxeridae) (Linnaeus) (Hemiptera: Aphididae)
Grapevine Leafhopper Complex (Hemiptera: Locust Borer, Megacyllene robiniae (Forster)
Cicadellidae) in Cyprus (Coleoptera: Cerambycidae)
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Lovebug, Plecia nearctica Hardy (Diptera: Onion Maggot, Delia antiqua (Meigen) (Diptera:
Bibionidae) Anthomyiidae)
Mango Mealybug, Rastrococcus invadens Williams Oriental Fruit Fly, Bactrocera dorsalis (Hendel)
(Hemiptera: Pseudococcidae) (Diptera: Tephritidae)
Mediterranean Fruit Fly Ceratitis capitata Pea Aphid, Acyrthosiphon pisum (Harris)
(Wiedemann) (Diptera: Tephritidae) (Hemiptera: Aphididae)
Melon Aphid, Aphis gossypii Glover (Hemiptera: Pea Leafminer, Liriomyza huidobrensis
Aphididae) (Blanchard) (Diptera: Agromyzidae)
Melon Fly, Bactrocera cucurbitae (Coquillett) Pear Psylla, Cacopsylla pyricola (Foerster)
(Diptera: Tephritidae) (Hemiptera: Psyllidae)
Melon Thrips, Thrips palmi Karny (Thysanoptera: Pepper Weevil, Anthonomus eugenii Cano
Thripidae) (Coleoptera: Curculionidae)
Melonworm, Diaphania hyalinata Linnaeus Phoracantha Longicorn Beetles (Coleoptera:
(Lepidoptera: Pyralidae) Cerambycidae)
Mexican Bean Beetle, Epilachna varivestris Pickleworm, Diaphania nitidalis (Stoll)
Mulsant (Coleoptera: Coccinellidae) (Lepidoptera: Pyralidae)
Migratory Grasshopper, Melanoplus sanguinipes Pine Weevil, Hylobius abietis (Coleoptera:
(Fabricius) (Orthoptera: Acrididae) Curculionidae)
Mole Crickets (Orthoptera: Gryllotalpidae) and Pink Hibiscus Mealybug, Maconellicoccus
Their Biological Control hirsutus Green (Hemiptera:
Monarch Butterfly, Danaus plexippus Linnaeus Pseudococcidae)
(Lepidoptera: Danaidae) Pistachio Seed Wasps, Eurytoma plotnikovi
Mormon Cricket, Anabrus simplex Haldeman Nikolskaya (Hymenoptera: Eurytomidae)
(Orthoptera: Tettigoniidae) and Megastigmas pistaciae Walker
Mountain Pine Beetle, Dendroctonus ponderosae (Hymenoptera: Torymidae)
Hopkins (Coleoptera: Curculionidae, Potato Aphid, Macrosiphum euphorbiae (Thomas)
Scolytinae) (Hemiptera: Aphididae)
Myndus crudus (Van Duzee) (Hemiptera: Potato Tuberworm, Phthorimaea operculella
Cixiidae) (Zeller) (Lepidoptera: Gelechiidae)
Neotropical Brown Stink Bug, Euschistus Plum Curculio, Conotrachelus nenuphar Herbst
heros (Fabricius) (Hemiptera: (Coleoptera: Curculionidae)
Pentatomidae) Pseudo-Curly Top Treehopper, Micrutalis
Neotropical Soybean Budborer, Crocidosema malleifera (Fowler) (Hemiptera:
aporema (Walsingham) (Lepidoptera: Membracidae)
Tortricidae) Red Imported Fire Ant, Solenopsis invicta Buren
Northern Corn Rootworm, Diabrotica barberi (Hymenoptera: Formicidae)
Smith & Lawrence (Coleoptera: Redlegged Grasshopper, Melanoplus
Chrysomelidae) femurrubrum (Degeer) (Orthoptera:
Olive Fruit Curculio, Rhynchites (= Coenorrhinus) Acrididae)
cribripennis Desbrochers (Coleoptera: Red Palm Weevil, Rhynchophorus ferrugineus
Attelabidae) (Olivier) (Coleoptera: Curculionidae)
Olive Fruit Fly, Bactrocera oleae (Rossi) (= Dacus Rhammatocerus schistocercoides Rehn
oleae) (Diptera: Tephritidae) (Orthoptera: Acrididae)
Olive Psyllids, Euplyllura spp. (Hemiptera: Rocky Mountain Wood Tick, Dermacentor
Psyllidae) andersoni Stiles (Acari: Ixodidae)
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Roundheaded Pine Beetle, Dendroctonus adjunc- Tarnished Plant Bug, Lygus lineolaris Palisot de
tus Blandford (Coleoptera: Curculionidae, Beauvois (Hemiptera: Miridae)
Scolytinae) Taro Caterpillar or Rice Cutworm, Spodoptera
Seedcorn Maggot or Bean Seed Fly, Delia platura litura (Fabricius)
(Meigen) (Diptera: Anthomyiidae) Tent Caterpillars, Malacosoma spp. (Lepidoptera:
Silkworm, Bombyx mori (Linnaeus) (Lepidoptera: Lasiocampidae)
Saturniidae) Termites (Isoptera) in South America
Silverleaf Whitefly, Bemisia argentifolii Bellows Timarcha Latreille (Coleoptera: Chrysomelidae,
and Perring (Hemiptera: Aleyrodidae) Chrysomelinae)
Small Green Stink Bug, Piezodorus guildinii Tomato Hornworm, Manduca quinquemaculata
(Westwood) (Hemiptera: Heteroptera: (Haworth) and Tobacco Hornworm,
Pentatomidae) Manduca sexta (Linnaeus) (Lepidoptera:
Small Hive Beetle, Aethina tumida Murray Sphingidae)
(Nitidulidae: Coleoptera) Tracheal Mite, Acarapis woodi Rennie (Acarina:
Small Honey Ant, Prenolepis imparis (Say) Tarsonemidae)
(Hymenoptera: Formicidae) Tsetse Flies, Glossina spp. (Diptera: Glossinidae)
Small Rice Stink Bug, Oebalus poecilus (Dallas) Turnip Aphid, Lipaphis erysimi (Kaltenbach)
(Hemiptera: Heteroptera: Pentatomidae) (Hemiptera: Aphididae)
Southern Green Stink Bug, Nezara viridula (L.) Turnip Root Maggot, Delia floralis (Fallen)
(Hemiptera: Heteroptera: Pentatomidae) (Diptera: Anthomyiidae)
Soybean Aphid, Aphis glycines Matsumura Twospotted Spider Mite, Tetranychus urticae
(Hemiptera: Aphididae) Koch (Acari: Tetranychidae)
Spined Soldier Bug, Podisus maculiventris (Say) Two-Spotted Stink Bug, Perillus bioculatus
(Hemiptera: Pentatomidae) (Fabricius) (Hemiptera: Pentatomidae)
Spotted Cucumber Beetle or Southern Twostriped Grasshopper, Melanoplus bivittatus
Corn Rootworm, Diabrotica undecimpunc- (Say) (Orthoptera: Acrididae)
tata Mannerheim (Coleoptera: Varroa Mite, Varroa destructor Anderson &
Chrysomelidae) Truemann (Acari: Varroidae)
Spruce Budworms, Choristoneura Lederer Variegated Cutworm, Peridroma saucia (Hbner)
(Lepidoptera: Tortricidae) (Lepidoptera: Noctuidae)
Squash Bug, Anasa tristis (DeGeer) (Hemiptera: Vegetable Leafminer, Liriomyza sativae Blanchard
Coreidae) (Diptera: Agromyzidae)
Squash Vine Borer, Melittia cucurbitae (Harris) Viburnum Leaf Beetle, Pyrrhalta viburni
(Lepidoptera: Sesiidaae) (Paykull) (Coleoptera: Chrysomelidae)
Stable Fly, Stomoxys calcitrans (Linnaeus) Vine Mealybug, Planococcus ficus Signoret
(Diptera: Muscidae) (Hemiptera: Pseudococcidae)
Sweetpotato and Silverleaf Whiteflies, Bemisia Western Balsam Bark Beetle, Dryocoetes confusus
spp. (Hemiptera: Aleyrodidae) Swain (Coleoptera: Curculionidae,
Sweetpotato Flea Beetle, Chaetocnema confinis Scolytinae)
Crotch (Coleoptera: Chrysomelidae Western Corn Rootworm, Diabrotica virgifera
Alticinae) virgifera Leconte (Coleoptera:
Sweetpotato Weevil, Cylas formicarius (Fabricius) Chrysomelidae)
(Coleoptera: Brentidae) Western Grapeleaf Skeletonizer, Harrisina
Taiga Tick, Ixodes persulcatus Schulze (Acari: brillians Barnes & McDunnough
Ixodida: Ixodidae) (Lepidoptera: Zyganeidae)
xxviii
Highlights of the Encyclopedia of Entomology

Western Harvester Ant, Pogonomyrmex occidentalis Winter Moth, Operophtera brumata (L.)
(Cresson) (Hymenoptera: Formicidae) (Lepidoptera: Geometridae) and Its
Western Thatching Ant, Formica obscuripes Biological Control
(Forel) (Hymenoptera: Formicidae) Wireworms, Several Genera and Species
Wheat Stem Sawflies: Cephus cinctus Norton, (Coleoptera: Elateridae)
Cephus pygmaeus (L.) and Trachelus tabidus Yellowstriped Armyworm, Spodoptera
(F.) (Hymenoptera: Cephidae) ornithogalli (Guene) (Lepidoptera:
White Grubs, Phyllophaga, and Others Noctuidae)
(Coleoptera: Scarabaeidae)
List of Contributors
Abivardi, Cyrus Gainesville, Florida 32611-0680
Institute of Integrative Biology USA
ETH Zurich
Universtt-Str.16 (CHN) Ajjan, Iskandar
CH-8092 Zurich University of Tishreen
Switzerland P.O. Box 740
Latakia
Abou-Fakhr, Efat M. Syria
Department of Plant Sciences
Faculty of Agricultural and Food Sciences Ajlan, Aziz
American University of Beirut Department of Plant Protection
P.O. Box 11-0236 College of Agricultural and Food Sciences
Bliss Street King Faisal University
Beirut P.O. Box 55009
Lebanon Hofuf, Al-Hasa 31982
Saudi Arabia
Adams, Byron J.
Department of Microbiology and Molecular
Albajes, Ramon
Biology
Universitat de Lleida
Brigham Young University
Centre UdL-IRTA
Provo, Utah 84602
Rovira Roure 177
USA
25199 Lleida
Catalonia
Adler, Peter
Spain
Department of Entomology
Clemson University
Box 340365 Alborn, Hans
114 Long Hall USDA, Agricultural Research Service
Clemson, South Carolina 29634-0365 Chemistry Research Unit
USA 1600-1700 SW 23rd Drive
Gainesville, FL, 32608
Agnello, Arthur M. USA
Department of Entomology
New York State Agricultural Experiment Station Aldryhim, Yousif
Cornell University P.O. Box 2460
Geneva, New York 14456-0462 Riyadh, 1141
USA Saudi Arabia

Agrios, George Alekseev, Andrey N.

Plant Pathology Department Russian Parasitological Society
University of Florida P.O. Box 738
xxx
List of Contributors

191186 Arif, Basil

St. Petersburg, D-186 Great Lakes Forestry Center
Russia 1219 Queen Street East
Sault Ste. Marie, Ontario P6A 5M7
All, John Canada
Department of Entomology
Armstrong, Earlene
University of Georgia
Department of Entomology
413 Biological Sciences Building
University of Maryland
Athens, Georgia 30602
4122 Plant Sciences Building
USA
College Park, Maryland 20742
USA
Alomar, scar
IRTA Arthurs, Steven
Centre de Cabrils Department of Entomology
Carretera de Cabrils s/n Biological Control Laboratory
08348 Cabrils Texas A&M University
Barcelona, Catalonia College Station, Texas 77843-2475
Spain USA

Asaro, Christopher
Alvarez, Juan M.
Department of Entomology
Aberdeen Research and Education Center
University of Georgia
University of Idaho
413 Biological Sciences Building
P.O. Box 870
Athens, Georgia 30602-2603
Aberdeen, Idaho 83210-0870
USA
USA
Attathom, Tipvadee
Amalin, Divina M. Department of Entomology
USDA-APHIS Kasetsart University
13601 Old Cutler Road Kamphaengsaen Campus
Miami, Florida 33158 Nakhon Pathom, 73140
USA Thailand

Amerasinghe, Felix P. Baldwin, Rebecca W.

International Management Institute Entomology and Nematology Department
127 Sunil Mawatha, Pelawatta P.O. Box 110620
Battaramulla, 10120 University of Florida
Sri Lanka Gainesville, Florida, 32611
USA

Anderson, Robert Barbara, Kathryn A.

Canadian Museum of Nature Entomology and Nematology Department
P.O. Box 3443, Station D University of Florida
Ottawa, Ontario K1P 6P4 Gainesville, Florida 32611-0620
Canada USA
 List of Contributors
xxxi

Barfield, Carl Behmer, Spencer T.

Entomology and Nematology Department Department of Entomology
University of Florida Texas A&M University
Gainesville, Florida 32611-0620 College Station, Texas 77843-2475
USA USA

Barrera, Juan F. Bellotti, Anthony C.

Departamento de Entomologa Tropical CIAT - Centro Internacional de Agricultura
El Colegio de la Frontera Sur Tropical
Tapachula, Chiapas, 30700 Apartado Areo 6713, Cali
Mxico Colombia
Barth, Martin
Beard, Charles E.
Friedrich-Miescher-Laboratorium der
Box 340315 - 114 Long Hall
Max-Planck-Gesellschaft
Entomology, Soils and Plant Sciences
Spemannstr. 39
Clemson University
720726 Tbingen
Clemson, South Carolina 29634-0315
Germany
USA
Baumgrtner, Johann
Bennett, Gary W.
International Centre of Insect Physiology and
Center for Urban and Industrial Management
Ecology (ICIPE)
Department of Entomology
P.O. Box 17319
Purdue University
Addis Ababa
1158 Smith Hall
Ethiopia
West Lafayette, Indiana 47907-1158
Baz, Arturo USA
Universidad de Alcala
Department Biologia Animal Bentz, Barbara J.
Alcala de Henares Rocky Mountain Research Station
Madrid, E-28801 Forestry Sciences Lab
Spain 860 N 1200 E
Logan, Utah 84321
Becnel, James J. USA
Center for Medical, Agricultural and Veterinary
Entomology Berisford, C. Wayne
USDA-ARS Department of Entomology
Gainesville, Florida 32611-0970 University of Georgia
USA 413 Biological Sciences Building
Athens, Georgia 30602
Beeman, Richard W. USA
USDA-ARS
GMPRC Berlinger, Menachem J.
1515 College Avenue Entomology Laboratory
Manhattan, Kansas Agricultural Research Organization
USA Gilat Regional Experiment Station
xxxii
List of Contributors

P.O. Box 7710 B-1000 Bruxelles

Beer-Sheva, 84843 Belgium
Israel
Borgemeister, Christian
Bernays, Elizabeth A. Institute of Plant Diseases and Plant Protection
Department of Entomology University of Hannover
University of Arizona Herrenheuser Str. 2
P.O. Box 2100 30419 Hannover
Tucson, Arizona 85721-0036 Germany
USA
Bostanian, Noubar J.
Berry, Colin
Horiticultural Research and Development
Cardiff School of Biosciences
Centre
Cardiff University
Agriculture and Agri-Food Canada
P.O. Box 911
430, Boulevard Gouin
Museum Avenue
St.-Jean-sur-Richelieu, Quebec J3B 3E6
Cardiff, Wales CF10 3US
Canada
UK

Boucher, Stphanie
Bidochka, Michael
Lyman Entomological Museum
Department of Biological Sciences
McGill University, Macdonald Campus
Brock University
Ste-Anne-de-Bellevue, Qubec H9X 3V9
St. Catharines, Ontario
Canada
Canada

Blackwell, Alison Boucias, Drion

Center for Tropical Veterinary Medicine Entomology and Nematology Department
University of Edinburgh University of Florida
Easter Bush Veterinary Centre Gainesville, Florida 32611-0620
Roslin, Midlothian EH25 9RG USA
UK
Bowles, David E.
Blum, Murray S. Resource Protection Division
Department of Entomology Freshwater Conservation Branch/River Studies
University of Georgia Program
413 Biological Sciences Building Texas Parks and Wildlife Department
Athens, Georgia 30602 P.O. Box 1685
USA San Marcos, Texas 78666
USA
Boev, Jean-Luc
Dpartement dEntomologie Brambila, Julieta
IRSNB-KBIN Florida Department of Agriculture and
Royal Belgian Institute of Natural Sciences Consumer Services
Rue Vautier 29 Division of Plant Industry
 List of Contributors
xxxiii

1911 SW 34th Street Burden, Beverly

Gainesville, Florida 32614 Department of Biological Sciences
USA Louisiana State University - Shreveport
One University Place
Brandenburg, Rick Shreveport, Louisiana 71115
Department of Entomology USA
North Carolina State University
P.O. Box 7613 Buss, Eileen A.
Raleigh, North Carolina 27695-7613 Entomology and Nematology Department
USA University of Florida
Gainesville, Florida 32611-0620
Brault, Aaron C.
USA
Centers for Disease Control and Prevention
National Center for Infectious Diseases
Division of Vector-Borne Infectious Diseases Byers, George W.
P.O. Box 2087 Snow Entomological Division
Foothills Campus Natural History Museum
Fort Collins, Colorado 80522 University of Kansas
USA 1460 Jayhawk Boulevard
Lawrence, Kansas 66045-7523
Brewer, J. Wayne USA
Department of Entomology
Auburn University Cabana, Jean
301 Funchess Hall AFA Environment Inc.
Auburn University, Alabama 36849-5413 1100, Rene-Levesque Boulevard West
USA 25th Floor
Montreal, Quebec H3B 5C9
Brown, Harley P. Canada
Department of Zoology
University of Oklahoma Caceres, Carlos
730 Van Vleet Oval, Room 314 FAO/IAEA
Norman, Oklahoma 73019-6121 Agricultural and Biotechnology Laboratory
USA A-2444 Seibersdorf
Austria
Brown, Susan J.
Division of Biology
Kansas State University Calabrese, Diane M.
9 Anderson Hall 1000 Robin Road
Manhattan, Kansas 66506 Silver Spring, Maryland 20901-1873
USA USA

Broza, Meir Cane, James H.

University of Haifa USDA-ARS
Oranim, Tivon 36006 Bee Biology and Systematics Laboratory
Israel Utah State University
xxxiv
List of Contributors

5310 Old Main Hill Cherry, Ron

Logan, Utah 84322-5310 Everglades Research and Education Center
USA University of Florida
3200 E. Palm Beach Road
Capinera, John L. Belle Glade, Florida 33430
Entomology and Nematology Department USA
University of Florida
Gainesville, Florida 32611-0620 Chiappini, Elisabetta
USA Istituto di Entomologia e Patologia Vegetale
Facolt di Agraria
Cardwell, Kitty F. Universit Cattolica del Sacro Cuore
USDA/CSREES Via Emilia Parmense, 84
Washington, D.C. Piacenza, 29100
USA Italy

Cave, Ronald D.
Choate, Paul M.
Entomology and Nematology Department
Entomology and Nematology Department
University of Florida
University of Florida
Indian River Research and Education Center
Gainesville, Florida 32611-0620
Ft. Pierce, Florida 34945-3138
USA
USA
Chouinard, Grald
Cdola, Claudia V.
Institut de Recherche et de Dveloppement en
CEPAVE
Agroenvironnement
Universidad Nacional de La Plata
3300 Sicotte
Consejo Nacional de Investigaciones Cientficas y
Saint-Hyacinthe, Quebec J2S 7B8
Tcnicas
Canada
2 No 584 (1900)
La Plata
Argentina Chow, Yien-Shing
National Museum of Natural Science
Chapman, Reg 1, Kuan Chien Road
Arizona Research Laboratories Taichung 404, Taiwan
Division of Neurobiology Republic of China
University of Arizona
P.O. Box 210077 Christian, Peter
Tuscon, Arizona 85721-0077 National Institute for Biological Standards and
USA Control
Potters Bar, Hertfordshire
Cheng, Lanna UK
Scripps Institution of Oceanography
University of California, San Diego Cilek, James E.
9500 Gilman Drive Biting Fly and Tick Control Section
LaJolla, California 92093-0202 John A. Mulrennan, Sr. Public Health Entomology
USA Research and Education Center
 List of Contributors
xxxv

Florida A&M University Cranshaw, Whitney

4000 Frankford Avenue Department of Bioagricultural Sciences and Pest
Panama City, Florida 32405-1933 Management
USA Colorado State University
Fort Collins, Colorado 80523-0001
Clement, Stephen L. USA
USDA-ARS
Western Regional Plant Introduction Station Cresswell, James
Washington State University School of Biological Sciences
59 Johnson Hall University of Exeter
P.O. Box 646402 Hather Laboratories
Pullman, Washington 99164-6402 Prince of Wales Road
USA Exeter, EX4 4PS
UK
Collier, Rosemary H.
Horticulture Research International Crist, Thomas O.
Wellesbourne, Warwick CV35 9EF Department of Zoology
UK Miami University
Pearson Hall Room 212
Conlong, Des E. Oxford, Ohio 45056-1400
SASA Experiment Station USA
Private Bag X02
Mount Edgecombe Crooker, Allen
Kwa Zulu-Natal, 4300 Biology Department
South Africa Hartwick College
Oneonta, New York 13820
Constantino, Reginaldo USA
Depto de Zoologia
Universidade de Braslia Cuda, James P.
70910-900 Braslia, DF Entomology and Nematology Department
Brazil University of Florida
Gainesville, Florida 32611-0620
Coons, Lewis B. USA
Integrated Microscopy Center
University of Memphis Cumming, Jeffrey M.
201 Life Sciences Building Canadian National Collection of Insects
Rooms LS 101-113 Arachnids and Nematodes
Memphis, Tennessee 38152-6040 Agriculture and Agri-Food Canada
USA K.W. Neatby Building, C.E.F.
Ottawa, Ontario K1A 0C6
Costas, MIguel Canada
Facultad de Biologa
Universidad Complutense de Madrid Cushing, Paula E.
28040 Madrid Department of Zoology
Spain Denver Museum of Nature and Science
xxxvi
List of Contributors

2001 Colorado Boulevard Danoff-Burg, James A.

Denver, Colorado 80205-5798 Department of Ecology, Evolution and
USA Environmental Biology
Columbia University
Cusson, Michel 1020 Schermerhorn Extension, MC5557
Natural Resources Canada 1200 Amsterdam Avenue
Canadian Forest Service New York, New York 10027
1055 rue du P.E.P.S. USA
P.O. Box 3800
Sainte-Foy, Quebec G1V 4C7 Davidson, Diane W.
Canada Department of Biological Sciences
University of Utah
257 South, 1400 East
Czl, Gyozo
Salt Lake City, Utah 84112-0840
Hungarian Natural History Museum
USA
Budapest
Hungary DeClercq, Patrick
Laboratory of Agrozoology, Department of Crop
Daane, Kent M. Protection
Division of Insect Biology Faculty of Agricultural and Applied Biological
ESPM Sciences
University of California Ghent University
Berkeley, California 94720 Coupure Links 653
USA B-9000 Ghent
Belgium
Dam, Nicole M. van
Denell, Robin E.
Netherlands Institute of Ecology
Division of Biology
Centre for Terrestrial Ecology
Kansas State University
P.O. Box 40
9 Anderson Hall
6666 ZG Heteren
Manhattan, Kansas 66506
The Netherlands
USA

Dame, David Denmark, Harold A.

Entomology and Nematology Department Florida Department of Agriculture and
University of Florida Consumer Services
Gainesville, Florida 32611-0620 Division of Plant Industry
USA 1911 SW 34th Street
Gainesville, Florida 32614
Daniels, Jaret C. USA
Entomology and Nematology Department
University of Florida Devorshak, Christina
Gainesville, Florida 32611-0620 USDA-APHIS-PPQ
USA Center for Plant Health Science and Technology
 List of Contributors
xxxvii

Plant Epidemiology and Risk Analysis Laboratory 1200 University Street

Raleigh, North Carolina Spearfish, South Dakota 57799-9003
USA USA

Dicke, Marcel Dunford, James, C.

Laboratory of Entomology Department of Entomology and
Wageningen University Nematology
P.O. Box 8031 University of Florida
6700EH Wageningen Gainesville, Florida, 32611
The Netherlands USA

Dietrich, C.H.
Center for Biodiversity Dyby, Susanne D.
Illinois Natural History Survey Res. Le Rambouillet Bat. B
607 East Peabody Drive 1 Alle des Lucioles
Champaign, Illinois 61820 Beaulieu-sur-Mer, 06310
USA France

Dorchin, Netta Easton, Emmett

Museum Koenig Department of Plant and Environmental
Adenauerallee 160 Protection Sciences
53113 Bonn University of Hawaii at Manoa
Germany 3050 Maile Way
Gilmore Hall 310
Downer, R.A. Honolulu, Hawaii 96822-2271
Laboratory for Pest Control Application USA
Technology
Ohio Agricultural Research and Development
Ebert, Timothy A.
Center
Laboratory for Pest Control Application
Ohio State University
Technology
1680 Madison Avenue
Ohio Agricultural Research and Development
Wooster, Ohio 44691-4096
Center
USA
Ohio State University
1680 Madison Avenue
Downie, D.A.
Wooster, Ohio 44691-4096
Department of Zoology and Entomology
USA
Rhodes University
Grahamstown 6140
South Africa Edmunds, Malcolm
Department of Environmental
Downing, Holly Management
Unit 9003 University of Central Lancashire
College of Arts and Sciences Preston, PR1 2HE
Black Hills State University UK
xxxviii
List of Contributors

Ellis, Amanda Felicioli, Antonio

Florida Department of Agriculture and Universita degli Studi di Pisa
Consumer Services Dipartimento di Anatomia, Biochimica e
Division of Plant Industry Fisiologia veterinaria
P.O. Box 147100 Viale delle Piagge n 2, 56100 Pisa
Gainesville, Florida 32614-7100 Italy
USA
Feng, Qili
Ellis, James D. Great Lakes Forestry Center
Entomology and Nematology Department 1219 Queen Street East
University of Florida Sault Ste. Marie, Ontario P6A 5M7
Gainesville, Florida 32611-0620 Canada
USA

Emmel, Thomas C. Finch, Stan

McGuire Center for Lepidoptera Research and Horticulture Research International
Conservation Wellesbourne, Warwick CV35 9EF
University of Florida UK
Gainesville, Florida 32611-0620
USA Finke, Mark D.
6811 Horned Owl Trail
Epsky, Nancy D. Scottsdale, Arizona 85262-8519
USDA/ARS USA
Subtropical Horticulture Research Station
13601 Old Cutler Road Fishel, Fred
Miami, Florida 33158 University of Florida,
USA Pesticide Information Office
PO Box 110710
Farag, Mohamed A. Gainesville, Florida 32611-0710
Department of Chemistry and Biochemistry USA
Texas Tech University
Lubbock, Texas 79409-1061
Fitzgerald, T.D.
USA
Department of Biology
Fasulo, Thomas R. State University of New York at Cortland
Entomology and Nematology Department Cortland, New York 13045
University of Florida USA
Gainesville, Florida 32611-0620
USA Floate, Kevin D.
Agriculture and Agri-Food Canada
Feir, Dorothy Lethbridge Research Centre
Biology Department 5403 1st Avenue
St. Louis University P.O. Box 3000
St. Louis, Missouri 63103 Lethbridge, Alberta T1J 4B1
USA Canada
 List of Contributors
xxxix

Flowers, R. Wills Rondebosch 7700

Center for Biological Control/Entomology Cape Town
Division of Agricultural Sciences Republic of South Africa
Florida A&M University
Tallahassee, Florida 32307 Galante, Eduardo
USA CIBIO
University of Alicante
Fornasari, Luca 03080 San Vicente del Raspeig
Clas de lErmitage Alicante
636, ave. E. Jeanbrau Spain
34090 Montpellier
France Gall, Lawrence F.
Peabody Museum of Natural History
Frank, J. Howard Yale University
Entomology and Nematology Department P.O. Box 208118
University of Florida New Haven, Connecticut 06520-8118
Gainesville, Florida 32611-0620 USA
USA
Gangwere, Stan K.
Department of Biological Sciences
Franz, Gerald
Wayne State University
FAO/IAEA
Detroit, Michigan 48202
Agricultural and Biotechnology Laboratory
USA
A-2444 Seibersdorf
Austria
Garcia, Lloyd
North Carolina Department of Agriculture and
Froeba, Jason G. Consumer Sciences
Entomology and Nematology Department Plant Industry Division
University of Florida P.O. Box 27647
Gainesville, FL 32611-0620 Raleigh, North Carolina 27611
USA USA

Gabrys, Beata Gayubo, Severiano F.

Institute of Biotechnology and Environmental Area de Zoologa
Sciences Facultad de Biologa
University of Zielona Gora Universidad de Salamanca
Monte Cassino 21b 37071 Salamanca
65-561 Zielona Gora Spain
Poland
Gerberg, Eugene J.
Gde, Gerd Entomology and Nematology Department
Zoology Department University of Florida
University of Cape Town Gainesville, Florida 32611-0620
Private Bag USA
xl
List of Contributors

Gerlach, Gnter Goebel, Rgis

Botanischer Garten Mnchen - Nymphenburg SASEX-CIRAD
Menzinger Str. 65 Entomology Department
80638 Mnchen Private Bag X02
Germany Mount Edgecombe, 4300
South Africa
Gerling, Dan
Department of Zoology Goettel, Mark
Tel Aviv University Lethbridge Research Centre
Ramat Aviv, 69978 Agriculture and Agri-Food Canada
Israel 5403 1st Avenue South
P.O. Box 3000
Lethbridge, Alberta T1J 4B1
Ghiradella, Helen Canada
Department of Biology
State University of New York at Albany Gold, Clifford S.
Albany, New York 12222 CIAT (International Center for Tropical
USA Agriculture)
P.O. Box 6247
Giberson, Donna Kampala
Department of Biology Uganda
University of Prince Edward Island
550 University Ave. Goodman, Katie
Charlottetown, PEI C1A 4P3 Department of Biological Sciences
Canada Western Illinois University
Macomb, Illinois 61455
Giblin-Davis, Robin M. USA
Fort Lauderdale Research and Education Center
University of Florida Goula, Marta
3205 College Avenue University of Barcelona
Davie, Florida 33314-7719 Barcelona
USA Spain

Greco, Nancy M.
Gibson, G.A.P. CEPAVE
Agriculture and Agri-Food Canada Universidad Nacional de La Plata
960 Carling Avenue Consejo Nacional de Investigaciones Cientficas y
Ottawa, Ontario K1A 0C6 Tcnicas
Canada 2 No 584 (1900)
La Plata
Glenn, D. Michael Argentina
USDA-ARS, Appalachian Fruit Research Station
2217 Wiltshire Rd. Grewal, Parwinder S.
Kearneysville, WV 25430 Department of Entomology
USA The Ohio State University
 List of Contributors
xli

Columbus, Ohio 43210 Hall, Donald W.

USA Entomology and Nematology Department
University of Florida
Gruner, Susan V. Gainesville, Florida 32611-0620
Entomology and Nematology Department USA
University of Florida
Gainesville, Florida 32611-0620
Hall, Jason P.W.
USA
National Museum of Natural History
Guertin, Claude Smithsonian Institution
INRS Washington, D.C. 20560-0127
Institut Armand-Frappier USA
531 Boulevard des Prairies
Laval, Quebec H7V 1B7 Hall, Robert D.
Canada Office of Research
University of Missouri
Gupta, Virendra K. 205 Jesse Hall
Entomology and Nematology Department Columbia, Missouri 65211
University of Florida USA
Gainesville, Florida 32611-0620
USA
Handler, Alfred M.
Gwynne, Darryl T. Center for Medical, Agricultural and Veterinary
University of Toronto at Mississauga Entomology
Mississauga, Ontario L5L 1C6 USDA-ARS
Canada P.O. Box 14565
1700 SW 23rd Drive
Habeck, Dale Gainesville, Florida 32608
Entomology and Nematology Department USA
University of Florida
Gainesville, Florida 32611-0620 Hangay, George
USA 80 Gondola Road
Narrabeen, New South Wales 2101
Hahn, Daniel A.
Australia
Entomology and Nematology Department
University of Florida
Gainesville, Florida 32611-0620 Hansen, Laurel D.
USA Department of Biology
Spokane Falls Community College
Halbert, Susan 3410 W. Fort George Wright Dr.
Florida Department of Agriculture and Spokane, WA 99224-5288
Consumer Services USA
Division of Plant Industry
1911 SW 34th Street Harman, Dan M.
Gainesville, Florida 32614 University of Maryland
USA Center for Environmental Science
xlii
List of Contributors

Appalachian Laboratory Hernandez, Santiago

Frostburg, Maryland 21532-2307 Universities of Cordoba and Extremadura
USA Cceres, 10071
Spain
Haunerland, Norbert H.
Department of Biological Sciences Hilje, Luko
Simon Fraser University Plant Protection Unit
Burnaby, British Columbia V5A 1S6 7170 CATIE
Canada Turrialba, Cost Rica

Headings, Mark Hinkle, Nancy C.

Agricultural Technical Institute Department of Entomology
Ohio State University University of Georgia
1328 Dover Road 413 Biological Sciences Building
Wooster, Ohio 44691-8905 Athens, Georgia 30602
USA USA

Heath, Allen
Hirsch, Helmut V.B.
AgResearch Wallaceville
Department of Biology
Wallaceville Animal Research Centre
State University of New York at Albany
PO Box 40063, Upper Hutt, 5140
1400 Washington Avenue
New Zealand
Albany, New York 12222
USA
Held, David W.
Entomology Department
University of Kentucky Ho, Chyi-Chen
S-225 Agricultural Science Center Taiwan Agricultural Research Institute
BuildingNorth Department of Applied Zoology
Lexington, Kentucky 40546-0091 Wufeng
USA Taichung, Taiwan
Republic of China
Henneman, M.L.
Department of Biological Sciences Hodges, Greg S.
University of Bristol Florida Department of Agriculture and
Bristol, BS8 1TH Consumer Services
UK Division of Plant Industry
1911 SW 34th Street
Heppner, John B. Gainesville, Florida 32614
Florida State Collection of Arthropods USA
Florida Department of Agriculture and
Consumer Services Horton, David R.
Division of Plant Industry USDA/ARS
P.O. Box 147100 5230 Konnowac Pass Road
Gainesville, Florida 32614-7100 Wapato, Washington 98951
USA USA
 List of Contributors
xliii

Hou, Roger F. Hadassah Medical School

Department of Entomology Jerusalem
National Chung Hsing University Israel
Taichung 402, Taiwan
Republic of China Isman, Murray B.
Faculty of Agricultural Sciences
Howard, Forrest W. University of British Columbia
Fort Lauderdale Research and Education Center 248-2357 Main Mall
University of Florida Vancouver, British Columbia V6T 1Z4
Ft. Lauderdale, Florida 33314-7719 Canada
USA

Hoy, Marjorie A. James, Rosalind R.

Entomology and Nematology Department USDA/ARS, Bee Biology and Systematics
University of Florida Laboratory
Gainesville, Florida 32611-0620 Department of Biology, UMC 5310
USA Utah State University
5310 Old Main Hill
Huber, John Logan, Utah 84321-5310
Canadian Forestry Service USA
960 Carling Avenue
Ottawa, Ontario K1A 0C6 Jaffe, Klaus
Canada Universidad Simn Bolvar
Apartado 89000, Caracas 1080
Hunter, Fiona F. Venezuela
Department of Biological Sciences
Brock University Jeremas, Xavier
St. Catharines, Ontario L2S 3A1 Museum of Natural Sciences
Canada C./ Catalunya 28
08758 Cervell (prov. Barcelona)
Hurd, Hilary Spain
Keele University
School of Life Sciences
Keele, Staffordshire ST55BG Jolivet, Pierre
UK 67, Bd Soult
75012 Paris
Hurd, Lawrence E. France
Department of Biology
Washington & Lee University Jurez, M. Patricia
Lexington, Virginia 24450 Facultad de Ciencias Mdicas
USA Universidad Nacional de la Plata
Calle 60 y 120
Ioffe-Uspensky, Inna C.C. 455
Department of Parasitology La Plata, 1900
The Hebrew University of Jerusalem Argentina
xliv
List of Contributors

Kabissa, Joe C.B. Private Bag X134

Tanzania Cotton Lint and Seed Board Pretoria, 0001
Pamba House South Africa
Garden Avenue
P.O. Box 9161 Khan, Zeyour R.
Dar Es Salaam ICIPE
Tanzania P.O.B. 30772
Nairobi
Kalkar, . Kenya
Department of Entomology
Clemson University Kima, Peter E.
Clemson, South Carolina Microbiology and Cell Science Department
USA University of Florida
Building 981, Box 110700
Katsoyannos, Byron Gainesville, Florida 32611-0700
Aristotle University of Thessaloniki USA
Department of Agriculture
Laboratory of Applied Zoology and Parasitology Klassen, Waldemar
Thessaloniki, 541 24 Tropical Research and Education Center
Greece University of Florida
18905 SW 280th Street
Kathirithamby, Jeyaraney Homestead, Florida 33031-3314
Department of Zoology USA
Oxford University
South Parks Road Klotz, John H.
Oxford OX1 3PS, Department of Entomology
UK University of California
Riverside, California
Keeley, Larry L. USA
Department of Entomology
Texas A&M University Klowden, Marc J.
2475 TAMU Division of Entomology
College Station, Texas 77843-2475 University of Idaho
USA Moscow, Idaho 83844-2339
USA
Kerr, Peter H.
California Department of Food and Agriculture Koehler, Philip G.
Plant Pest Diagnostics Branch Entomology and Nematology Department
3294 Meadowview Rd. University of Florida
Sacramento, California 95832 Gainesville, Florida 32611-0602
USA USA

Kfir, Rami Kok, L.T.

ARC-Plant Protection Research Institute Department of Entomology
Rietondale Research Station College of Agriculture and Life Sciences
600 Soutpansberg Road Virginia Polytechnic Institute and State University
 List of Contributors
xlv

216 Price Hall Michigan State University

Blacksburg, Virginia 24061-0319 204 Center for Integrated Plant Systems
USA East Lansing, Michigan 48824-1311
USA
Kondratieff, Boris C.
Department of Bioagricultural Sciences and Pest Lawrence, Pauline O.
Management Entomology and Nematology Department
Colorado State University University of Florida
Fort Collins, Colorado 80523 Gainesville, Florida 32611-0620
USA USA

Kouloussis, Nikos A. Leather, Simon R.

Aristotle University of Thessaloniki Division of Biology
Laboratory of Applied Zoology and Parasitology Imperial College London
Thessaloniki, 541 24 Silwood Park Campus
Greece Ascot, SL5 7PY
UK
Krafsur, Elliot S.
206 Hidden Valley Circle Lebiush-Mordechi, Sarah
Shepherdstown, West Virginia 25443 Entomology Laboratory
USA Agricultural Research Organization
Gilat Regional Experiment Station
Lacey, Lawrence A. P.O. Box 7710
USDA-ARS Beer-Sheva, 84843
Yakima Agricultural Research Lab Israel
5230 Konnowac Pass Road
Wapato, Washington 98951 Lecoq, Michel
USA Centre de Coopration Internationale en Recher-
che Agronomique pour le Dveloppement
Lambdin, Paris L. Prifas
Department of Entomology and Plant Pathology TA 40/D
University of Tennessee 34398 Montpellier, Cedex 5
2431 Center Drive France
205 Ellington Plant Sciences Building
Knoxville, Tennessee 37996-4560 Lee, Clarence M.
USA Department of Biology
Howard University
Lapointe, Stephen L. 415 College Street N.W.
USDA-ARS, U.S. Horticultural Research Lab Washington, D.C. 20059
2001 South Rock Road USA
Fort Pierce, Florida 34945
USA Lee, How-Jing
Department of Entomology
Landis, Douglas A. National Taiwan University
Department of Entomology Taipei 106, Taiwan
Center for Integrated Plant Systems Republic of China
xlvi
List of Contributors

Legaspi, Benjamin C., Jr. Lloyd, James E.

USDA-ARS, FAMU-Center for Biological Entomology and Nematology Department
Control University of Florida
6383 Mahan Drive Gainesville, Florida 32611-0620
Tallahassee, Florida 32308 USA
USA
Long, Lewis S.
Legaspi, Jesusa C. Entomology and Nematology Department
USDA-ARS, FAMU-Center for Biological University of Florida
Control Gainesville, Florida 32611-0620
6383 Mahan Drive USA
Tallahassee Florida 32308
USA Lord, Cynthia C.
Florida Medical Entomology Laboratory
Legg, David University of Florida
Department of Renewable Resources 200 9th Street S.E.
College of Agriculture Vero Beach, Florida 32962-4699
University of Wyoming USA
P.O. Box 3354
Laramie, Wyoming 82071 Lord, Jeffrey
USA USDA-ARS
Northern Plains Area Grain Marketing and
Leppla, Norman C.
Production Research Center
Entomology and Nematology Department
Biological Research Unit
University of Florida
1515 College Avenue
Gainesville, Florida 32611-0620
Manhattan, Kansas 66502-2796
USA
USA
Leskey, Tracy
USDA-ARS Lounibos, L. Philip
Appalachian Fruit Research Station Florida Medical Entomology Laboratory
45 Wiltshire Road University of Florida
Kearneysville, West Virginia 25430 200 9th Street S.E.
USA Vero Beach, Florida 32962-4699
USA
Liburd, Oscar
Entomology and Nematology Department Luna, Mara G.
University of Florida Department of Ecology and Evolutionary Biology
Gainesville, Florida 32611-0620 University of California at Irvine
USA 321 Steinhaus Hall
Irvine, California 92697-2525
Liebman, Matt USA
Department of Agronomy
Iowa State University Lysyk, Tim
Ames, Iowa 50011-1010 Laboratory of Vector Ecology
USA Agriculture and Agri-Food Canada
 List of Contributors
xlvii

P.O. Box 3000 1600/1700 SW 23rd Drive

5403 1st Avenue South P.O. Box 14565
Lethbridge, Alberta T1J 4B1 Gainesville, Florida 32604
Canada USA

MacVean, Charles Manley, Donald G.

Instituto de Investigaciones PeeDee Research and Education Center
Universidad del Valle de Guatemala Clemson University
Aptdo. Postal 82 2200 Pocket Road
Guatemala City Florence, South Carolina 29506-9706
Guatemala USA

Magalhes, Bonifcio Mapes, Carol C.

EMBRAPA Recursos Genticos e Biotecnologia Biology Department
Parque Estao Biolgica Kutztown University
Final WS Norte Kutztown, Pennsylvania 19530
CEP 70770-900 USA
Brasilia-DF
Brazil
Marcos-Garcia, Maria Angeles
CIBIO
Maimala, S.
University of Alicante
Department of Agriculture
03080 San Vicente del Raspeig
Ministry of Agriculture and Cooperation
Alicante
Chatuchak, Bangkok
Spain
Thailand

Marshall, David Martnez, Javier

Ecology and Evolutionary Biology Universities of Cordoba and Extremadura
University of Connecticut Cceres, 10071
75 N. Eagleville Rd., U-3043 Spain
Storrs, Connecticut 06269
USA Martnez, Maricela
Instituto Mexicano de Tecnologa del Agua
Malakar-Kuenen, Raksha (IMTA)
Division of Insect Biology Paseo Cuaunhahuac 8532 Progreso
ESPM Jiutepec, Morelos
University of California Mexico
Berkeley, California 94720
USA Mason, Peter G.
Eastern Cereal and Oilseed Research Centre
Mankin, Richard Agriculture and Agri-Food Canada
USDA/ARS 960 Carling Avenue
Center for Medical, Agricultural and Veterinary Ottawa, Ontario K1A 0C6
Entomology Canada
xlviii
List of Contributors

Matthews, Deborah L. McSorley, Robert

Department of Entomology and Entomology and Nematology Department
Nematology University of Florida
University of Florida Gainesville, Florida 32611-0620
Gainesville, Florida 32611 USA
USA
Meagher, Robert
Matsumoto, Yoshiharu USDA-ARS
University of Tokyo Center for Medical and Veterinary Entomology
Tokyo 1700 SW 23rd Drive
Japan Gainesville, Florida 32608-1069
USA
Matthiessen, John N.
CSIRO Entomology Medal, Julio
Underwood Avenue Entomology and Nematology Department
Floreat, Western Australia 6014 University of Florida
Australia Gainesville, Florida 32611-0620
USA
McAuslane, Heather J.
Entomology and Nematology Department Meinke, Lance J.
University of Florida Department of Entomology
Gainesville, Florida 32611-0620 University of Nebraska
USA Lincoln, Nebraska 68583-0816
USA
McCravy, Kenneth W.
Department of Biological Sciences Meinking, Terri L.
Western Illinois University Department of Dermatology
1 University Circle University of Miami School of Medicine
Macomb, Illinois 61455 1600 NW 10 Avenue
USA P.O. Box 016960 (R-117)
Miami, Florida 33101
McFadyen, Rachel USA
CRC Australian Weed Management
Natural Resource Sciences Menalled, Fabin D.
Meiers Road Department of Agronomy
Indooroopilly, Queensland Iowa State University
Australia Agronomy Hall
Ames, Iowa 50011-1010
McIver, James USA
Forestry and Range Sciences Laboratory
Pacific Northwest Research Station Merkl, Ott
USDA Forest Service Hungarian Natural History Museum
1404 Gekeler lane H-1088 Budapest
LaGrande, Oregon 97850 Baross utca, 13
USA Hungary
 List of Contributors
xlix

Meyer, Jason Sakuragaoka 1-1-1

Entomology and Nematology Department Setagaya-ku
University of Florida Tokyo, 156-8502
Gainesville, Florida 32611-0620 Japan
USA
Mizell, Patricia A.
Meyerdirk, Dale E. North Florida Research and Education Center
USDA APHIS, PPQ University of Florida
National Biological Control Institute 155 Research Road
4700 River Road Quincy, Florida 32351
Unit 135 USA
Riverdale, Maryland 20737-1228
USA
Mizell, Russell F., III
Miller, Barry R. North Florida Research and Education Center
Centers for Disease Control and Prevention University of Florida
National Center for Infectious Diseases 155 Research Road
Division of Vector-Borne Infectious Diseases Quincy, Florida 32351
P.O. Box 2087 USA
Foothills Campus
Fort Collins, Colorado 80522 Moriya, Seiichi
USA Insect Ecology Laboratory
National Agricultural Research Center
Miller, Dini M. 3-1-1, Kannondai
Department of Entomology Tsukuba, Ibaraki 305-8666
Virginia Tech University, 216A Price Hall Japan
Blacksburg, Virginia 24061
USA Morrill, Wendell L.
Department of Entomology
Miller, Laura T. Montana State University
West Virginia Department of Agriculture Bozeman, Montana 59717-0001
Plant Industries Division USA
1900 Kanawha Boulevard, East
Charleston, West Virginia 25305-0191
Moya-Raygoza, Gustavo
USA
Universidad de Guadalajara
Mitcham, Elizabeth Departamento de Botnica y Zoologa
Department of Plant Sciences, Mail Stop 2 Apartado Postal 139
University of California Zapopan, Jalisco 45101
One Shields Avenue Mexico
Davis, California 95616
USA Mutun, Serap
Abant Izzet Baysal University
Mitsuhashi, Jun Department of Biology
Department of Bioscience Bolu, 14280
Tokyo University of Agriculture Turkey
l
List of Contributors

Nadel, Hannah Nayar, Jai K.

USDA-ARS SJVASC Florida Medical Entomology Laboratory
San Joaquin Valley Science Center University of Florida
9611 Riverbend Ave. 200 9th Street SE
Parlier, California 93648 Vero Beach, Florida 32962
USA USA

Nagoshi, Rod Nealis, Vince

USDA-ARS Natural Resources Canada-Canadian Forest
Center for Medical, Agricultural and Veterinary Service
Entomology Pacific Forestry Centre
P.O. Box 14565 506 W. Burnside Road
Gainesville, Florida 32608 Victoria, British Columbia V8Z 1M5
USA Canada

Napper, Emma Negron, Jose F.

Rothamsted USDA Forest Service
Harpenden, Hertfordshire AL5 2JQ Rocky Mountain Research Station
UK 240 West Prospect
Fort Collins, Colorado 80526
Naranjo, Steven E. USA
USDA-ARS
Neuenschwander, Peter
Western Cotton Research Laboratory
International Institute of Tropical Agriculture
4135 E. Broadway Road
08 B.P. 0932
Phoenix, Arizona 85040
Cotonou
USA
Bnin
Nation, James L. Neven, Lisa, G.
Entomology and Nematology Department USDA-ARS, Yakima Agricultural Research
University of Florida Laboratory
Gainesville, Florida 32611-0620 5230 Konnowac Pass Road
USA Wapato, WA 98951 USA

Navajas, Maria Nguyen, Khuong

Institut National de la Recherche Agronomique Entomology and Nematology Department
Campus International de Baillarguet University of Florida
CS 30016 Gainesville, Florida 32611-0620
Montferrier sur Lez cedex, 34988 USA
France
Nicolson, Sue
Navarette, Ignacio Department of Zoology & Entomology
Universities of Cordoba and Extremadura University of Pretoria
Cceres, 10071 Pretoria 0002
Spain South Africa
 List of Contributors
li

Noling, Joseph W. Okuda, Takashi

University of Florida National Institute of Agrobiological
Citrus Research & Education Center Sciences
700 Experiment Station Rd. Anhydrobiosis Research Unit, 1-2 Ohwashi
Lake Alfred, Florida 33850 Tsukuba, 305-8634
USA Japan

Norris, Douglas E. ONeill, Kevin M.

Johns Hopkins University Department of Land Resources and
Bloomberg School of Public Health Environmental Sciences
W. Harry Feinstone Department of Molecular Montana State University
Microbiology and Immunology Bozeman, MT 59717
615 North Wolfe Street Rm E5008 USA
Baltimore, Maryland 21205
USA Orphanides, George M.
Agricultural Research Institute
Northfield, Tobin P.O. Box 22016
University of Florida Nicosia, 1516
North Florida Research and Education Center Cyprus
155 Research Rd.
Otis, Gard W.
Quincy, Florida 32351
Department of Environmental Biology
USA
University of Guelph
Guelph, Ontario N1G 2W1
OBrien, Lois B.
Canada
College of Engineering Sciences, Technology and
Agriculture
Overholt, William Allan
Florida A&M University
Indian River Research and Education Center
Tallahassee, Florida 32307-4100
University of Florida
USA
Fort Pierce, Florida
USA
OHara, James, E.
Agriculture and Agri-Food Canada Panizzi, Antnio R.
960 Carling Avenue Embrapa Soja
Ottawa, Ontario K1A 0C6 Caixa Postal 231
Canada Londrina, PR 86001-970
Brazil
Oi, David H.
USDA-ARS Papadopoulos, Nikos T.
Center for Medical, Agricultural and Veterinary Aristotle University of Thessaloniki
Entomology Laboratory of Applied Zoology and
1600 SW 23rd Drive Parasitology
Gainesville, Florida 32608-1067 Thessaloniki, 541 24
USA Greece
lii
List of Contributors

Parra, Jos Roberto Postali P.O. Box 443051

Departamento de Entomologia Moscow, Idaho 83844-3051
Fitopatologia e Zoologia Agrcola. USA
Esalq/USP, C.P. 9 - 13418-900
Piracicaba, SP Pea, Jorge E.
Brazil Tropical Research and Education Center
University of Florida
Par, Paul W. 18905 SW 280th Street
Department of Chemistry and Biochemistry Homestead, Florida 33031-3314
Texas Tech University USA
Lubbock, Texas 79409-1061
USA Pendland, J.C.
Entomology and Nematology Department
Paulson, Gregory S. University of Florida
Shippensburg University Gainesville, Florida 32611-0620
Department of Biology USA
Shippensburg, Pennsylvania 17257
USA Pereyra, Patricia C.
CEPAVE
Peairs, Frank B. Universidad Nacional de La Plata
Department of Bioagricultural Sciences and Pest Consejo Nacional de Investigaciones Cientficas y
Management Tcnicas
Colorado State University 2 No 584 (1900)
Fort Collins, Colorado 80523-1177 La Plata
USA Argentina

Peck, Daniel C. Philogne, Bernard J.R.

Department of Entomology, Barton Laboratory Department of Biology
New York State Agricultural Experiment Station University of Ottawa
Cornell University Poste 4166
630 West North Street 30 Marie Curie Street
Geneva, New York 14456 Ottawa, Ontario K1N 6N5
USA Canada

Peck, Stewart B. Pickett, John A.

Department of Biology Rothamsted
4640 CTTC Building Harpenden, Hertfordshire AL5 2JQ
Carleton University UK
Ottawa, Ontario K1S 5B6
Canada Pinzauti, Mauro
Universita degli Studi di Pisa
Pellmyr, Olle Dipartimento di Coltivazione e Difesa delle
Department of Biological Sciences Specie Legnose
University of Idaho Via S. Michele degli Scalzi, n2, 56100 Pisa
Room 252, Life Sciences Building Italy
 List of Contributors
liii

Pollet, Marc Pszczolkowski, Maciej

Research Group Terrestrial Ecology Missouri State University and State Fruit
University of Ghent, Ghent, Belgium Experiment Station
and 9740 Red Spring Road
Royal Belgian Institute of Natural Sciences Mountain Grove, Missouri 65711
Brussels USA
Belgium
Punzo, Fred
Potter, Daniel A.
Department of Biology
Department of Entomology
University of Tampa
University of Kentucky
Box 5F
S-225 Agricultural Science Center Building North
401 West Kennedy Boulevard
Lexington, Kentucky 40546-0091
Tampa, Florida 33606
USA
USA
Powers, Ann M.
Centers for Disease Control and Prevention Purcell, Alexander H.
National Center for Infectious Diseases Division of Insect Biology
Division of Vector-Borne Infectious Diseases University of California
P.O. Box 2087 201 Wellman
Foothills Campus Berkeley, California 94720-3112
Fort Collins, Colorado 80522 USA
USA
Puterka, Gary
Preston, Catherine A. USDA-ARS, PSRL
USDA - ARS 1301 N. Western
Center for Medical, Agricultural and Veterinary Stillwater, Oklahoma 74074
Entomology USA
P.O. Box 14565
1700 SW 23rd Drive
Ragsdale, David W.
Gainesville, Florida 32608
Department of Entomology
USA
University of Minnesota
1980 Folwell Avenue
Prischmann, Deirdre
St. Paul, Minnesota 55108
USDA ARS NPA NCARL
USA
2923 Medary Ave.
Brookings, South Dakota 57006-9401
USA Raina, Ashok K.
USDA-ARS
Prokopy, Ronald J. Southern Regional Research Center
Department of Entomology Formosa Subterranean Termite Research Unit
University of Massachusetts 1100 Robert E. Lee Boulevard
Fernald Hall P.O. Box 19687
Amherst, Massachusetts 01003 New Orleans, Louisiana 70179-0687
USA USA
liv
List of Contributors

Randolph, Sarah Rey, Jorge

Department of Zoology Florida Medical Entomology Laboratory
University of Oxford University of Florida
South Parks Road 200 9th Street S.E.
Oxford, 0X1 3PS Vero Beach, Florida 32962
UK USA

Rashidan, Kia Ribes, Eva

University of Saint Boniface University of Barcelona
200 Avenue de la Cathedral Barcelona
Winnipeg, Manitoba R2H 0H7 Spain
Canada
Richman, David B.
The Arthropod Museum
Ratcliffe, Brett C.
Entomology, Plant Pathology and Weed Science
Systematics Research Collections
Department
University of Nebraska
New Mexico State University
Lincoln, Nebraska 68588-0514
MSC 3BE, Box 30003
USA
Las Cruces, New Mexico 88003
USA
Redborg, Kurt E.
Department of Biology Riddick, Eric W.
Coe College USDA-ARS
1220 First Avenue Biological Control and Mass Rearing Research
Cedar Rapids, Iowa 52402 Unit
USA 810 Highway 12 East
P.O. Box 5367
Reina, David Mississippi State, Mississippi 39762-5367
Faculty of Veterinary Sciences USA
Universities of Cordoba and Extremadura
Cceres, 10071 Riley, David G.
Spain Coastal Plain Region
University of Georgia
Resh, Vincent H. P.O. Box 748
Environmental Science, Policy and Management Tifton, Georgia 31793-0748
University of California USA
201 Wellman Hall
Rinkevich, Frank D.L.
Berkeley, California 94720
Department of Biology
USA
Millersville University
Millersville, Pennsylvania 17551
Retnakaran, Arthur USA
Great Lakes Forestry Center
1219 Queen Street East Rivers, David B.
Sault Ste. Marie, Ontario P6A 5M7 Department of Biological Sciences
Canada Butler University
 List of Contributors
lv

4600 Sunset Avenue Jacksonville, Florida 32224

Indianapolis, Indiana 42608 USA
USA
Rothschild, Marjorie
Roderick, George Integrated Microscopy Center
Environmental Science (ESPM) University of Memphis
University of California 201 Life Sciences Building
Berkeley, California 94720-3114 Rooms LS 101-113
USA Memphis, Tennessee 38152-6040
USA
Rogers, Michael E.
Department of Entomology Rust, Michael K.
University of Kentucky Department of Entomology
S-225 Agricultural Science Center North University of California, Riverside
Lexington, Kentucky 40546-0091 Riverside, California
USA USA
Roltsch, William J.
Rutledge, C. Roxanne
California Department of Food and Agriculture
Florida Medical Entomology Laboratory
Biological Control Program
University of Florida
3288 Meadowview Road
200 9th Street S.E.
Sacramento, California 95832
Vero Beach, Florida 32962-4699
USA
USA
Roe, Kelly
Sanborn, Allen F.
Department of Biological Sciences
Barry University
Western Illinois University
School of Natural and Health Sciences
Macomb, Illinois 61455
11300 NE Second Avenue
USA
Miami Shores, Florida 33161-6695
Rosenberg, David M. USA
Freshwater Institute
501 University Crescent Snchez, Norma E.
Winnipeg, Manitoba R3T 2N6 CEPAVE
Canada Universidad Nacional de La Plata
Consejo Nacional de Investigaciones Cientficas y
Ross, Edward S. Tcnicas
California Academy of Sciences 2 No 584 (1900)
Department of Entomology La Plata
Golden Gate Park Argentina
San Francisco, California 94118
USA Sanford, Malcolm T.
Entomology and Nematology Department
Rossi, Anthony University of Florida
Department of Natural Sciences Gainesville, Florida 32611-0620
University of North Florida USA
lvi
List of Contributors

Sarzynski, Erin Schneider, David C.

Entomology and Nematology Department Ocean Sciences
University of Florida Memorial University of Newfoundland
Gainesville, Florida 32611-0620 St. Johns, Newfoundland A1B 3X7
USA Canada

Schning, Caspar
Sastry, Shivashankar Department of Population Biology
National Institute of Mental Health University of Copenhagen
Saint Elizabeth Hospital Universitetsparken 15
U.S. Department of Health and Human Services 2100 Copenhagen
Washington, D.C. Denmark
USA
Schulthess, Fritz
IITA
Schabel, Hans G. Contonou
College of Natural Resources Republic of Benin
University of Wisconsin
Stevens Point, Wisconsin 54481 Schuster, Jack
USA Universidad del Valle
Aptd 82
Guatemala City
Scheffrahn, Rudolph H.
Guatemala
Fort Lauderdale Research and Education Center
University of Florida Scotti, Paul D.
3205 College Avenue The Horticulture and Food Research Institute of
Fort Lauderdale, Florida 33314 New Zealand
USA Mt. Albert Research Centre
Auckland
Scherer, Clay W. New Zealand
DuPont Professional Products
Seal, Dakshina R.
Wilmington, Delaware
Tropical Research and Education Center
USA
University of Florida
18905 SW 280th Street
Schmelz, Eric Homestead, Florida 33031-3314
USDA, Agricultural Research Service USA
Chemistry Research Unit
1600-1700 SW 23rd Drive Serrano, David
Gainesville, Florida 32608 Department of Entomology and Nematology
USA University of Florida
Gainesville, Florida32611
USA
Schmidt, Justin O.
Southwestern Biological Institute Setamau, Mamoudou
1961 W. Brichta Dr. Texas A&M Agricultural Experiment Station
Tucson, Arizona 85745 Weslaco, Texas 78596-8399
USA USA
 List of Contributors
lvii

Shaaya, Eli Shirk, Paul D.

Department of Food Science USDA-ARS
Agricultural Research Organization Center for Medical, Agricultural and Veterinary
The Volcani Center Entomology
P.O. Box 6 Box 110970
Bet Dagan, 50250 Gainesville, Florida 32611-0970
Israel USA

Shanower, Thomas G. Showler, Allan T.

USDA-ARS USDA-ARS, SARC
Northern Plains Agricultural Research 2413 East Highway 83
Laboratory Building 201
Pest Management Research Unit Weslaco, Texas 78596
1500 N. Central Avenue USA
Sidney, Montana 59270
USA Shukle, Richard H.
USDA-ARS
Department of Entomology
Shapiro-Ilan, David I.
Purdue University
USDA-ARS, SAA
West Lafayette, Indiana 47907
Southeastern Fruit and Tree Nut Research
USA
Laboratory
21 Dunbar Road
Sikes, Derek S.
Byron, Georgia 31008
University of Alaska Museum
USA
907 Yukon Drive
Fairbanks, AK 99775-6960
Shepard, B. Merle USA
Coastal Research and Education Center
Clemson University Sims, Kelly R.
2865 Savannah Highway Department of Entomology and Nematology
Charleston, South Carolina 29414-5333 University of Florida
USA Gainesville, Florida 32611
USA
Shields, Vonnie D.C.
Biological Sciences Department Sinclair, Bradley J.
Towson University Entomology, Ontario Plant Laboratories,
800 York Road Canadian Food Inspection Agency
Towson, Maryland 21252-3042 K.W. Neatby Building, C.E.F.
USA Ottawa, Ontario, K1A 0C6
Canada
Shippy, Teresa D.
Division of Biology Sivinski, John
Kansas State University USDA-ARS
Manhattan, Kansas Center for Medical, Agricultural and Veterinary
USA Entomology
lviii
List of Contributors

1700 SW 23rd Drive Soler Cruz, M.D. Amparo

Gainesville, Florida 32604-2565 Department of Parasitology
USA University of Granada
18071 Granada
Skevington, Jeff Spain
Agriculture and Agri-Food Canada
K.W. Neatby Building, C.E.F. Solter, Leellen F.
960 Carling Ave. Illinois Natural History Survey
Ottawa, Ontario K1A 0C6 607 East Peabody Drive
Canada Champaign, Illinois 61820
USA
Slaney, David
Somma, Louis A.
Ecology and Health Research Center
Department of Entomology and Nematology
Departmentof Public Health
University of Florida
Wellington School of Medicine and Health
Gainesville, Florida 32611
Sciences
USA
University of Otago
P.O. Box 7343
Soroka, Juliana J.
Wellington South
Agriculture and Agri-Food Canada
New Zealand
Saskatoon Research Centre
107 Science Place
Smagghe, Guy Saskatoon, Saskatchewan S7N 0X2
Laboratory of Agrozoology Canada
Faculty of Agricultural and Applied Biological
Sciences Sourakov, Andrei
Ghent University Entomology and Nematology Department
Coupure Links 653 University of Florida
B-9000 Ghent Gainesville, Florida 32611-0620
Belgium USA

Smith, Hugh Spafford, Helen

University of California Cooperative Extension School of Animal Biology (M0895)
624-A West Foster Road University of Western Australia
Santa Maria, California 93455 35 Stirling Highway
USA Crawley, W.A. 6009
Australia
Smith, John P.
John A. Mulrennan, Sr., Public Health Stange, Lionel A.
Entomology Research & Education Center Florida Department of Agriculture
Florida A&M University Division of Plant Industry
4000 Frankford Avenue P.O. Box 110980
Panama City, Florida 32405-1933 Gainesville, Florida 32611-0980
USA USA
 List of Contributors
lix

Steck, Gary J. Sullivan, Daniel J.

Florida State Collection of Arthropods Department of Biological Sciences
Division of Plant Industry Fordham University
1911 SW 34th Street Bronx, New York 10458
Gainesville, Florida 32608-1201 USA
USA
Swisher, Marilyn E.
Stocks, Ian Department of Family, Youth and Community
308 Long Hall Sciences
Department of Entomology, Soils, and Plant University of Florida
Sciences Gainesville, Florida 32611-0310
Clemson University USA
Clemson, South Carolina 29634-0315
USA Sword, Gregory
School of Biological Sciences
Steinkraus, Donald C. University of Sydney
Department of Entomology The Macleay Building A12
University of Arkansas Sydney, NSW 2006
Virology Laboratory Australia
319 Agriculture Building
Fayetteville, Arkansas 72701
Tabachnick, Walter J.
USA
Florida Medical Entomology Laboratory
University of Florida
Stewart, Kenneth W.
200 9th Street SE
Department of Biological Science
Vero Beach, Florida 32962-4699
University of North Texas
USA
P.O. Box 305220
Denton, Texas 76203-5220
Tanaka, Seiji
USA
Laboratory of Insect Life Cycles and Physiology
Division of Insect and Animal Sciences
Stonedahl, Gary
Independent Administrative Institution
106 Briza Court
Ohwashi 1-2, Tsukuba, Ibaraki 305-8634
Bellingham, Washington 98226
Japan
USA

Striganova, Bella R. Tartar, Aurlian

Laboratory of Soil Zoology and General Entomology and Nematology Department
Entomology University of Florida
A. N. Severtsov Institute of Ecology and Gainesville, Florida 32611-0620
Evolution USA
Russian Academy of Sciences
Leninsky Prospect, 33 Taylor, Steven J.
Moscow 119071 Center for Biodiversity
Russia Illinois Natural History Survey
lx
List of Contributors

607 East Peabody Drive (MC-652) Tinsaara, William

Champaign, Illinois 61820-6970 Bioversity International
USA P.O. Box 24384, Kampala
Uganda
Teal, Peter E.A.
USDA-ARS Tipping, Christopher
Center for Medical, Agricultural and Veterinary Delaware Valley College
Entomology 700 East Butler Ave.
1700 SW 23rd Drive Doylestown, Pennsylvania 18901
P.O. Box 14565 USA
Gainesville, Florida 32604
USA
Triplehorn, Charles
Tew, James E. Department of Entomology
Ohio State University Museum of Biological Diversity
1608 Madison Avenue Ohio State University
Wooster, Ohio 44691-1030 1315 Kinnear Road
USA Columbus, Ohio 43212-1192
USA
Thomas, Michael C.
Florida State Collection of Arthropods Trumble, John T.
Florida Department of Agriculture and Department of Entomology
Consumer Services University of California
P.O. Box 147100 Riverside, California 92521-0001
Gainesville, Florida 32614-7100 USA
USA
Tsai, James H.
Thompson, Sarah Fort Lauderdale Research and Education Center
Department of Entomology University of Florida
North Carolina State University 3205 College Avenue
P.O. Box 7613 Fort Lauderdale, Florida 33314-7799
Raleigh, North Carolina 27965-7613 USA
USA

Thompson, Vinton Tzanakakis, Minos E.

Roosevelt University Aristotle University of Thessaloniki
Chicago, Illinois 60605 Department of Applied Zoology and
USA Parasitology
Thessaloniki, 541 24
Tilgner, Erich Greece
Department of Entomology
University of Georgia Ueshima, Norihiro
413 Biological Sciences Building Matsusaka University
Athens, Georgia 30602 Matsusaka, Mie
USA Japan
 List of Contributors
lxi

Uspensky, Igor Verma, K.K.

Department of Chemistry HIG1/327, Housing Board Colony
A. Silberman Institute of Life Sciences Borsi, DURG - 491001
Hebrew University of Life Sciences India
Jerusalem 91904
Israel Vickerman, Danel B.
Department of Entomology
Valles, Steven M. University of California
USDA-ARS Riverside, California 92521-0001
Center for Medical, Agricultural, and Veterinary USA
Entomology
1600 SW 23rd Drive Villegas, Baldomero
Gainesville, Florida 32608 California Department of Food and Agriculture
USA Biological Control Program
3288 Meadowview Road
Vandergast, Amy G. Sacramento, California 95832
U.S. Geological Survey USA
San Diego, California
USA Vincent, Charles
Horticultural Research and Development Center
Agriculture and Agri-Food Canada
VanderMeer, Robert K.
430 Boulevard Gouin
USDA-ARS
Saint-Jean-sur-Richelieu, Quebec J3B 3E6
Center for Medical, Agricultural and Veterinary
Canada
Entomology
P.O. Box 14565
Wallace, John R.
1700 SW 23rd Drive
Department of Biology
Gainesville, Florida 32608
Millersville University
USA
Millersville, Pennsylvania 17551
USA
Vzquez, M. ngeles
Departamento de Zoologa y Antropologa Fsica Wang, Ping
C/ Jos Antonio Novais 2, pl.X Lab. 9 Entomology Department
Universidad Complutense de Madrid Cornell University
28040 Madrid New York State Agricultural Experiment Station
Spain Geneva, New York 14456
USA
Vega, Fernando E.
USDA-ARS Wang, Qiao
Insect Biocontrol Laboratory Institute of Natural Resources
Beltsville Agricultural Research Center Massey University
Building 011A, Room 214 PB 11122
Beltsville, Maryland 20705 Palmerston North
USA New Zealand
lxii
List of Contributors

Weber, Donald C. Comstock Hall

USDA, ARS, PSI, Insect Biocontrol Laboratory Ithaca, New York 14853-0901
Bldg. 011A, Rm. 107, BARC-West USA
Beltsville, MD 20705
USA Wheeler, Alfred G.
Department of Entomology
Weber, Richard G. Clemson University
Department of Entomology and Applied Ecology 114 Long Hall
University of Delaware Box 340365
Newark, Delaware 19716 Clemson, South Carolina 29634-0365
USA USA

Webster, Thomas C. Wiener, Linda

Atwood Research Facillity St. Johns College
Kentucky State University Santa Fe, New Mexico 87501
Frankfort, Kentucky 40601 USA
USA
Wild, Alex
Weinstein, Philip Department of Entomology
Ecology and Health Research Center, Department University of Arizona
of Public Health PO Box 2100
Wellington School of Medicine and Health Tucson, Arizona 85721-0036
Sciences USA
University of Otago
P.O. Box 7343 Williamson, R. Chris
Wellington South Department of Entomology
New Zealand University of Wisconsin
237 Russell Labs
Weintraub, Phyllis G. Madison, Wisconsin 53706-1520
Agricultural Research Organization USA
Gilat Research Station
D.N. Negev, 85280 Willis, John S.
Israel Department of Cellular Biology
University of Georgia
Weissman, David B. 724 Biological Sciences Building
Department of Entomology Athens, Georgia 30602-2607
California Academy of Sciences USA
Golden Gate Park
San Francisco, CA 94118 Willis, Judith H.
USA Department of Cellular Biology
University of Georgia
Weston, Paul A. 724 Biological Sciences Building
Department of Entomology Athens, Georgia 30602-2607
Cornell University USA
 List of Contributors
lxiii

Willmott, Keith R. Blacksburg, Virginia 24061-0406

McGuire Center for Lepidoptera Research and USA
Conservation
University of Florida Yu, Simon J.
Gainesville, Florida 32611 Entomology and Nematology Department
USA University of Florida
Gainesville, Florida 32611-0620
Wing, Steven R. USA
University of Florida
P.O. Box 115001 Zachvatkin, Yuri A.
Gainesville, Florida 32611 Department of Entomology
USA K. A. Timiryazev Agricultural Academy
Timiryazeva St., 49, Build. 12
Moscow 127550
Worner, Sue
Russia
National Centre for Advanced Bio-Protection
Technologies
Zhu, Kun Yan
Bio-Protection and Ecology Division
Department of Entomology
Lincoln University
Kansas State University
P.O. Box 84, Canterbury
123 Waters Hall
New Zealand
Manhattan, Kansas 66506-4004
USA
Wysiecki, Mara L.
CEPAVE Zaspel, Jennifer
Universidad Nacional de La Plata Entomology and Nematology Department
Consejo Nacional de Investigaciones Cientficas y University of Florida
Tcnicas Gainesville, Florida 32611-0620
2 No 584 (1900) USA
La Plata
Argentina Zuparko, Robert L.
Essig Museum of Entomology
Yousten, Allan A. University of California
Department of Biology 201 Wellman Hall
Virginia Tech Berkeley, California 94720-3112
2119 Derring Hall USA
A

Abafi-Aigner, Lajos (Ludwig original family name: Abafi-Aigner and changed

Aigner) his German Christian name Ludwig to the
Hungarian equivalent Lajos. However, despite
george hangay his successes in publication and writing his busi-
Narrabeen, New South Wales, Australia ness begun to decline in the 1880s and within a
few years he faced financial difficulties, which
Ludwig Aigner was born on the 11 February 1840 ultimately led to the closure of his famous book-
at Nagyjcsa, Torontl Shire, Transylvania, Hungary, shop. Disillusioned, he discontinued most of his
now Romania. His family moved to Temesvr, a business activities, and from 1890 he devoted all
large town in Transylvania, where he received a his time and energy to lepidopterology. In 1895,
formal education in commerce and begun his he published the results of his studies in the
career as a book merchant. His family was of ethnic Termszetrajzi Fzetek (Notebooks of Natural
German stock and young Ludwig only learned History), the journal of the National Museums
Hungarian when, in 1858, they moved to Pozsony Natural History Department and he was one of
(now Bratislava and in the Slovak Republic), a the authors of Fauna Regni Hungariae (Catalogue
large town with predominantly Hungarian inhab- of Hungarys Fauna). He resurrected Rovartani
itants. From here he soon moved on to Pest (now Lapok (Entomological Papers), which was estab-
Budapest) and in 1863, as it was the custom in lished in 1884 but ceased to exist in 1886. His
those years, he wandered all over Austria and treatment of the butterfly fauna of Hungary won
Germany. He completed his studies in Kln and the coveted Bugt Prize. Based on this work he
Stuttgart before returning to Pest. He always had published Butterflies of Hungary in 1907. The
an interest in entomology and he became a keen book was (and probably still is) one of the most
amateur lepidopterologist. However, besides ento- popular entomological publications in Hungary.
mology, he had a great variety of other interests It has inspired countless young entomologists and
too, especially in the field of publishing, writing, made the name of Abafi-Aigner well known to
historical research as well as aspirations in busi- every naturalist in the country. He passed away
ness. He found success in publishing and in estab- on the 19 June 1909.
lishing a popular bookshop. In 1870 he was
initiated as a Freemason and eventually he rose to
the highest positions in the Order. For 12 years he Reference
has worked on an extensive monograph of the
history of Freemasonry. He used his Hungarian Horvth C (1990) A rovartan tudsa. E let s Tudomny
pen name Abafi in a hyphenated form with his 45:290, 312
2
A Abaxial Surface

Abaxial Surface drawings of a quality that was very high for that
time. Some of the insect illustrations included
The lower surface of a leaf (contrast with adaxial not only adults, but also larvae and the plants on
surface). which they fed, and even observational notes. He
died about 1840.

Abbott, John
Reference
John Abbott was born in London in 1751. In Eng-
land, he was given drawing lessons and, through Mallis A (1971) American entomologists. Rutgers University
his drawing instructor, was introduced to Dru Press, New Brunswick, NJ, 549 pp
Drury, a collector of insects who had been presi-
dent of the Linnean Society. These two encoun-
ters encouraged him to collect insects and draw Abbott s Formula
them, but his father was training him to be an
attorney. Finding legal paperwork not to his lik- A mathematical technique commonly used to
ing, he emigrated to Virginia in 1773. After 2 assess mortality in insecticide trials when there is
years in Virginia, he relocated to Georgia, where need to correct for a change (decrease) in the
he served as a private in the Third Georgia Con- background population density (i.e., in the check
tinental Battalion during the Revolutionary War. or control plots). The formula is:
For his military service he received several hun- % corrected control = 100 (% alive in the check %
dred acres of land, and worked as a planter and alive in the treatment)/(% alive in the treatment)
schoolmaster. In Virginia he had collected Amer-
ican insects and bird skins, and drew and painted
insects and birds. Some of the specimens and
paintings were shipped to England for sale. Some Abdomen
of the paintings, after sale, adorned books on
birds, insects, and spiders written by various The posterior of the three main body divisions of
authors, not necessarily with acknowledgment an insect (Fig. 1).
to Abbott. In all, Abbott produced over 3,000 Abdomen of Hexapods

Abdomen, Figure 1 Cross section of an insect abdomen, showing components of the insect circulatory
system and direction of hemolymph flow (adapted from Evans, Insect biology).
 Abdomen of Hexapods
A 3

Abdomen of Hexapods primitive, the number of abdominal segments is

usually greater, as occurs in the Protura with 11
severiano f. gayubo segments (Figs. 25). An exception is the Collem-
Universidad de Salmanca, Salamanca, Spain bola, which only possess six. In addition, it is nec-
essary to keep in mind that, in certain cases, the
The abdomen constitutes the caudal tagma in the total number of visible segments does not coin-
hexapods and is usually larger than the other two, cide with what a particular individual actually
the head and the thorax. This region is also referred possesses, since some segments remain invisible
to as a visceral area because it houses the visceral upon being telescoped, particularly those of the
organs. Its form can vary depending on the group, posterior region of the abdomen.
and even on the species. The maximum number of According to Bitsch, a generalized abdominal
observed segments is 11, although certain authori- segment would be limited anteriorly by a preseg-
ties consider a twelfth segment that in fact corre- mentary domain, separated from the segmentary
sponds to a telsonic caudal region. In general, the domain proper (of greater size) by a suture that
number of segments decreases from the preimagi- begins an internal crest named the costa or antecosta.
nal phases to the adult stage, especially in those This crest anteriorly delimits an acrotergite or pre-
holometabolous insects in which the last segments costa in the tergal part and a presternite in the sternal
of the adults are formed from imaginal discs part. In this idealized model, the muscles would be
during pupation. In the groups considered most inserted in successive antecostas. No known struc-
ture is homologous to the thoracic furca.
The presence of the gonopore (double in
Ephemeroptera) in segments VIII and IX (in VII
in the case of Ephemeroptera), and fundamentally
of the external structures related to reproduction
(the genitalia), produce important modifications
in those segments. Considering the presence of
these genitalia, three regions of the abdomen are
recognized: an anterior (pregenital or visceral
region that includes the first eight segments),
median (genital region, eighth and ninth segments),
and caudal regions (postgenital region, tenth and
eleventh segments plus the telsonic region).

The Pregenital Region

In the most generalized condition, the first abdom-

inal segments conserve their basic structure, being
easily distinguished from the thoracic segments.
Nevertheless, the most frequent condition is that
which produces morphological modifications that
Abdomen of Hexapods, Figure 2 Diagram of a affect the thoracic-abdominal union. These modi-
proturan (Protura) showing abdominal segments fications usually consist of reductions that affect
and appendages: dorsal view (left), ventral view the sternal region and involve a greater or lesser
(right). desclerotization of different structures and their
4
A Abdomen of Hexapods

Abdomen of Hexapods, Figure 3 Diagram of chewing louse (Mallophaga) showing abdominal segments,
including numbering of segments: dorsal view (left), ventral view (right).

incorporation to the metathorax. In this sense, the modified appendages exist in Collembola. In
case of the Hymenoptera, Apocrita stands out, in Archaeognatha, very developed coxites are differ-
which a narrowing is produced between the sec- entiated, above which are inserted styli in a median
ond and the third abdominal segments, which position and the exsertile vesicles in the most
incorporate the thorax and is named the propo- internal position.
deum. The rest of the abdominal segments are The styli are elongated pieces, articulated in
called the gaster or metasoma. The region formed their base above the external face of the coxite.
by the propodeum and the thorax constitutes the They are unisegmentary and lack muscles
mesosoma. The narrowing allows a great ampli- inserted in their base, often presenting an apical
tude of movements of the metasoma, which per- spine. Taking into account their position and
mits stinging in the capture of prey in aculeates. In their embryonic development, the styli are con-
some groups, like Formicidae and Sphecidae (Acu- sidered by the majority of authorities as vestigial
leata), one or two segments of the metasoma form appendages, and more concretely as reduced
a narrower zone called the petiole. telepodites. The exsertile vesicles are considered
In the pregenital region, several appendicular internal coxal formations (internal coxalia of
structures can be found. Thus, three pairs of highly some authorities).
 Abdomen of Hexapods
A 5

least in part, it is of appendicular origin. In this

antenna
sense, it is clear that in the Archaeognatha the
pretarsus
tibiotarsus eye eighth and ninth segments are basically similar in
femur pronotum males and females and their structures are homol-
trochanter
coxa
mesonotum ogous to those already indicated for the pregenital
precoxae metanotum segments. Taking into account this relationship,
collophore the genitalia of Archaeognatha are considered
tenaculum (catch) primitive, and therefore fundamental to interpret
the genitalia of Pterygota.
In the eighth segment of the Archaeognatha,
the basal part of the appendicular structure is named
first gonocoxa or gonocoxite and bears the first
gonostylus; in the ninth is found the second gono-
manubrium coxa with its corresponding stylus. In both segments
dens
(at times in the eighth, always in the ninth) forma-
furcula
mucro (spring)
tions homologous to the exsertile vesicles appear,
which are called gonapophyses (parameters in the
males and gonapophysis proper in the females). The
fundamental difference between both sexes lies in
Abdomen of Hexapods, Figure 4 Diagram
the presence in the males of a phallic structure.
of springtail (Collembola) showing furcular
The female genitalia in the Pterygota constitute
appendage at tip of abdomen.
the ovipositor. The gonocoxites are incorporated
into the lateral wall of the genital segments in a
In Pterygota the abdominal appendages complete manner in the eighth segment, forming
remain restricted to the larval forms (Lepidoptera the first valvifer. In the ninth segment the basal part
and Hymenoptera, Tenthredinoidea), although is incorporated into the lateral wall, originating the
rough appendicular pairs already exist in the second valvifer, while the rest is extended, forming
polypodous type of embryos. These abdominal the third pair of valves (dorsal or lateral valves of
appendages are named false legs or prolegs and some authorities), which are not homologous in
are retractile, conical and membranous projec- Archaeognatha. The other two pairs of valves are
tions, with a circular planta that bears a crown, the ventral valves, corresponding to the eighth seg-
usually with hooks, to adhere to the substrate. ment, and the internal valves, corresponding to the
ninth segment. These two pairs of valves are homol-
ogous to the gonapophysis of Archaeognatha. In
The Genital Region the case of the generalized type of ovipositor like
that of Orthoptera, these three pairs of valves are
The transformations that affect the eighth and linked through the length of their course, forming
ninth abdominal segments are a consequence of in their interior a canal for oviposition.
the development of special external structures that Among the sclerites that are situated in the
in the case of the male serve in the transfer of base of the valves (in addition to the valvifers
sperm, and in the case of the female allow for ovi- already mentioned) are found the intervalves (inter-
position. These structures together are known by valvulae of the authorities) by way of elongated
the name genitalia. transverse formations, one in the base of the valves
The origin of the genitalia is controversial, of the eighth segment and another in the base of the
although the majority of authorities accept that, at valves of the ninth segment. The typical ovipositor
6
A Abdomen of Hexapods

Abdomen of Hexapods, Figure 5 Comparative development of cerci on earwig (Dermaptera, top left);
grasshopper (Orthoptera, top right); scorpion fly (Mecoptera, lower left); silverfish (Zygentoma).

that was just described can experience modifica- developed, in such a way that they can become
tions according to the functions that it carries out; telescoped, forming oviposition tubes; this type of
one of the most drastic is found in Hymenoptera, ovipositor is named the ovicauda. Not being
Aculeata, where it is transformed into a sting that homologous to the genitalia, many authorities call it
serves the females as an attacking organ, either to terminalia.
capture prey or as a defense. On the other hand, the The masculine genitalia present great mor-
process of oviposition can be carried out through phological variability, which together with their
other, different structures, as occurs in the females taxonomic importance, have been the object of an
of certain Diptera. In that case, the last segments are infinity of descriptions, many of them without
retractile and the intersegmental zones are highly truly anatomical criteria. This has originated the
 Abdomen of Hexapods
A 7

use of very varied terminologies that have done or on the contrary, increase in complexity, develop-
nothing but complicate its study and impede the ing spines and other types of processes named fla-
establishment of homologies even in the same group, gellum, virga or pseudovirga over the internal walls of
creating in this way a great nomenclatorial chaos. the endophallus. When the endotheca and the
In the males, in addition to the genitalia proper, endophallus are evaginated, the genitalia are converted
other structures (processes, lobes, etc). exist that into authentic intromittent organs.
intervene in functions other than those strictly The primitive position of the male genitalia
related to the transfer of sperm; among the most can be displaced through different types of turns;
common is the grasping of the female during mat- one of the most showy cases is that which occurs
ing. It has already been mentioned that the major- in some Hymenoptera, Symphyta that present the
ity of authorities consider that the interpretation of condition called strophandric, which is character-
the genitalia of Pterygota should be made by ized by a 180 rotation of the genitalia. Rotations
homology with the basic condition that is found in have also been observed in males of Diptera.
Archaeognatha. In this group, the phallic complex The postgenital region, as was mentioned in
is formed by a median organ, the phallus or penis, the beginning of this section, comprises the tenth
and a pair of segmented pieces named parameres, and eleventh segments plus the telsonic region. The
that in the case of maximum development can exist tenth segment has been detected in Protura,
in the eighth and ninth segments. The parameres Diplura, Archaoegnatha, Thysanura (Zygentoma),
correspond to the gonapophysis of the females Ephemeroptera, Plecoptera, and some Orthoptera.
(although the term gonapophysis is utilized indis- The morphology of this segment is basically simi-
tinctly for both sexes by some authorities). lar to the pregenital segments, although with cer-
Many morphological models have been pro- tain frequency it can form a ring when the tergum
posed to describe the male genitalia of Pterygota. and sternum unite, or the sternal region can be
The most complete, since it gathers and discusses membranous. In embryonic forms, a pair of appen-
early data, is that proposed by Bitsch. According dicular outlines is seen above this segment. In cer-
to this author, what together forms the copulatory tain holometabolous insects, structures of uncertain
organ (phallus or penis) and the structures associ- meaning appear, such as the socii of some
ated with the parameres (considered in the sense Hymenoptera.
expressed by the Archaeognatha) is named the The eleventh segment is recognized in the
phallic complex. majority of embryonic phases of hexapods. In
The aedeagus is a sclerotized tube, situated Archaeognatha and Thysanura it forms an annular
above a largely membranous phallobase, although structure from whose dorsal part is differentiated a
in more complex cases the phallobase presents an long and narrow process called filum terminale,
internal fold that remains membranous (endoth- while from the lateroventral position are differenti-
eca) while the external part is sclerotized (phalloth- ated the cerci that in the adults possess numerous
eca or theca). The aedeagus presents an invagination divisions. In the Pterygotes, the eleventh segment is
that forms a more or less developed internal cham- formed by the epiproct (tergal region) and the
ber (the endophallus), which communicates with paraprocts (in the lateroventral position); in the
the gonopore at its base and in the other extreme more primitive groups exist cerci (whose length
communicates with the exterior through the phal- and number of divisions are variable) situated in
lotreme. In counter-proposition to the endophallus, the membranous zones that exist between the
the part formed by the external walls of the phal- epiproct and the paraprocts. The telsonic, asegmen-
lobase and the aedeagus forms the ectophallus. The tary region constitutes the perianal membrane or
phallic complex can present variable development, periproct.
even being able to cause the aedeagus to disappear, Alimentary Canal and Digestion
8
A Abdominal Pumping

References Abnormality

Bitsch J (1979) Morphologie abdominal des insects. In: In insect pathology, deviation from the normal; a
Grass, P-P (ed) Trait de Zologie, VIII (II): 291600 malformation or teratology; a state of disease.
Bitsch J (1994) The morphological groundplan of Hexapoda:
critical review of recent concepts. Annales de la Socit
Entomologique de France 30:103129
Deuve T (2001) The epipleural field in hexapods. Annales de
la Socit Entomologique de France 37:195231
Abrocomophagidae
Matsuda R (1970) Morphology and evolution of the insect
abdomen. Pergamon Press, New York, NY A family of chewing lice (order Phthiraptera).
Snodgrass RE (1935) Principles of insect morphology. Chewing and Sucking Lice
MacGraw Hill, New York, NY

Abdominal Pumping Absolute Methods of Sampling

Contraction of the muscles associated with the Techniques used to sample insect populations that
abdomen can result in collapse and expansion of provide an estimate per unit of area (e.g., per
the air sacs. This forces relatively large volumes of square meter, per leaf or per plant). Types of abso-
air in and out of the insect through the spiracles, lute methods include unit of habitat, recapture,
promoting ventilation. This is called active ventila- and removal trapping. (contrast with relative
tion, in contrast with the more normal gas exchange methods of sampling).
mechanism of insects, diffusion or passive ventilation. Sampling Arthropods
To a small degree, abdominal pumping also pro-
motes gas exchange through the trachea, but the
trachea is quite resistant to change in shape. Acanaloniidae
Abdominal pumping is more important for larger
insects such as locusts, which display abdominal A family of insects in the superfamily Fulgoroidae
pumping almost continuously, but especially when (order Hemiptera). They sometimes are called
active. In these insects air is sucked in through planthoppers.
some spiracles and pumped out through others. Bugs
Active Ventilation

Abiotic Disease Acanthmetropodidae

A family of mayflies (order Ephemeroptera).
A disease caused by factors other than pathogens
Mayflies
(e.g., weather or nutrition).

Abiotic Factors Acanthopteroctetidae

Factors, usually expressed as factors affecting mor- A family of moths (order Lepidoptera). They com-
tality, characterized by the absence of life. Abiotic monly are known as archaic sun moths.
factors include temperature, humidity, pH, and Archaic Sun Moths
other physical and chemical influences. Butterflies and Moths
 Acaricides or Miticides
A 9

Acanthosomatidae applying a measured amount to the integument.

The lower the LD50 or LC50, the more toxic the
A family of bugs (order Hemiptera). poison.
Bugs An LC50 is obtained when a mite is exposed to
a particular concentration of toxicant but the actual
amount of toxicant the individual experiences is
Acaricide not determined. For example, if the pesticide is
applied to foliage and the mite walks about on the
A pesticide applied to manage mite populations. foliage, the actual amount of toxicant the mite is
An acaricide is also called a miticide. exposed to depends on the activity of the mite, the
Acaricides or Miticides amount taken up through the integument or by
feeding.
Figure 6 shows a concentration-response
Acaricides or Miticides curve in parts per million (ppm) for the acaricide
Omite (propargite) exhibited by adult females
marjorie a. hoy from colonies of the Pacific spider mite Tetrany-
University of Florida, Gainesville, FL, USA chus pacificus. The concentration required to kill
50% of the individuals is the LC50. The two types
An acaricide or miticide is a pesticide that pro- of F1 females (produced by crossing Chapla
vides economic control of pest mites and ticks. males and Bidart females, and vise versa) respond
Mites and ticks are collectively called either acari similarly and their concentration-response
or acarina. Some products can act as insecticides curves are about midway between those of the
or fungicides as well as acaricides. resistant (Bidart) and susceptible (Chapla) colo-
An acaricide is a pesticide used to kill mites nies, which indicates that resistance may involve
and ticks (Table 1). Always check with state and a semidominant mode of inheritance. The term
federal authorities to be sure products containing mode of inheritance describes how the trait is
these active ingredients are registered for use. inherited; for example, the resistance can be
Always read labels carefully and follow the direc- determined by a single major dominant (only
tions completely. one copy of the gene is required for the mite to
The toxicity of an acaricide is determined by a express the resistance) or recessive (two copies of
dose-response curve or a concentration-response the gene are required) gene. Or, the resistance
curve. Such curves are obtained by exposing test can be a quantitative trait determined by multiple
mites or insects to increasing concentrations or genes of equal and additive effect. In this exam-
doses of the pesticide and recording the resulting ple, the propargite resistance may be determined
mortality after a given time interval. One estimate a single semidominant gene with modifying
of toxicity used is the term LD50 (which is the dose genes, but additional tests are required to resolve
required to kill 50% of the test population). The whether more than one gene actually contributes
LC50 is the concentration required to kill 50% of to this resistance.
the test population. If the dose is introduced
through the insects mouth it is an oral LD50, if it is
introduced through the skin or integument it is a Acaricide Classification
dermal LD50, and if it is introduced through the
respiratory system it is the inhalation LD50. A mea- Pesticides are classified in several ways, including:
sured dose is applied to an arthropod by inserting (i) their mode of entry into the target pest, (ii)
a measured amount of toxicant into the gut or by chemical structure, or (iii) source.
10
A Acaricides or Miticides

Acaricides or Miticides, Table 1 Acaricides (miticides) currently or recently available for general and
restricted use to control mites and ticks*
Name** (chemical type) General Use (GU)*** Potential use
Some trade names Restricted Use (RU)
Abamectin (avermectin B1a; GU, Class IV (practically nontoxic) Also an insecticide; affects
produced from the bacterium nervous system and paralyzes
Streptomyces avermitilis) Affirm, insects or mites; used in citrus,
Agri-Mek, Avid, vertimec, Zephyr pears, nut tree crops
Amitraz (triazapentadiene) GU, Class III (slightly toxic) Used in pears, cotton, and on
Acarac, Mitac, cattle, and hogs to control
Ovidrex,Triatox,Topline insects, ticks and mites
Azadirachtin GU, Class IV Azadirachtin is similar to insect
(tetranortriterpenoid extracted hormones called ecdysones,
from the Neem tree) Align, Azatin, which control metamorphosis;
Turplex also may serve as a feeding
deterrent; used to control insects
and mites on food, greenhouse
crops, ornamentals and turf
Bifenazate (carbazate) Floramite Class IV Mites on greenhouse,
shadehouse, nursery, field, field,
landscape and interiorscape
ornamentals, not registered in
USA for use on food
Bifenthrin (pyrethroid) Talstar, RU, Class II (moderately toxic) Insecticide and acaricide that
Brigade, Capture affects the nervous system and
causes paralysis; used on
greenhouse ornamentals and
cotton
Carbaryl (carbamate) Adios, GU, Class I, II or III, depending General use pesticide to control
Bugmaser, Crunch, Dicarbam on insects on citrus, fruits, cotton,
formulation Hexavin, Karbaspray, forests, lawns, nuts, ornamentals,
Septene Sevin, Tornadao, Thinsec shade trees, poultry, livestock and
pets. Also works as a mollusccide
and acaricide
Chlorobenzilate (chlorinated RU, Class III, may cause tumors in Used for mite control on citrus
hydrocarbon) Acaraben, Akar, mice and in beehives; also kills ticks;
Benzilan, Folbex use cancelled in USA
Chlorfenapyr (pyrrole) Pylon, Class I Used to control spider mites,
Pyramite, Pirate broad ites, budmites, cyclamen
mite, rust mites and some insects.
Cinnamon oil (cinnamaldehyde) Exempt from registration under Broad spectrum miticide/
Cinnamite FIFRA insecticide/fungicide controls or
repels pests; could be phytotoxic
in some cases; used in ornamentals,
shade or nursery trees,
vegetables, herbs and spices
Citronella oil Exempt from FIFRA Repels insects and ticks
Demeton-S-Methyl No longer registered for use in Systemic and contact insecticide
(organophosphate) Meta-Systox, USA; Class I, highly toxic and acaricide, widely used
Azotox, Duratox, Mifatox against diverse pests
 Acaricides or Miticides
A 11

Acaricides or Miticides, Table 1 (Continued)

Name** (chemical type) General Use (GU)*** Potential use
Some trade names Restricted Use (RU)
Dicofol (organochlorine) Acarin, GU, Class II or III, depending on Miticide used on fruits,
Difol, Kelthane, Mitigan formulation vegetables, ornamentals and field
crops
Dicrotophos (organophosphate) RU Contact systemic pesticide and
Bidrin, Carbicron, Dicron, Ektafos acaricide used to control
sucking,boring and chewing
pests on coffee, cotton, rice,
pecans; used to control ticks on
cattle
Dienochlor (organochlorine) GU, Class III Contact material used for
Pentac, often formulated with plant-feeding mites on
other pesticides ornamental shrubs and trees
outdoors and in greenhouses;
disrupts egg laying of female
mites; use cancelled in USA
Dinocap (dinitrophenyl) GU, Class III Used as a fungicide and as an
Arathane, Caprane, Dicap, Dikar acaricide for ticks and mites; use
Karathane, Mildane cancelled in USA
Disulfoton (organophosphate) RU, Class I, highly toxic Systemic insecticide and acaricide
Disyston, Disystox, used to control sucking insects/
Dithiodemeton, Dithiosystox, mites on cotton, tobacco, sugar
Solvigram, Solvirex beets, cole crops, corn, peanuts,
wheat, grains, ornamentals,
potatoes
Endosulfan (chlorinated RU, Class I Contact insecticide and
hydrocarbon) Afidan, Cyclodan, acaricideused to control many
Endocide, Hexasulfan, Phaser, pests on tea, coffee, fruits,
Thiodan, Thionex vegetables, grains
Ethion (organophosphate) GU, Class II Insecticide and acaricide used on
Acithion, Ethanox, Ethiol, Nialate, wide variety of food, fiber and
Tafethion, Vegfru Foxmite ornamentals, including
greenhouse crops, citrus, lawns
and turf
Eucalyptus oil Exempt from FIFRA Repels mites; repels fleas and
mosquitoes
Fenamiphos (organophosphate) RU, Class I A nematicide that has some
Nemacur, Phenamiphos, Bay activity against sucking insects
68138 and spider mites
Fenbutatin oxide (organotin) RU Miticide used on perennial
Vendex fruits,eggplant and ornamentals
Fenitrothion (organophosphate) GU Acaricide and insecticide
Accothion, Cyfen, Dicofen, effective gainst a wide array of
Fenstan, Folithion, Mep, pests
Metathion, Micromite Pestroy,
Sumithion, Verthion
12
A Acaricides or Miticides

Acaricides or Miticides, Table 1 (Continued)

Name** (chemical type) General Use (GU)*** Potential use
Some trade names Restricted Use (RU)
Formothion (organophosphate) RU, Class II Systemic and contact insecticide
Aflix, Anthio, Sandoz S-6900 and acaricide, used against spider
mites on tree fruits, vines, olives,
hops, cereals, sugar cane, rice
Hexythiazox (ovicide, growth Class III Ovicide/miticide effective against
regulator) Savey spider mites on tree fruits,
christmas trees, strawberries,
hops, peppermint, caneberries
Lambda cyhalothrin (pyrethroid) RU, Class II Insecticide and acaricide used to
Charge, Excaliber, Granade, control a variety of pests in
Hallmark, Icon, Karate, Matador, cotton, cereals, hops,
Saber, Sentinel ornamentals, potatoes,
vegetables; controls ticks
Lindane (organochlorine) RU, Class II Most uses cancelled in Insecticide and fumigant; used in
Agrocide, Benesan, Benexane, USA because of potential to cause lotions, creams and shampoos for
BHC, Gammex, Gexane, HCH, Iso- cancer control of lice and mites (scabies)
tox, Kwell, Lindafor, Lintox, Lorex- in humans
ane, Steward
Methamidophos RU, Class I Systemic, residual insecticide/
(organophosphate) Monitor, acaricide/avicide with contact and
Nitofol, Tamaron, Swipe Patrole, stomach action, used to control
Tamanox chewing and sucking insects and
mites in many crops outside the
USA
Methidathion RU, Class I Insecticide and acaricide with
(organosphosphate) Somonic, stomach and contact action used
Supracide, Suprathion to control a variety of insects and
mites in many crops
Methomyl (carbamate) Acinate, RU, Class I Broad spectrum insecticide and
Agrinate, Lannate, Lanox, Nudrin, an acaricide to control ticks, acts
NuBait as a contact and systemic
pesticide
Mevinphos (organophosphate) RU, Class I Insecticide and acaricide effective
Fosdrin, Gesfid, Meniphos, Menite, against a broad spectrum of pests,
Mevinox, Mevinphos, Phosdrin, including mites and ticks; use
Phosfene cancelled in greenhouses
Monocrotophos RU, registration in USA withdrawn Systemic and contact insecticide
(organophosphate) Azodrin, in 1988 and acaricide
Bilobran, Monocil 40, Monocron,
Nuvacron, Plantdrin
Naled (organophosphate) GU, Class I Contact and somach insecticide
Bromex, Dibrom, Lucanal and acaricide, used against mites
in greenhouses
Oxamyl (carbamate) RU, Class I granular form is banned Insecticide/acaricide/nematacide
in USA that controls a broad spectrum of
mites, ticks and roundworms on
field crops, vegetables, fruits,
ornamentals
 Acaricides or Miticides
A 13

Acaricides or Miticides, Table 1 (Continued)

Name** (chemical type) General Use (GU)*** Potential use
Some trade names Restricted Use (RU)
Neem oil Trilogy Broad spectrum fungicide and
acaricide in citrus, deciduous
fruits and nuts, vegetables, grains
Permethrin (pyrethroid) Ambush, Class II or III, depending on Broad spectrum used on nut, fruit,
Cellutec, Dragnet, Ectiban, formulation RU in agriculture vegetable, cotton, ornamentals,
Indothrin, Kafil, Kestrel, Pounce, because of adverse effects on mushrooms, potatoes, cereals, in
Pramex, Zamlin, Torpedo aquatic organisms greenhouses, home gardens, on
domestic animals
Petroleum oils (refined petro- Class IV Kills by contact a wide range of
leum distillate) Sunspray and mite and insects; complete
others coverage is essential; may act as a
feeding or oviposition deterrent.
Phytotoxicity can occur if plants
are stressed, especially by lack of
water; some plant cultivars are
more susceptible than others.
Used as dormant and as foliar
sprays.
Phorate (organophosphate) RU, Class I Insecticide and acaricide used on
Agrimet, Geomet, Granutox, pests, including mites, in forests,
Phorate Rampart, Thimenox, root and field crops, ornamentals
Thimet, Vegfru and bulbs
Phosalone (organophosphate) GU, No longer for sale in USA due Broad spectrum insecticide/
to carcinogenic effects acaricide used on deciduous
trees, vegetables, cotton.
Phosmet (organophosphate) GU, Class II, some tolerances in Broad spectrum insecticide, used
foods changed in 1994 by EPA to control insect and mites on
apples, ornamentals, vines; is
used in some dog collars.
Propargite (organosulfide) GU Acaricide used in many crops but
Comite, Omite not USA
Rosemary oil (rosemary essential Meets requirements of USDA Broad spectrum contact
oil) Hexacide National Organic Program Exempt insecticide/miticide used in fruits,
from FIFRA nuts, vegetables. Could be
phytotoxic on some cultivars.
Soybean oil (essential oil) Low acute toxicity to humans,
generally recognized as safe
Spinosad (macrocyclic lactone) Broad spectrum insecticide and
Conserve miticide used on ornamentals and
in greenhouses.
Sulfur (sulfur) Cosan, Hexasul, GU, Check label for restrictions Fungicide and acaricide; used to
Sulflox, Thiolux control plant diseases, gall mites,
spider mites, used widely in food
and feed crops, ornamentals, turf
and residential sites; a fertilizer or
soil amendment, mixing with oil
can cause phytotoxicity
14
A Acaricides or Miticides

Acaricides or Miticides, Table 1 (Continued)

Name** (chemical type) General Use (GU)*** Potential use
Some trade names Restricted Use (RU)
Triforine (piperazine derivative) RU, Class I Fungicide used on almonds,
apples, asparagus, berries,
cheeries, hops, ornamentals,
peaches, rose; also controls spider
mites
Wintergreen oil (contains methyl Exempt from FIFRA Used to control mites (Varroa) in
salicylate) honey bees; causes contact
mortality and reduced fecundity
when mites feed on syrup

* The list is based on chemicals currently registered in the USA, which can change as new information regarding
environmental impact and human health effects become available. Inclusion in this list does not necessarily indicate that
the products are effective acaricides; application methods and resistance levels in individual mite populations can affect
efficacy.
**Most have a variety of trade or other names, as well as different formulations, which can affect their toxicity.
***Restricted Use (RU) means that pesticides may be purchased and used only by certified applicators. Check with
specific state regulations for local restrictions.

Mode of Entry
95
90 Chapla A pesticide can enter and kill mites as stomach
reciprocal F1 females
80 poisons, contact poisons, and or as fumigants.
A systemic acaricide is absorbed into a plant or
60
animal and protects that plant or animal from
40
pests after the pesticide is translocated through-
20 out the plant or animal.
10 Bidart
5
Chemical Structure
101 102 103
ppm propargite Pesticides are classified as organic or inorganic.
Inorganic pesticides do not contain the element
Acaricides or Miticides, Figure 6 This is a
carbon (but include arsenic, mercury, zinc, sulfur,
concentration-response curve showing the
boron, or fluorine). Most inorganic pesticides have
responses of a colony of Tetranychus pacificus
been replaced by organic pesticides.
resistant (Bidart) and susceptible (Chapla)
to propargite (Omite). The mortality of adult
females at different concentrations has Source
been transformed into a straight line. The
concentration-responses of the reciprocal F1 Organic pesticides include botanicals (natural
females in crosses between the susceptible organic pesticides) produced by plants (such as
and resistant populations are intermediate and natural pyrethrums, nicotine, rotenone, essential
similar. oils such as those from the neem tree, soybean
 Acaricides or Miticides
A 15

oil). Essential oils are any volatile oil that gives formulations also can influence toxicity to dif-
distinctive odor or flavor to a plant, flower or ferent species of both insects and mites.
fruit, such as lavender oil, rosemary oil, or citrus Many insecticides are effective acaricides (or
oil. Essential oils have been registered as pesti- at least they were before resistance to them devel-
cides since 1947 and at least 24 different ones are oped). For example, many OPs (such as azinphos-
available in registered products. These are used as methyl, parathion, ethion, dimethoate) were toxic
repellants, feeding depressants, insecticides, and to spider mites until resistance to these products
miticides. Botanicals have relatively high LD50 developed. Likewise, carbamates, formamides, and
values to mammals, so usually are considered many pyrethroids have both insecticidal and aca-
safe to humans. Some newer pesticides are ricidal properties. Other products have both fun-
derived from microbes, such as avermectin or gicidal and acaricidal properties. The reasons as to
spinosad. why these products are effective on particular tax-
Synthetic organic pesticides are commonly onomic groups are generally unknown.
used in pest management programs and can be
separated into groups based on their chemistry.
Themain groups are: chlorinated hydrocarbons Acaricide Types
(such as DDT and chlordane, which are banned
from use in most parts of the world), organo- Pesticide registrations change frequently so some
phosphates (such as malathion, parathion, azin- of the materials listed here may be obsolete. Always
phosmethyl), carbamates (carbaryl, propoxur), check with state and federal authorities to be sure
pyrethroids (permethrin, fenvalerate),and a products containing these active ingredients are
variety of newer products with very different registered for use. Always read labels carefully and
chemistries including nicitinoids, pyrroles, car- follow the directions completely.
bazates, and pyridazinones.

Chlorinated Hydrocarbons
Insecticides as Acaricides
Dienochlor (Trade name=Pentac) is a chlorinated
Many insecticides have acaricidal properties. hydrocarbon acaricide with long residual activity.
Sometimes an insecticide is more effective as an It has been used in greenhouses and on outdoor
insecticide than as an acaricide (lower concen- ornamentals. Pentac cannot be used on food crops
trations are required to kill the insect than are and has short residual activity when used outdoors.
required to kill the mite species). Some products It has a rapid effect on mites, stopping their feeding
are more toxic (often for unknown reasons) to within hours. Endosulfan and DDT have also been
mites than to insects. We think that mites have used as acaricides (as well as insecticides).
the same fundamental physiological responses
to toxic chemicals as insects, although mite
physiology and responses to pesticides have been Essential Oils
studied less often. Different mitespecies appear
to respond differently to different products, Soybean oil was first registered in 1959 for use as
which could be due to behavioral differences an insecticide and miticide. Three products cur-
(feeding behavior, location on plant, activity rently are registered to control mites on fruit trees,
levels), differences in cuticle thickness, differences vegetables and a variety of ornamentals. Soybean
in detoxification rates, or other biochemical, oil is not phytotoxic under most conditions. Many
morphological or behavioral factors. Different of these oils are approved for organic farming.
16
A Acaricides or Miticides

Inorganics Different types of petroleum oils are used with

different molecular weights. Most oils used are dis-
Sulfur is a good acaricide and fungicide, although it tillations of petroleum, although some oils derived
can be phytotoxic (cause plant injury), especially if from plants (sesame, almond, citrus) are used.
plants are not well watered during hot weather. Sul- Crude petroleum oil is a complex mixture of
fur is probably the oldest known acaricide. Sulfur hydrocarbons with both straight chain and ring
(dusts, wettable p owders and flowable formulations) molecules. Crude oil is separated into a range of
are usually highly effective acaricides for spider mites products by distillation and refining. The lightest
and rust mites, with two known exceptions. fractions include gasoline, kerosene, diesel and jet
Spider mites in California vineyards (Tetrany- fuel. As these lighter fractions distill or boil, they
chus pacificus and Eotetranychus willamettei) are separated into different fractions. Spray oils are
developed resistance to sulfur, probably because derived from the lighter lubricating oil fraction
sulfur was applied up to 20 times a season over and distill at a temperature range of 600 to900C.
many years to control powdery mildew. After a Currently used petroleum oils in the USA are
number of years, these spider mites became pests narrow-range oils and have had the waxes, sulfur,
because they were no longer controlled by the sul- and nitrogen compounds removed. Labels on
fur which had been applied to control powdery sprays usually describe the degree to which the
mildew. A number of years later, a predatory mite sulfur compounds have been removed and the
called Metaseiulus occidentalis was demonstrated percentage of active oil. The sulfur compounds
to have developed a resistance to sulfur. The resis- arelikely to cause phytotoxic effects, so the degree
tance to sulfur in this natural enemy of spider of removal of these compounds (called the UR
mites is based on a single major dominant gene; rating) is an important piece of information on
once the predator became resistant to sulfur it the label and commonly is greater than 92%. The
became an effective predator of spider mites in composition of oil should be greater than 60%.
San Joaquin Valley vineyards in California. Since the mid-1960s, narrow-range horticul-
The resistance to sulfur in M. occidentalis is tural oils have been used both as dormant or sum-
unusual; even very high rates of sulfur are non- mer oil sprays. These highly refined and narrow
toxic to the resistant populations. Interestingly, range petroleum oils rarely cause phytotoxicity and
populations of this predator collected from nearby increasingly are used for controlling both insect
almond orchards in California are susceptible to and mite pests on deciduous trees, citrus, and orna-
sulfur, indicating that populations are subjected to mental trees and shrubs. Oils have a wide range of
local selection and evolution. No genetic analyses activity against scales, mites, psyllids, mealybugs,
have been conducted on the resistance to sulfur in whiteflies, leafhoppers, and eggs of mites, aphids
the spider mites, so their mode of inheritance to and some Lepidoptera. Heavier dormant sprays are
sulfur resistance remains unknown. The biochem- used to control overwintering pests in deciduous
ical mechanism of resistance is unknown for both trees and vines. Summer oils are used to control
spider mites and their predators. pests during the growing season.
Oil kills mites and their eggs by contact. The
toxicity appears to be due to suffocation of the pest,
Petroleum Oils although it may also be due to chemical effects. Oils
block spiracles, reducing the availability of oxygen
Petroleum oils are excellent insecticides/acari- and suffocation occurs within 24 h. Penetration and
cides/fungicides for integrated mite management corrosion of tracheae, damage to muscles and
programs and have been used in pest management nerves may also contribute to the toxicity of oils.
programs for over 100 years. Oils are sometimes a repellent to pests. Once the oil
 Acaricides or Miticides
A 17

dries it is no longer toxic to most natural enemies; Organotins

thus the very short residual activity of oil makes it a
useful material for integrated mite management Cyhexatin (Plictran) and fenbutatin-oxide (Ven-
programs, although it also means that there is no dex) are examples of tin compounds that are pri-
residual toxicity to the pests. marily acaricides and fungicides. Plictran (cyhexatin)
No resistance to oils has been reported in pest was introduced in 1967 and was widely used for
arthropods, including mites, perhaps because oils many years before resistance developed in spider
have a relatively short residual activity. Oils are easy mites. Some people had assumed that the organotins
to apply, relatively inexpensive, and safe to handle. were immune to resistance problems. The organo-
They are relatively harmless to vertebrates, dissipate tins were useful products because they were more
quickly after spraying, and leave little or no residue toxic to spider mites than to phytoseiids and thus
on crops. Oils man be used by organic farmers. were very useful in integrated mite management
A disadvantage to petroleum oils is that they programs. Fenbutatin-oxide (Vendex) is another
have little residual activity and kill only upon organotin. These products were taken off the market
contact, so thorough and precise coverage is nec- in the USA due to concerns about safety.
essary to achieve effective control. Phytotoxicity
can occur even with these narrow-range oils, espe-
cially if plants are weakened or under moisture Insecticides with Acaricidal
stress. Thus, applications should not be made dur- Activity
ing droughts, or periods of very high temperatures.
Some varieties of plants are more susceptible to Organophosphorus Pesticides
phytotoxicity than others, so caution should be
taken when using oils for the first time on a par- The organophosphates (pesticides that include
ticular crop or cultivar. Oils are not compatible phosphorus) are derived from phosphoric acid
with sulfur or some other pesticides, causing seri- and are the most toxic of all pesticides to verte-
ous phytotoxicity problems. brates. They are, in fact, related to nerve gases by
structure and mode of action. Organophosphorus
pesticides (OPs) are less persistent in the environ-
Organosulfurs ment than the organochlorines such as DDT.
Organophosphorus pesticides (such as azin-
Tetradifon (Tedion) and propargite (Omite, Komite) phosmethyl, parathion, ethion, demeton, dimethoate)
are organosulfurs. These products contain sulfur as function by inhibiting important enzymes (cholin-
a central atom with two phenyl rings. Tedion is par- esterases) in the nervous system. Acetylcholine is the
ticularly toxic to mites, but has very low toxicity to chemical signal that is carried across synapses (where
insects. Organosulfurs are often ovicidal as well as the electrical signal is transmitted across a gap to a
toxic to active stages. Propargite was used for many muscle or another neuron. After the electrical signal
years (more than 20) and appeared to some to be (nerve impulse) has been conducted across the gap
immune to the development of resistance in spider by acetylcholine, the cholinesterase enzyme removes
mite populations. However, propargite resistance the acetylcholine so the circuit wont be kept on.
has now developed in many populations of spider When OPs poison an organism, the OP attaches to
mites around the world. Propargite is less toxic to the cholinesterase so it cannot remove the acetylcho-
beneficial phytoseiid predators than to pest spider line. The circuits then remain on because acetylcholine
mites, and thus could be used in integrated mite accumulates. This gives rise to rapid twitching of the
management programs, although at high concen- voluntary muscles and to paralysis, which is can be
trations it also is toxic to phytoseiid predators. lethal if it persists in the vertebrate respiratory system.
18
A Acaricides or Miticides

Not all OPs are highly toxic to vertebrates; Pyrethroids

if the phosphorus is modified by esterification
(adding oxygen, carbon, sulfur and nitrogen), six Many of the pyrethroids have acaricidal activity.
different classes of OPs can be produced. Some of Some (such as bioresmethrin, fenpropathrin and
these are relatively safe to vertebrates, such as mala- bifenthrin) are considered effective acaricides.
thion. The use of most OPs is being eliminated in Unfortunately, pyrethroids usually are very toxic
the USA due to the Food Quality Protection Act. to beneficial arthropods, including phytoseiid
predators. These detrimental effects can be very
long lasting because the residues persist a long
Carbamates time. Few have been found useful for integrated
mite management programs for this reason. Labo-
Carbamates (aldicarb, carbofuran, methomyl, ratory selection of phytoseiids ( Amblyseius falla-
propoxur) are derivatives of carbamic acid. The cis, Metaseiulus occidentalis, Typhlodromus pyri)
mode of action of carbamates is to inhibit cholin- for resistance to two pyrethroid insecticides has
esterase. The carbamates were introduced in the been successful. The pyrethroid-resistant strains
1950s. Carbaryl (Sevin) is one of the most popular were developed for use in apple pest management
products available to home gardeners for control- programs using both laboratory and field selec-
ling a variety of insect pests and has low mamma- tion methods.
lian oral and dermal toxicity. Methomyl (Lannate)
and aldicarb (Temik) are examples of other
carbamates. Pyrroles
Sevin is well known to induce outbreaks of spi-
der mites after applications are made to control Pyridaben is a novel pyrrole pesticide that works as
other pests. The outbreaks are due to two factors; (i) a mitochondrial electron transport inhibitor to
Sevin kills phytoseiid predators and other natural block cellular respiration, causing pests to become
enemies of spider mites, and (ii) it stimulates repro- uncoordinated and die. Can be used on both insects
duction of spider mites, a process called hormoligo- and mites.
sis. Even very low doses of Sevin appears to act like a
hormone to stimulate reproduction of the two-spot-
ted spider mite Tetranychus urticae. It is likely that Other Acaricides
the use of carbamates also will be eliminated or
greatly reduced in the USA due to the Food Quality Azadirachtin
Protection Act.
This is a triterpenoid extracted from the seeds
of the neem tree Azadirachta indica. Extracts
Formamides include a combination of compounds, the pro-
portion of which vary from tree to tree. Such
Formamides include chlorodimeform (Galecron or variability in this natural product makes it diffi-
Fundal), amitraz, and formetanate (Carzol). These cult to predict the precise effect of the product
products are effective against the eggs of Lepi- when extracted by local people. Commercial
doptera and also against most stages of mites and products may be more consistent in their effect
ticks. The mode of action of these products is because they have been tested to confirm their
unclear, but thought to be due to the inhibition of quality and are blended to achieve a consistent
monoamine oxidase, which results in the accumu- product. Azadirachtin blocks the action of the
lation of compounds called biogenic amines. molting hormone ecdysone.
 Acaricides or Miticides
A 19

Avermectin in spider mite populations in several locations

around the world, including Europe and Australia.
Avermectin is a natural product containing a macro-
cyclic lactone glycoside that is a fermentation product
of Streptomyces avermitilus, which was isolated from
Tebufenpyrad
soil.Avermectin is actually a mixture of two homologs,
This is a phenoxypyrazole and has been evaluated
both of which have biological activity. Avermectin has
under the trade name Pyranica in Australia, where
insecticidal and acaricidal properties and is closely
it was shown to be useful in integrated mite
related to ivermectin, which kills nematodes.
management programs in apples because it is selec-
At appropriate rates, abamectin is less toxic to
tive (relatively nontoxic) to phytoseiid predators.
beneficial phytoseiids than to spider mites; it para-
lyzes active spider mite stages, but is not toxic to
eggs. Avermectin has translaminar activity (mean- Acaricides and Fungicides
ing it is taken up by the plant tissue and subsequently
by spider mites feeding on the planttissues), but has Benomyl is a carbamate that has been used pri-
a short residual toxicity to phytoseiids. marily as a fungicide, but also has acaricidal prop-
Resistance to this product has been reported in erties. Benomyl is interesting because it acts as a
some populations of spider mites. A resistant strain sterilant of phytoseiid predators. Adult phytoseiid
of M. occidentalis was obtained after laboratory females treated with benomyl survive, but they do
selection, suggesting that resistance mechanisms not deposit eggs. This product apparently disrupts
may be present in field populations. spindle fiber formation in cells and interferes in
The mode of action of avermectin involves the synthesis of DNA, resulting in females that are
blocking the neurotransmitter gamma-aminobutyric unable to reproduce.
acid (GABA) at the neuromuscular junction. Mites
that are exposed to abamectin become paralyzed
and, although they do not die immediately, the para- Resistance in Mites
lyzed mites do stop feeding.
Resistance to pesticides is an increasingly serious
problem around the world. Resistance to one or
Clofentezine and Hexythiazox more pesticides has been documented in more
than 440 species of insects and mites. Spider mite
These are very interesting growth regulators of and tick species have readily developed resistance
mites; they kill eggs (ovicides) of spider mites, but to all classes of pesticides.
not the active stages of spider mites. The products Resistance is a decreased response of a popula-
have different chemistries, but both are nontoxic to tion of animal to a pesticide or control agent as a
phytoseiid mite eggs or active stages! In fact, the result of their application. It is an evolutionary or
phytoseiid mite Metaseiulus occidentalis can be genetic response to selection. Tolerance is an innate
fed a diet consisting solely of spider mite eggs ability to survive a given toxicant dose without prior
thathave been killed with these products and the exposure and evolutionary change. Cross resistance
predator females reproduce and their progeny is a genetic response to selection with compound A
develop normally. This selectivity makes the products that generates resistance to both compound A and
particularly useful for integrated mite management other compounds (B and C). Multiple resistance is
programs because predators can be maintained resistance to different compounds due to the coex-
while suppressing spider mite populations. Unfor- istence of different resistance mechanisms in the
tunately, resistance to these products has developed same individuals. Multiple resistances usually are
20
A Acaricides or Miticides

generated by sequential or simultaneous selection Slide Dip Bioassays

by more than one type of pesticide. Slide dip bioassays of adult female spider mites and
phytoseiids have been proposed as a standard
method for assessing resistance or tolerance. This
Methods for Evaluating Resistance method involves placing adult female on their backs
on to double-sided sticky tape applied to glass
There are a variety of methods available for assess- microscope slides and dipping the slides into a spe-
ing resistance to pesticides in mites. The test method cific pesticide concentration. This method has the
chosen will depend upon the goals of theresearcher. virtue of being relatively rapid and easy to conduct.
Each method has strengths and weaknesses. However, measuring toxicity to adult females after
Resistance is a genetically-determined change 24 or 48 h is not an appropriate assay for many pes-
in the ability to tolerate a pesticide. Therefore, one ticide types (for example ovicides, growth regula-
must have at least two different populations to test tors). Also, the results probably bear little relation to
one that is putatively resistant and one that exhib- the field toxicity of the product. It is very likely that
its the normal, wild type response. Unless these two many products are much more toxic to the mites
populations can be compared under identical labo- using this assay than they would be under field con-
ratory conditions, it is difficult to document resis- ditions, where mites can feed and move around and
tance because historical data are of questionable coverage is rarely complete, so this method may give
value in assessing whether a population is resistant. no information about whether the resistance level
This is because it is very difficult to conduct identi- induced is relevant to field concentrations used.
cal bioassays in two different laboratories, even
when attempts are made to use the same methods.
Leaf Dip or Leaf Spray Bioassays
Small differences in techniques can result in very
Leaf dip or leaf spray bioassays involve placing
large differences in toxicity data. For example, spi-
mites on leaf disks, which are then sprayed or
der mites tested on smooth leaves may respond
dipped into a specific concentration of pesticide.
very differently than spider mites tested on the same
This type of bioassay provides an exposure that is
plant species but on a variety with hairy leaves.
more similar that the mites would experience
Small differences in formulations and temperature
under field conditions and it is possible to mea-
also influence responses of mites to pesticides. Small
sure survival, fecundity, and ability to successfully
differences in age or feeding status also influence
develop on pesticide residues.
toxicity responses. Most conclusions about resis-
tance should be based on comparative data obtained
Whole Plant Bioassays
by the same researcher under identical conditions.
This approach, which involves spraying the entire
The apparent failure of a product to control a
plant, is very realistic, unless the plants (and pesticide
mite population under field conditions is NOT ade-
residues) are not exposed to sunlight or rain.
quate evidence for resistance. Field failure is a reason
to investigate further, but field failures can occur
for a variety of reasons that have nothing to do with Field Tests
resistance. Failures could occur because the pesti- Field trials are the most realistic method for assess-
cide applicator may have mixed the product improp- ing resistance, but it can be difficult to determine
erly, coverage may have been inadequate, the pH of why the predators or spider mites died (did other
the water used to mix the pesticide could have tolerant predators fly in and eliminate the pest?). If
altered the toxicity of the product, and the product adequately replicated over time and space, field trials
could have been old or degraded due to improper provide very relevant information. The relevance of
storage. application method (high or low volume), coverage,
 Accessory Gland
A 21

and droplet size can be assessed. Unfortunately, field the University of California-Davis, Oregon State, Michi-
trials are the most expensive to carry out so the gan State, Cornell and the University of Idaho.
Roush RT, Tabashnik BE (1990) Pesticide resistance in
methods described above are often used to save time arthropods. Chapman and Hall, New York, NY
and funds.
Insecticides
Insecticide Toxicity Accessory Cell
Insecticide Formulation
Detoxification Mechanisms in Insects A wing cell not normally present in the taxon.
Pesticide Resistance Management
Pesticide Application Accessory Circulatory Organ
Although the dorsal vessel (heart) is normally con-
References sidered to be the organ responsible for blood circu-
lation in insects, sometimes small sac-like structures
Cranham JE, Helle W (1985) Pesticide resistance in Tet-
ranychidae. In: Helle W, Sabelis MW (eds) Spider
are located at the base of appendages (antennae, legs,
mites: Their biology, natural enemies and control, vol. wings). These structures are capable of contractions
1B. Elsevier, Dordrecht, The Netherlands, pp. 405421 independent of the dorsal vessel, and assist in circu-
Croft BA (1990) Arthropod biological control agents and pes- lation. This is also called accessory pulsatile organ.
ticides. Wiley-Interscience, New York, NY
Davidson NA, Dibble JE, Flint ML, Marer PJ, Guye A
(1991) Managing insects and mites with spray oils. IPM
Education and Publications, Statewide IPM Project, Accessory Gland
Publication 3347. University of California, Division of
Agricultural Natural Resources, Oakland, California. A gland associated with the male or female repro-
EXTOXNET: extoxnet@ace.orst.edu This site provides infor-
mation about pesticides, including concepts in toxicology
ductive system, and producing substances associ-
and environmental chemistry. It is a cooperative effort of ated with the sperm or eggs, respectively (Fig. 7).
Male accessory glands produce such substances to

ovary
ovariole
calyx
lateral oviduct
spermatheca
accessory
gland
median oviduct
vagina

Accessory Gland, Figure 7 Diagram of the female reproductive system, as found in Rhagoletis (Diptera)
(adapted from Chapman, The insects: structure and function).
22
A Accessory Vein

facilitate sperm transfer, as a barrier to further Sampling Arthropods

insemination, as a means of altering female behav-
ior, and as a means of providing nutrition to the
female. Females produce substances for packaging Acephalous
their eggs, adhering them to a substrate, and provid-
ing a protective coating over the eggs. The condition of lacking an apparent head. This
term is usually applied to certain flies and wasps
that lack a well-defined head.
Accessory Vein
An extra branch of a longitudinal vein. Such veins Acerentomidae
normally are designated by a subscript of a.
Wings of Insects A family of proturans (order Protura).
Proturans
Accessory Hearts
Acetylcholine
Pulsatile, sac-like organs that assist in circulation of
the hemolymph into appendages such as the anten- The synaptic transmitter substance found in the
nae, wings, and legs. insect central nervous system. When released into
the synaptic cleft, it is bound to a receptor, depo-
Accidental Host larizing the postsynaptic membrane and stimulat-
ing nervous excitation.
A host in which the pathogenic microorganism
(or parasite) is not commonly found.
Acetylcholine Esterase
Accidental Species An enzyme that breaks down acetylcholine after it
is released into the synaptic cleft of insect neurons.
Species that occur with a low degree of consistency Interference with acetyl choline esterase, as by
in a community type. Such species are not useful exposure to some insecticides, results in prolonged
for community definition. stimulation of the nerves.

Acclimation
Achilidae
The adaptation of an organism s physiological
A family of insects in the superfamily Fulgoroidae
responses to existing environmental conditions. A
(order Hemiptera). They sometimes are called
nearly equivalent term is acclimatization, though
planthoppers.
acclimation may be a more rapid or laboratory-based
Bugs
phenomenon, whereas acclimatization is a long
term, field-based phenomenon.
Aclerididae
Accuracy
A family of insects in the superfamily Coccoidae
A measure of the closeness of an estimate to the (order Hemiptera).
true mean or variance of a population. Bugs
 Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)
A 23

Acoustical Communication in a stationary portion are needed. The movable

Heteroptera (Hemiptera: part is called the plectrum or scraper. The sta-
Heteroptera) tionary portion may be called the stridulitrum,
file, strigil (strigile, strigilis) or lima (pl., limae).
marta goula The stridulitrum is typically striated or finely
University of Barcelona, Barcelona, Spain tuberculated, and the plectrum is a structure with
a well-defined lip or ridge, tubercles, or provided
Acoustic signaling is found in many hemipteran with spines.
families. It serves a variety of purposes, particu- Different parts of the body may be involved
larly defensive behavior such as repelling poten- to function as the stridulatory device. The fore-
tial predators and signaling alarm or distress, wing edge is most commonly used as a stridu-
but also for species spacing within a particular litrum (file), while the hind femur is the most
habitat, reproduction, and coordination of group usual structure used as a plectrum (scraper).
actions. Vibratory signals for reproductive pur- Other stridulitrum may be located in the head,
poses may be produced by males and/or females, associated with the mouth (labium, maxillary
leading toaggregation to mate attraction, court- plate), the thorax (propleurum, metapleuron,
ship and copulation. Non-receptive females prosternal groove), the wings (metathoracic wing
may sing to reject copulation (male-deterring vein, hypocostal lamina or articulatory sclerite,
stridulation), as in the subfamily Triatominae underside of clavus), the legs (forecoxa, mesotro-
(Reduviidae) and in Pentatomidae (e.g., Nezara chanter, tibia, femora), and the abdomen (sternum,
viridula). the connexival margin, posterior margin of the
The vibratory signals produced by many pygophore). There are also a variety of locations
insect species cannot be heard by the human ear for the plectrum or scraper: the rostrum, the legs
because the sounds are low frequency and gener- (forecoxal cavity, coxal peg, hind tibia, and fore-,
ally transmitted by mechanical vibrations through middle or hind femur) or the abdomen. Some
the substrate, and not by the air. The study of stridulatory devices are present in several fami-
acoustical communication has greatly progressed lies, whereas others are only known from a few
in accordance with improvement of recording and genera or even a single species.
analyzing equipment, including the necessary Examples of stridulation devices are that of
computer software. the Corixidae (spinose area inside the front femur
against the clypeus, genitalia against abdomen
segments), Scutelleridae (wart-like, toothed tuber-
cles in the hind tibia against the femur), Reduvii-
Production of Vibrational Signals dae (tip of the labium against a cross-striated
and Songs furrow (Fig. 8) in the prosternal groove), some
Pentatomoidea and Lygaeiodea (dorsal abdominal
Vibrational signals and songs are produced by files against teeth on the under-sides of the hind-
stridulation (stridulatory device, stridulatory wings), some Miridae, Lygaeidae, Largidae and
organs), by body vibration, or by a simple tymbal Alydidae (hind femur against forewing edge) and
mechanism. Stridulation occurs widely in Het- some other Pentatomoidea (tubercles on the hind
eroptera, and is the act of producing sound or femora against strigose regions on abdominal
vibration by rubbing together certain body parts. sterna).
The first systematic survey of sound-producing Morphological differences in the stridulatory
devices in the Heteroptera was that of Handlirsh device may, in some cases, be related to differences
in 1900.To stridulate, usually both a movable and in the songs emitted by either males or females, as
24
A Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)

A tymbal is formed by abdominal tergal

plates fused together and which vibrate over a
hollow chamber within the abdomen. The tymbal
is activated by muscular contractions and pro-
duces body vibrations that are low frequency.
Tymbals have been found in Piesmatidae, Pen-
tatomidae, Acanthosomatidae, Cydnidae, Lygaei-
dae, Coreidae and possibly Reduviidae, and
similar vibration-producing mechanisms have
been found in Plataspidae and Rhopalidae. Dif-
ferences exist about precise abdominal parts
and muscle contraction mechanisms among the
tymbals of different families. For example, the des
Acoustical Communication in Heteroptera cription of the N. viridula tymbal follows: The
(Hemiptera: Heteroptera), Figure 8 The stridulatory first and second abdominal tergites are fused into
apparatus in Reduviidae: the tip of the labium a forward-backward movable tymbal-like plate
is rubbed against a cross-striated furrow in the that is loosely fixed, anterior and posterior, to the
prosternal groove. thorax and to the third abdominal tergum, by a
chitinous membrane, and more firmly, laterally,
occurs in the burrower bugs (Fig. 9) Scaptocoris to the pleurites. Longitudinal and lateral com-
castanea and S. carvalhoi. In S. castanea, males pressor muscles contract synchronously and in
have a longer stridulitrum than females. However, phase with these vibratory waves.
in S. carvalhoi the stridulitrum length does not dif- All Heteroptera species investigated so far
fer between sexes. Instead, in S. carvalhoi the male emit low frequency narrow-band signals by body
stridulitrum has more teeth than in the female stri- vibration, and/or broadband signals produced by
dulitrum. There are no intersexual differences for stridulation. For example, in Cydnidae and Pen-
this latter morphological trait in S. castanea. tatomidae, vibratory mechanisms produce a low
Differences in the stridulatory apparatus frequency vibration (around 100 Hz), and the
maybe related to interspecific differences, with a stridulatory vibration extends up to 10 kHz.
specific diagnostic value. In the genus Triatoma
(Reduviidae), it is possible to distinguish between
T. guazy and T. jurbergi at any nymph stage or in Reception of Vibrational Signals
the adults by studying the stridulatory sulcus (stri- and Songs
dulitrum). As T. jurbergi is naturally infected with
Trypanosoma cruzi, the causal protozoan of Cha- Although sound production is found quite widely
gas disease (American trypanosomiasis), identifi- in Heteroptera, it is not common to find structures
cation of specimens along their whole life cycle is specialized for sound reception. Sound reception
of great medical importance. in Heteroptera is possible due to the presence of
In other instances, morphological differences either scolopophorous organs or tympanal organs.
in the stridulatory device do not cause differences Scolopophorous organs are mechanoceptors,
in their song patterns. For example, in Reduviidae and they occur widely in insects. They are com-
of the subfamily Triatominae, individuals of the posed of sensory sensilla (scolopodia), which may
same species have stridulatory grooves with differ- be arranged in groups, and are distally attached to a
ent inter-ridge distances, though the frequency membrane in the body wall or to the body wall
spectra and repetition rates are similar. itself. Scolopophorous organs may be located in
 Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)
A 25

antennae (Johnstons organ), legs (subgenual are four scolopodial organs: femoral, tibial, tarso
organ, joint chordotonal organ), thoracic pleura, or pretarsal and subgenual organs. The receptor neu-
abdominal terga. rons may be low frequency (most sensitive between
Legs are the site of sensory organs that detect 50 and 100 Hz) or high frequency sensitive (there
vibratory signals with highest sensitivity. For exam- are two types: middle frequency neurons being
ple, at the dorsal side of each leg of N. viridula there sensitive around 200 Hz, and higher frequency

a b

c d

Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 9 Interspecific

differences in the stridulatory devices found in females of the burrower bugs Scaptocoris castanea
and S. carvalhoi (Hemiptera: Cydnidae). Images a and b are S. castanea; images c and d are
S. carvalhoi. Images a and c show the stridulitrum in the postcubital vein of the hind wings (scale
bar=100 ); images b and d show the central section of the stridulitrum, showing details of the teeth
(scale bar=10 ) (adapted from okl et al (2006) Physiol Entomol 31:371381).
26
A Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)

neurons sensitive around 7001000 Hz). Also, the Substrate-borne vibrations are less costly to
Johnstons organ of N. viridula has several vibra- the emitter. Also, substrate-borne vibrations are
tory sensitive organs which respond in the fre- more far-reaching signals for intraspecific com-
quency range between 30 and 100 Hz. When munication and not easily perceived by a potential
standing on its host plant, the male of N. viridula, predator or parasitoid. Usual substrates to trans-
by different combinations of legs and antennae, mit vibrational signals are plants or soil.
may compare the vibratory signals on two branches The characteristics of plants as transmission
of the host plant, and choose the best one in order media for insect-produced vibrations have been
to locate the singing female. The most probable described, and in many respects they determine
mechanism underlying resolution of direction by signal production and the mode of reception.
vibratory cues (vibratory directionality) may be Depending on the physical properties of the host
time-of-arrival differences (perception of vibratory plant, the vibratory signals are transmitted effec-
signals by two different receptors in the insect). For tively or not. Vibrations can be transmitted all along
example, when legs of the receptor bug are sepa- the stem, but the physical properties of a plant (e.g.,
rated by 2 cm, a time-of-arrival difference between elasticity, water content) affect resonance of insect
0.125 and 0.250 ms is created, very close to that vibrations. For transmission through plants, insects
found in scorpions, where vibrational directional- commonly emit broadbanded-mixed stridulatory
ity is well known. Reduviidae also receive vibratory and vibratory signals. Higher-frequency signals
signals via legs and antennae. Fewer data are avail- produced by stridulation are less relevant for long-
able on leg vibratory receptor organs in other land distance communication through plants. However,
bug species. Among land bugs, no sensory organs narrow-band and low frequency songs are efficient
for airborne sound have been found. in long-distance communication when well tuned
Tympanal organs have been found in the to the resonant spectra of their host plants. The
mesothorax of the Corixidae, and are in contact vibrational pulse reflects when attaining both the
with the physical gill air bubble. They are able to root area and top of the plant, and reflected waves
catch airborne sounds, and to respond to stridula- travel up and down the stem several times. Reflec-
tion frequencies produced by conspecific bugs. tions change the patterns of the input signal. Abiotic
factors (temperature, rain, wind) may significantly
modify plant resonance, masking insect vibratory
Transmission of Vibratory Signals signals and thus the effectiveness of the signal.
and Songs Plant-borne vibrations seem to be important in the
success of group-living, herbivorous insects for
Independent of their mode of production, vibra- locating and remaining in a group of conspecifics,
tional signals may be transmitted by the substrate for locating food resources, and to avoid predation.
(substrate-borne vibrations) or by the air (air- Also, small insects that are not able to emit airborne
borne vibrations). The signals may travel a short sounds efficiently at low frequencies in many cases
or long distance, or travel at a low or high speed. communicate with vibratory signals transmitted
Low-frequency components are more suitable for through plants.
longer-range communication through plants. Low In the stink bug Nezara viridula (Pentatomidae)
frequency signals travel longer distances, but (Figs.10 and 11), a species which has become a
slowly; high frequency signals travel shorter dis- model for all Pentatomorpha in relationship to
tances, but quickly. Long-range vibratory songs acoustical communication, its vibratory signals
are associated with pre-mating calling and vibra- were recorded and described first as airborne
tional orientation, and close-range vibratory songs sound. However, further investigations showed that
are associated with courting rivalry and repelling. their most important mode of transmission is as
 Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)
A 27

substrate-borne vibrations. In N. viridula, a male of soil transmitted signals varied between 1.5 and
could perceive a female calling in a Cyperus stem 2 12.9 ms-1 at a distance of 0.5 cm.
m away from him, mechanically coupled only by
roots and the surrounding earth. Below the leg
of the singing bug, the intensity of signals was Acoustic Characteristics of
about 4 mm s1. On the bottom of the same stem (a Vibrational Signals
distance of 80 cm) it decreased to around 3 mm s1,
and at the place of the receiving bug, 200 cm away, A vibrational signal may be characterized by its
it was approximately 0.5 mm s1. temporal (pulse train duration, repetition times,
When transmitted through the soil, signals inter-pulse intervals) (Fig. 12) and spectral char-
travel a shorter distance and are more attenuated acteristics (dominant frequency). All of these
than when transmitted through a plant stem. For characteristics may be measured by the receptor
example, in Scaptocoris species (Cydnidae) the velocity insect, who may modify its behavior in response
to the message. The dominant frequency of signals
produced by the vibratory mechanism lies between
50 and 200 Hz in most Heteroptera. Between spe-
cies, songs differ in their time structure and ampli-
tude modulation of their units. On the other hand,
spectrally and temporally different pulse trains
trigger the same male behavior in N. viridula.
In Rhodnius prolixus (Reduviidae), the male-
deterring call has a main carrier frequency of about
1500 Hz, and the disturbance stridulation has a main
carrier frequency of about 2200 Hz. In Rhinocoris
iracundus (Reduviidae), low-frequency components
of carrier frequency below 200 Hz are exchanged
with frequency-modulated stridulatory components
whose dominant frequency lies between 1 and
2 kHz. In Triatoma infestans (Reduviidae), distress
songs have a peak of frequency between 700 and
800 Hz, although in other reduviids the carrier fre-
quency may reach about 2000 Hz.
In N. viridula, dominant frequencies between
80 and 150 Hz were found in songs either as air-
borne sounds, or substrate or body vibrations.
Body vibrations are around 100 Hz, and lie close
to the range of best frequency sensitivity of low
frequency receptor cells.

Acoustical Communication in Heteroptera

(Hemiptera: Heteroptera), Figure 10 Oscillograms of Specificity and Variability of
songs emitted by males and females of the southern Vibratory Signals
green stink bug, Nezara viridula (Pentatomidae)
(adapted from okl, Virant-Doberlet (2003) Annu Sounds, especially those involved in the reproduc-
Rev Entomol 48: 2950). tive process (attraction, courtship, copulation),
28
A Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)

Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 11 Laser vibrometer

recordings taken from a plant fed upon by Nezara viridula showing the pattern of recordings at
various distances (in cm) from the point of stimulation (adapted from Miklas et al (2001) J Insect Behav
14:313332).

can be very complex and highly species-specific,

and may be used as taxonomic characters of land
bugs. In contrast, signals are much less specific
when they provide information about enemies,
rival mates, or serve as distress (disturbance or
alarm) signals.
Females of N. viridula sing to trigger the male
approach, and to evoke emission of the male
Inter pulse trains courtship song. Females coming from popula-
Duration interval (IPI)
(D)
tions of different geographic origin emit different
calling songs, which can be differentiated by
Repetition time (RT)
males. Females of N. viridula may emit a song that
rejects copulatory attempts of males and stops
Acoustical Communication in Heteroptera their courting, andthis is also known in the redu-
(Hemiptera: Heteroptera), Figure 12 Temporal viid Rhodnius prolixus. The courtship songs of
parameters of a vibratory signal (adapted from both males and females in different populations
Miklas et al (2003) Behav Process 61: 131142). are not markedly different, but the calling songs
 Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)
A 29

may differ in some features and may be the

source of reproductive isolation among popula-
tions. Nezara viridula produces four different Oscilloscope
Video camera VCR
species and sex-specific songs, and two of them
play a vital role in mate location. There is song
variability within populations (inter-individual
variability). To assess those differences, the tem-
poral song (pulse train duration, repetition
times, inter-pulse intervals) and spectral song
characteristics (dominant frequency) may be Accelerometer Amplifier
measured. Males usually show a preference for
the females of their own population, although Acoustical Communication in Heteroptera
they may recognize females from other popula- (Hemiptera: Heteroptera), Figure 13Experimental
tions as potential partners. setupused to study substrate-borne signals
In Tritoma infestans, stridulation songs dif- produced by stridulation in Rhodnius prolixus
fer in their syllable durations, repetition rate and (Hemiptera: Reduviidae). The accelerometer
main carrier frequency, depending on the song generated a signal with voltage proportional to the
function. Differences come from rubbing their instantaneous acceleration of the moving object,
rostrum (scraper) at different speeds on the pros- electrical signals were amplified and monitored
ternal file. Also in Rhodnius prolixus, the different by an oscilloscope, then this information was
frequency between deterrent and disturbing stored in the sound track of a videotape. Also,
signals can be explained on the basis of a differ- the behavior of the bugs was simultaneously
ent rubbing velocity by the proboscis against the videotaped (adapted from Manrique, Schilman
prosternal stridulatory organ (Fig. 13). (2000) Acta Trop 77:271278).
In Scaptocoris carvalhoi and S. castanea
(Cydnidae), two sympatric burrower bugs, high
individual variation of the dominant frequency Corixidae
was observed in both male and female emissions
(Fig. 14). In Corixidae, males or both sexes use species-
specific sound for mate attraction and in court-
ship. The sounds are produced by stridulation,
Vibratory Signaling in the Families i.e., rubbing together specially modified parts of
of Heteroptera the body, or the partners body.

Vibratory signaling has been reported in several

Dipsocoromorpha and Leptodomorpha, but has Notonectidae
been better studied in the following families:
Veliidae (Gerromorpha), Nepidae, Corixidae, In Notonectidae, males produce species-specific
Notonectidae (Nepomorpha), Reduviidae, Miridae, courtship sounds by rubbing roughened parts of
Tingidae, Nabidae (Cimicomorpha), Aradidae, their front tibiae and femora against a special
Acanthosomatidae, Cydnidae, Pentatomidae, stridulatory region at the base of the rostrum
Scutelleridae, Tessaratomidae, Thaumastellidae, (Fig. 17). In genus Buenoa, the sound can be heard
Colobathristidae, Lygaeidae, Piesmatidae, Largi- at a distance of several meters. While next to the
dae, Alydidae, Coreidae, Rhopalidae (Pentatomor- female, but before clasping her, the sound pattern
pha) (Figs.15 and 16). Selected examples follow: can change.
30
A Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)

Scaptocoris carvalhoi
Male Female

1s
1s

0.2s B
A 0.2s

Scaptocoris castancea
Male Female

1s
1s

0.2s 0.2s

Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 14 Vibratory emissions of male

and female burrower bugs Scaptocoris carvalhoi (above) and S. castanea (below) (Hemiptera: Cydnidae).
A and B designate the two types of female song found in S. carvalhoi. Time scales are marked below
oscillograms (adapted from okl et al. (2006) Physiol Entomol 31:371381).

Reduviidae silent environment, the sound is audible at about

1 m away. A disturbance call hasbeen described
Distress (disturbance or alarm) signals in Reduvii- in the following triatomine species: Dipetalogaster
dae may be produced either as nymphs or adults maxima, Triatoma infestans, T. guasayana, T. sordida,
(males and/or females). In Panstrongylus rufotuber- Panstrongylus megistus and Rhodnius prolixus.
culatus (Reduviidae), stridulation occurs only under In the spined assassin bug, Sinea diadema,
conditions of extreme provocation. Its sound is agonistic interactions between adult females may
audible by the human ear, which is unusual among be resolved by stridulation in 33% of the cases.
stridulating Triatominae, and is similar to the Stridulating individuals retreated more often than
sound of sandpaper scraping wood. The tip of the their non-stridulating opponents, indicating that
rostrum is rubbed along the transversely ridged stridulation may be a startle mechanism employed
prosternal groove with an anterior-posterior move- by temporarily disadvantaged individuals to
ment; the return stroke (posterior-anterior) is silent. escape from encounters. Together with other signs,
Stridulation lasts for about 5 min, although the insect stridulations provide information on the identity
remains immobile when held for a longer time. In a and relative fitness of the opponent.
 Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)
A 31

Acoustical Communication in Heteroptera

(Hemiptera: Heteroptera), Figure 16 Phyllomorpha
laciniata (Hemiptera: Coreidae): (above) dorsal
view of pronotum with scraper (plectrum) at its
Acoustical Communication in Heteroptera
margin, (below) detail of spines of scraper (adapted
(Hemiptera: Heteroptera), Figure 15 Artabanus
from Moulet 1995 Faune de France 81).
lativentris (Hemiptera: Aradidae): (above) ventral
view of abdomen, with file (stridulitrum), (below)
hind leg with detail of scraper (plectrum) in the Tingidae
interior surface of the hind tibia (adapted from
Schuh and Slater 1995 True bugs of the world In the tingid Corythuca hewitti, vibrational sig-
(Hemiptera-Heteroptera): classification and natural naling during group movements may occur as
history. Cornell University Press, Ithaca, NY, 335 pp). groups of nymphs are attended by a female. It has
been reported that a disturbance of the leaf where
The acoustic repertoire of the ambush bug, C. hewitti aggregated caused feeding to stop and
Phymata crassipes, is quite large and may be displayed dispersal by the bugs, with occasional stopping of
by females, males or nymphs. Its vibrational songs the bugs to vibrate the abdomen in a vertical
may be emitted in response to, and alternating with, plane, a behavior followed by conspecifics.
calls from conspecifics, or even human speech or
whistle. Sound emission is related to disturbance,
interaction with other males and females, or court- Cydnidae
ship. Signals are produced by locomotory, stridula-
tory and/or vibratory mechanisms. Airborne signals In cydnids, the low species and sex specificity of
directly or indirectly stimulate vibrational receptors. pure stridulatory signals indicates that these
Bugs within a group respond to each other only via vibratory emissions may play a role in distur-
substrate, even in close proximity. bance (defensive) behavior, as in Tritomegas
bicolor. Stridulatory signals are also related to
aggregation or some other unspecific behavioral
Miridae context. Cydnid bugs engage in rival singing and
also distress (disturbance or alarm) signals, either
Although a stridulatory device has been described in as nymphs or adults (males and/or females).
several tribes and subfamilies, the functions of acous- Courtship, acceptance and rivalry songs
tical communication in Miridae are still unknown. show higher specificity and in most cases are
32
A Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)

of the emitted signals and the uniformity of

songsindicate that calling and courtship may be
mediated by signals of other modalities. The lack
of low frequency signals may be explained by the
direct contact of the bug with soil, which mechan-
ically prevents free vibration of the abdomen.

Pentatomidae

Pentatomid bugs engage in rival singing. For

example, Nezara viridula and Rhapigaster nebu-
losa may alternate rival songs until one or both
stop singing, and in P. lituratus, males perform
rival singing. Vibrational directionality has been
demonstrated in host or prey searching in the
predatory stink bug Podisus maculiventris.
The general pattern of singing during pre-
mating behavior is similar for all Pentatomoidea.
Calling starts with the emission of the female calling
song, which triggers males to respond with calling
Acoustical Communication in Heteroptera and courtship songs, activates them to walk on the
(Hemiptera: Heteroptera), Figure 17 Male Anisops plant, and enables directional movement toward
megalops (Hemiptera: Notonectidae): (above) the female. Alternation of male and female songs
foreleg with detail of scraper (plectrum) in the may result in more or less complex duets, as is the
interior surface of the fore-tibia, (below) lateral case in N. viridula. Nezara viridula vibrates its body
view of the head with file (stridulitrum) on the as part of intersex communications (courtship,
labium (adapted from Schuh and Slater 1995 directional cue for locating the mate, mate recogni-
True bugs of the world (Hemiptera-Heteroptera): tion), which implies that substrate-borne signals
classification and natural history. Cornell arehighly species-specific. The female song causes
University Press, Ithaca, NY, 335 pp). the male to walk, to respond with the calling and
courtship songs, and to approach the source of the
roduced by low frequency body vibration and/or
p song with characteristic search behavior. In con-
by stridulation. Tritomegas bicolor produces court- trast, females show no reaction to vibratory stimu-
ship, mating, and male rivalry calls by stridulation lation and no vibrational directionality.
and body vibration. In Sehirus luctuosus, the males Insect Acoustics
courtship call is produced by body vibration, Cicada Acoustics
giving a drumming song. Two types of species- Vibrational Communication
specific male courtship songs, produced by stridu-
latory and vibratory mechanisms, have been
described. The first type triggers female response,
References
a species-specific agreement song. The second type
stimulates pair formation.
okl A, Virant-Doberlet M (2003) Communication with
In the group-living species of genus Scapto- substrate-borne signals in small plant-dwelling insects.
coris, the absence of low frequency components Annu Rev Entomol 48:2950
 Acoustic Communication in Insects
A 33

okl A, Nardi C, Bento JMS, Hirose E, Panizzi AR (2006) predators of an unpleasant experience if predation is
Transmission of stridulatory signals of the burrower
attempted, but it is also possible that clicks function
bugs Scaptocoris castanea and Scaptocoris carvalhoi
(Heteroptera: Cydnidae) through the soil and soybean. as startle sounds, allowing escape. This latter expla-
Physiol Entomol 31:371381 nation seems unlikely, however, as caterpillars usu-
McGavin GC (1993) Bugs of the world. Blandford, London, ally move very slowly, so escape is not very likely.
UK, 192 pp
Miklas N, okl A, Renou M, Virant-Doberlet M (2003)
Acoustic Communication in Insects
Variability of vibratory signals and mate choice selectiv- Vibrational Communication
ity in the southern green stink bug. Behav Process
61:131142
Reyes-Lugo M, Daz-Bello Z, Abate T, Aviln A (2006) Stridu- Reference
latory sound emission of Panstrongylus rufotuberculatus
Champion, 1899 (Hemiptera: Reduviidae: Triatominae).
Braz J Biol 66(2A):443446 Brown SG, Beottner GH, Yack JE (2007) Clicking caterpillars:
Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera acoustic aposematism in Antheraea polyphemus and
Heteroptera): classification and natural history. Cornell other Bombycoidea. J Exp Biol 210:9931005
University Press, Ithaca, NY, 335 pp
Wheeler AG Jr (2001) Biology of the plant bugs. Cornell
University Press, Ithaca, NY, 507 pp Acoustic Communication in
Insects
Acoustic Aposematism (Clicking) allen sanborn
by Caterpillars Barry University, Miami Shores, FL, USA

Adult Lepidoptera are well known to perceive sound, Sound is used by a wide variety of insects for
such as the ultrasonic cries of insectivorous bats. diverse purposes. It is difficult to evolve an acous-
Some even produce sounds that are used for social tic communication system. There must be modifi-
communication. Less well known is the sound pro- cations to produce sound, transmit the sound in
duction and reception of larvae. Some caterpillars the environment and modify the sound to specific
employ vibrational signals with ants (e.g., Lycaenidae biological purposes, as well as the evolution of
and Riodinidae), communicate about space with structures that will receive and decipher the sig-
conspecifics (e.g., Gracillariidae), or detect insect nals. Arthropods are one of only two major groups
predators or parasitoids (e.g., Noctuoidea and of animals (along with the vertebrates) that have
Gracillariidae). However, clicking sounds are an evolved acoustic communication and insects are
audible sound produced by caterpillars of silk moth the primary group of arthropods to exhibit acous-
(Saturniidae) and hawk moth (Sphingidae). This tic behavior. At least ten orders of insects possess
noise has also been described as squeaking or species that produce acoustic signals.
crackling, and originates with the mandibles.
Defensive sounds are usually categorized as startle
or warning behaviors; startle sounds warn a poten- Sound
tial predator, causing momentary hesitation and
escape of the potential prey, whereas warning sounds Sound is generated by causing the repeated com-
alert a potential predator that it is inadvisable to pression and rarefaction of an elastic medium. The
attack. Associated with the clicking sound is regurgi- waves of compression produced will then travel
tation behavior, and both actions follow disturbance through the medium to the receptor or target. The
of the larva. Regurgitant usually is adverse to preda- medium can be air, water or a substrate so sound
tors, and is a widespread defensive behavior among also encompasses vibrations. As the sound energy
insects. Thus, clicking is thought to warn potential travels through the environment, it is modified
34
A Acoustic Communication in Insects

by various interactions with the components of to decrease the acoustic short circuiting of a small
that environment. In addition, sound waves are dipole sound source, mole crickets (Gryllotalpidae)
reflected as they move through any environment. dig burrows which act as loudspeakers that amplify
This bending of sound waves can initiate interac- and direct their calls skyward, and the hollow
tions among the waves. The signal begins to dete- abdomen of male cicadas (Cicadidae) acts as a res-
riorate as a result of these wave interactions and onating structure to amplify the acoustic signals
with the variations in the signal initiated due to produced by the tymbals.
temperature and humidity. Acoustic energy is also The sound producing systems of insects are
lost as it is absorbed by structures in the environ- generally vibrating structures. These structures
ment and as a result of spherical spreading from are necessary because muscles cannot contract
the sound source. The loss of signal integrity due rapidly enough to produce high frequency sounds.
to these environmental interactions is termed the The sound generating structures vibrate multiple
excess attenuation of the signal. The amount of times for each muscle contraction, so the sound
excess attenuation varies with the habitat and the producing systems act as frequency multipliers.
original signal properties. Once the vibrations are initiated, the sound can
To complicate matters, the small size of insects be modified by attached resonant structures.
requires that they use high frequencies (Fig. 18) to There are many different schemes that can be
transfer energy efficiently to the signal. This will employed to describe insect calls. The variety of
limit the range of a given signal because higher fre- sound production mechanisms has led to a variety
quencies attenuate more rapidly in the environment. of terminologies. No one terminology has been suc-
To use lower frequencies, insects must modify their cessful in describing the different sound production
bodies or behaviors to increase the efficiency of mechanisms or phylogenetic relationships of insects.
sound production. For example, tree crickets (Gryl- When sounds are recorded and analyzed in any
lidae) create a baffle by inserting their body in a leaf acoustic work, each analysis of acoustic signals in

20
19
kHz

18
17
16

A
0.5 sec

B 50 msec

Acoustic Communication in Insects, Figure 18 Acoustic signal produced by the cicada Beameria venosa
(Uhler). (a) Sonogram of calling song illustrating energy distribution of the call. Middle trace is an
oscillogram illustrating the temporal pattern of the call. (b) Expanded oscillogram to show individual
sound pulses within the call.
 Acoustic Communication in Insects
A 35

insects should provide a detailed description of

the terminology used to describe the signals,
and illustration of the terminology on any oscillo-
gram or sonogram in the work.

Sound Production

There are several different types of sound produc-

tion mechanisms that have evolved in insects. The
relatively low muscle contraction frequency means
that additional structures had to evolve in order to Acoustic Communication in Insects,
produce the high frequency sounds that small Figure19Stridulatory apparatus of the cicada
body size will require to generate acoustic signals Tettigades undata Torres. The file (illustrated) is
efficiently. located on the mesothorax in this group of cicadas.
The primary mechanism used by insects to The plectrum is located on the tegmina. Sound
produce sound is a stridulatory apparatus. The chi- pulses are p
roduced as the tegmina is rubbed over
tinous exoskeleton and jointed appendages of the series of m
esothoracic ridges.
insects are preadapted for modification into stridu-
latory apparati. Each stridulatory apparatus is com-
posed of a file and plectrum or scraper. The file is muscle (Fig. 20). The tymbal buckles as the tymbal
generally a row of small cuticular teeth that is muscle contracts. Sound pulses are produced when
rubbed against a ridge or blade (the plectrum) on the tymbal buckles, when individual ribs buckle
some other body part (Fig. 19). The teeth are bent and potentially when the tymbal returns to its
as they catch on the plectrum and pop forward as relaxed position. The unbuckling of the tymbal is
they release from the plectrum. The release causes assisted by the resilin within the tymbal. The reso-
the teeth to vibrate alternately compressing and nant frequency of the tymbal determines the fre-
expanding air molecules producing sound. In quency of the sound pulses produced. Additional
general, these vibrations will occur in a single structures such as the opercula, tymbal covers, var-
plane, resulting in a dipole being formed that pro- ious muscles and the abdominal air sacs can mod-
duces an asymmetrical sound field at close range. ify the sound produced. The abdominal air sacs can
The joints and exoskeleton of insects have permit- become rather large as in the bladder cicada Cysto-
ted stridulatory apparati to evolve in many loca- soma saundersii Westwood whose abdomen is so
tions on the body. There are file and scrapers found large, to resonate at a low frequency, that the male
between antennal segments (Phasmatodea), sepa- has difficulty flying. The tymbal is a common organ
rate mouthparts (Orthoptera), head and thorax in the Hemiptera and acts as the ultrasonic pulse
(Coleoptera), abdominal segments (Hymenoptera), generator in the Lepidoptera.
wings and thorax (Lepidoptera, Hemiptera), body Percussion is another mechanism of sound pro-
parts and legs (Hemiptera, Orthoptera), legs and duction used by insects. Crepitation, a clicking sound
wings (Orthoptera, Lepidoptera, Coleoptera), legs produced by the wings, is another percussion mecha-
and legs (Thysanoptera, Hemiptera), between nism in insects. The wings are clapped together or
wings (Orthoptera), and between segments on the banged on the substrate to produce a sound pulse in
genitalia (Lepidoptera, Hemiptera). A tymbal organ some Hemiptera. It is relatively rare for airborne sig-
is a specialized sound production organ. It is a nals which are generally produced as a by-product of
ribbed, chitinous membrane attached to a tymbal flight. The wings may strike each other or the legs
36
A Acoustic Communication in Insects

production in insects. This method of sound pro-

duction has been described in a number ofinsects,
most notably the Madagascan hissing cockroach
(Gromphadorhina portentosa [Schaum]), the
Deaths Head hawk moth (Acherontia atropos [L.])
and some African Sphingids (Lepidoptera).
In addition to the airborne signals produced by
acoustic insects, it has now been shown that vibra-
tional signals are also produced by sending infor-
mation through the substrate. These vibrational
signals are primarily produced by tremulation but
also can be important in deciphering anairborne
signal, particularly at close range to the sound
source. Vibrational signals have been identified in
members of the Neuroptera, Diptera, Hemiptera,
Plecoptera, Coleoptera, Orthoptera, Mecoptera,
Raphidioptera, Lepidoptera and Hymenoptera.

Acoustic Communication in Insects, Figure 20 Sound Reception

Tymbal organ of the cicada Beameria venosa
(Uhler). The internally attached tymbal muscle A receptor for acoustic signals is necessary for a
buckles the tymbal to produce a sound pulse. communication channel to exist. Because sound is
produced by changing air pressure, a modified
during flight-producing sound pulses as in the mechanoreceptor is needed to sense the acoustic
acridid grasshoppers (Orthoptera). However, spe- information. The receptors can be classified as
cialized percussive sound production systems have either a pressure detector or a particle detector.
evolved. A castanet is found on the costal margin of Pressure detectors are membranes that bend when
the tegmina in some moths (Lepidoptera) which pressure is unequal on the two sides of the detec-
produces a pure tone when struck. The acridid grass- tor. Particle detectors are long structures that move
hopper Paratylotropidia brunneri Scudder can snap when impacted by many particles moving in the
their mandibles together to generate sound. Percus- same direction. The movement of the particle
sion has been observed in Hemiptera, Isoptera, Ple- detector alternately stretches and compresses sen-
coptera, Lepidoptera, and Orthoptera. sory cells at the base of the organ.
Tremulation is the vibration of unspecialized The primary type of pressure receptor organ is
body parts to generate sound. The abdomen is a tympanum, which has evolved independently in at
often moved dorso-ventrally or laterally to send least eight orders of insects. Tympana are generally a
vibrations through the legs to the substrate. This thin membrane system stretched over a closed cav-
mechanism has been well studied in the lacewings ity. The tympanum bends away from the side of
(Neuroptera). Wing vibrations can also be used to higher pressure setting up oscillations as the sound
send information over short distances. This type waves strike the membrane. Each tympanum has a
of signal is produced by members of the Diptera resonant frequency based on its thickness, size and
(flies and mosquitoes) and Hymenoptera. shape. The resonant frequency is generally tuned to
The expulsion of tracheal air is the final the carrier frequencies of the communication chan-
and relatively rare mechanism of insect sound nel to increase the efficiency of information transfer.
 Acoustic Communication in Insects
A 37

The tympana are associated with other mechanore- conditions are not optimal for other signal pathways.
ceptor organs to transduce the signal for the nervous However, sound is energetically costly to produce
system. As the tympana oscillate, vibrations are sent and advertises your position to potential predators
to various types of receptors, generally a specialized as well as potential mates. Even with these potential
chordotonal organ called a scolopidial organ, which problems, insects have evolved diverse functions for
act as the input site to the central nervous system. acoustic signals. Acoustic signals are used for a vari-
There can be elaborate structures associated with the ety of purposes in insects including sexual signaling,
tympana to transduce energy into the central ner- courtship signals, aggression, social recruitment and
vous systems such as the crista acoustica of the crick- defense.
ets and katydids (Orthoptera) and Mllers organ of A primary function of acoustic signals is as an
locusts (Orthoptera), which provides frequency dis- intraspecific communication channel. Sounds are
criminating abilities. These pressure receptors are used to attract mates and to isolate species repro-
generally found in pairs, one on each side of the body. ductively. Each species has a characteristic call that
This provides an animal with a means to determine can prevent related species from cross mating. The
the direction from which the sound originated. calls produced by individual signalers can be com-
The sensory structures for vibrational signals pared by receivers providing the opportunity to
are trichoid sensilla generally found on the feet or select a mate who is producing a call that exhibits
cerci or through specialized subgenual and metatar- specific characteristics. This is particularly true
sal organs located in the legs. The subgenual organs when callers have congregated into localized areas,
are located just distal to the femoral-tibial joint in all which is another function of acoustic signaling.
six legs to promote detection and directional hear- Mates may be selected based on the number of
ing. They are similar to tympana in that they are calls, the temporal patterns, loudness, etc. The spe-
chordotonal organs but lack the tympanal mem- cific characteristics used by a given species are
branes and tracheal air sacs of the tympanal system. usually chosen based on their ability to demon-
Particle receptors are generally specialized strate the viability of the caller. Duets between
structures found in specific groups of insects. For individuals (either intrasexual or intersexual) can
example, female fruit flies (Diptera) sense the also act as mechanisms to determine mate choice.
courtship signals produced by the male with a spe- The signals often change as potential mates
cial antennal segment called an arista. Male mos- approach. These courtship sounds are modified
quitoes and midges (Diptera) have plumose advertisement calls which provide further oppor-
antennae which detect the species-specific wing tunities for mate assessment. Acoustic signals can
beat frequencies produced by females. Johnstons also be used intraspecifically to space individuals
organ is a more complex chordotonal organ found in the environment, as aggression signals, or as
in the antennal pedicel of some Diptera and competitive signals to jam the signal of a neighbor.
Hymenoptera which is stimulated by the vibration Eusocial insects use acoustic signals as warnings,
of the antennal flagella. The long bristles and anten- to recruit a defensive response within the colony,
nae provide a mechanical advantage to the sensory and to recruit foragers to specific food sources.
cells increasing the sensitivity of the receptor. Predator deterrence is another significant
function of acoustic signals. The loud sounds pro-
duced by many insects (e.g., cicadas [Hemiptera]),
Functions of Acoustic Signals can startle a potential predator giving the insect a
chance to escape. The percussion sounds pro-
Sound has many potential benefits in that the sig- duced by acridid grasshoppers (Orthoptera) are
nals can be used day or night, can be modified thought to be defensive displays. Sound produc-
quickly, and can travel a significant distance even if tion has evolved specifically for this anti-predator
38
A Acrididae

function in click beetles (Coleoptera). The Greenfield MD (2002) Signalers and receivers: mechanisms
and evolution of arthropod communication. Oxford
acoustic systems that use air movement in the
University Press, New York, NY, 414 pp
Deaths Head moth (Lepidoptera), cockroaches
(Blattodea) and grasshoppers (Orthoptera) also
have anti-predator functions. Moths (Lepi- Acrididae
doptera) have evolved a sound production system
that is used to jam the ultrasonic signals of the A family of grasshoppers (order Orthoptera). They
bats that prey upon them. The arctiid moths emit commonly are known as shorthorned grasshoppers.
ultrasonic pulses as bats approach which act to Grasshoppers, Katydids and Crickets
confuse the bat as to the exact location of its tar-
get. This gives the moth a chance to escape while
the bat circles around for another attempt at Acriology
capturing the insect. These pulses may also have
an aposomatic function warning bats of a poten- The study of grasshoppers, katydids, crickets and
tially distasteful meal. their relatives (Orthoptera). This is sometimes
Insects have also evolved specialized acous- expanded to include the orders of insects related
tic receptors as a means of avoiding predation. to Orthoptera (the Orthopteroids) such as cock-
Bat-detectors have evolved independently in roaches (Blattodea), mantids (Mantodea), stick
geometrid, noctuid and hawk moths (Lepi- insects (Phasmatodea), earwigs (Dermaptera), and
doptera), lacewings, (Neuroptera), praying man- gladiators (Mantophasmatodea).
tises (Mantodea), beetles (Coleoptera), crickets, Classification
locusts and katydids (Orthoptera). These bat- Grasshoppers, Katydids and Crickets
detectors provide an early warning system for the
insects that a bat is nearby giving the insect a
chance to escape before the bat can sense an Acrobat Ants (Hymenoptera:
insect in the vicinity. Formicidae)
Sound Production in the Cicadoidea
Acoustic Aposematism A term applied to ants of the genus Crematogaster.
Drumming Communication and Intersexual Typically they are small, shiny brown or black, and
Searching Behavior of Stoneflies (Plecoptera) possess a pedicel with two nodes. They elevate the
gaster (tip of the abdomen) over the thorax or
head when alarmed. Acrobat ants usually are
References
found in association with wood or trees, including
the tunnels of termites and wood boring beetles.
Bailey WJ (1991) Acoustic behavior of insects, an evolution-
ary perspective. Chapman and Hall, London, UK, 225pp They are omnivorous and tend aphids. Their bite
Drosopoulos S, Claridge MF (eds) (2006) Insect sounds and can be painful.
communication: physiology, behavior, ecology and evo- Ants (Hymenoptera: Formicidae)
lution. CRC Press, Boca Raton, FL, 532 pp
Elliot L, Hersberger W (2007) The songs of insects. Hough-
Ant-Plant Interactions
ton-Mifflin Company, Boston, MA, 228 pp
Ewing AW (1989) Arthropod bioacoustics: neurobiology and
behavior. Comstock Publishing Associates, Ithaca, NY, Acroceridae
260 pp
Gerhardt HC, Huber F (2002) Acoustic communication
A family of flies (order Diptera). They commonly
in insects and anurans: common problems and
diverse solutions. University of Chicago Press, Chicago, are known as small-headed flies.
IL,531 pp Flies
 Aculeus
A 39

Acrolepiidae Active Ingredient (A.I.)

A family of moths (order Lepidoptera). They com- The toxic component of an formulated pesticide. It
monly are known as false diamondback moths. also is known as the toxicant.
False Diamondback Moths
Butterflies and Moths
Active Space
Acrolophidae The area or space in which the concentration of
pheromone (or other behavioral chemical) is at or
A family of moths (order Lepidoptera). They com-
above threshold concentration necessary to elicit a
monly are known as tube moths.
response from the receiver.
Tube Moths
Butterflies and Moths

Active Ventilation
Acron
Although most gas exchange in insects occurs
A preoral, unsegmented portion of the body, ante- through diffusion (passive ventilation), in some
rior to the first true body segment. This is also cases it is inadequate to meet the oxygen needs
known as the prostomium. of insects, particularly large or flying insects.
Thus, muscular contractions acting via hydro-
static pressure (pressure on the hemolymph)
Acrosternite compress the trachea and air sacs to force carbon
dioxide out and allow more rapid intake of air.
The narrow marginal region at the anterior edge The exact mechanism varies among taxa, but
of a sternite. It appears to be the posterior edge of usually involves contraction of the abdomen, and
the preceding sternite, and includes the interseg- synchronization of opening and closing of the
mental fold. It is found on the abdominal sterna, spiracles.
but absent from the thoracic sterna. Abdominal Pumping

Action Threshold
Aculae
A level of pest abundance that stimulates action to
protect plants from serious damage. Small spines on the wing membrane of Lepidoptera.
Economic Injury Level (EIL) and Economic
Threshold (ET) Concepts in Pest Management
Aculeus
Active Dispersal
This term has several meanings depending on
the taxon of insects under consideration. In
The redistribution of animals caused by their own Hymenoptera, it is synonymous with the sting,
actions such as flying or walking. The wings of an eversible hollow cylindrical structure at the
insects allow active dispersal frequently (contrast tip of the abdomen used to deliver venom.
with passive dispersal). Though derived from the ovipositor, it is not used
40
A Acute

to deliver eggs. Among Diptera, this term is Adaptation of Indigenous Insects

sometimes used to refer to a pointed, sclerotized to Introduced Crops
structure associated with the reproductive sys-
tem in males. Among Lepidoptera, this term wendell. l. morrill
refers to hair-like structures on the body and Montana State University, Bozeman, MT, USA
wings of primitive moths; these also are known
as microtrichia. Host range expansion, or adaptation of insects to
new crops, is a world-wide phenomenon that has
been observed repeatedly and extensively. It is
Acute particularly well documented in North America,
where forests and prairies consisting of indige-
Of short duration, characterized by sharpness or nous plants were planted extensively to intro-
severity. duced cultivated crops only after European
emigrants arrived in the eighteenth century.
Although many new insect pests were also acci-
Acute Bee Paralysis dentally introduced from Europe into Canada
and the United States, many species of native
A disease of honey bees caused by a picornavirus. insects adapted to the new crops and became eco-
Symptoms include trembling, sprawled append- nomically important pests (Table 2).
ages, and sometimes hairlessness (contrast with Prior to widespread introduction of cultivated
chronic bee paralysis). crops, some species of native insects fed on a wide
range of plants and therefore might be expected to
accept the new crops readily. Although polypha-
Aculeate gous insects such as grasshoppers (Orthoptera:
Acrididae), wireworms (Coleoptera: Elateridae),
Pertaining to the stinging Hymenoptera (suborder
and cutworms (Lepidoptera: Noctuidae) readily
Aculeata), a group including the bees, ants, and
accepted corn, wheat and other crops, not all of
many wasps.
the species within these groups became agricul-
Wasps, Ants, Bees and Sawflies (Hymenoptera)
tural pests. For example, several hundred species
of cutworms and grasshoppers are present, but
Acute Toxicity only about a dozen species in each group have
achieved regular pest status.
The toxicity of a pesticide determined after 24 h. The Other native insect species had a narrower
toxicity resulting from a single dose or exposure. host range, and therefore adapted to a more nar-
Insecticide Toxicity row range of crops, or perhaps only a single crop.
Insecticides In the south the boll weevil, Anthonomus grandis
grandis Boheman (Coleoptera: Curcullionidae),
originally fed on native plants in Mexico related to
Adaptation cultivated cotton, and dispersed northward into
the new cotton belt of the southeastern United
This term has at least two meanings: changes in States as cotton was planted extensively. In the
the form or behavior of an organism during its life, north, the wheat stem sawfly, Cephus cinctus Nor-
and natural selection of organisms in evolutionary ton (Hymenoptera: Cephidae), fed on hollow-
time. In entomology, usually the latter definition is stemmed wild grasses, and within 10 years after
intended. tillage began in Alberta, wheat was damaged from
 Adaptation of Indigenous Insects to Introduced Crops
A 41

Adaptation of Indegenous Insects to introduced Crops, Table 2 Examples of American insect pests that
have adapted to introduced crops
Insects with wide host ranges Old host plant New host plant
Apple maggot, Rhagoletis pomo- Hawthorne Apple
nella (Walsh) Diptera: Tephritidae
Chinch bug, Blissus leucopterus Grasses Corn
leucopterus Heteroptera:
Lygaeidae
Western corn rootworm, Diabrot- Grasses Corn
ica virgifera virgifera LeConte
Coleoptera: Chrysomelidae
Western bean cutworm, Loxagro- Solanaceous weeds Corn, beans
tis albicosta (Smith) Coleoptera:
Chrysomelidae
Colorado potato beetle, Leptino- Buffalo burr Potato
tarsa decemlineata (Say)
Coleoptera: Chrysomeliodae
Carrot weevil, Listronotus oregon- Umbelliferous weeds Carrots, etc.
ensis (LeConte) Coleoptera:
Curculionidae
California red scale, Aonidiella Shrubs and trees Citrus
aurantii (Maskell) Hemiptera:
Diaspididae
Boll weevil, Anthonomus grandis Malvaceous weeds Cotton
Boheman Coleoptera:
Curculionidae
Insects with wide host ranges Old host plant New host plant
Sugar beet wireworm, Limonius Weeds, grasses Field and vegetable crops
californicus Coleoptera:
Elateridae
White grubs, Phyllophaga spp. Weeds, grasses Field and vegetable crops
Coleoptera: Scarabidae
False chinch bug, Nysius raphanus Weeds, grasses Field and vegetable crops
Howard Hemiptera: Lygaeidae
Tarnished plant bug, Lygus line- Weeds, grasses Field and vegetable crops
olaris (Palisot de Beauvois)
Hemiptera: Miridae
Army cutworm, Euxoa auxiliaris Weeds, grasses Field and vegetable crops
(Grote) Lepidoptera: Noctuidae
Yellow striped armyworm, Weeds, grasses Field and vegetable crops
Spodoptera ornithogalli (Guene)
Lepidoptera: Noctuidae
Redlegged grasshopper, Melano- Weeds, grasses Field and vegetable crops
plus femurrubrum (de Geer)
Orthoptera: Acrididae
42
A Adaptation of Indigenous Insects to Introduced Crops

Adaptation of Indegenous Insects to introduced Crops, Table 2 (Continued)

Insects with wide host ranges Old host plant New host plant
Migratory grasshopper, Melano- Weeds, grasses Field and vegetable crops
plus sanguinipes (Fabricius)
Orthoptera: Acrididae

the Canadian prairie provinces south into Mon- feeding on a plant (species richness) does not
tana and North Dakota. In the eastern United increase indefinitely, leveling off after less than 300
States the apple maggot, Rhagoletis pomonella years if there is not an increase in crop acreage.
(Walsh) (Diptera: Tep hritidae), expanded its host We can observe insects with both broad and
range to included newly introduced cultivated narrow host selection behavior expanding their
fruits, especially apples. The Colorado potato bee- host range to include introduced crop plants. This is
tle, Leptinotarsa decemlineata Say (Coleoptera: not surprising for generalist species, which feed
Chrysomelidae) originally fed on solanaceous broadly on many plants, but it is quite interesting
weeds in Mexico or the southwestern United when insects with a narrow host range adopt new
States, and quickly spread across the United States hosts. In such cases the species with a narrow host
on potatoes once it gained access to potato acre- range usually are pre-adapted to accept the foreign
age. These are just a few examples of insects accept- crops because they feed on plants in the same fam-
ing new hosts, and the same phenomenon is well ily as the introduced crop. North America possesses
documented for important tropical crops such as close relatives to nearly all the introduced crops
sugarcane and cacao, and other crops, as they were among its indigenous flora, so it is not surprising
introduced and cultivated in various locations that insects associated with the native plants would
around the world. adapt to the introduced crops. The presence of sec-
Some of the native insect populations origi- ondary plant metabolites (allelochemicals) such as
nally occurred at low levels because their host plants alkaloids, terpenoids, and cyanogenic glycosides
were relatively sparse. Large acreage of newmono- often serves to keep non-adapted insects from feed-
crop habitats therefore resulted in an abundant food ing extensively on plants, but may serve as chemical
supply, excellent survival, and eventually in pest cues or stimulants for insects that are adapted. Thus,
population outbreaks. Also, the native environ- insects that specialize on cruciferous weeds and
ments were relatively stable, and supported a wide crops are attracted to allylisothiocyanate, and
range of beneficial insects suppressed herbivorous insects that feed on cucurbitaceous weeds and crops
insects. However, soil tillage within the agricultural are attracted to cucurbitacin.
environments produced highly disturbed systems, Host selection behavior by insects is not a
and pests with high fecundity were not effectively static situation, nor is it as simple as the single-
suppressed by predators and parasitoids. chemical scenario presented above. It is constantly
Americas native insects displayed consider- evolving in response to various biotic characteris-
able plasticity in acquiring new hosts. This trend tics such as herbivory, and even to crop cultural
has been noted everywhere agriculture is practiced, practices. Some natural selection of insect strains
and we can expect the number of pests to increase may have occurred during the adaptation from
with time, and especially with the area planted to native to introduced plants. In the northern Great
each particular crop, as indigenous species adapt to Plains, wheat matures earlier in the season than
imported host plants or crops are exposed to addi- wild grasses. Therefore, after a century, adult wheat
tional potential pests in new geographic areas. stem sawflies are now active nearly a month earlier
However, species accrual occurs most rapidly soon than previously, and now are more effective in
after plant introduction, and the number of species utilizing wheat.
 Adelidae
A 43

Changes in farming practices that have also in a continuing stream of new pest problems for
impacted populations of native insect pests in crop plants.
croplands. Originally, horses were used for farm- Host Plant Selection by Insects
ing, and oats were needed for their feed. Later, the Allelochemicals
horses were replaced by tractors, and the need for Plant Resistance to Insects
oats was reduced. Oats are resistant to wheat stem
sawflies, and when oats was eliminated from the
cropping system, the vast acreages of wheat resulted References
in a population explosion of the sawflies. More
recently, canola has been included in the Canadian Bernays EA, Chapman RF (1994) Host-plant selection by phy-
tophagous insects. Chapman and Hall, New York, NY
Prairie Provinces, and populations of grass-feeding Connor EF, McCoy ED (1979) The statistics and biology of
insects are somewhat disrupted by the presence of the species-area relationship. Am Nat 113:791833
a non-host, cruciferous crop. Other water and Kim KC (1993) Insect pests and evolution. In: Kim KC,
McPheron BA (eds) Evolution of insect pests; patterns
soil conservation practices such as alternate-year
of variation. Wiley, New York, NY, pp 325
summer fallow, strip cropping, and chemical fallow Morrill WL, Kushnak GD (1996) Wheat stem sawfly
have affected the prevalence of both pest and (Hymenoptera: Cephidae) adaptation to winter wheat.
beneficial insects. Environ Entomol 25:11281132
Strong DR (1979) Biogeographic dynamics of insect-host
Beneficial insect populations were also plant communities. Annu Rev Entomol 24:89119
impacted by tillage and cultural practices, and
changes in the chemical constituency of crop
plants. Parasitoids have complex host searching
Adaxial Surface
behavior that begins with finding plant envi-
ronments in which their hosts could occur.
The upper surface of a leaf (contrast with abaxial
Therefore, it was necessary for the parasitoids
surface).
to learn that the new crops could be sources of
hosts. In the case of the wheat stem sawfly, only
two of the known parasitoid species have cur-
rently adapted from wild grasses to wheat. Par-
Adeheterothripidae
asitoids may be more favored by one plant
A family of thrips (order Thysanoptera).
cultivar than another, or less favored by a crop
Thrips
than a similar weed. The availability of food for
the adult parasitoid or predator, either nectar
from blossoms or extra floral nectaries or pol-
Adelgidae
len from blossoms, is often implicated in dif-
ferential survival of beneficial insects among
A family of insects in the order Hemiptera. They
different plants.
sometimes are called pine and spruce aphids.
Overall, adaption by herbivorous insects to
Aphids
new host plants is a dynamic and widespread phe-
Bugs
nomenon. Though sometimes it is difficult to
determine whether it is the change in the constitu-
ency of the host plant that accounts for insect
acceptance, or it is some other factor such as wide- Adelidae
spread host plant availability that accounts for
insect abundance, it is clear that the relationship A family of moths (order Lepidoptera). They
between insects and plants is not static, resulting commonly are known as long horned fairy moths.
44
A Adephaga

Long horned Fairy Moths Adipohemocyte

Butterflies and Moths
A type of hemocyte, ovoid in shape and likely
secretory in function.
Adephaga Hemocytes of Insects: Their Morphology and
Function
One of four suborders of beetles (Coleoptera), and
one of two suborders that contain numerous and
important beetles (the other is suborder Polyphaga). Adipokinetic Hormone (AKH)
It is comprised of about nine families, the principal
ones being Carabidae, Gyrinidae, and Dytiscidae. A decapeptide hormone synthesized in neurose-
Nearly all groups are predatory, and many are cretory cells of the corpora cardiaca and impor-
aquatic. tant in the regulation of lipid metabolism, and
Beetles (Coleoptera) sometimes carbohydrate or proline metabolism
and other physiological functions.
Adipokinetic and Hypertrehalosemic
Aderidae Neurohormones

A family of beetles (order Coleoptera). They com-

monly are known as antlike leaf beetles. Adipokinetic and
Beetles Hypertrehalosemic
Neurohormones

gerd gde, heather g. marco

Adfrontal Areas University of Cape Town, Rondebosch, Republic
of South Africa
A pair of narrow oblique sclerites on the head of a
caterpillar. The adfrontal areas border the front,
The adipokinetic hormones and hypertrehalosemic
which normally is triangular, so the adfrontal areas
hormones of insects comprise a family of peptide
take on the shape of an inverted V.
hormones that primarily regulate the levels of
Head of Hexapods
energy metabolites, such as trehalose, diacylglycerol
and proline that circulate in the hemolymph. These
peptide hormones are products of neurosecretory
Adelphoparasitism neurons located in the corpora cardiaca, neuroen-
docrine glands attached to the brain. The structural
A type of hyperparasitism occurring in organization of the insect corpora cardiaca is simi-
Hymenoptera: Aphelinidae in which the males are lar to the hypothalamus-neurohypophysis of the
parasitoids of females of their own species (the vertebrate endocrine system.
females parasitize Hemiptera).

Historical Perspective
Adherence
The existence of hypertrehalosemic hormones
The ability of a material such as a pesticide to stick was discovered with the observation that injec-
to a surface. tions of extracts of corpora cardiaca elevated the
 Adipokinetic and Hypertrehalosemic Neurohormones
A 45

concentration of trehalose in the hemolymph of missing in S. gregaria. Subsequently, three research

cockroaches (hypertrehalosemia). Unlike verte- groups ultimately reported, in the same year, the
brates that use glucose as the major blood carbo- presence of two octapeptides from the corpora
hydrate, the hemolymph of insects generally cardiaca of the American cockroach, Periplaneta
contains the disaccharide trehalose, an -1-1- americana, that were structurally related to the
gluco-glucoside, as its major circulating carbohy- locust AKHs and the crustacean RPCH. These two
drate. In addition, the enzyme glycogen peptides were isolated on the basis of myotropic
phosphorylase in the fat body of cockroaches was or heartbeat acceleration bioassays and are referred
demonstrated to be activated when these insects to as cardio acceleratory hormones (Peram-CAH-I
were injected with an extract from the corpora and Peram-CAH-II), but they also produced
cardiaca. Subsequently, studies in locusts showed hypertrehalosemia in the cockroach and represent
that injections of corpora cardiaca extracts ele- the hypertrehalosemic hormones. These pioneer-
vated hemolymph diacylglycerols, instead of tre- ing studies, along with numerous subsequent stud-
halose, and this action was referred to as an ies, demonstrated that there are, so far, about forty
adipokinetic or hyperlipemic effect. Injections of structurally related, but distinct, peptides with
locust corpora cardiaca extracts into cockroaches adipokinetic and hypertrehalosemic effects in the
produced the hypertrehalosemic response, and insects and one in crustacean (Table 3). The name
vice versa. Hence, it was likely that the adipoki- adipokinetic hormone/red pigment-concentrating
netic hormone (AKH) of locusts and the hyper- hormone (AKH/RPCH) family was coined for this
trehalosemic hormone (HrTH) of cockroaches general family of peptides, which likely encom-
were related, or identical, peptides. passes the arthropods.
The locust adipokinetic hormone was isolated
and characterized first. It was obtained from the
migratory locust, Locusta migratoria, and its pri- Chemistry of the AKH/RPCH Family
mary structure consisted of ten amino acids. It was
designated Locmi-AKH-I according to the newest The members of the adipokinetic hormone/red
nomenclature for naming insect neurohormones. pigment-concentrating hormone family share
The amino acid composition and sequence of Loc- numerous structural features. They consist either
mi-AKH-I had a remarkable similarity to a previ- of eight, nine or ten amino acids, depending on the
ously reported red pigment-concentrating hormone insect species from which they are isolated. They
(Panbo-RPCH) obtained from the shrimp Pandalus are blocked by pyro-glutamate at the N-terminus
borealis and later found in various crustaceans. It and by an amide moiety at the C-terminus. Pre-
was shown that Locmi-AKH-I was also present in sumably, blocked termini prevent degradation of
the desert locust, Schistocerca gregaria. the neuropeptides by amino- and carboxypepti-
Subsequently, both L. migratoria and S. gregaria dase enzymes while circulating in the hemolymph.
were shown to contain a second adipokinetic hor- Aromatic amino acids, usually phenylalanine and
mone (Locmi-AKH-II and Schgr-AKH-II, respec- tryptophan, always occupy positions 4 and 8,
tively) that differed from each other by the amino respectively, but aromatic amino acids can also
acids in position 6. The two locust AKH-IIs were occupy other positions. The peptides are usually
octapeptides with sequences similar to those of neutral under physiological conditions, but a few
Locmi-AKH-I and Panbo-RPCH. A third octa- have a negatively charged aspartate at position 7.
peptide AKH (Locmi-AKH-III) was also found in Glycine is always present at position 9 as deduced
L. migratoria and a similar octapeptide (desig- from cDNA analysis of the precursor. The terminal
nated Phymo-AKH-III) occurs in pyrgomorphid glycine is converted to the amide moiety on the
and pamphagid grasshoppers, but an AKH-III is tryptophan in the octapeptides.
 46
Adipokinetic and Hypertrehalosemic Neurohormones, Table 3 Representative sequences of adipokinetic/hypertrehalosemic peptides from vari-
A
ous insect orders
Order Peptide name Genus Structure
1 2 3 4 5 6 7 8 9 10
Odonata Libau-AKH Libellula, Pantala, pGlu Val Asn Phe Thr Pro Ser Trp NH2
Orthetrum
Anaim-AKH Anax, Aeshna pGlu Val Asn Phe Ser Pro Ser Trp NH2
Psein-AKH Pseudagrion, pGlu Val Asn Phe Thr Pro Gly Trp NH2
Ischnura
Blattodea Peram-CAH-Ia Periplaneta, Blatta pGlu Val Asn Phe Ser Pro Asn Trp NH2
Blattidae a
Peram-CAH-II Periplaneta, Blatta pGlu Leu Thr Phe Thr Pro Asn Trp NH2
Blaberidae
Bladi-HrTH Blaberus, pGlu Val Asn Phe Ser Pro Gly Trp Gly Thr NH2
Blattellidae
Nauphoeta
Leucophaea,
Adipokinetic and Hypertrehalosemic Neurohormones

Blattella
Gromphadorhina
Mantodea Emppe-AKH Empusa, pGlu Val Asn Phe Thr Pro Asn Trp NH2
Sphodromantis
Phasmatodea Carmo-HrTH Carausius, Sipy- pGlu Leu Thr Phe Thr Pro Asn Trp Gly Thr NH2
loidea, Extatosoma
Mantophasmatodea Manto-AKH Not known pGlu Val Asn Phe Ser Pro Gly Trp NH2
Orthoptera, Caelifera Locmi-AKH-I Locusta, pGlu Leu Asn Phe Thr Pro Asn Trp Gly Thr NH2
Schistocerca
Locmi-AKH-II Locusta pGlu Leu Asn Phe Ser Ala Gly Trp NH2
a
Schgr-AKH-II Schistocerca, pGlu Leu Asn Phe Ser Thr Gly Trp NH2
Phymateus
Locmi-AKH-III Locusta pGlu Leu Asn Phe Thr Pro Trp Trp NH2
Phymo-AKH-III Phymateus pGlu Ile Asn Phe Thr Pro Trp Trp NH2
a
Orthoptera, Ensifera Grybi-AKH Gryllus, Acheta, pGlu Val Asn Phe Ser Thr Gly Trp NH2
Gryllodes
=Schgr-AKH-II Tettigonia, Decticus pGlu Leu Asn Phe Ser Thr Gly Trp NH2
Order Peptide name Genus Structure
1 2 3 4 5 6 7 8 9 10
Isoptera Micvi-CC Microhodotermes pGlu Ile Asn Phe Thr Pro Asn Trp NH2
Dermaptera =Grybi-AKH Labidura, Forficula pGlu Val Asn Phe Ser Thr Gly Trp NH2
Hemiptera/Homoptera Placa-HrTH Platypleura, Munza, pGlu Val Asn Phe Ser Pro Ser Trp Gly Asn NH2
Cacama, Magici-
cada, Diceroprocta
Hemiptera, Pyrap-AKH Pyrrhocoris, pGlu Leu Asn Phe Thr Pro Asn Trp NH2
Heteroptera Disdercus
=Peram-CAH-II Pyrrhocoris, pGlu Leu Thr Phe Thr Pro Asn Trp NH2
Disdercus
Corpu-AKH Corixa pGlu Leu Asn Phe Ser Pro Ser Trp NH2
Letin-AKH Lethocerus pGlu Val Asn Phe Ser Pro Tyr Trp NH2
Nepci-AKH Nepa pGlu Leu Asn Phe Ser Ser Gly Trp NH2
Neuroptera =Grybi-AKH Palpares pGlu Val Asn Phe Ser Thr Gly Trp NH2
Coleoptera Scade-CC-I Scarabaeus, Gareta, pGlu Phe Asn Tyr Ser Pro Asp Trp NH2
Onitis
Scade-CC-II Scarabaeus, Gareta pGlu Phe Asn Tyr Ser Pro Val Trp NH2
Oniay-CC Onitis pGlu Tyr Asn Phe Ser Thr Gly Trp NH2
=Peram-CAH-I Leptinotarsa pGlu Val Asn Phe Ser Pro Asn Trp NH2
=Peram-CAH-II Leptinotarsa pGlu Leu Thr Phe Thr Pro Asn Trp NH2
a
Lepidoptera Manse-AKH Manduca, Vanessa, pGlu Leu Thr Phe Thr Ser Ser Trp Gly NH2
Bombyx, Heliothisb
Helze-HrTH Heliothisb pGlu Leu Thr Phe Ser Ser Gly Trp Gly Asn NH2
Hymenoptera Tenar-HrTH Tenthredo pGlu Leu Asn Phe Ser Thr Gly Trp Gly Gly NH2
=Schgr-AKH-II Xylocopa, Bombus pGlu Leu Asn Phe Ser Thr Gly Trp NH2
=Grybi-AKH Vespula, Vespa pGlu Val Asn Phe Ser Thr Gly Trp NH2
=Manse-AKH Apis pGlu Leu Thr Phe Thr Ser Ser Trp Gly NH2
Adipokinetic and Hypertrehalosemic Neurohormones
A
47
 48
A

Adipokinetic and Hypertrehalosemic Neurohormones, Table 3 Representative sequences of adipokinetic/hypertrehalosemic peptides from vari-
ous insect orders (Continued)
Order Peptide name Genus Structure
1 2 3 4 5 6 7 8 9 10
Diptera Phote-HrTH Phormia, pGlu Leu Thr Phe Ser Pro Asp Trp NH2
Adipokinetic and Hypertrehalosemic Neurohormones

Drosophila
Anoga-AKH Anopheles pGlu Leu Thr Phe Thr Pro Ala Trp NH2
Tabat-AKH Tabanus pGlu Leu Thr Phe Thr Pro Gly Trp NH2
Crustacea Panbo-RPCH Pandalus pGlu Leu Asn Phe Ser Pro Gly Trp NH2

a
Note that the peptide in certain orders is identical. For example: Peram-CAH-I and -II of the Blattodea, Blattidae is also present in Coleoptera (Leptinotarsa); Schgr-AKH-II
of Orthoptera, Caelifera is present in Orthoptera, Ensifera and in Hymenoptera (Xylocopa, Bombus); Grybi-AKH of Orthoptera, Ensifera is also present in Dermaptera, Neu-
roptera and Hymenoptera, etc.
b
Heliothis is revised to Helicoverpa.
 Adipokinetic and Hypertrehalosemic Neurohormones
A 49

Some of the members of this peptide family anbo-RPCH peptide which has a chromatophoro-
P
have additional post-translational modifications tropic effect. Panbo-RPCH has also been found in
besides the blocked termini. For example, two an insect species, the heteropteran stinkbug, Nezara
HrTH decapeptides are present in the corpora viridula, where it has an adipokinetic effect.
cardiaca of the stick insect, Carausius morosus; Phylogenetic relationships of the HrTHs have
one of these decapeptides is glycosylated and has a been proposed for the cockroaches based on mor-
unique C-glycosylation where the sugar is linked phological, behavioral and physiological charac-
to the C-2 atom of the indole ring of tryptophan. ters congruent with the distribution of the various
Another unusual modification has been found in structures of the HrTHs within the order.
an AKH of the protea beetle, Trichostetha fascicu-
laris: the corpora cardiaca contain two AKHs, one
of which is an octapeptide with a phosphothreo- Physiological Actions
nine at position 6.
The relationships between individual AKH The general physiological action of the adipoki-
and HrTH peptides and insect species are complex. netic and hypertrehalosemic hormones in insects
There are no clear rules concerning which peptide is to elevate the hemolymph metabolites that are
occurs in which order of insects. Several species used by the muscles and other tissues as a source
within an order may share the same peptide and of energy, regardless of the nature of the metab-
have other species-specific sequences, and the same olites. This is accomplished by stimulating the
peptide may be present in species of different fat body, which is the hormones target tissue, to
orders. As described above, the two locust species, convert its stores of triacylglycerides or glycogen
S. gregaria and L. migratoria, share an identical to diacylglycerides or trehalose, respectively, or
decapeptide (Locmi-AKH-I); each species pos- to synthesize proline. The diacylglycerides, tre-
sesses a second, unique octapeptide (Locmi- halose or proline are released from the fat body
AKH-II; Schgr-AKH-II); and L. migratoria contains to increase their respective levels in the hemo-
a third octapeptide (Locmi-AKH-III) that does not lymph. The same peptides that elevate diacylg-
have a complement in S. gregaria. Cockroach spe- lycerides in locusts elevate trehalose when
cies of the families Blattellidae and Blaberidae administered to cockroaches, and vice versa, and
share a single hypertrehalosemic decapeptide hor- the hormones of locusts and cockroaches elevate
mone (Bladi-HrTH), whereas cockroaches of the proline in the Colorado potato beetle. The deci-
family Blattidae contain two octapeptide hormones sion as to whether lipid-, carbohydrate-, or pro-
(Peram-CAH-I and -II). In addition, there is over- line-mobilizing pathways are activated is a
lap between orders. Grybi-AKH is present in cer- species-related function of the enzyme composi-
tain crickets and in species of Neuroptera, tion in the fat body.
Dermaptera and Heteroptera. Peram-CAH-I and Muscular activity for animal locomotion can
-II of the blattid cockroaches are also found in the involve either long-term or short-term events.
Colorado potato beetle, Leptinotarsa decemlineata, Long-term activities might entail sustained, non-
and Peram-CAH-II is shared with the heteropteran emergency actions such as migration or persistent
bug, Pyrrhocoris apterus. Whereas Peram-CAH-I searching for food, mates or shelter. Short-term
and -II mobilize glycogen from the fat body of the activities might consist of local searching activi-
cockroach to increase hemolymph trehalose, the ties but may also require immediate, brief, emer-
same or similar peptides increase hemolymph pro- gency responses such as evading attack by a
line in beetles to serve as the major flight substrate. predator or defending a breeding territory. Long-
Unlike the complex situation in insects, the term events require a steady supply of energy
crustaceans apparently possess only the single metabolites, whereas short-term events may be
50
A Adipokinetic and Hypertrehalosemic Neurohormones

brief but intense, and, if successful, they can be By contrast, insects such as cockroaches,
followed by a period of recovery to replenish bees and flies use only carbohydrate (trehalose)
exhausted metabolites. as the primary source of energy for muscular
The adipokinetic hormones are often involved activity and locomotion. These species do not
in prolonged, constant muscular activity such as migrate and lack the adipokinetic response, but
migration. This is characteristically true for the they are faced with emergency situations of pred-
locusts whose migratory behavior has been ator evasion, and in such cases, the hypertreha-
described since biblical times. Migration is a sus- losemic hormone mobilizes trehalose in response
tained flight activity that uses muscular oxidation to the emergency. However, injections of hyper-
of fatty acids to produce energy, since fatty acids trehalosemic hormone show that significant ele-
deliver more energy per mole than carbohydrates. vation of the hemolymph trehalose may take as
However, carbohydrate serves as the major source long as 1030 min. This delay in elevating hemo-
of muscular energy during initial flight, and lipid lymph carbohydrate is too long to significantly
becomes the major source for energy as flight per- assist the insect in evading capture. Furthermore,
sists and becomes sustained. Based on differing the open circulatory system of insects does not
physiological effects, it is speculated that the three efficiently direct circulating metabolites to the
AKHs may exert different regulatory actions on muscles in the manner of the closed circulatory
metabolite mobilization and use during the differ- system of vertebrate animals. Energy metabolites,
ent stages of migration. Locmi-AKH-II is likely to such as trehalose, must constantly be maintained
be the major carbohydrate-mobilizing hormone at high levels in the hemolymph to meet urgent,
that provides trehalose for initial flight; Locmi- immediate demands. Hence, the role of the
AKH-I is the major hormone responsible for fat hypertrehalosemic hormone appears to be to
mobilization during sustained flight and Locmi- replace depleted hemolymph trehalose and main-
AKH-III may be responsible for regulating energy tain it at high levels. Maintenance of high treha-
metabolism during rest. Furthermore, during lipid lose levels allows the insect to make quick
mobilization, AKH performs several distinct but responses to elude capture that may require only
related actions. In the fat body, AKH activates seconds, or at most, several minutes to conclude.
lipase for triacylglyceride degradation; this is If the insect is successful at escape, the hormone
achieved by binding of the AKH to a G-protein stimulates the degradation of fat body glycogen
coupled receptor at the cell membrane, activation to restore the high trehalose levels by activating
of adenylate cyclase resulting in the second mes- specifically the enzyme glycogen phosphorylase
senger cAMP which, in conjunction with Ca2+, is after the hormone has bound to a G-protein cou-
responsible for lipase activation. In the hemo- pled receptor on the membrane of a fat cell and
lymph, AKH increases the lipid-carrying capacity had activated a phospholipase C, resulting in the
of lipophorins (proteins) resulting in increased production of inositol trisphosphate and the
amounts of low-density lipophorin for shuttling release of Ca2+ from internal stores (influx of
lipids from the fat body to the muscles. At the flight external Ca2+ is also activated by HrTH) which
muscle level, AKH increases the rate of lipid oxi- sets in motion a cascade of activation of kinases
dation. Recent research on a number of terrestrial and, finally, glycogen phosphorylase. Removal of
and aqueous heteropteran bugs that have various the hypertrehalosemic hormone does not affect
feeding patterns (plant sap sucking, predators, the ability of such insects to be active for the
obligatory hematophagous), also established a lip- short term (several minutes), but after exhaus-
id-based activity (flight and/or swimming) metab- tion, lengthens their recovery time.
olism that is regulated by the respective AKHs of Tsetse flies and various beetle species fuel
these insects. their flight metabolism by the partial oxidation of
 Adjuvants
A 51

proline and the production of alanine. For con- individual biology of the insect species in which
tinuous flight or replenishment of proline reserves they are found. They display a unique relation-
in the fat body a unique system exists in these ship with their target tissue in that the hormone
insects to synthesis proline: the respective AKHs carries the endocrine message to the target tissue
activate a lipase in the fat body and the fatty acids (fat body) to mobilize energy stores, but the tar-
that are liberated from triacylglyerols undergo get tissue determines which metabolic pathways
-oxidation, and the resulting acetyl CoA units are are activated depending on the biology of the
used in conjunction with alanine to synthesize species. It is this biology that determines the
proline. Alanine, which is derived from the partial nature of the muscular activity (prolonged
oxidation of proline, is re-used for proline synthe- migration; briefpredator evasion) and its meta-
sis and can be viewed as a shuttle system for the bolic need for consuming carbohydrates, lipids
transport of acetyl units. or proline as a source of energy.
Although the mobilization of energy for
flight and other metabolically intense situations
is likely the major function for the adipokinetic
References
and hypertrehalosemic hormones, the hormones
exhibit pleiotropic actions. The hypertreha-
Beenakkers AMT (1969) The influence of corpus allatum and
losemic hormones were isolated originally based cardiacum on lipid metabolism in Locusta. Gen Comp
on their cardioacceleratory action on the heart. Endocr 13:492
This is a logical action for the hormone since ele- Fernlund P, Josefsson L (1972) Crustacean color-change hor-
mone: amino acid sequence and chemical synthesis.
vated heartbeat rate would facilitate distribution Science 177:173175
of the energy metabolites throughout the body Gde G (1989) The hypertrehalosaemic peptides of cock-
and assure their ready access to the muscles. In roaches: a phylogenetic study. Gen Comp Endocr
keeping with the stimulatory action of AKH on 75:287300
Gde G (2004) Regulation of intermediary metabolism and
lipid degradation in locusts, lipid synthesis is water balance of insects by neuropeptides. Annu Rev
inhibited by AKH. Other, less well characterized Entomol 49:93113
actions include: inhibition of RNA and protein Mayer RJ, Candy DJ (1969) Control of haemolymph lipid
concentration during locust flight: an adipokinetic hor-
synthesis related to vitellogenesis in locusts and
mone from the corpora cardiaca. J Insect Physiol
crickets, and the stimulation in cockroaches of 15:611620
the oxidative capacity of mitochondria during fat Steele JE (1961) Occurrence of a hyperglycemic factor in the
body maturation, and of gene expression for a fat corpus cardiacum of an insect. Nature 192:680681
Stone JV, Mordue W, Batley KE, Morris HR (1976) Structure of
body cytochrome P450 related to lipid oxidation. locust adipokinetic hormone, a neurohormone that regu-
These latter actions by the hormones may be lates lipid utilization during flight. Nature 263:207221
equally important as their effects on mobilization Vroemen SF, van der Horst DJ, van Marrewijk WJA (1998)
of energy metabolites, but they are poorly eluci- New insights into adipokinetic hormone signalling. Mol
Cell Endocrinol 141:712
dated because of insufficient research, and they
cannot yet be placed into perspective as to their
physiological significance. Other actions in which
AKHs seem to be involved are an enhanced acti- Adjuvants
vation of the locust immune system and, possi-
bly, in the activation of an antioxidant protection Chemicals added to insecticides to improve their
mechanism in potato beetles. effectiveness. Examples of adjuvants include toxic-
In summary, the adipokinetic-hypertreha- ity, stability, and adhesion.
losemic-hyperprolinemic hormones constitute Insecticide Formulations
a family of peptides that are adapted to the Insecticides
52
A Adoption Substance

Adoption Substance Adventive

A secretion presented by a social parasite that An organism that has arrived in an area from else-
induces the host insects to accept the parasites as where. It is not native, and likely arrived as an
members of their colony. invader or accidental introduction. It is also known
Social Insect Pheromones as nonindigenous.
Invasive Species

Adult
Aedeagus
The sexually mature stage of an animal. The adult
is usually the winged stage in insects. With rare The intromittent (copulatory) organ of the male;
exceptions, the adult does not molt again. the distal portion of the phallus. Sometimes
Metamorphosis referred to as the penis.
Abdomen of Hexapods

Adulticide
A pesticide used to kill adult insects. This term
Aenictopecheidae
often is used to describe products used to kill adult
A family of bugs (order Hemiptera).
mosquitoes. (contrast with larvicide)
Bugs
Insecticides

Adultoid Reproductive Aeolothripidae

In higher termites, a supplementary reproductive A family of thrips (order Thysanoptera). They
that in indistinguishable morphologically from commonly are known as broad-winged thrips or
the reproductive. banded thrips.
Thrips

Adult Transport
A behavior in which social insects (usually ants)
Aepophilidae
drag or carry their nestmates to a new location.
A family of bugs (order Hemiptera). The some-
This normally occurs during colony emigration.
times are called marine bugs.
Bugs

Adventitious Veins
In some insects, additional wing veins are present Aeshnidae
which are neither secondary nor intercalary veins.
They usually are the result of the lining up of cross A family of dragonflies (order Odonata). They
veins. commonly are known as darners.
Wings of Insects Dragonflies and Damselflies
 African Armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae)
A 53

Aetalionid Treehoppers even though it causes no economic loss. The

presence of some insects in homes or on orna-
Members of the family Aetalionidae (order mental plants are examples of aesthetic pests,
Hemiptera). though in the latter case if they inhibit the ability
Bugs to market plants then the same insect can be
come an economic pest.
Economic Injury Level (EIL) and Economic
Aerial Photography Threshold (ET) Concepts in Pest Management

In pest management, photographs taken by an air-

plane or satellite that are used to identify varia- Aestivation
tions within fields/crops to help make management
decisions. A state of inactivity or curtailment of normal
activity during the summer months. Diapause

Aeropile
Aetalionidae
The opening in the egg surface (chorion) through
which air enters. A family of insects in the order Hemiptera. They
sometimes are called aetalionid treehoppers.
Bugs
Aerosol Treehoppers

The air suspension of liquid or solid particles of

small diameter. This is a common formulation for African Armyworm, Spodoptera
flying insects or for household use where noaddi- exempta (Walker) (Lepidoptera:
tional formulation or preparation is desired. Noctuidae)
Insecticides
Insecticide Formulations joe c. b. kabissa
Tanzania Cotton Lint and Seed Board, Dar Es
Salaam, Tanzania
Aesthetic Injury Level
The African armyworm (Fig. 21) is a larva of a
The level of pest abundance above which aesthetic, nocturnal moth, Spodoptera exempta (Walker).
emotional, or sociological considerations require This species, although commonly referred to as
pest control actions. Economic considerations are the African armyworm, occurs rather widely in
not relevant. the grasslands of tropical and subtropical Africa
Economic Injury Level (EIL) and Economic and Asia. In Africa, where S. exempta is of major
Threshold (ET) Concepts in Pest Management economic importance, its occurrence is confined
to countries south of the Sahara: Tanzania, Kenya,
Uganda, Ethiopia, Somalia, Malawi, Zimbabwe,
Aesthetic Pest Zambia and South Africa. Outside Africa, S.
exempta has been reported from southwest Saudi
A pest which, through its presence or actions, is Arabia in the republic of Yemen, southeast Asia,
deemed objectionable and in need of elimination Australia, New Zealand and Hawaii.
54
A African Armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae)

African Armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae), Figure 21 African armyworm:
top left, adult female, top right, adult male; middle left, solitary form of larva; middle right, gregarious form
of larva; lower left, pupae in soil; lower right, eggs on foliage.

During an armyworm outbreak, larvae of exceed 1,000 per m2 over areas covering tens or
S. exempta march together in long columns, akin even hundreds of square km.
to army columns, in search of susceptible plant In Africa, S. exempta is adapted for survival on
material. This is the basis for the name army- seasonal grasslands by combining a high intrinsic
worm. When susceptible plant material is found, rate of increase with migration to places of rainfall
it is often voraciously devoured to ground level. In where grasses are suitable for survival of its cater-
typical armyworm outbreaks, larval density may pillars. Because of its capability to move over long
 African Armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae)
A 55

distances, hundreds and sometimes thousands of Adults emerge within 712 days after pupa-
km across national boundaries freely, S. exempta is tion and can live up to 14 days if appropriately
truly an international pest. Often times it appears fed. In their lifetime, females can lay up to 1,000
sporadically and suddenly in dense outbreaks capa- eggs. Spodoptera exempta is not known to enter
ble of causing extensive and enormous damage to into any type of diapause. This probably explains
susceptible rangeland grasses, cereal crops and sug- why this species has to migrate soon after
arcane. Because of its ability to appear suddenly and emergence.
then disappear equally suddenly, the African army- Spodoptera exempta exhibits a phenomenon
worm has sometimes been referred to by farmers as called polyphenism, or phase polymorphism (i.e.,
the mystery worm. The scale of devastation to the occurrence in a population of two or more
crops and pastures by armyworm is comparable phenotypes due to exposure to different environ-
only to that caused by locusts. Thus, the armyworm mental conditions). For example, up until the
is greatly feared wherever it occurs. third molt, all larvae of S. exempta remain green
in body color. However, at this stage, depending
on whether there are many larvae or just a few,
Biology and Ecology they will turn black or remain in various shades
of green or brown. If there are large numbers of
Adult moths of S. exempta have a wing span in the larvae present as in a typical outbreak situation,
range of 2037 mm. The forewings are character- larvae tend to be characteristically velvety black
ized by an overall dull gray-brown appearance. The on top with pale lines on each side and green-
hind wings are whitish with dark veins. The two ish-yellow underside; this phenotype is called
sexes can be distinguished by examining the num- the gregarious phase. It is during this phase that
ber of bristles on the frenulum (the mechanism S. exempta is most devastating to crops. Larvae
that couples the fore and hind wings during flight), in the gregarious phase tend to be very active
which are single in the males and multiple in the and often march on the soil in one direction only
females. A characteristic feature of the African looking for fresh food. They also feed high on the
armyworm is the presence of racquet-shaped scales plant during the day.
at the tip of the abdomen of the males and black However, if not crowded, the developing lar-
scales on the tip of the body of the females. vae remain one of the many shades of green, pink
Females of S. exempta lay between 100 and or brown color until they pupate. In contrast to
400 eggs per night in a mass covered by black black gregarious larvae, they are sluggish, living
scales from the tip of their abdomen. Eggs are mostly at the bases of plants and are not as
small, 0.5 mm in diameter, whitish in color, but destructive to crops. Although their appearance is
then turn black prior to hatching. Eggs are often so different, they are the same insect and one may
laid on the lower side of leaves and hatch in about easily be converted into the other. Nevertheless,
24 days after oviposition. There are six larval because moths derived from gregarious and soli-
instars extending over a larval period of between tary larvae exhibit the same level of readiness to
14 and 22 days depending on the temperature and fly, phase change in S. exempta is construed as
the host plant on which the larvae have been being merely a stress phenomenon associated
reared. Fully grown sixth instar larvae are often with crowding. It is unknown whether this aspect
2535 mm long. Pupation occurs 23 cm below of phase polymorphism is of any evolutionary
the soil surface. This process is often preceded by a significance to S.exempta. In the case of locusts,
sudden and synchronized disappearance of larvae it is thought that the solitary form is the one
that quickly burrow into the ground, particularly that enables the populations to persist at a low
if soil conditions are moist enough. level during the dry season when there are no
56
A African Armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae)

outbreaks occurring. It is worth speculating, in temporary loss of contact with the main popula-
the case of S. exempta, that at such low densities, tion in remote and perhaps uninhabited areas.
its populations continue to breed during the dry This continuity implies that the first outbreaks to
season in areas where grasses remain green, such appear in East Africa are due to the migration of
as in the cool highland areas and, more especially, parent moths from the north at the end of the sea-
the coastal areas where it is hot and there are peri- son. Although there is ample evidence of adult
odic showers during the dry season. This form dispersal on the wind over distances up to several
may, therefore, be of some critical survival value hundred km in a few successive nights, there is lit-
for this pest. tle evidence in support of a southward dispersal at
the start of an armyworm outbreak in East Africa.
The concentration hypothesis, on the other
Seasonal Movements and hand, postulates that because of occasional cap-
Armyworm Outbreaks ture of moths in traps during the off-season, as
well as the finding of rare caterpillars after con-
Upon emergence, adult moths of S. exempta are certed searches, S. exempta persists during such
fully capable of movement from their breeding times of year as uncrowded populations (the soli-
sites to new areas. Such flights can be very short, or tary phase, in which caterpillars remain green and
very long, depending on whether they are carried unreported), and that the first outbreaks of the
in a downwind direction or not. Nevertheless, season are due to concentration of moths before
because they are one-way journeys, they cannot, the synchronized mating and egg laying.
therefore, be regarded as migration in its strict Thus, there seem to be two types of armyworm
ethological sense where there is invariably a outbreaks: primary and secondary outbreaks. Dur-
return flight to breeding sites. ing primary outbreaks, sources of outbreaks are the
The question of how armyworm outbreaks low density populations that survive and breed
start has baffled scientists and farmers alike for a during dry seasons in green areas of the coast and
long time. Because moths emerge over a period of the highlands. Secondary outbreaks occur down-
up to 12 days, and can also fly off on migration at wind from the coast near the first highlands. Dur-
different times, they become widely dispersed and ing years of serious armyworm outbreaks, the first
do not form swarms as occurs with locusts. More- outbreaks often start in Tanzania, Zimbabwe and
over, the moths are weak fliers and are often carried Malawi at about the beginning of the wet season in
in a downwind direction. Thus, moths disperse in December, and are followed by a progression of
space and time downwind. For purposes of this outbreaks at about one generation time-intervals
narrative, an armyworm outbreak is simply from Tanzania through Kenya, Uganda, Ethiopia,
described as the sudden appearance of larval infes- Somalia to the Yemen and from Zimbabwe to
tations, often simultaneously on many farms in South Africa. Wind convergence plus localized
one region. weather and moth behavior provide the mecha-
Two hypotheses, the continuity and the con- nism for transporting and concentrating moths
centration hypotheses, have been put forward in emerging from primary outbreaks.
order to explain how outbreaks begin during an Flight mechanisms of S. exempta prior to out-
armyworm season. The continuity hypothesis, breaks have been the subject of extensive studies.
which is based on biogeographical analyses of past After drying and hardening their wings, moths first
outbreaks, proposes that much of the armyworm move up into the trees. Then, when they are ready,
population is always at crowded, outbreak densi- they fly up several hundreds of meters into the air,
ties, and that the seasonal absence of reports rep- where if caught up by prevailing wind, are carried
resents not a real absence of outbreaks, but a away downwind. When dawn arrives, the moths
 African Armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae)
A 57

descend and hide on the ground in the grass, but at the dry season. But since they have no diapause,
dusk they take off again. They will continue to do they must be living and breeding somewhere. It
this for several days, either until they die, or until has now been established that they survive in quite
they come to an area where rain is falling. Rain low numbers along the coastal area, where some
causes the moth to descend to the ground. The rain falls in every month of the year. When the
winds coming out of the rainstorm have the effect rains begin again in central Tanzania, small num-
of concentrating the moths, rather as though they bers of moths migrate inland from the coast and it
were being swept together with a brush. This is the is these that cause the first outbreaks.
reason why armyworms occurring during out-
breaks are not evenly distributed. Upon descent to
the ground, moths tend to drink water if this is Economic Importance of
available, mate and then lay their eggs. At this stage Outbreaks of S. exempta
dispersal will have come to an end.
In Africa, seasonal rains are brought by the During armyworm outbreaks, feeding damage by
meeting of large scale winds from the northeast S. exempta to cultivated and wild host plants is
and the southwest at the Inter-Tropical Conver- almost entirely restricted to the leaves, although
gence Zone (ITCZ). The position of the ITCZ when food is scarce, the young stems or flowers,
moves with the sun across the tropical zone twice particularly of wild grasses, may also be eaten up.
each year, from north to south between July and The young larvae at first eat the upper and lower
December and from south to north between Janu- surface tissue of the leaves, which results in the
ary and June. The first outbreaks, designated as skeletonization, or windowing, of the leaves. As a
primary outbreaks in East Africa, usually occur in rule, armyworm larvae tend to prefer young plants
central Tanzania in November or December. and recently germinated crops, often defoliating
Occasionally they occur further south, in Mbeya, them to ground level. It is estimated that two lar-
Mtwara and Lindi regions of Tanzania. More vae can completely destroy a 10-day-old maize
rarely, they occur in southeastern Kenya. plant with 67 leaves and a single larva can con-
Moths produced by these primary outbreaks sume 200 mg of dry mass of maize leaves in the
are then carried by the wind towards the ITCZ, course of the sixth instar.
which has meanwhile moved north. The moths are Destruction of cereal crops such as maize,
thus concentrated in areas where the rains are just rice, wheat or sorghum often necessitates replant-
beginning, and so they breed and multiply yet again. ing of the entire affected crop. S. exempta larvae
If conditions are suitable, they will increase at an are most damaging to cultivated and wild host
enormous rate. Although the first outbreaks are only plants during outbreaks when gregarious bands of
a few hectares in extent, by February and March larvae travel together on the ground. Such army-
there may be outbreaks of hundreds of square km. worm outbreaks are often capable of causing total
Thus, as the ITCZ takes the rains northwards, so crop loss within hours at the local level. Thus, crop
the moths, carried by the prevailing wind, move with losses as a result of armyworm outbreaks can be
it, bringing new armyworm outbreaks, designated potentially devastating to local and national econ-
secondary outbreaks, to northern Tanzania, Kenya, omies as they occur in some of Africas most
Somalia, Ethiopia, Sudan and eventually Yemen. impoverished economies. Losses are sometimes
Armyworm outbreak seasons vary greatly in sever- difficult to assess quantitatively because of hidden
ity, extent and timing in each of these countries. costs such as effects of forage destruction, damage
From September to November, there are sel- to subsistence farms, the expense of additional
dom armyworm outbreaks in any part of eastern seed and, most importantly, food aid from interna-
Africa. The armyworm seems to disappear during tional donors.
58
A African Armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae)

Survey and Control associated with armyworm monitoring, forecast-

ing and control in countries most ravaged by this
Circumstantial evidence from light and phero- pest is the inadequacy of funding for these
mone traps shows that long distance migrations operations.
occur between moth emergence and the next Because elimination of all primary outbreaks
breeding areas which are in the vicinity of seasonal is almost impossible to achieve, management
passages of low-level wind convergence such as strategies for S. exempta tend to focus more on
Inter-tropical Convergence Zone or African Rift suppression of secondary outbreaks. This approach
Convergence Zones. Furthermore, increasing lev- has invariably been dependent on the application
els of moth catches in light and pheromone traps of pesticide sprays. To date, a series of low toxicity
have been found to be followed by increased prob- pesticides are often used (e.g., synthetic pyre-
ability of infestations of larvae occurring 24 throids, carbamates and organophosphates). Pre-
weeks later at up to 200 km from the trap. viously, highly toxic, persistent and broad spectrum
Because primary outbreaks of S. exempta orig- pesticides such as DDT, BHC, dieldrin and a series
inate from moths taken downwind from sources of others were used due to lack of alternative, safer
nearest the coasts of eastern Africa, and concen- products. However, due to the need for rapid
trate where heavy rains are falling, control of this intervention and coverage of fairly extensive areas
pest involves accurately detecting primary out- during outbreaks, newer oil-based pesticides are
breaks and eliminating them before the subsequent being applied as ultra-low volume (ulv) formula-
moths emerge and move downwind causing sec- tions using hand held, battery driven applicators.
ondary outbreaks in another region or country. Nevertheless, suppression tactics are only cost-
The major objective is to kill as many armyworms effective when applied in a timely manner on
as possible on pasture or crops before subsequent farmland. Outbreaks occurring on uncultivated
moths emerge and move downwind. Normally, the land often remain unchecked.
largest and densest outbreaks are attacked first. Unfortunately, control of armyworms by less
This approach is referred to as strategic control. toxic means has received far less attention than in
However, because primary outbreaks often remain the case of other international migratory pests
unnoticed until after secondary outbreaks have such as locusts, which have been the targets for
occurred, direct elimination of the latter becomes tests involving fungi, protozoa and even viruses.
the main objective in multiple outbreak situations. Extensive studies in eastern Africa have con-
Monitoring possible sources of the moths that firmed that all life stages of the armyworm are
cause primary outbreaks has involved deployment subject to attack by a diversity of natural enemies.
of a network of light and pheromone traps, as well For example, up to 90% of armyworm caterpillars
as ground searches for low-density larvae in the in the last instar can be killed by a nuclear polyhe-
off-season in areas historically known to be sites drosis virus (NPV). Similarly, pupal and prepupal
of primary outbreaks. In addition, for all primary stages can be killed by a cytoplasmic virus. The
outbreak areas, rainfall stations must report on a only fungus known to attack armyworms during
weekly or daily basis the amount of rainfall during conditions of high humidity and temperature is
the first month of the rainy season. Recently, there Normuraea rileyi. Armyworms infected by this
have been attempts to introduce predictive models fungi typically climb to the top of grass blades
that integrate African Real Time Environmental where they die amidst masses of mycelia.
Monitoring and Information System (ARTEMIS) Armyworm larvae are also subject to parasit-
and satellite imagery and synoptic weather data ism by some 28 species of tachnid flies (Diptera:
that has been applicable for detection and elimina- Tachinidae). In cases of parasitism from wasps
tion of gregarious locusts. The major challenge (Hymenoptera), some 25 parasitoids have been
 African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae)
A 59

isolated from eggs, larvae and pupae of S. exempta. 2

Florida Department of Agriculture and Con-
Apart from attack by parasitoids, there are several sumer Services, DPI, Gainesville, FL, USA
arthropod predators that prey on armyworms,
including ants (Hymenoptera: Formicidae) and The African honey bee (Apis mellifera scutellata
beetles (Coleoptera), which often prey on eggs and Lepeletier) is a subspecies (or race) of western
early larval stages of S. exempta. To date, there has honey bee (A. mellifera L.) that occurs naturally in
been no effort to study the potential of some of sub-Saharan Africa but has been introduced into
these natural enemies for commercialization. the Americas. More than 10 subspecies of western
Armyworm outbreaks also attract flocks of avian honey bees exist in Africa and all justifiably are
predators, notably storks such as Marabou storks, called African honey bees. However, the term
white (European) storks and Abdims storks. Occa- African (Africanized) honey bee refers exclu-
sionally, such assemblages of predators help to sively to A.m. scutellata in the bees introduced
eliminate small primary or secondary outbreaks range (Fig. 22).
of S. exempta. Subspecies of western honey bees are native
For the more foreseeable future, it is evident to Europe and Africa but have been spread widely
that preventive control of armyworms will con- outside their native range due to their economic
tinue to rely on diligent surveillance during reces- importance as pollinators and producers of honey.
sions and, as outbreaks occur, intensified scouting Initially, only European subspecies of honey bees
will be necessary to locate and then eliminate (hereafter referred to as European bees) were
pockets of solitary morphs before outbreaks. introduced into the Americas, where they were
found to be productive in temperate North America
but less so in Central and South America where
tropical/subtropical climates dominate. In response
References to the poor performance of European bees in
Brazil, Warwick Kerr, a Brazilian scientist, traveled
Regional Armyworm Programme of Desert Locust Control to southern Africa to screen African honey bee
Organization for Eastern Africa (1992) The African
armyworm DLCO-EA, Addis Ababa, Ethiopia, 19 pp
subspecies for productivity and viability. His visit
Meinzingen WF (ed) (1993) African armyworm. In: A guide resulted in the importation of A.m. scutellata into
to migrant pest management in Africa. FAO AGP, Rome, Brazil in the late 1950s.
Italy, pp 7185 Dr. Kerr hoped that through experimentation
Rose DJW (1979) The significance of low-density popula-
tions of the African armyworm, Spodoptera exempta. and selective breeding, the African bee could be
(Walker). Philos Trans R Entomol Soc London B made manageable and available for use by Brazilian
287:393402 beekeepers. As such, he initiated efforts to breed
Odiyo PO (1979) Forecasting infestation of a migrant pest:
gentleness into the African stock while amplifying
the African armyworm, Spodoptera exempta. (Walker).
Philos Trans R Entomol Soc London B 287:403413 its many positive traits. The breeding effort was
not carried to completion because the African
bees swarmed accidentally, ending their initial
quarantine. Following this, the bees began to
African Honey Bee, Africanized spread throughout Brazil and into other parts of
Honey Bee, or Killer Bee, Apis South America.
mellifera scutellata Lepeletier All subspecies of Apis mellifera can interbreed
(Hymenoptera: Apidae) or hybridize. Consequently, African bee hybrid-
ization with European bees became frequent as
jamie ellis1, amanda ellis2 African bees moved into areas previously occu-
1
University of Florida, Gainesville, FL, USA pied by European bees. It is this hybridization with
60
A African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae)

African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier
(Hymenoptera: Apidae), Figure 22 The natural distribution of Apis mellifera scutellata in Africa (modified
from Hepburn HR, Radloff SE (1998) Honeybees of Africa. Springer-Verlag, Berlin, 370 pp), and its
distribution in the Americas.

European honey bees that earned them the name ovement through South and Central America
m
Africanized honey bees. Traditionally, African was rapid and largely unassisted by humans, African
and Africanized have been used interchangeably bees earned the reputation of being the most suc-
although the former really refers to the pure race cessful biologically invasive species of all time. In
and the latter to the hybrid. 1990, populations of African honey bees had satu-
The spread of African bees throughout South rated South and Central America and begun to
and Central America, fueled by rapid hybridization move into the USA. As of 2006, African honey bees
with European subspecies and the dominance of were established in the southernmost USA: Texas,
African alleles over European ones, occurred at a California, New Mexico, Arizona, Oklahoma, Lou-
rate of 200300 miles per year. Because their isiana, Arkansas, Alabama, and Florida.
 African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae)
A 61

The spread of African bees in the U.S. contin- of honey bee colonies by humans) is more com-
ues, albeit at a much slower rate than what occurred mon in Europe, where the native honey bees have
throughout South and Central America. This been bred for gentleness and ease of management.
slowed rate of territory expansion appears due to In contrast, honey hunting (near-complete
climatic limitations. African bees do not survive in destruction of hive to harvest contents) is more
temperate climates as well as European bees do. common in Africa, resulting in a bee that is more
Therefore, they have failed to establish populations defensive of its nest. Other selection pressures
below about 32 latitude in the southern hemi- that led to a heightened defensiveness in African
sphere. Although they have expanded beyond bees include climatic stresses, resource availabil-
this parallel in the northern hemisphere, African ity, and predation by birds, mammals, and various
bee expansion northward also appears limited reptiles. These selection pressures resulted in an
climatically, being found only below about 34 African race of bee that can be 10+times more
latitude currently. defensive than any of the various European races
of bee.
All honey bees readily defend their nests, and
Description and Behavior an attack usually means that the victim is too close
to the nest. While European races of bees may
African honey bees cannot be distinguished from attack a nest intruder with >10 bees, African bees
European honey bees easily, although they are may attack the same intruder with >1,000 bees.
slightly smaller than the various European races. Further, African bees defend a larger radius around
Laboratory personnel use morphometric analy- their nest and require lower levels of stimuli to ini-
ses to determine the likelihood that a given col- tiate an attack. Because of these characteristics,
ony is Africanized or fully African. With honey African bees are capable of killing large mammals,
bees, the measurement of wing venation patterns including man. This defensiveness has earned
and the size and coloration of various body parts them the nickname killer bee. It is important to
(morphometry) are important determinants of note that their ability to kill humans has nothing
identification at the subspecific level. Morphom- to do with their size or the potency of their venom.
etry has been used to differentiate honey bee African bees are smaller than European bees and
races since the 1960s and remains the first round probably deliver a comparatively smaller dose of
of identification when suspect colonies are dis- venom to their victim than do European bees.
covered. Morphometric analyses were first used Because both bees use the same type of venom,
to differentiate Africanized and European honey human deaths are a result of the number of stings
bees in South America in 1978. A more rigorous they receive rather than an increased potency of
identification is achieved by genetic analysis and African bee venom.
often is necessary when the suspect bees are a Another behavioral difference between Afri-
hybrid between African bees and the European can and European bees concerns colony level
subspecies. reproduction and nest abandonment. African
Other differences between African and Euro- honey bees swarm and abscond in greater frequen-
pean bees manifest themselves behaviorally. To cies than their European counterparts. Swarming,
the casual bystander, the primary identifying bee reproduction at the colony level, occurs when a
behavioral characteristic of Africanized bees is single colony splits into two colonies, thus ensuring
their heightened defensiveness compared to that survival of the species. European colonies com-
of European subspecies. Selection pressures monly swarm 13 times per year. African colonies
induced by man are, in part, responsible for this may swarm >10 times per year. African swarms
increased defensiveness.Beekeeping (management tend to be smaller than European ones, but the
62
A African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae)

African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier
(Hymenoptera: Apidae), Figure 23 (a) African bees swarm readily and nest in unusual locations,
including (b) exposed on tree limbs, (c) within cavities in the soil, (d) within discarded furniture.

swarming bees are docile in both races. Regardless, volume than European honey bees and have been
African colonies reproduce in greater numbers found in water meter boxes, cement blocks, old
than European colonies, quickly saturating an area tires, house eaves, barbecue grills, cavities in the
with African bees. Further, African bees abscond ground, and hanging exposed from tree limbs, just
frequently (completely abandon the nest) during to name a few places. One rarely finds European
times of dearth or repeated nest disturbance, while colonies in any of these locations because they
this behavior is atypical in European bees. prefer to nest in larger cavities like those provided
Another common difference between African by tree hollows, chimneys, etc. As one can imagine,
and European honey bees is their choice of nest humans inadvertently provide multiple nesting
locations. African honey bees are less selective sites for African bees. Therein lies the primary rea-
when considering a potential nesting site than are son African bees are encountered frequently by
European bees. They will nest in a much smaller humans (Fig. 23).
 African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae)
A 63

A final behavioral curiosity of African bees bees, but key differences confer adaptive benefits
concerns nest usurpation (or colony takeover) to the former.
of European colonies. Small African swarms Virgin queens of all western honey bees
containing a queen often land on the outside emerge from peanut hull-shaped waxen cells. After
infrastructure of a European colony (a wall, a short time of further maturation, a virgin queen
beekeeper-managed hive, etc.). As time passes, will leave the colony to mate with drones. All mat-
the worker bees in the African swarm begin to ing occurs in the air, with the fastest drones being
exchange food/pheromones with the European the most successful suitors. Queens will mate mul-
workers from the colony. This gradually ensures tiple times over the course of 710 days and during
the adoption of the African bees into the European this time they will mate with an average of 1220
colony. Somewhere during this process, the drones. Queen bees store semen in an organ called
European queen is lost (perhaps killed by the a spermatheca. African colonies produce more
African bees her fate remains uncertain at this drones/colony so drone populations in an area
point) and the African queen is introduced into tend to favor African bees. As such, virgin European
the colony, thus becoming the reigning matri- queens are more likely to mate with African drones
arch. European bees do not display this behavior rather than European ones. Further, flight time and
but often fall victim to it, thus creating an African distances of mating flight from the colony tend to
colony from a preexisting European one. result in European queens encountering African
Other behavioral differences between African drones more often than European drones, thus
and European races exist and are worth discuss- setting the stage for hybridization.
ing briefly. For example, African bees are more All honey bees undergo complete metamor-
flighty than European bees, meaning that when phosis but the time from egg to adult varies by
a colony is disturbed, more of the bees leave the subspecies. The newly-mated queen bee oviposits
nest rather than remain in the hive. African bees in wax cells constructed by worker bees. Fertilized
use more propolis (a derivative of saps and resins eggs result in female offspring, either workers or
collected from various trees/plants) than do queens. If fed a diet rich in royal jelly, the female
European bees. Propolis is used to weather-proof larva will develop into a queen, with the reciprocal
the nest and has various antibiotic properties. true for the development of workers. Drones result
African colonies produce proportionally more from unfertilized eggs and consequently only
drones (male bees) than European bees. Their inherit genetic material from their mother (they
colonies grow faster and tend to be smaller than have no father).
European colonies. Finally, they tend to store Developmental time varies by caste member
proportionately less food (honey) than European (see Table 4) and favor African honey bees because
bees, likely a remnant of being native to an envi- they generally develop faster than European bees.
ronment where food resources are available When bee colonies decide to make a new queen,
throughout the year. newly emerged female larvae are fed royal jelly
constantly. Because Africanized offspring, includ-
ing queens, develop faster than European off-
Life Cycle and Genetic Dominance spring, a queen having an African genotype is
more likely to emerge earlier than a queen with a
Mating biology and developmental time play an European genotype. The first queen to emerge
important role in the success of African bee colo- kills all of her queen sisters that have not yet
nies in replacing European colonies in an area. emerged from their cells. The Africanized virgin
For the most part, mating and developmental proceeds to mate in an area having higher den-
biology are similar for African and European sities of African drones. Over time, this results
64
A African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae)

in the colony becoming more African with the Africanized honey bees have been established.
European phenotype being replaced almost alto- These precautions are not suggested to make peo-
gether. This process is exacerbated further due to ple fearful of honey bees but only to encourage
the dominance of African genetic traits over Euro- caution and respect of honey bees. The precau-
pean ones. tions include remaining alert for honey bees flying
Finally, African bees are more resistant to into or out of an area (suggesting they are nesting
many honey bee pests/pathogens than are Euro- nearby), staying away from a swarm or nest, and
pean bees. Western honey bees face a myriad of having wild colonies removed from places that
pests and diseases, the most severe of which humans frequent. The latter is perhaps the most
include varroa mites (Varroa destructor), tracheal important advice one can heed when dealing with
mites (Acarapis woodi), small hive beetles (Aethina African bees. In the USA, a large percentage of
tumida), and American foulbrood (Paenabacilis African bee attacks occur on people who know a
larvae). These bee pests almost eliminated all wild nest is present but elect not to have it removed (or
colonies of European honey bees in North America. try to do it themselves).
Because African bees are resistant to many of these If an attack occurs, remembering a few simple
pests/diseases, their survivorship in the wild is recommendations will increase ones chances of
favored over that of European bees. minimizing the effects and severity of the attack. If
attacked, a victim should run away from the area
using his shirt to cover his head and especially
Public Risks airways. Running through tall grass or small trees
will help to disrupt the attacking bees. The victim
Due to their heightened defensive behavior, should not stand and swat at the bees. The bees are
African honey bees can be a risk to humans. Chil- defending their nest, and the victim needs to get
dren, the elderly, and handicapped individuals are away from that nest as quickly as possible. It is
at the highest risk of a deadly attack due to their important that the victim get cover in a bee-proof
inability or hampered ability to escape an attack. vehicle or structure if either is available. One
African honey bees are agitated by vibrations like should not jump into the water or hide in bushes.
those caused by power equipment, tractors, lawn The bees can remain defensive and in the area for
mowers, etc. Further, their nesting habits often put some period of time, thus increasing the risk to
them in close proximity to humans. Because of the victim. If stung, the victim should remove the
this, precautions should be taken in an area where stinger quickly by scraping it rather than by pull-
ing it. One should see a doctor immediately if
breathing is affected.
African Honey Bee, Africanized Honey Many African bee attacks can be prevented by
Bee, or Killer Bee, Apis mellifera scutellata limiting the number of nesting sites that are avail-
Lepeletier ( Hymenoptera: Apidae), Table 4 The able to the bees. A homeowner, school worker, etc.
developmental time in days (from egg to adult) of can bee proof his or her property by eliminating
European and African honey bees possible nesting sites. This can be accomplished by
removing any unnecessary debris from an area
European honey African honey
bees bees
and closing off wall, chimney, electrical and
plumbing-related gaps that are >30 mm using a
Queen 16 14
small-mesh hardware cloth or caulking. This will
Worker 21 1920 limit bee access to potential nesting sites. Finally,
Drone 24 24 one should check walls and eaves of structures
regularly, looking for bee activity.
 African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae)
A 65

Managing African Bee Colonies suit, boots, gloves, and a bee veil. Bee veils (protec-
tive headgear) are worn by almost all beekeepers
It is important to remember that African honey worldwide. Traditionally, the veil mesh protecting
bees pollinate crops and produce honey just like the face is colored black to keep down the suns
other races of honey bees. Beekeepers in South glare. African bees (and most honey bees) attack
Africa use African honey bees as the bee of choice dark colors so black-faced veils often get covered
in their operations. So, African bees can be man- with bees. Consequently, beekeepers can use
aged efficiently and safely but the skills required to white-faced veils to keep the bees off of their veils.
manage African bee colonies differ from those Beekeepers managing African colonies often tape
required to manage European bee colonies. their bee suits to their boots and gloves to limit the
In general, the management of African bee possibility of bee access.
colonies has been discouraged in the US while Finally, some beekeepers in areas with African
accepted in Central and South America. This may bees try to requeen African bee colonies with
have to do with the public perception of honey European queens. This is not a common practice
bees, particularly African bees, in the USA and the in sub-Saharan Africa. Most African beekeepers
robust legal system in place in the USA. On the in areas having African bees gladly use the bee in
other hand, beekeepers in Central and South their operations, paying little attention to the bees
America routinely use African bees in their opera- defensiveness.
tions with slight management modifications. In
fact, some South American countries are among
the leading honey producers in the world, due
largely to the presence of African bees in the Conclusion
country.
Beekeepers in South and Central America The economic impact of African bees in an area
utilize a number of management practices in order can be substantial. Keepers of European bees
to keep African bees. First, they keep single bee often notice a decrease in resource availability
colonies on individual hive stands rather than for their bees because of the density of African
using one hive stand for multiple colonies. This bee colonies in an area, and thus the demand on
limits the management activity to one colony at a the available resources is high. Furthermore, cit-
time rather than aggravating other colonies while ies, municipalities, etc., often initiate eradication
working only one. programs, with much futility. Finally, the loss of
Secondly, beekeepers in South and Central animal and human lives is a tragic occurrence,
America use ample amounts of smoke when work- being beyond measurable cost.
ing African bee colonies. It is believed that smoke African bees also may affect the environment
masks the alarm pheromone of the bees, thus less- negatively. Colony densities as high as 300 African
ening the defensive response of the colony. Most bee colonies per square mile have been suggested.
South and Central American beekeepers agree If true, African bees may have a substantial impact
that copious amounts of smoke should be used on the native flora and fauna in an area. While this
when working African bee colonies. It is impor- impact often is not reported and largely is not
tant to smoke the colonies well before any work is understood, it could be significant considering the
done, for once bees from a colony are agitated, potential number of colonies and their need for
smoke may fail to calm them down. resources. Thus, the worlds most infamous honey
Beekeepers managing African bees wear bee is among natures most enigmatic creatures.
appropriate protective gear. A typical beekeeper Apiculture (Beekeeping)
working an African colony would wear a full bee Honey Bee
66
A African Horse Sickness Viruses

References midge involved in the transmission cycle. Most

species of equines can develop viremias sufficiently
Caron DM (2001) Africanized honey bees in the Americas. high to infect midges. Some tick species have been
The A.I. Root Co., Medina, OH, 228 pp shown to be able to become infected and transmit
Hepburn HR, Radloff SE (1998) Honeybees of Africa.
Springer-Verlag, Berlin, 370 pp
the virus in the laboratory, but the importance of
Winston ML (1992) Killer bees: the Africanized honey bee in this transmission route in nature is unknown.
the Americas. Harvard University Press, Cambridge, In endemic areas, African horse sickness
MA, 176 pp viruses circulate primarily between midges and
zebra, and frequently multiple serotypes are pres-
ent. Transmission rates can be very high. For
African Horse Sickness Viruses example, in the Kruger National Park, South
Africa, zebra foals typically are exposed to all nine
cynthia c. lord serotypes by the time they are 1 year old.
University of Florida, Florida Medical Entomol- The first outbreak outside the sub-Saharan
ogy Laboratory, Vero Beach, FL, USA zone began in 1959 in Saudi Arabia and Iran,
spreading to involve Afghanistan, Pakistan, Syria,
African horse sickness is a highly fatal, nonconta- Lebanon, Jordan, Iraq, Turkey, Cyprus and parts
gious disease of equines, particularly horses. The of India before being controlled by vaccination
African horse sickness virus group consists of nine campaigns and the loss of most susceptible horses
serotypes, in the genus Orbivirus, family Reoviridae. by the end of 1961. Another outbreak occurred in
It is closely related to the bluetongue viruses, which North Africa in 1965, crossing into Spain in 1966.
cause disease in cattle and sheep. Infection with any An outbreak of African horse sickness serotype 4
of the serotypes of African horse sickness virus usu- virus began in central Spain in 1987 and ulti-
ally results in severe disease and high mortality in mately encompassed a large part of Spain, along
horses. Donkeys and mules generally exhibit less with parts of Portugal and Morocco. This out-
severe disease and lower mortality, while wild equids break was the first recorded instance of an African
such as zebra generally show no signs of disease or horse sickness virus overwintering outside of
mortality after infection. The serotypes are differen- Africa. African horse sickness cases occurred for
tiated based on the host immune response, and there four subsequent years in Spain, and it was not
is some cross reaction between serotypes. eradicated until 1990. The most likely route of
All nine serotypes are endemic to sub-Saharan introduction was via zebra imported from
Africa, and have caused serious epidemics when Namibia. Control and eradication of the virus
introduced outside this area. African horse sick- was achieved only by extensive vaccination cam-
ness has had a significant impact on the history of paigns and slaughter of infected or exposed
some parts of Africa, as horses could not be used in equines. It is estimated that 2,000 horses died and
exploration and farming. Outbreaks of African over 350,000 were vaccinated during this out-
horse sickness have a significant economic impact, break. In 1989, an outbreak of serotype 9 occurred
resulting from the direct loss of animals, the costs in Saudi Arabia.
of control programs, and trade regulations and Spain was divided into African horse sick-
quarantines restricting movement of equines from ness-free and infected regions, in order to allow
infected areas. movement of horses for the 1992 Olympics held in
The virus is transmitted by biting midges in Barcelona. No vaccination was allowed in the Afri-
the genus Culicoides. Culicoides imicola has been can horse sickness-free region, so that any trans-
implicated in most outbreaks, while in endemic mission activity would be observed. Equine
areas there may be several species of Culicoides movement out of the infected region was prohibited.
 African Horse Sickness Viruses
A 67

A similar strategy is used in South Africa, with an horses, against all serotypes, is practiced in
African horse sickness-free zone in the Western endemic areas. Elsewhere, vaccination generally is
Cape Province, based on historically lowincidence not used routinely or is not allowed. In outbreak
of African horse sickness, and that C. imicola is situations, the virus is first typed to determine the
rare. Surrounding this zone is a surveillance zone serotype involved, then vaccination is targeted
and a protection zone. No vaccination is allowed against that serotype only.
in the free and surveillance zones, and strict move- Most countries restrict importation of equids
ment controls are in place for equines moving from endemic countries. An extended quarantine
from other areas of the country. The zoning cre- period usually is imposed, thus restricting the
ates an area where animals can be held prior to movement of horses for competition. Because it is
exportation. In 1999, there was an outbreak of difficult to differentiate between vaccinated and
African horse sickness in the surveillance zone, infected animals, generally there are restrictions
opening debate about the effectiveness of the on importing vaccinated animals.
movement restrictions and the vector species Antibodies to African horse sickness viruses
involved. Currently, the zoning is still in place and have been found in other animals such as elephants,
there have not been further outbreaks in the camels, and bovines, but there is no apparent ill-
African horse sickness-free zone. ness and their impact on the transmission cycle is
Clinical signs of African horse sickness in not known. Dogs can become infected and die by
horses generally begin with fever. There are three eating meat from the carcass of an infected animal.
forms of African horse sickness disease in horses: Antibodies to African horse sickness have been
pulmonary, cardiac, and febrile. The febrile form, found in wild canids and other carnivores, most
often referred to as horse sickness fever, does not likely also via feeding on infected carcasses.
progress beyond fever and generally resolves. The Humans have been infected only rarely, generally
pulmonary form begins with fever and progresses through laboratory accidents with vaccine strains.
to respiratory difficulty, coughing and nasal dis- African horse sickness has never been found
charge. Death is due to pulmonary edema and in the New World. However, there are species of
cardiac failure. The cardiac form also begins with Culicoides, particularly the C. variipennis complex,
fever, and subsequently edemas develop around present throughout the U.S. Some members of this
the head, neck and chest. Death results from car- complex are competent vectors of African horse
diac insufficiency and progressive pulmonary sickness viruses in the laboratory, and will be com-
edema. Mortality rates can be as high as 95% in petent vectors in the field should an African horse
horses, although donkeys and mules are much less sickness virus be introduced. Vector competence
susceptible and mortality rates are much lower. for the C. variipennis complex varies considerably
Movement of donkeys may be important in the for the closely related bluetongue viruses, but we
spread of these viruses outside the endemic area, lack information on similar variation for African
as they are rarely clinically ill and so infected ani- horse sickness viruses. The implications of this for
mals are not noticed. There is variation in virulence an introduction of any of the African horse sickness
between the nine African horse sickness serotypes, viruses is unknown, but requires further study.
along with differences between breeds of horse and
individual immune responses to the virus.
Vaccines have been developed against these
References
viruses, but due to the immunological differentia-
tion between the serotypes, cross protection is not
Bram RA, George JE, Reichard R, Tabachnick WJ (2002)
complete and full protection requires vaccination Threat of foreign arthropod-borne pathogens to live-
against each serotype. Routine vaccination of stock in the United States. J Med Entomol 39:405416
68
A Africanized Bees

Holbrook FR, Tabachnick WJ, Schmidtmann ET, McKinnon C, with peaks from May to August, i.e., during the
Bobian RJ, Grogan WL (2000) Sympatry in the Culicoides cool, dry season. Egg clusters are located mostly
variipennis complex (Diptera: Ceratopogonidae): a taxo-
nomic reassessment. J Med Entomol 37:6576 on the lower trunks of trees and consist of 24130
House JA (1993) Recommendations for African horse sick- glossy, globular or dimpled spheres, each about
ness vaccines for use in nonendemic areas. Rev lev 1mm in diameter. They hatch 610 days after ovi-
Md Vt Pays Trop 46:7781
Mellor PS, Boorman J (1995) The transmission and geo-
position, depending on the season (Fig. 24).
graphical spread of African horse sickness and blue- Caterpillars of various instars are found any-
tongue viruses. Ann Trop Med Parasitol 89:115 time between early March to the end of November,
Mellor PS, Boorman J, Baylis M (2000) biting midges: their role with periods of greatest abundance from June to
as arbovirus vectors. Annu Rev Entomol 45:307340
September. All larval instars are hairy and last
instars occur in two color phases. One of them is
Africanized Bees milky-green; the other, more common one, a highly
camouflaged, brown to greyish-white mottled bark
Honeybees in the Western Hemisphere that are pattern including up to three, more or less distinct
derived from hybridization of African and dorsal saddles. Caterpillars feed solitarily, and move
European subspecies of Apis mellifera. The degree with great speed and agility when disturbed, includ-
of hybridization is unresolved. ing a hopping and ballooning response during the
Bees first four instars. Early instars skeletonize Khaya
Honeybee leaflets at night and spend the day motionless on or
African Honey Bee underneath leaflets. Older instars are free feeders
and rest on the lower trunk during the day. All
instars shun the foliage of just-expanding shoots.
African Mahogany-Feeding There are five instars in males and six in females,
Caterpillar, Heteronygmia each of them lasting from 56 days.
dissimilis aurivillius (Lepidoptera: Pupae are found from late February to early
Lymantriidae) December, abundantly so from June to September.
They often are cradled in loose leaf shelters tied
hans g. schabel together by sparse strands of silk or in other hid-
University of Wisconsin, Stevens Point, WI, USA ing places, such as under bark scales.
The moths are present from February to
Several genera and species of mahoganies in various mid-November, most abundantly so from May to
parts of the tropics are highly valuable timber spe- September. They rest during the day and are
cies, among them African mahogany (Khaya spp.). attracted to lights at night. Slender male moths are
Relatively few defoliators are known to target this light to dark or reddish brown with substantial plu-
genus, among them caterpillars of several silkmoths, mose antennae, whereas the white to cream-colored
the nymphalid Charaxes and the lymantriid Hetero- females are bigger and more robust with smaller
nygmia. Only the latter, presumably monophagous antennae. Males have wingspans of about 40 mm
on Khaya, appears to have pest potential as indicated and are able fliers, while females with wingspans of
by small-scale outbreaks observed in Morogoro, about 50 mm, are reluctant to take to the air and
Tanzania, in the 1980s. then only as poor fliers. Both sexes have faint to
A succession of four generations per year more pronounced grey line markings and a small
allow Heteronygmia dissimilis to be active most of black dot on each front wing. Before oviposition, the
the year, except for a period of estivation during greatly distended abdomen of the female is greenish.
the hottest season, i.e., from November to February. Male moths reach adulthood after an average of 41
Eggs are found from early March to late October days (September/October), females after about 45
 African Mahogany-Feeding Caterpillar, Heteronygmia dissimilis aurivillius (Lepidoptera: Lymantriidae)
A 69

African Mahogany-Feeding Caterpillar, Heteronygmia Dissimilis aurivillius (Lepidoptera: Lymantriidae),

Figure 24 Egg (top left) (2x), last instar larva (top right) (1x), pupa (bottom left) (1.7x) and (mating) adult
stages (bottom right) (2x) of Heteronygmia dissimilis, respectively. Both sexes are represented in the
bottom figures, the larger females being above in each picture. (Photo: H. Schabel et al. 1988; reprinted
with permission from ICIPE, the International Centre of Insect Physiology and Ecology.)

days of development. On the average, each female Numerous arthropod predators of the cater-
produces about 200 eggs, laid in several batches. pillars and pupae are believed to be generalists with
While no field control of Heteronygmia has little impact. On the other hand, four hymenopter-
been undertaken to date, a laboratory study docu- ous and two dipterous parasites affecting various
mented full protection of Khaya leaves from defo- stages of H. dissimilis seem more specific. Season-
liation by H. dissimilis, following application of 1% ally, egg parasites in particular had significant
crude, aqueous seed extracts of the neem tree impacts on this insect and in conjunction with the
(Azadirachta indica). fungus Paecilomyces farinosus, which severely
70
A African Maiden Moths (Lepidoptera: Thyretidae)

ecimated pupae during the rainy season, were

d References
responsible for serious setbacks in the annual
buildup of H. dissimilis. As a result, natural controls Janse AJT (1945) On the South African species of Metarctia,
seem to be quite effective with this insect. with the description of a new species. J Entomol Soc
South Africa 8:9198
Kiriakoff SG (1949) Over de phylogenie van de Thyretidae fam.
nov. (Lepidoptera). Natuurwetenschappen Tijdschrift
References 30:310
Kiriakoff SG (1953) Les Thyretidae du Muse Royal du
Congo Belge (Lepidoptera Notodontidae). Annales du
Ballard E (1914) Two pests of mahogany in Nyasaland. Bull
Muse Royal du Congo Belge, Sciences Zoologiques
Entomol Res 5:6162
(8) 26:191
Rwamputa AK, Schabel HG (1989) Effects of crude aqueous
Kiriakoff SG (1957) Notes sur les Thyretidae (Lepidoptera:
neem extracts on defoliation of Khaya nyasica by Het-
Notodontidae). Bulletin et Annales de la Socit Royale
eronygmia dissimilis (Lepidoptera: Lymantriidae) in
Entomologique de Belgique 93:121160
East Africa. In: Alfaro RI, Glover SG (eds), Proceedings,
Kiriakoff SG (1960) Lepidoptera. Fam. Thyretidae. In: Genera
IUFRO Working Group on Insects Affecting Afforestation,
Insectorum. Brussels, 214:166
XVIII International Congress of Entomology. Vancouver,
British Columbia, Canada, pp 245250
Schabel HG, Schabel A, Msanga HP (1988) Bioecological
aspects of the mahogany defoliator Heteronygmia dis-
similis in Morogoro, Tanzania. Insect Sci Appl
9:179184
African Pine-Feeding
Grasshoppers, Plagiotriptus
pinivorus (Descamps) and
P.Hippiscus (Gerst.) (Orthoptera:
African Maiden Moths Eumastacidae)
(Lepidoptera: Thyretidae)
hans g. schabel
john b. heppner University of Wisconsin, Stevens Point, WI, USA
Florida State Collection of Arthropods, Gainesville,
FL, USA These grasshoppers are excellent examples of
indigenous insects that developed a preference for
African maiden moths, family Thyretidae, include an exotic plantation-grown crop, in this case pines.
212 species, all African. The classification remains Plagiotriptus pinivorus attained some prominence
controversial and various specialists also place the after causing persistently severe defoliation of
group within Arctiidae. The family is in the super- exotic pines, especially Pinus patula, in Malawi in
family Noctuoidea, in the section Cossina, subsec- the 1960s, resulting in significant tree mortality.
tion Bombycina, of the division Ditrysia. Adults A smaller scale defoliation of P. patula was
medium-size (2357 mm wingspan). Haustellum observed at Morogoro in Tanzania in the mid-
usually reduced or vestigial; antennae pectinate; 1980s, which was attributable to another, very
wings very elongated, with reduced hindwings closely related species, Plagiotriptus hippiscus.
(some with greatly reduced hindwings). Macula- Both of these grasshoppers are highly polypha-
tion typically dark with white or hyaline patches, gous, including herbaceous hosts, shrubs and both
or more colorful. Adults perhaps mostly diurnal; angiosperm and gymnosperm trees. The prime
often wasp mimics. Larvae are thought to be leaf requirement for P. pinivorus seems to be access to
feeders, but most species remain unknown bio- evergreen or semi-evergreen vegetation in areas of
logically. Host plant records include Thymelae- moderate to heavy rainfall, i.e., mostly at altitudes
aceae and Ulmaceae, for the few species known between 1,5252,135 m, but occasionally as low
biologically. as 490 m.
 African Pine-Feeding Grasshoppers, Plagiotriptus pinivorus (Descamps) and P.Hippiscus (Gerst.) (Orthoptera: Eumastacidae
A 71

Plagiotriptus pinivorus in Malawi exhibits of emergence two weeks in advance. Another

three generations every 2 years, and the complete smaller peak in emergence in August, however,
life cycle takes about 1 year. Nymphs and adults cannot be explained by rainfall. The first instar
have been observed on pines throughout the year, nymph is ephemeral (about 12 h), and will molt
except from December to late January. Copulation immediately when reaching the soil surface, before
occurs anytime, but peaks from October to January feeding on ground vegetation for the next 23
and May to June. During copulation, the small weeks. Advanced instars complete their life cycle
male assumes a characteristic dorso-lateral posi- on trees, each instar lasting about one and a half to
tion by clinging to one of the hind femurs of the over two months. Young instars are wasteful feed-
female. Both males and females are promiscuous. ers. There are generally six instars for males and
About 720 days after the last mating, females seek seven for females. Despite the extra instar, females
bare soil and dig a shallow pit to lay a batch of up develop more rapidly and reach adulthood at
to six eggs. They then resume voracious feeding in about the same time as do males.
the trees, before laying other batches of eggs at Adult males (Fig. 25) are about 1.52 cm
1735 day intervals. long, moderately robust grasshoppers. Their
Eggs incubate from 49248 days, with an abdomen, shield-like pronotum and greatly
average of 115 days. The winter population hatches enlarged hind femora are strongly compressed. A
from April to May, maturing in November, while minute set of non-functional wings, not found
the summer population hatches from December on nymphs, is hidden under the pronotum. The
to January and matures from May to July. Within thread-like antennae are about one third the
the same batch, an average of 34 days and a maxi- length of the head. The abdomen is strongly
mum of 88 days may elapse between first and reflexed over the back in the male. The insect is
lasthatch. largely leaf-green, but sports inconspicuous,
Nymphal peak emergence and rainfall are small areas of blue, pink, red and white on various
strongly correlated in February, allowing prediction parts of the legs, wings, antennae and the pronotal

African Pine-Feeding Grasshoppers, Plagiotriptus pinivorus (Descamps) and P. hippiscus (Gest.)

(Orhthoptera: Eumastacidae), Figure 25 Plagiotriptus hippiscus female (above) and male (below) with
size comparison (shaded) (drawing, Paul Schroud).
72
A African Primitive Ghost Moths (Lepidoptera: Prototheoridae)

ridge. Eyes are golden yellow. Females are about present; labial palpi long and porrect, 3-segmented;
twice the size of males, more robust and gener- maxillary palpi short and 3-segmented; antennae
ally less compressed. They are uniformly leaf- short. Maculation is brown or gray, with various
green, except for the golden yellow eyes and darker spots. Biologies and larvae remain
valves of the ovipositor. Their wings are also min- unknown.
ute and hidden under the pronotal shield.
Numerous invertebrate and vertebrate preda-
tors, including skinks, birds and blue monkeys, as References
well as parasites were documented, but ultimately
they were deemed insufficient by themselves to Davis DR (1996) A revision of the southern African family
reduce populations of the grasshopper to non- Prototheoridae (Lepidoptera: Hepialoidea). Entomol
Scand 27:393439
damaging levels. As a result, sticky bands and Davis DR (2001) A new species of Prototheora from Malawi,
chemical controls were relied on for monitoring with additional notes on the distribution and morphol-
and control purposes, respectively. In the 1960s in ogy of the genus (Lepidoptera: Prototheoridae). Proc
Malawi, gamma-BHC at 0.5% proved the most Entomol Soc Wash 103:452456
Davis DR (2003) Prototheoridae. In: Lepidopterorum Catalogus,
effective insecticide for ground and aerial applica- (n.s.). Fasc. 11. Assoc Trop Lepid Gainesville, 8 pp
tions at ultra-low volume formulations. Spraying Janse AJT (1942) Prototheoridae. In: Janse AJT (ed) The
of road banks was particularly recommended, as moths of South Africa, Pretoria, 4(1): 6574
insects clustered there for oviposition in the bare
ground.
African Red Tick, Rhipicephalus
evertsi, (Acarina: Ixodidae)
References
This important tick, known as African red tick,
Lee RF (1972) A preliminary account of the biology and ecol- affects ungulates in Africa.
ogy of Plagiotriptus spp. (Orthoptera: Eumastacidae). Ticks
Malawi Forest Research Institute Research Record 48,
Forestry Research Institute of Malawi, Zomba, 100 pp
Schabel HG, Hilje L, Nair KSS (1999) Economic entomology
in tropical forest plantations: an update. J Trop For Sci
Xth Anniversary Issue: 303315. African Skipper Moths
(Lepidoptera: Apoprogonidae)

African Primitive Ghost Moths john b. heppner

(Lepidoptera: Prototheoridae) Florida State Collection of Arthropods, Gainesville,
FL, USA
john b. heppner
Florida State Collection of Arthropods, African skipper moths, family Apoprogonidae,
Gainesville, FL, USA includes only a single species from South Africa.
The family is in the superfamily Uranioidea, in
African primitive ghost moths, family Prototheo- the section Cossina, subsection Bombycina, of
ridae, comprise 12 species of small moths from the division Ditrysia. Adults medium size (4656
South Africa. The family is in the superfamily mm wingspan), with head rough scaled and eyes
Hepialoidea, in the infraorder Exoporia. Adults large; haustellum naked; labial palpi porrect;
small (18mm wingspan), with head rough-scaled; maxillary palpi minute, 1-segmented; antennae
haustellum reduced and vestigial mandibles clubbed (hooked at tip). Wings triangular and
 African Swine Fever
A 73

African Slug Caterpillar Moths

(Lepidoptera: Chrysopolomidae)

john b. heppner
Florida State Collection of Arthropods, Gainesville,
FL, USA

African slug caterpillar moths, family Chrysopo-

lomidae, are a small African family of about 30
known species. Two subfamilies are known:
Ectropinae and Chrysopolominae. The family is
in the superfamily Cossoidea (series Limacodi-
African Skipper Moths (Lepidoptera: formes) in the section Cossina, subsection Cos-
Apoprogonidae), Figure 26 Example of African sina, of the division Ditrysia. Adults medium
skipper moths (Apoprogonidae), Apoprogones size (2452 mm wingspan), with head scaling
hesperidis Hampson from South Africa. smooth; haustellum and maxillary palpi absent;
antennae short and bipectinate in males. Body
short; body robust. Maculation dark gray with robust. Wings rounded and broad (some with
some pale markings, plus pale discal spot on irregular distal margins). Maculation mostly
fore- and hindwings. Adults presumed diurnal, pale brown, often with subapical wing line and
but nothing is known of the biology or larvae light discal spot; hindwing with forewing line
(Fig. 26). and coloration continued (Fig. 27). Adults noc-
turnal as far as is known. Larvae leaf-feeding
and slug-like, with small spines; often colorful.
References Host plants include Celastraceae. No economic
species are known.
Janse AJT (1932) Family Sematuridae. In: The moths of South
Africa, 1:8789. Pretoria [Apoprogones]
Seitz A (1926) Subfamilie: Apoprogeninae [sic]. In: Seitz A
(ed) Die Gross-Schmetterlinge der Erde. Teil 14. Die References
afrikanischen Spinner und Schwrmer, pl. 1. A. Kernen,
Stuttgart, pp 1617
Aurivillius C (1911) Chrysopolomidae. In Lepidopterorum
catalogus, 1:14. W. Junk, Berlin.
Hering EM (1928) Familie: Chrysopolomidae. In: Seitz A.
African Sleeping Sickness (ed) Die Gross-Schmetterlinge der Erde. Teil 14. Die
afrikanischen Spinner und Schwrmer, pl. 76. A. Kernen,
Stuttgart, pp. 477479
A disease of humans caused by protozoans in the Herring EM (1937) Revision der Chrysopolomidae (Lep.).
genus Trypanosoma. It is also known as human Ann Transvaal Mus 17:233257, pl. 9
sleeping sickness or human trypanosomiasis. The
same disease, when infecting other vertebrate ani-
mals, is called nagana. It is transmitted by tsetse
flies in Africa. African Swine Fever
Sleeping Sickness or African Trypanosomiasis
Trypanosomes A viral disease of hogs, this tick-transmitted
Tsetse Flies disease is found on several continents.
Nagana Ticks
74
A Agaonidae (Hymenoptera)

opening. The females of some species actively gather

and carry pollen in thoracic pockets or specialized
leg structures. The cultivated fig, Ficus carica, has
many varieties that no longer rely on pollination to
produce edible ripe syconia. However, a few varieties
still require the pollination service provided by the
agaonid partner, Blastophaga psenes.
Wasps, Ants, Bees and Sawflies
Fig Wasps

African Slug Caterpillar Moths (Lepidoptera: References

Chrysopolomidae), Figure 27 Example of African
slug caterpillar moths (Chrysopolomidae), Bronstein JL (1988) Mutualism, antagonism, and the fig-pol-
Chrysopoloma similis Aurivillius from South Africa. linator interaction. Ecology 69:12981302
Galil J, Eisikowitch D (1968) On the pollination ecology of
Ficus sycomorus in East Africa. Ecology 49:259269
Galil J, Zeroni M, Bar Shalom D (Bogoslavski) (1973) Carbon
Agaonidae (Hymenoptera) dioxide and ethylene effects in the co-ordination between
the pollinator Blastophaga quadriceps and the syconium
in Ficus religiosa. New Phytol 72:11131127
hannah nadel Machado CA, Jousselin E, Kjellberg F, Compton SG, Herre EA
USDA-ARSSan Joaquin Valley Science Center, (2001) Phylogenetic relationships, historical biogeography
Parlier, CA, USA and character evolution of fig-pollinating wasps. Proc R
Soc London B 268:685694
Ramirez BW (1969) Fig wasps: mechanisms of pollen trans-
fer. Science 163:580581
A tropical family of about 750 species of miniscule Weiblen GD (2002) How to be a fig wasp. Annu Rev Entomol
wasps (order Hymenoptera) that are mutualistically 47:299330
associated with fig plants (Ficus spp.). The associa- Wiebes JT (1966). Co-evolution of figs and their insect polli-
nators. Annu Rev Ecol Syst 10:112
tions are usually between a unique pair of fig and
wasp species and are crucial for the reproduction of
both. The winged female wasp enters a young floral
receptacle, the flask-like syconium, and lays single Agathiphagidae
eggs in many of the tiny female flowers lining its
inner surface. Carrying pollen from her natal fig, she A family of moths (order Lepidoptera). They com-
deposits it onto the stigmas during oviposition, monly are known as Kauri moths.
ensuring seed production for the fig and food for Kauri Moths
her own offspring. The syconium will generally not Butterflies and Moths
ripen without pollination. The female is trapped
inside the syconium and dies there. After the larvae
develop and pupate in seed-galls, the wingless adult
males emerge first and chew holes into galls to mate Agassiz, Jean Louis Rodolphe
with the quiescent females inside, and then coopera-
tively chew an opening through the syconial wall. Louis Agassiz was born at Mtier-en-Vuly, Swit-
The changed atmosphere inside the syconium wakes zerland, on May 28, 1807. He displayed an early
the females, which chew out of their galls, actively interest in natural history. In 1824 he entered
or passively pick up pollen, and leave through the Universitt Zrich for medical training, then
 Agnathous
A 75

moved to Universitt Heidelberg in Germany. In Nordenskild E (1935) The history of biology: a survey. Tudor,
New York, 629 pp.
Heidelberg his interest in natural history increased.
His next move was to Universitt Mnchen and,
while there in 1829 and still only 21 years old, he
published a work on Brazilian fishes, using the Age Polythism
collected materials of von Martius and von Spix.
His next zoological endeavor was to begin research This refers to the division of labor within a colony
on fossil fishes. In 1831, he moved to Paris still of social insects wherein the responsibilities of the
with the ambition of completing his medical individuals change as they mature.
training. However, he spent part of each day
studying fossil fishes and he came under the influ-
ence of Cuvier and adopted the latters views of Aggregation
creation. Thus, according to Agassiz, each species
was the result of separate creation, not of evolu- A group of individuals consisting of more than just
tion. In 18321846 he was a professor at Univer- family members; a coming together of individuals
sit de Neuchtel, Switzerland. In 1836, Louis to form a group. (contrast with colony)
began to study glaciers and their effects, on which Cycloalexy
he published works in 1840, 1846 and 1847. In Allelochemicals
Switzerland, he also published a large catalog
Nomenclator zoologici of the names of animals,
of which some fascicles were on insects. In 1846
Aggregation Pheromone
he moved to the USA, was welcomed as a famous
scientist, and in 1848 was appointed professor of
A pheromone that causes insects to aggregate. This
zoology and geology at Harvard University. At
type of pheromone is used by insects for mating,
Harvard, he clashed with Asa Gray, professor of
feeding, or oviposition.
botany, about evolution, because Gray supported
Pheromones
Darwins theory. However, it was Louis efforts and
influence that led to the foundation of the Museum
of Comparative Zoology at Harvard University,
an institution that became very influential in Aggregative Response
research on insect systematics. He also was a co-
founder of the U.S. National Science Foundation. The response of predators in which they increase
He died in Cambridge, Massachusetts, on December their time spent in areas with more prey, leading to
14, 1873. His son Alexander and two daughters higher predator density, and fewer prey.
of his first marriage accompanied him to the Learning in Insects
USA (his first wife having died in Switzerland). Predation: The Role of Generalist Predators in
Alexander Agassiz (18351910) likewise became Biodiversity and Biological Control
a zoologist. Louis Agassiz remarried in 1850 in
the USA.
Agnathous

References This term is used to refer to insects that lack man-

dibles, which essentially means that they lack
Anon (1998) Jean Louis Rodolphe Agassiz. Encyclopedia of mouth structures.
world biography, 2nd ed. Gale, Detroit, MI Mouthparts of Hexapods
76
A Aggressive Mimicry

Aggressive Mimicry Agricultural Crop Pests in

Southeast Asia Including
This is a type of mimicry in which a predator mim- Southern China
ics their prey, allowing ready capture and con-
sumption of the victim. emmett r. easton
Mimicry University of Hawaii at Manoa, Honolulu, HI,
Myrmecomorphy USA
Myrmecophiles
Southeast Asia is often called the Oriental faunal
region and includes the provinces of southern
Agonoxenidae China south of the Yangtse river (Anhui, Fujian,
Guangdong, Guangxi, Guizhou, Hainan, Hubei,
A family of moths (order Lepidoptera). They com- Hunan, Jiangshu, Jiangxi, Sichuan, Yunnan and
monly are known as palm moths. Zhejiang) as well as the island of Taiwan, islands
Palm Moths and peninsular area of Hong Kong, Macao and
Butterflies and Moths those countries to the south including Vietnam,
Malaysia, Singapore, Myanmar (Burma), Cambodia
and Laos, as well as portions of Pakistan and India.
The northern provinces of India share similar fau-
Agricolous nal elements as southern China as both are at a
similar latitude. The insect fauna of northern
This refers to species that dwell in agricultural China is more Palearctic in nature and many of
habitats. the northern species will differ from those in the
southern provinces or elsewhere in Southeast Asia.

Agricultural Chemicals
Insects of Rice
Pesticides, adjuvants, and other chemicals, other
than fertilizers, that are used to enhance crop What are believed to be key pests, or those of
production. major importance as opposed to minor can vary
Insecticides from country to country. In Vietnam and south-
Acaricides or Miticides ern China, the rice stemborer complex of lepidop-
terous insects includes the yellow or small rice
borer, Scirpophaga incertulas (Wlk), the striped
Agricultural Consultant rice-stalk borer, Chilo suppressalis (Wlk), the dark-
headed rice borer, C. polychrysus (Meyr) (all
Someone trained in the agricultural and manage- Pyralidae) and the noctuid pink borer, Sesamia
ment sciences who provides plant and animal inferens (Wlk). Although they are considered
production and protection services for a fee. Inde- minor pests in some regions, because the rice
pendent crop consultants sell the advising service plants are able to tolerate some damage and can
only, deriving no income from sale of products, compensate for light infestations, these insects
whereas other crop consultants usually derive some have been ranked as major pests in the countries
income from product sales such as pesticides or of Malaysia and Thailand. The yellow or small rice
fertilizer. borer, Sc. incertulas, has a wide distribution in
Careers in Entomology Southeast Asia and is found in India, Pakistan,
 Agricultural Crop Pests in Southeast Asia Including Southern China
A 77

Sri Lanka, Bangladesh, Myanmar (Burma), Viet- Cicadellidae) and Nilaparvata lugens (Stl) and the
nam, Singapore, Taiwan and Hong Kong. brown plant-hopper (Hemiptera: Delphacidae).
The common names of these insects generally These leafhoppers are important in Thailand and
refer to the color of the larval stage such as the pink Malaysia as well as in India and Pakistan, while the
borer, S. inferens, with pinkish-colored larvae, or planthopper is more widely distributed and is
the yellow larvae of the small rice borer. The head found in southern China, India, Taiwan, Japan and
capsule in larvae of C. suppressalis is brown in color some of the Pacific Islands. The planthopper is
while larvae of Sc. incertulas are yellow with brown unusual in that it is able to migrate between land
heads and the pink borer caterpillar, Sc. inferens, is masses and migrates from East China to Japan
pink in color and larger when mature than the annually. This insect also has migrated to Macao
other species. The larvae tunnel as caterpillars (where rice is no longer grown due to urbaniza-
intothe stems of the rice plants. There they feed on tion) from mainland China.
the plant tissues and destroy the growing points of Nephotettix virescens is an important vector
the plant causing wilting of new shoots, eventually of two viral diseases in Malaysia. The first disease
producing a condition known as dead heart. In is similar to yellow dwarf disease and the second is
mature plants, empty panicles appear white in called Tungro disease. Both cause a stunting of
color, and the condition is known as white-head. plant growth, the first disease a general yellowing
Masses of eggs are generally laid on the leaves in and profusion of tillers, while the second causes a
the case of the female dark-headed borer or striped reddening of the leaves. Both diseases decrease
rice borer. Pupation generally occurs in the stem crop yield.
with these species. The female pyralid moths in the The eggs of the rice leafhoppers are laid in
genus Scirpophaga have a scale tuft at the tip of rows within leaf-sheaths. The five nymphal stages
their abdomens, while female moths in the genus are completed in l7 days in Malaysia. Leafhoppers
Chilo have no scale tuft at the end of the abdomen. generally feed on the upper parts of the plant, while
The female Sc. incertulas has a yellow forewing, the planthopper, Nilaparvata, feeds at the base of
which is whitish in Sc. nivella. the plants near the water line. The brown planthop-
The eggs of stemborers are often attacked by per is sometimes considered the most serious pest
the parasitoid wasps Trichogramma sp. (Tricho- of rice in Asia. They cause a scorching of the
grammatidae) and Telenomus rowani (Scelioni- plants, or a condition known locally as hopper-
dae). In Malaysia, granular insecticides have burn, when the number of nymphs and adults per
been used to control rice stem borers when the clump of rice exceeds 900 or more. The eggs are
incidence in stems (tillers) exceeds l0%, but generally laid in plant tissue. The young resemble
this practice is not recommended in southern the parents except for their smaller size and absence
China or in northern Vietnam where the plants of wings. Five nymphal stages generally require
are able to tolerate some damage and compensate two weeks to develop. Predators can include the
for injury. staphylinid beetle Paederus fuscipes and the coc-
cinellid beetle Harmonia octomaculata.
In Thailand and Malaysia, another important
pest of rice is the rice gall midge, Orseolia oryzae
Rice Leafhopper and Planthopper (W.-M.) (Diptera: Cecidomyiidae), which is also
Complex found in Pakistan, India, Bangladesh, Sri Lanka
and parts of Indonesia as well as in southern
The rice leafhopper and planthopper complex China, where it is considered of minor impor-
includes Nephotettix virescens (Dist) and N. nigropictus tance. The larvae of the fly feed between the leaf
(Stl), the green rice leafhoppers (Hemiptera: sheaths and, when reaching the apical buds, can
78
A Agricultural Crop Pests in Southeast Asia Including Southern China

lacerate tissue and can cause the formation of a Sugar Cane Insects
gall known locally as a silver or onion shoot. The
adults are delicate looking midges, long and brown The lepidopterous sugar cane borer complex in
in color with long legs. Upon hatching, the pale, Thailand includes several pyralids including the
1mm long larva grows to 3 mm and becomes red- yellow top or early shoot borer, Chilo infuscatellus
dish in color. The pupa, when formed, is pinkish (Snellen), the sugar cane stem borer, Chilo sac-
and turns red with age. Grassy vegetation near the chariphagus (Bojer), the white top borer, Scirpoph-
rice fields is often associated with the presence of aga excerptalis (Walker) and the noctuid sugar
the midge. cane stalk borer, Sesamia inferens (Wlk).
The rice leaf folder, Cnaphalocrocis medinalis The larvae of these insects bore into the
(Gn), (Lepidoptera: Pyralidae), is considered one shoots of sugarcane. As the common name sug-
of the more important pests of rice in southern gests, the larvae of the yellow top or early shoot
China as well as in Malaysia and Thailand. It is also borer tunnel into the growing shoots of the plant,
found in India, Pakistan, Sri Lanka and Bangladesh. while the larvae of C. sacchariphagus bore into
The larvae fold the leaf while feeding and trans- the stems. The noctuid moth larvae of purple
parent patches form so that the rice plant appears stalk borer, Sesamia inferens, previously discussed
ragged. The adult moths lay eggs on young, 4 to as a pest of rice, also affects sugar cane, but sugar
6-week-old plants or in nursery stock in Malaysia. cane is not preferred for oviposition as are rice
Early instar caterpillars feed by scraping the epi- and grasses. The larvae are colored purple to pink
dermis from rice leaves, while later instar caterpil- dorsally and white ventrally and have a reddish-
lars fold them. The opposite edges of the leaf, or orange head capsule. The adult moth is fawn-
one edge of the leaf, is attached to the midrib by colored with dark brown streaks on its forewings
silken threads produced by the larvae. Pupation and whitish hindwings.
occurs inside a silken cocoon within the folded In Malaysia, the white sugar cane aphid, Cera-
leaf. Parasitoid wasps, such as Apanteles opacus tovacuna lanigera Zehntner, a mealybug-like insect
(Braconidae) or Temelucha philippinensis (Ichneu- (Hemiptera), causes injury. The non-winged
monidae), often keep populations in check in females and nymphs are covered by a waxy layer,
Malaysia. while the winged adults are bluish-green in color
The lepidopterous armyworm and cutworm and are not covered with a layer of wax.
complex, including the rice armyworm, Mythimna
loreyi (Duponchel), and the rice ear-cutting cater-
pillar or paddy armyworm, Mythimna separata Fruit Tree Insects:
(Wlk), are important pests in Thailand and southern Mango-Citrus-Banana-Litchi
China. The paddy armyworm affects rice in
Pakistan, Sri Lanka, India and Bangladesh. The One of the most important fruit tree insects is con-
larvae feed on leaves and stems and can defoliate sidered to be the Oriental fruit fly, Batrocera
the plants. dorsalis Hendel (Tephritidae). It is found in Hawaii
The rice skipper, Parnara guttata (Bremer & as well as in other Pacific islands and the southeast
Grey) (Lepidoptera: Hesperiidae), was formerly Asian countries of Thailand and Malaysia where it
considered a major pest in southern China, but is a serious mango pest. In southern China, where
recent mass production and release of parasitic there are fewer mangoes grown, it is considered a
wasps has probably lowered its status to a minor minor pest. In addition to mangoes, the guava and
pest. The larvae roll the apical portion of the leaves, carambola are affected in Malaysia. The larvae or fly
web the sides and cut off the apex, forming long, maggots feeding inside the skin of the fruit cause it
conspicuous tubes. to decay. Female flies puncture the skin of the fruit
 Agricultural Crop Pests in Southeast Asia Including Southern China
A 79

with their ovipositors, laying several eggs inside. i ncreasingly important, particularly in the Pacific
The larvae can hatch in one day and develop through island area. The first instar in these Papilionid but-
three instars in about a week. When mature, they terflies are colored differently than older larvae,
are able to leave the fruit by flipping themselves in which may be an adaptation that protects them
the air and dispersing to enter the ground to pupate. from predators such as birds or lizards. The early
Fruits can be protected from these flies by bagging stage larva resembles a bird or lizard dropping as it
them using paper bags. The use of traps treated with is dark brown in color with white markings that
methyl eugenol as an attractant has met with some may appear to be unappetizing to the predator.
success, but as only the males are attracted, it is not When the caterpillar is older, its color changes to
totally effective as a control. green with grey and white markings. Hand picking
In Malaysia, a longhorn beetle known as the the larvae is probably an adequate control in young
mango shoot borer, Rhytidodera stimulans (White), plants.
tunnels into the young growing shoots of the tree. The orange spiny whitefly, Aleurocanthus
Eventually it kills the outer branches, which often spinifera (Quaintance) (Hemiptera: Aleyrodidae),
break off during subsequent wind storms. In is an important insect in southern China as well
southern China, the citrus long-horn beetle, Ano- as India, Sri Lanka, Bangladesh, Malaysia and
plophora chinensis (Forst.) (Cerambycidae), is Thailand. The adults are l mm in length and lay
considered one of the most important pests of cit- eggs on the undersides of leaves. There are three
rus trees. The larvae of these beetles tunnel under nymphal stages and the third-stage nymph appears
the bark of young trees and sometimes into the blackish in color with waxy secretions on the outer
heartwood, which can cause the death of the edge of the body so it looks superficially like an
plants. The adult beetles have striking black and insect pupa. Both the nymphs and the adults
white body coloration. Parasitoid wasps have dif- remove plant nutrients when feeding, and the
ficulty reaching the larvae that bore into young honeydew produced by the nymphs encourages a
healthy trees. sooty moldto grow on the upper surfaces of the
Butterflies (Lepidoptera) are not considered leaves and the fruits. Heavy infestations of this
to be serious pests of agricultural crops in the insect cause fruit production to fall off. A parasitic
northern hemisphere with the exception of the wasp, Eretmocerus serius (Aphelinidae), has been
small white, Pieris rapae. However, in the semi effective in regulating the orange spiny whitefly in
and tropical regions of the world, cold climatic Malaysia.
conditions are not as severe and the insects often Aphids, such as the black citrus aphid, Tox-
do not have to enter diapause (hibernation), so optera aurantii (Bayer de Fonscolombe), and the
there can be continuous generations in some brown citrus aphid, Toxoptera citricida (Kirkaldy),
regions almost throughout the year. Papilionid are important in southern China and also range
butterflies, as well as several species of skippers into India, Sri Lanka and Bangladesh.
(Hesperiidae), cause injury to plants because they Fruit-piercing moths, such as Othreis fullo-
are able to oviposit in both the spring and the fall. nia (Cl.) (Noctuidae), pierce the ripening fruits
In Southeast Asia, the lemon or lime butterfly, of citrus, mango, papaya and guava or banana in
Papilio demoleus (L.), and another species known order to obtain sap. A short, stout proboscis with
by the common names of the common Mormon a barbed tip enables the moth to puncture the
swallowtail or the white-banded swallowtail, skin of the fruit and can permit the entry of plant
Papilio polytes L., lay their eggs on the undersides pathogens such as viruses or secondary rots that
of leaves of citrus plants and are considered impor- can cause premature fruit drop. Fruit-piercing
tant in southern China as pests of citrus. Another moths are considered of major importance
species, Papilio xuthus L., is also becoming today in southern China. Management of their
80
A Agricultural Crop Pests in Southeast Asia Including Southern China

populations is difficult as the immature of O. ful- Vegetable Insects

lonia do not feed on citrus trees. Instead, the cat-
erpillars feed on the foliage of the Erythrina The diamondback moth, Plutella xylostella (L.)
species of shade trees. On the Pacific island of (Lepidoptera: Plutellidae), is currently considered
Guam, the eggs can be laid on the foliage all year among the top 25 most important arthropod pests
round and the insects are considered to be major in southern China. It was the first agricultural pest
pests as they feed on ripe banana, mango, papaya, in Malaysia to be reported resistant to pesticides,
pomegranate and guava as well as tough-skinned and it is also an important pest in Thailand as well
citrus fruits. as in India. Its distribution has been considered cos-
On banana plants, there are two species of mopolitan. Cruciferous plants, such as the cabbages,
leaf rollers or banana skippers in Southeast Asia, are affected. The caterpillars penetrate the epider-
one of which is Erionota thrax (Hesperiidae), which mis of leaves, mining the tissue and making win-
rolls the banana leaves in Malaysia, Thailand and dows or holes in it. The adult is recognized by the
in southern China. The caterpillars cut and roll pale triangular or diamond-shaped marks seen on
strips of banana leaf, then hide in the roll that is the midline of the back when the wings are closed.
held together by silken threads. They emerge at The caterpillar is pale green in color, and it wrig-
night to feed and are often covered with a white gles violently when disturbed, sometimes falling off
powdery secretion. the edge of the leaf. A microbial insecticide, Bacillus
thuringiensis, is effective in the control of the dia-
mondback moth, but farmers in some areas of Malay-
Litchi and Longan Fruit Insects sia have not accepted it because this method takes
longer to kill the caterpillars than other insecticides.
The litchie stink bug, Tessaratoma papillosa The green stink bug, Nezara viridula (L.)
(Drury) (Hemiptera: Tessaratomidae), has been (Hemiptera: Pentatomidae), is a cosmopolitan
considered the most important pest of litchi insect in Southeast Asia that damages developing
(Litchi chinensis) and longan (Euphoria longan) vegetables, such as potato, sweet potato, tomato
fruit trees in the Guangdong region of southern and cotton, by their feeding punctures. Three color
China, including Hong Kong and Macao as well varieties or subspecies of this insect are recognized
as Vietnam and Thailand. The adults are mostly in southern China. An all-green form, known as
brown dorsally and whitish underneath. Imma- N. viridula smaragdula, is the most common,
ture bugs, more brightly colored than the adults, accounting for 7580% of vegetable bugs observed
have red markings dorsally often with a white in Macao in l996. A second form with yellow on
waxy secretion underneath. Plant sap is taken the head and pronotum, N. viridula torquata,
from the stems of fruit trees. The saliva of the bug makes up about 10% of the stink bug population,
can stain the clothing of fruit tree workers. Also, while the least common form is mostly all yellow
the fluid is extremely irritable if it gets in the eyes. with green spotting on the hemelytra and abdo-
An effective biological control of the litchie stink men, and is called N. viridula aurantiaca (1.0%).
bug has been developed in southern China by the The small white butterfly, Pieris rapae (L.) (Lep-
Guangdong Entomological Institute in which the idoptera: Pieridae), along with two other species, is
egg parasitic wasp, Anastatus japonicus (Eupelmi- still considered important in southern China and
dae), has been mass-reared and released to achieve Southeast Asia. The small cabbage butterfly, Pieris
control in the Fujian, Guangdong and Guangzi canidia (Sparrman), also damages nasturtium. In
provinces. Biological control of the litchie stink both species, larvae feed singly in the cabbage heart,
bug has also been reported from the northern make holes in the leaves and cause frass accumulation.
highlands of Thailand. The insects are also found in India, Taiwan and the
 Agroecology
A 81

Philippines, and breeding can be continuous with Agroecology is the application of ecological prin-
up to eight generations annually, which is not the ciples to agricultural production systems and the
case in northerly regions, where overwintering resources needed to sustain them. A convenient
occurs in the pupal stage. unit of study is the agroecosystem, often a single
The Asian corn borer, Ostrinia furnacalis agricultural field. A major difference between an
(Guenee) (Lepidoptera: Pyralidae, Pyraustinae), is agroecosystem and a natural ecosystem is in the
more important in the northern countries of level of human intervention and management
Southeast Asia including southern China where involved. Like natural ecosystems, agroecosystems
corn is grown. The Guangdong Entomological consist of living (biological) and nonliving (chem-
Institute rates it as a highly important pest there. ical, physical) portions. The science of agroecology
The larvae bore into the stalks and the ears of corn, examines the living organisms (collectively called
and can also survive on foxtail millet, Setaria ital- the community) in the system, their interactions
ica, and on Panicum grasses. The eggs are laid in with one another, and the environmental factors
clusters of 1040 underneath leaves about a week that influence them.
before the plant forms its inflorescence. The young
larvae can scarify the leaves and later, bore into the
stem. Pupation generally occurs within the stalk, Nutrient Cycling
but can occur within the ear. The Asian corn bor-
ers range includes India, SriLanka, Korea, China, The organisms within an ecological community
Hong Kong, Taiwan, Vietnam, Japan, Malaysia, depend on one another for energy and materials.
Thailand, Singapore and Indonesia. Green plants are referred to as producers since they
Tropical Fruit Pests and Their Management are at the base of the food chain in ecosystems. Ini-
Sugarcane Pests and Their Management tially, carbon and energy are stored in plant tissues
Vegetable Pests and Their Management through the process of photosynthesis. Consumers
must obtain their carbon and energy by eating
References plants or other organisms. Therefore carbon and
other materials move from green plants to herbi-
Denton GWR, Muniappan R, Austin L, Diambra OH (1999) vores to carnivores, including predators and para-
Fruit-piercing moths of Micronesia. Agricultural Experi- sites. The different levels of energy production and
ment Station, University of Guam. Tech Report #217, 26 pp
Hirose Y (ed) (1992) Biological control in South and East
consumption (producers, herbivores, predators)
Asia. Kyushu University Press, Fukuoka, Japan, 68 pp are called trophic levels, although in reality many
Ooi PAC (1999) Insects in Malaysian agriculture. Tropical organisms do not restrict their feeding to one level.
Press, Kuala Lumpur, Malaysia, 106 pp For instance, some Hymenoptera that are parasi-
Robinson GS, Tuck KR, Shaffer M (1994) Field guide to
smaller moths of Southeast Asia. Malaysian Nature toids as larvae may feed on pollen or nectar as
Society, Kuala Lumpur & Natural History Museum, adults. As a result, the paths along which materials
London, 308 pp move through the organisms in the community
Waterhouse DF (1998) Prospects for the classical biological
can be quite complicated, and collectively they
control of major insect pests and weeds in Southern
China. Entomologia Sinica 5:320341 make up the food web within the community.
Many nutrients, including nitrogen, phospho-
rus, potassium, and other elements, are essential
components of plant and animal tissues. These
Agroecology nutrients have distinct cycles in ecosystems, and
they cycle in food webs along with carbon and other
robert mcsorley materials. Nutrients are released into the soil during
University of Florida, Gainesville, FL, USA decomposition of organic molecules, where they
82
A Agroecology

are converted into forms that can be taken up by some regions, and many variations exist. Some
plant roots, completing the nutrient cycle. Microar- tropical subsistence intercropping systems are espe-
thropods such as mites and springtails are particu- cially diverse and complicated.
larly important in the decomposition process.

Pest Management
Cropping Systems
The cropping system used has a direct effect on
Crop performance depends on a range of key pest management, which is an important aspect of
resources including nutrients, water, soils, andother agroecology. For example, monoculture may
environmental factors, and many agricultural man- encourage buildup of some pests, such as corn
agement practices are aimed at optimizing and con- rootworms (Diabrotica spp.) or wireworms (Elat-
serving these resources. Various types of cropping eridae), that can be managed by appropriate crop
systems may be selected to address specific goals or rotation. In many cases, the use of intercropping
conservation issues. Conservation tillage and other has resulted in less severe pest outbreaks and
reduced tillage practices are important for soil con- increased diversity of natural enemies compared
servation and reduction of erosion. The crop resi- to monocultured systems.
dues that remain on the soil surface in uncultivated Tritrophic (plant-herbivore-predator) inter-
sites can also aid in conservation of water and actions and the structure of the food web may be
organic matter, and may provide some nutrients affected by changes in the cropping system, such
when they decompose (Fig.28). Monoculture as use of an intercrop, or changes in crop variety or
allows a grower to specialize by growing only one fertility level. The development and use of biologi-
crop, while polyculture permits a grower to diver- cally based pest management tactics such as use of
sify by growing multiple crops on the same land. natural enemies or resistant varieties require a
Multiple cropping on the same site may occur at the detailed knowledge of pest biology and ecology,
same time or over time. In the United States, the including life cycle, population dynamics, and
most common form of multiple cropping is crop interactions with the physical and biological envi-
rotation, in which different crops are grown on the ronment, including potential competitors, preda-
same site in different seasons or years. Cover crops tors, and parasites. Such tactics may be directed
are crops with limited market value that are grown toward preventing pest buildup rather than react-
on the site during seasons that are unfavorable for ing to high pest numbers already present in crisis
growing the main economic crops for the region. In situations. However, the design of a system in
the southeastern United States for example, a winter which pest numbers are less likely to reach crisis
cover crop of rye (Secale cereale) or crimson clover levels, due to the presence of effective natural ene-
(Trifolium incarnatum) may be grown in a field mies for example, requires advanced planning
reserved for cotton or peanut production during based on sound ecological data.
the summer. Cover crops can provide various
advantages, including erosion reduction, increased
supply of nitrogen, competition with weeds, or hay Landscape Ecology
for animals. Green manures, which are usually
legume cover crops, are grown specifically for their An individual agroecosystem does not stand alone,
nitrogen-rich residues and soil fertility benefits. since organisms, materials, and energy move freely
Intercropping, or mixed cropping (Fig.29), refers to in and out of the system. Landscape ecology exam-
the growing of two or more crops at the same time ines the agroecosystem in the context of the
on the same land. The practice is quite common in surrounding region or landscape, an essential
 Agroecology
A 83

Agroecology, Figure 28 Residues from a previous rye crop cover the soil surface between plant rows in
this conservation tillage system.

approach in dealing with migrating insects or Many natural ecosystems are highly depen-
regulated pests. The condition of field borders, dent on recycling, since cycles of nutrients, water,
hedgerows, and adjacent fields critically affects and other materials tend to be relatively closed.
pest management within a specific field. Move- In contrast, an agroecosystem is not a closed sys-
ment of pesticides, fertilizers, and other potential tem, because its purpose is to produce harvest for
pollutants from the agroecosystem to natural eco- export to other ecosystems. This process depletes
systems is a major environmental concern. essential resources from the agroecosystem
84
A Agromyzidae

Agroecology, Figure 29 One of the simplest forms of intercropping is to use one crop as a windbreak,
like the sugarcane planted along with the eggplant crop shown here.

which must be restored if the system is to remain Gliessman SR (1998) Agroecology: ecological processes in
productive. The movement of essential resources sustainable agriculture. Sleeping Bear Press, Chelsea, MI
Jackson LE (ed) (1997) Ecology in agriculture. Academic
into the agroecosystem and the recycling of exist- Press, San Diego, CA
ing resources are therefore critical concerns, to Powers LE, McSorley R (2000) Ecological principles of
anticipate and ensure that supplies of critical agriculture. Delmar Thomson Learning, Albany, NY
resources for agricultural production will be con-
served over time to sustain future agricultural
production. Agromyzidae
Organic Agriculture
Integrated Pest Management (IPM) A family of flies (order Diptera). They commonly
Conservation Biological Control are known as leaf-miner flies.
Flower Strips as Conservation Areas for Pest Flies
Management Leaf-miner Flies (Agromyzidae)
Plant Resistance to Insects
Cultural Control of Insect Pests
Agyrtidae

References A family of beetles (order Coleoptera). They com-

monly are known as primitive carrion beetles.
Altieri MA (1994) Biodiversity and pest management in Beetles
agroecosystems. Food Products Press, New York, NY
Cavigelli MA, Deming SR, Probyn KL, Harwood RR (eds)
(1998) Michigan field crop ecology. Extension Bulletin
E-2646. Michigan State University, East Lansing, MI A.I.
Coleman DC, Crossley DA Jr (1996) Fundamentals of soil
ecology. Academic Press, San Diego, CA
Collins WW, Qualset CO (eds) (1991) Biodiversity in agro- An abbreviation for active ingredient, the active
ecosystems. CRC Press, Boca Raton, FL component of an insecticide, or the toxicant.
 Alarm Pheromones of Insects
A 85

Insecticides heromone also is employed when the respond-

p
Insecticide Formulation ing individuals are stimulated to show aggression
Insecticide Toxicity towards the attacking agent. This is common in
the social Hymenoptera; for example, the honey-
bee, Apis mellifera (Hymenoptera: Apidae), and
Alarm-Defense System many ant species respond aggressively to their
alarm pheromones.
Defensive behavior that also serves as an alarm As alarm pheromones can benefit the sur-
signaling mechanism. vival of members of the species involved, it is
common for insects that employ alarm phero-
mones to live in congregations for some or all of
their life cycle. In the case of social Hymenoptera,
Air Sacs the colony is genetically related, and in asexually
reproducing aphids, the colony is clonal.
The trachea of insects are sometimes dilated or Although the survival of siblings or clones by
expanded to form pouch-like structures called air alarm pheromone response at the cost of the
sacs. Their occurrence varies among taxa, but their attacked individual appears altruistic, in geneti-
presence lowers specific gravity and enhances air cally related colonies, genes from the individual
exchange, thus enhancing flight. will predominate in the survivors and be passed
Active Ventilation on to their kin.
Abdominal Pumping

Hemipteran Alarm Pheromones

Alarm Pheromone
Alarm Pheromones of Aphids
A pheromone released to trigger alertness, disper- (Hemiptera: Aphididae)
sion or group defense by insects.
Alarm Pheromones of Insects When disturbed or attacked, many aphid species
Chemical Ecology release alarm pheromone from droplets secreted
from tube-like structures called cornicles on their
dorsal posterior. This phenomenon has been stud-
Alarm Pheromones of Insects ied exclusively in the asexual forms and most often
in asexually reproducing wingless females. Aphids
emma napper, John. a. pickett nearby exhibit a variety of behaviors ranging from
Rothamsted, Harpenden, Hertfordshire, UK stopping feeding and moving away, to running or
dropping off the plant and even attacking the
Alarm pheromones are defined as chemical sub- predator. However, not all aphids in a group
stances, produced and released by an organism, respond. The relative risks of predation and costs
that warn or alert another of the same species of of escape, for example, cessation of feeding and
impending danger. This is exemplified by many risk of desiccation, affect the likelihood of any par-
species of aphids (Hemiptera: Aphididae) in ticular response. In studies of the peach-potato
which the pheromone is caused to be released by aphid, Myzus persicae, the pea aphid, Acyrthosi-
attack, for example, by predators, with ensuing phon pisum, and the rose-grain aphid, Metopolo-
dispersal by which individual aphids may avoid phium dirhodum, early stages were found to be less
a subsequent attack. However, the term alarm sensitive to alarm pheromone than later ones.
86
A Alarm Pheromones of Insects

However, older wingless M. persicae require the with resistance, which could affect mobility or sensi-
greatest stimulation of alarm pheromone before tivity of the nervous system to stimuli.
responding, while winged M. persicae, particularly Aphids that have dropped from a plant may
those not feeding, are extremely sensitive to alarm re-colonize or may move to another host plant fur-
pheromone. The lack of response from the early ther away. The turnip aphid, Lipaphis erysimi, and
stages suggests that the risk of predation to these M. persicae dislodged by alarm pheromone are less
nymphs is lower than the risk involved in ceasing likely to return to the original host plant than when
to feed and dropping from the plant. When young mechanically dislodged. Similar patterns of behav-
M. dirhodum respond to alarm pheromone, they ior are found in A. pisum. Aphids dislodged by a
do so by moving to another part of the plant rather predator or experimentally with synthetic alarm
than by dropping. Winged adults, on the other pheromone spend longer running before the
hand, are more responsive to alarm pheromone, search for a host plant began, whereas aphids dis-
perhaps because they can more readily move off lodged mechanically are more likely to begin to
the host. The sugarcane woolly aphid, Ceratova- search for a host plant immediately.
cuna lanigera, also shows different reactions to Droplets secreted from the cornicles comprise
alarm pheromones at different life stages; it shows two types of material: a volatile, rapidly vaporizing
attack behavior until adult, when the normal aphid fraction which is the alarm pheromone, and a waxy
dispersal response takes over. fraction, consisting mainly of triglycerides, that
Considerable variation is seen between aphid crystallizes on contact with foreign particles outside
species in their sensitivity to alarm pheromones of the aphids body. The waxy component appears
and in both the speed and the form of the response. to function as a sticky or quick-setting irritant to
This variation often can be explained by differ- predators and parasitoids and a releasing substrate
ences in the ecology of the species. Some aphids, for the alarm pheromone component.
particularly those tended by ants, stay on the plant The main component of the alarm pheromone
and respond by walking or waggling their abdo- (Fig.30) of many aphids is the sesquiterpene
mens rather than falling off the plant. These aphids hydrocarbon (E)- -farnesene (1). Other compo-
appear to depend more on the protection afforded nents may also be present as found in the alarm
by their ant attendants than their own defensive pheromone blend of the vetch aphid, Megoura
mechanisms. Aphids that walk away from a source viciae, which contains the monoterpenes (-)- -
of alarm pheromone tend to form new clusters a pinene, (-)- -pinene, (Z,E)- -farnesene and
short distance from the original site, thus ensuring (E,E)- -farnesene, in addition to (E)- -farnesene.
continued ant attendance. There is a high degree of cross-activity of both nat-
Susceptibility to insecticide also has been found ural alarm pheromone and (E)- -farnesene among
to correlate with responses to alarm pheromone. Sus- species within the aphid subfamilies, Aphidinae
ceptible strains produce more pheromone and and Chaitophorinae. This is typical of insect alarm
respond more quickly and in higher numbers than pheromones in general, since such cross-activity
insecticide-resistant strains. In addition, clones col- does not reduce their evolutionary value. However,
lected from around the world showing knockdown the main component of the alarm pheromone of
resistance to pyrethroid insecticides, and esterase- the spotted alfalfa aphid, Therioaphis maculata,
based insecticide resistance, showed lower levels of and the sweet clover aphid, T. riehmi, in the
disturbance to the synthetic alarm pheromone. These Drepanosiphinae, is the cyclic sesquiterpene
aphids may therefore suffer increased predation or (-)-germacrene-A (2).
parasitism in the absence of insecticides, affecting In the turnip aphid, L. erysimi, it has been
the evolutionary fitness of insecticide resistant clones. demonstrated that isothiocyanates, acquired from
This may be due to physiological effects associated chemicals in the host plants, synergize the effect of
 Alarm Pheromones of Insects
A 87

the alarm pheromone. These isothiocyanates are metathoracic gland, while in nymphs it is the dorsal
likely to be released from aphid honeydew so that, abdominal glands. These are precursors to the
when there is a high number of other aphids in the metathoracic gland in adults and perform the same
immediate vicinity, the percentage of aphids defense function. The chemical content of these
responding to alarm pheromone increases. secretions is similar throughout the order; for
example, the components of the secretion of the
stinkbug Cosmopepla bimaculata are a complex
Alarm Pheromones of True Bugs mixture of hydrocarbons, aldehydes and esters. The
(Hemiptera, Heteroptera) secretion, which can be ejected from either or both
metathoracic glands in controlled amounts or even
The Pentatomidae is the dominant family of stink- resorbed, displays a defensive function as a preda-
bugs, or shield bugs. The family comprises many tor repellent. In one case, researchers have shown
species that are pests of economic importance, uncommon dedication in describing the repellency
especially in warmer climates. These insects secrete by squeezing adults in their mouths and chewing
a complex mixture of chemicals when strongly nymphs. The effects were a burning sensation and
molested. The energetic cost of the defense numbness of the tongue for up to two hours. In
response, especially production of defense chem- addition to repelling predators, the secretions
icals, is significant and considerable provocation possess alarm pheromone activity and cause adults
usually is required to cause release. In adults, to drop off plants. In the field, C. bimaculata are
the source of the defense compounds is the found highly clumped and the occurrence of large

Alarm Pheromones of Insects , Figure 30 Defense secretion of Cosmopepla bimaculata showing a typical
range of compounds produced by stinkbugs. Chemical structures of alarm pheromones are referenced
in the text by bold numbers.
88
A Alarm Pheromones of Insects

Alarm Pheromones of Insects, Figure 30 (Continued)

numbers living together gives an evolutionary spread the oily secretion so that the aldehydic
advantage to possessing an alarm pheromone. components can exert full irritant effect. (E)-2-
Six-carbon-long aldehydes, in particular (E)- Hexenal has been reported to have the added dual
2-hexenal, are common components of defensive functions of both alarm and aggregation phero-
secretions and are found in many families of het- mone, depending on the stimulus concentration,
eropterous insects, including the Pentatomidae, as well as use as a defense chemical. In the case of
Coreidae, Pyrrhocoridae, Cimicidae, Cynidae and the bed bug, Cimex lectularius, and Eurydema
Alydidae. it is thought that the general irritant rugosa, low concentration of (E)-2-hexenal acts as
properties of aldehydes provide a repellent effect an aggregation pheromone while high concentra-
to predators with hydrocarbons such as n-tride- tion produces an alarm response. Alternatively, it
cane, another ubiquitous component, acting to has been reported that n-tridecane, the other
 Alarm Pheromones of Insects
A 89

The pentatomid bug Erthesina fullo is a major

pest of pine and hardwood trees. Both sexes pro-
duce a secretion from the metathoracic gland
causing conspecific adults to drop from plants,
fly or move away. The secretion comprises nine
identified compounds, esters and aldehydes
(about 35%) including (E)-2-hexenal and (E)-4-
oxo-2-hexenal (3) and long chain alkanes, including
50% n-tridecane. Likewise, adult and nymph
secretions from Dysdercus cingulatus (Het-
eroptera: Pyrrhocoridae) revealed 55 identified
compounds, although the major components are
again aldehydes and n-tridecane, features com-
mon with several more species of pentatomids
from the genus Chlorochroa and Piezodorus
guildinii.
The leaf-footed bug, Leptoglossus zonatus
(Heteroptera: Coreidae), is an economically
important pest of Brazilian corn. An extract
obtained from the metathoracic gland by immer-
sion in hexane showed that the major com-
pounds were all of six-carbon length: hexanal,
hexanol, hexyl acetate, hexanoic acid, and (E)-4-
oxo-2-hexenal (3). (E)-2-Hexenal was found in
the nymph extracts but not in the adult, an
example of the general rule that exocrine chem-
istry of heteropterous nymphs is distinct from
that of the adult. In this case, different life-stages
possess different alarm pheromone systems.
When tested individually, all components pro-
duced varying degrees of alarm response in
Alarm Pheromones of Insects, Figure 30 (Continued) adults and nymphs and even mating insects
would stop and disperse, over-riding the sex
biquitous component of defense secretions, is a
u pheromone response. These compounds are not
bifunctional pheromone for the southern green species specific and are, for instance, found in
stinkbug, Nezara viridula (Heteroptera: Pentato- L.oppositus and L. clypealis, a situation that mir-
midae), which causes dispersal at high concentra- rors the cross-activity of (E)--farnesene in
tion (one individual equivalent) and aggregation many aphid species (see above), providing more
at low concentrations. The multifunctional aspect evidence that this non-specific activity does not
of these compounds has important repercussions reduce alarm pheromone value in evolutionary
for their practical use as dispersal agents for pest terms.
species in the field, as the low concentration Adults of the bean bug, Riptortus clavatus
response of aggregation may dominate once the (Heteroptera: Alydidae), a pest of Japanese soy-
applied high concentration of compounds has bean, secrete (E)-2-hexenyl acetate in its defensive
diminished. response. This causes an alarm response in adults
90
A Alarm Pheromones of Insects

and nymphs. Interestingly, adults also produce Alarm Pheromones of Social

(E)-2-hexenal, and although some response was Insects (Hymenoptera)
found when tested at high concentration, there
was no response at physiological concentration, The Honeybee (Hymenoptera: Apidae)
suggesting that this compound is not an alarm
pheromone. When the honeybee (Apis mellifera) is attacked,
The examples shown above demonstrate alarm pheromones released serve to muster help
that alarm pheromones of heteropteran families and to direct the attack. Specialized guard bees
are based on a chemical selection general to present at the nest entrance carry out attacks.
insects of a wide taxonomy and show little spe- Although these guards are relatively few compared
cies specificity. The alarm behavior caused by to the colony population, release of alarm phero-
high concentrations of n-tridecane or (E)-2- mone can result in synchronized attacks by more
hexenal is rationalized easily but the aggregation than 100 workers against an intruder. Guard bees
due to low concentrations is more difficult to initiate attacks by raising their abdomens, protrud-
explain. Perhaps these substances are constantly ing their stings and releasing alarm pheromone
emitted in very small quantities due to their vol- from the sting chamber. The workers then alert the
atility and act so as to direct individuals to a rest of the hive by wing beating, aiding dispersal of
region where conspecifics can be found and the pheromone, and by running into the hive. After
therefore where food most probably is located, a few seconds, many excited bees may rush out of
as well as the defensive advantage in being part the hive entrance and search, or stop and assume a
of a large group. characteristic tense and aggressive posture with a
Triatomine bugs (Heteroptera: Reduviidae) slightly raised body, wings extended, mandibles
are blood-sucking insects that live throughout agape and antennae waving. In this highly activated
the Americas and cause public health problems state, they will fly to attack at the slightest further
by transmitting the protozoa Trypanosoma cruzi, provocation. These two stages of alarm response
the causative agent of Chagas disease, to humans. are called alerting and activation and are charac-
Secretions from Brindleys gland (a simple sac, teristic of alarm pheromones.
metathoracic in origin) of several species all Alerted workers need to search for and dis-
revealed isobutyric acid as the major component. cover the enemy to prevent any further threat. To
Subsequently, other short-chain and branched- do this, they rely on other cues to direct the attack
chain fatty acids have been identified, and such as odor, jerky movement and hairy body
together with isobutyric acid, they act as a pow- covering. Once the threat is located, it is stung,
erful defensive secretion. Pure isobutyric acid injecting a dose of venom. However, the shaft of a
vapor, however, also caused an alarm response in sting is barbed and a bee is unable to withdraw it
Rhodnius prolixus while another report revealed from the skin of vertebrates, so the sting, together
that low concentrations of isobutyric acid with associated motor apparatus and glands, are
attracted R. prolixus adults. This defense com- severed from the bee as it attempts to fly away
pound therefore shows the same multifunctional and are left attached to the enemy. The severed
alarm and aggregation properties as described sting apparatus continues to pump venom into
for components of the stinkbug secretions (see the victim and alarm pheromone is dispersed
above). Triatomine bugs are inactive and hide from the exposed under-surface of the sting shaft
during the day, congregating in protective sites. membrane to mark an enemy and make it a more
This aspect of group living can help explain the obvious target.
evolutionary advantage in possessing aggrega- The main alarm pheromone component of
tion and alarm responses. the sting gland was identified in 1962 as isopentyl
 Alarm Pheromones of Insects
A 91

acetate (4). Although a number of other com- threat is closer to the nest and may be specialized
pounds are known to be present, isopentyl acetate to deal with vertebrate predators. Also, workers
and (Z)-11-eicosen-1-ol (5) account fully for the of the Texas leaf-cutting ant, Atta texana (Formi-
activity of the sting pheromone. The roles of the cidae: Myrmicinae), have a lower threshold for
two compounds in the pheromone appear to dif- alarm pheromone response than the queen and
fer, with (Z)-11-eicosen-1-ol responsible for pro- males. Other factors governing the type and
longing the activity of isopentyl acetate. Other intensity of alarm response are the age and size of
compounds such as 1-hexanol and 1-butanol ant colony. When alarm pheromone is present in
increase the number of bees responding. sufficient concentration to excite the workers,
Stinging bees often grip an enemy with their other stimuli are needed to direct an attack.
mandibles and deposit an alarm substance. At the Workers often will touch everything they encoun-
hive entrance, more bees examine mandibular ter and the full-scale alarm response may rely on
gland extracts of worker honeybees applied to fil- additional cues, such as the presence of an alien
ter paper than examined unscented filter paper. object. Alarm pheromones also may function
2-Heptanone (6) has been identified from the with acoustic alarm signals. Ant species in the
mandibular gland secretion, and when filter papers sub-family Dolichoderinae produce vibration
or small corks carrying 2-heptanone were placed signals using their mandibles to scratch the
at the hive entrance, the guard bees were alerted ground or the abdomen to hit the ground, increas-
and attacked them. As the mandibles are used for ing alarm behavior in other workers. Vibrations
grasping an intruder, it seems likely that the main are produced also by leaf-cutting ants which act
function of 2-heptanone is to label the intruder to as warning signals. Alarm pheromones also are
be attacked. used by ants to attract attention if they are
Under certain circumstances, honeybee alarm trapped, and may be released by reproductive
pheromones are repellent. The presence of alarm ants just before mating flights to ensure that
pheromone deters honeybees from foraging at aggressive workers protect them from potential
dishes of sugar syrup and from exposing their predators.
Nasonov glands and fanning which normally The context in which a worker encounters an
attracts other bees. Furthermore, a high concen- alarm pheromone also influences the response.
tration of alarm pheromone repelled foraging Workers of the grass-cutting ant Atta capiguara
beesfrom crops including oilseed rape, normally (Formicidae: Myrmicinae) are less likely to show
highly attractive to bees, in an area that had many alarm behavior if already engaged in a task. Forag-
honeybee colonies. ers carrying leaves do not respond to alarm phero-
mone, whereas minor workers and foragers that
are not carrying leaves do respond.
Alarm Pheromones of Ants Ant alarm pheromones may be produced
(Hymenoptera: Formicidae) from one or several sources. The army ants or
Eciton ants (Formicidae: Ecitoninae) and the rare
The Formicidae is a huge family comprising Leptanilla sp. (Formicidae: Leptanillinae) of
thousands of ant species, all of which are social Indonesia have large mandibular glands, which
insects, living in colonies that vary hugely in size. are believed to be the sole source of the alarm
Members of an ant colony may be differentiated pheromone. However, other species rely on a
into castes that specialize in carrying out particu- combination of secretions from several glands.
lar tasks and vary in their response to alarm Formica and Myrmica species use products from
pheromone. Soldiers show a more aggressive the poison and Dufours gland (both opening
response, are more likely to respond when the near the base of the sting), as well as the
92
A Alarm Pheromones of Insects

andibular gland. Ponerine ants (Formicidae:

m believed to be patrollers as they have a stronger
Ponerinae) use secretions from the pygidial gland response to alarm pheromone than foragers and
as alarm components, whereas the poison gland soldiers. Minors of other Atta species are also
is the most important gland of several other spe- more efficient at recognizing intruding ants than
cies, including the harvester ant, Messor barbarus other castes.
(Formicidae: Myrmicinae). As is the case with honeybees described above,
Ants are able to detect and respond to spe- the complete alarm response can be described by a
cific isomers of their alarm pheromone. Myrmica number of behaviors. These behaviors and their
rubra and M. scabrinodis use 3-octanol (7) as the elicitors have been dissected in an elegant piece of
alarm pheromone produced from mandibular research on the African weaver ant, Oecophylla
glands. Experiments carried out using the two longinoda. The major workers produce a secretion
optical isomers (8a, b) of this compound showed from the mandibular gland comprising four active
that M. rubra workers only responded to one of components: hexanal, hexanol, (E)-2-butyl-2-
the isomers, (R)-3-octanol (8a), while M. scabrin- octenal (10), a dimer of hexanal produced chemi-
odis workers reacted more strongly to the natural cally by self-condensation, and 3-undecanone
9:1 mixture of R and S isomers. This work sug- (11). Hexanal, a highly volatile component with an
gests that there may not only be specific chemi- active space of 510 cm (the area around an emis-
cals but also species-specific mixtures of isomers. sion where the concentration is at or above that
Many other Myrmica species have 3-octanol and required for a behavioral response), causes the
3-octanone as alarm pheromones but may have ants to be alerted, making quick runs in random
species-specific ratios of the two, which allow ant and changing direction with mandibles open and
species to only show a full alarm reaction to their antennae waving. Hexanol attracts directly to the
specific alarm pheromone blend. source at a range of 15 cm; it is repellent at very
Myrmica species of grass-cutting ants share close range and also causes further excitement. As
the main component of alarm pheromone, the hexanol disperses, 3-undecanone is attractive
4-methyl-3-heptanone (9), but they have species- over this close range and, along with (E)-2-butyl-
specific modifying components. The response to 2-octenal, acts as a marker for attack and biting
4-methyl-3- heptanone was compared to that elic- to hold the source occurs. This process is called
ited by the bodies of workers that had their heads alocal attack. In addition, O. longinoda also has a
crushed to release the natural alarm pheromone. mass attack alarm response. The poison gland of
4-Methyl-3-heptanone and bodies caused the same the major and minor workers contains venom that
level of attraction but the full range of alarm beha is ejected by raising the gasters above vertical when
vior was seen only with the bodies. In contrast, an attacked object is held in the jaws. The venom
workers of the giant tropical ant, Paraponara contains a blend of straight chain hydrocarbons
clavata (Formicidae: Paraponera), produce two and formic acid. Formic acid initiates approach
components, 4-methyl-3-heptanone and 4-methyl- and attack while n-undecane causes mandible
3-heptanol. opening, gaster raising and also short-range
Atta capiguara is a grass-cutting ant species approach to the source. The combination of these
that lives in colonies with hundreds of thousands behaviors allows location and initial attack of still
of workers. Workers are polymorphic, varying in and moving objects followed by recruitment of
size from small minors and medias to the larger workers to continue attack.
foragers and soldiers. Minors and medias do most The properties that make alarm pheromone
of the nest tasks whereas foragers collect the grass; cues for conspecifics also enable them to act as cues
however, minors often are found on foraging trails for parasites and predators of ants to find their
despite the fact they do not carry grass. They are prey. Apocephalus paraponerae is a parasitic fly that
 Alarm Pheromones of Insects
A 93

attacks the ant Paraponera clavata. Females and Cockroach Alarm Pheromones
males of A. paraponerae are attracted to injured, (Blattodea: Blattidae)
fighting or freshly killed workers. After finding a
worker, the female lays a few eggs, which will hatch Defensive secretions are well known in cockroaches.
and then feed on the victim for 37 days. Both male They are produced from ventral inter-segmental
and female A. paraponerae also feed on the wounds glands and comprise an organic and an aqueous
of the injured workers and gather near their vic- phase. In the case of the Florida woods cockroach,
tims to mate. The heads of P. clavata workers Eurycotis floridana (Dictyoptera: Blattidae), 90% of
contain two chemicals, 4-methyl-3-heptanone and the organic phase (which comprises 85% of the total
4-methyl-3-heptanol, which are particularly attrac- secretion) is (E)-2-hexenal, a compound found in
tive to A. paraponerae. These compounds are com- many heteropteran bugs and discussed above. The
mon alarm pheromone components of ants and rest of the organic secretion comprises approxi-
are released when the workers are stressed. How- mately 40 other components, including mainly alde-
ever, it has been suggested that because these para- hydes, alcohols and carboxylic acids, while the
sites use alarm pheromone for finding their host, aqueous phase contains gluconic acid, glucose and
P. clavata may be under pressure to reduce the gluconolactone. The secretion acts as a conspecific
amount of alarm pheromone released and that this alarm pheromone in these gregarious insects with
ant may even have lost alarm behavior response as nymphs responding at lower concentrations than
a result of this pressure. Similarly, the zodariid spi- adults do. Ethanolic extracts of the American cock-
der, Habronestes bradleyi (Zodariidae), a predator roach, Periplaneta americana, also repel conspecifics
of the meat ant, Iridomyrmex purpureus, detects from aggregations in daytime shelters. However,
the alarm pheromone, in this case 6-methyl-5- there was no evidence that this repellent is released
hepten-2-one (12), given out by fighting workers by living insects as an alarm pheromone but is
and uses it to locate its prey. instead endogenously produced from dead insects
and is effective against other cockroaches with
diverse phylogenetic relationships. The effect, there-
Alarm Pheromones of Thrips fore, is not pheromonal, as the authors explain the
(Thysanoptera: Thripidae) activity in terms of unsaturated fatty acids (oleic,
linoleic and linolenic acids) which emerge as signals
Thrips are small, economically important pest of death and injury among organisms from a wide
insects, often known as thunderflies. The defensive phylogenetic background. Both of the reports
behavior of thrips includes raising and lowering described above provide evidence that the use of
the abdomen and secretion of a droplet of anal alarm pheromones to increase dispersal for pest
fluid highly repellent to predatory ants. Western management purposes will be of limited value. Due
flower thrips, Frankliniella occidentalis (Thys- to the aggregation effect at low concentration, treated
anoptera: Thripidae), are not social but tend to be areas could become attractive. Also, if low concen-
found in clumped distributions. Adults and nymphs trations were used as attractants in a lure and kill
of western flower thrips produce an anal droplet approach, dead insects would repel others before
containing decyl acetate and dodecyl acetate (13) they become ensnared.
in a molar ratio of 1.5:1. Each component, at levels
of 1 ng, produces the alarm response of walking Alarm Pheromones of Beetles
away from the source or dropping from leaves. The (Coleoptera)
response, however, is only over short distances and
limits the potential for pheromone use in pest Despite the vast numbers of species in the order
management. Coleoptera, inhabiting a wide range of ecological
94
A Alarm Pheromones of Insects

niches, little is known of the existence of behavioral Conclusions

responses to alarm pheromones they may possess.
Species of beetles that are group-living are most It can be seen that alarm pheromones are used
likely to demonstrate alarm responses. Gyrinid bee- widely by a broad taxonomic diversity of insects
tles (Coleoptera: Gyrinidae), known as whirligig and elicit equally varied behavioral responses,
beetles, live in open habitats on fresh water surfaces including escape or aggressive behavior. Alarm
and typically aggregate in groups containing hun- pheromones are generally low molecular weight,
dreds of individuals, dispersing in the evening to organic compounds and so are volatile, dispersing
forage. Although easy to detect by fish, they are sel- quickly, and do not persist in the environment. In
dom preyed upon due to a repellent secretion addition, the chemical nature of the alarm phero-
released as a last resort to physical attack. The secre- mone often is unstable, increasing the lack of per-
tion also acts as an alarm pheromone over short sistence. This allows conspecifics to be alerted very
distances, increasing locomotory activity and defen- quickly over a fairly large area and yet not cause
sive movement, such as diving and active underwa- false alarm after the danger has passed. Alarm pher-
ter swimming. Although alarm dispersal after attack omones are often produced in glands responsible
can occur, the aggregations of beetles themselves for biosynthesis, storage or release of defense secre-
indicate to experienced predators to avoid the group tions. This association between alarm pheromones
and confer an aposematic effect acting at the group and defense glands, including those near the sting
level rather than the individual level. or mandibles, has led to the hypothesis that alarm
pheromones have evolved from chemicals that
originally had a defensive role, or are themselves
Lacewing Alarm Pheromones defense compounds that have taken on an addi-
(Neuroptera: Chrysopidae) tional alarm pheromonal role. The fact that known
defense components have additional multifunc-
The green lacewing, Chrysoperla carnea (Neu- tional pheromonal roles of alarm (high concentra-
roptera: Chrysopidae), is an important predator of tion) and aggregation (low concentration) also
pest aphids and, as such, is a beneficial insect. It dis- points to the possibility that these pheromonal roles
charges a malodorous secretion from glands at the have evolved from compounds originally used for
anterior of the prothorax. The major component of defense. Of particular interest is the common lack
this secretion has been identified by gas chroma- of species specificity found in alarm pheromones,
tography, mass spectroscopy and chemical synthe- which is in contrast to that of other pheromones.
sis as (Z)-4-tridecene (14) and gas chromatography Sex pheromones, for example, are so specific that
coupled electroantennagrams revealed that it is they can be the sole identifiable trait in defining
detected by the lacewing antennae. Predatory ants morphologically identical populations, such as
displayed avoidance behavior in response to it, sug- within the species complex of the sandfly, Lutzo-
gesting a defensive function, and in laboratory myia longipalpis (Diptera: Psychodidae). However,
experiments, adult lacewings avoid entering areas the alarm pheromone of different aphid species is
where it is present. In the field, it acts as an antago- (E)--farnesene and different species of Atta grass-
nist to trap catches using known attractants and, as cutting ant use 4-methyl-3-heptanone. In addition,
such, could be described as an alarm pheromone. production of (E)-2-hexenal and n-tridecane is
Another species of lacewing, Peyerimhoffina ubiquitous as multifunctional pheromone compo-
gracilis, also produces the identical compound. As nents in terrestrial true bugs, and it is possible that
lacewings are not known to be gregarious, the exact (E)-4-tridecene may reveal itself tobe common in
ecological purpose of this compound is being green lacewings. Discrimination between these
investigated. behavioral signal compounds, therefore, is not
 Alderflies and Dobsonflies (Megaloptera)
A 95

essential to their function as alarm pheromones, robably aid the dorsal diaphragm in providing sup-
p
and there may even be evolutionary benefits in port for the heart, the part of the dorsal vessel in the
being able to respond to alarm pheromones of abdomen. The muscle fibers fan out from a small
related species of insects. point of origin on the lateral wall of the dorsum to a
broad insertion on the heart in many insects, pre-
senting the typical delta appearance. In some insects,
however, the delta shape is not so evident. Some
References
alary muscle fibers pass beneath the heart and extend
laterally from side to side, and thus help to support
Aldrich JR, Blum MS, Lloyd HA, Fales HM (1978) Pentato-
mid natural products. Chemistry and morphology of the heart. In places, the fibers may also run parallel
the III-IV dorsal abdominal glands of adults. J Chem to the long axis of the heart for a short distance. The
Ecol 4:161172 pairs of alary muscles tend to agree with the number
Bowers WS, Nault LR, Webb RE, Dutky SR (1972) Aphid
of pairs of ostia, the (usually) lateral openings in the
alarm pheromone: isolation, identification, synthesis.
Science 177:11211122 dorsal vessel that allow hemolymph to flow into the
Bradshaw JWS, Baker R, Howse PE (1979) Multicomponent heart in the abdomen. Alary muscles generally do
alarm pheromones in the mandibular glands of major not occur in the thorax, but in some insects, a few
workers of the African weaver ant. Physiol Entomol
4:1525
ostia open outward in the thorax, allowing hemo-
Dawson GW, Griffiths DC, Pickett JA, Woodcock CM (1983) lymph to flow outward.
Decreased response to alarm pheromone by insect- In addition to support, the alary muscle may
resistant aphids. Naturwissenschaften 70:254255 assist in the expansion (diastole) of the heart after
Free JB, Pickett JA, Ferguson AW, Simpkins JR, Smith MC
(1985) Repelling foraging honeybees with alarm phero- each contractile wave passes a given point, and
mones. J Agric Sci 105:255260 thus aid in pulling hemolymph into the incurrent
Hlldobler B, Wilson EO (1990) The ants, 1st ed. The Belknap ostia. They are not necessary for diastole, however,
Press of Harvard University Press, Cambridge, MA
as evidenced by severing them with little or no
Nault LR, Phelan PL (1984) Alarm pheromones and sociality
in pre-social insects. In: Chemical ecology of insects. apparent effect on the heart beat.
Chapman and Hall, London, UK, pp 237256
Pickett JA, Griffiths DC (1980) Composition of aphid alarm
pheromones. J Chem Ecol 6:349360
Alate (pl., Alatae or Alates)

The winged forms of insects, particularly aphids.

Alarm-Recruitment System

Recruitment of nest members to a particular loca- Alderflies

tion to aid in colony defense.
Sociality of Insects Members of the family Sialidae (order Megaloptera).
Alderflies and Dobsonflies

Alary Muscles
Alderflies and Dobsonflies
james l. nation (Megaloptera)
University of Florida, Gainesville, FL, USA
lionel stange
The alary muscles, so named because of their general Florida Department of Consumer and Agricul-
wing or delta shape in many insects, lie immediately tural Services, Division of Plant Industry, Gainesville,
on top of the dorsal diaphragm. The muscles FL, USA
96
A Alderflies and Dobsonflies (Megaloptera)

The order Megaloptera comprises about 190 spe-

cies in 60 genera in two families. All the larvae are
aquatic. The larvae, especially of Corydalinae, are
among the most primitive of the Holometabola.
The metamorphosis from larva to adult is rela-
tively simple.
The family Sialidae, commonly called alder-
flies, is a small group of about 70 species in about
eight genera. They are worldwide. Most of the
adults have a similar appearance and are usually
dark brown to black in coloration. They lack ocelli
and have the fourth tarsomere bilobed. They are
an ancient group known from the Permian, about
200 million years ago, and evidently have not
evolved much since then. In fact, the wing vena-
tion has many features in common with the Pro-
toperlaria, a fossil order considered by some as
ancestral to the Plecoptera. The adult life span is
probably short since the reduced mouthparts do
not seem adapted for extensive feeding. The eggs
are laid in rows, forming large masses situated on Alderflies and Dobsonflies (Megaloptera),
branches, bridges, and other objects overhanging Figure31 Adult dobsonfly (Corydalidae).
the water. The larvae hatch and fall into the water
where they are predacious on other aquatic The Corydalinae with about 60 species, is dis-
insects, especially caddisflies. There are as many tributed in the New World (three genera), South
as 10 larval instars which may last up to two or Africa (one genus) and Asia (five genera). This
more years until pupation. The larva crawls out of subfamily does not have pectinate antennae and
the water and digs into the bank to form an the head is usually quadrate, often with a postocu-
earthen cell several feet from theedge of the water. lar spine. Often there are more than four crossveins
The genera are restricted geographically. The between the radius and radial sector. The male ter-
genus Sialis Latreille is Holarctic, Protosialis minalia are distinctive with a well developed ninth
Van der Weele is South American, Austrosialis gonostylus. Many of the species are very large.
Tillyard and Stenostialis are Australian, Haplosia- Corydalis Latreille is the largest genus in the New
lis Navas is from Madagascar, Leptosialis is African, World with about 30 species. The males of this
Indosialis Lestage is Oriental and Nipponsialis genus often have the mandibles greatly extended
Kuwayama is Japanese. The larva has seven lateral which is similar to Acanthacorydalis Van der Weele
processes and the abdomen terminates in an elon- from Asia. Platyneuromus christil (Navs) from
gate process. The only world compilation is by Central America, has a tremendously expanded
Van der Weele (1910) but is greatly out of date. postocular flange. The larva has eight lateral pro-
The family Corydalidae, or dobsonflies, is cesses and the abdomen ends in a pair of claw-like
characterized by having three ocelli and the anal structures. In America, the larvae are called hell-
region of the hindwing is very wide, folded fanlike grammites and are used for fishing. In one case, a
at rest (Fig.31). The fourth tarsomere is not modi- larva was found inside a fish stomach many hours
fied. There are several hundred species in about 20 after ingestion. Glorioso (1982) has provided a
genera and two subfamilies. good reference.
 Alexander, Charles Paul
A 97

The Chauliodini was reviewed by Kimmins References

(1954) who recognized 12 genera. The genera are
restricted in distribution similar to the Corydalinae Beier M (1973) The early naturalists and anatomists during
and are found in the Cape region of South Africa the renaissance and seventeenth century. In: Smith RF,
(two genera), North America (four genera), Chile Mittler TE, Smith CN (eds) History of entomology.
Annual Reviews, Inc., Palo Alto, CA, pp 8194
(three genera), Australia (one genus), Madagascar Nordenskild E (1935) The history of biology: a survey.
(one genus), and Asia (four genera). Males and Tudor, New York, NY, 629 pp
rarely females have pectinate antennae in some
genera.

Aldyidae
References
A family of bugs (order Hemiptera). They some-
Glorioso MJ (1981) Systematics of the dobsonfly subfamily times are called broad-headed bugs.
Corydalinae (Megaloptera: Corydalidae). Sys Entomol Bugs
6:253290
Kimmins DE (1954) A new genus and some new species of
the Chauliodini (Megaloptera), with notes on certain
previously described species. Bull Br Mus Nat Hist Aleyrodidae
Entomol 3:417444
Van der Weele (1910) Megaloptera. Collections Zoologiques A family of insects in the order Hemiptera. They
du Baron Edm. de Selys Longchamps, fasc 5, 93 pp
sometimes are called whiteflies.
Whiteflies
Bugs
Aldrovandi, Ulisse (Ulysse,
Ulysses)
Alexander, Charles Paul
Ulisse Aldrovandi was born in Bologna, Italy,
in 1522. He studied law in Bologna, and then Charles Alexander was born in New York state on
philosophy and medicine in Padua and Rome, earn- September 25, 1889. He entered Cornell Univer-
ing a doctorate in medicine in 1552. In 1560, he was sity in 1909, receiving B.Sc. and Ph.D. degrees in
appointed professor in Bologna, a position that he 1913 and 1918, respectively. He was employed as
held for 40 years. He lectured mainly on pharma- systematic entomologist in the Snow Entomologi-
cology, but he collected natural history objects and cal Museum at the University of Kansas in 1917
employed artists to draw them. He published four 1919 and then by Illinois Natural History Survey
large volumes during his lifetime, but his friends in 19191922. Next he moved to Massachusetts
and pupils used his voluminous manuscripts to Agricultural College and was placed in charge of
publish 10 more volumes after his death. His (1602) teaching entomology. He served as chairman of
De animalibus insectis libri VII was the first book the Department of Entomology and Zoology for
to be published on insects, although the insects 10 years, for the last three of which he was dean of
included various other kinds of invertebrates. A the School of Science (of what had by then become
chapter was devoted to the structure of the insect the University of Massachusetts). He was presi-
body. Insect reproduction and metamorphosis were dent of the Entomological Society of America in
described; respiration and the senses of touch, taste, 19411943 (two terms). His almost exclusive sub-
and smell are discussed, and the life of honey bees is ject of research was the family Tipulidae (crane
described. He died in 1605. flies) about which he published over 1,000 papers
98
A Alfalfa Leafcutting Bee, Megachile Rotundata (Hymenoptera: Megachilidae)

and described over 10,000 species, an enormous commercial scale. M. rotundata is of eastern Medi-
production. After retirement from teaching, he terranean origin and was first found in North
moved his insect collection to his house and con- America in the 1940s near seaports. It probably
tinued working on it until the death of his wife, gained entry as diapausing pre-pupae within tun-
Mabel, in 1979. Two years later he transferred his nels in the wood used to make shipping crates or
collection to the National Museum of Natural pallets.
History in Washington, DC. He died at home in
Massachusetts on December 12, 1981.
Life History

Reference Once a suitable tunnel has been found, the female

uses her mandibles to neatly cut oblong pieces of
Byers GW (1982) In memoriam Charles P. Alexander 1889 leaves or flower petals which she uses to build
1981. Journal of the Kansas Entomological Society cells end to end in the tunnel, starting at the far
55:409417
end and finishing near the entrance (Fig.32).
About 15 leaf pieces are arranged in overlapping
layers and cemented together to form a thimble-
Alfalfa Leafcutting Bee, Megachile shaped cell with a concave bottom. The cell is then
rotundata (Hymenoptera: provisioned with nectar and pollen. During this
Megachilidae) process, the female enters the tunnel head first,
regurgitates the nectar, then turns around to
mark s. goettel remove the pollen from the scopa (the pollen-
Agriculture and Agri-Food Canada, Lethbridge, collecting hairs on the underside of her abdomen)
AB, Canada and tamps the pollen into the nectar with the
tipof her abdomen. The provisions for each cell
The alfalfa leafcutting bee, Megachile rotundata consist of about two-thirds nectar and one-third
Fabricius (Hymenoptera: Megachilidae), has been pollen, requiring 1525 provisioning trips. It is
successfully semi-domesticated within the last 50 while collecting the nectar and pollen that the
years to pollinate alfalfa for seed production in bees pollinate the flowers that they visit. When
North America. Honey bees are inefficient polli- the cell has been adequately provisioned, the
nators of alfalfa and, although bumbles bees and female lays a single egg directly on the surface of
some other wild bees are efficient pollinators, they the provisions and then caps the cell with several
have proved difficult to manage. The use of the circular leaf pieces. She then proceeds to con-
alfalfa leafcutting bee has succeeded in greatly struct the next cell, repeating this process until
increasing the seed yield of alfalfa. In western the tunnel is filled. She then plugs the end of the
Canada, the average alfalfa seed yield using this tunnel with 1015 leaf pieces cemented together
bee exceeds 300 kg/ha, whereas without it is usu- to form a plug. Females continue filling tunnels
ally less than 50 kg/ha. The genus Megachile con- with cells until pollen and nectar sources are no
tains many species that nest in tunnels in dead longer available. Upon hatching, the larva imme-
trees or fallen logs. Most are solitary, but M. rotun- diately begins feeding on the provisions within its
data is gregarious and, although each female cell, undergoing four instars before reaching
constructs and provisions her own tunnel, she maturity. It then deposits a ring of fecal pellets
willtolerate close neighbors. This behavioral char- within the cell and spins a tough silken cocoon
acteristic is one of the main reasons why this within which it overwinters as a diapausing
species has been amenable to management on a pre-pupa. During the feeding period, the waste
 Alfalfa Leafcutting Bee, Megachile Rotundata (Hymenoptera: Megachilidae)
A 99

Alfalfa Leafcutting Bee, Megachile Rotundata (Hymenoptera: Megachilidae), Figure 32 Alfalfa leafcutting
bee, Megachile rotundata. (1) Adult on alfalfa flower. Flowers are pollinated while the bees visit the flowers
to collect nectar and pollen for provisioning their cells. (2) A single egg is deposited on the surface of pollen/
nectar provisions within a cell which the female constructs within tunnels using oblong pieces of leaves or
flower petals. (3) The egg placed into the cell hatches within 2 to 3 days and the larva immediately begins to
consume the provisions. The larva pupates after undergoing 4 instars. (a) single egg, (b) 3rd instar, and (c) 4th
instar larvae within the cell. Cell caps have been removed. (4) X-ray of leafcutting bee cells used to determine
quality of c ommercial bees. (a) empty cell, (b) chalkbrood cadavers, (c) Pteromalus venustus parasitoid cocoons.
(5) Nesting boards separated to show arrangement of bee cells constructed within the tunnels. In the fall, the
boards are removed from the field and the cells are stripped from the boards using specialized automated
equipment. (6) Chalkbrood cadaver within the cell. Note the ring of frass deposited on the outside edge of the
cell. Normally, the larva would spin a tough silken cocoon within which it overwinters as a diapausing pre-pupa.
Larvae infected with chalkbrood usually succumb just after defecating and just prior to cocoon spinning.
100
A Alfalfa Leafcutting Bee, Megachile Rotundata (Hymenoptera: Megachilidae)

products of digestion are accumulated internally R.H. and 30C. A few days before the bees are due to
until the larva defecates just before forming the emerge, the trays are moved to especially designed
cocoon. In the spring, the pre-pupa pupates. After shelters spaced throughout the alfalfa seed fields. By
a pupal period of 34 weeks, the adult emerges selecting the date when incubation begins, and if
and chews its way out of the cocoon. Mating takes necessary manipulating the incubation tempera-
place soon after emergence of the adults. Females ture, the emergence of the bees can be adjusted to
store enough sperm from a single mating to fertil- coincide with the start of alfalfa bloom.
ize all of their eggs. Soon after mating, the females An advantage of the loose cell system of
seek out suitable sites in which to excavate tun- management is that it facilitates the control of
nels or select suitable preexisting ones, either nat- parasitoids, predators and disease, and assess-
ural or man-made. ment of the quality of the progeny. Leafcutting
beekeepers routinely send samples of cells to
specialized leafcutting bee cocoon testing cen-
Domestication ters, where they are x-rayed and incubated to
provide estimates of numbers of intact cells,
The gregarious nature of M. rotundata and its incidence of parasites and pathogens, and sex
willingness to accept artificial domiciles has per- ratio. These data are used to determine stocking
mitted the commercial scale management of this rates and to set a price if bees are to be marketed.
species for crop pollination. Initially, observant The proportion of females, which is usually only
alfalfa seed producers in the northwestern U.S.A. about a third, is of particular interest because
noticed that this species, which had undergone a they are the primary pollinators.
population increase following natural establish-
ment, would nest in man-made structures such as
shingled roofs and they started to provide artificial Natural Enemies
tunnels by drilling holes in logs positioned around
the edges of the seed fields. The next step was to About 20 species of insects are known to parasitize
provide nests consisting of wooden blocks drilled or prey on the immature stages of the alfalfa leaf-
with closely spaced tunnels. Although reasonably cutting bee. The most important of these are sev-
successful on a small scale, this method was not eral species of chalcid wasps, including Pteromalus
suitable for the management of the large numbers venustus Walker, Monodontomerus obscurus West-
of bees (50,00075,000/ha) required for commer- wood, Melittobia chalbii Ashmead and Diachys
cial alfalfa seed production. Consequently a loose- confusus (Girault). The most widespread and dam-
cell system was developed. This system uses 10 mm aging is P. venustus, which probably arrived in
thick boards of wood or polystyrene which are North America with its host. The female parasit-
grooved on both sides and stacked together to form oid pierces the host cocoon with her ovipositor,
hives of closely packed tunnels about 7 mm in stings the larva or pupa to paralyze it, and then
diameter and 150 mm in length. At the end of the lays some eggs on its surface. The parasitoid larvae
season, the boards are separated and the cells then feed upon the bee larva eventually killing it.
removed using specialized automated equipment. Normally 1520 adult P. venustus emerge from
After being stripped from the boards the cells are each host cocoon.
tumbled and screened to remove loose leaf pieces, Two other enemies, which are more of bio-
molds and some parasites and predators. The clean logical interest than economic significance, are
cells are then placed in containers for overwinter- several species of cuckoo bees, Coelioxys (Mega-
ing storage at about 50% R.H. and 5C. In the spring, chilidae) and the brown blister beetle, Nemogna-
the cells are placed in trays for incubation at 70% tha lutea LeConte. Cuckoo bees are very similar to
 Alfalfa (Lucerne) Pests and their Management
A 101

leafcutting bees, but lack the structures required way through infected cadavers in order to exit
for collecting pollen. The female cuckoo bee lays their nesting tunnels. Chalkbrood can be ade-
her egg in the partially provisioned cell of the leaf- quately managed through strict hygiene and
cutting bee while the rightful owner is out forag- decontamination of the bee cells, nest materials
ing. When partly grown, the cuckoo bee larva kills and shelters. Initially, decontamination was per-
the leafcutting bee larva and usurps the provi- formed by dipping in household bleach. However,
sions. Brown blister beetle females lay their eggs fumigation with paraformaldehyde has become
on flowers and the first instar larvae (triungulins) the method of choice, and is highly effective for
attach themselves to any bee that visits the flower. the control of both A. aggregata and foliar molds,
When the bee returns to its nest, the triungulin which can sometimes pose a health risk to the
detaches and begins feeding on the cell contents, beekeeper.
destroying 2 or 3 cells before reaching maturity. Bees
Several stored-product insects including the
driedfruit moth, Vitula edmandsae serratilinnella
Ragonot, and stored-product beetles such as the
References
sawtoothed grain beetle, Oryzaephilus surinamen-
sis (Linnaeus), the red flour beetle, Tribolium cas-
Goerzen DW, Watts TC (1991) Efficacy of the fumigant
taneum (Herbst) and the confused flour beetle, paraformaldehyde for control of microflora associated
Tribolium confusum (Jacquelin du Val) can cause with the alfalfa leafcutting bee, Megachile rotundata
serious damage during overwintering storage, (Fabricius) (Hymenoptera: Megachilidae). BeeScience
1:212218
especially if sanitation practices are lax. Goettel MS, Richards KW, Goerzen DW (1993) Decontami-
Most of the parasitoids and predators can be nation of Ascosphaera aggregata spores from alfalfa
largely controlled by proper construction of hives leafcutting bee (Megachile rotundata) nesting materials
and nesting materials, physical removal during by fumigation with paraformaldehyde. BeeScience
3:2225
the loose-cell processing and strict hygiene during Hill BD, Richards KW, Schaaljie GB (1984) Use of dichlorvos
storage. However, successful control of the major resin strips to reduce parasitism of alfalfa leafcutter
pest, the chalcid P. venustus, often requires care- bee (Hymenoptera: Megachilidae) cocoons during
incubation. J Econ Entomol 77:13071312
fully controlled fumigation using dichlorvos (2,
Richards KW (1984) Alfalfa leafcutter bee management in
2-dichloro-vinyl dimethyl phosphate) resin strips. Western Canada. Publication #1495E. Agriculture
The only disease causing significant losses to Canada, Ottawa, Canada, 53 pp
the leafcutting bee industry is chalkbrood, caused Richards KW (1987) Alfalfa leafcutter bee management in
Canada. Bee World 68:168178
by the fungus Ascosphaera aggregata Skou. The Vandenberg, JD, Stephen WP (1982) Etiology and symptoma-
disease was first reported in leafcutting bees in tology of chalkbrood in the alfalfa leafcutting bee,
1973, and remains most severe in the western U.S. Megachile rotundata. J Invertebr Pathol 39:133137
states, where losses of more than 65% of bees are
not uncommon. Bee larvae become infected after
consuming pollen provisions contaminated with Alfalfa (Lucerne) Pests and their
the fungal spores which germinate within the Management
midgut and penetrate into the hemocoel. Larvae
soon die and turn a chalk white color as the myce- john l. capinera
lium fills the body. Sporogenesis occurs beneath University of Florida, Gainesville, FL, USA
the host cuticle resulting in the formation of asco-
spores which are bound in spore balls within Alfalfa (lucerne), Medicago sativae, is one of the
ascomata. At this stage, the cadaver turns black. most important legumes used in agriculture. It is
Spores are spread by adults that must chew their the principal roughage for ruminants, as well as
102
A Alfalfa (Lucerne) Pests and their Management

being an important source of protein in animal climates it is irrigated. It is tolerant of cold, grow-
diets. It is surpassed only by grass, corn, and soy- ing well in cool and cold climates. It does not tol-
bean as an animal feed, and is especially important erate hot, humid climates, however.
to the dairy industry. The USA is the worlds larg- Alfalfa often is cut and dried before it is baled
est producer of alfalfa, but it also is an important and stored. To speed up the process of drying, alfalfa
crop in Australia, Europe, Argentina, China, South is commonly flailed or passed through a set of roll-
Africa, and the Middle East. ers to break or crush the stems, facilitating the dry-
There are other uses for alfalfa, though they are ing process. The crushing process is called crimping
minor. Alfalfa sprouts are a salad ingredient, alfalfa and sometimes can cause problems for horses
shoots are sometimes consumed as a leafy vegeta- because blister beetles (Coleoptera: Meloidae) are
ble, and dehydrated alfalfa is sometimes formulated incorporated into the hay (see below, blister beetles).
as a tablet to be consumed as a dietary supplement. Dried alfalfa is tied into bales of various sizes,
Alfalfa is a cross-pollinated species. It relies on including large cylindrical bales, and stored under
insects, often domesticated leafcutting bees, honey shelter, or packaged in plastic, to avoid moisture. If
bees, alkali bees, and various wild bees, for pollina- the alfalfa is to be fed to cattle, however, it is not
tion. Wind pollination does not occur because the dried, and instead it is finely chopped and stored in
blossom is structured in a way that physical trip- trenches, silos, or bags where it can ferment and
ping to expose the stigma to the anthers is required. maintain high nutrient levels. Cattle are not very
Bees manipulate the blossom when foraging for susceptible to poisoning by blister beetles.
nectar and pollen and thereby trip the blossom, an Alfalfa has undergone considerable breeding
action that results in the bee being struck in the to produce strains that have not only suitable agro-
head. An interesting aspect of pollination is that nomic conditions, but also are disease and pest
some bees learn to avoid the tripping process to resistant. Nevertheless, insects can damage alfalfa
avoid being struck, thereby robbing the flower with- nearly everywhere it is grown. Some of the impor-
out pollination occurring. Older honey bees are tant pests are listed in the table, and the most
good at avoiding tripping, but nave young honey important are discussed below.
bees trip the blossom and provide pollination.
Alfalfa is normally harvested before, or at, the
initiation of flowering, which maximizes protein Alfalfa Weevil, Hypera postica
content of the harvested hay. Because pollinators (Gyllenhal) (Coleoptera:
are often present in alfalfa fields during the bloom Curculionidae)
period, care must be taken when using insecticides
for pest suppression to avoid products that are In many regions, this is the most important pest of
highly toxic to pollinators, at least if seed produc- alfalfa. It is found in Europe, the Middle East, Cen-
tion is a concern. However, most alfalfa is grown tral Asia, and North America. Alfalfa weevils over-
only for forage, and without regard for seed pro- winter as adults in the soil of weedy, brushy areas
duction. Thus, insecticide use may include the near alfalfa fields. They disperse to alfalfa in the
bloom period, though if pollinator populations spring and oviposit within the stems. The eggs are
are reduced, other crops that require pollination oval and yellow. Early instars developing from
may be inadvertently affected. these eggs are slate colored, but develop a bright
Alfalfa is unusual as a field crop in that it is a green color and a white stripe down the middle of
short-lived perennial, living 312 years. It may be the back as they mature. Larvae have a black head
harvested from once to 12 times per year, depend- capsule. They display four instars and will grow to
ing on climate and growing conditions. It has deep about 810 mm in length. After feeding for 34
roots, and is resistant to drought, though in arid weeks, larvae spin loosely constructed cocoons on
 Alfalfa (Lucerne) Pests and their Management
A 103

Alfalfa (Lucerne) Pests and their Management, Table 5 Some pests of alfalfa (lucerne), and locations
where they are considered to be damaging
Feeding behavior Primary taxon Common name Scientific name Location
Above-ground, Coleoptera Sitona weevil Sitona discoides Australia
chewing
Small lucerne Atrichonotus Australia
weevil taeniatulus
Vegetable weevil Listroderes Australia
obliquus
Alfalfa weevil Hypera postica Europe, Asia,
N.America
Clover leaf weevil Hypera punctata Europe, Asia,
N.America
Clover head weevil Hypera meles Europe, N. America
Blister beetles Epicauta spp. N. America
Flea beetles Epitrix, Systena, N. America
Disonycha spp.
Orthoptera Grasshoppers Melanoplus spp. N. America
Wingless Phaulacridium Australia
grasshopper spp.
Lepidoptera Armyworm Mythimna spp., Australia
Armyworm Persectania spp. Australia
Armyworm Pseudaletia N. America
unipuncta
Variegated Peridroma saucia Europe, Asia, Africa,
cutworm N.America
Army cutworm Euxoa auxiliaris N. America
Granulate cutworm Agrotis N. America, S.America
subterranean
Black cutworm Agrotis ipsilon N. America, Europe,
Africa
Beet armyworm Spodoptera Asia, N. America
exigua
Fall armyworm Spodoptera N. America, S.America
frugiperda
Budworm Helicoverpa Australia
punctigera
Corn earworm Helicoverpa zea N. America, S.America
Alfalfa looper Autographa N. America
californica
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A Alfalfa (Lucerne) Pests and their Management

Alfalfa (Lucerne) Pests and their Management, Table 5 Some pests of alfalfa (lucerne), and locations
where they are considered to be damaging (Continued)
Feeding behavior Primary taxon Common name Scientific name Location
Lucerne leafroller Merophyas Australia
divulsana
Alfalfa caterpillar Colias eurytheme N. America
Webworms Loxostege spp. N. America, Europe,
Asia
Collembola Lucerne flea Sminthurus Australia, Europe,
viridis Africa
Diptera Alfalfa blotch Agromyza Europe, N. America
leafminer frontella
Above-ground, Acari Redlegged earth Halotydeus Australia
sucking mite destructor
Clover mite Bryobia spp. Australia
Twospotted spider Tetranychus No. America
mite urticae
Collembola Lucerne flea Sminthurus Europe, N. Africa,
viridis Australia
Hemiptera Pea aphid Acythosiphum Europe, Asia, Australia,
pisum N. & S. America
Blue alfalfa aphid Acythosiphum Mediterranean,
kondoi Australia, N. & S.
America
Spotted alfalfa Therioaphis Mediterranean,
aphid maculata Australia, N. America,
Asia
Potato leafhopper Empoasca fabae N. America
Lucerne leafhopper Austroasca Australia
alfalfae
3-cornered alfalfa Spissistilus N. America
hopper festinus
Meadow spittlebug Philaneus N. America
spumarius
Tarnished plant Lygus spp. Europe, N. America
bugs
Alfalfa plant bug Adelphocoris Europe, N. America
spp.
Thysanoptera Flower thrips Frankliniella spp. Europe, Asia,
N.America
Below-ground Coleoptera Clover root Sitona hispidula Europe, N. & C.
curculio America
 Alfalfa (Lucerne) Pests and their Management
A 105

Alfalfa (Lucerne) Pests and their Management, Table 5 Some pests of alfalfa (lucerne), and locations
where they are considered to be damaging (Continued)
Feeding behavior Primary taxon Common name Scientific name Location
Alfalfa snout beetle Otiorhynchus N. America
ligustici
African black Heteronychus Africa, Australia
beetle arator
Whitefringed Naupactus Australia, S. America
beetle leucoloma
Small lucerne Atrichonotus Australia
weevil taeniatulus

plants or in litter on the soil, pupate, and emerge as aethiopoides Loan and M. colesi Drea (Hymenoptera:
adults in 12 weeks. Adults are 56 mm long, have Braconidae) Oomyzus incertus (Ratzenberg)
a long snout, and have a dark stripe down the back. (Hymenoptera: Eulophidae); Dibrachoides dynas-
They are light brown at emergence and darken in tes (Forester) and Peridesmia discus (Walker)
several days. The number of generations varies (Hymenoptera: Pteromalidae); and Anaphes luna
according to climate, but eventually they leave (Girault) (Hymenoptera: Mymaridae). A fungal
fields for grassy, brushy, weedy areas where they pathogen, Zoophthora phytonomi Arthur (Phyco-
become inactive until the onset of winter. mycetes: Entomophthoraceae), attacks weevil lar-
Damage is caused by the larval stage which vae and can control populations in several days,
feeds on leaves; damage ranges from pinholes to though it is most effective under moist conditions.
skeletonization of leaves. Adults generally cause These biological control agents are extremely effec-
minor damage. Peak damage is usually just prior tive control measures in all but major outbreak
to the first cutting or after the first cutting, as both periods. However, when fields show damage on
larvae and adults feed on new growth; this can 3540% of plant tips more than 710 days prior to
seriously affect regrowth of the stand. Also, cool, harvest, chemical suppression is often initiated.
cloudy weather exacerbates damage done by the Early harvest (first crop) is very effective in
alfalfa weevil. Cool and cloudy weather conditions killing larvae, and is preferred to chemical control if
slow the regrowth rate of alfalfa, and also increase the planned harvest is less than 710 days away. If
the daily feeding period of the weevil because both harvesting is used to control alfalfa weevil, the stub-
larvae and adults tend to hide under crop residue ble and debris should be examined closely for adults
during bright sunlight and will not actively feed and larvae, and stems should be examined for feed-
during such periods. ing signs. It may be necessary to spray stubble,
Weevil larvae can be found early in the Spring. though in many areas producers can avoid insecti-
It is important to scout for live larvae and injured cide use consistently through timing of harvest.
terminals on the first crop, but also subsequent
crops. Sweep net sampling can be used to detect
weevil presence. Several species of wasps can be Root Weevils, Sitona spp.,
effective in maintaining weevil populations below Atrichonotus taeniatulus (Berg),
economic threshold levels. Among the effective Others (Coleoptera: Curculionidae)
parasitoids are Bathyplectes curculionis (Thomson),
B. anurus (Thomson) and B. stenostigma (Thomson) Root weevils such as clover root curculio, Sitona his-
(Hymenoptera: Ichneumonidae); Microctonus pidula (Fabricius), in North America; and sitona
106
A Alfalfa (Lucerne) Pests and their Management

weevil, Sitona discoideus Gyllenhal, small lucerne c ontain crushed blister beetles that may prove toxic
weevil, Atrichonotus taeniatulus (Berg), in Australia, to horses that ingest the hay. The most abundant
and whitefringed beetle, Naupactus leucoloma Bohe- blister beetle in alfalfa fields generally is the black
man in Australia and South America, can be signifi- blister beetle, E. pensylvanica (De Geer). However,
cant pests of alfalfa. Although the adults commonly the species that is most toxic is E. vittata (Fabricius).
feed on the foliage, the principal damage is due to Most blister beetles are recognized by the
larval feeding on the roots of the alfalfa plant. shape of their body. They are narrow, cylindrical,
Eggs are laid in fall or spring, on the soil sur- and soft. The region between the head and wings is
face or lower parts of plants. Eggs hatch in the distinctly narrower than the wings, and is usually
winter or spring. White, legless larvae move into narrower than the head. Most species have one
the soil and feed on roots until they pupate. Pupae generation per year, although some have two.
are found just below the soil surface. Adults emerge Blister beetles overwinter as larvae. The adults
in the summer months and live up to a year. The begin to emerge in the Spring and adults deposit
adults are brown or black, blunt-snouted weevils their eggs where grasshopper egg pods may occur,
up to about 10 mm long. There is one generation as larvae feed on the grasshopper eggs.
per year. Adults migrate by crawling, and thus If grasshoppers are not abundant, then blister
infest new areas rather slowly. beetles are unlikely to be abundant. When both
The adults feed on alfalfa leaf margins, leaving are numerous, it is advisable to harvest alfalfa
crescent-shaped notches, and chew on stems and early, before bloom, as this is the only time that
leaf buds of seedlings, but this tends to cause beetles are attracted to the crop. There is some
minor loss. Most damage is caused by the larvae. yield loss associated with this approach, of course,
First larval instars feed on root nodules and lateral and an alternative it to treat the crop with insecti-
roots; later instars feed on the taproot. Feeding on cides. If insecticide is used, alfalfa should be har-
the taproot can girdle the plant, resulting in plant vested as soon as possible after the pre-harvest
death. Such damage also weakens the overall vigor interval expires, to get hay out of the field before it
of a stand, perhaps contributing to winter-kill and is re-infested. A principal problem with blister
increased susceptibility to disease. beetle management is that the beetles tend to
It is difficult to control larvae because they are aggregate. Thus, there may be relatively few bee-
in the soil and largely protected from insecticide. tles in field, but a large number in one location,
Suppression aimed at adults usually requires mul- and these may be crushed together and concen-
tiple applications. It is inadvisable to plant alfalfa trated into one or a few bales of hay. Thus, they are
into a field which has previous ly been infested, to hard to detect by standard sampling methods.
plant into fields previously supporting legume When alfalfa hay is purchased for horses, it is
crops, or to seed alfalfa next to established stands. advisable to acquire early-crop hay, or hay from
areas free of high grasshopper populations. Alter-
natively, inspection of the hay as it is fed to horses
Blister Beetles (Epicauta spp.) can reveal the presence or absence of beetles.
(Coleoptera: Meloidae)

There are several species of North American blister Potato Leafhopper, Empoasca
beetles that can be of concern in alfalfa. They are a fabae (Harris) (Hemiptera:
problem not because of their food habits (they tend Cicadellidae)
to feed mostly on blossoms) but because they con-
tain the toxin cantharidin within their bodies. When Potato leafhopper is indigenous to eastern
alfalfa is harvested, if the hay is crimped it may North America. Adults are about 3.5 mm long,
 Alfalfa (Lucerne) Pests and their Management
A 107

wedge-shaped, winged, and green. Nymphs are Although the potato leafhopper has natural
similar in appearance, but are smaller, yellowish- enemies, they often get left behind when the adults
green to fluorescent green, and wingless. Each disperse. Thus, a combination of crop monitoring
Spring, potato leafhoppers migrate north from and insecticide suppression is often the principal
southern states where they overwinter. Timing of management strategy. Chemical control of potato
the first and subsequent arrivals in the north is leafhopper is effective, but should not be used if
heavily dependent on weather patterns. Adults lay harvest is within seven days of harvest. Cutting
eggs in stems and leaf veins; eggs hatch in 69 days will kill a large percentage of nymphs, and will
in mid-summer. Each generation takes approxi- force adults out of the field. Cutting is the control
mately 3035 days to mature, resulting in several of choice if thresholds are reached within seven
generations. days of harvest. Additionally, early harvest may be
Adults and nymphs both feed on alfalfa with an alternative to insecticides when thresholds are
piercing-sucking mouthparts, sucking plant sap reached late in the year.
and injecting a toxin into the plant. Damage is
called hopperburn, and is a yellow wedge-shape
area beginning at the tips of leaves. The leaves may Aphids (Hemiptera: Aphididae)
eventually turn entirely yellow or reddish. Plants
may become stunted. Leafhoppers cause yield loss, Several aphids are pests of alfalfa, including pea
reduced nutritional quality of alfalfa, and reduced aphid, Acyrthosiphon pisum (Harris); blue alfalfa
plant vigor that results in increased winter-kill and aphid or bluegreen aphid, Acyrthosiphon kondoi
slower regrowth of the crop the next spring. Shinji, cowpea aphid, Aphis craccivora Koch; green
In some regions of the USA, the potato leafhop- peach aphid, Myzus persicae Sulzer; and spotted
per is the worst insect pest of alfalfa, and can cause alfalfa aphid, Therioaphis maculata Buckton.
losses of 80% or more if not controlled. Leafhoppers All these aphids are small, measuring 3 mm
are not generally a problem in the first crop in an or less. Their color varies, depending on species.
established stand, but as the population increases, all They may or may not be winged. In most climates,
subsequent crops will need to be monitored for in early Spring nymphs hatch from eggs that were
infestation. The characteristic hopperburn will not laid in the fall; these aphids are all female. Females
appear until some yield and quality loss has occurred, can reproduce without mating when conditions
so it is important to scout for leafhoppers weekly are favorable, and they do so in Spring and Sum-
onthe second and subsequent crops. Scouting may mer. In the Summer, the entire life cycle takes
be concluded 710 days prior to harvest. only a few days. Males appear in late Summer,
Potato leafhopper economic thresholds are and mate with females to produce eggs capable of
based on plant height. Scouting is accomplished overwintering.
by sweep net sampling. As an example, following Aphids use piercing-sucking mouthparts to
are treatment thresholds recommended for remove plant sap, and prefer to feed on young
Minnesota, USA. growth. Aphid feeding can result in stunted or
wilted plants. The plants may also turn yellow.
Average plant height # adult leafhoppers/ Aphids commonly attain high densities in
sweep alfalfa, but in most years natural enemies keep
< 3 inches 0.3 aphid populations at levels that are not economi-
37 inches 0.5
cally important. Many natural enemies of pea
aphids exist, including green lacewing larvae
812 inches 1.0
(Neuroptera: Chrysopidae), damsel bugs
> 12 inches 2.0
(Hemiptera: Nabidae), and parasitic wasps
108
A Alfalfa (Lucerne) Pests and their Management

(Hymenoptera, various families), lady beetles Most egg laying occurs in late summer and fall in
(Coleoptera: Coccinellidae), and disease (fungi). production areas; most species prefer uncultivated,
grassy or weedy areas, and lay eggs 13 cm below
the soil surface.
Plant Bugs (Hemiptera: Miridae) Grasshoppers are generally considered a
minor pest except during periods of great abun-
Several species of plant bugs affect alfalfa, but the dance, and then they can do great damage. An
most common are tarnished plant bug, Lygus line- exception is Australia, where wingless grasshop-
olaris (Palisot de Beauvois), and alfalfa plant bug, per has become an increasingly severe pest of
Adelphocoris lineolatus (Goeze). Adult tarnished alfalfa. Damage has increased in Australia due
plant bugs are brown, winged, and 46 mm long; to widespread cultivation of alfalfa, which is
nymphs are green, wingless, and the third and more suitable than grasses for nymphal growth
subsequent instars have black spots. Adult alfalfa and survival. Grasshopper nymphs and adults
plant bugs are light green, winged, and 7.510 mm damage alfalfa by chewing on leaves from the
long; nymphs are green, wingless, and have red margin inward in an irregular pattern. Attacks
eyes. Tarnished plant bugs overwinter as adults; are often on new growth, but will occur on any
alfalfa plant bugs overwinter as eggs in plant tis- stage. The margins of fields are most likely to be
sue. During the growing season, the entire life damaged.
cycle takes 2050 days, depending on temperature. In North America, grasshopper infestations
There are two to five generations per year. are more severe in warm and dry years. Warm,
Plant bugs suck sap from plants and inject dry weather immediately following egg hatch
toxic saliva into the plant. They cause leaves to favors survival of nymphs, because nymphal
crinkle, plants to be stunted, and flower buds to growth rates and survival are lower in cool, wet
abort. They are abundant in all but the earliest weather. Long, warm autumns prolong the egg-
portions of the season. Although traditionally laying season, and result in larger populations in
considered mostly a seed pest, plant bugs also the next growing season. It can take 35 years for
contribute to forage yield reductions. If bugs are populations to build to economically important
abundant more than seven days prior harvest, levels. In Australia, drought also is implicated,
chemical control may be warranted. but mermithid nematodes are a critical element
in grasshopper biology. Absence of rainfall, and
clearing of drier, higher elevation pasture impedes
Grasshoppers (Melanoplus spp. the ability of the nematodes to parasitize the
and Phaulacridium spp.) grasshoppers.
(Orthoptera: Acrididae) Grasshoppers are naturally suppressed by
numerous natural enemies, but when weather con-
Everywhere alfalfa is grown, grasshoppers and ditions favor the grasshoppers their populations
locusts will feed on the crop. However, they are increase quickly. The natural enemy population
only casually associated with alfalfa, attacking the increases as their food supply becomes more avail-
crop only when abundant. None feed preferentially able, but the lag in natural enemy abundance can
on alfalfa. In North America, the principal pests are result in crop damage by the grasshoppers. Weedy
Melanoplus spp., and in Australia Phaulacridium fence rows, irrigation ditches, and fallow fields are
spp. is the major grasshopper pest. These economi- important sources of grasshoppers. Weed popula-
cally important grasshoppers overwinter as eggs. tions should be managed, which may require tillage
Populations disperse into cultivated fields or pas- or burning to make these habitats less productive
tures as their populations build through the season. for grasshoppers.
 Alfalfa (Lucerne) Pests and their Management
A 109

Cutworms, Armyworms and ability and its minute size, not because it is a flea
Budworms (Lepidoptera: or related to fleas. This species has a patchy dis-
Noctuidae) tribution in Europe and North Africa, and has
been accidentally introduced to Australia, where
The caterpillars of several moths can become it is most injurious. It also affects lupine flowers,
abundant enough to cause significant loss to lentils, beans, and field peas. Immature lucerne
alfalfa.Among these are the armyworms Mythimna fleas consume small patches of foliage, whereas
spp., Persectania spp., and Pseudaletia unipuncta adults consume the entire leaf except for the
Haworth; variegated cutworm, Peridroma saucia veins. Early season spraying of insecticide is the
(Hbner); army cutworm, Euxoa auxiliaris most common recommendation to curb their
(Grote); granulate cutworm, Agrotis subterranea damage.
(Fabricius); beet armyworm, Spodoptera exigua
(Hbner); budworm, Helicoverpa punctigera
(Wallengren), and many others. The important Mites (Acari)
species vary among regions, though they are simi-
lar ecologically. Mites generally are not major pests of alfalfa, but
The larvae of cutworms, armyworms, and under arid conditions or along the margins of
budworms range in color from greenish-yellow to fields they can be quite damaging. The most impor-
brownish-black. Larvae are 25 cm long at matu- tant are clover mites, Bryobia spp. (Acari: Tetrany-
rity. The wings of the adults vary from tan to dark chidae), and redlegged earth mite, Halotydeus
brown with mottling or stripes. Pupae are 13 cm destructor Tucker (Acari: Penthaleidae), in Austra-
long and are reddish-brown to black in color. lia, and twospotted spider mite, Tetranychus urticae
There are one to six generations per year. Larvae Koch (Acari: Tetranychidae) in North America.
overwinter in the larval or pupal stage, depending They rupture the cells of leaf tissue, imparting a sil-
on species. ver or yellow appearance, and reducing yield.
Larvae feed on stems and leaves of plants, and
can limit regrowth after harvest. Larvae will also
cut the stems of seedlings. Their occurrence as Pest Management in Alfalfa
economic pests is sporadic. Although these insects
have many natural enemies, when they are abun- Alfalfa is an excellent crop for the practice of mod-
dant insecticides are the preferred approach to ern pest management tactics because (i) it is quite
population reduction. tolerant of damage; cosmetic injury is not impor-
tant; (ii) it is a perennial crop, providing harbor-
age throughout the year for an immense assemblage
Lucerne Flea, Sminthurus viridis of insects, including predators and parasitoids;
(Collembola) (iii) it is an important crop, so extensive research
on the pests have been conducted; (iv) it is amena-
Sminthurus viridis, the lucerne flea or clover ble to various cultural manipulations, and pro-
springtail, is an insect relative (hexapod) belong- duces multiple crops over a large portion of the
ing to the order Collembola (the springtails). It year; and (v) it is a favorite crop for rotations, so
is bright green with a roughly spherical body there is ample opportunity to integrate its culture
and may swarms in large numbers on living with the culture of other crops.
plants, including alfalfa or lucerne, thus the first The principal tactics used for alfalfa produc-
part of the common name. The second part of tion include scouting and use of an economic
the common name was given for its jumping threshold for decision making, natural and classical
110
A Alfalfa Weevil, Hypera Postica (Gyllenhal) (Coleoptera: Curculionidae)

biological control, cultural control, and chemical populations. Strip cropping is commonly recom-
control. The economic threshold varies among mended because the uncut areas retain popula-
insect species, geographic locations, crop manage- tions of natural enemies, allowing the beneficial
ment practices and economic conditions, but most insect to move into newly harvested alfalfa as it
locations have established such benchmarks for regrows and becomes infested with pests. Farmers
initiating chemical control. A large number of rarely embrace this approach, however, opting for
insecticides are registered for this crop, so growers operational efficiency over economic pest control.
have ample opportunity to select products accord-
ing to their need and budget. A modest level of
host plant resistance apparently exists in alfalfa, References
and although resistance is effective mostly against
aphids, there is also some success with alfalfa wee- University of California (1981) Integrated pest management
vil and leafhoppers. for alfalfa hay. Publication #3312, 98 pages
A large number of beneficial arthropods have Summers CG (1998) Integrated pest management in forage
alfalfa. Integr Pest Manage Rev 3:127154
been moved around the world in an effort to attain
biological suppression of invading alfalfa-feeding
insects. In some cases this has met with success. For
example, alfalfa blotch leafminer, Agromyza fron- Alfalfa Weevil, Hypera postica
tella (Diptera: Agromyzidae), was considered a seri- (Gyllenhal) (Coleoptera:
ous pest when it first invaded the eastern USA, but Curculionidae)
following release of wasp parasitoids it fell to minor
pest status. Similarly, the status of spotted alfalfa An important defoliator of alfalfa (lucerne).
aphid, pea aphid and blue alfalfa aphid was affected Alfalfa (Lucerne) Pests and their Management
by importation of beneficial insects. A native ento-
mopathogenic fungus, Zoophthora phytonomi, has
adapted to the invasive alfalfa weevil and sometimes Alga (pl., Algae)
provides good suppression. Pea aphid is affected by
the fungus Erynia neoaphidis under favorable An aquatic non vascular plant, often very small in
weather conditions. Generalist predators such as size. Algae can reach pest status when weather and
lacewings, lady bird beetles, nabids, soft-winged nutrient levels favor its growth, and pesticides may
flower beetles, big-eyed bugs, and minute pirate be needed to suppress it.
bugs are often active in alfalfa, and provide good
suppression of aphids, thrips, and also consume Alien
eggs and young larvae of caterpillars.
Cultural manipulations are the most impor- An organism that is native elsewhere. These are
tant tactics for management of alfalfa pests. In also referred to as exotic or foreign.
particular, early harvesting can provide acceptable Invasive Species
or even nearly complete control of alfalfa weevil,
alfalfa blotch leafminer, several caterpillars, aphids,
and leafhoppers because when the crop is cut the Alienicolae
insects are exposed to lethal levels of heat and dry-
ness, or the environment becomes so unsuitable In heteroecious aphids, viviparous parthenoge-
that the insects move elsewhere. Crop rotation is netic females developing on herbaceous (second-
most important for root feeding pests, many of ary) host plants.
which take several years to develop damaging Aphids
 Alimentary Canal and Digestion
A 111

Alimentary Canal and Digestion

james l. nation
University of Florida, Gainesville, FL, USA

Insects feed upon many different kinds of food,

including paper, wood, plant phloem and xylem
sap, plant leaves, roots and stems, animal tissues,
hair, wool, and vertebrate blood. The alimentary
canal (often simply called the gut in much of the
literature) evolved to accommodate such diverse
foods in a variety of morphological and physio-
logical ways. Thus, there is no typical insect ali-
mentary canal just as there is no typical insect.
Nevertheless, there are similarities in the structure
of the alimentary canal in all insects andnearly all
must digest some of the same complex molecules,
such as proteins, lipids, and carbohydrates.
In every insect alimentary canal three regions
can be identified morphologically and physiolog-
Alimentary Canal and Digestion, Figure 33 A
ically: the foregut or stomadeum, the midgut or
generalized drawing of the alimentary canal
mesenteron, and the hindgut or proctodeum
in a cockroach to show the major divisions of
(Fig.33). One or more of these regions may be
the c anal. Many variations occur in the overall
greatly reduced in size, or expanded in size,
structure of the alimentary canal in insects, and
depending upon the feeding behavior of the
this is not i ntended to suggest that the cockroach
insect. A cuticular layer, the intima, attached to
alimentary canal is typical of insects.
the epithelial cells, lines the fore- and hindgut
regions. The old intima is partially digested and with the food, lubricate the food, and may begin
the residue sloughed off into the gut and excreted some carbohydrate digestion. In some insects the
at each molt, and a new intima is secreted. The crop is not a noticeably modified part of the
midgut does not have anattached cuticular lin- foregut, but often the crop comes off the foregut as
ing, but may have a non-attached peritrophic a diverticulum. In other insects it is an enlarged
membrane that separates the food enclosed portion of the foregut. In opportunistic and pos-
within from the delicate surface of the midgut sibly irregular feeders such as praying mantids, the
cells. If a peritrophic membrane is present, it is crop composes more than half of the alimentary
often secreted several times each day. canal, apparently an evolutionary development to
store a large amount of food when available and
tide the mantid over periods when prey is scarce.
The Foregut Some insects (for example, many orthopterans)
regurgitate enzymes from the midgut into the
The buccal cavity (mouth), pharynx, esophagus, crop, and these enzymes, along with salivary secre-
crop, proventriculus and attached salivary glands tions, digest food in the crop. The digested food
comprise the foregut. Secretions from the salivary components still enter the midgut to be absorbed,
glands attached near the mouth are swallowed and there is no evidence that the crop ever secretes
112
A Alimentary Canal and Digestion

enzymes itself. The cuticular intima creates a bar- in nidi (nests). The regenerative cells grow into
rier even against the absorption of water from the mature epithelial cells to replace cells worn out or
crop. The proventriculus controls the entry of food those that disintegrate to release digestive
into the midgut in liquid feeders, but in many enzymes. Midgut cells may be completely replaced
insects it is modified into a grinding apparatus every few days in insects that live longer lives.
with hard, sclerotized ridges and spines, and heavy Gastric caeca, small finger or sac-like diverticula
musculature for breaking and tearing the food from the midgut, often arise at or near the origin
into smaller particles. of the midgut, but may be located at various points
along the midgut. The caeca appear to secrete
digestive enzymes and may be important in
The Midgut absorption of digested products.
The midgut does not have an attached cuticu-
The midgut in most, but not all, insects is the main lar lining on the surface of the cells, but midgut
site for digestion, absorption, and secretion of cells in the majority of insects secrete a thin mem-
digestive enzymes. The epithelium is a single layer brane composed of chitin and protein, the peri-
of cells, but several types of cells occur in some trophic membrane, that surrounds the food and
insects. The most common cells are tall, relatively shields the delicate microvilli of the midgut cells
narrow ones called columnar or primary cells by from contact with potentially rough and abrasive
various authors. They have extensive microscopic food particles. Although the peritrophic mem-
microvilli on the apical or lumen surface (Fig.34) brane is thin, varying from 0.13 m to about 0.4
and extensive invaginations of the basal cell mem- m thick, it also is thought to make it more diffi-
brane, features that greatly increase the surface cult for viruses, fungi, bacteria, and protozoans to
area on both sides of the cell over which secretion get to the surface of the midgut cells where they
and absorption occur. The columnar cells are the might be able to enter the cells and create an infec-
primary cells that secrete digestive enzymes and tion. Some insects produce several peritrophic
absorb digested products. In all insects that feed membranes per day, each encasing the one before
as adults and live for days or weeks, there are small it, perhaps increasing protection from random
regenerative cells distributed at the base of the breaks or punctures by larger food particles, and
columnar cells, or sometimes clustered together thus affording more protection for the midgut

Alimentary Canal and Digestion, Figure 34 A brush border of microvilli on the lumen surface of midgut
cells in a mole cricket.
 Alimentary Canal and Digestion
A 113

cells from possible fungi, parasites, viruses, and the epithelium cells and the gut lumen and seem to
bacteria ingested with the food. A peritrophic play a major role in amino acid absorption. The
membrane occurs in living representatives of some high midgut pH may provide plant feeding insects
of the earliest insects to evolve, and it is believed to some protection against tannins that are common
have evolved very early in a generalist scavenger in the food plants of phytophagous insects. Tan-
feeder in which protection of midgut microvillar nins can complex with an insects own enzymes
surfaces from food particles, sand, or other hard and proteins in the food, and may result in reduced
substances coincidentally ingested was likely to be digestion and absorption. Many details and the
important. A peritrophic membrane is present in precise metabolic components in the cell mem-
many insects that do not feed upon rough or solid brane that support and enable these secretory and
food, such as some blood feeders (but not all blood absorptive mechanisms remain to be elucidated,
feeders), and in adult lepidopterans that take but what is already known emphasizes the com-
flower and plant nectars. Although the peritrophic plexity of insect digestive functions.
membrane is not present in all groups of insects,
like other gut features, it has been conserved over
long evolutionary time, lending support to views The Hindgut
that it has multiple functions, especially protec-
tion from disease invaders and may even have The hindgut is not only a posterior extension of
properties that could bind toxicants and limit their the alimentary canal, but it also plays a major role
access to cells. in excretion through secretion of some substance
Absorption of digested food substances has into the lumen, and reabsorption of useful sub-
not been studied in most insects, but one mecha- stances such as ions, water and some nutrients
nism has been partially elucidated for absorption from the Malpighian tubule effluent. The Mal-
of amino acids derived from protein digestion in pighian tubules typically arise at the origin of the
larvae of Lepidoptera. Interspersed among the tall hindgut (but exceptions do occur) and pass rela-
columnar cells lining the midgut in larvae of Lepi- tively large volumes of an ultrafiltrate of hemo-
doptera (and some other groups of insects as well) lymph components minus proteins into the
are cells shaped much like a goblet and called, beginning of the hindgut. The cuticular lining on
appropriately enough, goblet cells. The apical cell hindgut cells is thinner and has larger pores than
membrane of the goblet cavity has metabolic the lining in the foregut, permitting reabsorption
machinery that uses energy derived from splitting of water, some ions, and useful metabolites that
ATP to push or pump protons (H+) into the goblet are returned to the hemolymph. In most terres-
cavity. A different set of machinery in the goblet cell trial insects, water conservation is vital to life, and
membrane, an antiporter mechanism, reabsorbs the hindgut must conserve the water that the Mal-
the protons and simultaneously secretes potassium pighian tubules flush into the hindgut. Waste
ions into the goblet cavity. The net result of the products such as undigested food material (cel-
secretion of potassium ions is that a strongly alka- lulose, for example, which most plant-feeding
line midgut (a midgut pH as high as pH 8 to about insects cannot digest and use), uric acid, and other
11) is produced, and a high voltage (up to 240 mV allelochemicals picked up from the food are con-
in some reports) is created between the gut lumen centrated in the rectum and eventually excreted.
(positive) and the interior of cells lining the gut. The hindgut secretes some molecules into the
The voltage created by the pump enables an absorp- lumen for excretion. Experimental evidence indi-
tive mechanism in membranes of columnar cells to cates that secretion and selective reabsorption
reabsorb K+ and amino acids from protein diges- helps regulate pH of the hemolymph in some
tion. Thus, potassium ions are recycled between insects. Specialized cells, the rectal papillae and
114
A Alimentary Canal and Digestion

rectal pad cells, in the rectum of many insects of the nutrient value of the food source. Some
have characteristic ultrastructure and physiologi- insects reflux enzyme secretions and partially
cal mechanisms typical of highly reabsorptive digested products by repeatedly sucking up and
cells. Water conservation by the rectum results in reinjecting the liquefied juices into the food.
the relatively dry frass or fecal pellets characteris- Refluxing mixes the secretions and fluids and
tic of many terrestrial insects. extends the effective life of the digestive enzymes,
The highest degree of specialization in the and is particularly effective when the food con-
hindgut occurs in those insects that digest cellu- tains a limiting boundary, such as the shell of a
lose, such as termites. In termites, the hindgut is seed or the cuticle of an insect that acts as a con-
usually divided into several chambers harboring tainer for the liquefying body contents.
either bacteria or protozoa that secrete all or part
of the cocktail of enzymes needed to digest cellu-
lose. Glucose, liberated from cellulose digestion, Carbohydrate Digestion
may be fermented by the resident microorgan-
isms, with the end products being short chain Starch and sucrose are the typical carbohydrates
fatty acids (principally acetic acid) that can be that insects digest from plant food, and glycogen
absorbed by the termite and used as an energy and various sugars are present in animal tissue
source. Some termites release methane, a green- eaten by carnivorous insects. Cellulose, the major
house gas, from the metabolic activities of their complex polysaccharide present in plant tissue,
microorganisms, but whether this is a significant cannot be digested by most insects. Carbohydrate
natural source of methane is a topic of debate by digestion begins with the action of -amylase, an
various scientists. enzyme present in the salivary gland secretions of
many insects. Amylase works best at slightly acid
pH, and hydrolyzes interior glucosidic linkages
Digestive Enzyme Secretion ofstarch and glycogen, resulting in a mixture of
shorter dextrins. In the midgut -glucosidase and
Midgut cells secrete and release digestive enzymes oligo-1, 6-glucosidase (isomaltase) digest smaller
in several ways. They may enclose digestive dextrins, releasing glucose. Many insects also have
enzymes in small vesicles surrounded by a mem- one or more - or -glycosidases that digest
brane and then release the enzymes into the ali- a broad range of small carbohydrates, such as
mentary canal by fusing the vesicle membrane maltose, sucrose, trehalose, melezitose, raffinose,
with the cell membrane. In some insects, parts of stachyose, melibiose, raffinose, and stachyose.
the cell (some of the microvilli) or the entire Some insects can secrete trehalase in the gut to
midgut cell may disintegrate and release enzymes digest trehalose, the principal blood sugar typi-
into the gut lumen. Of course, when the entire cell cally in high concentration in insects. -glucosidase,
breaks down, the cell must be repaired or replaced. -galactosidase, and -fructofuranosidase act
Replacement occurs through the growth of the upon various substrates to release simple sugars
regenerative cells. in the gut. An insect usually has only a few of
Extraoral digestion (digestion outside the these carbohydrate digesting enzymes, depending
insect body) occurs in some insects, including upon the food it eats. For example, Apis mellifera
seed feeders and some predatory insects. By inject- honeybees have several -glucosidases or sucrases
ing enzymes from the salivary glands and midgut that act rapidly upon sucrose, usually the princi-
into the food source (animal or plant material) pal carbohydrate in the nectar taken by honey-
and then sucking back the liquefied digestion bees. They utilize the resulting glucose and
products, insects can utilize very high percentages fructose for an immediate energy source and for
 Alimentary Canal and Digestion
A 115

making honey. Termites, some beetles, a few cock- including insects, get their amino acids from
roaches, and woodwasps in the family Siricidae digestion of dietary proteins. Within insects as a
digest cellulose with aid (usually) from fungi, bac- group, there are several different types of protein
teria, or protozoa, which produce some or all of digesting enzymes, some of which act at acid pH,
the complement of three enzymes necessary for others at slightly alkaline pH, and some at highly
cellulose digestion. alkaline pH. Usually a particular species will have
several different proteinases, but no insect is
known to have both an acid-effective proteinase
Lipid Digestion and an alkaline-effective proteinase. The pH of
the alimentary canal is important to the action
The major storage forms of lipids (fats) in both of any digestive enzyme, and no insect is known
plants and insects are triacylglycerols, esters of to have an alimentary canal that is strongly acid
fatty acids with glycerol. Midgut cells, and in some in one part and strongly alkaline in another
cases symbionts, secrete lipases, which are enzymes part.
that hydrolyze triacylglycerols and release fatty Proteinases are classified broadly as serine,
acids and glycerol. Amino acids, proteins, and fatty cysteine, aspartic acid, and metallo-proteinases
acylamino complexes act as emulsifiers in the depending upon the amino acid or metal at the
midgut of some insects facilitating the digestion of active site of the enzyme. Trypsin and chymotrypsin
fats. The glycocalyx layer, a viscous protein and are two endoproteinases with alkaline pH optima
carbohydrate complex that often lies on the sur- (about pH 8) that are common in many insects and
face of the microvilli, probably aid in emulsifying which attack large proteins internally at the linkage
fats and in promoting contact between lipases and between certain amino acid, thus breaking the pro-
triacylglycerols. Fatty acids released from triacylg- tein into smaller polypeptides. Most insects appear
lycerols are resynthesized into the insects own to have several types of exopeptidases that remove
triacylglycerols and stored in fat body cells. Imma- the terminal amino acid from a protein or peptide
ture insects typically store relatively large amounts chain. Thus, through the concerted action of both
of triacylglycerols, and use some of the released types of digestive enzymes, a protein can be com-
fatty acids during pupation and for egg develop- pletely digested with release of its component amino
ment. Some insects, for example Orthoptera, Lepi- acids. Cysteine- and aspartic acid-proteinases have
doptera, and some aphids, mobilized fatty acids mildly acid pH optima, and are called cathepsins by
rapidly enough to use fatty acid metabolism to some authors. All members of a taxonomic group
support flight, but other groups such as Diptera may not have the same type of proteinases. Many
and Hymenoptera cannot release fatty acids from beetles have cysteine proteinases most active at
the fat body and transport them to the flight mus- slightly acid pH, while some scarabeid beetles
cles rapidly, and so they only use carbohydrates for secrete serine-proteinases that act at the high
flight energy. They still can use lipids during pupa- midgut pH typical of these insects, and they have
tion, and for other metabolic processes that occur no detectable cysteine-proteinases. Lepidoptera
more slowly. typically secrete trypsin-like enzymes active at
alkaline pH.
One defense mechanism that has evolved
Protein Digestion against herbivory in many plants is the presence of
proteinase inhibitors, some of which inhibit serine
All animals must have a pool of amino acids proteinases while others act upon cysteine pro-
available for synthesis into proteins, and for teinases. Experimentally, it has been shown that
repair of tissues and organs. Most animals, some insects secrete multiple trypsin enzymes
116
A Alimentary Canal and Digestion

(isozymes of trypsin) and others just secrete larger Gut pH

amounts of the same few isozymes after consum-
ing a trypsin inhibitor. This counter action by the The pH of the alimentary canal is highly variable
insect probably allows some protein digestion to in different species of insects. The pH of a gut seg-
escape ingested inhibitors, but transgenic plants ment influences the action of enzymes secreted
designed to have proteinase inhibitors have been into or carried with the food into the gut, influ-
tested and proven to have adverse effects upon the ences solubility and toxicity of toxins and plant
growth of some insects. allelochemicals, and may alter the population of
gut microorganisms. In most insects, the crop has
little or no presence of buffering agents and tends
Absorption of Digested Products to be slightly acidic, a factor favoring carbohydrate
digesting enzymes. Larvae of Lepidoptera and Tri-
Few details are known about the absorption of choptera tend to have a very high midgut pH,
digested products by insects. In many verte- varying from about 8 to 10, promoted by goblet
brates, glucose absorption from the alimentary cells that secrete potassium and bicarbonate into
canal requires an active mechanism involving the lumen of the midgut. They have protein digest-
ATP to supply the energy. In those insect that ing enzymes that are favored by the high pH, and
have been studied, glucose from digestion of car- the high pH may afford some protection from tan-
bohydrates is rapidly absorbed passively by a pro- nins and other allelochemicals that they ingest
cess known as facilitated diffusion, and with their plant food.
involvement of ATP is not necessary. Fat body
cells on the hemolymph side of the gut rapidly
synthesize absorbed glucose into the disaccharide Illustrative Examples of Diversity
trehalose, keeping the hemolymph concentration in Food, Form and Function of the
of glucose low in most insects. Consequently, Alimentary Canal
even low concentrations of glucose in the gut
have a favorable diffusion pathway to the hemo- The following examples are not intended to be a
lymph and continue to be absorbed passively. In comprehensive review of foods, and alimentary
larvae of a few lepidopterans that have been canal structure and physiology, but will merely
carefully studied (Manduca sexta, Philosamia highlight interesting diversity.
cynthia, Bombyx mori), amino acids are actively Opportunistic feeders may have evolved modi-
absorbed by transport proteins in the apical fications to capture and store food when available,
membranes of midgut columnar cells. Energy and thus survive lean periods when food is not avail-
for absorption comes from the high K+ concen- able. For example, the foregut of the praying mantis,
tration in the gut lumen and high transepithelial Tenodora sinensis, is long and wide, and occupies
potential created by the proton-ATPase pump nearly the entire length of the body, apparently an
active in midgut goblet cells. The transport pro- adaptation for storage of prey when it can be cap-
teins in these membranes show strong specificity tured. The midgut, eight gastric caeca, and hindgut
for particular amino acids, and transport sys- are compressed into the last three abdominal seg-
tems for at least six different amino acids are ments. Probably much of the digestion occurs in
known, and transport systems for other amino theposterior part of the crop with enzymes passed
acids probably will be discovered. In the Colo- forward from the small midgut.
rado potato beetle, Leptinotarsa decemlineata, Considering the universal presence of cellu-
transport proteins for leucine and tyrosine have lose in plant tissues, relatively few insects evolved
been demonstrated in midgut tissue. the ability to use cellulose as a source of nutrients.
 Alimentary Canal and Digestion
A 117

Termites, some beetles, a few hymenopterans, and protein poor. Fungi growing in the dead wood and
a few cockroaches do use cellulose as a carbohy- ingested by the larvae may provide additional
drate source. The hindgut of termites is highly spe- nutrients and/or enzymes for digesting the wood.
cialized for housing gut microbiota that provide Hemiptera take xylem or phloem sap, both of
the cellulase enzymes needed to digest cellulose, which are poor in amino acids and protein, but
although there is some evidence that certain ter- usually rich in sucrose (150 to more than 700 mM).
mites may be able to produce some or all of the They typically excrete a copious, dilute fluid, and
several enzymes necessary to completely digest in some, such as aphids, the fluid contains so much
cellulose. Gut variation exists among the castes in a sugar that it is called honeydew. They have to
colony; for example, soldiers in the family Rhinot- ingest large volumes of fluid to get the amino acids,
ermitidae are fed liquid food by the worker caste, and then they have to get rid of the excess water
and do not have to digest cellulose so they have and sucrose. A characteristic evolutionary feature
reduced gut structure. The workers are responsible of the gut in Hemiptera is the filter chamber in
for colony construction and nutrition, and they which a loop of the hindgut is in direct contact
have highly evolved hindgut chambers to hold var- with part of the foregut and a great deal of the
ious types of microbiota. Termites hatch without ingested fluid diffuses directly into the hindgut
their gut microbiota, and lose most of their gut from the foregut without passing through the
symbionts at each molt, but they become reinfested midgut. This, of course, causes loss of some
by feeding upon fluid and excreta from older amino acids and other components that may be
nymphs. Termites in the family Termitidae have needed, but water and sucrose, both of which are
symbiotic bacteria in the hindgut, while termites in in excess of needs, are the major components lost.
some other families have flagellate protozoans as The filter chamber is able to concentrate gut fluid
well as bacteria in a multi-compartmented hindgut, up to 10-fold in some xylem feeders (Cicadoidea
and they get some or all of their cellulase(s) from and Cercopoidea), but only about 2.5-fold in
their symbionts. Some termites, the Macrotermi- members of the Cicadelloidea, which are phloem
tinae, cultivate fungus gardens in their under- feeders. Xylem feeders probably need to concen-
ground nests and get their cellulases from the trate xylem fluids more because of the lower amino
conidiophores of the fungus. Symbionts in the acid content (310 mM amino acids per liter in
hindgut of some termites can capture atmospheric xylem fluid) than do phloem feeders (1565 mM
nitrogen in an organic form, which is probably amino acids per liter in phloem fluid).
quite important to many termites because their Pre-oral digestion with enzymes secreted into
diet of wood is relatively low in proteins. Some the prey occurs in many of the predacious beetles.
fungus-growing termites convert some of the Seed feeders also employ pre-oral digestion by
protons (H+) and carbon dioxide from the initial injecting salivary secretions and possibly regurgi-
fermentation of glucose into methane (CH4), and tated midgut enzymes into the seed, allowing these
some investigators have suggested that termites are to liquefy part of the seed, and then sucking the
a significant environmental source of methane, a nutrients and enzymes back. Pre-oral digesters
greenhouse gas. often reflux the liquefied contents by repeatedly
Larvae of the woodwasp (Hymenoptera, imbibing and then reinjecting the mixture of
Symphyta, Siricidae, genus Sirex) acquire cellulase enzymes and digested nutrients into the seed.
and xylanase from fungi ingested with the wood Refluxing likely conserves enzymes longer, gives
on which they feed. Larvae of cerambycid beetles them more opportunity to function, and allows
and of some other beetles feed upon wood in the insects to use more of their potential food.
down or dying trees; they generally have long life In honeybees and some other related
cycles because wood is so nutrient poor, especially hymenopterans, the midgut is closed off from the
118
A Alimentary System

hindgut by a plug of cellular tissue during larval midgut so that digestion can begin. Feeding is
development, and any food that cannot be nearly continuous when plenty of food is avail-
digested and absorbed into the body must remain able, and larvae may ingest more than their body
in the midgut. Just before pupation the connec- weight in food daily. Food moves rapidly through
tion between midgut and hindgut is opened, and the relatively straight gut and frass droppings are
accumulated undigested residue, such as the frequent in phytophagous caterpillars. Because
shells of pollen grains, is excreted into the cell. the larval and adult forms of Lepidoptera have
Adult honeybees clean the cell and the larva very different life histories and food habits, the
pupates inside the cell. adult gut is quite different from that of the larva.
Nectar taken by male and female mosquitoes Many adult Lepidoptera feed only upon nectar,
is stored in a large, sac-like crop that is a diver- which is stored in the crop and slowly released
ticulum from the foregut, but blood meals taken into the midgut for digestion to simple sugars.
by the females are passed directly into the midgut Some adult Lepidoptera have vestigial mouth-
for the beginning of digestion. The midgut is dif- parts and do not feed at all; they survive and
ferentiated functionally into an anterior and a (females) produce eggs at the expense of body
posterior region. The anterior part secretes carbo- substance, and they generally live only a few
hydrate digesting enzymes, and nectar compo- days. An unusual food utilized by Tineola bissel-
nents are digested as fluid from the crop and is liella larvae (clothes moth) is wool, and larvae
passed into the anterior midgut. This arrange- have a very strong reducing action in the midgut
ment keeps possible trypsin inhibitors that may that breaks disulfide bonds between adjacent
be present in nectar away from the site of protein loops of the proteins, causing the wool proteins
digestion, which occurs in the posterior midgut. to lose their three-dimensional shape and unfold.
Simple sugars resulting from digestion, or those This allows more access for protein digesting
already in the nectar, are absorbed in the anterior enzymes.
midgut. The posterior midgut cells secrete trypsin-
like enzymes and protein (blood) digestion and
absorption occur in the posterior midgut. The References
posterior midgut cells, more so than anterior
midgut cells, have extensive microvilli and basal Chapman RF (1998) The insects: structure and function.
infoldings characteristic of secretion and absorp- Cambridge University Press, Cambridge, UK, 770 pp
Klowden MJ (2002) Physiological systems in insects. Aca-
tive processes. The midgut cells in this region get demic Press, New York, NY, 415 pp
stretched by the large volume of blood that a mos- Nation JL (2002) Insect physiology and biochemistry. CRC
quito takes if it is allowed to feed to repletion. Press, Boca Raton, FL, 485 pp
Consequently, the cells have several types of con-
necting structures (desmosomes) between cells to
help hold them together and prevent excessive Alimentary System
leaking of materials in or out between cells while
they are stretched. The alimentary system (canal) is a system of tubu-
Larvae of Lepidoptera have a very short lar structures that takes in food at the mouth,
foregut, a large, long, relatively straight midgut, stores the food, fosters digestion and absorption of
and a short hindgut. There is no storage or diges- nutrients, and allows excretion of waste materials
tion in the short, nearly vestigial foregut. Nearly from the rectum. It is conveniently divided into
all lepidopterous larvae are phytophagous feed- the foregut, midgut, and hindgut (Fig.35).
ers, and the gut modifications appear to be an Alimentary Canal and Digestion
adaptation to pass food quickly into the long Foregut
 Allegheny Mound Ant, Formica exsectoides (Hymenoptera: Formicidae)
A 119

foregut midgut hindgut

gastric
esophagus crop ventriculus pylorus ileum rectum
caecum
pharynx

buccal anus
cavity proventriculus
mouth Malpighian tubule

Alimentary System , Figure 35 Generalized insect alimentary system (adapted from Chapman, The
insects: structure and function).

Midgut likely have other effects as well, but they are still
Hindgut relatively unknown (contrast with allatostatins).
Juvenile Hormone

Alinotum
Alleculidae
The notal plate of the meso- or metathorax in a
pterygote insect. A family of beetles (order Coleoptera). They com-
Thorax of Hexapods monly are known as comb-clawed beetles.
Beetles
Alitrunk
The portion of the thorax to which the wings are Allegheny Mound Ant, Formica
attached. exsectoides (Hymenoptera:
Thorax of Hexapods Formicidae)

gregory s. paulson
Allatostatins Shippensburg University, Shippensburg, PA, USA

These are neuropeptides from neural and non- The Allegheny mound ant, Formica exsectoides
neural tissues that affect the corpora allata, inhib- Forel, is a common mound-building ant of the
iting production of juvenile hormone. They likely northeastern and central United States. Workers
have other effects as well, but they are still rela- are approximately 3/8 inch long (1 cm) with a
tively unknown (contrast with allatotropins). reddish-tan head and thorax, and a dark brown
Juvenile Hormone abdomen. In suitable habitat, F. exsectoides will
form dense populations, their presence easily dis-
cernible due to conspicuous mound-type nests
Allatotropins which can be as large as 15 feet (4.6 m) in diame-
ter and 4 feet (1.2 m) high. At one site near
These are neuropeptides from neural and non- Altoona, Pennsylvania, researchers counted more
neural tissues that stimulate the corpora allata, than 30 large mounds per acre. Despite the con-
resulting in synthesis of juvenile hormone. They spicuous nature of F. exsectoides nests and its wide
120
A Allegheny Mound Ant, Formica exsectoides (Hymenoptera: Formicidae)

geographic range, relatively few papers concern- Habitat has a significant effect on physical char-
ing this species have been published since H.C. acteristics of F. exsectoides nests. Forest nests tend to
McCooks first paper in 1877. be significantly larger in height, width, length, nest
Nests tend to be clustered in the habitat footprint and volume than nests in meadows. In
(Fig.36). Nests in each cluster often will share for- general, the nests are round, but it is not uncommon
aging trails and resources. Although there is little to find elongated nests that are orientated to the sun.
aggression between workers from different nests or The shape of a nest and its orientation may help the
nest clusters, the workers still show fidelity to a ants to maintain a relatively constant internal tem-
home nest. Nests of F. exsectoides have multiple perature and relative humidity.
queens (polygynous) although there is tremendous
variation in the number of queens per mound.
Over 1,400 queens were reported in one mound,
but that is probably an anomaly. Most mounds
References
probably contain fewer than 20 queens. Due to the
Andrews EA (1925) Growth of ant mounds. Psyche
large number of queens, the reproductive output of 32:7587
a nest can be prodigious resulting in large numbers Andrews EA (1927) Ant mounds as to temperature and sun-
of workers in a colony. More than 250,000 workers shine. J Morphol Physiol 44:120
have been found in some nests. Reproductive forms Bristow CM, Cappaert D, Campbell NJ, Heise A (1992) Nest
structure and colony cycle of the Allegheny mound ant,
(alates) are present in the nests from mid-summer Formica exsectoides. Forel (Hymenoptera: Formicidae)
until early fall. Activity of the ants is related to Insectes Sociaux 39:385402
ambient conditions but, in general, workers are Bristow CM, Yanity E (1999) Seasonal response of workers of
the Allegheny mound ant, Formica exsectoides.
active from late March until November. Formica
(Hymenoptera: Formicidae) to artificial honeydews of
exsectoides are generalist predators, scavengers and varying nutritional content. Great Lakes Entomol
collect honeydew from symbiotic hemipterans. 32:1527

Allegheny Mound Ant, Formica Exsectoides (Hymenoptera: Formicidae), Figure 36 Three large nest
mounds of Formica exsectoides in a Pennsylvania forest clearing.
 Allelochemicals
A 121

McCook HC (1877) Mound-making ants of the Alleghenies, of years, plants have done everything possible to
their architecture and habits. Trans Entomol Soc Am
make life miserable for insects. On the other hand,
6:253296
Rowe HC, Bristow CM (1999) Sex ratio and sexual dimor- insects have returned the favor many times over. In
phism in Formica exsectoides, the Allegheny mound ant recent geological time, plants and insects have
(Hymenoptera: Formicidae). Great Lakes Entomol changed their spots (plant-feeding strategies),
32:207218
resulting in an incredible point-counterpoint rela-
tionship of these organisms that is characterized by
some remarkable developments.
Allele As far as nutrients are concerned, different
kinds of plants (species) are fairly similar and can
One of two or more alternative forms of a gene at provide an insect herbivore with the basic nutri-
a particular locus. If more than two alleles exist, ents required for growth and development. These
the locus is said to exhibit multiple allelism. compounds (chemicals) are called primary com-
pounds because they are required for the insects
growth, development, and reproduction. All insects
Allelochemic require these compounds and in theory they
should be readily available from a wide variety of
A non-nutritional chemical produced by one plant species. But most species of insects, rather
species (often a plant) that affects the growth, than feeding on many different kinds of plants,
health, or behavior of another species (often an limit their plant menu to a relatively small number
herbivore). of plant species (monophagy), most of which are
Allelochemicals related. Significantly, the limited preferences that
insects have for their food plant species are due to
non-nutritive compounds that usually vary from
Allelochemicals one plant group to another. These compounds are
not related to the primary compounds identified
murray s. blum with growth and development, and it is apparent
University of Georgia, Athens, GA, USA that these plant-derived compounds (allelochemi-
cals) generally have functions related to other spe-
For thousands of years insects and plants have been cies of organisms. These compounds are obviously
locked in a battle for which survival is the ultimate not primary compounds but rather secondary
prize. For insects, plants constitute food sources for compounds (non-nutritive) whose manufacture
growth and development, and in some cases, sites has been described as secondary metabolism.
for reproduction. On the other hand, plants attempt Indeed, these allelochemicals appear to be respon-
to counter insects feeding on their tissues (her- sible for both the associations and non-associations
bivory) so that their own vigorous growth and that insects have with specific groups of plant spe-
development will occur and lead to reproductive cies. In essence, it would be no exaggeration to state
success. The consequences of this warfare are great that the host-plant preferences of insects really
and for humankind the outcomes of these battles reflect the ability of an insect species to either tol-
may be of major economic significance in terms of erate, or be repelled by, an allelochemical. Alle-
the production of various foods. The welfare of lochemicals are not mysterious compounds but
various human populations can be threatened if rather are a very important part of the everyday
hordes of ravenous insects consume specific crops world, especially in terms of human food prefer-
that are the mainstays of these populations. But ences. In a sense, the strong food preferences
plants do not take this lying down. Over thousands exhibited by insects are not so different from those
122
A Allelochemicals

of humans, with one striking exception. Many icotine in the leaves before they are ten years old.
n
insect species are locked in to specific food plants, Nitrogen-containing compounds (alkaloids) pro-
and these insects will reject a foreign plant species duced by opium poppies are powerful repellents
and die in the absence of their normal food plant. for a wide range of insect species, and there is no
On the other hand, there is little evidence that doubt that compounds such as morphine and her-
human beings will subject themselves to starvation oin, which are powerful human narcotics, were
if their favorite foods are not readily available. evolved to deter herbivores rather than to func-
tion as narcotics for humans.
Alkaloids such as nicotine have been adapted
A World of Allelochemicals to function as insecticides, and a variety of plant
products such as derris, rotenone, ryania, and
Fruits and vegetables possess characteristic odors sabadilla are also used as insecticides in different
and tastes that create desire (preference) for these cultures. In some cases, allelochemicals such as
foods. Significantly, these tastes and smells are prunasin in cherry leaves cause poisoning in
notidentified with the primary compounds respon- livestock. Not to be outdone, humans have fre-
sible for plant growth and development, such as quently utilized the alkaloid strychnine to murder
sugars, fats, and proteins. Therefore, the plant has people. However, it would be a mistake to lose
invested in producing a variety of chemicals that track of the fact that, human abuses notwithstand-
will not help it grow or reproduce. While an onion ing, these allelochemicals were evolved as plant
may possess a distinctive odor and taste for both protectants long before humans appeared. Obvi-
insects and humans (not necessarily the same odor ously, allelochemicals do not provide plants with
and taste for both), this fact hardly justifies the absolute protection against herbivores. Indeed,
onion spending its energy and resources to produce probably all plants containing allelochemicals
an onion fragrance. On the other hand, if the taste arefed upon by insects, and in many cases these
and odor of onions combine to make this vegetable herbivores are only found on a limited number of
distasteful and repellent to most plant-feeding host plant species. For example, monarch butterfly
insects, then these allelochemicals perform a very caterpillars are limited to the milkweed species.
vital function. In essence, it is generally believed Bark beetles limit their attacks to pines and related
that these secondary compounds are responsible conifers, developing in environments that are rich
for protecting plants from herbivores and possibly in toxic turpentines. These insects have breached
pathogens as well. A brief examination of some the chemical defenses of their hosts, and in so
well-characterized allelochemicals offers a means doing, they have captured specific kinds of food
of examining these compounds as agents of defense plants that are either repellent or highly toxic to
both as toxins and as repellents. most other species of insects. Guaranteed these
Oleander, which has a very limited number of forbidden fruits, these herbivores should have to
herbivores, is extremely toxic because of the pres- share their food resources with very limited num-
ence of allelochemicals that are somewhat related bers of competitors. Barring an ecological disaster
to cholesterol. The odor of the plant probably con- does not devastate the populations of their host
stitutes an early-warning system that makes poten- plant species, this specialization should have much
tial herbivores aware of the danger of feeding on to recommend it. On the other hand, many insect
this plant. The same can be said for the tobacco species choose a lifestyle which is characterized by
plant which, like oleander, does not have too many feeding on a variety of unrelated plant species.
insect herbivores. Leaves of the tobacco plant are Insects like the monarch butterfly and bark
quite toxic, but in some South American popula- beetles that are restricted to a limited number of
tions young children become addicted to the related plant species are referred to as specialists.
 Allelochemicals
A 123

These herbivores have become resistant to the grasshoppers, aphids, lacewings, beetles, wasps,
toxic effects of their host plant allelochemicals, butterflies and moths. In general, these insects are
and in many cases they appear to be completely brightly (= warningly) colored, a characteristic
immune to the plant toxins they ingest. In the case described as aposematic. Armed with the toxins
of monarch caterpillars feeding on milkweeds, it from their food plants, large insects such as bril-
has been demonstrated that these larvae actually liantly colored grasshoppers move very slowly, as
grow more rapidly on milkweed plants containing if to advertise their poisonous qualities to the
the highest concentration of toxins. world. Obviously the term toxic is relative, since
Indeed, allelochemical concentrations may these insects routinely sequester these allelochem-
begenerally quite high, often averaging 510% of icals during normal feeding. However, since these
the dry weight of the plant. By contrast, plant- specialists are physiologically adapted for ingest-
feeding generalists feed on a wide range of plant ing these compounds, their ability to tolerate these
species, often unrelated. However, in general, allelochemicals is really not surprising. On the
theseherbivores select plant species in which the other hand, non-adapted species (e.g., predators)
concentrations of allelochemicals are not too would certainly encounter toxic reactions if they
high, enabling them to process low levels of a ingested these toxic plant products.
widevariety of plant toxins. The fates of allelochemicals, which are usually
The immunity of specialists to the toxic effects present in mixtures, are not at all predictable after
of the allelochemicals in their diets demonstrates ingestion by an adapted herbivore. Although many
that for these insects these compounds can no lon- compounds are sequestered immediately after
ger be considered poisons. Surprisingly, the basis ingestion, others may be metabolized before being
for this important allelochemical resistance, which stored, or even eliminated after being metabolized.
has great economic significance, was only under- In other cases selected allelochemicals in a mixture
stood about thirty years ago. may be absorbed and sequestered whereas other
compounds in the mixture may be eliminated
immediately. An examination of the options for
Sequestration and its initially processing ingested allelochemicals
Consequences emphasizes the versatility of specialists in treating
the toxic compounds produced by their food
Insects such as the monarch butterfly store com- plants.
pounds in their tissues that render them unpalatable
to predators. These compounds, the cardenolides,
were ingested by the larvae from their milkweed food Sequestration of Insect Toxins by
plants, and retained in their bodies into the adult Vertebrates: A Significant
stage. The storage of these milkweed compounds is Allelochemical Phenomenon
called sequestration, and constitutes a widespread
phenomenon among specialists feeding on alle- It has become evident that the allelochemical rela-
lochemical-rich plants. In a sense, sequestration rep- tionship of insects and plants is paralleled by a
resents the insects success in utilizing the plants similar relationship of amphibians and insects. It is
chemical defenses for its own purposes. Indeed, now recognized that the sequestration of ingested
sequestration can be regarded as a form of detoxica- toxic insect compounds by vertebrates differs little
tion since potentially toxic compounds are removed from this phenomenon in insect herbivores and
from the circulation and stored in the tissues. plants. In essence, a variety of insect toxins is
Sequestration has been detected in at least sequestered by amphibians and these compounds
seven orders of insects including species of toxic have similar protective functions for frogs and
124
A Allelochemicals

insects (see Allelochemicals as phagostimulants). rocessing it.An insect species may utilize a vari-
p
Frogs exploit insect allomones (defensive com- ety of adaptive strategies for processing a single
pounds) as if they were animal allelochemicals, compound that is characteristic of the host plant
and it seems worthwhile to emphasize this congru- defense.
ency in examining the scope of allelochemistry.
Frogs in the genus Dendrobates contain mono-,
di-, and tricyclic alkaloids which are clearly of ant Immediate Allelochemical Excretion
origin. The alkaloids, termed pumiliotoxins, appear
to be products of ant species in the genera Brachy- Some insects essentially fail to absorb ingested
myrmex and Paretrechina and constitute the only allelochemicals from the gut. These compounds
known dietary source of alkaloids of these frogs, are excreted directly and are concentrated in
not unlike the specialist insects feeding on narrow the feces. A lymantriid moth larva that is a
plant diets enriched with allelochemicals. The same specialist on the coca plant, which is the source
phenomenon has been described for the myrmicine of the alkaloid cocaine, rapidly excretes this
ant Myrmicaria melanogaster which synthesizes ten compound with only traces being found in the
alkaloids. Some of these alkaloids have previously blood. However, cocaine may still have defen-
been identified in a dendrobatid frog and a toad. sive value for the larva as part of an oral regur-
Neurotoxic steroidal alkaloids, the batrachoto- gitate that is externalized when the larva is
xins, have been isolated from New Guinea birds in disturbed.
the genera Pitohui and Ifrita. These compounds are Three different species of moth larvae that
among the most toxic natural substances known, feed on tobacco plants rapidly excrete nicotine,
and they are not produced by captive birds, sug- a very toxic and reactive alkaloid. There is no
gesting a dietary source. Recently, the batrachotox- evidence that nicotine is absorbed from the gut
ins were identified in beetles in the genus Chloresine of any tobacco feeder, but as is the case for the
(Melyridae) which are normally fed on by the bird moth larva excreting cocaine, nicotine in oral or
species. Since the genus Chloresine is cosmopoli- anal exudates constitutes an excellent defensive
tan, it is the possible source of some of the avian compound.
alkaloids found in birds in different areas.
Vertebrate sequestration of alkaloids from
insects has only recently been explored. Clearly Allelochemical Metabolism
this chemical storage has a common denominator
with sequestration of alkaloids by insects (see Alle- Many insect specialists rapidly metabolize
lochemicals as pheromonal precursors) and should ingested allelochemicals which are then seques-
be examined as a paradigm of comparative physi- tered, or in some cases excreted. Nicotine, which
ology. Clearly, insects are pivotal to both systems, is both highly reactive and very toxic, is con-
either as food for vertebrates or food for insects, verted to a non-toxic metabolite called cotinine
with sequestration the major common feature. by both tobacco-feeding insects and those that
are not tobacco feeders. Since cotinine has virtu-
ally no toxicity to insects, it is probable that its
Initial Processing of production from nicotine constitutes true
Allelochemicals by Specialists detoxication.
Cabbage-feeding insects feed on plants
Once an adapted insect has ingested an alle- that are rich in sinigrin, a compound that yields
lochemical, a menu of options is available for a highly toxic mustard oil when metabolized.
 Allelochemicals
A 125

Although sinigrin can be sequestered without Selective Biomagnification of

generating the reactive mustard oil in a variety Allelochemicals in Tissues
of cabbage-feeding species, cabbage butterflies
(whites) actually break down sinigrin and seques- There is little indication that the profiles of insect-
ter the highly reactive mustard oil. For these stored allelochemicals in any way mirror those of
butterflies, the mustard oil is more suitable for their host plant. In a sense, each insect species treats
storage than sinigrin. ingested allelochemicals distinctively, so that a com-
Larvae of the tiger moth Seirarctia have pound totally excreted by one species may consti-
evolved a novel strategy for coping with the toxic tute the main sequestration product of another.
effects of MAM, a compound derived from cycasin The very toxic grasshopper Poekilocerus bufo-
which is a constituent in the cycad leaves upon nius sequesters only two of the cardenolides that it
which they feed. When larvae encounter MAM, ingests from its milkweed food plant. Similar
they convert it to cycasin which is absorbed through selectivity is shown by moth larvae (Syntomeida
the gut wall before being sequestered. Since the species) which sequester oleandrin, the main ste-
enzyme that produces cycasin or MAM is only roid found in the leaves of oleander. On the other
found in the gut, once cycasin crosses the gut wall hand, a variety of other insects feeding on olean-
into the blood prior to sequestration there is no der leaves do not sequester oleandrin.
chance of MAM being generated from cycasin. Similar unpredictability characterizes the
Many species of moths, butterflies, and sequestration of pyrrolizidine alkaloids by moth
grasshoppers feed on plant species that produce larvae. Tiger moths (Amphicallia species) seques-
extremely toxic compounds known as pyrroliz- ter the alkaloids crispatine and trichodesmine,
idine alkaloids. These alkaloids, present as mix- whereas the main alkaloid present is crosemper-
tures, are frequently sequestered by these ine. Another tiger moth (Tyria species) concen-
specialist insects and, in some cases, metabolized trates senecionine in its tissues in spite of the fact
plant compounds are the preferred storage forms. that this compound is a trace constituent in the
For example, larvae of the tiger moth (Tyria spe- leaves. Tyria is no less curious as a sequestrator
cies) feed on ragwort and primarily sequester because it stores jacobine, jacozine, and jacoline as
the alkaloid seneciphylline, although this com- minor constituents in adults, yet these three com-
pound is present in the plant as the N-oxide. pounds are major alkaloids in the leaves.
Conversely, the grasshoppers of the Zonocerus
species convert the ingested alkaloid monocro-
taline to its N-oxide before sequestering the The Diverse Functions of
compound. Captured Allelochemicals
Insects feeding on milkweed metabolize the
toxic cardenolides (steroids) produced by these While highly concentrated allelochemicals may
plants, converting them into compounds that constitute a major deterrent to non-adapted
can be readily sequestered. The milkweed bug insects, these compounds can represent a real
(Oncopeltus species) oxidizes cardenolides as a treasure trove for species for which these plant
mechanism for converting these steroids into products are non-toxic. Indeed, in the course of
compounds that can be efficiently sequestered. exploiting for their own protection compounds
Similarly, larvae of the monarch butterfly store that are repellent or toxic to most insect species,
metabolized cardenolides in tissues after oxidiz- specialists have gone beyond the point of simply
ing these compounds into suitable chemical being resistant to allelochemicals. In many cases, a
forms for sequestration. variety of specialist species have utilized the rich
126
A Allelochemicals

allelochemical pool that is available in order to association is typical of a variety of insect species
develop a menu of remarkable functions. and their bacterial symbiotes, then a multitude
of insect-bacterial relationships may require re-
evaluation of possible examples of insect seques-
Insect Sequestration of Bacterial tration of bacterial allelochemists.
Compounds and their Glandular Non-pathogenic bacteria are commonly housed
Secretion in insects and, in a sense, these prokaryotes are
sequestered by their insect hosts. Furthermore, if the
Prokaryotes (bacterial types) are almost every- bacteria synthesize toxic compounds which may be
where and their widespread association with externalized from a defensive gland (prothoracic
insects is certainly well established. But the bases glands of dytiscids), then the bacterial products may
for these diverse bacteria-insect relationships are, be regarded as bacterial allelochemicals that have
for the most part, terra incognita. However, very been sequestered. Indeed, bacterial compounds of
recent research suggests one very surprising func- symbiotic bacteria of insects clearly constitute an
tion for bacteria in insect glands. unrecognized group of allelochemicals.
All major types of metabolism evolved in
prokaryotes and the success of these organisms
was both cause and effect of changing environ- Additives in Defensive Glands
ments on earth. If these bacteria are sequestered in
insect secretory glands, their great metabolic abili- Milkweed bugs (Oncopeltus species) add cardeno-
ties could be utilized to biosynthesize bacterial lides, derived from their milkweed host plants, to
allelochemicals which could be used as potent their thoracic defensive gland secretion which
defensive compounds. This possibility appears to considerably enhances the deterrency of their
have been realized as a product of the virtual ubiq- secretion. Similarly, a warningly colored generalist,
uity of both insects and their biosynthetically ver- the lubber grasshopper (Romalea guttata) incor-
satile prokaryotes. porates a large number of allelochemicals derived
Predaceous diving beetles (Dytiscus species) from a variety of plant species into its thoracic
are distinguished by their ability to produce gland secretion. This grasshopper generally feeds
defensive steroids, some of which are novel ani- on plants with low concentrations of allelochemi-
mal products that are limited to species of diving cals, but if it is fed high concentrations of plants
beetles. Furthermore, insects do not synthesize with known repellents (e.g., onion), the odorous
cholesterol which in insects must be obtained secretion can be highly deterrent.
from exogenous sterols. However, it now appears Another toxic grasshopper, Poekilocerus bufo-
that the surprising steroidal versatility of dytisc- nius, utilizes allelochemicals as the mainstay of its
ids may reflect the biosynthetic elegance of bacte- defensive secretion. This aposematic (very warn-
ria rather than insects. ingly colored) insect sequesters two of six carde-
Adult diving beetles may contain concentra- nolides from its milkweed diet which are the major
tions of at least 10 bacterial species, mostly detected irritants in the secretion when it is sprayed at
in a variety of organs. Culturing individual bacte- adversaries. Utilization of allelochemicals as
rial species resulted in the identification of diverse defensive gland constituents is particularly pro-
steroids that had previously been characterized in nounced in the swallowtail larvae of Atrophaneura
the prothoracic defensive glands of the adults. The alcinous, which feed on leaves that are rich in toxic
steroid-rich secretions of these glands function as aristolochic acids. Seven aristolochic acids are
vertebrate deterrents that can cause emesis of fish sequestered by the larvae and all are transferred
that swallow these beetles. If the dytiscid-bacterial tothe defensive gland in the head. The acids are
 Allelochemicals
A 127

concentrated in the gland and are the major deter- Allelochemicals as Inhibitors of Toxin
rents for birds. Production

Some plant toxins are present in plants in an

Regurgitation and Defecation of inactive form only to be converted to toxic
Allelochemicals compounds after ingestion by herbivores. This is
particularly true for many cyanogens (cyanide-
The intestines of stimulated grasshoppers can dis- containing toxins) that generate cyanide when
charge ingested plant products which may serve as the leaf surface is broken as would occur with a
repellents for predators. Regurgitated allelochem- plant feeder. It now appears that cyanogenesis
icals can effectively repel ants, as is the case for (producing cyanide) in damaged leaves may be
anal discharges from the hind gut. When tactually inhibited by allelochemicals that are compart-
stimulated, the milkweed bug, Oncopeltus fascia- mentally isolated from the cyanogens in the
tus, also defecates a solution containing repellent intact leaves.
allelochemicals. In this case, they are cardenolides Leaves of papaya, Carica papaya, contain two
ingested from their milkweed food plant. cyanogens that yield hydrogen cyanide after enzy-
matic attack. However, tannins, which are widely
distributed in plants, inhibit the release of cyanide
Allelochemicals as Tissue Colorants caused by the action of enzymes that attack the
cyanogens. Insects attacking plants containing
The cuticular (skin) coloration of many insects is cyanogens may have adapted tannins to prevent
diet-dependent and is highly adaptive since it cyanide release, a strategy that may be suitable for
enables the insect to respond in a positive way to other plant groups that yield toxic products after
its background color. Diet-induced changes may leaf damage.
result in the insect being cryptic (background
matching), whereas aposematic species can be
background contrasting. Background quality,
which is of great survival value, appears to be Allelochemicals as Pheromonal
controlled by allelochemicals that are widespread Precursors
in the diets of moths, butterflies and true bugs.
These insects are particularly sensitive to the Bark beetles (Scolytidae) in the genera Dendroc-
carotenoids (e.g., tomato red) that fortify their tonus and Ips convert the hydrocarbons pro-
host plants. duced by their pine hosts into alcohols that are
If the large white butterfly, Pieris brassicae, is utilized as either aggregation or sex pheromones
reared on its normal diet of cabbage leaves, the (communication compounds) by the attacking
pupae are green and contrast with their back- beetles. Similarly, butterflies in the family
ground. This toxic insect contains high concentra- Nymphalidae and moths in the family Arctiidae
tions of carotenoids, and the carotenoid lutein is convert pyrrolizidine alkaloids (PAs) into sex
concentrated in the cuticle. On the other hand, if pheromones that are especially critical during
these insects are reared on an artificial diet lacking courtship. The PAs may be collected from dam-
carotenoids, they possess a turquoise-blue color- aged plants by males to be transformed into
ation and exhibit no response to background. In sexual pheromones that constitute the key to
the absence of carotenoids, these insects are quite reproductive success. For these males, the alle-
conspicuous on their background and could be lochemicals (PAs) are identified with reproduc-
readily detected by predators. tive fitness.
128
A Allelochemicals

Allelochemicals as Structural Paint Beetle larvae in the genus Chrysomela also

convert a toxic allelochemical into a metabolite
Some insects actually paint structures with with considerable importance in growth and
ingested compounds possessing considerable bio- development. These larvae feed on leaves of wil-
logical activity. Larvae of the parsnip webworm, low (Salix), a rich source of salicin, a toxic metab-
Depressaria pastinacella, apply ingested alle- olite. Metabolism of salicin yields a very effective
lochemicals to silk-webbed flowers that serve as defensive compound that is sequestered by the
housing units. The applied compounds are derived larvae in defensive glands. In addition, this metab-
from wild parsnip, a food plant that is rich in olism generates enough glucose to account for
highly toxic furanocoumarins. These compounds about one-third of the daily caloric requirements
are sequestered in the silk glands before being of the larvae. Salicin should be regarded as an alle-
applied to the flowers in which the larvae reside. lochemical nutrient.
Since the larvae are quite sensitive to ultraviolet
light, the presence of UV-absorbing furanocou-
marins on their silken housing is highly adaptive. Allelochemicals as Agents of Sexual
In addition, because these allelochemicals possess Development
pronounced antimicrobial activity against bacte-
ria and fungi, their presence on the silk can act as Tiger moths in the genus Creatonotus feed on
a major barrier to pathogens. plant species that produce high concentrations of
pyrrolizidine alkaloids (PAs). These compounds
are converted to sex pheromones by the males.
Allelochemicals as Metabolites in Additionally, these allelochemicals control the
Primary Metabolic Pathways development of important secondary sexual char-
acters called coremata. The coremata are eversible
Some specialist herbivores metabolize the charac- andraconial (male) organs that are the source of
teristic allelochemicals in their host plants into the volatile sex pheromones of the males, and their
compounds that are of major significance in degree of development is controlled by the amount
growth and development. In essence, these spe- of PAs ingested by the developing larvae. In effect,
cialists exploit their food plants by utilizing not PAs are functioning as male hormones that regu-
only their primary nutrients for growth and devel- late both sex pheromone production and develop-
opment, but their allelochemicals as well. ment of the coremata.
Larvae of the bruchid beetle, Carydes brasil-
iensis, develop exclusively on seeds of a legume
(pea family) that contains canavanine, a foreign Allelochemical Discharge from Non-
amino acid related to arginine. Canavanine is glandular Reservoirs
highly toxic when incorporated into proteins by
non-adapted herbivores. On the other hand, lar- Some insects sequester ingested allelochemicals in
vae of C. brasiliensis metabolize canavanine into non-glandular reservoirs that can be evacuated
products of great metabolic significance. Large upon demand. Gregarious larvae of the European
amounts of ammonia are generated for fixation pine sawfly, Neodiprion sertifer, sequester toxic tur-
into organic compounds, and an amino acid is pentine terpenes in foregut pouches. These pine-
produced from canavanine for ready metabolism. derived compounds can be discharged upon
Thus, the very toxic allelochemical of the legume demand to function as highly effective predator
has been thoroughly exploited by the beetle larvae deterrents. Similarly, lygaeids such as the milkweed
as a source for key nutrients. bug, Oncopeltus fasciatus, sequester cardenolides
 Allelochemicals
A 129

from their milkweed hosts in dorsolateral spaces alkaloid sources, the copulatory bonus ensures that
on the thorax and abdomen. Significantly, high these toxic allelochemicals will be available to protect
concentrations of cardenolides are stored in these both the female and her eggs. It is also very significant
spaces, resulting in a concentrated deterrent dis- that the resistance of the spermatozoa to the known
charge which repels potential predators. toxic effects of the pyrrolizine alkaloids enables the
copulatory bonus strategy to be highly adaptive.

Allelochemicals as Defensive Agents

ofEggs Allelochemicals as Synergists
forPheromones
Insects ingesting allelochemicals often utilize these
compounds as protectants for the next generation The intimate relationship of specialist insects and
of insects. These plant compounds may be seques- their food plants is exemplified by the turnip aphid,
tered in the eggs in order to provide a formidable Lipaphis erysimi, and its alarm pheromone. This
defense against predators and pathogens. The aphid is typical of many aphid species. Paired glands
insect embryo must be resistant to the toxic effects near the tip of the abdomen secrete an alarm phero-
of the allelochemicals that have been sequestered mone that causes both adults and larvae to disperse
in the reproductive system. For example, chry- and drop off of the food plant. The alarm phero-
somelid beetle adults feeding on willow and pop- mones synthesized by the aphids are key communi-
lar sequester the toxic allelochemical salicin which cations chemicals that enable these insects to
is used to fortify the eggs. Salicin has different abandon ship when threatened by a predator. Sur-
functions in the embryo and the larvae. For the prisingly, (E)-B-farnesene, the major alarm agent
embryo, salicin is a deterrent toxin which can kill for a large variety of aphid species, is only weakly
ants. For the young larvae, salicin is converted to active when secreted by the turnip aphid. However,
salicylaldehyde, a powerful repellent that is not the activity of this pheromonal secretion is increased
frequently encountered in insects. A wide variety appreciably by allelochemicals that act as powerful
of allelochemicals are sequestered in insect eggs synergists for the major alarm pheromone. These
which includes pyrrolizidine alkaloids, aristo- synergists are derived from typical food plant com-
lochic acids, cannabinoids, quinones, cardenolides pounds that have been modified by the aphids.
and mustard oils. It is evident that the females of a
large number of species have appropriated their
host-plant defenses (allelochemicals) for protec- Allelochemicals as Phagostimulants
tion of their eggs.
The close relationship of insect specialists and
their allelochemicals is further demonstrated by
Allelochemicals as a Copulatory Bonus some species of sawflies and chrysomelid beetles
which feed on very bitter food plants. Adults of
Females may obtain allelochemicals suitable for their the turnip sawfly, Athalia rosae, feed on the sur-
own protection and that of their eggs from the semi- face of a plant that is not a larval food plant. Com-
nal ejaculate. For example, males of ithomiine but- pounds in the leaf surface that are responsible for
terflies gather pyrrolizidine alkaloids (PAs) from their bitter taste are powerful phagostimulants for
flowers and decomposing foliage and about half of A. rosae. In addition, these bitter compounds are
the PAs are channeled to the spermatophore (sperm incorporated into the cuticle, thus providing these
packet) that is transferred to the female during copu- sawflies with a cuticular set of armor to protect
lation. Since the females are rarely found feeding on against aggressive predators.
130
A Allelochemicals

Similarly, species in three genera of chry- eridania, from a host of allelochemicals. Unrelated
somelid beetles utilize cucurbitacins, compounds plant compounds rapidly induce enzymatic in
found in their squash and pumpkin hosts, as creasesof 2 to 3-fold in larvae. Significantly, the rise
phagostimulants that are biomagnified in their in P-450 activity is immediate and proceeds rapidly
bodies. The beetles are rendered distasteful and, over much of its course during the first few hours.
as is the case for the sawflies, the allelochemicals These results strongly suggest that P-450 induction
possess dual roles that both induce ingestion is critical to allelochemical tolerance.
and promote sequestration of highly distasteful
compounds.
Allelochemicals as Allomonal Precursors

Allelochemicals as Inducers of In some cases, insects have produced powerful

Detoxifying Enzymes repellents from allelochemicals in their food plants
and have thus exploited the plants defensive chem-
Both generalist and specialist insects can encoun- istry in a very efficient way. Such a strategy is par-
ter a diversity of allelochemicals with varying ticularly adaptive because the insect has benefited
degrees of toxicity. For generalists this is particu- both nutritionally and defensively from feeding on
larly true since a generalist diet can sample a wide its host.
variety of plant species containing a large diversity Host plant exploitation is particularly pro-
of allelochemicals. On the other hand, specialists nounced in some chrysomelid beetle larvae in the
may encounter fewer allelochemicals but it is likely genera Chrysomela and Phratora. The larvae feed
that these compounds will be at high concentra- on willow and poplar leaves, both of which con-
tions. In the case of both feeding modes, it is tain salicin, a well known feeding deterrent for
obviously necessary to possess mechanisms for non-adapted species. The beetle larvae convert
blunting the toxic properties of the ingested allelo- salicin to salicylaldehyde and glucose, utilizing the
chemicals. Detoxication would appear to consti- former for defense and the latter for growth. For
tute the key process for neutralizing the toxicities these chrysomelid larvae, the conversion of salicin
of ingested allelochemicals. The enzymes chiefly to salicylaldehyde is doubly beneficial. Very little
identified with converting allelochemicals into energy is used to synthesize salicylaldehyde, com-
less toxic compounds are the mixed-function pared to what is required to produce other defen-
oxidases, particularly cytochrome P-450. sive compounds that must be totally synthesized.
Mixed-function oxidases metabolize fat-soluble Because salicylaldehyde is a far more effective
toxins into water-soluble ones that can be excreted. repellent than salicin, the beetle larvae receive a
The level of these enzymes may determine the toler- very important double bonus by converting the
ance of an insect for a particular allelochemical. allelochemical into a compound that can be read-
For a generalist ingesting a large diversity of ily stored and secreted from the defensive glands.
allelochemicals derived from many plant species,
the induction of a variety of these oxidases would
promote the possibility of detoxifying many kinds Allelochemicals as Communicative
of plant compounds. For a specialist, fewer oxidases Jamming Agents
at very high levels would enable the herbivore to
detoxify the very high concentrations of allelochem- In theory, plant species could reduce or eliminate
icals in its restricted food plants. herbivory if the plants generated volatile com-
Mixed-function oxidases play a key role in pounds identical to or similar to the pheromones
protecting the southern armyworm, Spodoptera utilized by herbivores as signals. If these signals
 Allelochemicals
A 131

were behaviorally disruptive, feeding could be commonly exploited plant compounds as key ele-
appreciably diminished, to say the least. ments in their phytochemical defenses.
The wild potato, Solanum berthaultii, has A compound commonly produced by conifers
effectively jammed the pheromonal alarm signal is a-pinene, which inhibits diverse microorganisms
of its potential aphid herbivore. (E)-B-farnesene, including the insect pathogen Bacillus thuringien-
an alarm pheromone of the aphid Myzus persicae, sis. Along with several related compounds, -pinene
is also produced by wild potatoes, resulting in reduces the infectivity of B. thuringiensis for larvae
repellency and dispersion of the aphids. In effect, of the Douglas fir tussock moth, Orgyia pseudot-
the potato has exploited the aphids herbivory by sugata. At concentrations approximating those
utilizing a highly disruptive compound that has found in fir needles, a-pinene increases the 50%
been evolved by aphids as a warning signal. lethal dose for B. thuringiensis by 700-fold.
A pathogenic fungus, Nomuraea rileyi, fre-
quently attacks lepidopterous (moth) larvae such
Quenchers of Phototoxic Allelochemicals as the corn earworm, Helicoverpa zea. However,
thepathogenicity to this larva can be reduced if the
Diverse plant species produce photo-activated moth ingests a tomato alkaloid, -tomatine. If the
compounds that are highly toxic to insects after larvae ingest -tomatine prior to exposure to fungal
digestion. In essence, these compounds generate conidia, it increases larval survivorship considerably.
highly toxic species of oxygen that attack key bio- The alkaloid is a further asset to H. zea because it is
chemicals such as nucleic acids. On the other quite toxic to larval parasites of the corn earworm.
hand, if the herbivore simultaneously ingests The pathogenicity of viral pathogens of H. zea
allelochemicals that are effective quenchers of can also be compromised by host plant allelochem-
toxic oxygen species along with the phototoxins, icals. Chlorogenic acid, a common plant compound,
then survival and prosperity are possible. The is oxidized to chlorogenoquinone by plant enzymes,
availability of these allelochemical antioxidants and this oxidation product binds to a nuclear poly-
has enabled some insect species to utilize food hedrosis virus. Binding to this baculovirus results in
plants that are forbidden fruits for most a reduction in digestibility and a decrease in infec-
herbivores. tivity. Furthermore, it appears that the liberation of
Larvae of the tobacco hornworm feed on a infective virons in the midgut, which is a require-
variety of plant species that contain the phototoxin ment for successful infection, is impaired by the
-terthienyl, a constituent of many species of asters binding of chlorogenoquinone to the baculovirus.
(Asteraceae). However, the additional ingestion of
-carotene reduces mortality from 55% (controls)
to 3% (+carotene) during 48 h. -carotene, an Specialists and Generalists: Two
effective quencher of toxic oxygen species, is con- Selected Case Studies
centrated in the tissues of the larvae where it can
serve as a potent antioxidant for photoactivated Although specialists and generalists may be highly
toxins found in its food plant. efficient sequestrators, the storage characteristics of
both groups differ considerably. Some insights into
how these insects manipulate the allelochemicals in
Antibiotic Functions of Allelochemicals their diets have been provided by recent studies of
the fates of a variety of ingested plant chemicals. An
The demonstrated range of allelochemicals against analysis of these studies demonstrates that the par-
insect-associated viruses, fungi and bacteria ticulars of sequestration are, if nothing else, very
makes it probable that these arthropods have unpredictable.
132
A Allelochemicals

The Monarch Butterfly, Danaus plexippus in the gut fluid but high concentrations in the
hemolymph. However, before wing expansion in
The monarch is a specialist that feeds exclusively the newly developed adult, the cardenolide level
on different species of milkweeds. Milkweeds con- in the hemolymph is at its lowest, only to
tain steroids called cardenolides, which are some- increase to the highest level in any life stage.
what related to vertebrate hormones such as The presence of high levels of cardenolides in
testosterone. These compounds are toxic and the blood of the adult demonstrates that these
highly emetic, vomiting often following their compounds are not locked in tissues but rather are
ingestion by non-adapted species. circulating freely, possibly to be utilized upon
Polar (water soluble) cardenolides are seques- demand. The warningly colored (aposematic)
tered in the large volume of gut fluid possessed by adult monarch utilizes a defensive system based
the larvae. Sequestration is much more efficient on compounds that it did not ingest as an adult.
from plants with low level cardenolide concentra- Although the complexities of cardenolide seques-
tions than with high concentrations. Significantly tration in this species are evident, it is highly sig-
for the monarch, and not necessarily for other nificant to understand these ingested steroids are
milkweed feeders, it is the large volume of gut fluid an extraordinarily dynamic state.
that makes it possible to feed and develop on these
plants.
The cardenolide-rich gut fluid, which may The Lubber Grasshopper, Romalea
exceed one-third of the larvas total liquid volume, microptera (also known as R. guttata)
is withdrawn at pupation to become part of the
hemolymph (blood) pool, stored primarily under This large grasshopper found in the southeastern
the wings. Subsequently, the wing scales (bird United States is quite conspicuous because of it red,
predators beware), along with the hemolymph, black and yellow coloration. It is one of the most
become the richest sources of cardenolides in the aposematic (warningly colored) species in its habi-
body after being withdrawn from the gut fluid. The tat. This brightly colored grasshopper is especially
volume of gut fluid decreases before pupation only distinctive because it is a generalist that feeds on a
to increase again before pupal molting. Again, gut very wide range of plants belonging to a variety of
fluid diminishes during pupal development only to species. Lubber grasshopper is known to feed on
increase again in the new adult. The cardenolide- 104 plant species belonging to 38 families, many of
rich gut fluid is again converted to hemolymph which produce toxic allelochemicals. Both imma-
during adult development so that very little remains ture and mature grasshoppers are capable of caus-
to be lost when the newly developed adult evacu- ing emesis in predators such as lizards,demonstrating
ates accumulated waste products from its gut. that all stages of these insects are protected from at
The polar cardenolides in the gut fluid least some predatory vertebrates.
clearly are the source of the defensive com- Immature individuals of R. microptera produce
pounds manipulated by the monarch at all defensive compounds that cause emesis in both liz-
stages. The larval and pupal exuviate (cast skins) ard and bird predators. Additionally, mature and
eliminated after molting are an excretory form adult grasshoppers secrete defensive compounds
for the cardenolides, as is the case for these from paired tracheal (respiratory) glands in the
compounds in the wing scales. Excretion not- metathorax. These glands only become active near
withstanding, the ability of all life stages to the adult period and their secretion can be extremely
manipulate the cardenolide pool is quite pro- repellent to small predatory insects such as ants. At
nounced. This is evident in 2-day-old pupae least 50 compounds are produced by the defensive
that contain low concentrations of cardenolides glands, the secretions varying intraspecifically, so
 Allelochemicals
A 133

that components of females of the same age and mode in the presence of a preferred host plant is
population sometimes differ by 70-fold, with some not unreasonable, and can result in a secretion
compounds being absent in certain individuals. with a high a concentration of sequestered alle-
However, in addition to the compounds synthesized lochemicals as is characteristic of some specialist
in the metathoracic glands, a number of allelochem- insects.
icals are sequestered in these glands as a reflection Lubber grasshopper is quite unpalatable and
of an individual grasshoppers diet. Indeed, the emetic to a variety of vertebrates, especially birds.
composition of the metathoracic gland secretion of Diverse bird species have been demonstrated to
each grasshopper appears to be unlike that of any vomit after ingestion of these grasshoppers, pre-
other grasshopper, since no two of these generalist sumably as a consequence of Romalea-synthesized
grasshoppers have identical diets from which to toxins that fortify their bodies. While Romalea
sequester allelochemicals. For a predator, each lub- would appear to be completely defended against
ber secretion may be sufficiently distinctive to make birds, as is often the case, the best defense has been
it impossible to learn an olfactory pattern that overcome by a better offense. Shrikes, predatory
clearly identifies the prey as lubber grasshopper. birds that impale their insect prey on spines or even
Lubber grasshopper is unusual in being a barbed wire, capture lubber grasshoppers and
polyphagous (eating many plant species) insect impale them. However, the birds wait for about 48 h
species that sequesters allelochemicals. In general, before they remove and eat the grasshoppers.
monophagous (feeding on one group of plant spe- Though shrikes store all their food in this manner,
cies) and stenophagous (feeding on a limited range in all likelihood the emetic toxin(s) produced by
of plant species) insect herbivores characteristi- Romalea decomposes during the time the grass-
cally sequester plant compounds, but not general- hopper is impaled.
ist feeders. Furthermore, if R. microptera is
presented with a restricted diet (specialist feeding
mode), the number of compounds in the secre-
tions and their concentrations are reduced, and References
the relative composition of the secretion is mark-
edly different from that of field-collected grass- Blum MS (1981) Chemical defenses of arthropods.
Academic Press, New York, NY
hoppers. Significantly, if grasshoppers are presented Blum MS (1983) Detoxication, deactivation, and utilization
with only a single-host plant as a food source, they of plant compounds by insects. In: Hedin P (ed), Plant
frequently feed readily, sequestering host-plant resistance to insects. American Chemical Society,
Washington, DC, pp 265275
volatiles, and exhibit no immediate ill effects. Lub-
Bowers MD (1990) Recycling plant natural products for
bers feeding only on wild onion sequester a large insect defense. In: Evans DL, Schmidt JO (eds), Insect
number of onion volatiles which impart a strong defenses. Adaptive mechanisms and strategies of prey
onion odor to the secretion. The secretion is a and predators. State University of New York, Albany, NY,
pp 353386
powerful repellent to hungry ants and is consider- Evans DL, Schmidt JO (eds) Insect defenses. Adaptive mecha-
ably more active than the secretions of field- nisms and strategies of prey and predators. State Uni-
collected grasshoppers. Compounds in other versity of New York, Albany, NY, 482 pp
single-plant diets (e.g., catnip) produce secretions Gibson RW, Pickett JA (1983) Wild potato repels aphids by
release of aphid alarm pheromone. Nature 302:608609
that are similarly active. Pasteels JM, Gregoire JC, Rowell-Rahier M (1983) The chemical
The secretion of lubber grasshopper clearly ecology of defense in arthropods. Annu Rev Entomol
has both a dietary and an individual origin that 28:263289
Whitman DW (1988) Allelochemical interactions among
correlates with great variations in secretory com-
plants, herbivores, and their predators. In: Barbosa P,
ponents. The possibility that these grasshoppers Letourneau D (eds), Novel aspects of insect-plant inter-
can temporarily switch to a monophagous feeding actions. Wiley, New York, NY, pp 1164
134
A Allelopathy

Allelopathy Allomone
The ability of a plant species to produce substances A chemical that is released by one species that
that are toxic to certain other plants. Allelopathic influences the behavior or physiology of a differ-
chemicals may affect germination, growth or ent species. The organism releasing the substance
reproduction of plants. usually benefits. Allomones are a type of
semiochemical used in warning.
Chemical Ecology
Allens Rule
Among mammals and birds, individuals of a spe- Allopatric
cies occurring in colder climates tend to have
shorter appendages, and a correspondingly lower Having separate and mutually exclusive areas of
surface to volume ratio, than members of the same distribution (contrast with sympatric).
species living in warmer climates. This trend
results from the need to conserve heat in cold cli-
mates but to eliminate excess heat in hot climates. Allopatric Speciation
A variant of this is Bergmanns rule. These rules do
not apply to ectothermic animals such as insects. A mechanism of speciation resulting from geo-
Bergmanns Rule graphic separation of populations, particularly
Thermoregulation physical barriers such as mountains and oceans.
Speciation Processes Among Insects

Allochronic Speciation
Allophagic Speciation
A mechanism of speciation wherein new species
develop in the same place but are separated due to A mechanism of speciation wherein new species
their tendency to occur at different times. develop in the same place, but are separated by
Speciation Processes Among Insects their preference for different food.
Speciation Processes Among Insects
Allogenic Succession
Allozyme
A temporal succession of species that is driven by
processes from outside the community (contrast
Allozymes are a subset of isozymes. Allozymes are
with autogenic succession).
variants of enzymes representing different allelic
alternatives of the same locus.
Allometric Growth
A growth pattern in which different parts of an Almond Seed Wasp, Eurytoma
organism grow at defined rates. In some cases, the amygdali Enderlein
body parts remain proportional (isometric (Hymenoptera: Eurytomidae)
growth), in other cases they do not. Departure
from isometric growth is used to explain castes of nikos a. kouloussis
social insects, which may have disproportionately Aristotle University of Thessaloniki, Thessaloniki,
large heads, mandibles, etc. Greece
 Almond Seed Wasp, Eurytoma Amygdali Enderlein (Hymenoptera: Eurytomidae)
A 135

The almond seed wasp is a serious pest of almonds, the translucent nucellar tissue. After oviposition, the
Prunus amygdalus Batch, in several countries of female deposits onto the fruit surface a host-marking
southeastern Europe and the Middle East, and pheromone. This pheromone enables females to dis-
also in Armenia, Azerbaijan, and Georgia. The criminate between the infested and uninfested fruit,
adult female is 68 mm long and has a black head and to select the latter for oviposition. Thus, a uni-
with dark brown eyes. The thorax and the spindle- form distribution of eggs among available fruits is
shaped abdomen are shiny black. The tibiae and achieved, and an optimal use of the available fruit for
tarsi are light brown while the remaining parts of larval development. The newly hatched larva bores
the leg are black. The male is usually smaller than through the nucellus and the embryo sac to feed on
the female (46 mm long). The larva is whitish, the developing seed embryo. The larva attains full size
legless, tapering in both ends, curved and clearly in midsummer, and enters diapause within the seed
segmented. Its head is light brown and very small. integument of the destroyed almond, which usually
Its length when fully grown is about 6 mm. remains on the tree in a mummified condition.
Almond seed wasp is a univoltine species, with Owing to oviposition by the wasp certain
a small part of the population completing its life varieties suffer a heavy premature drop. In most
cycle in two or more years because of prolonged dia- varieties though, the main damage consists in
pause. The diapause terminates during the winter. theconsumption of the seed by the larvae. This
Pupation takes place inside the fruit in late winter to damage varies depending on the variety. Certain
early spring. Adults emerge after boring a circular soft-shelled varieties may lose up to 90% of their
exit hole through the hard pericarp with their man- crop. Others are nearly immune because by the
dibles. Shortly after adult emergence, virgin females time females emerge in spring their pericarp has
release a volatile sex pheromone to attract males for become too thick and endocarp too hard for the
mating. Within a few days they mate and the females ovipositor to penetrate. Though not a common
start ovipositing (Fig.37) into unripe, green almonds. practice, planting of resistant varieties might be
Using her long ovipositor, the female drills through an effective strategy against this pest.
the pericarp of unripe, green almonds and the integ- The pest can be controlled by collection
ument of the seed, and deposits a stalked egg within anddestruction of mummified fruits before adult

Almond Seed Wasp, Eurytoma Amygdali Enderlein (Hymenoptera: Eurytomidae), Figure 37 Female
Eurytoma amygdali ovipositing into an almond.
136
A Alpha Taxonomy

emergence in spring, which is an effective measure Beta Taxonomy

if applied in large areas by multiple growers. How- Gamma Taxonomy
ever, the method most commonly used is the appli-
cation of systemic insecticides against the neonate
larvae within the oviposited almonds. This strategy Alternate Host
is meant for varieties that do not suffer fruit drop
because of oviposition. Recent studies have indi- One of the hosts of a pathogen or insect where a
cated that a single spraying can be effective if applied portion of the life cycle occurs. Often this term is
when 1050% of the eggs have hatched. This per- used to refer to a weed host of a crop pest or
centage can be determined by dissecting sampled disease.
almonds under a binocular microscope. Estimates
of egg hatch can be obtained by knowing the time Alternation of Generations
the first adults emerge from infested almonds in
spring. This can be determined by following the exit Some insects undergo reproduction that involves
of adult wasps from infested almonds kept in cages alternation of sexual and asexual generations. Typ-
in the orchard, or by following the population of ically, females produce both males and females but
males with the use of sex pheromone traps contain- at some point females cease producing males and
ing live virgin females as lures. produce only females parthenogenetically. Later
generations then commence production of males
again, allowing sexual reproduction to occur before
References the parthenogenetic cycle begins again. This occurs
most often in Hymenoptera and Hemiptera.
Katsoyannos BI, Kouloussis NA, Bassiliou A (1992) Monitor- Aphids (Hemiptera: Aphididae)
ing populations of the almond seed wasp, Eurytoma Gall Wasps (Hymenoptera: Cynipidae)
amygdali, with sex pheromone traps and other means,
and optimal time of chemical control. Entomologia
Experimentalis et Applicata 62:916
Kouloussis NA, Katsoyannos BI (1991) Host discrimination
Altruism
and evidence for a host marking pheromone in Eury-
toma amygdali. Entomologia Experimentalis et Appli- Self destructive behavior that is performed for the
cata 58:165174 benefit of others; sacrifice.
Plaut HN (1971) On the biology of the adult of the almond
seed wasp, Eurytoma amygdali End. (Hym., Eurytomi-
dae) in Israel. Bull Entomol Res 61:275281
Plaut HN (1972) On the biology of the immature stages of the Alucitidae
almond wasp, Eurytoma amygdali End. (Hym., Euryto-
midae) in Israel. Bull Entomol Res 61:681687 A family of moths (order Lepidoptera). They com-
Tzanakakis ME, Papadopoulos NT, Katsoyannos BI, Drakos
monly are known as many-plumed moths.
GN, Manolakis E. Premature fruit drop caused by Eury-
toma amygdali (Hymenoptera: Eurytomidae) on three Many-Plumed Moths
almond varieties. J Econ Entomol 90:16351640 Butterflies and Moths

Alpha Taxonomy Alula

The identification of organisms, and particularly The expanded membrane at the base of the trail-
the description and naming of organisms (species) ing edge of the front wing.
new to science. Wings Of Insects
 Amber Insects: DNA Preserved?
A 137

Amazonian Primitive Ghost vertebrates that got stuck in the sticky exudate.
Moths (Lepidoptera: The hardened resin was preserved in the earth for
Neotheoridae) millions of years, especially in regions where it
was deposited in dense, wet sediments such as clay
john b. heppner or sand that formed in the bottom of an ancient
Florida State Collection of Arthropods, Gaines- lagoon or river delta. For thousands of years, peo-
ville, FL, USA ple have collected amber. Many people use amber
as a gem, but scientists find amber a magnificent
Amazonian primitive ghost moths, family way to identify ancient organisms.
Neotheoridae, are defined on the basis of a single Amber can be found in a variety of sites
species from the Amazonian area of southern around the world. The composition, color, clar-
Brazil, although two additional species have been ity, and other properties of amber vary accord-
discovered for the family recently. The family is ing to age, conditions of burial and type of tree
part of the superfamily Hepialoidea, in the that produced the resin. The oldest amber is
infraorder Exoporia. Adults medium size (38 mm from the Carboniferous (360285 million years
wingspan), with head roughened; haustellum ago, mya) and can be found in the United King-
short and vestigial mandibles present; labial palpi dom and in Montana in the USA. Permian
long, porrect and 3-segmented; maxillary palpi amber is 185145 million years old and found
very small and 2-segmented. Wing maculation is most often in Russia. Triassic amber (245215
dark and unicolorous. Biologies and larvae remain mya) can be found in Austria, and Jurassic
unknown. amber (215145 mya) is found in Denmark.
Cretaceous amber (65140 mya) is found in
many locations around the world and represents
References the time when dinosaurs reigned and flowering
plants evolved along with a variety of insects.
Kristensen NP (1978) A new familia of Hepialoidea from For example, the rich amber deposits in central
South America, with remarks on the phylogeny of New Jersey in the USA are from the Turonion
the subordo Exoporia (Lepidoptera). Entomologia
Germanica 4:272294
period of the Upper Cretaceous, about 92 mya.
Kristensen NP (1999) The homoneurons Glossata. In: Other Cretaceous-period amber is found in
Kristensen NP (ed), Lepidoptera, moths and butterflies, North Russia and Japan. Baltic amber is found
vol 1: evolution, systematics, and biogeography. Handbuch in the Baltic sea where amber has been collected
der Zoologie. Band IV. Arthropoda: Insecta. Teilband
35:5163. W. de Gruyten, Berlin and made into decorative objects for at least
13,000 years. In the Dominican Republic, amber
deposits 2330 million years old are found in
rock layers. Dominican amber is particularly
Amber Insects: DNA Preserved? rich in insect inclusions. This amber was formed
from the resin of an extinct tree in the legume
marjorie a. hoy family. Tertiary amber deposits are found in
University of Florida, Gainesville, FL, USA several locations around the world and are from
1.6 to 65 million years old. Tertiary deposits in
Amber is a polymerized form of tree resin that the USA are found in Arkansas. Some websites
was produced by trees as a protection against dis- with photographs showing amber inclusions
ease agents and insect pests. The resin hardened can be viewed at:
and, sometimes, captured insects, seeds, feathers, Amber Inclusions at: http://www-user.uni-bremen.
microorganisms, plants, spiders, and even small de/~18m/amber.html;
138
A Amber Insects: DNA Preserved?

Amber on-line at: www.ambericawest.com/amberpics. amber-preserved insects has yet to be reproduced

html; in independent laboratories, despite multiple
American Museum of Natural History at: www.amnh. attempts to do so, which has cast doubt on the
org/exhibitions/amber/; or authenticity of the reports.
The Amber Room at: http://home.earthlink.net/-skurth/ One of the most controversial claims involved
AMBER.HTM. the isolation of a living bacterium from the abdo-
men of amber-entombed bee. Bacterial DNA from
a 25-million-year-old bee was obtained and
Insect DNA in Amber? sequenced and a bacterial spore was reported to
be revived, cultured, and identified. The classifica-
The ability to amplify dinosaur DNA from insects tion of the bacterium is controversial because the
preserved in amber in the film Jurassic Park cap- bacterium could have come from a currently
tured the imagination of the public. Subsequently, undescribed species of the Bacillus sphaericus
the PCR was used to amplify DNA fragments from complex. The modern B. sphaericus complex is
insects preserved in ancient amber, but these incompletely known, so the new sequence
results have been controversial, as have been the obtained could be that of a modern, but previously
results from amplifying dinosaur DNA. unidentified, bacterium because this group of bac-
Why the controversy? Is amber a special form teria often is isolated from the soil.
of preservative that allows DNA to persist for Other claims of amplifying ancient DNA have
unusually long periods of time (millions of years)? been disproved. For example, the mitochondrial
Amber entombs insect specimens completely, cytochrome b sequence of an 80-million-year-old
after which they completely dehydrate so the tis- dinosaur from the Upper Cretaceous in Utah was
sue is effectively mummified. Terpenoids, which later discovered to be, most probably, of human
are major constituents of amber, could inhibit origin. Likewise, a 20-million-year-old magnolia
microbial decay. Certainly, preservation of amber- leaf produced sequences that were similar to those
embedded insects seems to be exceptional and of modern magnolias. The authenticity of the
insect tissues in amber appear comparable in qual- magnolia sequences were cast into doubt because
ity to the tissues of the frozen wooly mammoth they were exposed to water and oxygen during
(which is only 50,000 years old). But is the DNA preservation and DNA is especially vulnerable to
in these tissues preserved? degradation under such conditions.
DNA has been extracted from a variety of The most common ancient DNA analyzed is
insects in amber, including a fossil termite Masto- usually mitochondrial DNA because it is so abun-
termes electrodominicus estimated to be 2530 dant; however, this abundance makes it easy to
million years old, a 120- to 130-million year old contaminate the ancient sample with modern
conifer-feeding weevil (Coleoptera: Nemonychi- mtDNA. The amplification of ancient DNA
dae) and a 25- to 40-million year old bee. These remains highly controversial because the technical
are extraordinary ages for DNA! difficulties are great.
The DNA sequences obtained from all amber- DNA is a chemically unstable molecule that
preserved insects meet several, but not all, criteria decays spontaneously, mainly through hydroly-
of authenticity; the fossil DNA sequences make sis and oxidation. Hydrolysis causes deamina-
phylogenetic sense and DNA has been isolated tion of the nucleotide bases and cleavage of
from a number of specimens in several cases base-sugar bonds, creating baseless sites. Deami-
(although the weevil example was derived from a nation of cytosine to uracil and depurination
single specimen). However, the extraction and (loss of purines adenine and guanine) are two
amplification of fossil DNA sequences from types of hydrolytic damage. Baseless sites weaken
 Ambrosia Beetles
A 139

the DNA, causing breaks that fragment the DNA selection of well-preserved specimens, choice of
into smaller and smaller pieces. Oxidation leads tissue samples that are likely to have best DNA
to chemical modification of bases and destruc- preservation, and surface sterilization to elimi-
tion of the ring structure of base and sugar resi- nate surface contamination. The operations
dues. As a result, it is almost always impossible should be carried out in a laboratory dedicated to
to obtain long amplification products from work on ancient specimens and work on ancient
ancient DNA. DNA should be separated from that on modern
PCR products from ancient DNA often are DNA. Most importantly, multiple negative con-
scrambled. This is due to the phenomenon trols should be performed during DNA extrac-
called jumping PCR, which occurs when the tion and PCR set up, although a lack of positives
DNA polymerase reaches a template position in the negative controls is not definitive proof of
which carries either a lesion or a strand break authentic ancient DNA. Another crucial step is
that stops the polymerase. The partially extended the authentication of the results. Putatively ancient
primer can anneal to another template fragment DNA sequences should be obtained from differ-
in the next cycle and be extended up to another ent extractions of the same sample and from dif-
damaged site. Thus, in vitro recombination can ferent tissue samples from different specimens.
take place until the whole stretch encompassed The ultimate test of authenticity should be inde-
by the two primers is synthesized and the ampli- pendent replication in two separate laboratories.
fication enters the exponential part of the PCR. So far, this type of replication has not been
This phenomenon makes it essential that clon- achieved for DNA from amber-preserved arthro-
ing and sequencing of multiple clones be pod specimens.
carried out to eliminate this form of error in
interpretation.
Most archeological and paleontological speci- References
mens contain DNA from exogenous sources such
as bacteria and fungi, as well as contaminating Austin JJ, Ross AJ, Smith AB, Fortey RA, Thomas RH (1997)
DNA from contemporary humans. Aspects of Problems of reproducibility does geologically ancient
burial conditions seem to be important in DNA DNA survive in amber-preserved insects? Proc R Ento-
mol Soc London B 264:467474
preservation, especially low temperature during Hofreiter M, Serre D, Poinar HN, Kuch M, Paabo S (2001) Ancient
burial. The oldest DNA sequences reported, and DNA. Nat Rev Genet 2:353359
confirmed in other laboratories, come from the Poinar G Jr, Poinar R (2001) The amber forest: a reconstruc-
remains of a wooly mammoth found in the Sibe- tion of a vanished world. Princeton University Press,
Princeton, NJ
rian permafrost; these sequences are only 50,000 Poinar HN, Stankiewicz BA (1999) Protein preservation and
years old rather than millions of years old. DNA retrieval from ancient tissues. Proc Natl Acad Sci
Theoretical calculations and empirical USA 96:84268431
Yousten AA, Rippere KE (1997) DNA similarity analysis of a
observations suggest DNA should only be able
putative ancient bacterial isolate obtained from amber.
to survive, in a highly fragmented and chemi- FEMS Microbiol Lett 152:345347
cally modified form, for 50,000100,000 years.
Because only tiny amounts of DNA usually can
be extracted from an archeological specimen,
stringent precautions and multiple controls are Ambrosia Beetles
required to avoid accidental contamination with
modern DNA. Some members of the subfamily Scolytinae (order
A methodology to deal with ancient speci- Coleoptera, family Curculionidae).
mens has been proposed that includes careful Beetles
140
A Ambush Bugs

Ambush Bugs Reference

Members of the family Reduviidae (order Konradsen F, de Silva A, van der Hoek W (2005) Felix P.
Hemiptera). Amerasinghe. American Entomologist 51:191
Bugs

American Butterfly Moths

(Lepidoptera: Hedylidae)
Ameletopsidae
john b. heppner
A family of mayflies (order Ephemeroptera). Florida State Collection of Arthropods,
Mayflies Gainesville, FL, USA

American butterfly moths, family Hedylidae, total

Amelitidae only 40 known species, all Neotropical. The family
is in the superfamily Geometroidea, in the section
A family of mayflies (order Ephemeroptera). Cossina, subsection Bombycina, of the division
Mayflies Ditrysia. Adults medium size (3565 mm wing-
span), with head scaling normal; haustellum
naked; labial palpi upcurved; maxillary palpi 1 to
2-segmented; antennae filiform. Wings triangular,
Amerasinghe, Felix P with forewings somewhat elongated and often
with apex emarginated (Fig.38); hindwings usually
Felix Amerasinghe was a noted Sri Lankan medi- more rounded. Body usually narrow. Maculation
cal entomologist. He was known for his work on somber hues of brown and gray, often with apical
the taxonomy and ecology of disease-transmitting dark patch and some speckling, plus pale or hya-
arthropods. Amerasinghe graduated from the line patches (rarely mostly pale or hyaline). Adults
University of Peradeniya, Sri Lanka, and received nocturnal. Larvae are leaf feeders. Host plants are
his Ph.D. from the University of Bristol, United recorded in Euphorbiaceae, Malvaceae, Sterculi-
Kingdom, in 1977. He made important long-term aceae, and Tiliaceae.
studies in the effects of irrigation on mosquito
populations and malaria transmission, and became
an authority on Japanese encephalitis. The devel-
opment of keys for the identification of South
Asian mosquitoes was one of his important con-
tributions, greatly enhancing disease surveillance
programs.
Amerasinghe worked principally at the Uni-
versity of Peradeniya, but also at the University of
Sri Lanka, and in later years joined the Interna-
tional Water Management Institute as research
leader, initiating studies on the socioeconomic American Butterfly Moths (Lepidoptera:
impact of malaria, malaria parasitology, and Hedylidae), Figure 38 Example of American
molecular biology. He died in Colombo, Sri Lanka, butterfly moths (Hedylidae), Macrosoma lucivittata
on June 7, 2005. (Walker), from Ecuador.
 American Grasshopper, Schistocerca Americana (Drury) (Orthoptera: Acrididae)
A 141

References

Aiello A (1992) Nocturnal butterflies in Panama, Hedylidea

(Lepidoptera: Rhopalocere). Quintero D, Aiello A (eds),
Insects of Panama and Mesoamerica. Oxford University
Press, Oxford, pp 549553
Scoble MJ (1986) The structures and affinitxies of the Hedy-
loidea: a new concept of the butterflies. Bull Br Mus Nat
Hist Entomol 53:251286
Scoble MJ (1990) An identification guide to the Hedylidae
(Lepidoptera: Hedyloidea). Entomologica Scandinavica American False Tiger Moths (Lepidoptera:
21:121158 Dioptidae), Figure 39 Example of American false
Scoble MJ (1998) Hedylidae. In Lepidopterorum Catalogus, tiger moths (Dioptidae), Josia gigantea Druce,
(n.s.). Fasc. 93. Association for Tropical Lepidoptera,
Gainesville, FL, 9 pp from Mexico.
Scoble MJ, Aiello A (1990) Moth-like butterflies (Hedylidae:
Lepidoptera): a summary, with comments on the egg. J References
Nat Hist 24:159164
Bryk F (1930) Dioptidae. Lepidopterorum catalogus, 42:165.
W. Junk, Berlin, Germany
Miller JS (1987) A revision of the genus Phryganidia Packard,
American Dog Tick with description of a new species (Lepidoptera: Diopti-
dae). Proc Entomol Soc Wash 89:303321
Ticks Prout LB (1918) A provisional arrangement of the Dioptidae.
Novitates Zoologicae 25:395429
Seitz A (ed) (19251927) Familie: Dioptidae. In: Die Gross-
Schmetterlinge der Erde. 6. Die amerikanischen Spinner
American False Tiger Moths und Schwrmer, pl. 6771. A. Kernen, Stuttgart,
(Lepidoptera: Dioptidae) Germany, pp 499534
Todd EL (1981) The noctuoid moths of the Antilles Part I
(Lepidoptera: Dioptidae). Proc Entomol Soc Wash
john b. heppner 83:324325
Florida State Collection of Arthropods,
Gainesville, FLa, USA

American false tiger moths, family Dioptidae, total American Grasshopper,

507 species, primarily Neotropical (505 sp.); actual Schistocerca americana (Drury)
fauna likely exceeds 800 species. Two subfamilies are (Orthoptera: Acrididae)
known: Dioptinae and Doinae. Some specialists
place the family within the Notodontidae. The fam- john l. capinera
ily is in the superfamily Noctuoidea, in the section University of Florida, Gainesville, FL, USA
Cossina, subsection Bombycina, of the division
Ditrysia. Adults medium size (2258 mm wingspan) This grasshopper is found widely in eastern North
(Fig.39). Maculation mostly very colorful, with var- America, from southern Canada (where it is an
ious patterns of large spotting, and some lustrous. occasional invader) south through Mexico to
Larvae and pupae often also colorful Adults are northern South America. In the midwestern states,
mostly nocturnal, but some are diurnal or crepuscu- where it is common, the resident population
lar. Larvae are leaf feeders, particularly toxic plants receives a regular infusion of dispersants from
in families like Aristolochiaceae, Euphorbiaceae, southern locations. In the southeast it is quite
Passifloraceae, and Violaceae, but also on various common, and one of the few species to reach epi-
others like Fagaceae. Very few are economic. demic densities. It is native to North America.
142
A American Grasshopper, Schistocerca Americana (Drury) (Orthoptera: Acrididae)

Life History than ventral orientation but the wing tip does not
exceed the first abdominal segment. In the sixth
In warm climates, American grasshopper has two instar (Fig.41) there are 2426 antennal segments
generations per year and overwinters in the adult and the wing tips extend beyond the second
stage. In Florida, eggs produced by overwintered abdominal segment. The overall body length is
adults begin to hatch in April-May, producing about 67, 1213, 1618, 2225, 2730, and 3545
spring generation adults by May-June. This spring mm for instars 16, respectively. Development
generation produces eggs that hatch in August- time is about 46, 46, 46, 48, 68, and 913
September. The adults from this autumn genera- days for the corresponding instars when reared at
tion survive the winter. about 32C.
The eggs of S. americana initially are light The adult (Fig.40) is rather large, but slender
orange in color, turning tan with maturity. They bodied, measuring 3952 and 4868 mm in length
are elongate-spherical in shape, widest near the in the male and female, respectively. A creamy
middle, and measure about 7.5 mm in length and white stripe normally occurs dorsally from the
2.0 mm in width. The eggs are clustered together front of the head to the tips of the forewings. The
in a whorled arrangement, and number 75100 forewings bear dark brown spots, the pronotum
eggs per pod, averaging 85 eggs. The eggs are
inserted into the soil to a depth of about 4 cm and
the upper portion of the oviposition hole is filled
by the female with a frothy plug. Duration of the
egg stage is about 14 days. The nymphs, upon
hatching, dig through the froth to attain the soil
surface.
Normally there are six instars in this grass-
hopper though sometimes only five. The young
grasshoppers are light green in color. They are
extremely gregarious during the early instars. At
low densities the nymphs remain green through-
out their development, but normally gain increas- American Grasshopper, Schistocerca Americana
ing amounts of black, yellow, and orange coloration (Drury) (Orthoptera: Acrididae), Figure 40 Adult
commencing with the third instar. Instars can be of American grasshopper, Schistocerca americana
distinguished by their antennal, pronotal, and (Drury).
wing development. The first and second instars
display little wing development but have 13 and
17 antennal segments, respectively. In the third
instar, the number of antennal segments increases
to 2022, the wings begin to display weak evi-
dence of veins, and the dorsal length of the ven-
tral lobe of the pronotum is about 1.5 times the
length of the ventral surface. Instar four is quite
similar to instar three, with 2225 antennal seg-
ments, though the ratio of the length of the dorsal American Grasshopper, Schistocerca Americana
to ventral surfaces of the pronotal lateral lobe is (Drury) (Orthoptera: Acrididae), Figure 41 Sixth
2:1. In instar five there are 2425 antennal seg- instar of American grasshopper, Schistocerca
ments, and the wing tips assume a dorsal rather americana (Drury).
 American Grasshopper, Schistocerca Americana (Drury) (Orthoptera: Acrididae)
A 143

dark stripes. The hind wings are nearly colorless. Damage

The hind tibiae normally are reddish. Overall, the
body color is yellowish brown or brownish with Grasshoppers are defoliators, eating irregular
irregular lighter and darker areas, though for a holes in leaf tissue. Under high density conditions
week or so after assuming the adult stage a pinkish they can strip vegetation of leaves, but more com-
or reddish tint isevident. monly leave plants with a ragged appearance.
Adults are active, flying freely and sometimes American grasshopper displays a tendency to
in swarms. They normally are found in sunny swarm, and the high densities of grasshoppers can
areas, but during the warmest portions of the day cause severe defoliation.
will move to shade. Adults are long lived, persist- Because American grasshopper is a strong
ing for months in the laboratory and apparently in flier, it also sometimes becomes a contaminant
the field as well. This can lead to early-season situ- of crops. When the late-season crop of collards
ations where overwintered adults, all instars of in the Southeast is harvested mechanically, for
nymphs, and new adults are present simultane- example, American grasshopper may become
ously. Mild winters favor survival of overwintering incorporated into the processed vegetables.
adults and apparently lead to population increase Although most grasshoppers can be kept from
if summer weather and food supplies also are dispersing into crops near harvest by treating
favorable. the periphery of the crop field, it is much more
Adults of American grasshopper tend to be difficult to prevent invasion by American grass-
arboreal in habit, and a great deal of the feeding hopper because it may fly over any such barrier
by adults occurs on forest, shade, and fruit trees. treatments.
The nymphs, however, feed on a large number of Populations normally originate in weedy
grasses and broadleaf plants, both wild and cul- areas such as fence rows and abandoned fields.
tivated. During periods of abundance, almost no Thus, margins of fields are first affected and this is
plants are immune to attack, and vegetables, where monitoring should be concentrated. It is
grain crops, and ornamental plants are injured. highly advisable to survey weedy areas in addition
American grasshopper consumes bean, corn, to crop margins if grasshoppers are found, as this
okra, and yellow squash over some other vegeta- gives an estimate of the potential impact if the
bles when provided with choices, but free-flying grasshoppers disperse into the crop. Also, it is
adults normally avoid low-growing crops such important to recognize that this species is highly
as vegetables, corn (maize) being a notable dispersive in the adult stage, and will fly hundreds
exception. of meters or more to feed.
The natural enemies of S. americana are not
well known. Birds such as mockingbirds, Mimus
polyglottos polyglottos (Linnaeus), and crows, Cor- Management
vus brachyrhynchos brachyrhynchos Brehm have
been observed to feed on these grasshoppers. Fly Foliar applications of insecticides will suppress
larvae, Sarcophaga sp. (Diptera: Sarcophagidae) grasshoppers, but they are difficult to kill, particu-
are sometimes parasitic on overwintering adults. larly as they mature. Bait formulations are not
Fungi have also been investigated for grasshopper usually recommended because these grasshoppers
suppression and Metarhizium anisopliae var. spend little time on the soil surface, preferring to
acridum kills American grasshopper quickly under climb high in vegetation.
laboratory conditions. This fungus is effective Land management is an important element
under adverse field conditions in Africa, so it may of S. americana population regulation. Grass-
prove to be a useful suppression tool. hopper densities tend to increase in large patches
144
A American Foulbrood

of weedy vegetation that follow the cessation of (= Bacillus) larvae, form heat- and drought-
agriculture or the initiation of pine tree planta- resistant spores that persist for years and germi-
tions. In both cases, the mixture of annual and nate under favorable conditions. It is expressed in
perennial forbs and grasses growing in fields older larvae and young pupae, though infection
that are untilled seems to favor grasshopper occurs earlier, and young larvae are more suscep-
survival, with the grasshoppers then dispersing tible than older larvae. Infected individuals turn
to adjacent fields as the most suitable plants are darker in color, then black, and eventually collapse
depleted. However, as abandoned fields convert into a hardened mass in the cell. Signs of infection
to dense woods or the canopy of pine planta- include a sour odor, perforated or sunken caps on
tions shades the ground and suppresses weeds, the cells, and the presence of black deposits in the
the suitability of the habitat declines for cells. If foulbrood is present, insertion of a twig or
grasshoppers. probe into a suspect cell will result in a gummy,
Disturbance or maturation of crops may cause stretchy substance being drawn out of the cell,
American grasshopper to disperse, sometimes over often forming a thread or rope and called ropy.
long distances, into crop fields. Therefore, care Field diagnosis is possible by experienced inspec-
should be taken not to cut vegetation or till the soil tors, but is best confirmed microscopically or by
of fields harboring grasshoppers if a susceptible molecular techniques. There are several subspe-
crop is nearby. Planting crops in large blocks cies of P. larvae, and P. larvae ssp. larvae is consid-
reduces the relative amount of crop edge, and the ered responsible for American foulbrood, with
probability that a crop plant within the field will be other subspecies also affecting honey bees.
attacked. Transmission occurs by feeding infected
Grasshopper Pests in North America honey or pollen, by using infected equipment, and
Grasshoppers and Locusts as Agricultural Pests sometimes by installing infected package bees or
Grasshoppers, Katydids and Crickets queens. Feeding bees sugar syrup therefore is pref-
(Orthoptera) erable to feeding them honey, and disinfection of
hive tools is always recommended. Natural trans-
References mission from hive to hive can occur through rob-
bing behavior. Queens and workers can carry the
Capinera JL (1993) Differentiation of nymphal instars in disease. Bee colonies that are infected normally
Schistocerca americana (Orthoptera: Acrididae). Fla are eliminated by burning them. Antibiotics can
Entomol 76:175179 be fed to colonies to prevent infection.
Capinera JL (1993) Host-plant selection by Schistocerca amer-
Honey Bees
icana (Orthoptera: Acrididae). Environ Entomol
22:127133 Apiculture
Capinera JL, Scott RD, Walker TJ (2004) Field guide to the Paenibacillus
grasshoppers, katydids, and crickets of the United States.
Cornell University Press, Ithaca, NY, 249 pp
Kuitert LC, Connin RV (1952) Biology of the American
grasshopper in the southeastern United States. Fla
Entomol 35:2233
References

Alippi AM, Lpez AC, Aguilar OM (2002) Differentiation

ofPaenibacillus larvae subsp. larvae, the cause of Amer-
American Foulbrood ican foulbrood of honeybees, by using PCR and restric-
tion fragment analysis of genes encoding 16S rRNA.
Appl Environ Microbiol 68:36553660
Historically, this is the most virulent disease
Morse RA, Nowogrodzki R (1990) Honey bee pests, preda-
of honey bees throughout the world. The bacte- tors and diseases, 2nd ed. Cornell University Press,
rium responsible for the disease, Paenibacillus Ithaca, NY, 474 pp
 American Serpentine Leafminer, Liriomyza Trifolii (Burgess) (Diptera: Agromyzidae)
A 145

American Serpentine Leafminer, measuring about 1.0 mm long and 0.2 mm wide.
Liriomyza trifolii (Burgess) Initially they are clear, but soon become creamy
(Diptera: Agromyzidae) white in color.

This leafminer has long been found in eastern

North America, northern South America, and the Larva
Caribbean. However, in recent years it has been
introduced into California, Europe, and elsewhere. Body and mouth part size can be used to differenti-
Expanded traffic in flower crops appears to be the ate instars; the latter is particularly useful. For the
basis for the expanding range of this species. Liri- first instar, the mean and range of body and mouth
omyza trifolii (Burgess), sometimes known as the parts (cephalopharyngeal skeleton) lengths are
American serpentine leafminer, readily infests 0.39 (0.330.53) mm and 0.10 (0.080.11) mm,
greenhouses. As a vegetable pest, however, its respectively. For the second instar, the body and
occurrence is limited principally to tropical and mouth parts measurements are 1.00 (0.551.21)
subtropical regions. mm and 0.17 (0.150.18) mm, respectively. For the
third instar, the body and mouth parts measure-
ments are 1.99 (1.262.62) mm and 0.25 (0.22
Life Cycle and Description 0.31) mm, respectively. A fourth instar occurs
between puparium formation and pupation, but
Leafminers have a relatively short life cycle. The this is a nonfeeding stage and is usually ignored by
time required for a complete life cycle in warm authors. The puparium is initially golden brown in
environments is often 2128 days, so numerous color, but turns darker brown with time.
generations can occur annually in tropical cli-
mates. Growth at a constant 25C requires about
19 days from egg deposition to emergence of the Adult
adult. Development rates increase with tempera-
ture up to about 30C; temperatures above 30C Adults (Fig. 42) are small, measuring less than 2 mm
are usually unfavorable and larvae experience high in length, with a wing length of 1.251.9 mm. The
mortality. At 25C, the egg stage requires 2.7 days head is yellow with red eyes. The thorax and abdo-
for development; the three active larval instars men are mostly gray and black although the ven-
require an average of 1.4, 1.4, and 1.8 days, respec- tral surface and legs are yellow. The wings are
tively; and the time spent in the puparium is 9.3 transparent. Key characters that serve to differen-
days. Also, there is an adult preovipostion period tiate this species from the vegetable leafminer,
that averages 1.3 days. The temperature threshold Liriomyza sativae Blanchard, are the matte, grayish
for development of the various stages is 610C, black mesonotum and the yellow hind margins of
except that egg laying requires about 12 C. the eyes. In vegetable leafminer the mesonotum is
shining black and the hind margin of the eyes is
black. The small size of this species serves to dis-
Egg tinguish it from pea leafminer, Liriomyza huidob-
rensis (Blanchard), which has a wing length of
Eggs tend to be deposited in the middle of the 1.72.25 mm. Also, the yellow femora of Ameri-
plant; the adult seems to avoid immature leaves. can serpentine leafminer help to separate it from
The female deposits the eggs on the lower surface pea leafminer, which has darker femora. Oviposi-
of the leaf, but they are inserted just below the epi- tion occurs at a rate of 3539 eggs per day, for a
dermis. Eggs are oval in shape and small in size, total fecundity of200400 eggs. The female makes
146
A American Serpentine Leafminer, Liriomyza Trifolii (Burgess) (Diptera: Agromyzidae)

American Serpentine Leafminer, Liriomyza Trifolii (Burgess) (Diptera: Agromyzidae), Figure 42 Adult of
American serpentine leafminer, Liriomyza trifolii.

numerous punctures of the leaf mesophyll with crops that are readily infested and which are
her ovipositor, and uses these punctures for feed- known to facilitate spread of this pest include
ing and egg laying. The proportion of punctures chrysanthemum, gerbera, gypsophila, and mari-
receiving an egg is about 25% in chrysanthemum gold, but there are likely many other hosts, espe-
and celery, both favored hosts, but only about 10% cially among the Compositae. Numerous
in tomato, which is less suitable for larval survival broad-leaved weed species support larval growth.
and adult longevity. Although the female appar- The nightshade Solanum americanum, Spanish
ently feeds on the exuding sap at all wounds, she needles, Bidens alba, and pilewort, Erechtites hier-
spends less time feeding on unfavorable hosts. The acifolia, were suitable weed hosts in Florida.
males live only two to three days, possibly because
they cannot puncture foliage and therefore feed
less than females, whereas females usually survive Damage
for about a week. Typically they feed and oviposit
during much of the daylight hours, but especially Punctures caused by females during the feeding
near mid-day. and oviposition processes can result in a stippled
appearance on foliage, especially at the leaf tip
and along the leaf margins. However, the major
Host Plants form of damage is the mining of leaves by larvae,
which results in destruction of leaf mesophyll.
Liriomyza trifolii is perhaps best known as a pest The mine becomes noticeable about three to four
of chrysanthemums and celery, but it has a wide days after oviposition, and becomes larger in size
host range. For example, at least 55 hosts are as the larva matures. The pattern of mining is
known from Florida, including bean, beet, carrot, irregular. Both leaf mining and stippling can
celery, cucumber, eggplant, lettuce, melon, onion, greatly depress the level of photosynthesis in the
pea, pepper, potato, squash, and tomato. Flower plant. Extensive mining also causes premature
 American Serpentine Leafminer, Liriomyza Trifolii (Burgess) (Diptera: Agromyzidae)
A 147

leaf drop, which can result in lack of shading and active miners. Adults can be captured by using
sun scalding of fruit. Wounding of the foliage also adhesive applied to yellow cards or stakes.
allows entry of bacterial and fungal diseases.
Although leaf mining can reduce plant growth,
crops such as tomato are quite resilient, and capa- Insecticides
ble of withstanding considerable leaf damage. It is
often necessary to have an average of one to three Chemical insecticides are commonly used to pro-
mines per tomato leaf before yield reductions tect foliage from injury, but insecticide resistance is
occur. Leafminers are most damaging when they a major problem. Insecticide susceptibility varies
affect floricultural crops due to the low tolerance widely among populations, and level of susceptibil-
of such crops for any insect damage. ity is directly related to frequency of insecticide
application. In Florida, longevity of insecticide ef
fectiveness is often only two to four years, and then
Natural Enemies is usually followed by severe resistance among the
treated populations. Rotation among classes of
Parasitic wasps (parasitoids) of the families Braco- insecticides is recommended to delay development
nidae, Eulophidae, and Pteromalidae are impor- of resistance. Reduction in dose level and frequency
tant in natural control, and in the absence of of insecticide application, as well as preservation of
insecticides usually keep this insect at low levels of susceptible populations through nontreatment of
abundance. At least 14 parasitoid species are some areas, are suggested as means to preserve
known from Florida alone. Species of Eulophidae insecticide susceptibility among leafminer popula-
such as Diglyphus begina (Ashmead), D. interme- tions. Insect growth regulators have been more sta-
dius (Girault), D. pulchripes, and Chrysocharis ble, but are not immune from the resistance problem.
parksi Crawford are generally found to be most Insecticides also are highly disruptive to naturally
important in studies conducted in North America, occurring biological control agents, particularly
although their relative importance varies geo- parasitoids. Use of many chemical insecticides
graphically and temporally. Predators and diseases exacerbates leafminer problems by killing parasi-
are not considered to be important, relative to par- toids of leafminers. This usually results when insec-
asitoids. However, both larvae and adults are sus- ticides are applied for lepidopterous insects, and use
ceptible to predation by a wide variety of general of more selective pest control materials such as
predators, particularly ants. Bacillus thuringiensis is recommended as it allows
survival of the leafminer parasitoids. Because para-
sitoids often provide effective suppression of leaf-
Management miners in the field when disruptive insecticides are
not used, there has been interest in release of para-
Sampling sitoids into crops. This occurs principally in green-
house-grown crops, but is also applicable to field
There are many methods to assess leafminer abun- conditions. Steinernema nematodes have also been
dance. Counting mines in leaves is a good index of evaluated for suppression of leaf mining activity.
past activity, but many mines may be vacant. High levels of relative humidity (at least 92%) are
Counting live larvae in mines is time consuming, needed to attain even moderately high (greater than
but more indicative of future damage. Puparia can 65%) levels of parasitism. Adjuvants that enhance
be collected by placing trays beneath foliage to nematode survival increase levels of leafminer mor-
capture larvae as they evacuate mines, and the tality, but thus far nematodes are not considered to
captures are highly correlated with the number of be a practical solution to leafminer infestations.
148
A American Silkworm Moths (Lepidoptera: Apatelodidae)

Cultural Practices

Because broadleaf weeds and senescent crops may

serve as sources of inoculum, destruction of weeds
and deep plowing of crop residues are recom-
mended. Adults experience difficulty in emerging
if they are buried deeply in soil.
Vegetable Pests and Their Management
Flies

References
American Silkworm Moths (Lepidoptera:
Capinera JL (2001) Handbook of vegetable pests. Academic Apatelodidae), Figure 43 Example of American
Press, San Diego, CA, 729 pp
silkworm moths (Apatelodidae), Apatelodes palma
Leibee GL (1984) Influence of temperature on develop-
ment and fecundity of Liriomyza trifolii (Burgess) Druce, from Ecuador.
(Diptera: Agromyzidae) on celery. Environ Entomol
13:497501
Minkenberg OPJM (1988) Life history of the agromyzid fly Some researchers consider the family part of
Liriomyza trifolii on tomato at different temperatures.
Bombycidae. The family is in the superfamily
Entomologia Expimentalis et Applicata 48:7384
Minkenberg OPJM, van Lenteren JC (1986) The leafminers Bombycoidea (series Bombyciformes), in the
Liriomyza bryoniae and L. trifolii (Diptera: Agromyzi- section Cossina, subsection Bombycina, of the
dae), their parasites and host plants: a review. Wagenin- division Ditrysia. Adults (Fig. 43) small to
gen Agric Univ Pap 862. 50 pp
Parrella MP, Robb KL, Bethke J (1983) Influence of selected
medium size (2074 mm wingspan), with head
host plants on the biology of Liriomyza trifolii (Diptera: scaling roughened; haustellum absent (rarely
Agromyzidae). Ann Entomol Soc Am 76:112115 vestigial); labial palpi small; maxillary palpi
Schuster DJ, Gilreath JP, Wharton RA, Seymour PR (1991) absent; antennae bipectinate; body robust. Wings
Agromyzidae (Diptera) leafminers and their parasitoids
in weeds associated with tomato in Florida. Environ broadly triangular; hindwings rounded. Macula-
Entomol 20:720723 tion varied but mostly shades of brown or gray,
Zehnder GW, Trumble JT (1984) Spatial and diel activity of rarely more colorful, with various markings.
Liriomyza species (Diptera: Agromyzidae) in fresh mar-
Adults are nocturnal. Larvae are leaf feeders.
ket tomatoes. Environ Entomol 13:14111416
Host plants include various records in Aquifoli-
aceae, Betulaceae, Bignoniaceae, Lauraceae,
Oleaceae, Rosaceae, among others.
American Silkworm Moths
(Lepidoptera: Apatelodidae)

john b heppner References

Florida State Collection of Arthropods,
Gainesville, FL, USA Franclemont JG (1973) Apatelodidae. In: Dominick RB, et al
(eds), The moths of America north of Mexico including
American silkworm moths, family Apatelodidae, Greenland. Fasc. 20.1, Bombycoidea, 1623. Classey EW,
London
are exclusively New World, and total 252 species, Seitz A (ed) (1929) Familie: Bombycidae. Die Gross-Schmet-
mostly Neotropical (247 sp.). Three subfamilies terlinge der Erde, 6:675711, pl. 89, 140142. A. Kernen.
are known: Apatelodinae, Epiinae, and Phiditiinae. [Apatelodidae], Stuttgart, Germany
 American Tropical Silkworm Moths (Lepidoptera: Oxytenidae)
A 149

American Swallowtail Moths Larvae are leaf feeders, but few known biologically.
(Lepidoptera: Sematuridae) Host plants are unrecorded.

john b. heppner
Florida State Collection of Arthropods, References
Gainesville, FL, USA
Seitz A (ed) (1930) Familie: Uraniidae [part]. Die Gross-
American swallowtail moths (Fig. 44), family Schmetterlinge der Erde, 6:829837, pl. 139. A. Kernen,
Sematuridae, total 36 Neotropical species, one of Stuttgart, Germany
Fassl AH (1910) Die Raupe einer Uranide. Zeitschrift fr
which just reaches into the United States, in southern
Wissenschaftliches Insektenbiologie 6:355
Arizona. The family is in the superfamily Uran- Strand E (1911) Zur Kenntnis der Uraniidengattung Coro-
ioidea, in the section Cossina, subsection Bom- nidia Westw. and Homidia Strand n. g. (=Coronidia
bycina, of the division Ditrysia. Adults medium to auct. p.p.) (Lep.). Deutsche Entomologische Zeitschrift
1911:635649
large (42100 mm wingspan), with head rough- Westwood JO (1879) Observations on the Uraniidae, a family
ened and eyes large; haustellum naked; labial palpi of lepidopterous insects, with a synopsis of the family and
upcurved, with long second segment and correctly a monograph of Coronidia, one of the genera of which it
angled short, smooth apical segment; maxillary is composed. Trans Zool Soc London 10:507542, 4 pl

palpi minute, 1-segmented; antennae thickened,

with elongated club (slightly hooked at tip). Wings
triangular, with hindwings tailed (usually hind- American Tropical Silkworm
wings with some emarginations); body sometimes Moths (Lepidoptera: Oxytenidae)
robust. Maculation various shades of darker brown,
with vertical lines and bands, often brightly colored john b. heppner
in the hindwings; often with eyespots on the tails. Florida State Collection of Arthropods,
Adults are nocturnal but some may be crepuscular. Gainesville, FL, USA

American tropical silkworm moths, family Oxyteni-

dae, include 60 species, all Neotropical. Some spe-
cialists consider this family a subfamily of
Saturniidae. The family is in the superfamily Bom-
bycoidea (series Saturniiformes), in the section
Cossina, subsection Bombycina, of the division Dit-
rysia. Adults medium size to large (4598 mm
wingspan), with head vertex somewhat roughened;
haustellum developed; labial palpi very large; max-
illary palpi absent; antennae bipectinate; body
somewhat slender or robust but with hair-like
scales. Wings triangular with with falcate apex but
sometimes rounded; hindwings somewhat angled
and with short tails or sometimes rounded. Macula-
tion mostly white with paired dark gray vertical
American Swallowtail Moths (Lepidoptera: striae and hindwings similar, but some species are
Sematuridae), Figure 44 Example of American dark brown with indistinct markings. Adults noc-
swallowtail moths Sematuridae), Sematura lunus turnal. Larvae are leaf feeders; some mimic snakes.
(Linnaeus), from Costa Rica. Host plants recorded in Rubiaceae.
150
A Ametabolous

References respectively. The cysts of the honeybee amoeba

are ingested and excyst, releasing slender pri-
Heppner JB (2003) Oxytenidae. Lepidopterorum catalogus, mary trophozoites that penetrate and multiply
(n.s.). Fasc. 115. Association for Tropical Lepidoptera, in the midgut epithelium. Secondary trophozo-
Gainesville, FL, 12 pp ites emerge from these cells and migrate to the
Jordan K (1924) On the Saturnoidean families Oxytenidae
and Cercophanidae. Novitates Zoologicae 31:135193 lumen of the Malpighian tubules. These tro-
Schssler H (1936) Oxytenidae. Lepidopterorum catalogus, phozoites, having pseudopodia, feed in the
W. Junk, The Hague, 75:120 lumen and cause a flattening of the epithelial
layer and a distension of the tubules. The brush
border in contact with the amoeba swells in
Ametabolous size and loses the associated secretory trans-
port vesicles. Infected tubules contain a mix of
Organisms that do not display the process of secondary trophozoites, precysts, and cysts. The
metamorphosis. In ametabolous organisms there primary damage to the host bee is the malfunc-
is little change in body form during growth and tion of the Malpighian tubules. Both numbers
molting. of amoeba and the presence of other disease
Metamorphosis agents determine the severity of the amoebiasis
in the bee. In general, this disease either induces
stress or under appropriate conditions in the
Ametropodidae
springtime can be debilitative, resulting in hive
A family of mayflies (order Ephemeroptera). dwindling.
Mayflies Malamoeba locustae, also known as Malam-
oeba locusta, has been detected in a wide range of
grasshopper species and in a single Thysanuran
Amino Acid species. Its life cycle is very similar to that observed
with M. mellificae. The host grasshoppers ingest
Chemical compounds that may occur free, or the resistant uninucleate cysts, and excysted pri-
linked by peptide bonds into proteins. mary trophozoites invade the midgut and caecal
tissues. Within these tissues the trophozoites grow
and divide, and within about 10 days release prog-
eny secondary trophozoites into the lumen. These
Ammophilous cells migrate to the lumen of the Malpighian
tubules and undergo additional cell divisions
Sand loving. Organisms inhabiting or preferring (Fig. 45). The vegetative development of this
sandy habitats are called ammophilous (adjective) amoeba damages the serosal membrane of the
or ammophiles (noun). tubules, inhibiting their response to insect diuretic
hormone. The infected tubules become packed
with trophozoites and cysts. At high levels,
M. locustae may inhibit the excretory function of
Amoebae the tubules and cause the grasshoppers to become
lethargic prior to death. The distended, amoeba-
The two best-studied insect amoebae are Mal- infected tubules may rupture, releasing both
pighamoeba mellificae and Malamoeba locustae, trophozoites and cysts into the hemocoel. These
which are associated with the honeybee, Apis amoebas are quickly recognized as non-self
mellifera, and the Melanoplus grasshoppers, and are encapsulated by circulating phagocytic
 Amphitheridae
A 151

Amoebae, Figure 45 Light micrograph of the cysts of Malamoeba locusta released from infected
Malpighian tubules.

hemocytes. This disease, although a problem in lab- Amphienotomidae

oratory cultured grasshoppers, is rarely detected
in natural populations. A family of psocids (order Psocoptera).
Bark-Lice, Book-Lice, or Psocids

References
Amphiposocidae
Brooks WM (1988) Entomogenous Protozoa. In: Ignoffo C (ed),
Handbook of natural pesticides, vol 5. Microbial insec- A family of psocids (order Psocoptera).
ticides. Part A. Entomogenous protozoa and fungi. CRC
Press, Boca Raton, FL, pp 1149 Bark-Lice, Book-Lice, or Psocids
Liu TP (1985) Scanning electron microscopy of developmen-
tal stages of Malpighamoeba mellificae Prell in the hon-
eybee. J Protozool 32:139144 Amphipterygidae
A family of damselflies (order Odonata).
Amoebiasis Dragonflies and Damselflies

Infection of an insect by amoebae.

Amphitheridae
Amorphoscelididae A family of moths (order Lepidoptera) also known
as double-eye moths.
A family of praying mantids (Mantodea). Double-Eye Moths
Praying Mantids Butterflies and Moths
152
A Amphitoky

Amphitoky Anagrus species (Mymaridae), among the smallest

insects known, are endoparasitoids of eggs of
A type of parthenogenesis in which both females Odonata and Hemiptera. The genus is worldwide
and males are produced. and about 60 species is now recognized.

Amphizoidae Taxonomy and Adult Morphology

A family of beetles (order Coleoptera). They com- The metasoma of Anagrus is not constricted basally,
monly are known as trout stream beetles. so it appears broadly sessile, the hypochaeta in front
Beetles of the marginal vein is basal to the first macro-
Wasps, Ants, Bees and Sawflies chaeta, the tarsi are 4-segmented, the posterior
scutellum is longitudinally divided, and the foretibia
has a comb-like spur. Adult males and females are
Amplification similar, differing mainly in their antennae, with nine
segments and clubbed in females (Fig. 46) and 13
In molecular biology, the production of additional segments and filiform in males. Body color is often
copies of a chromosomal sequence, found as either darker in males. The genitalia, both in males (the
intrachromosomal or extrachromosomal DNA. In aedeagus) and in females (the ovipositor), have
medical entomology, the production of increased features of taxonomic importance.
numbers of virus in a host. This is often a prerequisite The genus is subdivided into three subgenera
to acquisition and transmission of the virus by a Anagrella, Anagrus, and Paranagrus.
blood-feeding insect.

Biology
Amplification Hosts
Like all holometabolous insects, Anagrus species
Hosts of viruses that allow amplification of the virus, have three distinct immature stages, egg, larva and
usually used in the context of arboviruses. Some pupa. The egg is stalked, with an ovoid body that
hosts do not allow amplification, and so serve as an swells during embryogenesis. There are two, apodous,
end-point in the virus cycle. larval instars (Fig. 47), which appear completely dif-
Dead-end Hosts ferent from one another. The first instar is sacciform
and usually attached to the egg chorion. It does not
show any cuticular structure that could serve to feed,
Ampulicidae breathe or feel. It is completely immobile and proba-
bly obtains nourishment and breathes through its
A family of wasps (order Hymenoptera). cuticle. The second instar is divided weakly into six
body segments, has a mouth and a salivary gland
opening, two mandibles and an anus, and various
Anagrus Fairyflies (Hymenoptera: other, probably sensory, structures. No spiracle is
Mymaridae) present. Second instar larvae are very active and
fight each other when in the same host egg. The
elisabetta chiappini mature larva (prepupa) develops inside the egg
Universit Cattolica del Sacro Cuore, into an exarate pupa and does not spin a cocoon.
Piacenza, Italy When development is complete, adults are
 Anagrus Fairyflies (Hymenoptera: Mymaridae)
A 153

Anagrus Fairyflies (Hymenoptera: Mymaridae), Figure 46 Adult female of Anagrus sp.

females insert their ovipositor into the slit made

by the host or through the plant tissue itself,
depending on the species. Adults occur in various
habitats, both natural and cultivated, depending
on where their hosts occur. This includes dry habi-
Anagrus Fairyflies (Hymenoptera: Mymaridae), tats such as vineyards and beet fields to damp or
Figure 47 Larva of Anagrus sp. aquatic ones (ponds) where host eggs are found in
plants such as Cyperus or Nuphar.
r ecognizable through the host egg chorion, through Certain Anagrus species can develop both as
which they chew a hole to exit. After emergence the solitary or gregarious parasitoids in eggs of differ-
adults shed their waste products (meconium). Males ent size, whereas others appear to be much more
are usually protandrous. specialized on eggs of the same size, in which they
always develop as solitary parasitoids.
Many Anagrus are extremely important
Behavior and Ecology because they provide control of potentially serious
pests on many agricultural crops. The most impor-
Reproduction is bisexual or parthenogenetic. The tant examples are against leafhoppers such as
latter reproduction is usually arrhenotokous but, Empoasca vitis Goethe and Zygina rhamni (Fer-
rarely, thelytokous parthenogenesis has been rari) in vineyards in Europe and Erythroneura spp.
recorded. Females are ready to oviposit as soon as in North America, against leaf- and planthoppers
they emerge. Copulation, if it occurs, is usually such as Nilaparvata spp. and Sogatella spp. on rice
very quick (some tens of seconds) and insemi- in eastern Asia, and against Perkinsiella sachari-
nated females generally do not copulate again. cida Kirkaldy on sugarcane in Hawaii.
When fed with sugar water, honey or nectar, adults Some biological supply companies mass pro-
may live for up to 10 days. It is thought that adult duce and sell Anagrus atomus L. for biological
host feeding may occur as in other parasitoids. control. Care must be taken to ensure the sanitary
Anagrus species mainly parasitize leafhoppers conditions of the product as the parasitoid is bred
(Cicadellidae), planthoppers, (Delphacidae) and on the natural host eggs inserted into plant tissue,
damsel- or dragonfly (Odonata) eggs, all of which which could be a potential vehicle for other pests
are embedded in plant tissue. To reach the eggs, or diseases.
154
A Anajapygidae

References abdominal segment; in caterpillars (Lepidoptera) it

refers to a ventral projection at the tip of the abdo-
Chiappini E, Lin NQ (1998) Anagrus (Hymenoptera: Mymari- men that is used to eject frass; in some beetle
dae) of China, with descriptions of nine new species. (Coleoptera) larvae it refers to cerci-like projections
Ann Entomol Soc Am 91:549571 near the tip of the abdomen.
Chiappini E, Triapitsyn SV, Donev A (1996) Key to the Hol-
arctic species of Anagrus Haliday (Hymenoptera:
Mymaridae) with a review of the Nearctic and Palaearc-
tic (other than European) species and descriptions of Anal Gills
new taxa. J Nat Hist 30:551595
Moratorio MS (1990) Host finding and oviposition behavior Gills found at the tip of the abdomen and usually
of Anagrus mutans and Anagrus silwoodensis Walker
(Hymenoptera: Mymaridae). Environ Entomol
consisting of three to five small clusters.
19:142147 Abdomen of Hexapods
Moratorio MS, Chiappini E (1995) Biology of Anagrus incar-
natosimilis and Anagrus breviphragma. Bollettino di
Zoologia Agraria e di Bachicoltura, Serie II, 27:143162 Anal Hooks
Triapitsyn SV (1997) The genus Anagrus (Hymenoptera:
Mymaridae) in America south of the United States: a
review. Ceiba 38:112 In Lepidoptera, small hook or club-shaped struc-
Triapitsyn SV (1998) Anagrus (Hymenoptera: Mymaridae) tures at the tip of the abdomen that serve to anchor
egg parasitoids of Erythroneura spp. and other leafhop- the pupa to the cocoon or silk pad.
pers (Hemiptera: Cicadellidae) in North America vine-
yards and orchards: a taxonomic review. Trans Am
Entomol Soc 124:77112
Anal Furrow
The suture-like groove in the membrane of the
Anajapygidae wing.
Wings of Insects
A family of diplurans (order Diplura).
Diplurans
Anal Legs (Prolegs)
Anal Angle In holometabolous larvae, especially Lepidoptera
larvae, the appendages of the tenth abdominal
The hind angle of the forewings. segment (the terminal prolegs).
Wings of Insects

Anal Lobe
Anal Cell
The posterior region of the wing, occupied by the
A cell in the anal area (anal lobe) of a wing. anal veins.
Wings of Insects Wings of Insects

Anal Comb Anal Loop

This term is applied to a variety of structures that A cluster of cells between the anal wing veins, or
differ depending on the taxon. In flea (Siphonaptera) between the cubitus and anal vein, in Odonata.
larvae, it refers to several rows of setae on the tenth Wings of Insects
 Andean Moon Moths (Lepidoptera: Cercophanidae)
A 155

Anal Plate Andean Moon Moths

(Lepidoptera: Cercophanidae)
The shield-like plate or dorsal covering on the ter-
minal segment in caterpillars, and some other lar- john b. heppner
vae. It usually is dark in color, and is also called the Florida State Collection of Arthropods,
anal shield. Gainesville, FL, USA

Andean moon moths, family Cercophanidae,

include 30 species of mostly austral South Ameri-
Anal Tube
can moths. There are two subfamilies: Cercophani-
nae (four sp.) and Janiodinae (26 sp.). Some
Eversible, tubular organs in the anal region of lar-
specialists consider this family a subfamily of Sat-
val Coleoptera. These organs are armed with
urniidae. The family is in the superfamily Bomby-
microspines and assist in attachment to the
coidea (series Saturniiformes), in the section
substrate.
Cossina, subsection Bombycina, of the division
Ditrysia. Adults (Fig. 48) medium size to large
(24105 mm wingspan), with head vertex rough-
Anal Vein ened; haustellum absent; labial palpi very large;
maxillary palpi absent; antennae bipectinate; body
Longitudinal unbranched vein, or veins, extending robust, with long hair-like scales. Wings broadly
from the base of the wing to the outer margin of triangular, often with apex falcate, or more rounded;
the wing, below the cubitus vein. hindwings rounded or emarginated but sometimes
Wings of Insects with tails. Maculation various, but mostly shades of
brown with diagonal line and fainter markings, but
some with long tails and lighter tan, and with eyes-
pots. Adults are nocturnal. Larvae are leaf feeders.
Anamorphosis
Postembryonic development in which additional
abdominal body segments are added at the time of
molting (the opposite of epimorphosis).

Anaxyelidae
A family of wood wasps (order Hymenoptera,
suborder Symphyta). They commonly are known
as incense-cedar wood wasps.
Wasps, Ants, Bees and Sawflies

Andean Moon Moths (Lepidoptera:

Ancistrosyllidae
Cercophanidae), Figure 48 Example of Andean
A family of fleas (order Siphonaptera). moon moths (Cercophanidae), Cercophana venusta
Fleas (Walker) from Chile.
156
A Andesianidae

Host plants recorded in Celastraceae, Lauraceae, Australia Department of Agriculture. He began a

Saxifragaceae, and Tiliaceae. study of a weevil pest of fruit trees, Otiorhynchus
cribricollis, that required detailed autecological
studies. In 1933, he moved to Melbourne, appointed
References by the CSIR as assistant research officer, to work on
the autecology of Thrips imaginis, a pest of apple
Angulo AO, Heppner JB (2004) Cercophanidae. Lepidoptero- trees. He worked in the School of Agriculture and
rum catalogus, (n.s.). Fasc. 116. Association for Tropical Forestry at the University of Melbourne. While
Lepidoptera, Gainesville, FL, 8 pp
Jordan K (1924) On the Saturnoidean families Oxytenidae
working, he was able to complete a thesis for which
and Cercophanidae. Novitates Zoologicae 31:135193, he was awarded the degree of Master of Agricul-
pl. 621 tural Sciences. He married, and in 1935 moved to
Schssler H (1936) Cercophanidae. Lepidopterorum catalo- the Waite Agricultural Research Institute in Ade-
gus, W. Junk, The Hague, 76:112
Ureta RE (1943) Revisin del gnero Polythysana Wlk. (Sat- laide. His main duties now turned to a study of
urniidae). Boletin del Museo Nacional de Historia Nat- Austroicetes cruciata, a plague grasshopper, and
ural de Chile 21:5570, 4 pl diapause of its eggs. However, his supervisor, who
Wolfe KL, Balczar LMA (1994). Chiles Cercophana venusta
had been working on Thrips imaginis, died sud-
and its immature stages (Lepidoptera: Cercophanidae)
Trop Lepidoptera 5:3542 denly, leaving copious unanalyzed data, whose
completion and publication fell to Herbert. The
published work was criticized because it con-
cluded that climatic factors were all-important in
Andesianidae the population dynamics of the pest, without
room for action of biotic factors. But it led to
A family of moths (order Lepidoptera) also known collaboration with L.C. Birch on a book (1954)
as valdivian forest moths. The distribution and abundance of animals.
Butterflies and Moths Then, after Herbert moved to the Zoology
Valdivian Forest Moths Department of the University of Adelaide, it led
to a book designed as a textbook for students:
(1961) Introduction to the study of animal pop-
ulations. In 1962, Herbert was appointed chair-
Andrenidae man of the Zoology Department. In the 1960s,
with collaborators, he developed a program for
A family of bees (order Hymenoptera, superfamily control of Dacus tryoni, Queensland fruit fly,
Apoidae). by release of sterile males. His next book, also
Bees co-authored with L.C. Birch was (1984) The
Wasps, Ants, Bees and Sawflies ecological web. He died on January 27, 1992, fol-
lowing his wife by some years, but survived by his
son and daughter.

Andrewartha, Herbert George

Herbert Andrewartha was born in Perth, Australia,

Reference
on December 21, 1907. In 1924, he entered the Uni-
Birch LC, Browning TO (1993) Herbert George Andrewartha
versity of Western Australia from which he obtained 19071992. Historical Records of Australian Science
a bachelors degree in agriculture. He was then 9(3), Available at www.asap.unimelb. edu.au/bsparcs/
appointed as assistant entomologist by the Western aasmemoirs/andrewar.htm Accessed August 2002
 Angel Insects (Zoraptera)
A 157

Androconia Angel Insects (Zoraptera)

In Lepidoptera, glandular wing and body scales. This is a small group of minute insects. They are
Scent scales. infrequently encountered, and poorly known. The
order name is based on the Greek words zoros
(pure), a (without), and pteron (wing). There are
Androparae only about 30 species described, all in the family
Zorotypidae.
In aphids, viviparous females that are produced on
the secondary host in the autumn, and then fly to
the primary host to produce males. Characteristics
Aphids
Angel insects are only about 3 mm long, with a
wing span of 7 mm. They are dimorphic: a wing-
Anemometer less form that lacks eyes, ocelli, and is only
slightly pigmented, and a winged form (Fig. 49)
An instrument used for measuring wind speed, an that bears eyes, ocelli, and is darker in color. They
important tool when considering use of pesticides have chewing mouthparts. The antennae are
because high wind speeds can result in pesticide filiform, and consist of nine segments. The
drift. legs are unspecialized, the tarsi 2-segmented.
The wings have simplified venation, and the
wings can be shed, as is the case with termites.
Anemotaxis The abdomen is cylindrical and consists of
11segments. Very short, 1-segmented cerci
A movement in response to air movement or air occur near the tip of the abdomen. Metamor-
currents. phosis is not pronounced.

Angel Insects (Zoraptera), Figure 49 A diagram of an angel insect showing a dorsal view. The wings are
removed from the left side of the body.
158
A Angoumois Grain Moth, Sitotroga cerealella (Lepidoptera: Gelechiidae)

Biology In humans the same disease is known as African

sleeping sickness or human trypanosomiasis. It is
Angel insects are found beneath bark, in humus, transmitted by tsetse flies in Africa.
decaying wood, and sometimes in association with Trypanosomes
termites. They are believed to feed on fungi. Appar- Tsetse Flies
ently they swarm, and drop wings after swarming. Sleeping Sickness or African Trypanosomiasis
They are gregarious, but there is no evidence of
social organization.
Anisembiidae
References A family of web-spinners (order Embiidina).
Web-spinners
Arnett RH Jr (2000) American insects, 2nd edn. CRC Press,
Boca Raton, FL, 1003 pp
Riegel GT (1987) Order Zoraptera. In: Stehr FW (ed) Imma-
ture insects, vol 1. Kendall/Hunt Publishing, Dubuque,
Anisopodidae
Iowa, pp 184185
Gurney AB (1938) A synopsis of the order Zoraptera with A family of flies (order Diptera). They commonly
notes on the biology of Zorotypus hubbardi Caudell. are known as wood gnats.
Proc Entomol Soc Wash 40:5787
Flies

Angoumois Grain Moth, Sitotroga Anneal

cerealella (Lepidoptera:
Gelechiidae) The process by which the complementary base
pairs in the strands of DNA combine.
This is an important primary pest of stored grain.
Stored Grain and Flour Insects
Annual
Angulate
A plant that normally completes its life cycle of
seed germination, vegetative growth, reproduc-
Forming an angle.
tion, and death in a single growing season or year.

Anholocyclic Life Cycle

Anobiidae
A life cycle in which there is a complete lack of
male insects (generally aphids). In this type of life A family of beetles (order Coleoptera). They com-
cycle only viviparous parthenogenetic females are monly are known as death-watch beetles.
present throughout the year. (contrast with holo- Beetles
cyclic life cycle)
Aphids
Anomosetidae
Animal Sleeping Sickness A family of moths (order Lepidoptera). They also
are known as Australian primitive ghost moths.
Also known as nagana, this is a disease of animals Australian Primitive Ghost Moths
caused by protozoans in the genus Trypanosoma. Butterflies and Moths
 Antennae of Hexapods
A 159

Anoplura Antennae of Hexapods

A suborder of wingless ectoparasitic insects com- severiano f. gayubo
monly known as sucking lice (order Phthiraptera). Universidad de Salamanca, Salamanca, Spain
It is sometimes treated as an order.
Chewing and Sucking Lice According to the known data on anatomy and
embryology, the antennae are postoral structures
of an appendicular nature that have been dis-
Anostostomatidae placed, and now situated secondarily above the
anterolateral regions of the cranium, in front of
A family of crickets (order Orthoptera). They the mouth.
commonly are known as wetas and king crickets. Taking into account their intrinsic muscula-
Grasshoppers, Katydids and Crickets ture, two fundamental types of antennae can be
distinguished:
Anteclypeus
The lower of the two divisions of the clypeus. Segmented Type
Mouthparts of Hexapods
Each antennal division (antennomere) possesses
intrinsic musculature (although the last segment
generally lacks it). This type is found in Diplura
Antagonist and Collembola.

An antagonist usually is an organism (usually a

pathogen) that does no significant damage to the Annulated Type
host, but its colonization of the host protects the
host from significant subsequent damage by a pest. Three segments are recognized that, from the basal
to the apical zone of the antenna, are called scape,
pedicel and antennal flagellum (Fig. 50).
Antecosta (pl., antecostae) The scape is a robust segment that unites the
head capsule with a cuticular reinforcement (Fig. 51),
An internal ridge on the anterior portion of a ter- the antennal socket (also called the torulus). In the
gum or sternum. It serves as a point of attachment antennal socket one or two condyles are distin-
for the longitudinal muscles. guished, which serve to articulate the scape. The
second segment is called the pedicel, and it
usually varies in form and development, although
Antenna (pl., antennae) it is generally small. Lastly, the flagellum is usu-
ally divided into several divisions called
The paired segmented sensory organs, borne one flagellomeres.
on each side of the head. The antennae commonly The movement of the antennae is carried
protrude forward. Each antenna (Figs. 50 and 51) out through extrinsic or motor muscles of the
consists of three segments: the basal scape, a small scape, generally forming three or four functional
pedicel, and an elongate flagellum. The flagellum groups. Depending on the insect group, these
is usually subdivided into many sections. muscles are inserted in the head capsule or in
Antennae of Hexapods the tentorium.
160
A Antennae of Hexapods

lateral ocellus
compound eye
scape
pedicel postocular area
cervix
flagellum
gena

cervical sclerites
tentorial suture
basimandibular sclerite
maxilla
clypeus labium

labrum labial palpus

mandible

maxillary palpus

Antennae of Hexapods, Figure 50 Side view of the head of an adult grasshopper, showing some major
elements.

The antennae usually have bristles and antennae with respect to the head, the direction
s ensilla of different types that act as chemore- and force of the wind, or of the water currents in
ceptor-, thermoreceptor- or hygroreceptor-type aquatic insects. In addition, it can act as an audi-
sensory organs. In addition, the antennae of tory organ in male mosquitoes and chirinomids,
males display modifications tending to increase which perceive the sound produced by the
their surface area, which permits harboring a females in flight.
great number of sensilla and acting as detectors The number of flagellomeres is a character
that detect pheromones emitted by the females, that, in certain cases, is related to the sex, as
and enable (usually) the males to locate the occurs in some Aculeate Hymenoptera in which
females for reproductive functions. Certain the males display 11 flagellomeres and the
modifications in the antennae of the males can females 10. In others, it represents an important
also be related to particular courtship behavior taxonomic character, emphasized in this sense
prior to mating. the family Argidae (Hymenoptera: Symphyta)
In relation to the functions carried out by whose individuals display the flagellomere
the antennae, it is necessary to highlight the undivided.
presence, in the pedicel, of Johnstons organ, Various types of antennae exist (Fig. 52), the
which is formed by cordotonal sensilla. It is appearance of which is owed fundamentally to the
fundamentally a proprioreceptor organ that variation in form and development of the flagellom-
provides information about the position of the eres. The most important are:
 Antennae of Hexapods
A 161

vertex flagellum

antenna
frons pedicel
scape

median ocellus

face

anterior tentorior pit

basimandibular sclerite
frontoclypeal suture
mandible
clypeus
clypeolabral suture
labrum

maxillary palpus
maxilla

labial palpus
Antennae of Hexapods, Figure 51 Front view of the head of an adult grasshopper, showing some major
elements.

Filiform Aristate

The flagellomeres, normally numerous, are nar- The last flagellomere is normally very wide and
row, cylindrical, and of similar size. It is the most bears a conspicuous bristle named the arista.
common type in the insects. Examples are found in Diptera (Syrphidae and
Muscidae).

Moniliform

There exists a narrowing in the union of each Stylate

flagellomere, which are more or less spherical, with
the antenna acquiring a rosaried appearance The last flagellomere is prolonged apically in a
(like the beads of a rosary). There are examples in fine and elongated process named the style. Exam-
various families of beetles. ples are found in Diptera (Rhagionidae and
Asilidae).

Setaceous

The flagellomeres are extremely fine and dimin- Clavate

ish in diameter gradually toward the tip; the
antenna thus acquires an appearance of seta or The flagellomeres increase in diameter gradually
hair. The antennae of Odonata constitute a typical toward the apex. Examples are found in Coleoptera
example. (Coccinellidae and Tenebrionidae).
162
A Antennae of Hexapods

Antennae of Hexapods, Figure 52 Some common types of antennal forms: A, filiform; B, moniliform;
C, capitate; D, clavate; E, setaceous; F, serrate; G, pectinate; H, bipectinate; I, plumose; J, aristate;
K, stylate; L, lamellate; M,flabellate; N, geniculate.

Capitate Pectinate

In this case the last flagellomeres are of greater The flagellomeres project laterally, forming a fine
diameter, in contrast with the preceding, forming and more or less elongated projection. When it is
aclub ormace. Examples are found in Coleoptera produced over two sides of each flagellum, the
(Nitidulidae and Silphidae). antennae are called bipectinate. Examples are
found in Coleoptera (Pyrochroidae).

Serrate Flabellate

The flagellomeres display pointed, lateral prolon- The flagellum displays long, flattened or more or
gations, on one side or on both. Examples are less cylindrical expansions. Examples are found in
found in Coleoptera (Elateridae). some species of Coleoptera (Scarabeidae).
 Anther Smut of Carnations
A 163

Lamellate Antennal Fossa

Only the last flagellomeres display long, lateral A groove or cavity in which the antennae are
expansions. Examples are found in Coleoptera located or concealed. This is also called the anten-
(Scarabeidae, subfamily Melolonthinae). nal insertion.
Antennae of Hexapods

Plumose
Antennal Sclerite
Flagellomeres with numerous long hairs are
arranged in a feather-like or whorled form. Exam- A ring into which the basal joint of each antenna
ples are found in male mosquitoes (Diptera). is inserted.
Antennae of Hexapods

Geniculate
Antennation
The scape is relatively long, forming a clear angle
Sensory or tactile movements with the antennae
with the rest of the antenna (pedicel plus flagel-
that result in contact of the antennae with an object.
lum). Examples are found in Hymenoptera (For-
micidae and Chalcidoidea), and in Coleoptera
(Lucanidae). Within this type of antenna, particu-
Antennule
lar variations can exist, as in the case of the
Ormyridae (Hymenoptera: Chalcidoidea), in A small antennal or feeler-like process.
which the first divisions of the flagellum are of a
lenticular type (lens shaped, or double convex).
Anterior
References This term usually is used to refer to the end of the
body containing the head, or the direction of
Denis JR, Bitsch J (1973) Morphologie de la tte des insects.
In: Grass PP (Dir) Trait de Zoologie, VIII (I):1593
thehead, or the front of the insect.
Gillot C (1995) Entomology, 2nd edn. Plenum Press, New
York, NY
Manton SM (1977) The Arthropoda. Habits, functional mor-
phology and evolution. Clarendon Press, Oxford, UK
Anthelidae
Quinnec E (2001) Insights into arthropod head evolution.
Two heads in one: the end of the endless dispute? A family of moths (order Lepidoptera) also known
Annales de la Socit Entomologique de France as Australian lappet moths.
37:5170 Australian Lappet Moths
Snodgrass RE (1951) Comparative studies on the head of
mandibulate Arthropods. Comstock, Ithaca, NY Butterflies and Moths

Antennal Club Anther Smut of Carnations

On a clubbed antenna, the enlarged distal This is a fungal disease of carnations that is trans-
segments. mitted by insects.
Antennae of Hexapods Transmission of Plant Diseases by Insects
164
A Anthicidae

Anthicidae utterflies and moths (Lepidoptera), wasps, ants

b
and bees (Hymenoptera), but also numerous
A family of beetles (order Coleoptera). They com- flies (Diptera), beetles (Coleoptera) and thrips
monly are known as antlike flower beetles. (Thysanoptera).
Beetles Pollination and Flower Visitation
Butterfly Gardening
Night Blooming Plants and their Insect
Anthocoridae Pollinators
Pollination by Yucca Moths
A family of bugs (order Hemiptera). They some- Apiculture
times are called minute pirate bugs. Plant Extrafloral Nectaries
Bugs

Anthribidae
Anthomyiid Flies
A family of beetles (order Coleoptera). They com-
Members of the family Anthomyiidae (order
monly are known as fungus beetles.
Diptera).
Beetles
Flies

Anthomyiidae Anthrophagy

A family of flies (order Diptera). They commonly Feeding on humans by other organisms. The most
are known as anthomyiid flies or root maggots. common anthrophagous organisms are insects,
Flies particularly biting flies, followed by lice, fleas, and
ticks.
Mosquitoes
Anthomyzid Flies Lice
Fleas
Members of the family Anthomyzidae (order Ticks
Diptera). Pathogen Transmission by Arthropods
Flies

Anthrophoridae
Anthomyzidae
A family of bees (order Hymenoptera, superfamily
A family of flies (order Diptera). They commonly
Apoidae). They commonly are called cuckoo bees,
are known as anthomyzid flies.
digger bees, and carpenter bees.
Flies
Bees, Wasps, Ants and Sawflies

Anthophilous Anthropocentric
Flower loving. Most insects that feed on nectar An interpretation based on the belief that humans
or pollen are anthophilous, including many are the central fact or element of the universe,
 Antlions
A 165

and interpreting everything in relation to human Anti-Drift Agent

values of interests.
A compound that is added to pesticides to
reduce the number of droplets produced at the
Anthropomorphism
spray nozzle, and therefore to reduce the possi-
bility of the product drifting away from the
The attribution of human qualities or forms to
target.
animals or their behaviors.

Anthropophilic Antixenosis

An insect that prefers humans as a source of food. An effect due to a characteristic, often a physical
A blood-sucking insect that feeds on humans. or chemical attribute of a plant, that deters
feeding or oviposition. This is also called
nonpreference.
Antibiosis Plant Resistance to Insects

A characteristic, often a chemical within a plant,

that inhibits survival or reproduction when an
insect feeds upon it. Antlike Flower Beetles
Plant Resistance to Insects
Members of the family Anthicidae (order
Antibiotic Coleoptera).
Beetles
A chemical produced by a microorganism that
affects the ability of another microorganism to
survive or grow. Antlike Leaf Beetles

Members of the family Aderidae (order

Anticodon Coleoptera).
Beetles
The triplet of nucleotides in a transfer RNA mol-
ecule that is complementary to and base pairs with
a codon in a messenger RNA. Antlike Stone Beetles

Members of the family Scydmaenidae (order

Antidote
Coleoptera).
A treatment used to treat the effects of chemical Beetles
(e.g., insecticidal) poisoning.

Antlions
Antidiuretic Hormones
Members of the family Myrmeleontidae (order
Hormones acting on the hindgut to promote water Neuroptera).
reabsorption and conservation. Lacewings, Antlions and Mantidflies
166
A Ant-plant Interactions

Ant-plant Interactions microbes contribute to the colonys N economy

through N-recycling and possibly upgrading (con-
diane w. davidson version of non-essential to essential amino acids).
University of Utah, Salt Lake City, UT, USA When disturbed by ants, many active insects
and other animals can simply fly or walk to safety,
Drop a spoon at a picnic and the ubiquity of ants but for plants and their seeds, as well as for com-
(family Formicidae) is soon apparent. Ants are paratively immobile nesting animals and juvenile
everywhere, lurking in leaf litter or brazenly scour- insects, there are no ready escape routes. It is in
ing terrestrial and arboreal habitats for food in any these organisms that we find some of the most
form. Except in extreme climates that are inhospi- unique or unusual adaptations for both defending
table to insects, most terrestrial organisms have against ants and exploiting their behaviors to
necessarily evolved ways to reduce the damage advantage. Here, several categories of interactions
ants can cause, and many have managed even to between ants and plants are explored, together
extract benefits from them. Relationships between with some of the myriad ways in which plants have
ants and humans provide examples: not only have evolved to reduce or promote association with
we devised means of protecting our food stores these ubiquitous insects. Included also are the
from ants, but we have utilized ants to protect our influence of plant resources on ant ecology and
food. Centuries ago, nests of Old World weaver evolution, and the effects of ants on the evolution
ants (Oecophylla smaragdina) were cultivated in of plant defenses.
Asian orchards to control plant pests. Workers of
this highly predatory species captured and
devoured both the juvenile and adult stages of Ants as Seed Predators
herbivorous (plant-eating) insects.
In some ways, early ants were better suited to In warm deserts and other arid regions, ants are
serve plants than to injure them. Descended from often both abundant and diverse, and annual and
predatory wasps, they were poorly adapted for perennial plants are present more often as seeds
herbivory (consumption of plant tissues), and no than as adults. Here, seed-eating ants abound and
ant is truly folivorous (leaf-eating). Unable to may exert strong selection pressures on plant.
digest cellulose themselves, ants also differ from Selection is mediated mainly by seed consump-
termites in lacking gut microbes that can do this tion, but also by ant effects on soil disturbance and
for them. Although much of the plant world is nutrient availability. Seed-eating harvester ants
therefore not available to ants, plant sap, seeds, typically return seeds individually to a central nest
and fruit pulp are relatively easy to digest, and site where they husk and then cache them in
many (mostly arboreal) taxa feed on those underground granaries, often for long time peri-
resources. Such foods tend to be rich in carbohy- ods. By storing foods that degrade slowly over
drate (CHO) but poor in nitrogen (N) (amino time, ant colonies can persist in habitats where the
acids, peptides and proteins), and dietary excesses production of seeds and other resources is spo-
of energy-rich CHOs may have subsidized coloni- radic and unpredictable. During periods of low
zation of the arboreal zone, where foragers must food availability, many of these ants simply remain
commute around a three-dimensional and poorly underground and forego the risks and poor
connected environment. Most ants also scavenge rewards of external activity.
N-rich arthropod carrion, and many are active The small individual sizes and ectothermy of
predators that can potentially benefit plants by ants are correlated with low foraging costs, enabling
attacking their herbivores. In some taxa, associa- these insects to forage economically even for
tions with intracellular and extracellular gut tiny seeds with dispersed distributions. Ants can
 Ant-plant Interactions
A 167

vertebrate seed-eaters like rodents and birds. Those

taxa have higher foraging costs and tend to spe-
cialize in feeding on seeds in high density
hotspots, either in soils or on the plants them-
selves. Though reduced seed densities can poten-
tially affect both plant densities and community
composition, ants may commonly have less impact
on plant communities than do vertebrate seed
predators. This is so because seed predation by
ants tends to fall most heavily on offspring of
small-seeded plant species, whereas that by verte-
brates often targets large seeds. Seedlings germi-
nating from large seeds begin life with more
resources than do those from small seeds and are
therefore superior competitors within plant com-
munities. Consequently, the removal of small seeds
by ants has comparatively little effect on the densi-
ties of large-seeded species, while the removal of
large seeds by rodents may lead to increases in the
densities of small-seeded species.
In at least some localities, differences in seed
size specialization by ants and rodents account for
disparities in the short-term and long-term effects
of these granivores on one anothers populations.
When seed-eating rodents were removed experi-
mentally in one study, densities of harvester ants
first increased and then declined. The short-term
increase was likely due to competition between
the two types of granivores, as there was some
overlap in the sizes and species of seeds used by
the two groups. However, rodent removal eventu-
ally led to increases in the densities of large-seeded
plants, which subsequently out-competed small-
seeded species, to the long-term detriment of
ants.
Coexisting species of harvester ants often dif-
fer in worker body sizes, and small ants cannot
carry the largest seeds. To a degree, therefore,
worker size differences may remove small and
Ant-plant Interactions, Figure 53 An extensive
large ants from resource competition with one
nest of leaf-cutter ants in the genus Atta (above)
another, and also determine disparate effects on
and high rates of leaf removal from an unlucky
plant communities. When ant communities are
tree (below).
disturbed, either directly or by the introduction of
therefore reduce soil seed banks to lower levels non-native ants, there can be consequences for
than can large, endothermic (warm-blooded) plant communities. Pathways of interaction can be
168
A Ant-plant Interactions

indirect and complex. For example, if an intro- adjacent to the anterior digestive tract in the head.
duced ant species produces a decline in popula- After mating, she removes her wings, excavates a
tions of a native harvester ant, plant species on terrestrial nest, begins to cultivate her fungal gar-
which the native ants specialize may increase at den, and feeds her first worker brood on trophic
the expense of other components of the plant eggs composed of resources from her degraded
community. Such changes in community compo- wing muscles.
sition are hard to predict, and often become appar- Workers eventually take over cultivation
ent only over long time periods, especially in arid and maintenance of the fungal gardens. Larger
lands with variable climates. castes cut, drop, and carry the leaf fragments,
On an evolutionary time scale, some plants while their smaller nestmates hitch-hike rides
have acquired adaptation that reduce depredation on leaf fragments to defend larger workers
of their progeny by ants. An example of such an against parasitic phorid flies, and care for brood
adaptation is the use of hygroscopic awns (e.g., inside the nest. There, they lick and shred leaf
that of Erodium cicutarium) that alternately extend fragments into finer pieces, and then chew their
and coil when wet and dry, respectively, pushing edges, depositing fecal droppings with digestive
the attached seeds beneath the soil surface. Unlike enzymes to aid in decomposition. Protein-de-
seed-eating rodents, harvester ants have little grading enzymes are recycled from the fungi
access to individually buried seeds, so such awns themselves through the ants digestive system,
do appear to proffer a refuge from predation by which lacks enzymes to degrade them. New leaf
granivorous ants. Whether mechanical, chemical, fragments are then inoculated with mycelia of
or phenological (e.g., timing of seed production), older parts of the garden and fertilized with
mechanisms of seed escape from granivorous ants plant material (recent attines) and/or feces and
remain poorly explored. animal matter (early attines). Through applica-
tion of growth hormones, enzymes, nutrients,
and antibiotics, higher attines maintain their
Early Farmers (Attines) fungi almost in monocultures. Nevertheless,
recent studies by M. Poulsen, C.R. Currie, and
To the uninitiated, the cutting and transport of leaf, colleagues have identified a virulent fungal
flower and fruit fragments by New World ants in pathogen of the gardens, as well as a bacterium
the tribe Attini looks a great deal like herbivory living in fovea (small depressions) in worker
(Fig. 53). However, as was originally proposed by exoskeleton. These filamentous bacteria, or
Thomas Belt, a nineteenth century British mining actinomycetes, produce antibiotics directed
engineer and amateur naturalist, the ants them- mainly toward the common pathogen.
selves do not digest cut leaves. Rather, they culti- Although most folivorous insects are limited
vate fungi that degrade cellulose and other plant to eating a narrow spectrum of plant species, use of
products otherwise inaccessible to the ants. In fungi as agents of digestion may explain leafcutter
more recent members of this group (species of Atta tolerance of more varied diets. Nevertheless, differ-
and Acromyrmex), the workers themselves feed on ent taxa of higher attines specialize on grasses or
plant sap released from cut leaves, whereas larvae dicots, and specialization exists even within those
are fed gonglydia, or swollen tips of fungal hyphae categories. Like other herbivores, leafcutters are
(arms). Together, fungal mycelia and gongylidia especially likely to harvest tender young leaves,
supply CHOs (simple sugars, as well as glycogen in which lack the fiber and lignin to make them tough.
Acromyrmex), lipids and N (amino acids and pro- For Atta cephalotes, J.J. Howard and colleagues
tein). On her nuptial flight, the queen carries frag- showed that, the diet is apparently not chosen in
ments of fungal gardens in her infrabuccal chamber, response to energy, nitrogen, or moisture content,
 Ant-plant Interactions
A 169

but rather to avoid various terpenoids that could

poison fungi.
According to U.G. Mueller and colleagues, all
attines appear to have descended from a common
ancestor that forged relationships with fungi either
growing on walls of leaf-litter nests or using ants
to disperse their spores. Together, with gene
sequence data, the fossil record, and confinement
of this group to the New World, suggests that this
ant-fungal partnership first formed between 45
and 65 million years ago. Direct transmission of
fungi from queens to reproductive daughters pro-
vided opportunities for greater specialization and
dependency to evolve in both partners. Neverthe-
less, new fungal species have also been domesti-
cated by older, less specialized ant taxa in recent
times.
The success of the attine-fungal partnership is
measurable in its impact on the forest. Mature Atta
nests can range over several hundreds of square
meters, and worker columns can reach trees more
than 100 m from the colony along trails cleared of
vegetation. In tropical areas not regularly flooded,
attines can be very abundant and exact a consider-
able toll on plants. Some accounts in the literature
judge them to be responsible for 1217% of all
herbivory, but these figures may be too high
because they fail to include the mostly invisible
losses of plant resources to sap-feeding insects.
Throughout much of the Neotropics, higher attines
also thrive in disturbed areas dominated by poorly
defended pioneer (weedy) plant species. They are
similarly destructive to agriculture, and cause mil-
lions of dollars in losses annually to crop plants Ant-plant Interactions, Figure 54 Ants tending
that have been selected by humans for low Hemiptera outside and inside plant stems: (above)
toxicity. Azteca tending mealy bugs ( Pseudococcidae) in
the New World tropics, and (below) Podomyrma
sp. tending scale insects (Coccidae, arrows)
Pastoralists inside branches of Chisocheton (Meliaceae) near
Madang, Papua New Guinea.
Ants may also affect plants indirectly through the
farming (or tending) of insects in the order include aphids, leafhoppers, treehoppers, scale
Hemiptera. With mouthparts highly modified as sty- insects, and the like. Because plant sap is N-poor, sap-
lets, or soda straws, these insects are phloem- or feeding hemipterans must process large quantities of
xylem-sucking consumers of plant sap (Fig. 54) and these liquids to concentrate sufficient nitrogen for
170
A Ant-plant Interactions

growth and reproduction. Moreover, while they feed, This net outcome can be positive if herbivores are
their relatively immobile immature or nymphal abundant and tending ants are effective in driving
stages are exposed for long time periods to the risks them away. However, as hemipteran populations
of predation and parasitism. As a by-product of pro- thrive and grow under ant protection, removal of
cessing large quantities of sap for N, many Hemiptera large quantities of sap can threaten the host plants
release excess sugars as honeydew from their abdo- health. Living in intimate contact with hosts,
mens. When compensated by this attractive resource, Hemiptera also transmit viral and other plant
ants forego predation of these insects and even pro- pathogens. Not surprisingly then, plants appear to
tect them from other natural enemies. Relatively have fought back over evolutionary time. For
N-rich tissues like young leaves, and the pedicels of example, hairs (trichomes) on leaves or stems pre-
flowers and fruits, are particularly good sites for sap- vent hemipteran stylets from reaching the plant
feeders and the ants which herd them there. In Asian surface. Other evolved responses are best under-
rain forests, where plant reproduction is highly spo- stood in the context of the old adage that the
radic, ants in the genus Dolichoderus have evolved as enemy of my enemy is my friend. Thus, many
migratory herdsmen, carrying their sap-feeding plants may have short-circuited the Hemiptera out
mealy bugs over long distances in search of optimal of these tripartite interactions by paying the ants
feeding sites. directly, i.e., by provisioning them with carbohy-
Hemipteran tending, often compared to drate rewards in the form of sugar-rich extrafloral
human tending of domestic livestock, is a main- nectars (EFNs, Fig. 55) or lipid-rich pearl bodies
stay for many arboreal ants. Still, to balance their (PBs). J.X. Beccera and D.L. Venable hypothesize
diets, ants occasionally harvest some of the tender that by increasing the CHO:protein ratio in the
hemipteran nymphs and consume N-containing ants own diets, plants induce ants to consume
hemolymph of these and other arthropods. The more of their Hemiptera. Arguing against this
relative strengths of positive and negative effects hypothesis for the origin of EFNs are observations
of the ants (herbivore reduction vs. hemipteran of ants tending both sap-feeders and EFNs. Despite
tending) determine the net effect of ants on a such observations, D.W. Davidson and colleagues
plants well-being and reproduction (i.e., its fitness). have proposed that the hypothesis might help to

Ant-plant Interactions,Figure 55Myrmecophyte-produced food rewards for ants: (left) Extrafloral

nectaries (EFNs) at the junction of leaf blade and petiole of Endospermum medullosum (Euphorbiaceae)
near Madang, Papua New Guinea; (right) pearl bodies (PBs) on lower leaf surface of Cecropia engleriana
(Cecropiaceae) at Cocha Cashu, Peru. Both EFNs and PBs also occur in myrmecophilic plants.
 Ant-plant Interactions
A 171

explain early divergence in foraging habits of provisioning of resources, and the plants indirectly,
major ant taxa that differ in their propensity to usually through deterrence of damaging herbi-
tend hemiptera versus EFNs. vores. Mostly, these interactions are opportunistic
and unspecialized, depending on which ants, her-
bivores, and plants co-occur within a community.
Biotic Defenses of Plants Plants with opportunistic ant associations based
on production of food rewards alone are said to be
Even in relationships not (or no longer) involving myrmecophilic or ant-loving. In contrast, at
Hemiptera, production of ant attractant foods tropical latitudes, many ant-plant relationships
should increase the presence of ants on vegetative have become more highly specialized and obliga-
and reproductive plant tissues and help to deter a tory. That is, in the context of their natural com-
variety of insect and other herbivores. Plant adap- munities, partners cannot survive and reproduce
tations for defense by ants, wasps and other poten- in the absence of their associates. In this case, resi-
tial predators of insect herbivores are referred to dent phytoecious ants protect their host plants,
as biotic defenses, since they require the collabo- (Fig. 56) and myrmecophytes (true ant-plants)
ration of other living things. provide not only food but housing in stem or leaf
structures termed domatia. Individual ant colonies
and myrmecophytes may live together over sub-
Some Definitions and Constructs stantial portions of their life histories in relation-
ships therefore termed symbiotic mutualisms.
Whether the anti-herbivore protection of plants by (Although often used incorrectly in place of
ants is afforded through consumption of Hemiptera mutualism, the term symbiosis - literally living
or deterrence of other herbivores, such protection together - is value neutral, including negative
completes the requirement for what are termed interactions like parasitism, as well as mutually ben-
mutualistic interactions. Both parties in these eficial interactions.) Cheater ants, which benefit plants
relationships benefit, the ants directly from plant less than the evolved partner, or otherwise negatively

Ant-plant Interactions, Figure 56 Caulinary (left) and foliar (right) domatia of ant-plants. Forming the
domatia of many myrmecophytes are swollen stems or support structures, either naturally hollow or with
weak pith, removed by ants. Shown here (left) is a branch of Duroia hirsuta (Rubiaceae, vic. Iquitos, Peru),
swollen at attachment of large opposite leaves. Tiny ants in genus Myrmelachista inhabit these n aturally
hollow caulinary domatia. Foliar domatia, like that shown here for Tococa sp. (Melastomataceae, from
Cocha Cashu, Peru) (right) are highly modified and more obviously evolved to accommodate ants.
172
A Ant-plant Interactions

impact hosts, may occasionally prevail in sym

bioses because they are better colonists or
competitors.
In symbiotic ant-plant relationships, partners
are more likely to have undergone coevolution, i.e.,
reciprocal genetic (evolutionary) responses to
selection pressures exerted by each partner on the
other. Coevolution has two aspects: coadaptation
and cospeciation, and only the former occurs fre-
quently in symbiotic ant-plant partnerships. Illus-
trating coadaptation (reciprocal adaptation), many
plants have evolved restrictive (Fig. 57) entrances
to their domatia as a means of favoring coloniza-
tion by certain ant taxa over others, while queens
of phytoecious ants have responded by evolving
traits enabling them to recognize and colonize such
entrances expeditiously. Similarly, plants and ants
may have coadapted with respect to the types or
sizes of food rewards offered (Fig. 58) and their uti-
lization or accessibility. In contrast, cospeciation
(the co-radiation of ant and plant lineages to give
congruent phylogenies) appears to be quite rare
even in tropical symbiotic ant-plant relationships.
Rarity likely results from the fact that ant and plant
propagules (i.e., new queens and seeds) disperse
independently, leaving much opportunity for new
partnerships to form over evolutionary time. Seeds
must germinate and produce seedlings of a thresh-
old size before the next generation of hosts can
support ant colonies. Environmental variation or
randomness in the abundances of, and proximities

Ant-plant Interactions, Figure 57 The prostomata

(stem entrances) of Cecropia species come in
various sizes and forms correlated with host use
by different ant taxa: Cecropia engleriana (above)
produces a narrow inverted prostoma, recognized
and colonized by comparatively small queens
of Azteca australis (Dolichoderinae) (center);
in c ontrast (below), those of Cecropia sp. nov
(pungara) are convex and covered in u rticating
hairs; this host species attracts much larger
queens of a ponerine ant, P achycondyla luteola.
Both photos are from Cocha Cashu, Peru.
 Ant-plant Interactions
A 173

Plants Ants

Ant-plant Interactions, Figure 59 A hypothetical

case of cospeciation, illustrated by the congruent
or mirror-image phylogenies (= genealogies, solid
dark lines) of associated (dotted lines) ant and plant
taxa. On each occasion when a plant species splits
into two distinct taxa, the associated ant lineage
also undergoes a speciation event. For cospeciation
to have occurred, splits in plant and ant lineages
must have occurred contemporaneously and be
attributable to selection imposed by the partner.
Otherwise, an ant lineage may have just radiated
secondarily over a pre-existing plant lineage.
The dotted and grey lines depict two kinds of
evolutionary colonization events: respectively,
host switching and de novo colonization by a
previously unassociated ant lineage.

icture contrasts sharply with that for, e.g., higher

p
attines and their fungi; there, I.H. Chapela and col-
leagues have shown that queens transmit fungi
between generations of colonies, and phylogenies
of the two lineages are largely congruent (Fig. 59).
Despite little evidence for cospeciation in sym-
biotic ant-plant associations, contemporaneous
diversification within partner lineages may occur
through diffuse coevolution, defined by D.H. Janzen
as reciprocal evolutionary responses to a suite
Ant-plant Interactions, Figure 58 Food bodies of
of potential partners. Additionally, if host availabil-
myrmecophytic Cecropia also come in different
ity were often limiting, phytoecious ants may
sizes, as shown here for Cecropia membranacea
frequently have colonized non-myrmecophytic rel-
(above), usually associated with tiny Azteca ants,
atives of those plants, exerting new selection on
and closely related Cecropia sp. nov. (pungara)
these species to evolve ant-attractive traits. Based
(below), housing the much larger Pachycondyla
on multiple independent origins of myrmecophy-
luteola. Both are from at Cocha Cashu, Peru.
tism in older and more recent Asian Macaranga,
to, sources of colonizing queens, provide ample S.-P. Quek and colleagues have proposed just such a
opportunity for host-switching or de novo coloni- scenario. A parallel argument is that, lacking their
zation by previously uninvolved ant taxa. This typical associates, habitat-switching hosts could
174
A Ant-plant Interactions

have provided evolutionary opportunity for the ori- against vertebrates (including many an unfortu-
gin of new phytoecious ant taxa. nate investigator), they appear often to include
These examples are relevant in the context of comparatively weakly competitive ant taxa that
the different selection pressures driving diversifi- persist only in association with myrmecophytes.
cation in myrmecophytes versus phytoecious ants. Several plant traits, separately or in combination,
As noted by D.W. Davidson and D. McKey, prolif- contribute to the capacity of these plants to serve as
eration of plant species has been driven principally refugia from natural enemies. First, many myrme-
by colonization of new habitats, accompanied by cophytes produce nutritionally complete food
evolution of new defensive strategies and (corre- rewards that eliminate the need for resident ants to
lated) growth rates, etc. In contrast, ants have forage in more competitive environments off their
diversified mainly in response to biogeographic hosts. Acacia and Macaranga are examples. Second,
factors and (especially) plant traits favoring cer- derived from taxa in which stem hairs are com-
tain associates over others (below). Why this asym- mon, a number of myrmecophytes possess stems
metry? Plants grow through seedling stages and domatia covered with long, dense hairs
without their ants, and their success during this (trichomes, Fig. 55) that exclude larger-bodied
most vulnerable period depends on factors such as enemy ants, competitors and perhaps predatory
light and nutrient regimes, i.e., on habitat. Addi- army ants, while permitting tiny resident taxa to
tionally, any of several ant taxa may provide commute among them. Such hosts include Cordia
acceptable protection against herbivores. In con- nodosa, Duroia hirsuta, and Hirtella spp., with tiny
trast, phytoecious ants are typically restricted to Allomerus and Azteca ants, as well as a variety of
their hosts throughout the life history, and dispari- myrmecophytic Melastomataceae. Third, many
ties in host characteristics (e.g., habitat-correlated myrmecophytes, e.g., Macaranga and Cecropia,
growth rates and investment in biotic defense) grow as little-branched, pole-like plants with few
should be highly consequential. This asymmetry points of contact over which enemy ants might
in selection pressures is reflected in both the invade from neighboring vegetation. Fourth, the
specificity of partnerships and evidence for coad- mutualism between ants and Macaranga has been
aptation. Individual Cecropia species can house shown by S.-P. Quek, S.J. Davies, and colleagues to
ants in different genera or even sub-families, while have originated on hosts with irregular wax
associated ants do not inhabit plants outside this blooms on stems. Many insects, including most
genus. Similarly, phytoecious ants of bamboos ants, have difficulty walking on epicuticular waxes,
have adapted to these hosts by evolving means of but as W. Federle and colleagues have demon-
water evacuation from nest culms (active bailing strated, wax-running ants in at least two genera
or passive engineering), and they do not live else- (Crematogaster and Camponotus) evolved to utilize
where. In contrast, no bamboo has been deter- the slippery hosts. During the co-radiation of plant
mined to have evolved ant attractants. and Crematogaster lineages, stem types (waxy or
smooth) continued to constrain host shifts.
All of the previously described traits are attri-
Factors Driving Evolutionary butes that likely preadapted plants to associate with
Specialization competitively inferior ants searching for sanctuary.
In addition, phytoecious ants themselves have often
Factors driving evolutionary specialization in phy- evolved to reduce interaction with enemies by
toecious ants are apparent from assessing both the pruning vines and other vegetation contacting
taxonomic affiliations of these ants and traits of their hosts. (This behavior may coincidentally
coadapted partners. Despite the frequent impres- enhance the hosts light environment.) At least one
sion that such ants are ferociously aggressive such ant species (Pseudomyrmex dendroicus on
 Ant-plant Interactions
A 175

Triplaris americana) even prunes leaves of its own the axillary buds of its host (Acacia drepanolo-
host when they bear invasions of enemy ants. In bium), killing apical meristems (growing tips) and
the Neotropics, a majority of pruning ants defend greatly curtailing host reproduction in the pro-
themselves using proteinaceous stings, which tend cess. However, by reducing lateral spread, destruc-
to be very effective against vertebrate enemies, but tion of meristems may also diminish potential
less effective than chemical sprays against social contacts between branches of hosts and those of
insect enemies, including many other arboreal ant neighboring acacias, some with competitively
taxa. Also suggesting that pruning evolved to limit superior ants that threaten resident colonies. Tet-
invasions of competitors, Federle and colleagues raponera penzigi, a second, competitively subordi-
find that ant taxa living on waxy-stemmed Macar- nate occupant destroys EFNs of its host, perhaps
anga hosts do not prune as intensively as do those making it less attractive to more dominant ants on
inhabiting more recent non-waxy species. The lat- neighboring hosts.
ter ants are also more recent, and the evolution of Similar conflicts of interest are apparent in
pruning in ants may have benefited host plants by neotropical ant-plant relationships. The most com-
reducing the cost of epicuticular waxes. The advent mon inhabitant of Cordia nodosa in southeastern
of pruning coincides with a switch to more gener- Peru is an Allomerus that destroys flowers and
alized host associations, as ant taxa from waxy stem fruits of its host. D.W. Yu and N.E. Pierce have
hosts expanded their host ranges to non-waxy shown that ant fecundity is greater on plants with
hosts. Finally, M. Frederickson has shown that phy- curtailed reproduction, because hosts produce
toecious ants best at pruning are not always those more domatia and associated leaves, sites of food
that are best at protecting plants from herbivores. body production. Cordia populations might be
Therefore, a myrmecophytes failure to filter out expected to decline to local extinction under such
supposed cheaters that didnt prune may be due cheating by Allomerus, but Yu and colleagues
to alternative benefits provided by the ant species have also demonstrated that alternative and benefi-
in question. cial Azteca ants are better long-distance colonists,
and that the frequency of association with these
ants increases as plant density declines. Finally, T.J.
Conflicts of Interest between Partners Izzo and H.L. Vasconcelos report that selection on
plants to fight back under similar circumstances is
As for partners in virtually all interspecific inter- apparent in relationships between Allomerus and
actions, the evolutionary interests of paired ants another Amazonian ant plant, Hirtella myrmeco-
and plants are often in conflict. For example, phila. Reproductive structures of this understory
although selection may favor ant colonies that treelet are produced only on older branches from
extract the maximum resource possible from their which leaf domatia have been aborted, and where
hosts (e.g., by tending sap-feeders, as well as con- worker ants are therefore few or absent.
suming plant-produced ant rewards), selection on
plants should magnify cost-efficiency by produc-
ing the greatest protection for the least investment Long-Term Evolutionary Histories of
in resources devoted to housing and feeding of Ant-Plant Associations
ants. The most striking examples of evolutionary
conflicts of interest come from cases where ants Over long-term evolutionary history, one can expect
modify plant architecture in ways that are benefi- ownership of host taxa to have changed hands in
cial to them but harmful to their hosts. Working in concert with changes in the fortunes of one-time ant
African savannahs, M.L. Stanton and colleagues partners and their competitors for the benefits of
have shown that Crematogaster nigriceps attacks mutualistic association. Are there regularities in the
176
A Ant-plant Interactions

trajectories that these relationships take over time? supay chacras, or devil gardens. These are
One might speculate that competition among ants orchard-like stands where all but one or two
for plants, together with filtering of ants by plants, myrmecophytes (and sometimes small, herbaceous
could produce even greater specialization by the resource plants) are killed by the tiny workers that
associated taxa, and that this might be a one-way cut major leaf veins and deposit formic acid in the
and largely irreversible process. For ants, possible wounds. Leaves necrose and die, and none but
examples involve several closely related genera of favored host and resource plants are able to recruit
tropical arboreal, stem-nesting ants in the formicine new individuals inside these bizarre areas. In sum-
tribe Plagiolepidini. (Together, these genera are set mary, it is possible that basal Myrmelachista species
apart from others in the tribe by workers possessing persist only in the absence of strong competitors, or
just 9 or 10 antennal segments.) Two Old World where competitively dominant ant taxa have driven
tropical genera, Petalomyrmex and Aphomomyrmex, lowland lineages toward increasing specialization
are each represented by just a single West African that permits coexistence with strong competitors.
species and are specialized to one and two host plant However, this hypothesis will remain conjecture
species, respectively. Because the probable closest until tested rigorously after reconstructing phyloge-
relatives of these taxa (Myrmelachista and Brachy- netic histories of associated lineages.
myrmex) occur as free-living species in the New Natural selection to magnify the colonizing
World, it seems likely that ancestors of the African and competitive abilities of particular ant associ-
species were once free-living and more widely dis- ates, coupled with that to filter cheaters, may even-
tributed, and that competition could have driven tually reduce partnerships to relationships between
Petalomyrmex and Aphomomyrmex to extreme single, highly specialized ant and plant species,
specialization. The genus Myrmelachista includes whose persistence is balanced precariously on the
both free-living and plant-associated species. On premise that each partner will thrive despite
average, the former (mainly with 10-segmented changes in the abiotic (physical) and biotic envi-
worker antennae) have generalized foraging and ronment. However, natural selection is short-
stem-nesting habits and reside mainly in high eleva- sighted, capable only of enhancing short-term
tion cloud forests along the Andean and Central fitness. Over the long term, it can neither anticipate
American mountain chains, normally above the nor respond to the threat of loss of the sole partner.
elevational ranges of dominant free-living competi- Therefore, it is reasonable to speculate that fewer
tors in ant genera Crematogaster and Azteca. At than all of the ant-plant associations that have ever
intermediate and low elevations, and within the existed still exist today. Nevertheless, the most
ranges of these dominants, J.T. Longino has found thoroughly studied evolutionary trajectories of
that congeneric species are mostly phytoecious ants, phytoecious ants are those described by S.-P. Quek
principally inhabiting hosts in plant families Lau- and colleagues for Crematogaster of Macaranga,
raceae and Meliaceae. Myrmelachista hosts generally and show wax runners breaking away from hosts
lack domatia and food rewards (i.e., are not true with waxy stems to occupy plants that should con-
myrmecophytes), and associated ants tend sap- stitute a more competitive environment.
feeders inside stem nests. At least some phytoecious
Myrmelachista occurring at intermediate elevations
apparently do not attack encircling vines, though Implications of Exudate-Feeding
a congeneric species at lower elevations (likely for the Evolutionary Ecology of
M.flavocotea in a more competitive environment) Ants
does prune vegetation contacting itshost.
Finally, in Central Amazonia, at least two dif- The most conspicuous effects of plants on ant ecol-
ferent Myrmelachista species occupy and maintain ogy and evolution involve phytoecious ants whose
 Ant-plant Interactions
A 177

colonies are specialized to live their entire life his- (above). Recently, D.W. Davidson and S.C. Cook
tories on myrmecophytic plants. However, more found that rainforest plants supply EFN at sugar
generally, plants appear to have markedly influ- concentrations far exceeding those acceptable to
enced the biology of ant taxa feeding substantially most arboreal ants. They therefore suggest that
as herbivores, either directly on plant wound high sugar concentrations may serve to manipu-
secretions and EFN, and/or indirectly, on insect late communities of attending ants by favoring the
honeydew. Such foods, collectively termed exu- most protein-limited taxa that would not forage
dates, consist principally of sugars (EFN) and for sugar at lower concentration.
water and are notoriously poor sources of essen- Finally, widespread availability of CHO-rich
tial amino acids and proteins. Though a certain plant foods in the arboreal zone undoubtedly
amount of carbohydrate might be paired with selected for domination of these foods by placing
available nitrogen sources as the nutritionally nests near the food source. For ants already nest-
complete food needed to subsidize growth and ing in leaf-litter twigs, this transition may not have
reproduction, exudate-feeders should be left with been difficult, but appropriate cavity space would
an excess of CHOs. Natural selection may then not always have been available. Many arboreal ant
favor colonies that are able to deploy excess CHO taxa have therefore evolved the capacity to con-
for acquisition of more limiting nutrient, N. struct their own nests from carton, silk, or leaves
Across the spectrum of exudate-feeding ants, cemented to one another to create cavity space.
species appear to accomplish this in one or more of
several ways. First, they may use excess CHOs to
subsidize rapid locomotion, leading to what have Some Parallels Between Ants and
been termed higher dynamic densities. Faster Plants
locomotion enables workers to cover more area per
unit time, and potentially, to encounter protein A central theme running through this article has
resources at a faster rate. Second, defense of true been that the balance of resources accessible to
spatial territories is rare among ants generally, but animals (Hemiptera and ants) affects the evolu-
appears to be commonest in species most apt to tionary ecology of these organisms by determin-
have excess CHOs to fund this costly behavior. ing the types of resources available for various
Third, N-starved ants may also reduce percent body organismal functions. This argument is no less
weight N, though there are competing explanations true for myrmecophytic plants and, in fact, was
for this pattern. Thus, evolutionary transitions from adopted by ant biologists based on its explanatory
predation and scavenging to substantial depen- power in plants. In rainforest plants, for example,
dence on plant and insect exudates correlate with E.W. Schupp and D.H. Feener have shown that N-
transitions in chemical weaponry. N-rich proteina- free but carbon-rich food rewards for ants (EFNs
ceous compounds, or N-containing alkaloidal com- and PBs) are more typical of taxa growing in dis-
pounds (both mediated by stings) are replaced by turbed habitats under high light, than of groups
N-free compounds released as volatile sprays or typical of the dark forest understory. Apparently,
sticky glues from the same or different glands. high rates of carbon-gain in open habitats enable
Whether such transitions are due to N-limitation, plants to divert some of that carbon to defense.
or the ineffective nature of C-based weaponry in A second reason why biotic defenses may
killing or paralyzing prey, is currently unsettled. occur at high frequency in fast-growing, pioneer
By paying ants mainly in CHO-rich food species of disturbed sites may relate to the shorter
rewards, myrmecophilic and myrmecophytic average leaf life spans of those species. D. McKey
plants may encourage predatory behavior by has argued persuasively that shorter leaf life spans
attending ants seeking to balance their diets should favor foliar defenses that are reclaimable,
178
A Ant-plant Interactions

i.e., can be diverted from aging leaves to more Acacia and Inga contradict this theory, and sug-
valuable young leaves as time passes. In contrast, gest that chemical and biotic defenses may be tar-
much higher, but one-time, investment in non- geted at different types of herbivores.
reclaimable defenses (e.g., the lignin and fiber With respect to ants and other social insects,
contributing to leaf toughness) are warranted only parallel reasoning might predict an inverse rela-
when the life expectancy of leaves is relatively tionship between colony growth rate and invest-
long. One can speculate that the pattern in plants ment in defense of incipient (young) colonies. One
might also be applied to predict aspects of ant form of protection for young colonies is produc-
biology. For example, a substantial, one-time tion of nanitic workers, scaled-down in size. This
investment in producing thicker (N-rich) exoskel- strategy enables young colonies to make more
eton might only be warranted in ant species with workers from a given resource base, and to spread
long-lived workers. This interesting hypothesis has the risks of foraging over more individuals. Are
yet to be tested. young workers smaller relative to normal workers
Two final patterns in defensive investment are in otherwise comparable species with intrinsically
apparent in at least some myrmecophytic plants, slow growth rates? Again, relevant data are
and may extend as well to ants and other social lacking.
insects. Comparing closely-related pairs of Cecro- In summary, ant colonies and plants share
pia species from different microhabitats at the some intriguing features that make models devel-
same rainforest site, it appears that relatively slow- oped in one taxon potentially useful to investiga-
growing taxa from shaded habitats invest in biotic tors of the other taxon. Both types of organisms
defenses both earlier and more heavily than do live anchored to a central place (not perfectly true
their faster-growing relatives from sunny habitats. for ants), grow to indeterminate size set by local
The latter pattern is understandable in the context resource availability, and add vegetative and repro-
of a cost-benefit analysis of defense. For species ductive parts in a modular way. These commonali-
growing regularly at low light, leaf replacement is ties suggest that we might eventually discover
very slow due to resource limitation, so plants additional models that are useful in explaining life
ought to defend existing leaves well. Moreover, history traits and other characters shared by the
any opportunity cost of defense (calculated in lost two groups.
growth, survivorship, and reproduction) would be
low in comparison to that for species capable of
growing rapidly in high light. The combination of Nutritional Benefits to Plants
high replacement costs and low opportunity costs (Myrmecotrophy)
is thought to select for high defensive investment.
(Applied to ants, this pattern suggests the cur- Among plants evolving associations with benevo-
rently untested hypothesis that mean colony lent ants are certain epiphytic higher plants.
growth rates are inversely related to defensive Depending on trunks and branches of other plant
investment in individual workers.) C. Brouat and species for structural support, epiphytes grow
D. McKey have argued that, in myrmecophyte lin- without directly parasitizing their hosts and obtain
eages with interspecific variation in developmen- water and nutrients from rainfall and aerial depo-
tal onset of biotic defense, precocious (early) onset sition. Because high humidity and warm tempera-
should be the derived state; however, few data are tures are conducive to this lifestyle, epiphytic
available to test this prediction. Others have sug- higher plants are exceptionally diverse and abun-
gested that costly chemical defenses produced dant in tropical lowland wet forests, and (espe-
early in development should be abandoned after cially) in misty montane forests. (Tropical Africa
onset of biotic defense, but recent tests in genera is exceptional in this regard, due to frequent and
 Ant-plant Interactions
A 179

severe droughts during the evolutionary histories were devoted principally to water storage. Ant-
of its plant life, and small expanses of montane associated species in several different genera have
forests in contemporary times.) By virtue of small reduced their investments in storage and allocated
size, these unrooted plants stand to benefit signifi- space within their tubers to two types of cavities
cantly from even small quantities of nutrients used by the ants. Colonies of Anonychomyrma and
amassed as workers retrieve prey, discard refuse, Philidris nest in smooth- and dry-walled cavities,
and defecate within a confined area. From a mix of while placing feces and refuse in wet-walled cavi-
vegetable fiber, glandular secretions, refuse, and ties with warts, actually modified roots. The epi-
feces, many ants build carton shelters (for them- phytes satisfy a significant fraction of their nitrogen
selves and tended Hemiptera), and carton can requirements by tapping into these wastes. Epi-
potentially contribute to plant nutrition. phytic Dischidia species (Asclepiadaceae) fre-
Two categories of plants, New World ant- quently grow adjacent to the Hydnophytinae on
garden epiphytes and Australasian ant-house the same hosts and are inhabited by the same ant
epiphytes, have evolved a variety of traits that colonies. In addition to their normal leaves,
increase frequency and intimacy of relationships which grow appressed to tree trunks, these species
with beneficial ants. To encourage seed dispersal to produce highly modified leaves, involuted to form
nutrient hotspots in ant nests and carton, both sets the cavities in which ants live. Stomata are concen-
of species produce seeds with attractive chemicals trated on internal cavity walls formed by abaxial
and/or food bodies. The common occurrence of (lower) leaf surfaces. Through their stomata, plants
methyl-6-methyl-salicylate on seeds of 11 unre- take up the carbon dioxide (CO2) needed for pho-
lated ant-garden epiphytes, combined with the use tosynthesis. When stomata (Fig. 60) open to per-
of these same compounds as pheromones (within- form this chore, they lose precious water, an
species communication chemicals), suggests that especially limiting commodity for unrooted epi-
this chemical could function as an ant attractant. phytes of the hot, dry canopy. However, stomata of
Generations of seed dispersal by ants appears to ant-house Dischidia open into a relatively moist,
have allowed ants to capture the evolution of their enclosed space where the partial pressure of CO2
epiphytes, just as humans have captured and is enhanced by ant respiration, and this alleviates
diverted the evolutionary histories of their crop transpirational water losses. Using stable isotope
species. (Alternatively, in both of these systems, technologies, K.K. Treseder and colleagues showed
plants may have captured and diverted the evolu- that Dischidia major from Bako National Park in
tionary histories of their gardeners!) The successes Sabah, Malaysia, obtains about 39% of its carbon
of ant-epiphyte partnerships are evident from their from ant-respired CO2. Isotopic studies of N
often remarkable abundances. Ant gardens can revealed that about 29% of the plants N comes
account for the majority of epiphytic higher plants from ant feces, refuse and carton, into which plants
in forests with a distinct dry season, and ant-house insert adventitious roots from the bases of both
plants dominate the epiphytic floras of open keran- normal leaves and leaf domatia.
gas forests in Asia. Whereas other epiphytes cannot Often growing with the Hydnophytinae and
survive extended periods of drought, ant-garden Dischidia are ant-occupied ferns in the genus
taxa benefit from moisture absorbed from the air Lecanopteris, and any of several ant taxa can
and stored in the rich, organic ant cartons. occupy each of these epiphytes. Although associa-
Ant-house epiphytes have evolved even more tions between ants and epiphytes are not obligate
elaborate adaptations to procure benefits from for either party, it is rare to find one partner in the
their ant inhabitants. Those in the sub-family Hyd- absence of the other. This is likely due to the com-
nophytinae (Family, Rubiaceae) are descended bination of frequent nest site limitation in ants,
from tuberous ancestors whose storage tissues and water and nutrient limitation in epiphytes.
180
A Ant-plant Interactions

Ant-plant Interactions, Figure 60 Myrmecotrophic epiphytes: (upper left) At Cocha Cashu, Peru, 11
different epiphyte species from seven plant families can occur in carton ant-gardens. This garden
contains mainly seedling Peperomia macrostachya; (upper right) Myrmecodia tuberosa (Rubiaceae,
Hydnophytinae) growing on a stunted tree in open kerangas forest at Bako National Park, Sarawak;
(lower left) cross section of Anthocephalus sp., vic. Wau, Papua New Guinea, showing dry-walled cavities
inhabited by ants, and wet-walled cavities with warts (modified roots) that extract nutrients deposited
as ant refuse and feces; (lower right) Bornean Dischidia major (Asclepiadaceae, also from Bako): small,
circular, flat leaves are typical of non-myrmecotrophic members of the genus, whereas much larger,
involuted leaves have evolved in myrmecotrophic species and house associated ants.
 Ant-plant Interactions
A 181

Myrmecotrophy is commonest in epiphytes,

but as P. J. Solano and A. Dejean have shown, it can
also occur where ants leave waste in abandoned
domatia as colonies move to new growth. Thus, in
Maieta guianensis, protrubances on domatia walls
appear to take up N from waste of Pheidole
minutula. By an as yet poorly defined mechanism,
some rattan palms also benefit nutritionally from
ants that build carton nests among spines on exter-
nal stems. Another monocot (Guadua bamboo),
apparently cannot take advantage of ant waste
inside stems and actually loses N to scale insects
tending by resident carpenter ants.
Ant-plant Interactions, Figure 61 Seeds of Acacia
cana (northwestern New South Wales, Australia)
Ants as Seed Dispersers, have white arils contrasting with black seeds and
Pollinators and Partners of are displayed at the soil surface, where ants are
Insectivorous Plants most likely to find them.

Seed Dispersal Ant-dispersed plants, bearing small food

rewards for ants, are common in habitats ranging
Tropical epiphytes are not the only group of plants from rain forests (e.g., herbs in the Marantaceae)
to take advantage of the willingness of ants to to temperate deciduous forests (e.g., violets) and
transport seeds. In general, plants are thought to aridlands (North American jimson weed and some
be selected for both distance dispersal and direc- Australian acacias and saltbushes, Fig. 61), but the
tional dispersal, and the balance of selection for greatest diversity of myrmecochores may occur in
the two objectives almost certainly varies from areas with infertile soils, Mediterranean climates,
species to species. Distance dispersal, or seed dis- and high fire frequency, e.g., especially African fyn-
persal away from the maternal parent, is impor- bos and Australian heath. Depending upon habitat
tant for avoiding both asymmetrically strong characteristics, hypotheses for the adaptive value of
competition from the mature plant against its myrmecochory have included giving seeds refuge
seedlings, and transfer of pathogens and seed from fire (chaparral), from competing plants (tem-
predators to these offspring. Because ants gener- perate deciduous forests, where ant nests may be the
ally forage over relatively short distances from a only vacant sites), or from seed predators (diverse
central place, they are probably more important in habitats), as well as dispersal to nutrient hotspots on
directional dispersal, i.e., directing seeds to safe ant mounds (e.g., the nutrient-poor soils of arid
sites or favorable microhabitats. The importance Australia). While controversies continue about par-
of both forms of dispersal may explain why some ticular plants and sites, it is likely that each of these
diplochorous species accomplish both objectives, hypotheses holds for a subset of plant species.
e.g., by first explosively propelling seeds away from The rewards that plants offer for seed dispersal
the parent and then using ants to target seeds to a fall mainly into the category of elaiosomes, a kind
preferred location. The majority of ant-dispersed of aril (= dry fruit) that is rich in oils. Both birds
seeds are taken to or near the nest site, if not into and mammals also feed on arillate fruits. When
the nest itself, and evolutionary advantages of ant-dispersed species were compared with
myrmecochory (dispersal by ants) are usually bird-dispersed (ornithochorous) species in the
discussed in relation to these sites. same sub-genus of Australian Acacia, fruits and
182
A Ant-plant Interactions

seeds of the two types of species differed in size, aril between myrmecochorous plants and ants, one or
composition, color, and presentation. Myrmeco- more ant species may often have a disproportion-
chorous seeds were somewhat smaller on average, ate effect on plant reproductive success. For exam-
with arils poorer in lipids (an energy source) and ple, at increasing frequency, disruption of ant
water, but marginally richer in N (amino acids or communities by non-native species (e.g., Argentine
proteins). In contrast to the colorful arils that orni- ants, Linepithema humile) threatens populations of
thochores display prominently on the host, arils tar- native plants, including rare and endemic (geo-
geting ants were white (contrasting readily with graphically restricted) species.
black seeds) and presented on the ground after
dehiscing. A study by L. Hughes and colleagues
compared the elemental composition of myrmeco- Ants as Pollinators
chore arils with that of fleshy fruits from diverse
vertebrate-dispersed plant plants. A difference in While we think most often of bees, flies and hum-
potassium (K) levels suggested that vertebrate fru- mingbirds as agents of plant pollination, ants can
givores may require comparatively high levels of K also be effective pollinators under a restrictive set of
in their fruits. Species growing in poor soils may circumstances. This is apparent despite observations
simply have too little K to produce K-rich fruits, by A.J. Beattie and colleagues that antibiotic com-
and so may be relegated to myrmecochory. Hughes pounds produced by the ants metapleural and poi-
and colleagues have also identified fatty acids (espe- son glands can suppress pollen germination and
cially 1,2-diolein) as important components of pollen-tube growth. (Unlike their wasp ancestors,
elaiosomes, which may mimic the composition of ants often inhabit nests for multiple generations, and
insect prey (especially haemolymph) and therefore metapleural glands with hygienic function appeared
induce a variety of carnivorous and omnivorous ant early in ant evolution.) Nevertheless, M. Ramsey
species to transport seeds to the nest. Given the suggests that if ubiquitous ants were otherwise effec-
ubiquity of ants in most habitats, plants may have tive pollinators, some or even many plant species
evolved to attract ant species that consume only the might be expected to have evolved pollen insensitive
appendage and not the seed itself. Together, these to metapleural secretions. The apparent rarity of
studies point to syndromes of traits characterizing such immunity suggests that ants may be inadequate
species with different dispersal agents. as pollinators for some other reason(s). A signal
Inconstancy in availability of elaiosomes prob- attribute of ants is their tendency to revist food
ably prevents ants from specializing on fruits of a sources such as extrafloral nectaries and Hemiptera.
particular plant species. Moreover, aside from mak- Very likely, conservatism in ant movements detracts
ing a dispersal unit smaller or larger, it is difficult from their ability to transmit pollen effectively
logistically to direct seeds to particular ant species. among individual plants, a requisite for reproduc-
Not surprisingly then, relationships between ants tion by self-sterile taxa. Nonetheless, ants may play a
and myrmecochorous plants tend to be diffuse role in pollination where smaller plants (e.g., epi-
rather than species-specific, with a variety of ants phytes or annual herbs) occur at high densities, or
carrying seeds of a given plant, and often more by enhancing rates of self pollination when more
than one type of elaiosome in an ant diet. Never- effective pollinators are scarce.
theless, all ant species are not equal in their effects Among the few plant taxa pollinated by ants, a
on plant reproductive success. Interspecific differ- suite of traits, or an ant-pollination syndrome (a
ences among carriers affect transport distances, term coined by J.C. Hickman) points to the
frequency of dropping without retrieval, and rates circumstances under which ants can be induced to
of seed burial and escape from seed predators. move among individual plants. Ant-pollinated
Despite the opportunistic nature of interactions plants (Fig. 62) tend to be small in stature and mostly
 Ant-plant Interactions
A 183

prostrate in growth form, so as to preclude the need distributions of such nectars remain poorly known.
tocompensate ants energetically for walking verti- J.Ghazoul presents some of the strongest evidence
cally rather than horizontally. As a consequence of for floral ant repellents, demonstrating that a
paying little reward, plants encourage workers to diversity of ants are repelled by something in floral
keep moving in search of additional nectar or fuel. tissues themselves. Still unresolved is the extent to
Other aspects of the ant-pollination syndrome are which protection of nectar versus pollen has been
white color, and open structure, granting ants access the p
rincipal stimulus for the evolution of ant repel-
to floral nectars, but just small amounts of pollen, lents. At least some pseudomyrmecine and myrmi-
and thereby diminishing the need for ants to groom cine (Cephalotes) ants feed on pollen, but nectar
pollen from their bodies. Ant-pollinated flowers also feeding is more widespread in ants, probably
have relatively few ovules, which may all be polli- because less specialization of the digestive system
nated even by small pollen deliveries. was required to use that resource. Nevertheless,
Given their general ineffectiveness as pollina- early in their evolution, flowering plants must
tors, and their almost universal taste for sweet solu- have found ways of protecting nutritious pollen
tions, ants mostly interact with flowers as parasites from the ubiquitous and often protein-limited ants.
of the relationships between plants and their real
pollinators. Almost certainly for this reason, numer-
ous plants have evolved barriers to exclude ants Relationships Between Ants and
from floral rewards, e.g., with dense fields of hairs Insectivorous Plants
or sticky bands inside the corolla. It has even been
suggested that nectars are made toxic or disagree- Carnivorous plants of diverse forms occur on
able to ants, though the taxonomic and geographic infertile soils in various locations throughout the

Ant-plant Interactions, Figure 62 Mymecocystus species pollinate flowers of at least two desert annuals:
Eriogonum abertianum (Polygonaceae) (left) at Portal, AZ, and Euphorbia sp. (Euphorbiaceae) (right) from
southern California. The latter is more typical of ant-pollinated plants because of its prostrate growth
form. Individual flowers of both species produce minute quantities of nectar, so ants must walk back and
forth among individual plants to fill their crops. However, on both species, workers can commute among
individuals without energetically costly vertical movement. E. abertianum is rare except in years when
winter rains continue through the spring; then it grows in almost monospecific stands with branches of
adjacent individuals overlapping at the same level.
184
A Ant-plant Interactions

world, and are united by their use of trapped insects genera Cecropia (Cecropiaceae), Macaranga
as N sources. Pitcher plants are a particularly fasci- (Euphorbiaceae), Ocotea (Lauraceae), Tachigali
nating life form. They lure insects to the slippery (Fabaceae), Triplaris (Polygonaceae) Tococa and
edges of steep-walled pitchers into which fluids Clidemia (Melastomataceae), as well as in various
with digestive enzymes are secreted and protected genera of ant-house epiphytes in sub-family
from dilution by rainfall by a sort of roof. Ants are Hydnophytinae (Rubiacae).
among the most abundant prey of pitcher plants, Ants
being attracted to the pitcher edges by a form Leaf-Cutting Ants
of extrafloral nectar. However, C.M. Clarke and Pollination
R.L. Kitching show that one Camponotus species Insectivorous Plants
has evolved a more complicated relationship, per- Carnivorous Plants
haps a mutualism, with a carnivorous pitcher plant
in Borneo. Thus, the hollow tendrils of Nepenthes References
bicalcarata house ants that feed on both large
insects trapped by its pitchers and mosquito larvae Davidson DW (1997) The role of resource imbalances in the
therein. Unlike smaller prey, large insects appar- evolutionary ecology of tropical arboreal ants. Biol J
Linn Soc 61:153181
ently overwhelm the plants digestive capacity and
Davidson DW, Epstein WW (1989) Epiphytic associations
lead to accumulation of ammonia in the pitcher with ants. In: Lttge U (ed), Vascular plants as epiphytes.
fluids. Removal of excess prey by Camponotus pre- Springer-Verlag, New York, NY, pp 200233
vents putrefaction of the fluids. Therefore, although Davidson DW, Inouye RS, Brown JH (1984) Granivory in a
desert ecosystem: experimental evidence for indirect
the ants do rob some prey from their host plants, facilitation of ants by rodents. Ecology 65:17801786
the net effect of their presence may be positive. Davidson DW, McKey D (1993) Ant-plant symbioses: stalk-
ing the Chuyachaqui. Trends Ecol Evol 8:326332
Federle W, Maschwitz U, Bert Hlldobler (2002) Pruning of
host plant neighbours as defense against enemy ant
Effects of Ant-Plant Interactions on invasions: Crematogaster ant partners of Macaranga
the Diversification of Ants protected by wax barriers prune less than their conge-
ners. Oecologia 132:264270
Ghazoul J (2001) Can floral repellents pre-empt potential
Given the extraordinary diversity and widespread
ant-plant conflicts? Ecol Lett 4:15
abundance of interactions between plants and Hickman JC (1974) Pollination by ants: a low-energy system.
ants, the two groups would be expected to have Science 184:12901292
influenced one anothers evolutionary histories. Hlldobler B, Wilson EO (1990) The ants. Belknap Press of
Harvard University, Cambridge, MA
This conjecture is supported by recent molecular Izzo TJ, Vasconcelos HL (2002) Cheating the cheater: stability
phylogenetic studies by C. Moreau and colleagues, of a mutualism between an ant-plant and its associated
who show that the diversification of ant crown ants. Oecologia 133:200205
groups (contemporary major taxa) occurred Mueller UG, Schultz TR, Currie CR, Adams RM, Malloch D
(2001) The origin of the attine ant-fungus mutualism. Q
coincidentally with that of flowering plants (angio- Rev Biol 76:169197
sperms) in the Late Cretaceous and early Eocene, Palmer TM, Stanton ML, Young TP (2003) Competition and
and involved major taxa of litter ants, as well as the coexistence: exploring mechanisms that restrict and
maintain diversity within mutualist guilds. Am Nat
arboreal ants reviewed in the present article.
162:S63S79
With respect to plants, relationships with ants Quek SP, Davies SJ, Itino T, Pierce NE (2004) Codiversifica-
likely contributed to recent and rapid diversifica- tion in an ant-plant mutualism: stem texture and the
tion of species in the genus Inga (Fabaceae), defined evolution of host use in Crematogaster (Formicidae:
Myrmicinae) inhabitants of Macaranga (Euphorbi-
in part by EFNs on leaf rhachis, and containing an aceae). Evolution 58:554570
estimated 300450 species. Major radiations of Yu DW, Pierce NE (1998) A castration parasite of an ant-plant
ant inhabited plant taxa have also occurred in mutualism. Proc R Entomol Soc London 265:375382
 Ants (Hymenoptera: Formicidae)
A 185

Ants reproductives are capable of producing fertile off-

spring. The non-reproductives, or workers, per-
Certain members of an order of insects (order form tasks necessary for colony survival, such as
Hymenoptera) foraging for food, caring for immature ants and
Ants (Hymenoptera: Formicidae) reproductives, and nest building. Eusocial insects
Wasps, Ants, Bees and Sawflies have a competitive advantage over nonsocial
insects because there is a better probability that
groups of sterile workers will be able to complete a
Ants (Hymenoptera: Formicidae) task necessary for the survival of the reproductive
queen, and also complete a series of tasks simulta-
david h. oi neously. If a task is not completed by one worker,
U.S. Department of Agriculture, Agricultural another worker can finish the job. This is opposed
Research Service, Gainesville, FL, USA to a solitary insect where the entire burden of
completing tasks from start to finish rests with the
Ants are one of the most highly evolved and dom- individual.
inant insect groups. They are the largest family of Caste determination, or what causes an ant
insects in terms of the diversity of species and to develop into a reproductive or a worker, is
certainly sheer numbers of individuals. Currently thought to be due to differential genetic expres-
there are well over 12,000 described species of sion stimulated by environmental factors. Based
ants, and some suggest that a similar number is on a limited number of species, at least six fac-
yet to be discovered. Individual colonies of some tors have been identified as being influential in
species can contain over 20 million members. reproductive and worker caste determination:
Ants belong to the family Formicidae, which (i) Egg size, where eggs with more yolk and
consists of 23 subfamilies and 287 genera that are hence larger in size will more likely become
not extinct. queens. (ii) Chilling, eggs and larvae that have
Order Hymeoptera been exposed to sufficiently cold winter temper-
Suborder Apocrita atures tend develop into reproductives in the
Superfamily Vespoidea spring. (iii) Larval nutrition, where food quality
Family Formicidae and quantity affect larval size. Larvae that reach
They are found in all terrestrial regions of the a threshold size by a critical developmental time
world, including the cold subarctic tundra and become the reproductives. (iv) Temperature, lar-
drydeserts. About half of the worlds precinctive vae that grow in optimal developmental temper-
genera are from the Neotropics and a third atures tend to become queens. (v) Caste
from the Afrotropical [sub-Saharan Africa] inhibition, production of new queens is inhib-
region. The subfamily with the greatest number ited by the presence of a mother queen. (vi)
of species is the Myrmicinae, and is followed by Queen age, where younger queens generally pro-
the Formicinae. duce more workers. Regulating the occurrence
Ants are true social (eusocial) insects, which of some of these factors are titers of juvenile
is defined by the following characteristics: (i)coop- hormone. Depending on species and colony
erative brood care, where immature ants are tended conditions, all or just some of these factors may
by groups of adults that are not their parents; be involved and the degree of the factors influ-
(ii) overlapping generations, where at least two ence also varies. A sequence of criteria may need
different generations of adults occur simultane- to be met for an egg to more likely develop into
ously in the same colony; and (iii) reproductive a queen, otherwise it will be a worker. To illustrate,
and non-reproductive castes, where only the for an egg to develop into a queen the following
186
A Ants (Hymenoptera: Formicidae)

criteria may need to be met more or less sequen- tremendous earth-movers because of their
tially: (i) is the egg of sufficient size, (ii) did it underground nest building, and thus contribute
receive enough winter chilling, (iii) was food greatly to the cycling of nutrients. They disperse
sufficient and (iv) temperatures optimal forthe seeds, scavenge dead organisms, and are a major
larva to reach a critical size by the right time, (v) predator of other arthropods and small inverte-
are mother queens young and preventing new brates. In some instances they are directly benefi-
queen development? Meeting criteria will bias cial to man by being major predators of pests
or increase the probability of the development of such as crop feeding caterpillars, and ticks of
a queen. Determination of major (soldiers) and livestock.
minor workers in some species is under both
environmental and genetic regulation, thus
maintaining a characteristic major: minor ratio Morphology
within a colony. Recently, genetic regulation of
workers and queens was found to be absolute in Ants are easy to distinguish from other insects
a hybridization zone between two species, where mainly because of the combination of a thin-waist
workers were heterozygous and reproductives and the presence of elbowed antennae. The waist
were homozygous at marker loci for caste refers to a segmented constriction called the peti-
determination. ole, located between the thorax and the gaster. The
Communication needed to coordinate the gaster is composed of the broad 4 or 5 posterior
activities within a colony is mediated by chemical segments of the abdomen. Morphologically ants
signals called pheromones. Some of the phero- are distinguishable by having a one or two-seg-
mones that have been isolated include a queen mented waist (Fig. 63); always consisting of a peti-
pheromone that allows worker ants to recognize a ole if one-segmented, and both a petiole and a
queen, trail-following pheromone which workers postpetiole if two-segmented. The petiole and
use to mark paths between the nest and food, and postpetiole are actually the second and third seg-
alarm pheromones which cause ants to disperse ments of the abdomen that are reduced or con-
and/or attack. Chemical cues also are used in the stricted in size. They often have a distinctive
recognition of colony nest mates, and play a role node-like form, however in some species it is
in aggression and establishing territorial boundar- scale-like or just a small cylindrical segment. Fol-
ies between colonies. lowing (Table 6) is a list of four terms that describe
Ants are omnivorous and mobile, allowing sections of the ant abdomen and the correspond-
them to exploit a wide range of habitats. This is in ing abdominal segments for ants with one- and
contrast to termites, another abundant eusocial two-segmented waists.
insect, which are restricted to feeding on wood or The adult workers and queens have antennae
other vegetation. Moist environments are condu- that are geniculate, meaning bent or elbowed. The
cive to microbial contamination. Secretions from elbowed appearance arises from having a long
the ants metapleural gland contain antibiotics first, or basal, antennal segment called the scape,
that disinfect moist environs. Having a portable followed by 311 short segments (collectively
means of sanitation allows ants to exploit areas called the funiculus). The basal segments in male
that other organisms may not be able to live in. antennae are usually not long, and thus, the anten-
These attributes permitted ants to become a nae will not appear to be elbowed. Another unique
dominant terrestrial organism, especially in the feature of ants is the small opening or orifice of the
tropics. With their large populations and adapta- metapleural gland. This is located just above the
tion to a plethora of ecological niches, ants play basal segment of the third leg, but often requires
an important role in natural ecosystems. They are magnification to be visible.
 Ants (Hymenoptera: Formicidae)
A 187

Head Thorax Abdomen Life/Colony Cycle

2-segmented waist
scape petiole & postpetiole
Ants are holometabolous, having a complete life
gaster
cycle consisting of eggs, larvae, pupae, and adults.
Thus, little adult ants do not grow into big adult
ants. The eggs, larvae, and pupae are collectively
called brood. In general, colony development is as
funiculus follows: ant colonies originate after a mating flight
a when winged virgin queens mate with winged
males. After mating, the males die, while the newly
1-segmented petiole
mated queen sheds her wings and finds a protected
location or excavates a chamber in soil. Within
this chamber she will lay a batch of eggs and care
for the subsequent larvae and pupae until they
become adults. These adults are usually sterile
females, which are the worker caste, and they will
b
assist the queen by caring for additional brood,
foraging for food, and expanding the nest. An
important aspect to the survivorship and growth
Ants (Hymenoptera: Formicidae) , Figure 63 of ant colonies is trophallaxis, or the exchange of
Distinguishing morphological structures of ants: regurgitated food among nestmates. Trophallaxis
(a) two-segmented petiole or (b) one-segmented ensures that food is distributed to all members
petiole. Elbowed antenna consisting of a long of the colony including the queen and brood.
basal segment (scape) and 311 short segments Oncethe colony is well established, winged virgin
(funiculus); posterior portion of abdomen beyond females and males (reproductives) will be pro-
petiole (gaster) [drawings modified from M.R. duced and will proceed to have a mating flight
Smith 1965, (a) Monomorium minimum, when environmental conditions are suitable. The
(b) Dorymyrmex pyramicus]. original colony will continue to be maintained and
produce new reproductives as long as the queen is
able to produce viable eggs. Depending on the
species, queens have been reported to live from
Ants (Hymenoptera: Formicidae), Table6
less than a year to as long as 29 years. A major
Abdominal segments that compose sections of
variation to this cycle is the absence of a mating
the abdomen for ants with one- and
flight by the virgin queens in some species. Mating
two-segmented waists
takes place within the nest with either their broth-
Abdominal One-segmented Two-segmented ers or males that fly in from other colonies. New
Sections waist waist
colonies are formed by budding, where a portion
Propodeum abdominal segment 1 fused to of the colony, containing adults, brood, and either
posterior of thorax
or both mated or virgin queen(s), separate from
Petiole abdominal abdominal the original colony and move to a new location.
segment 2 segment 2
In addition to the tremendous number of ant
Postpetiole None abdominal species, there is a broad range of interesting behav-
segment 3
iors or life styles among species. Many species
Gaster abdominal abdominal
have mutualistic relationships with honeydew-
segments 37 segments 47
producing insects such as aphids and mealybugs
188
A Ants (Hymenoptera: Formicidae)

(Hemipteran). Ants will transport and protect immatures are allowed to develop into adult work-
these insects in order to harvest the honeydew ers and carry out colony maintenance tasks for
they produce. In essence, these ants tend and herd their abductors. In fact, the Polyergus workers are
the honeydew producers as if they were cows. so specialized for raiding and killing other ants
Some hemipterans carry plant pathogens, and dis- that their jaws are like sharp curved sabers, mor-
ease spread is facilitated by ants moving the phologically ill-suited for nest building, tending
infected hemipterans to other plants. immatures, and food gathering.
Another agrarian life-style is that of the leaf- More extreme extensions of this parasitism
cutting ants that raise their food in fungal gardens are species without a worker caste. These species
within their nest. These ants use leaves and other contain only males and queens that are cared
fresh vegetation to provide a substrate on which to for by the workers of a host colony, which they
grow the fungus, and these ants can defoliate trees have infiltrated. They are either fed by the workers
overnight. Leaf-cutting ants cut pieces of leaves or or steal food from the host queen, which they often
flowers with their jaws and then carry them back mount and hold onto. The eggs of the parasite
to their nest. Once in their nest, they further chew arereared to adulthood by the host workers. Para-
the vegetation and add feces to form a suitable sitized host colonies can be smaller in size, pre-
medium for fungal growth. Finally, they plant and sumably because of the partial diversion of
maintain a specific fungus species on the substrate. resources to the parasites. Examples of these para-
In Central and South America, leaf-cutting spe- sitic ants include Solenopsis daguerrei, a parasite of
cies in the genus Atta and Acromyrmex (subfamily imported fire ants (Solenopsis invicta, S. richteri),
Myrmicinae) can have colonies with an estimated and Teleutomyrmex schneideri, a parasite of
18 million individuals. They build nests consist- Tetramorium caespitum and T. impurum (all in the
ing of an extensive network of subterranean subfamily Myrmicinae).
galleries, and are the most significant pests of In contrast to the symbiotic life-styles, many
agriculture in South America, feeding on citrus, species of ants are extremely predatory and have
forage grasses, and other crops. gained the reputation of being an unrelenting
Symbiotic relationships with plants been scourge of the jungle. The subfamily Dorylinae con-
reported for several ant species. One well-studied sists of a single genus, Dorylus, which contains the
mutualistic relationship is that between Acacia African driver ants, also referred to as army ants
cornigera trees and the ant Pseudomyrmex ferruginea or legionary ants. Most species are found in the
(subfamily Pseudomyrmecinae). The acacia tree Afrotropical region (sub-Saharan Africa), but a few
produces thorns, which serve as nesting sites for the species are also found in the southern Palearctic,
ants and it produces structures, called Beltian bod- Oriental, and Indo-Australian regions. The various
ies, that are eaten by the ants. The ants protect the species of African driver ants have colonies with
plant from herbivorous arthropods and vertebrates, millions of individuals, which regularly move nest-
and destroy competing plants that sprout nearby. ing sites and forage for food in large swarming
Besides their symbiotic interactions with columns or groups. The columns can fan out to pro-
plants and other insects, ant species also have par- duce a large moving front that preys on anything
asitic relationships among each other of which that remains in its path, especially arthropods.
slavery, or dulosis, is one of the more interesting At night the colony forms a bivouac, protecting
forms. The genus Polyergus (subfamily Formici- their queens and brood within a mass of worker
nae) consists entirely of slave-making species. ants. Thus, there is no permanent nest structure for
Workers of Polyergus colonies dash into the nests these nomadic ants. Besides the army ants in the
of ants in the genus Formica (subfamily Formici- Dorylinae, the subfamily Ecitoninae contain many
nae) and steal their larvae and pupae. The stolen species of army ants found in the Neotropics, and a
 Ants (Hymenoptera: Formicidae)
A 189

few species in the Nearctic. These armies are smaller days, but some can have hypersensitive reactions,
than the African species, with colonies of hundreds resulting in anaphylaxis and even death in rare
of thousands rather than millions. instances. Non-stinging ants, such as the Pharoah
The pillaging, nomadic life of the army ants ant (Monomorium pharaonis, subfamily: Myrmic-
requires a high level of organization and coopera- inae) may be a nuisance to building occupants
tion. Extraordinary cooperative behavior is further and are also known to contaminate sterile surgi-
exhibited during nest construction by the weaver cal units, supplies, and food items in hospitals.
ants in the genus Oecophylla (subfamily Formici- Invasive ant species, such as the red imported fire
nae). These ants are dominant arboreal ants of the ant and the Argentine ant (Linepithema humile
Afrotropical region. They link their bodies together subfamily: Dolichoderinae), establish and thrive
to form chains by grasping the petiole of an adja- in non-native locations, invade surrounding areas,
cent worker with their jaws. The living chains are and eventually become the dominant faunal spe-
used to pull the edges of leaves together. Once cies. Invasive ants are a major concern in many
leaves are held in a desired position, other workers areas, ranging from nature preserves to suburbia,
bring forth silk-producing larvae and individually because they displace native ants as well as other
press larval heads to one leaf surface then another, native organisms.
resulting in thousands of sticky silk threads being
drawn between the leaves to hold them together.
Eventually leaves and stems are bound together to Control
form a tent within which a nest of silken galleries is
constructed. This communal nest construction is Controlling pest ants can be a difficult task given
unique in that it involves the use of immature their broad habitat range, large populations, and a
stages that secrete silk on command. It has allowed social organization that protects the queen(s) from
these ants to build expansive networks of nests external influences such as insecticides. Because
across several trees, which can house a colony of traditional control approaches of excluding ants
over 500,000 individuals. from buildings by sealing cracks and crevices or
The adaptability and high reproductive out- applying insecticides directly to ants or nests gen-
put of many species of ants allow them to thrive erally do not target the queen, significant popula-
in many environments, including that of humans. tion reductions, if any, are temporary. Ant baits,
As such, ants that live in buildings or have high however, were developed to use the foraging and
populations in areas used by man are often con- nest mate feeding behaviors of ants to distribute a
sidered pests. Many pest ants have characteristics toxicant throughout a colony, including the
that typify the tramp species. These ants gener- queen(s). Ant baits typically contain a toxicant
ally (i) spread around the world via human com- dissolved into a liquid food preferred by the pest
merce; (ii) can thrive in man-made environments; ant species. This poisoned food can be mixed with
(iii) have colonies that are not territorial and thus an absorbent carrier such as corn grit or formu-
can result in interconnected nest sites; (iv) have lated into a gel to facilitate handling and applica-
many queens per colony; and (v) have limited or tion. Some baits are left in liquid form and must be
no mating flights resulting in colony reproduc- dispensed in a container that serves as a feeding
tion by budding. Ants that sting, such as red station.
imported fire ants (Solenopsis invicta, subfamily: Key to effective ant bait is a toxicant with the
Myrmicinae), are of veterinary and medical following three characteristics. First, the concen-
importance. Newborn livestock can be blinded or tration of toxicant used should not deter feeding
killed by stings at birth. People who are stung usu- on the bait, because ideally enough bait should be
ally develop itching pustules that last for several readily foraged upon to be shared with adults and
190
A Anus

immature stages of all castes within a colony. Sec- Ant-plant Interactions

ond, the toxicant should not immediately kill the Driver Ants
ants foraging upon the bait. In general, a delay in Leaf-cutting Ants
death or sickness of a minimum of 8 hours from Carpenter Ants
the time of ingestion is required to allow sufficient Castes
toxicant to be collected and fed to a significant
portion of the colony. If the toxicant causes sick-
ness or death too quickly, distribution of the bait References
to the rest of the colony stops before enough of the
colony is affected, and control will not be obtained. Agosti D, Johnson NF (eds) (2005) Antbase World Wide Web
Third, the toxicant should provide a delay in mor- electronic publication. antbase.org version (05/2005).
Accessed September 2007
tality over a wide range of concentrations (typi- Bolton B (1994) Identification guide to the ant genera of
cally at least a 10 fold range) because the toxicant the world. Harvard University Press, Cambridge, MA,
is diluted as it is shared among nest mates. Depend- 222 pp
ing on the type of toxicant and colony size, ant Bolton B, Alpert G, Ward PS, Naskrecki P (2006) Boltons
catalogue of ants of the world: 17582005. Harvard
baits may take from three days to several months University Press, Cambridge, MA
to eliminate a colony. Some bait toxicants do not Julian GE, Fewell JH, Gadau J, Johnson RA, Larrabee D (2002)
kill adults but instead disrupt reproduction by the Genetic determination of the queen caste in an ant hybrid
zone. Proc Natl Acad Sci USA 99:81578160
queen, whereby worker caste ants are no longer
Hlldobler B, Wilson EO (1990) The ants. Harvard University
produced. As the original adult worker population Press, Cambridge, MA, 732 pp
dies naturally, the lack of replacement workers Smith MR (1965) House-infesting ants of the eastern
dooms the colony to a slow death as functions that United States: their recognition, biology and economic
importance. United States Department of Agriculture,
sustain a colony such as food gathering, defense, Agricultural Research Service Technical Bulletin No.
nest repair, and queen care cannot be carried out. 1326. 105 pp
While ant bait development has been a major Williams DF (Ed) (1994) Exotic ants: biology, impact, and
focus for ant control, other strategies have been control of introduced species. Westview Press, Boulder,
CO, 332 pp
developed for specific species. For example, plant- Williams DF, Oi DH, Porter SD, Pereira RM, Briano JA (2003)
ing forage grasses that are a non-conducive Biological control of imported fire ants (Hymenoptera:
substrate forthe growth of fungus needed by leaf- Formicidae). Am Entomol 49:150163
cutting ants can significantly reduce their popula-
tions. Natural enemies of ants are also used to
suppress ant populations. In particular, tiny para- Anus
sitic flies, in the genus Pseudacteon, that develop in
the heads of ants, and a pathogen, Thelohania sole- The external opening of the digestive tract, through
nopsae, that debilitates queens are being used to which the food remnants and metabolic waste
suppress populations of imported fire ants. These products are passed.
natural enemies require development within fire Alimentary Canal and Digestion
ants and unlike chemical control measures, are Internal Anatomy of Insects
self-sustaining and can spread naturally among fire
ant populations. Effective control of pest ants, as
with most insect pests, generally requires the use Aorta
of several control tactics adapted for a particular
species and circumstance. A tube located dorsally in the insects body that
Myrmecophiles conducts blood from the heart forward to the
Myrmecomorphy head region.
 Aphids (Hemiptera: Aphididae)
A 191

Apatelodidae Aphids
Sugar Feeding in Blood-Sucking Flies
A family of moths (order Lepidoptera). They com- Aphidophagous
monly are known as American silkworm moths.
American Silkworm Moths
Butterflies and Moths Aphidophagous

Aphid feeding.
Aphelinidae Aphidivorous
Predation: The Role of Generalist Predatory in
Biodiversity and Biological Control
A family of wasps (order Hymenoptera). Natural Enemies Important in Biological
Wasps, Ants, Bees and Sawflies Control

Aphelocheiridae Aphids (Hemiptera: Aphididae)

daniel j. sullivan
A family of bugs (order Hemiptera). Fordham University, Bronx, NY, USA
Bugs
Aphids are among the most interesting, unusual, and
thoroughly studied of all insect groups. They are
Aphicide worldwide in distribution, and are also called plant
lice, antcows, green flies, die Blattluse, les aphides,
An insecticide that is especially effective against los fidos, etc. They have economic importance
aphids. because many aphid species are pestsof agricultural
crops, forest and shade trees. Although small in size
(110 mm) compared to many other insects, profes-
Aphididae sional as well as amateur entomologists have always
been intrigued by their specialized life cycles that are
A family of insects in the order Hemiptera. They influenced by their host plant relationships. This
sometimes are called aphids, green flies, and results in both sexual and asexual reproduction, with
plant lice. a highly dependent, almost parasitic mode of sessile
Aphids existence that can be parthenogenetic during lengthy
Bugs periods with a telescoping of generations. Yet, when
the photoperiod shortens and the temperature cools,
offspring are produced that reproduce sexually. In
Aphidivorous addition, aphids have life cycles with a polymorphism
in adults that have wingless (apterous) and winged
Aphid loving. Many insects are associated with (alate) forms or morphs, as well as polyphenism or
aphids because the feed on the honeydew pro- different morphs even within clones. As alates, migra-
duced by the aphids (e.g., many ants, some flies tion is enhanced, and this can be involved with over-
including mosquitoes) or on the aphids (e.g., many wintering behaviors because of host plant alternation.
lady beetles and flower flies). Those that feed on Hence, aphids are excellent animals for the study of
the aphids are said to be aphidophagous. multitrophic ecology, behavior, physiology, genetics,
192
A Aphids (Hemiptera: Aphididae)

evolution, biological control, molecular biology, etc. small number compared to many other insect taxa.
Besides using field studies of aphids for population However, adult polymorphism as winged (alate) and
sampling and damage assessment, many species can wingless (apterous) morphs, as well as polyphenism
be reared rather easily in the laboratory and green- within clones increases their overall diversity.
house, thus making them ideal subjects for precise
observation and experimentation.
Distribution

Classification Although aphids are found worldwide, their species

are most abundant in the temperate latitudes, and
Aphids are usually classified in the order Hemiptera, less so in the tropics. This preferential distribution
series Sternorryncha or sometimes suborder may have evolved in response to the selective pres-
Homoptera along with the psyllids, whiteflies, scale sures of the temperate regions having constantly
insects, and mealybugs. Another approach is to put changing, yet rather predictable, environmental
aphids in the order Homoptera and suborder Ster- conditions. As a result, unlike most other phytopha-
norryncha. Some taxonomists have increased the gous (herbivorous) insects, aphids show an inverse
number of aphid families to as many as 20 with a relationship between the number of aphid species
corresponding realignment of the subfamilies. Fur- and the number of plant species in different parts of
ther phylogenetic studies with molecular techniques the world. Hence, there are many more aphid species
are in progress, but in this overview summary the in the temperate latitudes than in the tropics,
following composite scheme of the major taxa in although there are more plant species in the tropics
aphid classification is given below such that there than in the temperate regions, but with fewer species
are 8 subfamilies in the family Aphididae: of aphids. Most aphids (70%) are in the subfamilies
Order Hemiptera Aphidinae and Calaphidinae (=Drepanosiphinae),
Series Stemorrhyncha (= Suborder Homoptera) and many are pests of crops in these temperate
Superfamily Aphidoidea zones. However, when some of these species are
Family Aphididae (aphids) introduced (accidentally) into tropical and subtropi-
Subfamily Aphidinae cal regions, they are still able to adapt and become
Tribe Aphidini pests in these new environments. In addition,
Tribe Macrosiphini although the tropics and subtropics are fairly con-
Subfamily Calaphidinae (= Drepanosiphinae) stant in temperature and photoperiod, it is surpris-
Subfamily Lachninae ing that there are some endemic species in these
Subfamily Chaitophorinae regions that are holocyclic in their life cycles (female
Subfamily Greenideinae cyclical parthenogenesis, alternating with sexual
Subfamily Eriosomatinae reproduction by males and females) which is more
Subfamily Hormaphidinae common in the temperate zones. This is in addition
Subfamily Anoeciinae to the expected anholocyclic life cycle (absence of
Family Adelgidae (adelgids) males, only parthenogenesis by females) which
Family Phylloxeridae (phylloxerans) would be normal in the tropics and subtropics.
Although the number and organization of the Aphids find their host plants by random search, and
subfamilies can vary, there is general agreement that ecologists emphasize the importance of the concept
within the family aphididae, the largest subfamily is of plant apparency. Of the more numerous species
the aphidinae, followed by the calaphidinae of aphids in the temperate regions, many are
(=Drepanosiphinae), and the Lachninae. There are monophagous (feed on one or only a few species of
over 4,000 species of aphids which is a relatively related host plants). However, in the tropics where
 Aphids (Hemiptera: Aphididae)
A 193

there are more species of plants and relatively fewer body weight could take advantage of air currents for
aphid species, these aphids are more polyphagous dispersal. Some consider monophagy as a recent
(feeding on a variety of host plants). Hence, some development in aphid evolution, although others
suggest that aphids originated in the northern hemi- speculate that like parthenogenesis, it could have
sphere, andthatthe tropics presented a barrier to a evolved early in the evolutionary history of the
similar multiplication of species in the southern Aphidoidea. Another characteristic which aphids
hemisphere. share with the adelgids and phylloxerids is the sim-
ple nymphal eye of three lenses (triommatidium).
From the Triassic Period (240205 million
Origin and Evolution years ago), only the front wing of one species of
aphid (Triassoaphis cubitus) from Australia is
Based on the classification given above, in the known, and it is not easily placed in any superfam-
hemipteran superfamily Aphidoidea are the families ily of later periods. Cytogenetic evidence indicates
Aphididae (aphids), Adelgidae (adelgids), and Phyl- that parthenogenetic reproduction by means of
loxeridae (phylloxerans). Paleontology and phylog- unfertilized eggs may have evolved over 200 million
eny are two sources of information used by years ago, before these three families (Aphididae,
systematists to study the evolutionary history of this Adelgidae, Phylloxeridae) became independent.
group. According to these experts, although paleon- This view is supported because a holocyclic life
tology should provide a time scale for their ages, cycle (cyclical parthenogenesis by females, alternat-
unfortunately the fossil evidence is very limited. ing with sexual reproduction by males and females)
Only about 125 fossil species have been described, is now common to all three groups. However, vivi-
while the number of extant aphid species is over parity (live birth) is a special characteristic of aphids,
4,000. Two kinds of fossils exist: (i)imprints from and must have evolved later because the modern
carbonized remnants in clay, limestone or other sed- adelgids and phylloxerans are only oviparous (lay
iments, which provide only minimal information eggs). By the Jurassic Period (205138 million years
because aphids are soft-bodied and are not well pre- ago), there had developed the recognizable shape of
served; and (ii) amber inclusions which have entire the body, wing venation, proboscis, and legs, while
specimens that are often caught in a natural posi- the siphunculi or cornicles and cauda evolved in the
tion, and so are much more important as fossils. Cretaceous Period (13865 million years ago).
Probably aphids, along with the closely related A major botanical event also occurred during
adelgids and phylloxerans, evolved from a common the Cretaceous with the evolution of angiosperms
ancestor about 280 million years ago in the late Car- (flowering plants), which coincided with the radia-
boniferous or early Permian Periods when there tion and species diversification of aphids. Within
were seasonal climatic changes associated with the the family Aphididae, the Aphidinae (the largest
glacial period. They are now classified together in subfamily of modern aphids) is not represented
the superfamily Aphidoidea, and their host plants in the fossil record until the late Tertiary Period
were primitive gymnosperms (Cordaitales, Cycado- (651.65 million years ago). Tribes of the second
phyta). By utilizing their specialized piercing suck- largest subfamily, the Calaphidinae (=Drepano-
ing stylets on the phloem and parenchyma tissues of siphinae), developed much earlier in the Upper
the gymnosperms, polyphagy was most likely the Cretaceous and early Tertiary Periods. Concerning
primitive feeding behavior of the superfamily Aphi- the third largest subfamily, the Lachninae, there is
doidea. As a result of their parasitic mode of life, limited palaeontological evidence of its evolution.
individual size in these three families (Aphididae, Hence, there is some debate as to the relative age of
Adelgidae, Phylloxeridae) was similar and rather the lachnids. Because 80% of them live on conifers
small. Although their wings were delicate, their light (which are older than the angiosperms), the lachnids
194
A Aphids (Hemiptera: Aphididae)

have generally been regarded as ancient, although being much smaller than the front wings. Alate
some genera may have a recent origin. aphids (but not apterous) bear three ocelli on the
front of the head. The antennae are usually long
and thin with five or six segments, and bear pla-
Metamorphosis coid sensilla called rhinaria which are the olfac-
tory organs. Legs of aphids do not show much
Regardless of whether aphids are born from an egg interspecific variation, although more active spe-
of oviparous sexual females or live from viviparous cies tend to have longer legs. Both sets of wings are
parthenogenetic females, their type of metamorpho- membranous with the fore wing having two longi-
sis is called simple or incomplete: the developmental tudinal veins, one being prominent and the other a
sequence is egg, to nymph(s), to adult. A nymph weak vein. Both veins run apically into the
resembles the adult, and usually develops in four pterostigma which is a dark, thickened area near
molts (four nymphal instars or stages) growing larger the leading edge of the fore wing. When flying, the
each time until the adult stage of sexual maturity is two pairs of wings work as one, being held together
reached. This type of metamorphosis is to be distin- by small hooklets or hamuli on the leading edge of
guished from complex or complete metamorphosis the hind wings that fit into a groove on the trailing
wherein the developmental sequence is from egg, to edge of the fore wings.
larva (several molts and instars), to pupa, to adult. On the dorsal surface of both the thorax and
the abdomen, many species have cuticular glands
that secrete copious quantities of waxy exudates that
External Morphology are powdery or filamentous or rod-like. As a result,
when these species are gregarious, the entire colony
Aphids are mostly soft-bodied insects and relatively appears as a white, powdery or cottony mass. At the
small (only 110 mm in length), usually being plump end and dorsal surface of the abdomen, there are
and ovoid in shape. Because they are plant-sucking usually a pair of tubular structures called siphunculi
insects, they feed by inserting their slender mouth- or cornicles. By contraction of a muscle, a droplet of
parts into the plant. These needle-like stylets consist a waxy exudate is discharged through the cornicles
of an outer pair of mandibles and an inner pair of which rapidly solidifies in the air. When an aphid is
maxillae. The inner faces of the maxillary stylets lock touched or attacked by a predator, one or both cor-
together to form two canals: a large central food- nicles may be raised and the sticky fluid released in
canal for the uptake of plant sap, and a fine duct a defensive role to gum-up the mouth parts and/or
down which saliva is injected into the plant. The tips antennae of an attacking predator. This may also
of these mouthparts also have a chemosensory func- function as a pheromone either as an alarm to warn
tion. When the stylets penetrate the plant, they often other aphids of a predator or for maintaining dis-
go between the cells instead of passing through the tance between aphids on a leaf. Above the anal open-
cells, and in this way they reach the phloem sieve ing, adult aphids usually have a distinct tail or cauda
tubes within the veins of the host plant. which varies in shape among species from being
Most aphids have well-developed compound short and stubby or long and tapering. In the latter
eyes (larger in the alates than in the apterous case, aphids can flick off a droplet of honeydew that
morphs) with a great many individual round emerges from the anus. Concerning the external
lenses called facets or ommatidia. In addition, at genital organs in the adults, the female genital open-
the posterior margin of the eye protrudes an ocu- ing or vulva is only a small slit because there is no
lar tubercle or triommatidium composed of three ovipositor. On the other hand, the male genitalia
lenses. Aphids without wings are called apterous, have prominent sclerotized claspers and an aedea-
while alate aphids have wings with the hind wings gus or penis that can be retracted.
 Aphids (Hemiptera: Aphididae)
A 195

Internal Anatomy thoracic ganglionic mass terminating in the ven-

tral nerve cord, and ganglia plus nerves of the
Digestive System stomatogastric system.

Aphids have the usual regions: pharynx, fore

gut, midgut, hindgut, etc. with subdivisions and Reproductive System
associated parts. However, some species have a fil-
ter chamber which is a special structure. With some Female aphids have two ovaries composed of 46
variations, it consists of a concentric filter system ovarioles. They are remarkable because different
in which the tubular anterior region of the midgut female morphs can reproduce parthenogenetically
is enveloped by the anterior region of the ectoder- (Fig. 64) and be virginopara/vivipara (give birth
mal hindgut forming a filter chamber. Perhaps this to live young by larviposition) without mating
permits selective filtering of the required nitrogen because males do not exist at this time. At other
compounds while rejecting the sugars and convey- times, females can reproduce sexually and be
ing excessive amounts of water to the hindgut. The ovipara (deposition of eggs that have been fertil-
precise function is not clear, and since most aphids ized by males). Development of the female embryo
do not have a filter chamber, it is probably not depends on whether it is destined to become a
essential to their method of feeding. vivipara (live birth) or an ovipara (lays eggs). Influ-
ences on the adult female can be genetic as well as
environmental. Realizing exceptions depending
Bacteriocytes on the aphid species and geographical location, in
general when the environment is favorable (long
Most aphids have specialized groups of cells photoperiod, moderate temperature), the vivipa-
called bacteriocytes (or mycetocytes) that usually rous mother will reproduce parthenogenetically.
contain the bacterium Buchnera aphidicola. This The embryonic female within her will be born
symbiotic association seems to be mutualistic, and it alive as a female nymph, and in turn will give live
is not surprising because many insects that live on birth to other viviparae also being all females (see
specialized and often unbalanced diets such as plant below about anholocyclic life cycle). On the other
sap do indeed possess symbionts. Although their hand, with less favorable conditions (shorter pho-
role in aphid biology is still not completely known, toperiod, cooler temperature), the oviparous
they may help the aphid with its nitrogen utilization, mother will reproduce sexually after mating with a
synthesis of vitamins, sterols, etc. Although numer- male, and she will lay fertilized eggs (see holocy-
ous at birth, the bacteriocytes decrease in number clic life cycle).
during growth. By the end of the aphids reproduc- The viviparous parthenogenetic female does
tive period, practically none remain, suggesting a not require fertilization, and eggs begin develop-
contribution to embryonic development. These bac- ment as soon as they are ovulated from the ovary.
terial symbionts are transmitted transovarially to Even ovarioles of newly born parthenogenetic
the embryos so that nymphs are born withthem. females contain developing embryos rather than
just eggs. Hence, telescoping of generations refers
to the fact that a mother can have in her ovarioles
Nervous System developing embryos which in turn also contain
embryos or future granddaughters. In the modern
The nervous system comprises four structural family Aphididae, therefore, development may com-
parts: brain or supraoesophageal ganglion in the mence even before the mother is born, resulting in a
head, suboesophageal ganglion under the brain, consequent telescoping of generations. As a result,
196
A Aphids (Hemiptera: Aphididae)

Aphids (Hemiptera: Aphididae), Figure 64 Aphid diversity. Top left, aphid giving birth to a nymph
(photo J.L. Capinera); top right, winged brown citrus aphid, Toxoptera citricida (photo Paul Choate);
second row left, green peach aphid, Myzus persicae (photo Jim Castner); second row right, corn leaf
aphid, Rhopalosiphum maidis (photo Paul Choate); third row left, turnip aphid, Lipaphis erysimi (photo
Jim Castner); third row right, oleander aphid, Aphis nereii (photo Jim Castner); bottom row left, Asian
woolly hackberry aphid, Shivaphis celti (photo Lyle Buss); bottom row right, cabbage aphid, B revicoryne
brassicae (photo Paul Choate). Note copious and moderate amounts of waxy exudate on woolly
hackberry and cabbage aphids, respectively.
 Aphids (Hemiptera: Aphididae)
A 197

postnatal development periods and generation times in addition, symbionts in the mycetomes may
are short, and reproductive rates are potentially very detoxify it as well.
high. Because aphids are born on the very host plant
where they can feed, in many species it requires only
714 days for an immature aphid or nymph to meta- Ingestion and Digestion
morphose by several molts into a sexually mature
adult when it can begin reproducing. When this is Both as nymphs and as adults, aphids feed by suck-
combined with a high fecundity (30 or more nymphs ing up the sap from the host plant. When the stylets
born to each aphid) in a short period of time, the penetrate the plant between the cells, they reach
rate of increase is very rapid not only for the indi- the phloem sieve tubes. In a healthy plant, the sap
vidual, but even more so for the entire colony. is under turgor pressure which forces the sap up
The offspring of viviparous parthenogenetic the food canal between the stylets which reduces
females are born rear first, and are fully active. A the energy needed by the aphid to suck the sap.
nymph is similar in shape to the adult, only much Nevertheless, there is also a muscular cibarial food
smaller. If destined to be a winged (alate) adult it is pump at the entrance to the pharynx which can be
either born with wing buds or in some species during used when the plant wilts and the sap ceases to be
the early postnatal period the nymph itself will under pressure.
develop them. This can be triggered by unfavorable Although this plant sap is rich in sugars, it is
conditions due to aphid crowding and/or plant dete- poor in amino acids that are essential for the growth
rioration as well as by seasonal changes such as of the aphid. Hence, aphids ingest large amounts of
shorter photoperiod and cooler temperatures. How- sap in order to acquire sufficient protein. Although
ever, colonies founded by alates usually produce there are less nitrogenous compounds in plant sap
only apterous offspring, and only later on might compared to leaf tissue (such as would be eaten by
alates develop. Hence, there seems to be abiological other phytophagous insects such as the larvae or
clock mechanism so that there is a gradual switch to caterpillars of lepidopterans), aphids make up for
alates that depends on an interval of time. this deficiency by imbibing sapat a very fast rate.
In the superfamily Aphidoidea, this viviparity The unneeded portion of thesapis mainly sugars
(live birth) characterizes the entire family Aphidi- which can be stored temporarily in a dilated rec-
dae. But only females in this family do this, and tum. This sugary material can be eliminated by
not females in the families Adelgidae and Phyllox- ejection from the anus in the form of a sugary
eridae. However, in all three of these families there droplet called honeydew (see section on Ant-Aphid
are sexual females (oviparae) that mate and deposit Mutualism). When aphids are numerous, the leaves
eggs (see Life Cycles). of their host plant can become coated with sticky
Male aphids usually have two to four follicles honeydew on which sooty mold fungus can develop
per testis, although the number, size, and shape causing an economic problem on fruit, vegetables,
varies between species. The vasa deferentia lead to and even cars parked under a tree.
the ejaculatory duct, and in some species there are
paired accessory glands.
Sex Determination

Excretion As expected, the number of chromosomes varies with

aphid species, but all aphids have sex chromosomes
Unlike most insects, aphids have no Malpighian for females designated as XX and males as XO. This
tubules, and excrete nitrogenous waste in the form system of sex determination is called the XX:XO type
of ammonia instead of uric acid. The large amounts wherein females have the full diploid complement of
of water in the diet may dilute the ammonia, and autosomes plus one pair of sex chromosomes: XX.
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Males also have a diploid set of autosomes, but they ofXO, they do have two sets of autosomes, but only
have only one sex chromosome (XO) rather than two one X chromosome.
(not the XY as in some other insects and even humans). Thelytokous parthenogenesis by females
As discussed below, in holocyclic life cycles (female produces only adult diploid (2n) females from
cyclical parthenogenesis, alternating with sexual unfertilized eggs, but no males. Female aphids seem
reproduction), sexual females and males are produced to have diploid parthenogenesis because there is
in response to cues/stimuli that could be external or no reduction division, and development starts from
internal. On the other hand, anholocyclic life cycles a cell with a complete set of chromosomes including
(absence of males, only parthenogenesis byunfertil- the XX sex chromosomes. Both the adult partheno-
ized females) usually exists when the environment genetic females and the sexual females are diploid
(photoperiod and temperature) is relatively constant. (2n) with XX sex chromosomes. In anholocyclic life
cycles (absence of males, only parthenogenesis by
unfertilized females), this reproductive method
Parthenogenesis could continue almost indefinitely, if the environ-
mental conditions permitted. However, in holocyclic
This is reproduction without mating, and there- life cycles (female cyclical parthenogenesis, alternat-
fore without a females egg being fertilized. As ing with sexual reproduction), sexual females and
mentioned above, all aphids have the normal males are produced. The sexual female produces
diploid autosomes, but the sex chromosomes for only haploid eggs (X), and requires mating and fer-
females are XX and males are XO (lacking an X). tilization by a male (X) resulting in a diploid zygote
Among insects in general (not just aphids), when with two XX sex chromosomes, such that all aphids
a females egg is not fertilized, there can be two hatching from these fertilized eggs are females.
types of parthenogenetic reproduction:
Arrhenotokous parthenogenesis by females
produces only male offspring that are all haploid (n) Life Cycles
from her unfertilized eggs (common in the order
Hymenoptera ants, bees, wasps). In aphids, some Life cycles in aphids are varied and complicated,
authors hold that the males XO sex chromosome but the essential terms are given below:
determination is only a type of arrhenotoky prob- Holocyclic life cycle: A viviparous partheno-
ably resulting from a mini-meiosis in the unfertilized genetic female produces live nymphs without mat-
female by which her two X-chromosomes pair and ing. But, this is cyclical because it is interrupted
then separate. Males are then XO with the result that during the year with the production of males and
they could produce two types of sperm (X and O). females that mate, and this oviparous sexual female
However, during meiosis in the male, those sperm deposits eggs.
without an X-chromosome (designated O) degener- Anholocyclic life cycle: This is the complete
ate. This leaves the X-chromosome as the only viable absence of males, so that only viviparous parthe-
sperm which can fertilize an adult females haploid nogenetic females exist with parthenogenetic
egg (X) resulting in all of her offspring being female reproduction continuing throughout the entire
(XX). Hence, males are produced by the loss of an X year with all the progeny being female.
chromosome during a meiotic division resulting in
the sex determination of XO. Adult male aphids then
produce haploid sperm all of which contain one X Host Plant Alternation
chromosome. However, this is not really arrheno-
toky as traditionally used with other insects because Host plant alternation in aphids involves the two
although male aphids have the sex determination types of life cycles:
 Aphids (Hemiptera: Aphididae)
A 199

Autoecious (monoecious) in which aphids spend autumn, winter, and spring on a primary
are host plant specific, and live on one or only a woody host, and the summer usually on secondary
few species of closely related plants even within a herbaceous plants. The primary and secondary host
particular genus during the entire year. Most aphid plants usually are unrelated and belong to different
species (over 90%) are of this type, and as a result, families of plants. Although such aphids may be
there is usually no need for an annual alternation classified as polyphagous, many species are really
between primary and secondary hosts, so that the sequentially monophagous if they live on only one
anholocyclic life cycle is common. host plant species at a time. This alternation of
Heteroecious or host plant alternation life host plants during the year is accomplished by the
cycle (Fig. 65) by which about 10% of aphid species holocyclic life cycle described above. These aphids

Aphids (Hemiptera: Aphididae), Figure 65 Life cycle of the heteroecious holocyclic black bean aphid,
Aphis fabae. (a) Fundatrix or apterous stem mother, (b) her apterous viviparous parthenogenetic f emale
progeny or fundatri-genia, (c) alate emigrant or spring migrant, (d) apterous virginopara, (e) alate
virginopara or summer migrant, (f) alate autumn remigrant or gynopara, (g) alate male, (h) apterous
ovipara or mating female, (i) egg (after Dixon 1998; Kluwer Academic Publishers).
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A Aphids (Hemiptera: Aphididae)

use a specialized reproductive strategy by which the seasonal alternation back to a primary (woody)
the sexual generation produces eggs on the primary host plant, and a behavioral change into an alate
(woody) host plant on which they overwinter. This autumn migrant or gynopara. This parthenogenetic
is done because eggs are better able to survive the female produces sexual females that will mate with
rigors of a cold winter, snow, etc. The cold period of males. Overwintering fertilized eggs are deposited,
winter is required before the embryo in the egg can and the cycle is repeated.
complete its development, and this suspended
physiological state is called diapause. The embryo
will not hatch until the warmth of spring arrives, Polymorphism and Polyphenism
and when it does, all of the offspring will be female.
This female fundatrix or stem mother on the pri- Polymorphism means that there are two or more
mary (woody) plant is the first individual to begin phenotypes or morphs in a population of the
the new parthenogenetic line which results in only same species. Polyphenism means that there are
female offspring all of which are genetic clones of two or more phenotypes or morphs in the same
herself. Spring not only provides nutrient availabil- clone. In other words, genetically identical individ-
ity, but also at this time natural enemies probably uals derived from the same mother by partheno-
have not arrived in dangerous numbers. Again there genesis can differ even though they are all clones.
is a trade-off such that all fundatrices are apterous, This phenomenon is more common in aphids than
thus avoiding unnecessary expenditure of energy in any other insect group, especially inaphids that
on developing wings that are not needed because have host plant alternation. In such a parthenoge-
they do not migrate. Instead, energy can be concen- netic system of genetic clones, females may have as
trated on embryological development resulting in many as eight different phenotypes that differ in
very high fecundity of more and more females by such characteristics as morphology, color, physiol-
viviparous parthenogenesis. ogy, timing of reproduction, developmental time,
When the colonies of female progeny on the numbers and sizes of offspring, longevity, host
primary (woody) plant become crowded, morphs plant preferences, and alternative host plant spe-
appear and become alate spring migrants that fly cies. It is probable that some of this variation is not
(often with the help of wind currents) to the sec- caused only by genetic differences, but also by vari-
ondary host plant. The summer secondary host ations in the host plant and/or theenvironment.
plant is usually herbaceous, and since these alate When environments are regularly cyclical,
migrants are all viviparous females, they will pro- then seasonal changes and predictable weather
duce only females parthenogenetically for as long patterns can influence the availability and quality
as this favorable summer weather continues. By dis- of phloem sap that is the basis of aphid feeding.
pensing with mating and egg-laying, their numbers Because of this predictability and reliability, the
can increase at an astonishing rate. These aphids are evolution of aphid species occurred mainly in
usually apterous and sessile, remaining on the host temperate zone habitats. With this in mind, it is
plant for long periods in a parasitic plant lice understandable that there has been an environ-
mode. But if there is crowding and/or the plant mentally induced morphological and behavioral
deteriorates, alates will develop in the next genera- trade-off so that because alate morphs have
tion, thus permitting movement to a new location energy-costly wings, their developmental time
and even to a new herbaceous hostplant. However, should be slower/longer with a reduced lifetime
such relocation need not be far away if the agroeco- fecundity compared to the apterous morphs that
system consists of many acres planted to monocul- do not have to expend their energy on wings but
ture. In the autumn, environmental cues (shorter rather on offspring production. Hence, there has
photoperiod and cooler temperature) will trigger evolved in aphids both polymorphism and
 Aphids (Hemiptera: Aphididae)
A 201

olyphenism that is adapted to changing yet pre-

p Intraclonal color variation is usually induced
dictable environmental conditions, and resulting by environmental factors, especially temperature,
in the types of sexual and migrant morphs already crowding, and poor nutrition. Therefore, it is
mentioned above in earlier sections. No other reversible if these factors revert to the previous
group of insects can match this diversity. state. On the other hand, interclonal color varia-
tion is genetically fixed between different color
morphs of males and females in some species or
Soldiers between the green and red-pink morphs in the
pea aphid (Acyrthosiphon pisum), green peach
In addition to the sexual and migrant morphs, aphid (Myzus persicae), and potato aphid (Mac-
there is still another of interest: soldiers. These are rosiphum euphorbiae). In the first two aphid spe-
female nymphs in only a few (1%) of the more cies, the red-pink allele is dominant to the green
than 4,000 species of aphids, and are found in allele, so there may be some biological differences
some but not all gall-forming aphids (see section influencing fecundity, reproductive rate, host
on Galling). They exhibit a behavior of defending plant preferences, selection of feeding sites, activ-
the colony against predators, but they do not molt ity, high or low temperature tolerance, etc. For
into reproductive adult females and will never instance, it seems that thermal conditions may
produce offspring. These soldiers aggressively influence the pea aphid when the red-pink morph
attack invaders, sometimes being suicidal. In appears in the summer with the green morph
some, the fore legs and middle legs are thickened doing better in cooler weather. Also crowding
which they use to hold and even crush the intruder. and/or reduced plant nutritional value may cause
If they have frontal horns, they will use these as the red-pink morph of the pea aphid to become
well as their stylets as weapons in combat. Both green. Any ecological significance such as defen-
soldiers and normal nymphs can be produced by sive behavior using camouflage or cryptic color-
the same mother aphid. In some species, soldiers ation has not been demonstrated. However,
(like males) do not have symbionts. Animal behav- colonies of some species may use color as apose-
iorists note the evolutionary convergence of altru- matic warning behavior against birds or other
ism in these aphid soldiers with the sterile soldier predators as with the oleander or milkweed
castes of ants, termites, and thrips. aphid, Aphis nerii, with its bright yellow color
contrasted with black cornicles and cauda, and
dark antennae and legs. In other species, some
Color Morphs color or pigmented bands may absorb solar
radiation that would be advantageous in cool
Coloration in aphids may be caused by: (i) brown weather.
or black pigmentation of the integument (mainly
the tergum) or by sclerotization of the cuticle
which can give a metallic shine; (ii) body contents Aphid Influence on Host Plants
show through the cuticle revealing pigments in
internal organs, tissues, hemolymph (types of gly- Negative Effect
cosides not found in any other group of animals or
plants), bacteriocytes, etc. Colors can vary between Aphids like many sucking insects can have a nega-
and even within species, but the color is usually tive effect on the host plant in one or more of the
green, yellow, reddish, creamy, or almost black; following ways as will be discussed below: nutri-
(iii) waxy exudates that form a pattern from glands ent drain, pathogen transmission, salivary toxins,
on the body and appear powdery white or grey. and honeydew excretion.
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A Aphids (Hemiptera: Aphididae)

Nutrient Drain into the next plant when it goes to feed. What is
especially dangerous about this mode of transmis-
When aphids are in sufficient numbers, they can sion is that once infected, the aphid maintains the
drain the plant of its nutrient sap and cause a virus for life, and so continues as a vector being
breakdown in its tissues. Ironically, it could be this able to infect many other plants in succession.
less-healthy situation for the plant that satisfies the In either case, more plant viruses are trans-
nutrient needs of this parasite. As a result, the mitted by aphids than by any other group of ani-
plant may have its leaf area reduced, growth mals, and they probably do more damage this way
slowed, early leaf fall, become stunted and/or die than by merely sucking the sap from plants. Vege-
before its time. tatively propagated plants such as potatoes are
especially susceptible because the disease is trans-
ferred with the seed tubers to the progeny causing
Pathogen Transmission further yield losses. Weeds sometimes act as host
reservoirs for such viruses.
The major danger to plants is probably the damage
done only indirectly by aphids sucking sap. The
greater harm is done when they are inadvertently Salivary Toxins
the vectors of plant pathogens that cause disease.
Most important of such plant pathogens are the Some aphids have toxins in their saliva that cause
viruses. There is a parallel here between aphids plant tissues to yellow around the feeding site, and
transmitting viruses to plants, and mosquitoes sometimes develop deformities such as leaf-curl,
transmitting such pathogens as protozoa and galls, etc. This can negatively influence plant
viruses to humans resulting in malaria, yellow fever, growth and reduce a productive yield of the crop.
etc. Like the mosquito, the aphids mouthparts are
ideally suited for such transmission because the sty-
lets act like a hypodermic needle injecting the virus Honeydew Excretion
into the plant as it probes and then sucks the sap.
Also, even if the aphid did not have the virus, it This very natural aspect of aphid biology and
would pick it up when it feeds on an already virus- behavior is discussed later in the section on Ant
infected plant. A winged aphid (alate) is especially Aphid Mutualism. In the present context, however,
like the mosquito because by flying it can disperse the honeydew that is deposited not only becomes
the pathogen to many other host plants. sticky to the touch, but can attract saprophytic
There are two ways in which an aphid vector sooty-mold fungi to the plant. This may cover the
can transmit a virus from one plant to another: (i) leaf surface and accelerate aging of the plant. It is
stylet-borne transmission, where the virus con- economically damaging if the fruit or vegetable is
taminates the mouthparts just by the aphids prob- blemished and rendered unattractive for sale in a
ing the host plant. However, this virus is market. Also, car owners are unhappy with this
non-persistent on the stylets, lasting only an hour sticky goo on their automobiles if they unknow-
or so, and therefore will eventually disappear on ingly parked under a tree infested with aphids.
the aphid vector. (ii) circulative transmission,
when the aphid actually feeds on an infective plant
already having the virus. As a result, the virus Beneficial Effect
invades the body of the aphid. After a latent period,
the virus multiplies in the aphids tissues and enters Some researchers suggest that aphids may be ben-
the salivary glands, from where it can be injected eficial to plants in a kind of symbiotic mutualism.
 Aphids (Hemiptera: Aphididae)
A 203

In this unproven scenario, plants benefit by having owever, this growth hormone normally is found
H
the aphids remove surplus sugars (especially tri- in the plant itself which may account for its pres-
saccharide melezitose) which can be utilized by ence in the sap-feeding aphid. Gall aphids synchro-
nitrogen fixing bacteria in the soil. As a result, nize their development with their host plant, and
these bacteria increase in the soil beneath aphid- may even modify the development of the host plant
infested plants and make more nitrogen available itself. Finally, some galling aphids are unusual in
for the plants growth, and hence are beneficial to having soldiers (see section above on Soldiers), and
the plant. these species tend to produce completely closed
galls on their primary hosts. However, not all aphid
galls are completely closed, but in those that are, a
Galling monoclonal colony of aphids can exist within the
gall that was started by a fundatrix. Hence, there is
Some species are called gall aphids because they probably a long evolutionary history between
cause the plant to develop swollen tissues called theplant as host and the aphid as parasite in this
galls that are usually on the leaf or petiole. This galling behavior. As is often true in similar host-
involves a combination of both inhibition and parasite relationships among animals, the host
stimulation of the plant tissue at the feeding site plant may not suffer unduly in this parasitic type
that results from stylet probing and injection of of symbiosis when both organisms have been in
saliva. Galls are hollow outgrowths on the plant contact with each other over millions of years.
and can appear as abnormalities or deformities.
This cecidogenesis or gall-forming behavior is not
limited to aphids, but is also produced by Ant-Aphid Mutualism
hymenopteran gall wasps and dipteran gall flies or
midges. Although relatively few species of aphids There is a symbiotic mutualism between these two
induce galls, the shape of the galls is often charac- major groups of insects by which the ants obtain a
teristic for each species of aphid, so that the aphid sugar-rich food (honeydew) from the aphids,
seems to have the major role in forming the shape while the ants protect aphids from predators and
of the gall. Galls not only give protection to the parasitoids (see section on Natural Enemies). This
aphid, but may also provide a better food source in is the result of a long-term evolutionary history.
the following way. A gall provides sheltered pro- An ant that imbibes this sugary honeydew can
tection for the aphid from insect predators and transport it to nestmates in its crop, and then
parasitoids, and the aphids feeding may influence transfer it to another ant by means called trophal-
the metabolism of the plant and cause physiologi- laxis. However, not all species of aphids are ant-
cal changes that could improve the aphids food attended, nor do all species of ants attend aphids,
supply. Often, there can be intense competition and even myrmecophilous (ant-loving) aphids
and aggressive behavior among gall aphids for the differ in their dependence on ants. Most myrme-
best feeding sites on a leaf or petiole where a gall cophilous aphids live above-ground and are gre-
can be formed. garious, rather large in size, and often conspicuously
The formation of a gall by the plant probably is colored. But as a result of this mutualism with
due to the plant tissues reaction to aphid feeding ants, these aphids do not have well-developed
when it probes with its stylets and injects large defensive structures on their bodies, and do not
amounts of saliva into the host plant. It is known display escape behavior to avoid an approaching
that a plant growth hormone called indole acetic ant nor even a predator or parasitoid, perhaps
acid (IAA) is present in aphid saliva, and so it may because they feel safe in the company of their ant
be that this chemical induces gall formation. protectors.
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A Aphids (Hemiptera: Aphididae)

This mutualistic behavior is all the more c olony or even to a different aphid species that
amazing when it is realized that most ant species might be nearby.
are aggressive predators that would normally Ants search plants for aphids, and when they
attack any available prey, especially rather helpless are discovered, the ant returns to the nest laying
aphids. Yet, the ants that associate with aphids do down a recruitment chemical pheromone trail
so in an almost tender way, and milk them for which worker ants from the nest follow to the
their sugary honeydew which comes from the aphids. Since many species of ants tend a variety of
anus. The ant may antennate or stroke the rear of species of aphids, it has been suggested that at least
the aphids abdomen to stimulate this release of some elements of the antsbehavior are learned
honeydew droplets which the aphid does in an rather than innate. Both ants and aphids make
accommodating way without any interruption in great use of intra-specific and perhaps even inter-
its normal feeding behavior. specific pheromonal communication. Most ant
Aphids that are not attended by ants behave colonies tend a number of aphid species simulta-
differently by raising and contracting the abdo- neously, and it seems likely that there is competi-
men/rectum, thus ejecting the droplet of honey- tion between the aphids for the antsattention.
dew some distance from themselves. Some Seasonal changes in ant availability and their
species even use their hind legs to flick the hon- demand for honeydew might be factors in this
eydew away, perhaps to avoid contaminating the competition. In temperate regions, host plant
colony with this sugary material that might availability for aphids and therefore honeydew
develop sooty-mold fungus. As a general rule, production vary seasonally, as does the antsability
aphids that are not ant attended have a long to collect these sugars.
cauda and long siphunculi or cornicles, perhaps It is unclear to what extent there may be
used for defensive purposes against predators predation of aphids by their ant protectors, but it
and parasitoids, since there are no ants to protect seems that a significant amount of predation does
them. indeed occur. Perhaps the ants need some protein
Studies have shown that ants can have a posi- as well as carbohydrates from honeydew, and in a
tive effect on the number of aphids, and even on coevolutionary way the aphids may find limited
the efficiency of feeding by increasing the inges- predation (especially in large colonies) a necessary
tion of phloem sap with a resulting increase in the price to pay for protection from natural enemies,
production of honeydew as a reward for the ants. and even for the removal of potentially contami-
Ant attended aphid colonies are usually larger, nating sugary honeydew.
feed more heavily, and produce fewer winged
(alate) offspring. There can also be a stabilizing
effect on aphids, so that the size of the aphid col- Natural Enemies of Aphids
ony may be dependent on the presence of ants.
However, when an aphid colony becomes too This discussion will be limited to the natural
large, the host plant will deteriorate more quickly enemies of aphids that are themselves insects,
and the aphids may move off it leaving the ants and not other animals such as birds, nor even
behind. To avoid this loss of honeydew source, it pathogenic fungi, etc., that also can kill aphids. In
may be that ants control the aphid population size entomology, insects that attack, feed on, and kill
and keep it stable so that the host plant will not be other insects are called entomophagous insects.
excessively harmed. On the other hand, if the However, in the present context, insects that kill
aphids become too few to produce an adequate aphids are more precisely called aphidophagous
supply of nutritious honeydew, the ants may switch insects. As a general introduction, some defini-
to another and larger myrmecophilous aphid tions must be given. Insects that attack, feed on,
 Aphids (Hemiptera: Aphididae)
A 205

and kill other insects (not just aphids) are divided increases in size, it can sometimes consume more
into two major categories: than 100 aphids per day. The larva has pointed
jaws which it uses to pierce the aphid cuticle. Saliva
is then injected into the aphid which digests the
Predators body contents into a semi-liquid which can be
sucked up. Solid remains of the aphid may be eaten
Predators are insects that attack, feed on, and kill later if the larva is large enough. However, cocci-
the prey directly. Depending on the species of nellids have their own natural enemies especially
predator, both males and females as well as the in the orders Diptera and Hymenoptera.
immature stage and/or the adult can do this. Usu-
ally, more than one prey is required for the preda-
tor to reach adult sexual maturity. Lacewings (Order Neuroptera, Families
Predators of aphids expend energy and time Chrysopidae, Hemerobiidae)
searching for prey, and so maximum efficiency is
achieved when the predator finds an entire colony These are delicate nerve-winged insects with
of aphids and not just an individual. Once in a large transparent wings that are often colored light
colony, many predators proceed slowly and stealth- green or brown as is the body. Depending on the
ily so as not to raise an alarm. An extreme example species, they feed both as larvae and adults, and
of such a predator would be the blind, legless larva are considered important predators of aphids
of a syrphid hoverfly (mentioned below). Exam- (perhaps second only to coccinellids) and have
ples of major predators of aphids are given next: therefore been used in biological control pro-
grams. The larvae have hook-like piercing jaws
that are used to suck up the body contents. The
Ladybird Beetles (Order Coleoptera, aphid prey is held up in the air while it is being
Family Coccinellidae) eaten. In some species, the adult lacewing lays eggs
with each one attached to the end of a vertical stalk
These are the best known of aphid predators, and which is quite visible when many eggs are laid
they feed both as immature larvae and also as together on a leaf.
adults. These are very familiar beneficial insects,
but often incorrectly called ladybugs because
bug should be limited to the true bugs in the Hoverflies (Order Diptera, Family
order Hemiptera that have piercing-sucking Syrphidae)
mouthparts. They have a convex shape and usually
colorful markings. Because they are very common As the name indicates, the adult flies hover in the
wherever aphids are found around the world, they air over one spot, and then dart to another loca-
have been intensely studied for their use in bio- tion. The adults can be seen visiting flowers where
logical control programs. The coccinellids that are they feed on nectar and pollen, and so are also
brightly colored are demonstrating warning or called flower flies. The abdomen is often brightly
aposematic behavior, i.e., they are distasteful to colored with bands of white or yellow contrasting
their own predators, such as birds. Even their eggs with a black background, perhaps as mimicry of
are often orange or yellow. The larvae that hatch wasps. It is not the adults that eat aphids, but rather
from these eggs are notorious for their cannibal- the female lays her eggs close to or within an aphid
ism on coccinellid eggs and other smaller sibling colony. From each egg hatches a dipteran larva or
larvae because they have to feed almost immedi- maggot that is blind and legless, dorso-ventrally
ately on some prey or die. As the larva molts and flattened and tapered at the anterior end. Like
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A Aphids (Hemiptera: Aphididae)

lacewings, the syrphid larva feeds on the aphid by true parasite (flea on a dog) usually does not kill
piercing and sucking out the body contents, while the host (dog).
holding the prey aloft. Parasitoids of aphids are micro-wasps (4 to
5 mm in length or smaller) in the order Hy
menoptera, and are usually classified both taxo-
Cecid Flies (Order Diptera, Family nomically and behaviorally in only two families,
Cecidomyiidae) Aphelinidae (superfamily Chalcidoidea) and
Aphidiidae (or Family Braconidae and Subfamily
These tiny flies are often called gall midges Aphidiinae) (superfamily Ichneumonoidea). These
although the species that attacks aphids do not parasitoids are quite host specific in using only
form galls on plants. Hence, these cecid flies are aphids as hosts (and no other group of insects).
also called aphid midges, but the adult does not But, even among the thousands of aphid species as
feed on aphids. Each female can lay about 100 eggs possible hosts, different parasitoid species display
on leaves and stems of plants infested with aphids. a feeding behavior that ranges from a continuum
It is the maggot-like larva that feeds by piercing of polyphagy to a certain host specificity of oligo-
the aphid with its long serrated mandibles, suck- phagy to monophagy, so that many species of par-
ing out the body contents. asitoids limit their attacks to only one or a few
species of aphids.
Using as an example a typical species in the
Anthocorid Bugs (Order Hemiptera, genus Aphidius in the family Aphidiidae, the
Family Anthocoridae) female micro-wasp is quite host-specific, and is
called endophagous because she lays an egg inside
These are called minute pirate bugs or flower the live aphid. Her ovipositional behavior is to
bugs because they are often found on flowers attack the aphid with a quick thrust of her oviposi-
where they may feed on plant juices. Most species tor which is usually brought forward between her
are general predators on thrips, mites, and other legs, and is positioned in front of and beneath her
small arthropods besides aphids. However, the head. After the egg has been successfully depos-
two genera Anthocoris and Orius are predomi- ited inside the live aphid, the female departs to
nantly aphid predators. Being hemipterans, they attack another aphid, and her involvement with
have simple or incomplete metamorphosis, and the first aphid is ended. Her offspring, however, is
the adults as well as the nymphs feed on aphids the parasitoid larva that hatches from the egg
by sucking out the insides through their styliform inside the live aphid that will ultimately kill the
mouthparts. aphid. Oddly enough, the aphid host usually con-
tinues to feed on the host plant as if nothing had
happened and without changing its normal behav-
Parasitoids ior. Over a period of approximately 810 days that
varies with the species of aphid and parasitoid, the
Parasitoids are insects (orders Hymenoptera and larva molts several times while gradually devour-
Diptera) in which the adult female attacks what is ing the aphid internally, finally killing it. Then the
called the host, but she only indirectly kills the fourth and last larval instar spins a cocoon inside
host because the female merely lays her egg in, on the dead aphid, whose exoskeleton becomes hard
or near it. It is the larval offspring from the egg and changes from its original color to brown
that actually feeds on and kills the host. In older (which is now referred to as a mummy). The
literature, these parasitoids were called parasites, parasitoid larva may fasten the ventral side of the
but this terminology was misleading because a mummy to the leaf. It pupates inside the mummy,
 Aphids (Hemiptera: Aphididae)
A 207

and approximately 45 days later (or about 1215 Since many aphid species are such worldwide
days after the original oviposition) the new adult pests, hyperparasitoids of aphids have been espe-
wasp parasitoid cuts a circular emergence or exit cially well-studied, and can be categorized as fol-
hole in the mummy (usually in the dorsum of the lows depending on their adult ovipositional and
abdomen) and pulls itself out. The adult wasp will larval feeding behaviors: (i) The female wasp of
find a mate within a short time after emerging endophagous hyperparasitoid species deposits her
from the dead aphid mummy. When fertilized, egg inside the primary parasitoid larva while it is
this new generation of adult female will start the still developing inside the live aphid, before the
cycle again by attacking and depositing her egg aphid is mummified. But, the egg does not hatch
inside another aphid. Note that it is the parasitoid until after the mummy is formed, and then the
larva that feeds on and kills the host aphid, not the hyperparasitoid larva feeds internally on the pri-
adult female that only oviposits inside the aphid mary larval host still inside the mummy. (ii) The
and then departs. Remember that during the mod- female wasp of ectophagous hyperparasitoid
erate summer months, there are long periods in species waits until the primary parasitoid larva
the life cycle of an aphid colony when it is sessile has killed the aphid and formed the mummy.
and does not move very far away as long as the Then she drills a hole through the mummy, and
host plant provides sufficient nourishment. Per- deposits her egg externally on the surface of the
haps for this reason, micro-wasp parasitoids of primary parasitoid larva inside. After hatching, the
aphids have been used quite successfully in bio- hyperparasitoid larva feeds externally on the pri-
logical control programs around the world. mary larval host while both are still inside the
mummy. In both cases, the hyperparasitoid larva
then pupates inside the mummy, and as with the
Hyperparasitoids primary parasitoid described above, the new adult
wasp hyperparasitoid cuts an emergence or exit
The micro-wasp parasitoid described above is hole in the mummy (usually in the dorsum of the
technically called a primary parasitoid, and it is abdomen) and pulls itself out. The adult wasp
considered beneficial because it kills the aphid hyperparasitoid will find a mate within a short
which may be a pest insect. However, there are time after emerging from the dead aphid mummy.
other species of micro-wasps also in the order When fertilized, this new generation of adult
Hymenoptera, but not in the same families as the female hyperparasitoid will start the cycle again
primary parasitoids of aphids just discussed. These byattacking and depositing her egg in or on a pri-
micro-wasps have evolved to a higher trophic mary parasitoid larva inside another aphid.
levelso that we have an example of multitrophic There is an economic interest in hyperparasit-
ecology and behavior. At the 1st trophic level is ism because if primary parasitoids are considered
the host plant, then at the second trophic level beneficial insects (especially when used in biologi-
isthe herbivorous or phytophagous aphid, and at cal control programs) then it would seem that
the third trophic level is the carnivorous or ento- hyperparasitoids that attack primary parasitoids
mophagous primary parasitoid. Finally, at the might be detrimental. On the other hand, some
fourth trophic level is a different species of micro- ecologists suggest that perhaps hyperparasitoids
wasp called a secondary parasitoid or hyperpara- play a positive role in the ecosystem by preventing
sitoid that attacks the primary parasitoid while it an excessive increase in the numbers of the primary
is still inside the aphid. This food web involving parasitoids that might so reduce the p hytophagous
four trophic levels of plant, to aphid, to primary host as to result in the local elimination not only
parasitoid, to hyperparasitoid has been used as a ofthe insect pest, but also the beneficial primary
model system in community ecology. species as well. If more phytophagous insects of
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A Aphids (Hemiptera: Aphididae)

thesame species (such as aphids for example) were (biological control), host plant resistance (HPR),
to move into this local area without sufficient modifying aphid behavior, and finally integration
primary parasitoids to attack them, then there of these methods (IPM).
might be a resurgence of the insect pest.

Aphid Defenses Chemical Control and Resistance

As mentioned earlier in the section on polymor- Prior to World War II, chemical control of aphids
phism, there are aphid soldiers in a few species was limited to nicotine and arsenical products. These
that perform an altruistic role. These are female aphicides were sprayed on the crop, and at the time
nymphs that have morphological adaptations to seemed to have little negative residual or systemic
defend a colony against predators. Even if they are effects. After the war, however, DDT and other chlo-
not killed in this action, they do not reproduce. rinated hydrocarbons were developed and widely
Usually, species that have soldiers tend to form used as broad-spectrum insecticides that were con-
closed galls on their primary hosts (see section on sidered to be a panacea not only for control of aphids,
Galling). However, the majority of aphid species but for many other insect pests as well. Although not
do not have soldiers, yet many species are still systemic, they did have residual effects that in the
capable of defending themselves by various means beginning seemed to be a benefit because they were
such as the following: aggressive kicking, thick long-lasting. But eventually, evidence from field
defensive cuticles and/or spines, waxing predators studies demonstrated that these residues persisted
and parasitoids, using stylets to attack and kill in the ecosystem, and accumulated in the food chain
eggsof predators and even other species of aphids, causing unexpected dangers to non-target organ-
or suddenly falling off the leaf onto the substrate isms, especially to fish, birds, and even mammals. In
as a tactic that permits their escape from an addition, the unintended killing of beneficial insects
impending attack by an aphidophagous natural that were the natural enemies of the insect pest
enemy. Some aphids also emit chemical alarm resulted in pest resurgence, traded-pests, etc. The
pheromones that warn other aphids nearby of excessive use of these chemicals with these danger-
imminent danger. In this regard, it is interesting ous side-effects was eventually banned in many
that some aphid alarm pheromones may also act countries around the world.
as kairomones (communication chemicals between New generations of chemical insecticides
different species) so that predator coccinellid were developed such as the organophosphates,
beetles are actually attracted to the aphids. carbamates, and pyrethroids. To control aphids,
special aphicidal properties were emphasized:

Control of Aphids 1. Selective toxicity: predators and parasitoids not

killed, nor any other non-target organisms.
Prevention of damage to plants is especially impor- 2. Systemic activity: chemical is applied not only to fo-
tant when a major agricultural crop could be liage and seeds, but especially to the soil where
destroyed by aphids at great financial loss to the the roots take it up via the vascular system where
farmer. Even forest and shade trees have economic aphids feed on the phloem sieve tubes.
as well as esthetic significance when they are used 3. Residues: Some residual activity may be needed to
for logging or as parks. Control involves using prevent aphids from reinfesting the crop. In the
methods to protect the crop from aphid attack by case of food and fodder crops, however, chemical
various means such as chemicals, natural enemies persistence can be dangerous. Aphicides on such
 Aphids (Hemiptera: Aphididae)
A 209

plants should decompose into harmless com- As a result of many years of subjection to
pounds before harvest. chemical insecticides, natural selection has devel-
4. Rapid action: to prevent transmission of non-persi- oped resistance in large populations of many aphid
stent viruses, quick mortality of aphids is neces- species not only in the field, but especially in
sary. Some synthetic pyrethroids show repellent greenhouses. The biochemical cause of resistance
action that deters aphids from settling. in aphids is still being studied, and there seems
5. Low phytotoxicity: the aphicide should not harm the to be a positive correlation between resistance
crop itself because the purpose of the chemical is andthe activity of enzymes (esterases). It has also
to protect the plant from aphids without having a been suggested that symbionts are involved in
toxic effect on the plant. resistance. In any case, although some chemical
aphicides may still need to be used, they should be
applied judiciously to avoid the typical insecticide
Application of Aphicides treadmill cycle of excessive dependence on chemi-
cals with unintended results such as pest resur-
No general rule can be given because so much gence, traded-pests, etc.
depends on local conditions, type of chemical,
length of growing season, aphid population size,
time of day, weather, etc. Sometimes soil or seed Biological Control
application is sufficient instead of dusting or spray-
ing, and of these two, if the crop is dense, then per- Biological control is the intentional use by humans
haps dusting is better than spraying. Farm advisors of an insect pests natural enemies such as benefi-
should be contacted because they know the local cial insect predators and parasitoids as well as
situation for making recommendations. pathogens (bacteria, viruses, protozoa, fungi, nem-
atodes, etc.) in order to lower the population level
of the insect pest below the economic threshold so
Resistance that crop loss is reduced and the farmer can have a
successful harvest. In the field, the aphidssessile
It is well-documented that chemical insecticides feeding behavior for long periods of the year makes
are powerful agents of natural selection so that them especially attractive to natural enemies. In
over time some mutated insects such as aphids addition, aphids are amenable to studies in the lab-
develop resistance. This renders the chemical oratory where many species can be rather easily
inefficient, resulting in attempts to restore suc- reared along with their natural enemies for research
cess by repeating applications, then increasing and experimentation in insect cages, growth cham-
the dosage, etc. In addition, as mentioned above, bers, and environmentally controlled walk-in
the beneficial natural enemies are also negatively rooms. As a result, and because of their worldwide
affected. There are reports of 20 or more aphid pest status (especially in the temperate zones),
species that have developed resistance to various aphids have been the target of many successful
chemical insecticides. The green peach aphid, biological control programs.
Myzus persicae (Sulzer), is an excellent example. There is an aspect of this method called
It is a notorious aphid pest that not only has sec- classical biological control wherein the natural
ondary hosts in over 40 different plant families, enemy is introduced as an exotic parasitoid or
but it is one of the most important vectors of predator from another country or even more fre-
over 100 plant viruses. Although M. persicae quently from another continent. Also, the insect
is probably of Asian origin, it is now found pest is often an exotic invader into a new habitat or
worldwide. the insect pest could be indigenous. In either case,
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A Aphids (Hemiptera: Aphididae)

it seems that the indigenous natural enemies are by A. ervi that was first introduced in the east.
incapable of keeping the new or old insect under However, good control of the pea aphid continu-
control so that it has now reached pest status. To es across the continent.
obtain the exotic natural enemy involves foreign
exploration and importation, mass rearing, colo- Unlike these three examples of classical bio-
nization, establishment, etc. Three examples of logical control involving exotic aphids, it can hap-
this type of classical biological control of aphid pen that for various ecological and behavioral
pests are given here because they are so well docu- reasons the aphid pest is indigenous and the native
mented, and can be easily referenced in the ento- natural enemies do not control it. In this case, at
mological literature: least the conservation of the existing, indigenous
natural enemies is of primary importance. This
1. The first case of successful aphid biological control can even be assisted by augmentation and inunda-
was against the wooly apple aphid, Eriosoma la- tive releases of these indigenous natural enemies
nigerum (Hausmann), a serious pest of apple in from mass-rearing insectaries. Sometimes, exotic
North America and now worldwide in distributi- but taxonomically closely related species to the
on. Beginning in 1920, an aphelinid wasp parasi- indigenous species of natural enemy might be
toid, Aphelinus mali, was imported from the Uni- imported from abroad and used to complement
ted States and became established in 42 countries the native species, thus improving the possibility
with generally satisfactory results. of controlling an indigenous pest.
2. Another success was with the spotted alfalfa aphid, In comparison with chemical control, biologi-
Therioaphis trifolii (=maculata) (Buckton), which cal control is non-polluting, non-toxic, and self-
invaded the southwestern United States in 1953. perpetuating, and makes no claim about completely
Two aphidiid wasp parasitoids, Trioxys compla- eradicating the insect pest. Instead, the population
natus and Praon exsoletum, as well as the apheli- level of the pest is lowered to an economic thresh-
nid Aphelinus exsoletum were imported from the old acceptable to the farmer. Since this involves a
Middle East, and resulted in excellent control of living ecosystem, biological control tends to be
this exotic aphid. This case was also important hi- permanent, and therefore less expensive. Needless
storically because the concept of integrated pest to say, whether the pest is an aphid or some other
management (IPM) was pioneered during this insect, proper scientific procedures demand that
period by entomologists at the University of Ca- extensive research be done on the biological
lifornia. aspects of both the insect pest as well as the natu-
3. Finally, although the pea aphid, Acyrthosiphon pisum ral enemies (indigenous and exotic) in relation to
(Harris), was a Palearctic species, it had existed the ecosystem.
as an exotic invader in North America since the Finally, pathogens such as bacteria, viruses,
end of the 1800s where it was a pest on alfalfa protozoa, fungi, nematodes, etc., can be used as
and peas. Indigenous predators and parasitoids microbial insecticides against insect pests. Aphid
seemed ineffective, so in 1958 the specialized diseases have been recognized for over 150 years,
aphidiid parasitoid, Aphidius smithi, was impor- but only entomogenic fungi in the order Ento-
ted from India into the western United States. mophthorales have been considered as the main
Later in 1963, the polyphagous aphidiid parasi- pathogen against aphids. Usually warm and humid
toid, Aphidius ervi, was introduced from Europe weather can spread the fungus very quickly into
into the eastern U.S. Both parasitoids have been an epizootic, especially when the aphid colony is
successfully established resulting in good control. crowded. The infected aphid becomes brown and
Of ecological interest here is that over time, it inflated with liquid when it dies of mycosis. This
seems that A. smithi is being replaced in the west can happen in the tropics and greenhouse, but in
 Aphids (Hemiptera: Aphididae)
A 211

field conditions in temperate regions humidity is constantly being mass-reared in the insectary.
not that predictable. Much can still be done to use These are used not only for laboratory studies of
the potential of fungi in biological control pro- insect-plant interactions, but especially for the pur
grams against aphids. The other pathogens such as pose of bringing them into the field for artificial
bacteria and protozoa do not seem to have been infestation. In the field, these insect pests are
demonstrated to cause infections in aphids. placed on the cultivar to be infested and eventu-
Although baculoviruses and picornaviruses can ally evaluated as to the amount of damage caused
be transmitted transovarially and reduce the lon- to the plant as it grows. It must be stated, however,
gevity of an aphid, no viral epizootics of aphids that HPR to one insect pest does not mean that a
have been reported. cultivar is resistant to other taxa or even to related
species. Furthermore, the genotype may not be
resistant to other biotypes or races of the same
Host Plant Resistance (HPR) insect pest species that initially showed host plant
resistance.
Many plant species have defenses against herbi- Concerning HPR for aphids, the same general
vores including insects that is genetically heritable, principles and procedures are used as just men-
and hence controlled by one or more genes. Resis- tioned above. Hundreds of cultivars have been
tance of plants to insect attack is related to the developed for resistance to aphids for more than
heritable qualities of the plant that may reduce the fifty important crop plants in the families Legumi-
damage. The main task of agronomists is to nosae, Gramineae, Compositae, Cruciferae, Cucur-
increase the yield and quality of a crop by standard bitaceae, Rosaceae, Solanaceae, etc. The problem of
breeding methods. However, this can also include biotypes or races also occurs among aphids because
trying to breed genotypes into crops that make of their parthenogenesis, telescoping of genera-
them resistant to insect attack by using one or tions, host plant alternation, etc.
more of the following mechanisms:

1. Antibiosis: physico-chemical characteristics of the Modifying Aphid Behavior

plant that kill the insect;
2. Antixenosis: pest insect is repelled by the plant or at Aphid behavior can be modified by both preven-
least has no preference for it; tion of landing by aphids in flight, and by repelling
3. Tolerance: the plant can recover even after some fee- aphids that have already landed.
ding damage by the insect. Flying aphids are attracted or repelled from
plants by light of a particular wavelength. When
Plant characteristics vary depending on the spe- winged aphids first fly, they are attracted to the
cies, but host plant resistance can be morphologi- blue-ultraviolet light from the sky. However, after
cal (leaf size, shape, color, pubescence, thickness, a period of flight this is reversed, and instead of
texture), biochemical (lack of nutrients, allomones flying upwards, the sky may repel them and they
[feeding repellents, ovipositional and feeding are attracted to the orange-yellow-green light
deterrents, toxins], kairomones [attractants for reflected from the leaves below. This behavior
natural enemies]). Entomologists work closely might be exploited by using yellow traps to lure
with the agronomists to test or screen the suppos- them away from crops in a field (though as yet this
edly resistant crops (but still as high-yielding as has not been demonstrated). The yellow trap can
possible) to see if indeed these genotypes are also be filled with some liquid that kills the aphids that
resistant to a particular insect pest that is being have landed in them. Yellow traps are used exten-
studied. To do this, hundreds of insect pests are sively to monitor flights of aphids.
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A Aphids (Hemiptera: Aphididae)

Plant odors are volatile substances produced and/or less important to the farmer; intercropping
by plants that attract aphids in their host selection. uses the same principle but alternates field rows or
Aphids on agricultural crops tend to be polypha- sections of the crop with another plant; tillage
gous, so perhaps specific volatile cues are not too (mechanical manipulation of soil to reduce weeds,
important. However, aphids on perennial crops improve drainage by plowing, hoeing, etc.); sanita-
and wild plants are more oligophagous and even tion is the removal of weeds or crop residues that
monophagous for which plant odors are needed. might provide the aphid an alternate host; water
Hence, attractant baits have been tried as well as management depends on the needs of the host
repellent chemicals that may also have a role in plant and the biology of the aphidspecies.
aphid control.
Alarm pheromones are released by some spe-
cies of aphids when they are attacked by natural Integrated Pest Management (IPM)
enemies. It would be advantageous for flying
aphids to avoid landing on a plant where aphid In their evolution, aphids have taken advantage of
colonies are being attacked and have released an favorable agricultural habitats especially through
alarm pheromone. Synthetic alarm pheromones monoculture, thus making the agroecosystem an
have been used successfully, but because some are attractive food source. Although different species
highly volatile, a formulation with a slow release of aphids vary in their host range from polyphagy
would enhance this control method. to monophagy, they are often able to survive on
Synthetic chemical repellents would be a non- herbs in the vicinity of the crop or simply to fly to
toxic alternative to insecticides, and are safer to another area where a more suitable host plant is
the applicator and to the environment. However, more available. Realistically therefore, eradication
there is a problem with aphids that are vectors of a is all but impossible. Because of various side effects
non-persistently transmitted virus. It would have mentioned earlier, reliance only on chemical
to have its repellent effect act very quickly before insecticides should not be the main option.
the aphid makes its first probe. Even chemical Instead, it is sensible to integrate as many of these
aphicides have this difficulty in not acting fast control methods just discussed. This concept of
enough to prevent that first probe by which an integrated pest management (IPM) was first devel-
uninfected aphid picks up the virus, or if already oped at the University of California during the late
infected, then before the aphid probes into a 1950s. An acceptable definition of integrated pest
healthy plant. There is a continuing need to study management (IPM) should include the following
the chemoreception of aphids and their resulting entomological and ecological aspects: a pest man-
behavioral responses. agement system that utilizes all suitable control
methods to reduce and maintain the pest popula-
tion level below that causing economic injury,
Cultural Control with special concern for the environment includ-
ing the insects natural enemies. This sound eco-
This method involves the use of normal agricul- logical philosophy should be applied to aphids and
tural practices to reduce pest damage not only by to other insect pests whenever possible.
aphids but also by other insects. Such cultural tech-
niques can include the following: timing of plant-
ing and/or harvesting to disrupt the normal cycle Important Aphid Species
of aphid landing and feeding; crop rotation varies
the crop during the season or annually with another Although there are over 4,000 aphid species, only a
plant that would be unattractive to the aphid small percentage of these are pests. Nevertheless, it
 Aphids (Hemiptera: Aphididae)
A 213

is not surprising that general interest and most of wherever it was planted which is now worldwide
the funded research at universities and institutes in distribution. Its secondary hosts are in over 40
should be concentrated on aphid species that indeed different plant families, including many that are
are pests of agricultural crops, forest and shade trees also economically important. In temperate
because of their commercial and economic impor- regions it is usually heteroecious holocyclic, but
tance. With this bias in mind, listed in alphabetical can be anholocyclic where peach is absent and
order (English names) is a sampling of some impor- the climate permits winter survival. Because it is
tant aphid species: black bean aphid, Aphis fabae relatively easy to rear in laboratories and green-
Scopoli; black citrus aphid, Toxoptera aurantii houses, this aphids biology, anatomy, physiology,
(Fonscolombe); blue alfalfa aphid, Acyrthosiphon etc., has been intensely researched. In addition,
kondoi Shinji; brown citrus aphid, Toxoptera citrici- because of its economic importance, the ecology
dus (Kirkaldy); cabbage aphid, Brevicoryne brassi- of M. persicae has been studied, especially for
cae (Linnaeus); corn leaf aphid, Rhopalosiphum use with biological control.
maidis (Fitch); corn root aphid, Aphis (Protaphis)
maidiradicis Forbes; cotton or melon aphid, Aphis
gossypii Glover; cowpea or black legume aphid, Black Bean Aphid
Aphis craccivora Koch; grain aphid, Sitobion avenae
(Fabricius); green apple aphid, Aphis pomi De Geer; Aphis fabae Scopoli is also heteroecious holocy-
green peach aphid, Myzus persicae (Sulzer); green- clic, and in Europe it alternates between Eurony-
bug, Schizaphis graminum (Rondani); oleander or mus (strawberry bush) and various secondary
milkweed aphid, Aphis nerii Fonscolombe; poplar hosts where it feeds on many agricultural crops
petiole gall aphid, Pemphigus populitransversus including Vicia faba (broad bean) and other
Riley; pea aphid, Acyrthosiphon pisum (Harris); legumes. Besides this polyphagous behavior, it is a
potato aphid, Macrosiphum euphorbiae (Thomas); vector of more than 30 plant viruses. It is wide-
rose aphid, Macrosiphum rosae (Linnaeus); spotted spread in temperate regions of the Northern
alfalfa aphid, Therioaphis trifolii forma maculata Hemisphere, as well as South America and Africa,
(Buckton); tulip-tree aphid, Illinoia liriodendri except for the hotter parts of the tropics and the
(Monell); walnut aphid, Chromaphis juglandicola Middle East. A. fabae may be a complex of species,
(Kaltenbach); woolly apple aphid, Eriosoma lanige- and outside of Europe where it seems to have orig-
rum (Hausmann). inated, its taxonomic status is unclear. However,
Several of these important aphid species are because of its importance, it too has been intensely
worth special mention: studied in both field and laboratory research
projects.

Green Peach Aphid

Cotton or Melon Aphid
Myzus persicae (Sulzer) is probably the most
polyphagous of all aphids. As a result, it is the Aphis gossypii Glover is very polyphagous not just
most important insect vector of plant diseases on cotton and cucurbits, but also on such diverse
including transmission of over 100 plant viruses crops as citrus, eggplant, okra, peppers, coffee,
such as curly top of sugar beets, peach yellows, potato, cocoa, and many ornamentals such as
cranberry false blossom, aster yellows, and vari- Hibiscus. In addition, it can transmit over 50 plant
ous potato viruses, etc. It is pr obably of Asian viruses to important crops such as beans, peas,
origin on its principal primary host Prunus soybeans, crucifers, celery, cowpea, sweet potato,
persica (peach), and then followed this host tobacco, tulips, strawberry. Its distribution is now
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A Aphids (Hemiptera: Aphididae)

worldwide including the tropics and many Pacific races and subspecies on different host plants, but
islands. In the temperate latitudes with cold tem- mostly important legumes such as alfalfa, clover,
peratures where crops are raised in greenhouses, peas, broad beans, etc. A. pisum is a vector of more
A. gossypii is a major pest. Perhaps it is of palaearc- than 30 virus diseases, and although probably palae-
tic origin because it is anholocyclic in Europe. arctic in its origin, it is now worldwide in its distri-
However, it seems to be holocyclic in North bution where it is holocyclic in the temperate
America, China, and Japan. regions, and perhaps anholocyclic in warmer cli-
mates. Because it can be reared easily in the labora-
tory with its micro-wasp parasitoids, as mentioned
Oleander or Milkweed Aphid earlier, it was an example of a classical biological
control program that was successful.
Aphis nerii Fonscolombe is an especially interesting
aphid because of its attractive bright yellow color
contrasted with black cornicles and cauda, and dark Summary
antennae and legs. Such aposematic behavior adver-
tises and warns potential predators that it is unpal- Aphids fascinate the non-entomologist as well as
atable and even harmful. This is because while amateur and professional entomologists because of
feeding, it has sequestered poisonous chemicals their sometimes unique and always unusual biolo-
(cardiac glycosides) from its host plants mainly in gies. Although small in size, their external morphol-
the families Apocynaceae and Asclepiadaceae such ogy and internal anatomy as well as their
as oleander and milkweed. It has thus coevolved by polymorphism and polyphenism make aphids
transferring for its own protection the poisonous interesting. One marvels at their reproductive
defense of these host plants. Instead of using cryptic behavior (parthenogenesis, telescoping of genera-
or camouflage defense as many other insects do, A. tions, sex determination), life cycles (host plant
nerii demonstrates behavioral convergent evolution alternation), antaphid mutualism, etc. Finally, of
with the similarly bright warning coloration (orange course, aphids have had an enormous economic
and black) of the monarch butterfly that also feeds impact as pests on the worlds agricultural crops,
on milkweed. A. nerii then reinforces this apose- forest and shade trees, not only by their feeding, but
matic behavior by forming dense colonies that are as vectors of plant viruses. This is a great challenge
frequently concentrated on young stems. Also to humankind to control them by using ecologically
unusual is its life cycle that seems to be only anho- safe as well as effective methods. Hence, aphids are
locyclic with no sexual morphs. It is widely distrib- a rewarding subject for observation and research.
uted in the warmer regions of the Old and New Bugs
World, plus the tropics and subtropics. Transmission of Plant Diseases by Insects
Plant Viruses and Insects

Pea Aphid
References
Acyrthosiphon pisum (Harris) is a large aphid with
slender appendages and long cornicles. There are Blackman RL (1974) Aphids. Ginn and Company, London,
both green and red-pink morphs, similar to the UK, 175 pp
potato aphid, Macrosiphum euphorbiae (Thomas), Blackman RL, Eastop VF (2000) Aphids on the worlds crops:
an identification and information guide, 2nd edn. Wiley,
that also has green and red-pink morphs with both Chichester, UK, 466 pp
aphid species being in the same aphidine tribe Mac- Dixon AFG (1998) Aphid ecology - an optimization approach,
rosiphini. The pea aphid seems to be a complex of 2nd edn. Chapman and Hall, London, UK, 300 pp
 Apiculture (Beekeeping)
A 215

Minks AK, Harrewijn P (eds) (1989) Aphids: their biology, Apiculture (Beekeeping)
natural enemies and control, vol 2A (450 pp), vol 2B
(364 pp), vol 2C (312 pp). Elsevier, Amsterdam, The
Netherlands malcolm t. sanford1, james e. tew2
van Emden HF (ed) (1972) Aphid technology: special refer-
ence to aphids in the field. Academic Press, New York, 1
University of Florida, Gainesville, FL, USA
NY, 344 pp 2
The Ohio State University, Columbus, OH, USA

The science and art of managing honey bees

Aphid Flies calledapiculture or beekeeping is a centuries-old
tradition. The first beekeepers were hunters, seek-
Members of the family Chamaemyiidae (order
ing out wild nests of honey bees, which often were
Diptera).
destroyed to obtain the sweet reward, called honey,
Flies
for which these insects are named. As interest in
honey bees grew, so too did the entomological and
biological knowledge needed to better manage
Aphodius Grubs (Coleoptera:
colonies of Apis mellifera. The innovations that
Scarabaeidae)
allowed modern beekeeping to arise were primar-
ily developed in the 19th century. The most impor-
At least two species of Aphodius are important
tant include the moveable-frame hive, smoker and
pests of turfgrass.
centrifugal extractor. It is remarkable that these
Turfgrass Insects and their Management
continue to be the hallmark of the beekeeper a
century and a half later.
Aphrophoridae Honey bees are native to the Old World, but
were quickly introduced into the Americas and
A family of bugs (order Hemiptera, suborder Australia as part of European settlement. This
Cicadomorpha). social, perennial insect is now found on all conti-
Bugs nents and in most environments. Although honey
continues to be an important product of honey
bees, their most valuable service is pollination.
Aphylidae A large commercial pollination effort exists in
many countries to ensure maximum quality and
A family of bugs (order Hemiptera, suborder quantity of crops pollinated by honey bees. The
Pentamorpha). major crops involved are nuts, berries, fruits and
Bugs vegetables.
Although the technology employed in bee-
keeping is traditional, the problems facing present
Apiary day apiculture are modern and formidable. This is
due primarily to worldwide distribution of exotic
A location where honey bees and bee hives are kept. diseases and pests that have devastated beekeeping
Apiculture (Beekeeping) industries and honey bees alike. The major prob-
lems affecting U.S. beekeeping over the last thirty
years come from introduction of the tracheal mite
Apical (Acarapis woodi), Varroa mite (Varroa destructor)
and small hive beetle (Aethina tumida). These have
A term pertaining to the apex (tip) or outer end. produced a new kind of beekeeping that is much
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A Apiculture (Beekeeping)

more aligned with production agriculture because Venom: A mixture of compounds injected by bees for
it has become associated with and/or reliant on defensive purposes.
chemicals. It is an irony that honey bees, heretofore
considered wild animals needing minimal human
intervention, have become more domesticated, The Honey Bee Colony
requiring human help to survive human-induced
introduction of exotic species. Honey bee biology is described elsewhere in this
In spite of the increase in time and effort document. The colony of Apis mellifera is com-
needed to keep bees in the modern setting, the posed of one queen (fertilized female), up to sev-
fascination presented by the honey bee and its eral thousand males (drones) and tens of thousands
products continues. Thus, a small but enthusiastic of workers (unfertilized females). For the purposes
cadre of novice beekeepers appears each season to of the beekeeper, worker bees are the most impor-
take up the challenge of managing one of natures tant; they are often divided into two classes, young
most complex creatures. This infectious joy of nurse bees (feed the young) and older forager bees
beekeeping continues to proliferate across the (collect pollen and nectar).
generations, afflicting both beginners and com-
mercial beekeepers generations removed from the
first person in their family to be smitten by the Major Developments in
beekeeping bug. Beekeeping
The purpose of this article is to describe
aspects of beekeeping that will be important for a Most new ideas in beekeeping are not novel. A
basic understanding of the craft by both novice scan of the literature usually will show that they
beekeepers and the general public. It includes have been developed, sometimes on several sepa-
information on the honey bee colony and its man- rate occasions, by enterprising apiculturists in the
agement, as well as that with reference to nectar past. Three eras have been identified in the devel-
and floral resources and the use of these important opment of the craft.
insects in commercial pollination. Beekeeping prior to 1500 was primitive (rus-
tic), and consisted of little more than honey hunt-
ing, robbing the sweet from established nests. A
Products of the Hive famous rock painting at Cueva de las Araas,
Spain, depicts this activity as early as 5000 b.c. The
Many people keep bees because they are fascinated Philistines dabbled in beekeeping as did the
by these social insects. The vast majority, however, ancient Egyptians, Greeks, Sumerians, and others.
are also interested in collecting the useful prod- Even before the honey bee was introduced to the
ucts of the hive, which include: Americas, other kinds of bees were kept for honey
Honey: Modified nectar collected by honey bees that is and wax. The Inca and Maya of the New World
mostly carbohydrate. cultured the stingless bees (meliponidae). There is
Pollen: The male floral part collected by honey bees that a renaissance in this activity in the American trop-
is mostly protein. ics, but the term beekeeping has always been
Propolis: A mixture of resins and oils collected by bees reserved for those managing the Old World
from plants used to glue hive parts together and western honey bee (Apis mellifera).
patch holes. From 1500 to 1851 (pre-modern beekeeping),
Beeswax: The material that makes up the bee nest. great strides occurred in knowledge about honey
Royal Jelly: A high-protein food that is used to feed bees. The queen was discovered to be female in
developing queens. 1586. Drones were first identified to be males in
 Apiculture (Beekeeping)
A 217

1609. Pollen was determined to be the male part of today. The Irish and Norwegians may have brought
plants in 1750. Drones were shown to mate with honey bees to the Americas as early as 900 a.d.
the queen in 1792 and recognized as partheno- They came to the colony of Massachusetts in 1665,
genic in 1845. where the aborigines called them white mans
Concurrently with biological knowledge, flies. These insects may have been introduced
management technique evolved. For example, the sooner into the New World by the Spanish con-
concept of supering (adding boxes on top of colo- quistadors via Mexico, Florida, or Cuba.
nies for honey storage) was developed in 1665. A Italian bees (Apis mellifera ligustica) were first
wide variety of so-called patent hives were mar- introduced into the United States in the 1860s,
keted in the 1800s, an era known for huge contro- and Frank Benton imported Cyprian and Tunisic
versy over size and style of box, none of which were stock in the 1870s. Many more introductions suc-
really suitable to launch a new kind of beekeeping. ceeded these first attempts. African honey bees
The modern beekeeping era began in 1851 (Apis mellifera scutellata) were brought to Brazil in
when the Reverend L.L. Langstroth discovered the 1957. Semen from these so-called killer bees was
significance of the bee space, which led to the introduced into the United States in the 1960s, but
invention of the movable-frame hive. Other natural migration through Latin America allowed
advances followed: Johannes Mehring developed a population to become established in the United
the first foundation in 1857. Major Hruschka pro- States only when it crossed the Texas border in
duced an extractor in 1865. Moses Quinby 1990. Varroa jacobsoni (now known as Varroa
invented the smoker in 1875 and published his destructor) was introduced to Apis mellifera in the
first bee book in 1853. Comb honey production 1950s via its original Asiatic host Apis cerana. This
began with W.C. Harbison of California in 1857. parasitic mite had spread to all continents except
The years 1859 to 1890 encompassed the era Australia by the 1990s. New bee foods, including
of comb honey, known as the golden age of bee- high fructose corn syrup and the Beltsville Bee
keeping. Samuel Wagner published the first issue Diet were introduced in the 1970s. Honey became
of American Bee Journal in 1861. Gleanings in Bee a world commodity in the 1980s. The small hive
Culture was first published in 1873; it became sim- beetle (Aethina tumida) was introduced from
ply Bee Culture in the 1990s. Migratory beekeep- South Africa into the United States in 1998.
ing up and down the Mississippi River began in
1878 (it occurred much earlier in ancient Egypt on
the Nile). Package bees were first used in 1879. Sources of Information
J. George Doolittle developed the concept of com-
mercial queen rearing in 1888, using the grafting Beekeeping information can be found many
(larval transfer) technique. places. Traditional print resources include:
Lloyd Watson first used instrumental insemi- Bee Culture, A.I. Root Co., P.O. Box 706, Medina, Ohio
nation of the queen bee in 1926. This technology 44258, phone 1-800-289-7668 extension 3220,
spawned studies in controlled genetics, which led fax 330-725-5624
to selection of commercial lines such as Starline American Bee Journal, 51 South 2nd Street, Hamilton,
and Midnite honey bees. This continues to be of Illinois 62341, phone 217-847-3324, fax 217-847-
importance and increasingly is responsible for 3660
advances in selecting for hygienic behavior (dis- The Speedy Bee, P.O. Box 998, Jesup, Georgia 31598-
ease resistance) and tolerance to pests. 0998, phone 912-427-4018, fax 912-427-8447
With recognition that apiculture was a legiti- The Internet is now a prime source on infor-
mate vocation, the honey bee has been spread mation. However, it is suggested beginners find
worldwide by beekeepers. This continues even the bee inspector and state university extension
218
A Apiculture (Beekeeping)

educator in their state and address questions directly Protective equipment for the beekeeper has
to them. Each year, the magazine Bee Culture pub- also followed the same route. New materials such
lishes a comprehensive list in the April edition. as plastic netting, Velcro and others have meant
that beekeepers can work with more peace of mind
during manipulation of colonies.
Equipment As already noted, traditional beekeeping
equipment is made from wood. However, plastic
Of all things in beekeeping that are affected by the equipment also is in use for the traditional bee
modern world, perhaps beekeeping equipment is box. Plastic is also widely used as a wax founda-
the best candidate to look at within the context of tion base and in single component plastic frames.
newly evolving technology. Plans for standard, Plastic frames resist damage, do not require paint-
traditional wooden beehives can be found in many ing, and do not require assembly. However, it often
publications. Some parts of a beehive are easily takes more resources by the bees to draw out
made at home, especially brood chambers, supers, plastic or beeswax-coated plastic foundation.
tops and bottoms. However, others may not be; Some disadvantages of plastic are its tendency to
frame construction, for example, is best left to warp and become brittle when exposed to sunlight
commercial manufacturers. and difficulty in being sterilized by heat. Various
A major equipment consideration is use of companies use plastic to make containers for bee
beeswax, recycled from the bees themselves. Tra- products. Such containers eliminate the extracting
ditionally bees have been guided to make their phase of beekeeping and provide a container for
nest (comb) through use of embossed beeswax honey in its natural comb.
foundation. This material not only guides the There are all manner of gadgets used in the
bees in making worker cells, but also saves much art and business of keeping bees that do not gener-
time and energy in the bargain. Plastic (wax- ally get mentioned in standard references. The
coated or not) is being increasingly used for following are some of these gems:
foundation.
Beekeeping equipment is available from 1. The slatted (or slotted) rack was used initially to take
many places across the nation. Several concepts up the space of a deep bottom board. It assists in
are important when considering equipment. ventilation and reduces brace and ladder comb.
These are: (i) standardization, usually based on Some beekeepers swear by it, some at it.
conserving the bee space; (ii) changes in nominal 2. A division board feeder is a hollow insert filled with
lumber size, contributing to availability and wast- syrup that takes the place of a frame in a super
age problems in cutting wooden ware; and (iii) when a population is small. Easily homemade from
constant development and evaluation of new a board and nails, they quickly feed a small colony.
materials. Although plastics come to mind, there 3. A robber screen can be used to protect small colonies
have even been hives made from concrete to with- from being foraged by larger colonies, especially
stand tropical conditions. Nevertheless, wood during nectar dearth.
continues to be the material of choice by most 4. Top feeders come in various styles. These avert the
beekeepers. necessity to open the colony and/or to fill a fra-
Because individual suppliers or equipment me-style division board feeder. Top feeders hold
and prices are constantly changing, only an over- more and are more accessible.
view of beekeeping implements and paraphernalia 5. A screened ventilated bottom board provides air
is possible here. For up-to-date prices, its best to circulation during both summer and winter.
consult the bee journals, which actively cater to Newer information also suggests these are useful
the trade and bee supply outlets. in controlling exotic mite populations.
 Apiculture (Beekeeping)
A 219

6. Various painted patterns on the front of colonies can protective coating. The average life of a bee box is
help bees identify their own home, thus reducing about seven years. Scraped and routinely painted,
drifting (bees losing their way and entering fo- equipment can go much longer. Since the inside
reign colonies). surfaces of bee hives should not be painted, the
7. Drip boards serve several purposes. They collect paint film on the outer surface is often stressed by
errant honey leaks from supers stored on them, water migrating to the film from the inside of the
provide air space between the floor and honey hive rather than from the outside. Oil-based paints
stored in frames, and a space for two-wheeled will readily peel within just a couple of years. Due
hand trucks to grip the stack. to ease of application and lower cost, latex paints
8. A screened division board placed between two alien are better. The rubber-based latex paints will flex
colonies enables them to access each others odors, and resist chalking and peeling much more than
while keeping them physically separate. The end oil paints, but they, too, will finally succumb to
result is two queens working together to produce mildew and peeling.
a large population. Eventually they can be joined Some commercial beekeepers and beekeepers
after this close but separate association, however, in other countries routinely dip equipment in par-
one of the queens is eliminated in the bargain. affin or beeswax. This is a good finish that protects
the wood from all sides and ends, but requires
working around hot, flammable paraffin. Once the
Building Equipment equipment has begun to show signs of wear, sim-
ply dip it again in hot paraffin to recoat the finish
Although it can rarely be built more cheaply than and to remove wax and propolis residue. In recent
it can be purchased, only basic woodworking skills years, polyurethane exterior stains have become
and tools are needed to build wooden beekeeping popular and have been consistently improved. As
equipment. Box joints are currently the most com- with paraffin impregnation, many of these stains
mon, and according to some, the strongest kind to are water repellent, resist mildew and fading, and
use in beekeeping applications. Producing them clean up with water and soap.
requires a jig, usually home made, to neatly and A final warning concerns pressure-treated
precisely cut the slots to line up with the fingers. wood. The materials used to preserve the wood
Butt joints are more forgiving; two boards are are usually toxic to honey bees. Thus, treated wood
butted together and simply nailed. The TIM joint is not recommended for bee colonies. Even the
is fast but weak. If a colony is not going to be sawdust is considered a health hazard and dust
moved, it will probably work okay. The dado joint, masks are recommended when working so-called
used by some manufacturers, is becoming more Wolmanized treated wood.
popular, and is strong enough to withstand the
rigors of moving and manipulation. When build-
ing equipment, in all instances, respect bee space Wearing Protective Equipment
requirements and be sure to build your equipment
to fit standard measurements. The most important protective equipment is the
veil, which protects the face, the most sought-after
target for guard bees. Veils can be used without a
Protecting Wooden Equipment helmet, or attached to a pith-type helmet, made of
plastic or other material. Almost any hat that keeps
Some wood may last longer while some may the veil material off the face and neck will work.
last much less time, depending on the climate, Veils usually have a mesh bottom that is snugged
but hives are definitely helped by some type of down over the collar onto the shoulders with a
220
A Apiculture (Beekeeping)

variety of ties and/or strings. Veils that attach to successfully. There is no better piece of advice for
the bee suit with a zipper are popular, mostly the novice beekeeper than to begin small and only
because they are convenient, easily maintained, expand as experience is gained. A vital ingredient
and virtually bee proof. They are also more of this experience is permanent, detailed record
expensive. keeping and knowing intimately the characteris-
Bee suits usually are light in color, but many tics of the honey bee ecotype one is working with.
wear whats available, simply to keep their clothes One must also master the basics of opening and
clean. The white coverall suit is most popular, with inspecting a colony with the aid of smoke, yet not
a variety of pockets, cuffs and attachments. White destroying its cohesiveness.
is also the most difficult to keep clean. They are Beekeeping knowledge comes about slowly
made from a variety of materials cotton, cotton and being able to implement it effectively often
blends and synthetics each with its own peculiar takes far longer than expected. In order to appre-
attributes. Suits should be roomy, to allow bend- ciate the techniques of beekeeping, one must first
ing and stretching and lifting room, and for other gain an understanding of the dynamics of the
clothes underneath. This also keeps the suit from colony during the year. A recommended exercise
stretching tautly over the skin underneath, which for the beginning beekeeper is to construct a bee-
bees can then easily sting through. keeping calendar. Regional characteristics of
Seasoned beekeepers seldom wear gloves beekeeping are easily identified through the use
because they feel they lose that delicate touch of the calendar, which shows average dates of
when manipulating colonies. However, many bloom, colony population characteristics and bee
beginners start with them. Most gloves have cloth manipulations. Such a timetable also can be bro-
gauntlets of some type to seal the sleeves of the bee ken down into a number of beekeeping activities,
suit. Glove materials range from full leather to each requiring certain decisions. These include
plastic to split leather to rubber. Some are venti- inspecting a colony in spring, feeding pollen and
lated, while others have no fingers. Wearing gloves sugar, monitoring population buildup, controlling
can help build confidence in manipulating bees. swarming, supering, monitoring and removing
As one gains experience, the finger tips can be cut the honey crop, requeening, preparing for winter
off, which still protects most of the hand, while and migrating in search of better nectar resources
ensuring a more sensitive manipulation. or to move bees into commercial plantings for
Boots and pants-cuff clasps range from high pollination.
top rubber boots to baling twine. The goal is to No year is ever the same, so the beekeeper
keep bees on the ground from crawling up pants must learn to think like a bee colony, closely
legs an unnerving experience. Comfort, durabil- watching environmental changes and anticipating
ity, safety and cost are all important. All equip- the potential effects on colonies. Major manage-
ment should fit the job. A hobbyist with a few ment problems in beekeeping are controlling
colonies will use, and need, different equipment swarming (the reproductive process of a colony),
than a commercial pollinator. requeening and managing diseases and pests.
Swarming has befuddled even experienced bee-
keepers. Requeening and queen introduction
Management techniques have been written about for many
years, but still confound beekeepers on occasion.
The meat and potatoes of beekeeping is manage- Several options often need to be considered for
ment. It is often the best manager who makes the successful introduction of new queens, the life
most honey from his/her bee colonies. Experience blood of any beekeeping operation. Finally, the
is extremely important if one is to manage bees challenges of diseases (American and European
 Apiculture (Beekeeping)
A 221

foulbrood) and exotic pests (mites, beetles) are with some races of bees). Southeast is the most
complex, requiring an understanding of many common, and probably works best.
possible treatment regimes under the rubric of Bee colonies must be protected from all man-
Integrated Pest Management (IPM). ner of pests and predators, including humans.
Although controversial, most beginners are Bear (electric fencing), skunks and possum (fenc-
advised to begin by managing two colonies. The ing), cattle and horses (regular fences, though
reasons for this are several. If a hive begins to fail, stout), and neighbor prying eyes (screening,
there are resources in the other the beekeeper can hedges) must all be considered. For large bee
use to help the weaker one along. If one colony is yards, an out-building that works as a storage shed,
lost entirely, the novice beekeeper may easily lose work area, extracting room (sometimes) and lunch
interest if another colony is not present to take room is needed. Most of all, a bee yard should be a
itsplace. pleasant place to visit. Scenic, quiet, distant and,
most importantly, not a challenge to use.

A Model Bee Yard

Inspecting Honey Bees
Somewhere the perfect bee yard exists, but if so, it
is not the general rule. Most are the result of a bee- The productivity of honey bee colonies should be
keepers style that fits both location and manage- actively monitored by the beekeeper, whose job it
ment philosophy. Bee yards should be is to recognize certain conditions and help a col-
right-up-next-to-the-hives easy to get to all year ony overcome those causing adversity. Generally,
long. Newly plowed fields, suddenly erected fences, inspection will determine the state of the colony in
rising creeks, muddy roads, locked gates and the terms of reproductive ability (queen condition;
like should be anticipated, and avoided. population of worker bees), nutritional resources
The most accessible location is worthless (honey and pollen stored in the comb) and whether
without something for the bees to forage on. There diseases or pests are present.
should be enough blooms to produce surplus The latter is increasingly important as exotic
honey for every colony in the apiary. Field crops, organisms continue to proliferate around the
hay crops, tree canopies, weed species, horticul- globe. Of special significance at the present are
tural or oil crops all can work. But there needs to two introduced mites, the internal Acarapis woodi
be large areas of blossoms blooming a relatively and external Varroa destructor. These mites have
long time. Water is required all season long, too. A caused beekeepers to take a closer look at and
lake, stream or pond is best. Swimming pools, cat- often use chemical controls inside the living bee-
tle troughs or leaky faucets cause potential neigh- hive with the concomitant risks that these sub-
bor problems and should be avoided as bee stances may harm the colony and/or contaminate
watering possibilities. its products. As a consequence, honey bees have
A wind break, especially during the colder become much more domesticated, as they are
months in temperate latitudes, is recommended. increasingly reliant on beekeepers in many areas
A tree line, fence or hill works best. Air drainage is of the world to help control exotic bee mites.
important. Cold air drains downhill; colonies at Other diseases that affect colonies are caused by
the bottom of a hill get dumped on in cold bacteria, fungi, viruses and protozoans. Of par-
weather. Hill tops, too, suffer winds and wind chill ticular significance are two bacterial conditions,
problems. Avoid both. Exposure seems important American foulbrood (Paenibacillus larvae
to some. Colonies receiving morning sun start to subspecies larvae) and European foulbrood
forage earlier than those in the shade (at least (Melissococcus pluton).
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American foulbrood, in particular, is caused and/or stinging. The belief that all honey bees
by a spore-forming organism that can resist harsh must behave or act similarly no matter the condi-
ecological conditions. Epidemics of this disease tions is the root of many beekeeping controversies
are the reason state bee inspection services exist, over the last two centuries, and the reason many
although many of these have been discontinued lay persons fail to understand the complexities of
recently due to budgetary constraints and lack of these stinging insects. Usually, beekeeping argu-
support. Discovery of sulfa drugs and later antibi- ments pertain to whether or not a certain man-
otics has caused a shift in beekeepers perceptions agement technique or a special kind of beekeeping
concerning the disease, which they have actively apparatus is practical or efficient. The kind of bee
kept at bay for decades. Unfortunately, the recent a beekeeper has in his apiaries often will determine
appearance of antibiotic-resistant strains of Paeni- whether some concept or idea works or doesnt
bacillus larvae subspecies larvae is causing second work. All too often, however, the bees genetics are
thoughts by many beekeepers concerning official ignored when contemplating solutions to many of
inspection backed up by apiary legislation. the mysteries of beekeeping.
An important adult disease is known as Unfortunately, most beekeepers really do not
nosema and is caused by the protozoan Nosem know what kind of bee they are using. Thats because
apis. This is probably present in every colony of present bee stock is literally a melting pot of honey
honey bees, but only becomes epidemic when bees bee genes. The predominant races (subspecies or
are put under stress. It may be far more important ecotypes) of bees which make up the honey bee
in determining bee colony health than is generally genetic mix found in the United States are: Italian
given credit. (Apis mellifera ligustica), Caucasian (Apis mellifera
There continue to be numerous so-called caucasica), Carniolan (Apis mellifera carnica) and
exotic organisms that impact colonies of honey German (Apis mellifera mellifera), the dark bee. Each
bees around the world. Ironically, two of these are population evolved under certain ecological condi-
ecotypes of honey bees themselves: the African- tions and natural selection over a long period of time
ized honey bee (Apis mellifera scutellata) and the that have provided them with their own particular
thelytokus Cape of Good Hope bee (Apis mellifera survival techniques. These ecotypes are thoroughly
capensis). In addition, various mites are found on intermixed and are extremely difficult to separate in
Asian honey bees (Apis cerana, Apis dorsata, Apis novel environments. In addition, other genes of other
laboriosa) that conceivably could transfer to Apis ecotypes also are present in small quantities.
mellifera as Varroa destructor did previously. No Because there is such great variability, how-
better example of this constant threat is the sur- ever, the possibility of quantum leaps in honey bee
prise introduction of the South African small hive selection programs is possible. With the coming of
beetle (Aethina tumida) into the United States in the mite Varroa destructor, however, the honey
the late 1990s. bees genetic base has narrowed in many parts of
the world. But fortunately there remain pockets of
bees that appear to be resistant (tolerant) and these
Honey Bee Ecotypes may provide the foundation for rebuilding a honey
bee stock devastated by this parasite.
All honey bees are not the same. This statement, it
seems, cannot be said too often around beekeep-
ers and/or the general public. There are those who Africanized Bees
manage bees exactly the same whether or not their
stocks have been selected for overwintering, One of the biggest biological stories of the Americas
swarming, rapid brood rearing, pollen collecting concerns honey bees. Introduction of the African
 Apiculture (Beekeeping)
A 223

honey bee ecotype (Apis mellifera scutellata) has other insects, brood, the queen, drones every-
been responsible for raising the public conscious- thing in the hive has an odor cue. As complicated
ness about these insects. This bee is nothing more as the bees odor communication system appears
than an ecotype adapted to tropical conditions, to be, the manner that beekeepers have developed
generally characterized by higher rates of defensive to overcome the bees ability to perceive odors,
behavior and reproduction. Unfortunately, its fear- both inside and outside the hive, is relatively
some reputation is an outgrowth ofsensationalized simple, and that is to puff cool, white smoke in
press coverage of stinging incidents by these and around the hive. For reasons not clearly
so-called killer bees, which caused deaths of ani- understood, smoke stimulates bees to move to
mals and people in Latin America. As a result many honey stores and engorge, which reduces their
people now view honey bees as aggressive rather propensity to sting.
than defensive, and think them responsible for a Early smokers were little more than a smol-
good many human fatalities. The reality is that the dering fire beneath or near a hive. Later, tobacco
number of verified deaths by honey bees is much pipes were modified to direct smoke into hives as
smaller than reported (almost all stinging insects were other devices. After evolving through many
are routinely called bees). This over-sensationalized different designs and styles, beekeepers in North
topic has affected beekeepers in several ways, most America have a small, but adequate range of
notably by loss of access to beekeeping locations. smoker designs from which to choose.
North America is the last frontier for the African- Smoker fuels are as numerous as are the bee-
ized (or African) honey bee and its final distribu- keepers who use them. Common types include
tion is still unknown. Nevertheless, the challenge grass clippings, pine straw, sumac pods, cloth rags,
for many beekeepers in the future will be to strike rotted wood, wood shavings, and burlap. Essen-
a balance in their communication with the public tially, anything can be used that produces cool,
about the risks/benefits of their bees. Beekeepers white billowing smoke and has not been treated
also will have to adapt to this ecotypes different with pesticides, fire retardants or other noxious
behavior, which often can be a radical departure chemicals. Under normal conditions, smoke is
from the European ecotypes previously present. effective for about 2 to 4 minutes before needing
A special ecotype inhabits Africa known as to be reapplied.
Apis mellifera capensis. This bee is characterized
by a high degree of thelytoky, which means work-
ers can become laying queens, producing diploid Moving Bees
females, in spite of laying unfertilized eggs. This
ecotype has created a crisis of sorts in African bee- Bees can be moved almost any way imaginable.
keeping. It is hoped that this honey bee will not be Some, of course, are easier and safer than others.
moved out of its homeland by beekeepers and Commercial operations need the economy of size
introduced to the rest of the world. The history of and efficiency. A large, flatbed truck serves that
honey bee introductions around the world over purpose. Some come with a flatbed trailer that
the last two centuries, however, is not a good omen attaches to the truck to increase efficiency. These
in this regard. trucks usually have customized tie-downs, tool
boxes and equipment storage areas. Getting the
bees on and off the truck can be done by hand
Smoking Bees (muscle) or machine.
Regular two-wheeled carts, sized to hold
Within and outside the dark hive, bees communi- hives, often are used for moving. Motorized carts
cate extensively by smell. Nectar, pollen, diseases, are common, as are booms and Tommy-lifts. Fastest
224
A Apiculture (Beekeeping)

are fork-lifts. There are several models available, in a day or so. Once installed, several precautions
from the standard, to large, specially designed are recommended. The first rule is: feed, feed, feed.
models for specific bee pallets. Some have cabs, Then feed more, until they dont take any more.
most have protective cages and large tires to navi- Feeding well into the summer may be required if
gate easily in muddy conditions. Some can swivel adequate forage is not available.
or pivot in the center. Checking for queen acceptance, and then
Once loaded on the truck bed (many are built queen production is a must, but there is a fine line
to hold an exact number of pallets), tie-downs can between too-often and too-seldom observations. It
be regular rope, self-tightening straps, or wide is safer to edge toward the too-often, but just barely.
canvas belts affixed to wooden frames that are Once established, remove feeders, add supers and
used for extra security. A secure net is required at prepare for the honey flow and harvest.
all times to avoid escaped bees on the road. Any-
time bees are moved, the boxes should be fastened,
entrances closed, the load netted and tied down to Dividing Colonies
prevent shifting.
An important consideration in moving bees is Splitting a colony is the easiest and least expensive
temperature. Traditionally this has been managed way to increase the number of hives managed. But
by periodically spraying the load of bees with fresh there are other reasons to split a colony, and there
water when signs of overheating are evident. are nearly as many ways to split one as there are
colonies to split.
The overall principle in making a split is to
Package Bees start with a large, healthy, populous colony (or
colonies). The goal is to remove some uncapped
The most common way to start a colony, or start brood, some honey and pollen resources to a new
beekeeping, is to install a package of bees into an box, or two, to start a new colony. A new queen
empty home-to-be by removing them from the may, or may not be, added. Usually the parent col-
shipping cage. Packages generally come in three- ony should not be reduced to less than half its
to five-pound sizes (3,500 bees equal a pound). resources so it can continue to keep pace with the
And there are nearly as many ways to get bees season. Bees, brood or food may be taken from
from the shipping cage to the functioning unit as more than one parent to successfully build a new
there are people doing the task. But basic biology split. Splits must have enough nurse bees to care
dictates certain principles be obeyed. A starter for the brood, some foragers to gather resources,
box with some or all drawn comb is better than sealed brood for immediate colony expansion,
just frames with foundation, as it gives the bees younger brood for continued expansion and some
some place to be, and store food immediately, and resources for immediate consumption.
reduces the amount of gathered food required for Splits are used to make increase, or for other
wax production, freeing it for brood food. reasons. Popular swarm control/prevention mea-
Bees can be moved in by dumping them sures include splitting a large colony to allow room
(they are often sprayed with water first to inhibit for expansion, and to relieve brood-nest congestion.
flying) inside the box (with three frames removed, Often the new colony is rejoined to the parent when
then replaced, to accommodate the resultant the swarming urge is over so the actual number of
mass); they also can be dumped directly in front, colonies does not increase. One technique used to
to march right in; or a combination of the above reduce mite infestation is to divide a colony later in
two techniques, where some are placed inside, the the season, eliminating the older, infested bees, and
remainder outside. The empty package is removed overwintering the younger, less infested bees.
 Apiculture (Beekeeping)
A 225

Feeding Colonies with wax. When the supers are filled, they are
removed and the honey is extracted from the comb
Providing food to colonies is one of the most time- using centrifugal force in special machinery
consuming and tedious tasks facing any beekeeper. (extractors). Sometimes honey is sold in the comb
Two types of food are required: carbohydrate and (known as section or comb and cut-comb).
protein. Generally, carbohydrates are provided by
nectar in nature and the best analogy to this is
sugar syrup, made up by dissolving cane sugar in Extracting the Honey Crop
water. This is then provided through various hive
modifications or feeders, some of which are men- A large honey crop is clearly a mixed blessing. The
tioned elsewhere in this article. more supers that go on, the more honey to be pro-
A relatively new bee food is high fructose corn cessed. More honey means more work, but it also
syrup (HFCS) that is manufactured in huge means more money. For years, clever people have
amounts to service the soft drink and candy trade. tried to develop equipment to make the uncap-
Two types exist: 42 and 55. The 55 is generally con- ping, extracting, pumping, filtering, and bottling
sidered more acceptable to bees because it has procedure more convenient, even easy. Though
more sugar solids. Many beekeepers consider feed- easy extracting has not yet been achieved, the
ing both sugar syrup and HFCS, depending on hive process has become much more streamlined. Old
condition. Sugar syrup high in sucrose is consid- processing equipment was made from galvanized
ered superior for colony population build up, while tin with lead solder joints. It was solid equipment
HFCS is used strictly to maintain populations. that was built to stand years of heavy use. The
Most suggested feeding regimens concentrate clutch-drive mechanism was simple, heavy-duty,
on providing carbohydrate. However, it must be and a bit dangerous. Belts, drives, shafts, and pul-
complemented with protein for a balanced diet. This leys were all exposed. In fact, a few early extractors
is provided by pollen to the honey bee in nature. The were powered by low compression gasoline
beekeeper, too, can trap and give back pollen or engines. Extracting was done outside on occasion,
combine it with soy flour and/or yeast (supplement). a practice that generally has been abandoned.
Protein supplement often is sold ready-made in Stainless steel with welded joints is now used
patties by beekeeping supply outlets. on extractors. Other metals may impart an objec-
tionable odor. Smaller hobby-type extractors may
use plastic barrels. In many instances, variable-
Producing the Honey Crop speed direct-current (DC) drive motors are used
that allow for the gentle extraction of full combs of
The beekeeper seeks to have as large a population honey. The equipment is mechanically simpler, but
of worker honey bees as possible coincidentally technologically more complicated. Its lighter and
when the most nectar-producing flowers are more maintenance free. Most commercial honey
blooming. This nectar is stored above a bee colony processing lines would be ordered as follows:
in the wild. Thus, beekeepers emulate this by add-
ing extra boxes on top of hives (supers) into which 1. uncapper
bees place the nectar. Nectar is modified by the 2. extractor(s)
bees into honey. The insects add enzymes, chang- 3. heated sump
ing the material chemically, and reducing the 4. honey pump
moisture content from 80% (nectar) to about 5. filter
18.6% (honey). The bees determine when the 6. settling tank
moisture is correct and then cap over the honey 7. bottler
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A Apiculture (Beekeeping)

Other equipment in honey processing can include and transported, a beekeeper can do many things
a barrel melter, a flash heater, wax spinner and with this bunch of bees. The deciding factor is
other equipment-moving devices. A second line often the size of a swarm. Large swarms, about
would drain honey from wax cappings to the four or five pounds of bees (3,500 bees equal one
sump. Dried cappings would be melted into bees- pound), can easily survive by themselves. Smaller
wax, which could be returned to the bees as swarms of one to three pounds can be combined
foundation. with other swarms to start a large colony; or added
to another colony to boost its nectar- and pollen-
gathering capability during a major flow.
Managing Swarming To be safe, all swarms should be considered
infested with mites and treated accordingly. As the
Swarms can be both reproductive and migratory. queen heading the swarm is from essentially
Little can be done about swarming once the unknown heritage, replacing her with a young one
impulse is generated in a colony. The best ways of known parentage should be considered.
to control swarming are providing room in the With the advent of the tropically adapted
colony and/or regularly requeening with younger Africanized (Apis mellifera scutellata) honey bee,
individuals. This is a preventive strategy that is another kind of swarming is increasingly seen.
much more effective. As stated earlier, once the This is the migratory swarm, thought to be brought
impulse to swarm gets going, it is almost impossi- on by stress such as lack of forage or water. This
ble to stop. Generally swarms are reproductive in kind of swarm often behaves differently than the
nature, especially with European honey bees, and reproductive one and may be much more defen-
can be both a blessing and a curse. The blessing sive, though not always so.
part is that one can be harvested and put to work
in an apiary. A secondary blessing, obviously, is
that a swarm happens. That means a colony is Managing and Rearing Queens
healthy enough to swarm, something all too rare
in these days of increasing stress on managed The queen is the key to managing the genetic com-
honey bees. ponent of a colony. She contributes one half of all
The first thing to do with a swarm is collect it. the genes found in a colony, whereas a single drone
At times this is easy, sometimes impossible. provides for less than half (queens mate with 17 to
Swarms high in the air can be collected with vac- 20 drones during a short period in their life just
uum devices, long ladders, or heroic gymnastics. after emerging from the cell). The colonys charac-
Most can be collected into bags, boxes, supers or teristics, therefore, have a good chance of being
whatever and transported to permanent housing. perpetuated in the queen and research has shown
The key is to provide ventilation; putting a strong that queen selection followed by open mating will
swarm into an air-tight container is a recipe for ensure a good deal of progress in breeding bees
disaster! Swarms are generally the gentlest of bees, with specific traits.
but if left exposed for several days, they can Queen rearing is one of the most demanding
become hungry and much more defensive. Always beekeeping activities, and more often than not is a
have a lighted smoker at the ready when working true art form. Anybody can produce a queen, but
swarms. rearing a quality queen with the correct genetic
The public relations aspect of swarm gather- complement for a beekeeping operation is far
ing should not be overlooked. But the macho more difficult. Queen rearing also is directly tied
image many beekeepers display while on the job to a timetable, which must be rigidly followed.
communicate a mixed message. Once collected Often the question is raised whether or not one
 Apiculture (Beekeeping)
A 227

should produce queens him/herself, let the bees An alternative to wintering is to simply
do it, or purchase a queen. There is no easy answer. c ollect all the stores and kill colonies off in winter,
The only reply may be to ask the question, Whose establishing new hives the following spring with
quality control is the best under the circumstances, package bees from more tropical areas. This was
that of nature or of human beings? routinely practiced by Canadian beekeepers who
Again, the queen honey bee usually mates simply purchased bees from the southern US
with many drones. This ensures large genetic vari- until the border was closed in the early 1980s
ability, but also means a lack of controlled breed- due to introduction of tracheal and then Varroa
ing. It is possible to instrumentally inseminate mites. To many beekeepers this was a repugnant
queen honey bees in an attempt to control genetics practice and they were not sorry to see it aban-
in a population. This is not easy, however, and can doned. Effective wintering continues to be an
only be accomplished by trained workers. Most important part of bee management as more col-
queen rearing facilities produce daughter queens onies are lost during this trying time than other
from selected stock that are open mated (uncon- seasons of the year.
trolled) in a natural setting.

Nectar and Pollen Sources

Managing Wintering
Nectar and pollen are the only natural foods of
The honey bee can live in almost any climatic honey bees, strictly vegetarian insects, and each
environment, but is most stressed by winter in geographic area has different sources of these
continental climates. Honey bees can produce a important foods. Every good beekeeper, therefore,
warm brood nest even in the coldest winters if must be somewhat of a botanist in order to make
supplied with the proper nutrition and number sure the bees are located so they have an adequate
of workers. This leads to the adage that honey food supply. Bee plants may also differ from each
bees never freeze to death, they starve to death. other in several ways, such as the kinds of nectar-
Beekeepers in cold climates, therefore, have a ies (nectar glands) each supports and/or the time
significant challenge to help their colonies over- of day they may secrete nectar and/or produce
come severe conditions of wind and cold. Many pollen.
pack their hives wintered outdoors in various Nectar and pollen production by flowers is
kinds of materials to conserve warmth. Others dependent on a great variety of environmental
move their colonies indoors to protect them. conditions such as soil moisture, pH, profile and
The latter activity was employed by old timers fertility, as well as rainfall distribution, tempera-
who put their colonies into cellars. This was ture and humidity. Over the last four decades,
risky as too much warmth would stimulate a there has been an overall decrease in honey bee
colony to begin to build population, a prescrip- forage in the United States due to many factors,
tion for disaster. With development of refrigera- especially changing agricultural patterns and
tion, however, it now is routine in some areas to increasing urban development. Improving nectar
bring smaller-than-normal hives (nuclei) into production by genetically selecting for varieties
climate-controlled buildings and keep them in a of certain crops that produce large amounts of
kind of human-induced diapause, which reduces nectar, or purposely planting nectar-producing
nutritional requirements to a minimum and con- varieties in so-called waste land, along roadways
serves worker bee energy and vitality so they or on lands reclaimed for mining, are some ways
can begin to rear brood quickly and efficiently suggested to reverse this systematic reduction of
in spring. bee forage.
228
A Apiculture (Beekeeping)

Few plants produce the vast quantities of nec- Commercial pollination is a service, a much
tar the honey bee needs to make a large honey different business than producing a product like
crop. In the state of Florida, for example, less than honey or pollen. As such, it is not suited to all
ten plants are responsible for sizeable honey crops beekeepers and each should look carefully at the
on a consistent basis. Fortunately, in most areas a characteristics of this enterprise before dedicating
number of minor nectar crops usually are found many resources to it.
which help support honey bees throughout the Recently, pollination has received more
year, although they often contribute little to the respect from the general public due to a scarcity of
beekeepers honey crop. It is of more than passing feral or wild honey bees caused by devastating
interest to know that many introduced plants assist effects of exotic bee mites. This represents a teach-
honey bees in a number of ways, and the insects able moment for beekeepers, who can now
may contribute to their proliferation. describe with pride the value of their insect charges
Though not as readily available as honey, to the public at large.
another type of sweet is collected and processed
by honey bees. Aphids and other sucking insects
often take more than they need from the plants. Honey Contrasted to Pollination
The excess is extruded and may be collected by
ants or honey bees. The resultant product is hon- Honey is a world commodity, and is labor inten-
eydew. Some think this might have been the sive to produce. As such, the price of the product
manna that descended from heaven as noted in can always be expected to be influenced by societ-
the Bible (Exodus 16:136). ies with low labor costs. Indeed, beekeeping is
being promoted aggressively as a development
tool in many countries because it is relatively envi-
Commercial Pollination ronmentally friendly and not capital intensive.
Although honey can be imported cheaply in
Honey bees are cosmopolitan pollinators, trans- many instances, a process exacerbated by global-
ferring pollen both within and between flowers. ization of world commerce, pollination services
Although important to many crops (fruits and cannot. In addition, because no food product is
vegetables), honey bees are not the most effective involved, chemical treatment for exotic pests
pollinators in many situations. This has led to (mites) can be applied in a more forgiving way to
some proclaiming that other bees should be used colonies used strictly for pollination. This means
in preference, such as bumblebees (Bombus sp.) that in the future there will always be a demand
and/or blue orchard bees (Osmia sp.). However, for pollination no matter the price of honey.
honey bees have significant advantages including Because commercial pollination seems more
very large populations that are easily moved, and a assured in the future, beekeepers should contin-
well-known rearing technology. ually carefully consider this activity in their
There is no stable pollination service in the enterprise mix.
United States of the kind described by S.E. MacGregor
in his classic volume on insect pollination. This means
that pollination is carried out by a number of inde- Conclusion
pendent contractors. More recently, pollination bro-
kers in the western United States have become more The future of beekeeping or apiculture continues
common. The vast majority of commercial pollina- tobe mixed. On one hand, the honey bee will be more
tion takes place in California on the almond crop. Lit- and more important as growers and the general public
erally hundreds of thousands of colonies are needed. continue to realize how necessary this insect is for
 Apivorous
A 229

producing a quality food supply through pollination. Agricultural Research Service. Online version accessed
June 17, 2002; http://bee.airoot.com/beeculture/book/
Because honey is a world commodity, italso is con-
index.html
tinually under price pressures in developed countries, Caron D (1999) Honey bee biology and beekeeping. Wicwas
as it represents a good source of income for countries Press, Cheshire, CT 363 pp
with a labor-intensive work force. Its reputation is also Caron D (2001) The Africanized honey bee in the Americas.
A.I. Root Co., Medina, OH
at risk, however, given the chemicals needed to keep Graham JM (ed) (1992) The hive and the honey bee. Dadant
(treated) bee colonies alive and the potential they and Sons, Hamilton, IL
have to damage the sweets reputation through con- Hooper T (ed) (1976) Guide to bees and honey. Rodale Press,
tamination. Whether or not honey and/or pollination Emmaus, Pennsylvania
Morse, Roger A (1972) The complete guide to beekeeping. E.P.
are primary, there also are other reasons to keep bees, Dutton, Inc., New York, NY
including using their products, both manufactured Morse, Roger A, Flottum K (eds) (1990) ABC and XYZ of bee
(royal jelly, honey, beeswax, venom) and collected culture. A.I. Root Co., Medina, OH
Morse, Roger A, Nowogrodzki R (1990) Honey bee pests,
(pollen, propolis), for the benefit of humanity, as well
predators, and diseases. Cornell University Press, Ithaca,
as for the general joy of communing with nature and NY
one of its fascinating social organisms. Sammataro D, Avitable A (1998) The beekeepers handbook.
The history of beekeeping activities is long, and Cornell University Press, Ithaca, NY
Taylor R (1984) The how-to-do-it book of beekeeping. Linden
it takes time and experience to become a proficient Books, Interlaken, NY
manager of honey bee colonies. This article can Webster TC, Delaplane K (2001) Mites of the honey bee.
provide only some of the basic information onthe Dadant and Sons, Hamilton, Illinois
craft. The authors hope that it will serve asacatalyst
for those thinking of taking up the activity, and also
a source of basic information for anyone interested Apidae
in one of humankinds most fascinating activities.
Honey Bee A family of bees (order Hymenoptera, superfamily
Bees Apoidae). They commonly are called bumble bees,
African Bee honey bees, and orchid bees.
Cape Honey Bee Bees
Varroa Mite Honey Bee
Small Hive Beetle Wasps, Ants, Bees and Sawflies
Bee Louse
Pollination by Osmia Bees
Polination and FlowerVisitation Apioceridae

References A family of flies (order Diptera). They commonly

are known as flower-loving flies.
Bee Culture, A. I. Root Co., Medina, Ohio, accessed June 7, 2002;
Flies
http://bee.airoot.com/beeculture/Electronic
American Bee Journal, Dadant and Sons, Hamilton, Illinois,
accessed June 7, 2002; http://www.dadant.com/.
Sanford MT. Beekeeping in the Digital Age, Bee Culture, accessed
Apivorous
June 7, 2002; http://bee.airoot.com/beeculture/digital/
Whos Who in Apiculture, Bee Culture, accessed June 7, 2002; Bee eating. Birds, and some predatory insects
http://bee.airoot.com/beeculture/who/who_2002.htm such as robber flies (Diptera: Asilidae) kill and
Online Source Book for Beekeeping, accessed June 7, 2002:
consume honey bees or, in the case of blister
http://www.beesource.com/suppliers/index.htm
McGregor SE (1976) Insect pollination of cultivated crop beetles (Coleoptera: Meloidae), ground nesting
plants. Agriculture Handbook 496, published by the bees.
230
A Apneumone

Apneumone provisioned by the parent. It occurs in ants, bees,

and wasps (Hymenoptera).
A chemical released by a nonliving substance
that is beneficial to the receiver. An apneumone is
a type of semiochemical. Apoid Wasps (Hymenoptera:
Chemical Ecology Apoidea: Spheciformes)
Semiochemicals
kevin m. oneill
Montana State University, Bozeman, MT, USA
Apodal
Apoid wasps are a morphologically, behaviorally,
The condition of lacking feet (tarsi). Fly larvae and and ecologically diverse group of insects that are
some beetle larvae, for example, have simple tubercles common in many habitats. Apoid wasps are most
that aid in movement, but lack legs, including tarsi. closely related to bees, and are placed with them in
the superfamily Apoidea, one of three superfami-
lies of the so-called stinging Hymenoptera or
Apodeme Aculeata; the other two subfamilies are
Chrysidoidea and Vespoidea (Table7).
A thickened section of the exoskeleton that The subfamily Apoidea is subdivided into the
serves as a point for muscle attachment. On the series Apiformes and Spheciformes, the latter of
external surface, it usually is marked as a suture which are the apoid wasps. Thus, the term apoid
or fold, but internally there may be a significant wasps refers to all members of the superfamily
invagination. Apoidea that are not bees. Of the four families
making up the Spheciformes (Heterogynaeidae,
Ampulicidae, Sphecidae, Crabronidae), all but the
Apodous Larva Heterogynaeidae were formerly placed in the sin-
gle family Sphecidae (sensu lato) in the superfamily
A larval body form that is legless, robust, and Sphecoidea. But recent consensus splits the old
C-shaped or spindle-shaped. The head may be well Sphecidae into the Ampulicidae, Sphecidae (sensu
developed, or not. Apodous larval types include stricto), and Crabronidae. The correspondence in
curculionoid, muscoid, and apoid. taxonomic names between this recent family-level
classification and what we might call the classical
system represented in Sphecid Wasps of the World
Apoidae by Richard Bohart and Arnold Menke is given
in the following table. The reason for the recent
A superfamily in the order Hymenoptera known taxonomic reworking is sound. The old Spheci-
as bees. It consists of several families. dae and Sphecoidea were artificial groupings
Bees evolutionarily, because the wasps in what we now
Wasps, Ants, Bees and Sawflies call the Crabronidae are actually more closely
related to bees than they are to the Ampulicidae or
the new Sphecidae.
Apoid Larva The Apoidea, as a whole, likely has its origins
in the early Cretaceous, and it is the wasps that
A larval body form that is robust, with a well- predate the bees. Species of over two dozen extinct
developed head, and cared for by nestmates or apoid wasp genera, including members of the
 Apoid Wasps (Hymenoptera: Apoidea: Spheciformes)
A 231

Apoid Wasps (Hymenoptera: Apoidea: Spheciformes), Table 7 Superfamilies of aculeate wasps

(classification of the Apoidea is after The bees of the world by Charles Michener)
Superfamily Series Families Included groups
Chrysidoidea multiple families cuckoo wasps, bethylid wasps,
and others
Vespoidea multiple families ants, social wasps, spider
wasps, velvet ants, and others
Apoidea Apiformes seven families bees
Spheciformes Heterogynaeidae apoid wasps
Ampulicidae
Sphecidae
Crabronidae

Ampulicidae, Sphecidae, Crabronidae, and the (though this may not have been their original
extinct family Angarosphecidae, have been found function).
in Cretaceous deposits. Over 9,500 described extant As a group, apoid wasps vary widely in habits
species of apoid wasps are unequally distributed and body size, form, and color. Most species are
among the four families and over 250 genera. Bees, sexually dimorphic to a greater or lesser extent,
in contrast, are divided among seven families, 425 females having almost universally larger body
genera, over 16,000 described species, and perhaps sizes and stouter mandibles. Also, only females
30,000 species overall (Table8). have stings. Females of ground-nesting species
As a group, apoid wasps share a number of also commonly bear two features not found in
traits that unite them with bees in a discrete evolu- either males or in females of species that nest in
tionary lineage: (i) a gap present between tegula other locations. The first feature is conspicuous
(at the base of the wings) and the apex of the pos- rows of rake spines on their foretibia that aid in
terior edge of the pronotum; (ii) a broadly digging in soil. The second feature is flattened
U-shaped pronotum when viewed dorsally; and pygidial plates that aid in tamping soil in place
(iii) the propodeal triangle on the dorsal poste- during nest construction. Males of some species
rior of the abdomen. A dozen or so shared traits exhibit peculiar anatomical structures used in
link bees in a single clade within the Apoidea. For courtship and mate competition. Examples include
example, bees feed pollen and nectar to their the clypeal and abdominal hair brushes that male
young, and continue to eat both pollen and nectar beewolves (Philanthus) use to disseminate sex
as adults. In contrast, with perhaps one exception, pheromones, and the expanded translucent fore-
all apoid wasps either feed their young arthropod tarsal plates of male Crabro that sport species-
prey or are brood parasites in the nests of other specific color patterns and which are apparently
carnivorous wasps; the single exception is the placed over females eyes during courtship.
genus Krombeinictus (Crabronidae) from India
whose females provision with pollen and nectar.
Adult wasps feed on nectar, sap, or honeydew, and Heterogynaeidae
some consume body fluids of prey. Another
marked difference between apoid wasps and many While the Heterogynaeidae are clearly apoid wasps,
bees is that body hairs are simple in the former, their exact relationship to the other three families is
but often branched or even plumose in the latter, somewhat controversial. Heterogynaeids are small
where they function to trap and carry pollen wasps, 1.55.0 mm in length, that are restricted in
232
A Apoid Wasps (Hymenoptera: Apoidea: Spheciformes)

Apoid Wasps (Hymenoptera: Apoidea: Spheciformes), Table 8 Correspondence of taxa names under the
classical (Bohart and Menke 1976) and revised (Pulawski 2007) systems of classification of the apoid wasps.
Note a few minor taxa have been left out of the table
Classical Revised taxonomy Number of Some important Nest Host/prey
taxonomy extant gen- genera (number of typeb ordersc
era/speciesa described
speciesa)
not included Heterogynaeidae 1/8 Heterogyna (8) Unknown
Sphecidae: Ampulicidae 6/198 Ampulex (131) C Bla
Ampulicinae Dolichurus (48) C Bla
Sphecidae: Sphecidae 19/731 Ammophila (201) S Lep
Sphecinae Chalybion (45) C Ara
Chlorion (20) S, Pa Ort
Isodontia (61) C Ort
Palmodes (20) S Ort
Podalonia (66) S Lep
Podium (23) C Blat
Prionyx (59) S Ort
Sceliphron (35) M Ara
Sphex (118) S Ort
Sphecidae: Crabronidae: 37/1021 Arpactophilus (43) C Hom
Pemphredoninae Pemphredoninae Diodontus (73) C Hom
Microstigmus (29) Ps Clm, Thy
Mimesa (71) S Hom
Passaloecus (35) C, P Hom
Pemphredon (43) C, P Hom
Pluto (58) S Hom
Polemistus (36) C Hom
Psen (92) R Hom
Psenulus (159) C Hom
Spilomena (86) C, P, R Hom, Thy
Sphecidae: Crabronidae: 4/151 Astata (80) S Hem
Astatinae (part) Astatinae
Diplopectron (20) S Hem
Dryudella (52) S Hem
Sphecidae: Crabronidae: 1/12 Dinetus (12) S Hem
Astatinae (part) Dinetinae
Sphecidae: Larrinae Crabronidae: 38/2686 Gastrosericeus (61) S Ort
Larrinae
Larra (63) Pa Ort
 Apoid Wasps (Hymenoptera: Apoidea: Spheciformes)
A 233

Apoid Wasps (Hymenoptera: Apoidea: Spheciformes), Table 8 Correspondence of taxa names under the
classical (Bohart and Menke 1976) and revised (Pulawski 2007) systems of classification of the apoid wasps.
Note a few minor taxa have been left out of the table (Continued)
Classical Revised taxonomy Number of Some important Nest Host/prey
taxonomy extant gen- genera (number of typeb ordersc
era/speciesa described
speciesa)
Liris (350) C, S Ort
Miscophus (183) S Ara
Nitela (60) C Pso, Hom
Palarus (34) S Hym
Pison (196) C, M Ara
Plenoculus (20) S Hem, Lep
Sericophorus (69) S Dip
Solierella (111) C Ort, Pso, Hem
Tachysphex (391) S Ort
Tachytes (294) S Ort, Lep
Trypoxylon (629) M Ara
Sphecidae: Crabronidae: 56/1886 Belomicrus (109) S Hem
Crabroninae Crabroninae Crabro (88) S Dip
Crossocerus (236) C, P, S Eph, Pso, Hom,
Mec, Tri, Lep, Dip
Ectemnius (184) P, R, S Dip
Entomognathus (63) S Col
Lindenius (60) S Dip
Oxybelus (262) S Dip
Podagritus (116) S Col
Rhopalum (277) P, S Hom
Sphecidae: Crabronidae: 84/1708 Alysson (42) S Hom
Nyssoninae Bembicinaeb Argogorytes (31) S Hom
Bembecinus (187) S Hom
Bembix (346) S Odo, Neu, Lep,
Dip, Hym
Bicyrtes (27) S Hem
Clitemnestra (67) S Hom
Gorytes (46) S Hom
Harpactus (73) S Hom
Hoplisoides (79) S Hom
Microbembex (34) S Artd
Nysson (102) Bp Apoe
Stictia (28) S Dip
Stizus (120) S Ort, Man
Stizoides (29) Bp Apoe
234
A Apoid Wasps (Hymenoptera: Apoidea: Spheciformes)

Apoid Wasps (Hymenoptera: Apoidea: Spheciformes), Table 8 Correspondence of taxa names under the
classical (Bohart and Menke 1976) and revised (Pulawski 2007) systems of classification of the apoid wasps.
Note a few minor taxa have been left out of the table (Continued)
Classical Revised taxonomy Number of Some important Nest Host/prey
taxonomy extant gen- genera (number of typeb ordersc
era/species described
a

speciesa)
Sphecidae: Crabronidae: 8/1141 Aphilanthops (4) S Hym
Philanthinae Philanthinae Cerceris (868) S Col, Hym
Clypeadon (9) S Hym
Eucerceris (41) S Col
Philanthus (137) S Hym
Trachypus (31) S Hym

a
number described species worldwide (see Pulawski 2007); genera included based on genus size and b iological interest
(but certain larger genera for which no biological data are available are left off the list).
b
Bp=brood parasite in nests of other wasps; C=cavity nests; M=mud nests; P=nest excavated in plant stems;
Ps=free-standing nest made of plant material bound with silk; R=nest excavated in rotten wood; S=nest excavated in soil.
c
Apo=apoid wasps; Art=Arthropoda; Ara=Araneae; Bla=Blattodea; Col=Coleoptera; Clm=Collembola;
Dip=Diptera; Eph=Ephemeroptera; Hem=Hemiptera; Hom=Homoptera; Hym=Hymenoptera; Lep=Lepidoptera;
Man=Mantodea; Mec=Mecoptera; Neu=Neuroptera; Odo=Odonata; Ort=Orthoptera; Pso=Psocoptera;
Thy=Thysanoptera; note that each species may prey upon a narrow range of families within each order.
d
females are scavengers of dead arthropods.
e
Nysson and Stizoides are brood parasites whose larvae feed on prey provisioned by other wasp species.

distribution to the eastern Mediterranean region, prey. Venoms of certain species are known to have
southern Africa, and Madagascar. Nothing is known specific pharmacological effects on cockroaches,
about their biology, but there are hints that it may which are somewhat subdued following stinging,
be unique among apoid wasps: females have such but remain active enough that the female wasp can
short wings as to make them flightless and they lead them to the nest cavity, as if walking a tethered
have been observed active at night; based on mor- cow to pasture. Nests of ampulicids may have mul-
phological evidence, it has been inferred that heter- tiple cells separated by partitions made of plant
ogynaeids are parasitoids, though they probably do debris, but are relatively simple compared to nests
not dig in soil. constructed by many Sphecidae and Crabronidae.

Ampulicidae Sphecidae

The Ampulicidae have rather elongate bodies and The wasps in what is now called the Sphecidae are
legs that make them proficient runners; they range sometimes referred to as thread-wasted wasps in
up to 3 cm or so in body size, and may be metallic reference to their narrow cylindrical petioles.
blue or green in color. Though geographically Sphecids often have quite striking body colors,
widespread, ampulicids appear to be relatively con- including the metallic blue (Chlorion aerarium),
sistent in their habits. Females of all species prey on black and yellow (Sceliphron caementarium), and black
cockroaches that are stung into temporary paraly- and orange with either silver (some Ammophila) or
sis, placed singly in existing cavities, and quickly golden hairs (Sphex ichneumoneus). The family
covered with debris after a single egg is laid on each includes some of the largest apoid wasps, including
 Apoid Wasps (Hymenoptera: Apoidea: Spheciformes)
A 235

members of the genera Dynatus, Parasammo- provisioners include solitary, communal, and
phila, and Sphex that can reach as long as 45 cm; eusocial species, the latter two of which will be
sphecids are rarely less than 1 cm long, though this is discussed in the following section. Unlike some
the case for some Ammophila and Prionyx. Sphec- apoid wasps, no vespid wasps or bees are parasit-
ids are more diverse in their nesting habits than are oids, and only the bees include brood parasites.
ampulicids. Some dig nest burrows in soil, others However, apoid wasps have just barely crossed the
nest in existing cavities in wood or construct mud threshold into eusociality, whereas bees and vespid
nests de novo. Certain species of Chlorion, on the wasps contain some of the most highly eusocial
other hand, are parasitoids that construct no nests Hymenoptera.
at all, but simply sting their cricket prey and then Among apoid wasps, parasitoids lay their
place it back in its own burrow. Prey of sphecids eggs singly on a host insect that has been stung by
include three orders of insects, along with spiders; the adult female wasp; no nest is constructed
some take prey that are large relative to their own bythe female parasitoid, though she may return
body size. Palmodes laeviventris (which preys upon the host to its own burrow and cover it with debris.
Mormon crickets, Anabrus simplex), Sphex ichneu- Parasitoids are found in the Ampulicidae, a few
moneus (which takes crickets and katydids), and genera of Crabronidae (Chlorion, Larra), and per-
certain Ammophila (that take large caterpillars) haps the family Heterogynaeidae, though this has
may provision with prey that approach or even yet to be confirmed. Brood parasitic apoid wasps
exceed the adult female in body mass. occur in the crabronid tribe Nyssonini (226 spe-
cies) and genus Stizoides of the Gorytini (29 spe-
cies). Brood parasites enter provisioned nest cells
Crabronidae of other apoid wasps and deposit their own eggs
(one per nest cell); the brood parasite larva then
The Crabronidae, the largest and most diverse of feeds on the hosts stored prey, the host egg having
apoid wasp families, contains 90% of the apoid been already killed either by the adult female par-
wasps. Crabronids range in size from 1.5 mm long asite at the time of oviposition (Stizoides) or the
Spilomena that prey on psyllids and thrips, to 35 mm parasite larva itself (Nyssonini).
long Sphecius speciosus that prey on cicadas, and The vast majority of female apoid wasps are
45 mm long Editha magnifica that take butterflies. solitary nest-provisioners that work without assis-
Even individual genera can exhibit wide size varia- tance from conspecifics to construct a nest and
tion; Philanthus in North America, for example, provision each of its brood cells with one or more
range from the 5 mm long Philanthus parkeri, paralyzed prey. The prey placed in a cell must pro-
predators of tiny andrenid bees, to 25 mm long vide all of the nourishment required by the mag-
Philanthus bicinctus, predators of worker bumble got-like larva (one per nest cell in almost all
bees. As a group, crabronids prey on insects of at species) that remains restricted to its own nest cell
least 17 orders, along with spiders. The reproduc- throughout development. Apoid wasp nest types
tive biology of the Ampulicidae, Sphecidae, and can be grouped in five categories: cavity nests;
Crabronidae are covered in more detail below. nests excavated in plant material; nests excavated
in soil; free-standing mud nests; and free-standing
nests made of various materials bound with silk.
Reproductive Biology of Females In some genera, different species may construct
nests in different categories.
The reproductive strategies of female apoid wasps Cavity nests, those built within existing cavi-
fall into three broad categories: parasitoidism, ties, are often constructed in old beetle tunnels in
brood parasitism, and nest-provisioning. The nest wood, but have also been found in such locations
236
A Apoid Wasps (Hymenoptera: Apoidea: Spheciformes)

as empty snail shells, old plant galls, pitcher plants, in flight from hunting grounds to the nest. Prey
rolled leaves, and gaps between stones or between are usually carried in the wasps legs, sometimes
boards on the siding of houses. Such nests usually with the aid of the mandibles, but some Oxybelus
contain multiple cells separated by a species-spe- tote prey impaled on their stings, whereas Clypea-
cific choice of materials; for example, Chalybion don females carry their ant prey grasped by the
uses mud; Isodontia, chopped grass fragments and thorax using structures on the terminal abdomi-
plant fibers; Passaloecus, conifer resins; Nitela, nal segments aptly referred to as ant clamps.
wood chips; and Podium, an eclectic mix of detri- When they leave nests to forage, females of
tus, mud, and resin. Wasps that excavate their own nest-provisioning apoid wasps face two problems
nest tunnels in plant materials may tunnel through in particular, other than the obvious need to find,
the pith of plant stems (e.g., in raspberry or sumac) sting, and transport their prey: the necessity to
or rotten wood in logs. Cells may be arranged in a protect the unguarded nest from natural enemies
linear sequence, and tunnels in the same nest may and the need to find their way home again. Before
diverge into separate branches. Nests excavated in departing to hunt, wasps often plug the entrance
soil are, by far, the most common type of nest temporarily as a means of excluding intruders.
among apoid wasps. They may be simple, And when a nest is completed, the female may
unbranched shallow tunnels terminating in the construct an even more elaborate closure and take
single brood cell, as is the case for some or all spe- steps to conceal the entrance; in ground nesting
cies of Ammophila, Bembecinus, Bembix, Podalo- species, this involves often elaborate and pro-
nia, and Prionyx. Other species dig branched nests longed leveling of the mound of excavated soil
with side tunnels leading to as many as 12 two adjacent to the nest entrance. Nevertheless,
dozen brood cells provisioned in succession over a although these actions are likely successful in
period of several weeks. Single and multi-celled many cases, apoid wasp larvae are plagued by a
nests can be found not only among different spe- variety of natural enemies that commence their
cies of the same genus, but among different females attacks at varying times in the life cycle of the
in one species. Free-standing nests constructed wasp. Brood parasites, which include not only
de novo by females may be built of mud sculpted into other apoid wasps, but mites, flies (Phoridae, Sar-
species-specific shapes, as is the case for species of cophagidae), and non-apoid wasps (Chrysididae)
Pison, Sceliphron, and Trypoxylon. Mud nests may that feed on the wasps own prey, may kill the
be attached to vines, trees, cliff faces, or nowadays, wasps young either directly or indirectly (through
buildings; they may also have multiple cells. starvation). Parasitoids that feed directly on wasp
In most cases, each nest cell is completely pro- larvae or pre-pupae include, among other insects,
visioned and closed off by the adult before the next flies (Bombyliidae), beetles (Rhipiphoridae), and
cell is begun, but there is some variation in the other aculeate wasps (Chrysididae and Mutillidae).
duration and timing of provisioning relative to the Several detailed studies attest to the fact that
developmental schedule of offspring. Most species female wasps often have excellent homing abilities
are mass provisioners that completely provision that lead them back to their nest, even when that
cells with one or more prey before the egg hatches. nest is one of many hundreds or thousands densely
More rarely, females are progressive provisioners packed into the apparently featureless soil surface
that continue to bring in prey after the egg hatches, of a nesting area. As far back as 1930, Niko Tinber-
sometimes until the larva is ready, or nearly so, to gens research showed that a Philanthus triangu-
spin its cocoon. Among solitary apoid wasps, only lum female can relocate her nest by learning the
certain Ammophila provision two cells simultane- image of the landscape surrounding the nest and
ously. During provisioning, females of those spe- matching the memorized image to the configura-
cies that hunt relatively small prey carry the prey tion of local landmarks when she later returns
 Apoid Wasps (Hymenoptera: Apoidea: Spheciformes)
A 237

with prey. The initial task of learning the image is and provisions it without assistance from conspe-
apparently accomplished during an orientation cifics. Nests of both ground- and mud-nesters do
flight, which in the case of P. triangulum, begins sometimes occur in dense aggregations, but true
when the female circles the nest in flight, then communal and eusocial behavior is relatively rare
gradually expands the diameter and height of her among apoid wasps. Communal nests, in which
loops before departing for her hunting grounds. small groups of females share a main nest burrow,
The form of the orientation flights varies among but in which each provisions her own brood cells,
species, but females of all species share an uncanny have been reported in several genera (e.g., Cerce-
ability to find their way home, even after being ris, Moniaecera, Spilomena). In the Neotropics,
transported several hundred meters away by Microstigmus comes is eusocial, inhabiting nests
researchers. in which (i) two generations of adult females
When we examine the ovaries of female apoid are present (likely a mother and her daughters),
wasps, we find several features that vary among (ii) each nest cell is provisioned cooperatively, and
species and correlate with overall reproductive (iii) one female is the primary egg layer. The nests,
strategies. First, although the paired ovaries of which are founded by one or more females, have
nest provisioning species each have three ovarioles as many as 18 brood cells and 10 adult females (as
(except for Oxybelus which have two), each ovary well as a smaller number of adult males). The nests
of brood parasitic species is comprised of four of Microstigmus are unique among apoid wasps,
ovarioles (and sometimes five in Stizoides renicinc- that of M. comes consisting of a 13 cm deep bag
tus). Second, although it is common for females of of plant fibers embedded in a matrix of silk and
nest provisioners (especially progressive provi- suspended from the underside of a leaf by a short,
sioners) to carry a maximum just one or two coiled petiole. Other Microstigmus create similar
mature oocytes in their ovaries at a any time, brood nests, but embedding small pieces of bark, wood,
parasites commonly carry 46 mature oocytes; leaf hairs, lichens, sand, or stone in the silk mesh.
and the parasitoid species Larra amplipennis can The use of silk produced by adults in nest con-
carry as many as 21. Third, the eggs produced by struction is limited among apoid wasps to
nest provisioners tend to be larger (relative to Microstigmus and other Pemphredoninae (e.g.,
overall body size) than those of brood parasites or Arpactophilus, Psenulus); however, larval apoid
of Larra. All in all, this meshes with the fact that wasps commonly incorporate silk into their
nest provisioning apoid wasps, because they invest cocoons. Finally, whereas other social insects build
so highly in individual offspring, have relatively nests gradually, expanding their size over time,
low lifetime fecundities compared to parasitoids Microstigmus construct their silken abodes all at
and brood parasites in their same families. Thus, it once and so are limited to their confines until all
is likely common that even the most successful cells in the nest are completed.
females of some nest provisioners can expect to have
fewer than ten offspring during their lives. This contrasts
markedly with the high potential fecundities of non- Mating Strategies
aculeate parasitoid Hymenoptera (e.g., Braconidae,
Ichneumonidae). In 1960, a comprehensive review of the diversity
of male apoid wasp behavior would have occupied
a brief paragraph, but we now have a much better
Communal and Social Species understanding of male behavior. Perhaps the best-
known male behaviors are the so-called sun
The vast majority of apoid wasps are solitary spe- dances of sand wasps (Bembicinae) in which
cies, each of whose females occupies a nest alone hundreds or thousands of males swarm over the
238
A Apoid Wasps (Hymenoptera: Apoidea: Spheciformes)

surface of nesting areas seeking newly emerged which the male induces the female to copulate.
virgin females (as in many species of Bembix). A This, however, is one of the least-studied aspects
variation on this theme sees males attempting to of apoid wasp reproductive biology.
rendezvous with females at the point at which they
emerge from the ground when they leave their
natal nests (e.g., Bembecinus quinquespinosus, Economic Significance of Apoid
Bembix rostrata, and Glenostictia satan). Wasps
In other species, males defend discrete terri-
tories that are often plots of ground in emergence A least one genus of apoid wasps, Larra, whose
or nesting areas, as is the case for Sphecius (cica- females prey on mole crickets, includes species
da-killers) and many Philanthus (beewolves). Or that have found some success as biological con-
males may defend individual nests that are in the trol agents. Other genera contain species that
process of being provisioned by females (as in may provide some natural control of pests such
some Trypoxylon and Oxybelus, for example). as aphids (Passaloecus), biting flies (Bembix, Stic-
Less commonly, males establish territories at tia), cutworms (Podalonia), grasshoppers (Pri-
hunting sites frequented by females (e.g., Aphilan- onyx, Tachysphex), Mormon crickets (Palmodes),
thops subfrigidus which defend territories in mat- and leafhoppers (many genera). On the negative
ing swarms of prey, and Mellinus rufinodus which side of the ledger, apoid wasps can be a nuisance
defend feces that attract flies hunted by females). to those people that cannot abide the presence of
In yet other species, territories are situated in a wasp, no matter what its activities. In North
locations that have no other apparent attractive- America, large territorial males of the cicada-
ness to females other than the presence of the killer wasp, Sphecius speciosus, sometimes bother
males themselves (e.g., Eucerceris flavocincta, homeowners and park visitors who mistake male
Philanthus basilaris). While defending their ter- investigatory flights for something more hostile.
ritories, male wasps may engage in rowdy battles The large nest mounds of female cicada-killers
that involve, depending on the species, wrestling, that appear in otherwise immaculate lawns are
biting, head butting, abdomen slapping, or mutual considered unsightly by some. In Africa, Palarus
flights in which the contestants swirl about one latifrons and Philanthus triangulum can be out-
another at dizzying speeds. One should not be right pests when large numbers of females
left with the impression, however, that males of invadeapiaries and decimate worker honey bee
any given species have just one way to find a mate, populations. And we know very little about the
as alternative mating tactics are common. Male potential effect of apoid wasp predators on the
Stictia heros, for example, may patrol the nesting biology of other beneficial insects such as native
area in the morning, but shift to defending terri- pollinators and biological control agents.
tories later in the day. And some males of Philan- Wasps, Ants, Bees and Sawflies
thus zebratus patrol the air space above the Bees
nesting area, while others simultaneously defend
scent-marked territories nearby.
Ultimately, it appears that in most cases it is References
the females that control which males are success-
ful. Females, after all, are usually the larger sex, so Bohart RM, Menke AS (1976) Sphecid wasps of the world: a
are physically dominant to males (and in the case generic revision. University of California Press,
Berkeley, CA, pp 695
of Philanthus basilaris, may even prey upon them). Evans HE (1966) The comparative ethology and evolution of
So mating is sometimes, though not always, the sand wasps. Harvard University Press, Cambridge,
preceded by obvious courtship activities during MA, pp 526
 Aposematism
A 239

Evans HE, ONeill KM (1988) The natural history and

behavior of North American beewolves. Cornell
Apolysis
University Press, Ithaca, NY, pp 278
Evans HE, ONeill KM (2007) The sand wasps: behavior and Separation of the epidermal cells from the inner
natural history. Harvard University Press, Cambridge, surface of the endocuticle. This is the first step in
MA, pp 340
Goulet H, Huber JT (1993) Hymenoptera of the world: an
the process of molting.
identification guide to families. Research Branch,
Agriculture Canada, Publication 1894/E. Centre for
Land and Biological Resources Research, Ottawa, Apomorphic
Canada, pp 668
Grimaldi D, Engel MS (2005) Evolution of the insects. Cam-
bridge University Press, New York, NY, pp 772 A character that is derived and not ancestral.
Krombein KV (1967) Trap-nesting wasps and bees: life histories,
nests, and associates. Smithsonian Press, Washington,
DC, pp 570.
Matthews RW (1991) Evolution of social behavior in the Apomorphy
sphecid wasp. In Ross KG, Matthews RW (eds) The
social biology of wasps. Cornell University Press, Ithaca, When considering classification and phylogeny, a
NY, pp 570602
Michener CD (2000) The bees of the world. The Johns
derived character state.
Hopkins University Press, Baltimore, MD, 913 pp
Melo GAR (1999) Phylogenetic relationships and classification
of the major lineages of Apoidea (Hymenoptera), with Apophysis
emphasis on the crabronid wasps. Natural History
Museum, University of Kansas, Scientific Papers 12:155
Melo GAR, Gonalves RB (2005) Higher-level bee classifica- An internal or external elongate projection of the
tions (Hymenoptera, Apoidea, Apidae sensu lato). body wall.
Revista Brasileira de Zoologia 22:153159
Ohl M, Bleidorn C (2006) The phylogenetic position of
the enigmatic family Heterogynaidae based on
molecular data, with description of a new, nocturnal Apoprogonidae
species (Hymenoptera: Apoidea). Syst Entomol
31:321337.
ONeill KM (2001) Solitary wasps: natural history and behav-
A family of moths (order Lepidoptera). They also
ior. Cornell University Press, Ithaca, NY, pp 406 are known as African skipper moths.
Pulawski WJ (2007) Catalog of the Sphecidae sensu lato African Skipper Moths
(=Apoidea excluding Apidae). California Academy of Butterflies and Moths
Sciences. Available at http://www.calacademy.org/
research/entomolog y/Entomolog y_Resources/
Hymenoptera/sphecidae/Genera_and_species_PDF/
introduction.htm
Tree of Life Web Project (1995) Apoidea. Bees, digger
wasps. Version 01 January 1995 (temporary). http://
Aposematism
tolweb.org/Apoidea/11190/1995.01.01 in The Tree
of Life Web Project. Available at http://tolweb.org/ heather j. mcauslane
University of Florida, Gainesville, FL, USA

Apolysal Space Aposematism is a strategy used by many organ-

isms that increases their conspicuousness, and
During molting, a very small space is created by alerts or warns potential predators of their
the separation of the epidermis from the old toxicity, their ability to inflict pain or, more
cuticle. This space, called the apolysal space, simply, their unpredictibility. Insects have
contains molting fluid during the process of evolved this strategy to a high degree, although
cuticle digestion. it is found occasionally in other terrestrial
240
A Aposematism

organisms such as snakes, lizards, and frogs, the toxins themselves often are emetic (for
and in aquatic organisms such as nudibranches. example, cardiac glycosides in the Monarch
Aposematic signals usually are visual in nature butterfly, Danaus plexippus, and lucibufagins in
and involve bright and contrasting coloration, Photinus fireflies), meaning that they cause the
usually black and red, yellow or orange or black predator to regurgitate the prey item before a
and white. Visual signals may be enhanced by lethal dose of the toxin has been absorbed. The
certain odors, sounds or behaviors, presenting toxins also are often bitter so that the predator
a multimodal signal that predators may recog- is less likely to pursue the attack once the bitter
nize and learn more easily. compounds have been contacted. In other
Visual aposematism as an antipredator insects, toxins are not stored within the body
strategy only works well against predators with but are injected into predators through sharp
color vision and good learning ability. Birds, urticating hairs or spines (for example, larvae
and to a lesser extent lizards and amphibians, of the saddleback moth, (Fig.68) Sibine stimu-
are the most common predators for which apos- lea). In these insects, the predator is warned of
ematic coloration (Figs.66 and 67) is an effec- the prey items distastefulness without having
tive deterrent. The nave predator associates the to breach the cuticle of the aposematic
particular color pattern of an aposematic organ- organism.
ism with the unpleasant after effects of eating The nave predator may need only one trial
or attempting to eat it. Aposematic insects usu- to associate the color pattern of the aposematic
ally back up their warning signal with chemical insect with emesis or a bitter taste but more
defenses (unless they are harmless mimics of often, learning takes several trials. The speed of
another toxic organism). These chemical learning can be enhanced in several ways. If the
defenses may be toxins that are stored inside predator encounters several toxic insects with
the insects body that could cause death if the same aposematic pattern within a short
ingested and absorbed by the predator. H
owever, period of time, it appears to learn the warning

Aposematism, Figure 66 Aposematic insects are often aggregated, perhaps increasing the rate at which
predators associate aposematic coloration with toxicity. The orange and black larvae of the o leander
caterpillar, Syntomeida epilais (Ctenuchidae), aggregate in the early instars on oleander, Nerium o leander,
a plant containing heart poisons (cardiac glycosides) (photo by James Castner).
 Aposematism
A 241

Aposematism, Figure 67 The black and white larvae of the Giant African Skipper (Hesperiidae) also
aggregate on their host plant (photo by Andrei Sourakov).

coloration faster. This may explain why apose- the visual pattern with acoustic signals or
matic insects are often gregarious, living in small, olfactory signals. Many aposematic insects hiss,
usually related, groups. For example, oleander cat- stridulate or make some other noise when
erpillars, Syntomeida epilais and oleander aphids, predators attack them. Arctiic moths and lubber
Aphis nerii live gregariously on oleander which grasshoppers, Romalea guttata, commonly do
contains heart poisons. Other factors that can this. The association of sound with the color pat-
increase the rate of learning are the pairing of tern and bitter chemical toxins in the aposematic
242
A Aposymbiotic

Aposematism, Figure 68 Larvae of the saddleback moth, Sibine stimulea (Limacodidae), advertise
their urticating hairs with a pronounced brown and white saddle on the lime-green bodies (photo by
James Castner).

insects help the predator better remember the Allelochemicals

color pattern. We are becoming increasingly Mimicry
aware that many insects release volatile pyra- Chemical Ecology
zine compounds when under attack. These
nitrogen-containing compounds are extremely References
odorous at low c oncentrations and are thought
to produce a universal warning odor in plants Guilford T, Nicol C, Rothschild M, Moore BP (1987) The
and animals. biological roles of pyrazines: evidence for a warning
odour function. Biol J Linn Soc 31:113128
Insects that are aposematic often exhibit Guildford T (1990) The evolution of aposematism. In: Evans
what we might call bold behavior, at least for DL, Schmidt JO (eds) Insect defenses: adaptive mecha-
an insect. They are usually active during the nisms and strategies of prey and predators. State Uni-
day and are not cryptic, rather feeding in an versity of New York Press, New York, NY, pp 2361
Huheey JE Bell WJ, Card RT (eds) (1984) Chemical ecology
exposed position. Aposematic adults may have of insects. Sinauer Associates, Inc., Sunderland, MA, pp
an exaggerated slow flight, as do Heliconius 257297
butterflies and many arctiid moths. Larvae may Rothschild M, Bergstrm G (1997) The monarch butterfly
caterpillar (Danaus plexippus) waves at passing
wave tentacles and other long protuberances
Hymenoptera and jet aircraft-are repellent volatiles
from their body to warn predators. Larvae of released simultaneously? Phytochemistry 45:11391144
the Monarch butterfly (Fig.69) integrate apos- Rowe C (2002) Sound improves visual discrimination learn-
ematic behaviors into their multimodal signal ing in avian predators. Proc R Soc Biol Sci B
269:13531357
to warn of their toxicity. In addition to being
conspicuously striped white, yellow and black,
they release pyrazine from the head collar
region when roughly handled and nod their Aposymbiotic
heads up and down every 2 s while simultane-
ously twitching their anterior filiform Separated from its symbiotes, or symbiote-free;
tentacles. this usually refers to mutualistic symbiotes.
 Apparent Resources
A 243

Aposematism, Figure 69 Larvae of the Monarch butterfly, Danaus plexippus (Danaidae), use a
multimodal signal to warn potential predators. Their aposematic coloration of black, white, and yellow
stripes is enhanced with the release of pungent pyrazine and the behavioral display involving rhythmic
nodding of the head and twitching of the filiform tentacles (photo by Lyle Buss).

Apotome Apparent Resources

A narrow anterior portion of each abdominal ster- Food resources (either insect or plant) that are easy
num, separated by a fold from the rest of the plate. to locate or apparent to potential predators or her-
They are present in Apterygota, but indistinct in bivores. Apparent resources often are protected
Pterygota. against consumption by generalist and specialist
Abdomen of Hexapods predators, and generalist or specialist herbivores, by
244
A Appeasement Substance

possessing broadly effective (though metabolically produce a curling of the leaves and, when feeding
expensive) chemical defenses such as digestibility on fruit, may cause it to be stunted or misshapen
reducing substance (contrast with unapparent and may change the sugar content, greatly impair-
resources). ing the flavor.
Many insects feed as miners in leaves or as bor-
ers in stems, roots, or fruits. Feeding between the
Appeasement Substance upper and lower surfaces of the leaf may cause as
much defoliation as external feeding. There areabout
A secretion presented by a social parasite that 500 leafmining species in the United States (e.g.,
reduces aggression by the host insects, and aids par- spotted tentiform and apple blotch leafminers).
asites in being accepted as members of the colony. Tunneling causes serious damage. Insects
thattunnel into fruit include codling moth, orien-
tal fruit moth, apple maggot, and plum curculio.
Apple Maggot Damage with more serious consequences can be
done by insects that tunnel into the tree trunk,
Apple Pests and their Management bark, or foliar shoots, such as apple-boring bee-
tles (roundheaded, flatheaded), dogwood borer,
American plum borer, European corn borer, and
Apple Pests and their oriental fruit moth.
Management Injection of a chemical into plant tissues while
the insect feeds causes abnormal growth (e.g., rosy
arthur m. agnello apple aphid) or produces a gall (woolly apple aphid).
New York State Agricultural Experiment Station, Each species of gall insect produces a characteristic
Geneva, NY, USA gall on a certain part of a particular plant.
Insects at the larval and nymphal stages (e.g.,
Insects with chewing mouthparts inflict great dam- woolly apple aphid) that live in the soil and attack the
age on foliage, causing leaves to be skeletonized, underground plant parts cause extensive damage.
riddled with holes, eaten around the edges, or entirely Shelters in plants are built by leafrollers and leaf
consumed (e.g., larvae of moths, sawflies, and folders, which roll or fold the leaves and tie them with
beetles). Other insects suck sap from leaves, stems, silk, feeding in the shelter so formed. Leaf tiers and
or other plant parts, producing a characteristic spot- webworms tie several leaves or even entire branches
ting or browning, curling, or wilting. Feeding on together, producing large silken webs or tents.
stems or twigs results in dwarfing or wilting. Dam- A few insects injure plants when they lay their
age is caused both by removal of the sap and by eggs, particularly in stems or fruits (e.g., plum cur-
injury to the plant tissue (e.g., scale insects, aphids, culio, apple maggot, periodical cicadas, tree crick-
and true bugs). Also included in this category ets, leafhoppers).
(Fig.70) are mites, such as the European red mite
and the two-spotted spider mite, which damage the
leaves by piercing the cell walls with bristle-like Major Economic Pests
mouthparts and ingesting their contents, including
the chlorophyll. The injury results in off-color foli- Early researchers in New York estimated nearly
age that, in severe cases, becomes bronzed. 500 species of insects known to feed on apple.
Scale insects are usually minute, but if they Fortunately, only a relatively small number of
are abundant enough to encrust bark, twigs, or these ever reach economic pest status. A survey
stems they can kill orchard and shade trees. Aphids conducted in the northeastern U.S. identified a
 Apple Pests and their Management
A 245

Apple Pests and their Management, Figure 70 Some North American apple pests: (a) codling moth;
(b) obliquebanded leafroller; (c) rosy apple aphid; (d) plum curculio; (e) spotted tentiform
leafminer; (f) European red mite attacked by predatory mite; within circle, apple maggot adult, larva
and pupa.
246
A Apple Pests and their Management

total of 191 phytophagous (plant-feeding) insect Decision Making

species in managed and abandoned apple
orchards. Most numerous were species of Lepi- Because rosy apple aphid populations are highly
doptera (mostly moths and their caterpillars, variable, it is important to assess their densities
43%) and Hemiptera (leafhoppers, plant bugs, before making a treatment. Sampling can begin at
aphids and scale insects, 32%). Current tabula- the tight cluster bud stage but is better done at the
tions of actual economic pests list just over 60 pink stage when rosy apple aphid nymphs are more
species in New York, approximately half of which easily seen. Rosy apple aphid densities are estimated
are considered important enough to warrant spe- by sampling 10 fruit clusters from the interior can-
cific control recommendations. This compares opy area of 10 trees. Treatment is generally recom-
with 17 pest species for pear, 12 for peach, and mended if one infested cluster is found, but for
seven for tart cherry and plum. Asimilar account- experienced samplers of rosy apple aphids, this is
ing in other production regions reveals certain probably too conservative and a threshold of three
species with a worldwide distribution, and others, to five infested clusters would be more appropriate.
largely representing the above major orders, that
are prevalent only in specific areas (Table 9). The
following are some of the key pests in the north-
Control
eastern U.S. growing regions.
It is not known how important natural enemies
(such as larvae of the fungus gnats, Cecidomyii-
dae) are in regulating rosy apple aphid popula-
Rosy Apple Aphid, Dysaphis
tions. Several pesticides can effectively control this
plantaginea (Passerini)
pest when applied at the pink bud stage. A mate-
rial should be used that will conserve natural
Biology and Impact
enemy populations, such as Typhlodromus pyri,
animportant mite predator.
The rosy apple aphid is the most damaging of the
aphids that attack apple. Its saliva, injected while
feeding, is translocated to nearby fruit, causing
leaf curling and small, deformed apples. The rosy Spotted Tentiform Leafminer,
apple aphid can be distinguished from other Phyllonorycter blancardella
aphids by its long cornicles and purple-rose color. (Fabricius)
It overwinters as an egg on twigs, in bud axils, and
in bark crevices. The overwintering eggs of the Biology and Impact
rosy apple aphid are oblong and pale green at first,
then turn shiny black. Rosy apple aphid nymphs The spotted tentiform leafminer was introduced
are visible beginning around the tight cluster bud from Europe in the 1880s. Its host plants include
stage but are most easily observed at the pink bud apple, wild cherry, hawthorn, quince, plum, and
stage. The first adults appear around bloom. Sec- crabapple. Spotted tentiform leafminer overwin-
ond-generation adults appear two to three weeks ters as a pupa in leaf litter on the ground. Adults
after petal fall. Some of these move to alternate emerge at the green tip apple bud stage and lay
hosts (such as narrowleaf plantain) and the rest small, flattened eggs that are deposited singly on
remain in the orchard. The third generation devel- leaf undersides. Egg laying begins when leaves
ops by mid-July and moves to alternate hosts. In unfold after the half-inch green bud stage, and
later summer, adult rosy apple aphids return to the deposition is nearly complete by the end of the
trees to lay eggs. pink bud stage. Its five larval stages are divided
 Apple Pests and their Management
A 247

Apple Pests and their Management, Table 9 Major insect and mite pests of apple
Taxon scientific and common name Geographical distribution Plant parts affected
Acari: Eriophyidae
Aculus schlechtendali (Nalepa), apple rust North America, South Amer- Foliage
mite ica, Europe, Australia/New
Zealand
Eriophyes pyri (Pagenstecher), pearleaf blis- North America, South Africa Foliage
ter mite
Acari: Tetranychidae
Bryobia praetiosa Koch, clover mite North America Foliage
Bryobia rubrioculus (Scheuten), brown mite Worldwide Foliage
Panonychus ulmi (Koch), European red mite Worldwide Foliage
Tetranychus canadensis (McGregor), North America Foliage
fourspotted spider mite
Tetranychus kanzawai Kishida, kanzawa Asia Foliage
mite
Tetranychus mcdanieli McGregor, McDaniel North America Foliage
spider mite
Tetranychus urticae Koch, two spotted spi- Worldwide Foliage
der mite
Tetranychus viennensis Zacher, hawthorn Asia Foliage
spider mite
Coleoptera: Bostrichidae
Amphicerus bicaudatus (Say), apple twig North America Twigs, Wood
borer
Coleoptera: Buprestidae
Chrysobothris femorata (Olivier), flatheaded North America Cambium, Wood
appletree borer
Coleoptera: Cerambycidae
Prionus imbricornis (Linnaeus), tilehorned North America Cambium, Roots
prionus
Prionus laticollis (Drury), broad necked root North America Cambium, Roots
borer
Saperda candida Fabricius, roundheaded North America Cambium, Wood
appletree borer
Coleoptera: Chrysomelidae
Nodonota puncticollis (Say), rose leaf beetle North America Fruit
Coleoptera: Curculionidae
Anthonomus pomorum (Linnaeus), apple Europe, Asia Buds
blossom weevil
Anthonomus quadrigibbus Say, apple North America Foliage, Fruit
curculio
Conotrachelus nenuphar (Herbst), plum North America Fruit
curculio
248
A Apple Pests and their Management

Apple Pests and their Management, Table 9 Major insect and mite pests of apple (Continued)

Taxon scientific and common name Geographical distribution Plant parts affected
Naupactus xanthographus (Germar), grape South America Buds, Foliage
snout beetle
Phlyctinus callosus Boheman, banded fruit South Africa Fruit
weevil
Scolytus rugulosus (Mller), shothole borer North America Cambium, Wood
Coleoptera: Scarabaeidae
Macrodactylus subspinosus (Fabricius), rose North America Foliage, Fruit
chafer
Popillia japonica Newman, Japanese beetle North America Foliage, Fruit
Dermaptera: Forficulidae
Forficula auricularia Linnaeus, European Europe Fruit
earwig
Diptera: Agromyzida
Liriomyza brassicae (Riley), serpentine North America Foliage
leafminer
Diptera: Cecidomyiidae
Dasineura mali (Kieffer), apple leafcurling North America, Europe, Aus- Foliage
midge tralia/New Zealand
Diptera: Tephritidae
Anastrepha fraterculus (Weidemann), South America Fruit
S.American fruit fly
Bactrocera tryoni (Froggatt), Queensland South America, Australia/ Fruit
fruit fly New Zealand
Ceratitis capitata (Wiedemann), Mediterra- South Africa Fruit
nean fruit fly
Ceratitis rosa Karsch South Africa Fruit
Rhagoletis pomonella (Walsh), apple North America Fruit
maggot
Hemiptera: Miridae
Atractotomus mali (Meyer), apple brown North America Fruit
bug
Campylomma liebknechti (Girault), apple Australia/New Zealand Fruit
dimpling bug
Campylomma verbasci (Meyer), mullein North America, Europe Fruit
plant bug
Lygidea mendax Reuter, apple red bug North America Foliage, Fruit
Lygocoris pabulinus (Linnaeus) Europe Fruit
Lygus lineolaris Palisot de Beauvois, North America Fruit
tarnished plant bug
Plesiocoris rugicollis Falln Europe Fruit
Hemiptera: Pentatomidae
 Apple Pests and their Management
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Apple Pests and their Management, Table 9 Major insect and mite pests of apple (Continued)

Taxon scientific and common name Geographical distribution Plant parts affected
Antestiopsis orbitalis Ghesquierei Car., South Africa Fruit
antestia bug
Heteroptera: Tingidae
Stephanitis pyri Fabricius Europe Foliage
Hemiptera: Aphididae
Aphis pomi DeGeer, apple aphid North America, South Amer- Foliage, Fruit
ica, Europe
Aphis spiraecola Patch, spirea aphid North America, South Amer- Foliage
ica, South Africa, Asia
Dysaphis plantaginea (Passerini), rosy apple North America, Europe Foliage, Fruit
aphid
Eriosoma lanigerum (Hausmann), woolly Worldwide Roots, Twigs
apple aphid
Myzus malisuctus Matsumura, apple Asia Foliage
leafcurling aphid
Rhopalosiphum fitchii (Sanderson), apple North America, South Buds, Foliage
grain aphid America
Schizaphis piricola Matsumura Asia Foliage
Hemiptera: Cicadellidae
Edwardsiana crataegi (Dg.), apple South America Foliage
leafhopper
Edwardsiana frogatti Baker Europe Foliage
Edwardsiana rosae (Linnaeus), rose North America Foliage
leafhopper
Empoasca fabae (Harris), potato North America Foliage
leafhopper
Empoasca maligna (Walsh), apple North America Foliage
leafhopper
Typhlocyba pomaria McAtee, white apple North America Foliage, Fruit
leafhopper
Hemiptera: Cicadidae
Magicicada septendecim (Linnaeus), North America Twigs, Wood
periodical cicada
Hemiptera: Coccidae
Parthenolecanium corni (Bouch), European North America Wood, Fruit
fruit lecanium
Hemiptera: Diaspididae
Aonidiella aurantii (Maskell), California red North America, South Africa Twigs, Wood
scale
Chionaspis furfura (Fitch), scurfy scale North America Cambium, Fruit
250
A Apple Pests and their Management

Apple Pests and their Management, Table 9 Major insect and mite pests of apple (Continued)

Taxon scientific and common name Geographical distribution Plant parts affected
Epidiaspis leperii (Signoret), Italian pear South America, Europe Cambium
scale
Hemiberlesia lataniae (Signoret), latania South America Cambium
scale
Lepidosaphes ulmi (Linnaeus), oystershell North America, South Amer- Cambium
scale ica, Europe
Quadraspidiotus forbesi (Johnson), Forbes North America Cambium
scale
Quadraspidiotus perniciosus (Comstock), San Worldwide Cambium, Fruit
Jose scale
Hemiptera: Flatidae
Metcalfa pruinosa (Say) Europe Fruit
Hemiptera: Margarodidae
Icerya purchasi Maskell, cottony cushion South Africa Wood, Twigs, Fruit
scale
Hemiptera: Membracidae
Stictocephala bisonia Kopp & Yonke, b
uffalo North America, Europe Twigs, Wood
treehopper
Hemiptera: Pseudococcidae
Pseudococcus calceolariae (Maskell), Europe, Australia/New Zea- Fruit
citrophilus mealybug land, South Africa
Pseudococcus comstocki (Kuwana), Com- North America Foliage, Fruit
stock mealybug
Hemiptera: Psyllidae
Cacopsylla mali (Schmidberger), apple North America, Europe Foliage
sucker
Hymenoptera: Tenthredinidae
Hoplocampa testudinea (Klug), European North America, Europe Fruit
apple sawfly
Lepidoptera: Arctiidae
Hyphantria cunea (Drury), fall webworm North America, Europe, Asia Foliage
Lophocampa caryae Harris, hickory tussock North America Foliage
moth
Lepidoptera: Carposinidae
Carposina niponensis Walshingham, peach Asia Fruit
fruit moth
Carposina sasakii Matsumura, peach fruit Asia Fruit
moth
Lepidoptera: Choreutidae
Choreutis pariana (Clerck), apple-and-thorn North America, Europe, Asia Foliage
skeletonizer
 Apple Pests and their Management
A 251

Apple Pests and their Management, Table 9 Major insect and mite pests of apple (Continued)

Taxon scientific and common name Geographical distribution Plant parts affected
Lepidoptera: Coleophoridae
Coleophora multipulvella (Chambers), pistol North America, Asia Foliage, Fruit
casebearer
Coleophora serratella (Linnaeus), cigar/birch North America, Europe, Asia Foliage
casebearer
Lepidoptera: Cossidae
Cossus cossus Linnaeus, European goat North America, Europe, Asia Cambium, Wood
moth
Zeuzera pyrina Linnaeus, leopard moth North America, Europe, Asia Wood, Twigs
Lepidoptera: Geometridae
Alsophila pometaria (Harris), fall North America Foliage
cankerworm
Operophtera brumata Linnaeus, winter moth North America, Europe, Asia Buds, Foliage, Fruit
Paleacrita vernata (Peck), spring North America Foliage
cankerworm
Lepidoptera: Gracillariidae
Marmara elotella (Busck), apple barkminer North America Cambium
Marmara pomonella Busck, apple fruitminer North America Fruit
Phyllonorycter blancardella (Fabricius), spot- North America, Europe, Asia Foliage
ted tentiform leafminer
Phyllonorycter crataegella (Clemens), apple North America Foliage
blotch leafminer
Phyllonorycter elmaella Doganlar & Mutuura, North America Foliage
western tentiform leafminer
Phyllonorycter ringoniella (Matsumura), Asia Foliage
apple leafminer
Lepidoptera: Lasiocampidae
Malacosoma americanum (Fabricius), North America Foliage
eastern tent caterpillar
Lepidoptera: Lymantriidae
Euproctis chrysorrhoea (Linnaeus), b
rowntail North America, Europe, Asia Foliage
moth
Lymantria dispar (Linnaeus), gypsy moth North America, Europe, Asia Foliage
Orgyia antiqua (Linnaeus), rusty tussock North America, South Amer- Buds, Foliage
moth ica, Europe, Asia
Orgyia leucostigma (J.E. Smith), North America Foliage, Fruit
whitemarked tussock moth
Lepidoptera: Lyonetiidae
Bucculatrix pomifoliella (Clemens), apple North America Foliage
bucculatrix
252
A Apple Pests and their Management

Apple Pests and their Management, Table 9 Major insect and mite pests of apple (Continued)

Taxon scientific and common name Geographical distribution Plant parts affected
Leucoptera malifoliella (Costa), pearleaf blis- Europe, Asia Foliage
ter moth
Lyonetia prunifoliella (Hbner), apple North America, Europe, Asia Foliage
lyonetid
Lyonetia speculella Clemens, apple North America Foliage
leafminer
Lepidoptera: Noctuidae
Amphipyra pyramidoides Guene, humped North America Foliage, Fruit
green fruitworm
Helicoverpa armigera (Hbner), cotton Europe, Asia, South Africa Fruit
bollworm
Lacanobia subjuncta (Grote & Robinson), North America Foliage, Fruit
Lacanobia fruitworm
Lithophane antennata (Walker), green North America Fruit
fruitworm
Orthosia hibisci (Guene), speckled green North America Foliage, Fruit
fruitworm
Xestia c-nigrum (Linnaeus), spotted North America, Europe, Asia Foliage
cutworm
Lepidoptera: Notodontidae
Datana ministra (Drury), yellownecked North America Foliage
caterpillar
Schizura concinna (J. E. Smith), redhumped North America Foliage
caterpillar
Lepidoptera: Pyralidae
Conogethes punctiferalis (Guene), yellow Asia, Australia/New Zealand Fruit
peach moth
Euzophera semifuneralis (Walker), American North America Cambium, Wood
plum borer
Ostrinia nubilalis (Hbner), European corn North America, South Amer- Foliage, Fruit
borer ica, Europe, Asia
Lepidoptera: Sesiidae
Podosesia syringae (Harris), lilac/ash borer North America Cambium, Wood
Synanthedon myopaeformis Borkhausen, Europe, Asia Cambium, Wood
apple clearwing moth
Synanthedon pyri (Harris), apple bark borer North America Cambium, Wood
Synanthedon scitula (Harris), dogwood North America Cambium, Wood
borer
Lepidoptera: Tisheriidae
Tischeria malifoliella Clemens, apple trum- North America Foliage
pet leafminer
Lepidoptera: Tortricidae
 Apple Pests and their Management
A 253

Apple Pests and their Management, Table 9 Major insect and mite pests of apple (Continued)

Taxon scientific and common name Geographical distribution Plant parts affected
Adoxophyes orana Fischer Von R
slerstamm, South America, Europe, Asia Fruit
summer fruit tortrix
Archips argyrospila (Walker), fruittree North America Foliage, Fruit
leafroller
Archips podana Scopoli, fruittree tortrix North America, Europe, Asia Foliage, Fruit
Archips rosana (Linnaeus), rose tortrix North America, Europe, Asia Fruit
Argyrotaenia citrana (Fernald), orange North America Fruit
tortrix
Argyrotaenia pulchellana Haworth Europe Foliage, Fruit
Argyrotaenia velutinana (Walker), North America Foliage, Fruit
redbanded leafroller
Choristoneura rosaceana (Harris), North America, South Foliage, Fruit
obliquebanded leafroller America
Cydia lobarzewskii Nowicki Europe Fruit
Cydia pomonella (Linnaeus), codling moth Worldwide Fruit
Epiphyas postvittana (Walker), light brown Europe, Australia/New Foliage, Fruit
apple moth Zealand
Grapholita molesta (Busck), oriental fruit Worldwide Fruit, Foliage, Twigs
moth
Grapholita prunivora (Walsh), lesser North America Fruit
appleworm
Hedya dimidioalba (Retzius), marbled North America, Europe, Asia Buds, Foliage
orchard tortrix
Pandemis heparana Denis & Schiffermller, North America, Europe, Asia Foliage, Fruit
fruittree tortrix
Pandemis limitata (Robinson), threelined North America Foliage, Fruit
leafroller
Platynota flavedana Clemens, variegated North America Foliage, Fruit
leafroller
Platynota idaeusalis (Walker), tufted apple North America Foliage, Fruit
budmoth
Proeulia auraria (Clarke), fruit leaf folder South America Foliage, Fruit
Pseudexentera mali Freeman, pale apple North America Foliage, Fruit
leafroller
Sparganothis sulfureana Clemens, North America Foliage, Fruit
Sparganothis fruitworm
Spilonota ocellana (Denis & Schiffermller), North America, Europe, Asia Foliage, Fruit
eyespotted bud moth
Tortrix capensana (Walker) South Africa Foliage, Fruit
Orthoptera: Gryllidae
254
A Apple Pests and their Management

Apple Pests and their Management, Table 9 Major insect and mite pests of apple (Continued)

Taxon scientific and common name Geographical distribution Plant parts affected
Oecanthus fultoni Walker, snowy tree North America Cambium, Wood, Twigs
cricket
Thysanoptera: Thripidae
Frankliniella occidentalis (Pergande), west- North America, Europe Foliage, Fruit
ern flower thrips
Taeniothrips inconsequens (Uzel), pear thrips North America, South Buds
America, Europe

into sap-feeders (instars 13) and tissue-feeders for sap-feeding mines should be done at approxi-
(instars 45). The second-generation adults mately 690degree-days (base 43F) after the start
begin emerging in early June in the northeastern of the flight of the second generation. On average,
states (average date is June 138 days), and lar- second-generation spotted tentiform leafminer
vae are usually present in early July. Third-gener- moths begin flying in early to mid-June. A decision
ation l arvae are usually present in late August. regarding the third generation is generally not
The spotted tentiform leafminer damages only required unless the density of the second brood
foliage, which the larvae eat and mine. This causes exceeds two mines per leaf.
reduced photosynthesis and possibly sequestered
nutrients. Foliar damage can cause smaller fruit
size, premature drop, and poor color. Damage Control
caused by the second generation is usually of the
greatest concern. Third-generation leafminers usu- Many parasitoids effectively limit spotted tentiform
ally are not a problem if the second generation was leafminer populations in some orchards. Most
controlled properly. important are the wasps Apanteles ornigis, Sympiesis
marylandensis, and Pnigalio maculipes. Insecticide
sprays applied in July and August probably do the
Decision Making most harm to these natural enemies. Some leaf-
miner pesticides are effective without being toxic to
A sequential sampling plan can be used to classify natural enemies such as mite predators. Depending
spotted tentiform leafminer egg density at the on the product chosen, application can be made any
pink stage or the density of sap-feeding mines time from initial egg deposition until the larvae
immediately after petal fall. Treatment is recom- enter the tissue-feeding stages.
mended ifeggs average 2 or more per leaf on leaves
2, 3, and 4 of a fruit cluster at the pink stage, or
if sap-feeding mines average 1 or more per leaf Obliquebanded Leafroller,
on these leaves at petal fall. Sampling can be Choristoneura Rosaceana (Harris)
completed in approximately 10 min.
Proper timing is essential for both the assess- Biology and Impact
ment of second-generation leafminer densities and
control, if required. If done too early, sampling The oblique banded leafroller prefers plants in the
will underestimate the population. If control is Rosaceae family but will feed on many unrelated
applied too late, it will not be effective. Sampling deciduous trees. This leafroller overwinters as a
 Apple Pests and their Management
A 255

second-or third-instar larva on the tree within average, summer-generation obliquebanded

closely spun cocoons or hibernacula. Larvae become leafroller moths start flying the first or second
active in the spring when buds begin to open. As week of June. The value of knowing the precise
foliage pushes from the buds, larvae oftentie leaves date of this event on a local basis cannot be over-
together and conceal themselves in the resulting emphasized. If information on adult moth flight is
chamber. Spring-generation moths emerge in early not available, July 5 to 10 is a rough approximation
June in the northeast, with peak activity in mid-June. of the appropriate sampling period in the north-
First-generation larvae complete their development east. At 600 DD after the start of the adult flight,
in late July or early August. Summer-generation populations can be classified according to whether
moths begin flying in early August. Second-genera- the average percentage of terminals infested with
tion larvae feed primarily on foliage, but may cause live larvae is greater than 3%.
surface injury to fruit if they are very abundant.
After feeding briefly, second-generation larvae enter
their winter hibernacula. Control
Spring-generation larvae may eat away large
portions of developing fruit. If the fruit survive, Several parasitoids attack the obliquebanded lea-
they are misshapen with large, deep cavities of froller, but their effectiveness in regulating leafrol-
healed-over injuries. Fruit damaged by first-brood ler populations in commercial orchards is largely
larvae generally falls off the tree. If not controlled, unknown. Most growers favor chemical sprays to
this spring generation of obliquebanded leafroller reduce damage caused by this insect. A contact
may cause only small fruit losses (24%). insecticide is sometimes applied at bloom to petal
The principal impact of summer-generation fall. Most orchards with a history of leafroller
obliquebanded leafroller is its feeding damage to infestation require 12 pesticide applications
the fruit. This generally occurs if a leaf is webbed against the second-generation larvae. Selective
to an apple or clustered apples touch each other. pesticides, including insect growth regulators and
Feeding areas on the fruit are shallow, irregular, those that are based on the bacterium Bacillus thu-
and may range from small punctures to large exca- ringiensis are compatible with IPM because they
vations. This injury is more serious than that are not toxic to natural enemies (especially mite
caused by the overwintering generation because predators).
most injured fruits remain on the tree.

European Red Mite, Panonychus

Decision Making ulmi (Koch)

During bloom or immediately after petal fall, Biology and Impact

spring-generation larval densities can be classi-
fied as above or below a treatment threshold The European red mite overwinters as an egg on
using a sequential sampling procedure. Treat- the tree. Egg hatch is usually closely correlated
ment is recommended if more than 3% of fruit with tree phenology, ordinarily beginning at the
spurs contain live obliquebanded leafroller early pink bud stage and continuing into bloom.
larvae. Sampling can usually be completed in If egg hatch does not coincide with the pink stage,
approximately 1015 min. it is usually delayed and starts during early bloom.
Sampling for the summer-generation larvae European red mite adults normally appear by
should take place approximately 600 DD (base petal fall, but few eggs are laid by the first genera-
43F) after the start of the first summer flight. On tion of adults on leaves until the first week after
256
A Apple Pests and their Management

petal fall. Early hatching European red mite for 10 days or 10mitesfeeding for one day. The
nymphs feed on older fruit cluster leaves and current economic threshold of approximately
may cause bronzing by petal fall if populations 550 total mite-days (for the growing season)
are high. Early season damage before petal fall is assumes that no significant accumulations of
usually insignificant, but some studies have mite-days occur before mid- to late June. Therefore,
shown that heavy damage in early to mid-June a protective prebloom oil treatment is currently
can reduce yields during the next season. recommended for control of early season European
In the summer months, the European red red mites.
mite damages apple leaves by inserting its mouth- During the summer, the need for a miticide
parts to feed on plant juices. This injury reduces to control the European red mite can be deter-
the capacity of the leaf to use sunlight as an mined from a sample of the mite population in an
energy source (photosynthesis), which may lead orchard. A sampling procedure is available that
to reduced yield and fruit quality. Recent studies determines mite presence based on examination
of European red mite impact have found that the of leaves of intermediate age. This procedure
only effect of moderate European red mite injury divides mite populations into three categories:
during the mid- to late season was a reduction in greater than threshold, below threshold, and much
the color of some red varieties of apples. These below threshold. The last two categories provide
results have identified the densities of mites that an indication of when the population must be
can be tolerated at various times of the growing sampled again. If the density is much below
season. threshold, the population should be sampled in
1116 days. If it is minimally below threshold, it
should be sampled again in 610 days. If mite
Decision Making predators are present, these intervals can be
lengthened by approximately 50%.
The natural mortality of overwintering eggs can Sampling involves recording on a chart the
besubstantial but is highly variable (10to 60%). presence or absence of mites in distinct samples
Therefore, sampling or rating schemes are gener- of leaves and continues until a decision on
ally not used for predicting the potential early whether to treat them can be reached. From petal
season severity of the European red mite in fall until June 30, a threshold of 2.5 mites per
commercial orchards by assessing the density of leaf is used. From July 1 to 31, the threshold is 5
overwintering eggs. During late bloom and petal mites per leaf. From August 1 to 15, a threshold
fall, the European red mite is concentrated on of 7.5 mites per leaf is used. Treatment for mites
older fruit cluster leaves, and therefore the over- is not currently recommended after mid-August.
all density of the first generation will be overesti- Adherence to these thresholds will prevent
mated by counting mites on theoldest leaves at serious injury.
that time.
Early control of the European red mite is
essential to prevent early season damage during Control
the postbloom period. One method used to quan-
tify mite presence is the mite-day concept, The European red mite is an induced pest in com-
which measures the number of mites and the mercial apple orchards. This means that pesticides
period of time they are present on the leaves. One used against other arthropods usually destroy
mite-day is equivalent to an average of one mite naturally occurring mite predators, allowing
feeding on a leaf for one day. Thus 10 mite-days European red mite numbers to increase to
can be accrued by one mite feeding on a leaf damaging levels. Several major predators of the
 Apple Pests and their Management
A 257

European red mite may be found in commercial conserve it. Because A. fallacis remains in the tree
orchards, depending on the part of the country year-round, even early season applications of
where they are located: pyrethroids are damaging to it.

Typhlodromus pyri (Scheuten) Metaseiulus occidentalis (Nesbitt)

Adults of T. pyri, a major predacious mite species, Predominantly found in drier climates such as the
are present in the tree at about the time of the northwestern states, this predator can also provide
European red mite hatch. These predators con- biological control of the European red mite in com-
trol low to moderate densities of European red mercial apple orchards. It has high reproductive
mites but do not regulate high populations. This and prey consumption rates, and disperses readily
mite predator is very effective against the European into orchards. However, it requires the presence of
red mite and when present in substantial num- an alternative prey population in the orchard, such
bers it will eliminate the need for chemical mite as apple rust mites, to preserve its population num-
control. T. pyri spends its entire life in the tree, bers when red mites are at low levels.
overwinters as an adult female, and is active by
bloom. It prefers to feed on the European red
mite but will sustain itself on other food sources. Zetzellia mali (Ewing)
Once established in an orchard, if it is not dis-
rupted by pesticides, T.pyri will keep European This minute yellow mite is present in nearly all
red mite populations to densities of less than one orchards, overwintering as a gravid female in con-
mite per leaf year after year. It may take two to cealed parts of the tree. Although it prefers older
three years for T. pyri to become abundant in an rust mites and the eggs and immature stages of
orchard once a selective pesticide regimen is European red mites and two spotted spider mites, it
adopted. feeds on all stages of these species. It undoubtedly
helps to control European red mites but is of little
benefit if it is the sole predator species present.
Amblyseius fallacis (Garman)

A. fallacis is also an effective predator of the Stethorus punctum (Leconte)

European red mite, but its continued presence in
the tree from year to year is not reliable. It over- This small, black ladybird beetle feeds on several
winters both in apple trees and in the ground small arthropods, including European red mites.
cover beneath them. Ground cover, however, It is more common in orchards in the middle
appears to have little influence on number and Atlantic states. Success in controlling European
movement of A. fallacis in the tree. A. fallacis was red mites depends on keeping a relatively high
previously believed to a poor biological control population of European red mites in the tree
agent because it did not move into the trees until (35mites per leaf).
late in the growing season after the European red For chemical control during the early season,
mite had reached problem levels. More likely, petroleum oil is often recommended (a 2% solution
A. fallacis numbers often remain low until late in at the half-inch green bud stage or 1% at the tight
the season because pesticides toxic to them are cluster stage) as an early season IPM program. Oil is
used early in the season. If a site has a history of relatively safe to predators, relatively economical,
A. fallacis, pesticides should be managed to and European red mite populations have never
258
A Apple Pests and their Management

shown resistance to it. Furthermore, a thorough overwintering adults remain active for two to six
application of oil applied before foliage is fully weeks after petal fall.
developed can kill nearly all the eggs present. Other Although adults may feed on blossoms, apples
early season treatment options include contact are not susceptible to damage until petal fall, at
miticides or ovicides applied at the pink bud stage which time adults damage fruit by both feeding
or at petal fall. Miticides will likely cover less of the and ovipositing. Unlike fruit injured by other pests,
foliage present by this time, and most are able to be many apples damaged by plum curculio will remain
overcome by the development of resistance in local on the tree until harvest. Because adults are not
mite populations, so this is a less desirable highly mobile, orchards near overwintering sites,
alternative. woodlands, and hedgerows are most susceptible to
Relatively few miticides can control Euro- attack. Fruit damage is usually most common in
pean red mite during the summer. The available border rows next to sites where adults overwinter.
contact miticides must be chosen by their indi-
vidual performance traits, including their activ-
ity against specific mite stages and beneficial Decision Making
arthropods, rate of action and length of residual
effectiveness, optimal application conditions for Monitoring for the plum curculio is not often rec-
each, and any possible resistance that may be ommended because of the amount of time and
exhibited by local mite populations. Because of labor involved and because it is generally assumed
the limitations of all contact miticides, good to be present in every orchard where populations
spray coverage is essential. are endemic. Nonetheless, various techniques have
Some research has been done on the use of been used to monitor plum curculio damage and
highly refined petroleum oils to control summer the presence of adults:
mite populations. Acceptable season-long control
has been achieved by using a multiple-spray pro- Clubs or shakers can be used to jar adults from limbs
gram starting at petal fall, followed by periodic into catching frames or cloths for counting.
monitoring throughout the summer. Potential dif- Polyethylene funnels hung under branches can be
ficulties with this approach include leaf damage used to capture adult PC.
and incompatibility with some of the fungicides Immature scout apples hung in trees near the edges
used to control summer diseases. of orchards serve to measure oviposition scars
before petal fall so potential damage can be esti-
mated before control sprays are applied.
Plum Curculio, Conotrachelus Oviposition scars on immature fruit can be counted
nenuphar (Herbst) in orchards starting at petal fall to estimate dama-
ge. Because substantial oviposition and damage
Biology and Impact can occur even after a single warm day and night,
frequent scouting for damaged fruit is necessary
Plum curculio adults move into orchards from after petal fall.
overwintering sites in hedgerows or the edges of
woods and are present in the trees from the late
pink stage to early bloom before the fruit is sus- Control
ceptible to damage. Adults are active in the spring
when temperatures exceed 60F. Adult females Several species of wasps parasitize the eggs and
oviposit in fruit during both day and night but larvae of the plum curculio. Ants, lacewings, and
feed mostly at night. Depending on temperature, ground beetles prey on larvae in the soil, and some
 Apple Pests and their Management
A 259

fungi kill larvae. These organisms are not usually Adults from the second or summer generation
sufficient to regulate populations of plum curculio of codling moth start to fly about mid-July, and the
in commercial orchards. peak flight occurs around the first week in August.
The plum curculio is difficult to control com- Larvae from this generation are active in fruit through-
pletely with insecticides. Relatively high rates out August. Fruit damage by second generation larvae
andpersistent applications are important because is generally more serious than that of the first.
adults may be active for two to six weeks after
petal fall depending on temperatures. Several
commercial products are available to control this Decision Making
insect. In normal orchards that are not near wood-
lots or hedgerows and have not suffered previous Adult males can be captured in pheromone traps,
damage, a single application at petal fall will pro- but numbers of males captured in these traps
vide seasonal control. In problem orchards, a petal cannot be related to potential fruit damage. Thus,
fall application followed by a second spray 1014 pheromone traps are used only to monitor the
days later will provide adequate control. In seasonal activity patterns of adults within an area.
orchards with chronic problems, or in seasons It is not practical to monitor commercial apple
when adult activity is prolonged by unusually orchards for CM eggs or larval fruit entries
cool and wet weather, two cover sprays applied because of the theoretical zero tolerance for
1014 days apart after petal fall may be necessary internal fruit damage. Developmental models,
to prevent late damage. Research on heat unit based on temperature accumulations after the
accumulation and plum curculio oviposition has first catch of males, can be used to predict the
proposed that control sprays are no longer neces- first egg hatch of codling moths. This approach is
sary whenever the last spray has been applied used to time initial control sprays for the codling
within 1014 days after the accumulation of 340 moth at 250360 DD (base 50F) after first adult
DD (base 50F) from petal fall. catch for the first generation, and 12601370 DD
after this same biofix date for the second
generation.
Codling Moth, Cydia pomonella
(Linnaeus)
Control
Biology and Impact
The codling moth is attacked by both parasites
The codling moth overwinters as a larva in a and predators, but these natural enemies can-
cocoon under loose bark on the tree trunk. not effectively control this pest in commercial
Adults emerge during bloom, and the first flight orchards. To kill the larvae before they enter
continues until about 30 days past petal fall. the fruit, chemical sprays for the codling moth
Eggs, laid singly on the upper surface of leaves must be initiated before the eggs hatch. The
or fruit, start to hatch at petal fall and continue codling moth is most effectively controlled by
for two to three weeks. Larvae feed only on fruit. the same conventional insecticides used against
Surface bites, referred to as stings, cause blem- the plum curculio, but it can also be controlled
ishes, and deeper injuries are caused by feeding by more selective pesticides such as bacteria
inside the fruit. Fruits injured by extensive (Bacillus thuringiensis), insect growth regula-
internal feeding usually drop in the middle of tors, viruses, and botanicals, although many of
June at which time early season damage becomes these products are less effective than standard
noticeable. insecticides.
260
A Apple Pests and their Management

Apple Maggot, Rhagoletis Theoretically, there is absolutely no tolerance

pomonella (Walsh) for apple maggot damage in fruit. In practice, apple
maggot damage is not usually detected in normal
Biology and Impact fruit inspections unless there is approximately 3%
fruit damage.
The apple maggot overwinters as a pupa in the soil.
Adults from the single annual generation of flies
emerge in late June to early July. Females cannot lay Control
eggs until they become reproductively mature, 710
days after emergence. Females lay eggs in fruit and the Small wasps parasitize apple maggot larvae in
larvae develop there, emerging in the autumn after fruit, and predators such as birds and crickets
the fruit has fallen and entering the soil to pupate. may eat larvae or pupae in or near the soil. In
Flies are active from July to mid-September, but com- natural, unsprayed apple and hawthorn trees,
mercial orchards require protection only from about apple maggot populations are not regulated by
mid-July through August. Flies do not reach orchards natural enemies. Parasites and predators are also
in large numbers until mid-July, and before this date, ineffective at controlling apple maggot in com-
fruit remaining on the tree is unfavorable for larval mercial orchards.
development so early infestations do not cause Apple maggot flies have a limited migratory
sustainable populations in the orchard. In addition, capability, so all apple and hawthorn trees within
for unknown reasons, fly activity between late August 1/4 to 1/2 mile of commercial orchards should be
and mid-September generally does not result in seri- removed if possible. Dropped fruit should not be
ous damage in most commercial orchards. allowed to remain beneath the tree for more than
Larval tunneling inside fruit causes it to become one or two days. Eliminating fruit drops will break
rotten and unmarketable. Early stings caused by the life cycle of flies in an orchard by preventing
punctures from female ovipositors may severely larvae from exiting the fruit and entering the soil.
deform the fruit of some varieties, even though no Apple maggot flies can be trapped in small,
larvae survive. well-pruned trees that are not near large sources of
outside infestations. A relatively high density of
sticky red spheres (plain or volatile-baited) is
Decision Making required, approximately 1 trap per 100 apples.
Mass trapping is usually less effective than chemi-
Monitoring to determine whether control sprays cal control, and apple maggot may still damage
are necessary is recommended only in orchards that 15% of fruit from mass-trapped orchards.
are not near large sources of outside infestation, such Most commercial orchards have no indige-
as abandoned orchards or those with no indigenous nous populations of flies. Therefore, chemical
infestations of flies. In early to mid-July, red sphere control sprays are usually directed against flies
traps baited with apple volatile lures are hung in immigrating into orchards from outside, unsprayed
trees along the edge of the block closest to an aban- hosts, including both apples and hawthorns.
doned orchard or a stand of woods. These traps are Most broad-spectrum insecticides are remarkably
checked one to two times per week. A spray of a suit- effective in controlling adults. Insecticides must
able insecticide is applied if a cumulative average of kill females before they oviposit in the fruit. Resid-
35 apple maggot flies per trap is captured. After ual effectiveness of insecticides is particularly
spraying, trap catches are not checked again until important in controlling apple maggot in com-
after a 10 to 14-day period, during which spray resi- mercial orchards when flies are continuously
dues would kill any immigrating flies. immigrating.
 Aquatic Entomology and Flyfishing
A 261

References Apterae
Helle W, Sabelis MW (1985) World crop pests, vol 1: spider Wingless forms, usually used in reference to wing-
mites: their biology, natural enemies and control. less parthenogenetic female aphids.
Elsevier, Amsterdam, The Netherlands
Metcalf RL, Metcalf RA (1993) Destructive and useful insects: Aphids
their habits and control, 5th edn. McGraw-Hill, New
York, NY, pp 1073
Minks AK, Harrewijn P (1987) World crop pests, vol 2: aphids: Apteropanorpidae
their biology, natural enemies and control. Elsevier,
Amsterdam, The Netherlands
Pimentel D (1991) CRC handbook of pest management in A family of insects in the order Mecoptera.
agriculture, vol 3. CRC Press, Boca Raton, FL Scorpionflies
Robinson AS, Hooper G (1989) World crop pests, vol 3: fruit
flies: their biology, natural enemies and control. Elsevier,
Amsterdam, The Netherlands
Van der Geest LPS, Evenhuis HH (1991) World crop pests, vol Apterous
5: Tortricid pests: their biology, natural enemies and
control. Elsevier, Amsterdam, The Netherlands A term used to denote that the insect is lacking
wings.
Apple Proliferation
This is an important insect-transmitted mollicute Apterygote
(bacterial) disease of apples in Europe.
Insect taxa that do not possess and never pos-
Transmission of Plant Diseases by Insects
sessed (in evolutionary time) wings. A member of
the class Insecta, subclass Apterygota.
Apple Rust Mite, Aculus
Schlechtendali (Acarnia:
Eriophyidae) Apystomyiidae

This is an important apple pest in some areas. A family of flies (order Diptera).
Four-Legged Mites Flies
Mites
Apple Pests and their Management
Aquatic Entomology and
Flyfishing
Apposition Eye
john r. wallace, frank d. l. rinkevich
A type of compound eye found in diurnal insects Millersville University, Millersville, PA, USA
in which the ommatidium is shielded bypigment.
This type of eye is also called a p
hototopic eye. The use of aquatic insects as lures for fish dates back
to the second century a.d. In the seventeen volume
Appressorium treatise, De Animalum Natura, the Roman Aelianus
discussed his observations of fish consuming insects
The swollen tip of a fungal hypha that facilitates at the water surface and how Macedonian fishermen
attachment to the host, and penetration by the used dry flies or spinners to catch what were thought
fungus. to be trout from the Astraeus River. Not until fifteen
262
A Aquatic Entomology and Flyfishing

centuries later did Charles Cotton propose the utility Semi-aquatic orders are largely terrestrial with a
of aquatic insects in fishing. In 1836, Alfred Ronalds number of families exhibiting life stages in or near
Fly Fishers Entomology was published. This publica- water. Coleoptera (beetles), Diptera (flies), and
tion elaborated on fly tying methods and fishing Lepidoptera (butterflies) represent semi-aquatic
techniques from an entomological perspective. Most orders.
recently, fly anglers are attempting to increase their Typically, anglers refer to an emergence of
knowledge about insects, specifically aquatic insects, insects (but more specifically to those with aquatic
in terms of imitating fish food items or matching the larval stages) as a hatch. What the angler will
hatch. This quest for entomological knowledge by calla nymph, the entomologist would refer to as
anglers, in addition to aquatic scientists and fish the larval stage of an insect. Mayflies are the only
managers, has prompted the need for better taxo- group of insects that have a non-reproductive
nomic and ecological treatments friendly to both the adult stage (the subimago); anglers refer to this
scientist and the angler. In order to create a functional stage as duns. Post-ovipositing mayflies typi-
artificial imitation of an insect to improve ones cally die with their wings spread on the water
chances of catching a trophy fish, the angler requires surface, and anglers term these spinners, refer-
basic identification, ecological and behavioral infor- ring to the spinning action they exhibit while
mation of both insects (prey) and fish (quarry). floating on the water surface. In addition, anglers
refer to reproductively mature insects that end
their life cycle on the water surface either by
Terminology: Entomology Versus nature or that accidentally hop, fly or are blown
Flyfishing onto the water surface as dry flies. Fly patterns
will mimic the larval and adult stages of both ter-
As with many fields of scientific study, understand- restrial and aquatic insects.
ing the complexities of both entomology and fly The sports angler often refers to insects by a
fishing requires an understanding of both lan- number of colloquialisms. Educated fishermen
guages. While the term fly fishing technically often use the term caddis or caddisfly in reference
refers to only one insect order, Diptera, in reality it to the order Trichoptera, fishflies for Megaloptera,
encompasses all insect and non-insect inverte- and sandflies for some Diptera. Mayflies are
brates used as food by fish. Representatives from known by a variety of names such as drakes or
several orders of terrestrial insects (e.g., upwings.
Hymenoptera, Orthoptera, Diptera, and Lepi-
doptera) are common food items of fish and are
mimicked with artificial flies. However, aquatic Morphological Importance
insects are the primary interest of anglers and are
the majority of fly patterns mimicked. For exam- Although the standard mantra of the dedicated
ple, there are thirteen orders of insects that are fly angler is that the three most important aspects
classified as aquatic. Only 3% of all insects have a to catch fish are presentation, size and pattern,
life stage in an aqueous environment. Some of anglers must be familiar with many aspects of
these orders are entirely aquatic whereas others insect morphology. Most often, hand-tied flies
have a few semi-aquatic representatives. Truly incorporate the obvious features of the insect
aquatic orders are those in which all of their mem- they are imitating. For many mayfly presenta-
bers exhibit some portion of their life cycle in an tions, large characteristics such as wing size, cau-
aquatic habitat. The orders, Ephemeroptera (may- dal filaments, and body color are considered
flies), Plecoptera (stoneflies), and Trichoptera when tying flies. Small traits such as specific seta-
(caddisflies) are examples of truly aquatic orders. tion, paraglossae, and tarsal segments are often
 Aquatic Entomology and Flyfishing
A 263

ignored largely due to their size relative to the the natural life cycle of the native insects. A sample
insect and the investment of time that would be taken with a kick seine or observation of emer-
spent including these features in a fly. A fish will gences will indicate what type of fly to use. An
not recognize these small features because, at emergence of mayflies in the summer is the rea-
times, they may see the lure for only a few son why an adult mayfly mimic presented on the
seconds. surface may outfish a wetfly of a caddisfly. Several
Flies fit into two general classes based on aquatic insect orders are often used as models for
their presentation. Dry flies are presented on the fly tying and as live bait. There are many fly imita-
surface and signify the adult stage. Wet flies are tions of caddisflies, mayflies and stonefly larvae
fished below the surface and represent larvae. (Fig.71), as well as aquatic Diptera larvae and
Success of the presentation is largely dependent adults, due to their ecological importance of pro-
on the time of the year. Presentation should mimic viding food for fish.

Insect Fly Imitation

A.

May Fly Dun (Subimago) Sidewinder No Hackle Dun

B.

Stone Fly Larva Rubber-Legged Stone Fly Nymph

C.

Adult Midge Adult Midge

D.

Emerging Dun Emerging Dun Imitation

E.

Adult Caddis Fly Hen Caddis

Aquatic Entomology and Flyfishing, Figure 71 A collection of common aquatic insects used as
mimics for wet and dry artificial fly patterns. (A, C, D, and E=represent dry flies; B represents a wet fly
or nymph). Illustrations by Mike Gouse (published in Swisher D, Richards C (1991) Emergers. Lyons &
Burford Publishers, New York, NY).
264
A Aquifer

Ecological and Behavioral References

Importance
Hafele R, Roederer S (1995) An anglers guide to aquatic
Though fly fishing strategists argue over imitation insects and their imitations for all North America.
Johnson Books Publisher, Boulder, Colorado, 182 pp
vs. presentation, fly fishing tactics that employ eco- McCafferty PW (1983) Aquatic entomology. Jones and Bar-
logical and behavioral aspects are as important as tlett Publishers, Boston, MA, 448 pp
using a fly pattern based on the appearance of natu- Merritt RW, Cummins KW (1996) An introduction to
ral insects. Although insect abundance is important, the aquatic insects of North America. Kendall/Hunt
Publishing, Dubuque, IA, 862 pp
fish will not eat the most abundant insect if it is not Swisher D, Richards C (1991) Emergers. Lyons & Burford
available to them. Three ecological aspects impor- Publishers, New York, NY, 120 pp
tant in the availability of a particular insect include:
stage of development, habitat use and activity (either
associated with drift or foraging for food). Aquifer
Although aquatic insect larvae are most abun-
dant after hatching, they are not as available as fish An underground formation of sand gravel or
food due to their small size and ability to avoid preda- porous rock that contains water. Aquifers are an
tors. In terms of energetics, a small insect is equivalent important source of water is some areas, and must
to small energetic payoffs. However, as aquatic insects be protected from pesticide contamination, affect-
grow and develop from one stage to the next they ing the type of pesticides and pesticide application
become more obvious to fish predators through their technologies that are used.
feeding activities. Thus, availability increases as insects
grow and develop. Emergence for aquatic insects is a
risky task. It is these emergers that are most available as Aradidae
they struggle to reach the water surface, plant stem or
emergent rock from which they attempt to emerge as A family of bugs (order Hemiptera). They some-
adults. Fish will concentrate feeding efforts on emerg- times are called flat bugs.
ing insects if the adult stage escapes quickly. Those Bugs
adult insects, both terrestrial and aquatic, that expire
on the water surface are readily fed upon by fish.
Aquatic insects inhabit a wide variety of micro- Arbovirus
habitats within a given stream or pond, including
rock or log surfaces, on plant stems or other sub- Viruses transmitted by arthropods. This is an acro-
merged vegetation, as well as swimming openly in nym for ARthropod-BOrne VIRUSes.
the water column. Habitat use by aquatic insects is
relative to their needs. For example, foraging for food
may put an insect in a different microhabitat other Archaic Bell Moths (Lepidoptera:
than used during non-feeding periods. Some may- Neopseustidae)
flies may exhibit this behavior switch. Diel feeding
activities among Phantom midges (Chaoboridae) john b. heppner
also is an example of this type of behavior. Finally, Florida State Collection of Arthropods, Gaines-
phenological aspects of aquatic insect activity related ville, FL, USA
to emergence, drift and oviposition increase insect
availability. Some of these ecological/behavioral phe- Archaic bell moths, family Neopseustidae,
nomena are tied to weather changes, lunar activity, include nine known species (six from Southeast
water temperature and current regime. Asia and three from Chile). The family forms a
 Arctics
A 265

monobasic superfamily, Neopseustoidea, and the only members of the superfamily Eriocran-
the only member of the infraorder Neopseustina, ioidea, which form the infraorder Dacnonypha
of the suborder Glossata and subcohort of the suborder Glossata. There are two subfam-
Myoglossata. Adults small (1427 mm wing- ilies: Acanthopteroctetinae and Catapteriginae.
span), with head roughened; haustellum short, Adults small (1116 mm wingspan, with rough-
with vestigial mandibles; labial palpi 3-seg- ened head scaling and only short 2-segmented
mented and somewhat upcurved; maxillary labial palpi; maxillary palpi are 5-segmented
palpi 5-s egmented; antennae are mostly rather and folded; haustellum is reduced and vestigial
long and somewhat thickened. Maculation is mandibles are present. Maculation is more som-
pale, usually translucent with gray spots, and ber than in Eriocraniidae and adults are thought
wing shapes rather broad and quadrate. When to all be diurnal. Larvae are blotch leafminers
resting the wings are held in a rounded shape on Ceanothus (Rhamnaceae) in the single known
that resembles a bell. Adults are crepuscular or biology.
diurnal. Biologies and larvae remain unknown,
but species in Chile are thought to possibly feed References
on native bamboos.
Davis DR (1969) A review of the genus Acanthopteroctetes
with description of a new species (Eriocraniidae). J Lepid
References Soc 23:137147
Davis DR, Frack DC (1987) Acanthopteroctetidae (Eriocran-
ioidea). In: Stehr FW Jr (ed) Immature insects, vol 1.
Davis DR (1975) Systematics and zoogeography of the family Kendall/Hunt Publishing, Dubuque, IA, pp 345347
Neopseustidae with a proposal of a new superfamily Zagulajev AK, Sinev SY (1988) Catapterigidae, a new familyof
(Lepidoptera: Neopseustoidea). Smithsonian Contribu- lower Lepidoptera (Dacnonypha). Entomol Obozrenie
tions to Zoology 210:145 68:593601 [in Russian] (English translation 1989:
Davis DR (1997) Neopseustidae. In Lepidopterorum Catalo- Entomol Rev 68:3543)
gus, (n.s.). Fasc. 7. Association for Tropical Lepidoptera,
Gainesville, p 8
Davis DR, Nielsen ES (1980) Description of a new genus
and two new species of Neopseustidae from South Archeognatha
America, with discussion of phylogeny and biological
observations (Lepidoptera: Neopseustoidea). Steen-
strupia 6:253289
An apterygote order of insects, also called
Microcoryphia. They commonly are known as
bristletails.
Bristletails
Archaic Sun Moths (Lepidoptera:
Acanthopteroctetidae)
Archipsocidae
john b. heppner
Florida State Collection of Arthropods, A family of psocids (order Psocoptera).
Gainesville, FL, USA Bark-Lice, Book-Lice or Psocids

Archaic sun moths, family Acanthopterocteti-

dae, are very similar to Eriocraniidae, and Arctics
include only four species, all North American
except for one in the Palearctic (originally Some members of the family Nymphalidae, sub-
described in a separate family Catapterigidae). family Satyrinae (order Lepidoptera).
The family, plus the related Eriocraniiidae, are Butterflies and Moths
266
A Arctiidae

Arctiidae The area-wide pest management strategy

includes several substrategies including (i) manage-
A family of moths (order Lepidoptera). They com- ment of the total pest population in all of an ecosys-
monly are known as tiger moths, footman moths, tem, (ii) management of the total pest population in
or wasp moths. a significant part of an ecosystem, (iii) prevention,
Tiger Moths which includes containment of an invading
Butterflies and Moths population and quarantine, and (iv) eradication of
an entire pest population from an area surrounded
by naturally occurring or man-made barriers suffi-
Arculus ciently effective to prevent reinvasion of the area
except through the intervention of man.
A small cross vein of the wing. The position of
the cross vein (Fig.72) varies among orders, but
is associated with the cubitus vein. Characteristics of Area-Wide Pest
Wings of Insects Management

Immigration of pests into a managed ecosystem

Area-Wide Insect Pest prevents their eradication. However, it is easy to
Management underestimate the tremendous impact of the
immigration of pests from small untreated foci
waldemar klassen into a managed area. For example, very few cod-
University of Florida, Homestead, FL, USA ling moths, Cydia pomonella (L.) develop in the
well managed commercial apple orchards, but
Area-wide pest management is one of several researchers found that the number of codling
major plans or strategies for coping with pest moths that overwintered in the in Wenas Valley of
problems. Management of localized populations Washington State dropped by 96% when a few
is the conventional or most widely used strategy, abandoned orchards and neglected noncommer-
wherein individual producers, other operators cial apple trees were either removed or sprayed
and households practice independent pest con- with insecticide. This study indicated that most of
trol. However, since individual producers or the codling moths in commercial orchards origi-
households are not capable of adequately meet- nated on untreated host trees that in aggregate
ing the challenge of certain very mobile and were <5% of the host resources of the codling
dangerous pests, the area-wide pest management moth. Similarly, experience in coping with the
strategy was developed. pink bollworm, Pectinophora gossypiella Saunders,

Arculus, Figure 72 Front wing of a dragonfly (Odonata).

 Area-Wide Insect Pest Management
A 267

and cotton boll weevil, Anthonomus grandis Bohe- generations will achieve greater suppression than
man, have shown that a few growers who do not a higher level of control on most, but not all, of the
destroy crop residues immediately after harvest population, each generation. Therefore, it is very
provide the food required by these pests to repro- important to eliminate any places of refuge or foci
duce and to enter diapause. This lapse in field sani- of infestation from which recruits could come to
tation can directly cause the occurrence of re-establish damaging densities of the pest popu-
devastating levels of these pests in the following lation in areas of concern.
season on neighboring farms. For the most part, the control of many highly
The implications of allowing a small fraction mobile and very destructive pests is carried out
of a population of a major pest species to repro- by individual producers who rely heavily on the
duce without control can be seen graphically use of insecticides. Although other control tech-
(Fig.73). E. F. Knipling calculated that over a period nologies are often incorporated into the produc-
of a few generations more pest individuals would ers integrated pest management (IPM) system,
be produced if 1% of the total population were these technologies, too, are usually applied by
allowed to reproduce without control, while 100% producers independently of other producers. Such
control was applied to 99% of the population, than an uncoordinated farm-by-farm IPM strategy
if only 90% control was imposed uniformly on the provides opportunities for the pest population
total population. Thus, Knipling elaborated the tobuild up and to establish damaging infestations
basic principle of total population suppression: in well-managed fields. Consequently, on most
Uniform suppressive pressure applied against farms insect pest populations increase to damaging
the total population of the pest over a period of levels each year, and the farmer is forced to apply

99% CONTROL OF 90% CONTROL OF

90% OF POPULATION 12.5+ TOTAL POPULATION
INSECTS
MIL

UNTREATED
POPULATION
1

TREATED
TREATED

0
1 2 3 4 1 2 3 4
GENERATION

Area-Wide Insect Pest Management, Figure 73 Results of a model that show that outcome of neglecting
to suppress a small fraction of a pest population in an agroecosystem versus the effects of uniformly
suppressing the entire pest population. On the left, 10% of the population is untreated and it produces a
large number of individuals in four generations, while the 90% of the population that is treated declines.
On the right, the entire pest population in the agroecosystem is suppressed uniformly and its n umbers
decline from generation to generation. (After Knipling, 1972. Reproduced with permission of the
Australian Journal of Entomology.)
268
A Area-Wide Insect Pest Management

broad-spectrum fast-acting insecticides as a res- involves less planning, tends to be reactive, and is
cue treatment (Table 10). This defeats the primary implemented independently by individual opera-
goal of the IPM system, which is to take maxi- tors or households. The area-wide strategy tends
mum advantage of naturally occurring biological to utilize advanced technologies, whereas the con-
control agents. ventional strategy tends to rely on traditional tac-
Moreover, application of insecticides when an tics and tools that can be reliably implemented by
insect pest population reaches the economic non-specialists.
threshold does not prevent the losses that occur The use of separate organizations to conduct
before the threshold has been reached. For com- area-wide programs provides opportunities to
modities that are planted on vast areas, such losses utilize sophisticated technologies and profes-
in aggregate are immense. For example, the world sional management. Computer-based models are
production of corn (maize) is roughly 600 million utilized in planning and management. Satellite
metric tons. Avoidance of a loss of 3% would make imagery is used in area-wide programs to identify
available 18 million metric tons, which could be a localities of alternate hosts that can be treated to
major factor in alleviating hunger. Some examples reduce pest populations that produce migrants
of crop losses caused by insects. that cause the damage in commercial production
Area-wide pest management differs from the areas. Area-wide programs acquire or develop
conventional pest management of local pest popu- highly sensitive detection systems, and employ
lations in several important ways. The area-wide geographic information systems software to
strategy focuses on managing the insect popula- help manage data. They may implement appr
tions in all of the niches in which they occur, while oaches to prevent or retard the development
the conventional strategy focuses narrowly on of insecticide resistance or loss of host plant
protecting the crop, livestock, people, buildings, resistance. Computer programs and real-time
etc., from direct attack by pests. The area-wide environmental data to predict insect popula-
strategy requires detailed multiyear planning and tions can be effectively used in an area-wide
an organization dedicated exclusively to imple- program but usually not on an individual farm
menting the strategy. The conventional strategy basis. Thus, pest immigration patterns, analysis

Area-Wide Insect Pest Management, Table 10 Percent crop losses in the USA caused by various insect
pests without and with control measures
Percent loss
Commodity Pest Without control With control
Bean Helicoverpa zea 37.0 6.0
Bean (snap) Epilachna varivestis 20.0 9.9
Beet (sugar) Tetanops myopaeformis 22.7 8.2
Corn (field) Diabrotica spp. 15.7 5.0
Corn (field) Ostrinia nubilalis 2.0
Corn (field) Helicoverpa zea 2.5
Cotton Helicoverpa zea 4.0
Cotton Pectinophora gossypiella 35.5 10.0
Peanut Helicoverpa zea 3.0
Soybean Pseudoplusia includens 15.7 4.8
Sugar cane Diatraea saccharalis 28.6 8.0
 Area-Wide Insect Pest Management
A 269

of weather to predict increase or decreases of management. The total costs of pest detection
populations, genetic analysis to determine and monitoring and suppression per hectare of
resistance levels, etc., are utilized in area-wide crop usually decline as the size of the managed
programs. area increases. However, the per hectare organi-
Finally, area-wide programs are able to zational costs usually increase as the project size
take advantage of the power and selectivity of increases because of the increased need for meet-
specialized methods of insect control that for ings and other communication costs. For these
the most part are not effective when used on a reasons, in very large programs such as the effort
farm-by-farm basis. These include the sterile to eradicate the cotton boll weevil from the USA,
insect technique (SIT), certain programs of the vast area was subdivided into a number of
inundative releases of parasites, semiochemi- zones. Also, considerable organizational cost sav-
cals, mating inhibitors, large scale trap crop- ings may be realized in instances where towns,
ping, treatment of hosts on public lands and in municipalities or cooperatives already have
private gardens, etc. structures in place for communication, decision-
making, collection of fees, etc.

Benefits of Area-Wide Pest

Management Contingencies Often Dictate
Changes in Strategy
Experience has shown that pest suppression on an
area-wide basis can be more effective than on a Contingencies often arise that require replacement
farm-by-farm basis for reducing losses caused by of one strategy with another. For example, at vari-
highly mobile pests and for capturing the benefits ous times during the 43-year campaign to remove
of highly mobile natural enemies. Area-wide pro- the screwworm from the United States, Mexico
grams enable many producers to pool resources in and Central America, different pest management
order to utilize technologies and expertise that are strategies had to be selected. This program began
too expensive for individual producers. These may when an unusual series of frosts beginning early in
include mass rearing facilities, aircraft, informa- December 1957 killed all screwworms in the
tion technologies and highly trained specialists. In southeastern USA north of a line in southern
addition, a coordinated area-wide program can Florida from Tampa to Vero Beach. Sexually ster-
achieve the avoidance or internalization of exter- ile flies from a culture in a research laboratory
nal costs. External costs (externalities) are the were released in a broad band north of this line to
harmful effects arising from pest control opera- contain the pest population while a high capacity
tions that affect parties other than the pest control rearing facility was being readied. This contain-
ker, but for which no compensation is paid to the ment strategy was replaced by the strategy of erad-
persons harmed. For example, spray drift onto ication in the summer of 1958 when the mass
neighboring properties frequently provokes dis- rearing facility was able to produce 50 million
putes. Also, pesticide use to protect agricultural sterile flies per week, and eradication was accom-
crops has caused insecticide resistance to develop plished in 1959.
in insect vectors of disease. A similar change of strategies was employed
Finally, economies of scale can be captured in in eradicating the screwworm from west of the
area-wide programs, although complex trade-offs Mississippi River. Beginning in 1962, the parasite
may be involved. The more mobile the pest and population was strongly suppressed north of the
the more uniform the damage caused by the pest, U.S. border with Mexico, and the influx of flies
the larger can be the area under coordinated from Mexico was retarded by the release of
270
A Area-Wide Insect Pest Management

s exually sterile flies in a 130 km-wide zone along it, caused Canada, Germany and Austria-Hungary
the entire USA-Mexico border. (For political to prohibit the admission of American fruit and
reasons in 1966, the U.S. Secretary of Agriculture living plants beginning in 1898. This crisis led to
declared the screwworm to be eradicated from the passage, by the U.S. Congress, of a series of
the United States, even though it was obvious to eleven federal acts beginning in 1905 on quaran-
entomologists that unless the parasite was tine and the regulation of interstate shipments in
removed from northern Mexico, it would con- the USA. In 1999, most of these acts were consoli-
tinuously reinvade the United States.) However, dated into the Agriculture Risk Protection Act of
the eradication strategy could be implemented 2000. Indeed, most countries adopted legislation
soon after the governments of the USA and on: (i) prevention of the introduction of new pests
Mexico reached an agreement in 1972 to eradi- from foreign countries, (ii) prevention of spread
cate the parasite as far south as the Isthmus of of established pests within the country or state,
Tehuantepec. Operations against the screw- (iii) enforcement of the application of control
worm in Mexico began in 1974, and the last measures to prevent damage by exotic pests, to
screwworm case occurred in the United States retard their spread or to eradicate them. In many
in 1982. countries, the law allows people who wish to orga-
In the next phase, these containment and nize a program against a pest to hold a referen-
eradication strategies were employed to eradicate dum. If the referendum passes by a certain margin
the parasite from all of Central America to Panama, (usually 67%) then all parties at interest must
where a sterile fly barrier was established in2001. cooperate in the venture.
Currently, in Florida, the program to eradi-
cate citrus canker has been delayed for several
Legal Authority for Area-Wide Pest years. This pathogen is carried considerable dis-
Management tances on driving rains, and to achieve eradica-
tion, the Division of Plant Industry has found it
The legal authority needed for area-wide and other necessary to destroy all citrus trees within a radius
regulatory programs is still evolving. In about of 578 m from an infected tree. Homeowners in
1860, the grape phylloxera, Phylloxera vitifoliae urban areas, who do not understand the need for
(Fitch), was transported from the United States to such drastic action, feel that workers who enter
France. Within 25 years of its arrival, this insect residential yards and destroy citrus trees as part of
had destroyed 1 million hectares of vineyards or the eradication program violate their rights. Thus,
fully one-third of the capacity of France to pro- the Broward County Circuit Court has ruled that
duce grapes. In order to protect the German wine program employees must have a separate court-
industry, the government of Germany in 1873 issued warrant to enter each privately owned
passed the first law that provided for quarantines property. The need to apply for tens of thousands
and regulatory control of agricultural pests. Other of warrants has prompted the Florida Department
governments quickly followed the example set of Agriculture and Consumer Services to appeal
by Germany. In 1881 representatives of many this ruling. The outcomes of this and other
European countries met and developed a set of judicial proceedings are likely to more clearly
regulations governing the movement of grape define procedures that must be followed in con-
propagating material. ducting eradication programs, and the levels of
In about 1880 the San Jose scale, Aspidiotus reimbursement owed to affected homeowners.
perniciosus Comstock, was established in California. Unfortunately, the tensions between urban and
Its rapid spread throughout the country on nurs- rural populations caused by the adversarial nature
ery stock, and the failure of a program to eradicate of this process are likely to persist for many years.
 Area-Wide Insect Pest Management
A 271

Apathy, Outrage and Area-Wide property or field operations, the perception that
Pest Management endangered species may be harmed, etc.
Acceptance of risk by the public is more
Some of the programs conducted on an area-wide dependent on the publics confidence in the risk
basis, especially those aimed at eradication, have manager than on the quantitative estimates of risk
aroused opposition. The strategy of eradication consequences, probabilities and magnitudes. The
emerged just over one century ago as the brain- public confidence in the managers of an area-wide
child of Charles Henry Fernald of the University program is of paramount importance.
of Massachusetts. Under Fernalds leadership, In each area-wide program, a special effort
Massachusetts attempted to eradicate an intro- must be made to anticipate and identify those fac-
duced pest, the gypsy moth, Lymantria dispar L.,in tors that may be emotionally upsetting to various
an 11-year campaign from 1890 to 1901. Initially, people and to take preemptive actions to avoid or
the primary eradicant was Paris green spray. The mitigate adverse reactions. Public officials must be
use of Paris green, which suffered from modest kept apprised, effective two way communication
efficacy and phytotoxicity, had to be abandoned with the public must occur, surrogates of the public
because of adverse public reaction including must be included in oversight and decision-making
threats of violence and mass protests. processes, and referenda may have to be conducted
Those stakeholders who are not primarily to secure support and funding for the program.
concerned with the economic dimension of the
pest problem tend to be highly concerned with
ecological, environmental, social and human Invasive Pests, Global Trade and
health implications of area-wide programs. There- Area-Wide Pest Management
fore, leaders of area-wide pest management pro-
grams need to be highly sensitive to the perceptions The rapid globalization of trade in agricultural
and attitudes of the public toward certain program products, and increasing tourism, have dramati-
operations. Often, eradication efforts must be con- cally increased the spread of invasive harmful
ducted by the ground rules of the urban rather organisms. We have entered an era of an unprece-
than the rural setting. In programs to eradicate the dented level of travel by exotic invasive organisms.
Mediterranean fruit fly in California and Florida, The greatest harm being done by non-indigenous
members of the public strongly protested the aerial invasive organisms is occurring on islands, and
pesticide applications even if the same insecticide major pests are becoming established with increas-
was used without dissent for mosquito abatement. ing frequencies on all continents except, perhaps,
On the other hand, the same public generally has Antarctica. For about one century many countries
applauded the release of Mediterranean fruit fly have relied on inspection of arriving cargo and
sterile males. passengers at the port of entry as a primary exclu-
Normally the public is apathetic towards tech- sionary strategy. However, volumes of arriving
nological programs. However, certain factors cargo are doubling every 56 years, and it is not
inherent in programs and in the manner in which possible to increase similarly the human and other
they are managed can precipitate an almost resources devoted to inspection at ports of entry.
irreversible shift of the publics attitude from apa- Clearly exclusion at the port of entry is no longer
thy to outrage. A sense of outrage can be evoked sufficient to protect against exotic pests, even
by involuntary exposure to pesticide residues, though a number of emerging technologies are
imposed levies or fees, quarantines, right of tres- likely to facilitate safeguarding activities. Thus, in
pass, unfair and inequitable sharing of risks, costs order to stem the influx of exotic pests, it is impor-
and benefits, temporary loss of control of ones tant to shift primary reliance from exclusion at the
272
A Area-Wide Insect Pest Management

port of entry to off-shore actions, namely on pest security requirements of fruit importing coun-
risk mitigation in the areas of production and tries. Chile used the sterile insect technique to rid
elsewhere, certification at the point of origin, and the entire country of the Mediterranean fruit fly,
preclearance at the port of export. Ceratitis capitata (Wiedemann). By 1980 the entire
An important approach to offshore mitiga- country of Chile had become a medfly-free zone,
tion is the creation of pest-free areas. Indeed, and since then Chilean fruits in huge volumes
countries that export raw agricultural commodi- have entered the U.S. market without the need for
ties can effectively remove the threat of exotic any quarantine treatments. This has dramatically
pests to the importing country by creating and strengthened the economy of Chile. Now Argen-
maintaining pest-free areas. A pest-free area is one tina, Peru and other countries have sterile insect
that lacks a quarantine-significant pest species, technique programs that they hope will enable
and is separated from infested areas by natural or them to become fly-free zones with free access to
artificial barriers. There are two types of pest-free markets in southern Europe, Japan and the United
areas: (i) pest-free zones are large geographic States. Also Mexico has used the sterile insect
areas, such as the entire country of Chile, that is technique to get rid of the Mediterranean fruit
certified free of tropical fruit flies of economic fly.Indeed Mexico is ridding large sections of its
importance, and (ii) pest-free production fields, territory of all fruit fly species of economic im
that require the demonstrated suppression of portance. The Mexican states of Baja California,
quarantine pests to non-detectable levels. Area- Chihuahua and Sonora have been freed of all eco-
wide pest management is an important tool for nomically important species of fruit flies, so that
promoting safe trade and contributing as much as citrus, stone fruits, apples and vegetables are being
possible to the complementary goals of food secu- exported from these states without any posthar-
rity and economic security for all countries. vest treatment.
Requirements to establish pest-free fields of A more recent, highly significant develop-
crop production include a sensitive detection pro- ment has been the continuous area-wide release of
gram, suppression of the quarantine-significant sexually sterile male medflies over the Los Angeles
pest to non-detectable levels, strict control of the Basin and around high-risk ports in southern
fields, and safeguards to prevent infestation during Florida. This further reduces the risk of pest estab-
packing and transit to the port of export. For lishment in these port areas.
example, Florida is able to export grapefruit to
Japan by creating pest-free grapefruit groves in
about 22 counties. Regulatory experts from Japan Selected Episodes in the History of
inspect the entire process of production, packing Area-Wide Pest Management
and transit. Similarly fruit groves free of the South
American cucurbit fruit fly, Anastrepha grandis Migratory Locusts
(Macquart), have been created in Mossoro, Brazil
and Guayaquil, Ecuador. Migratory locusts probably were one of the plagues
The concept of pest-free fields based on bait that caused prehistoric man to attempt forms of
sprays and the sterile insect technique was pio- group or area-wide control. Because migratory
neered during the early 1960s against the Mexican locust swarms can be seen approaching from a
fruit fly along the Mexico-USA border Mexico. distance and descending onto crops, it seems likely
Also in the early 1960s, the Citrus Marketing that people banded together and used whatever
Board in Israel developed a concerted area-wide means at hand to stamp out as many as possible.
program against the Mediterranean fruit fly that No doubt invasions of armyworms, leafcutter ants
has been able to meet the certified quarantine and other insects caused people to cooperate in
 Area-Wide Insect Pest Management
A 273

combating them. In China, since 707 b.c., more on inducing epizootics by inoculating breeding
than 800 outbreaks of Locusta migratoria manilen- populations with selective pathogens. A difficulty
sis L. have been recorded along the floodplains of in implementing the proactive strategy and mov-
the Hwang, Huai and Chang Jiang rivers. In 1929, ing toward the outbreak prevention strategy is that
an outbreak devastated 4.5 million hectares of donor support tends to wane in the absence of full-
cropland. Consequently, about 120 million people blown plagues.
were mobilized to modify the floodplains by dam-
ming, terracing and reforestation. Over almost
30 centuries, the Chinese slowly developed an Insect Vectors of Human Diseases
area-wide pest management program that now
folds together knowledge of biology, ecology, fore- Doubtless the scientific pioneers of area-wide
casting cultural practices, and water management. approaches were influenced strongly by concepts
During the late 1920s, catastrophic locust from the field of public health and hygiene.
plagues were widespread in Africa and southwest About 2,500 years ago the Greek spirit and the
Asia. Boris Uvarov and Zena Waloff of the British Roman capacity for organization had produced
Ministry of Overseas Development responded a highly developed system of hygiene in what is
by establishing the International Unit of Locust now southern Europe. The Romans procured
Research. This Unit became the Antilocust safe supplies of water by means of aqueducts,
Research Centre and it provided the focal point practiced daily bathing and removed garbage
for international cooperation in coping with from cities. The rationale for these measures was
plagues of the desert locust, the red locust and the explained by Varro (11627 b.c.), who served
African migratory locust. The Centre created data- Pompey and Julius Caesar. Varro asserted that
bases and provided a sustained regular flow of minute living creatures cause malaria. He wrote:
information on the status of locust populations In damp places there grow tiny creatures, too
throughout their ranges. The Centre developed a small for us to see, which make their way into
system of monthly forecasting. Uvarov was able our bodiesand give rise to grave illness. How-
to interest the FAO in creating the International ever, with the collapse of the Roman Empire and
Desert Locust Information Service to coordinate the storms of folk-migrations, classical hygiene
forecasting and the planning of campaigns. Lead- eroded. Nevertheless, raging outbreaks of
ership in these vitally important functions has malaria, typhoid, typhus and bubonic plague
been assigned to the FAOs Locust Group. during the latter Middle Ages reawakened con-
In recent decades locust experts have attempted cepts of hygiene and public health. Doctors and
to shift the prevailing strategy from reactive to pro- public authorities joined forces to erect walls
active, and eventually to outbreak prevention. The against these plagues. Dr. Johann Peter Frank
reactive strategy initiates interventions after plague (17451821) had considerable success in per-
status has been reached in order to contain the suading the rulers of Europe during the late
magnitude of the damage. The proactive strategy 1700s and early 1800s to establish public hygiene
seeks to prevent the occurrence of plague status by policies and to enforce them vigorously. While
intervening against localized outbreaks. Proaction only a 21-year old student at the University of
requires early detection of bands and swarms, Strasbourg, Frank called for systematic action
preferably still in breeding areas, and prepositioning by the authorities to intervene in the lives of all
of locust campaign supplies. The outbreak preven- citizens in order to forestall or halt epidemics.
tion strategy seeks to intervene before the phase The discoveries of Pasteur, Koch and others on
shift from solitary to gregarious. Possibly the out- the nature of diseases were foundation stones for
break prevention strategy would rely substantially rational policies of public health.
274
A Area-Wide Insect Pest Management

Mosquito-Borne Diseases ercentage rose to 74 by 1970. Malaria eradication

p
was claimed in 37 countries, and the incidence of
Through collective action within communities, malaria had dropped dramatically in many coun-
even without an overall national plan and central tries. In Sri Lanka, the number of cases dropped
coordination, malaria in southern Europe and from more than 2.8 million per year to just 17 in
North America largely disappeared in consequence 1963, but then the effort floundered as WHO was
of education, the universal adoption of window unable to deal with the widespread hue and cry for
screens, destruction of habitats of Anopheles larvae local control. In 1969, the Global Program disinte-
and the treatment of all cases with quinine. grated. Soon DDT was banned in the United States
Investigations conducted in the late 1800s and and WHOs resources for malaria were reallocated.
in early years of the 1900s on the transmission by Malaria resurged to more than half a million cases
mosquitoes of deadly diseases led to widespread per year in Sri Lanka and to more than 100 million
use of area-wide programs. Yellow fever, dengue, cases worldwide.
filariasis and malaria were shown to be transmitted In 1969 and 1970, the Indian Council for
by various species of mosquito. In 1892 Howard, Medical Research and the WHO initiated several
and in 1900 Ross, began to recommend that the projects relevant to area-wide control. Unfortu-
habitat of mosquito larvae over extensive areas be nately, in 1974 these projects became the target of
either treated with kerosene or drained. These a press campaign by writers who feared that these
practices were first implemented in west Africa to projects were actually a USA-funded effort to
combat malaria, and soon adopted by communities develop methods of biological warfare. Because
in many countries. Mosquito abatement districts the government of India was unable to restore
were pioneered by John B. Smith in New Jersey. The confidence, the projects were terminated.
New Jersey Mosquito Extermination Association, Many authorities maintain that the area-
founded in 1912, provided the model for the organi- wide use of insecticide impregnated bednets is
zation and operation of area-wide mosquito abate- superior to house spraying for suppressing
ment districts of which there are about 260 in the malaria, that a considerable pool of effective
United States and a thousand or more worldwide. technology relevant to the application of the SIT
Yellow fever was wiped out in Havana, Cuba, against mosquito vectors was developed three
under the leadership of Dr. W. C. Gorgas, who in decades ago, and that area-wide programs against
1898 implemented a strict sanitation program to malaria vectors can move ahead as soon as the
prevent breeding of the disease vector, Aedes aegypti international community develops the political
L. Subsequently, Gorgas implemented a program in will to do so.
the Panama Canal Zone against Aedes aegypti and
Anopheles spp. vectors of yellow fever and malaria,
respectively. This highly effective program was key Onchocerciasis Control Program in
to the successful construction of the Panama Canal. WestAfrica
Because the Plasmodium pathogen requires
12 days to develop in the mosquito vector before it River blindness is caused by the microflilariae ofthe
can be transmitted to man, residual sprays can Nematode Onchocerca volvulus, and is transmitted
sufficiently reduce the proportion of mosquitoes by the Simulium damnosum species complex of
that survive 12 days, and so interrupt malaria black flies. People and blackflies are alternate hosts
transmission. Therefore, in 1955 the World Health of this parasite, and it has no other hosts. The female
Assembly urged WHO to lead and organize world- parasite lives in the human skin and gives birth to
wide eradication of malaria. By 1959, almost 65% the microfilariae for most of her lifespan of 12 years.
of the people at risk were protected and this Microfilariae may invade the human eye, and
 Area-Wide Insect Pest Management
A 275

lindness typically sets in between the ages of 30

b training and coordinates devolution activities
and 39 years. A number of small-scale larviciding with participating countries.
operations against the vectors were mounted begin- The limits of the program area were extended
ning in 1950, and beginning in 1960 the European several times because of invasions of infective
Development Fund financed a major campaign in a black flies over greater distances than initially
60,000-km2 zone at the intersection of Mali, Burkina foreseen. Thus the program area expanded from
Faso and Cote dIvoire (Fig.74). 654,000 km2 in 1974 to 1,066,000 km2 by 1990.
In 1974 the international community ap Two intervention tactics have been employed
proved the Onchocerciasis Control Program and area-wide: larviciding largely by helicopter but also
the World Health Organization was designated as manually where streams are overgrown with vege-
Executing Agency. In order to manage the Pro- tation, and treatment of humans with the micro
gram, National Onchocerciasis Committees were filaricide, ivermectin. Because the period of
established in the seven participating countries development from egg to pupa rarely exceeds
(Benin, Burkina Faso, Cote dIvoire, Mali, Niger 1week, larviciding must be carried out on a weekly
and Togo). A Joint Programme Committee has basis. Seven insecticides are employed on a rota-
served as the supreme governing body and tional basis to prevent the development of resistance.
receives guidance from an Expert Advisory Com- In order to achieve the proper concentration of insec-
mittee. A Committee of Sponsoring Agencies ticide in the flowing water, an automated hydrological
coordinates the activities of the World Bank, FAO, surveillance network was created and real-time data
WHO and UNDP. The Onchocerciasis Fund was are fed to an on-board computer to enable the pilot to
created to accept donations, and the World Bank properly manage spray operations.
oversees it. The results of the program have been dramatic
The Programme Director is assisted by seven (Fig.75). As a result of this program, 25 million hect-
units: Office of Director, Administrative Manage- ares of land suitable for cultivation have become
ment, Epidemiological Evaluation, Vector Control, available, and rapid resettlement is underway. Because
Applied Research, Biostatistics and Information vector control operations were phased out in 2002,
Systems and Devolution. The latter conducts ivermectin remains as the only means of control.

Area-Wide Insect Pest Management, Figure 74 The original area of the Onchocerciasis Programme
established in 1974 and the subsequent western and southern extensions required to exclude migration
of the black fly vectors. (After World Health Organization, 1994.)
276
A Area-Wide Insect Pest Management

120

110 Vector control

100
Prevalence of infection
90
Prevalence of blindness

% of pre-treatment value
80 CMFL
Prevalence of adult female worms
70
Annual Transmission Potential
60

50

40

30

20

10

0
1970 1990 2010 2030 2050

Area-Wide Insect Pest Management, Figure 75 Actual and projected impact of 15 years of suppressing
black fly vectors of Onchocerciasis in the West Africa Programme. Reproduced from World Health
Organization, 1994. CMFL is the community microfilarial load (geometric mean of microfilarial levels in
all people in a given community).

Chagas Disease Vectors Chile, Paraguay, and Uruguay) plus Peru. This
10-year program was launched in 1991 under
Chagas disease, first recognized in 1909, has the leadership of the Pan American Health
been ranked as the most important parasitic Organization with funding, in part, from the
disease in the Americas. Although the infection European Union. Total program costs were esti-
is still largely incurable, transmission can be mated at US$190 million to $350 million. The
halted by (i) eliminating the domestic vectors, programs tremendous technical and economic
blood-sucking reduviids of the subfamily Tri- success (internal rate of return of 3060%
atominae, and (ii) screening blood donors to largely based on savings in health costs) spurred
avoid risk of transmission through transfusions. a similar Central America Initiative (El Salva-
Small-scale vector control programs began dur- dor, Guatemala, Honduras and Nicaragua) and
ing the 1940s based on spraying the interior of an Andean Pact Initiative (Colombia and
homes with benzene hexachloride or dieldrin to Venezuela).
control the primary vectors, Triatoma infestans Each program began with a centrally man-
(King) and Rhodnius prolixus (Stahl), as well as aged attack phase of about 3 years in which all
several other species of Triatoma. However, homes are sprayed by trained professionals, fol-
these programs suffered from under-funding lowed by a more community-based phase, which
and interruptions of funding, so that reinfesta- relies substantially on the efforts of homeowners
tion occurred. and local authorities. Adventitious transmission
In 1983 a national program was launched in may be accomplished by sylvatic vector species,
Brazil to eliminate the primary vector, Triatoma which can enter houses to form domestic colonies.
infestans, based initially on use of benzene In addition, migrant workers and other travelers
hexachloride and later on pyrethroids. Although can carry vectors. Currently, vector populations in
not without difficulties, this Brazilian program Mexico and the Amazon Basin remain as major
proved to be highly successful, and it inspired challenges. Elsewhere, the focus is shifting to epi-
an area-wide program encompassing the South- demiological surveillance and care of people
ern Cone countries (Argentina, Bolivia, Brazil, already infected.
 Area-Wide Insect Pest Management
A 277

Cattle Ticks c enturies, people began to understand the roles of

natural enemies in preventing insect outbreaks. Fur-
The discovery in 1889 by Theobald Smith and ther, the powerful synthetic insecticides were not
colleagues that cattle fever is caused by a tick- available to allow small holders independently to
transmitted parasite of red blood cells led to the protect their crops and livestock. The beneficial work
initiation in 1906 of a county-by-county effort to of coccinellids and other predators had been com-
eliminate the two Boophilus tick vectors (Fig.76) mon knowledge for centuries, and they were col-
from the United States. Many pastures were ren- lected and distributed for insect control. Insect
dered tick-free by excluding all host animals until parasitism was discovered only around 1700 by Leu-
all ticks had starved to death. Livestock were wenhoeck in the Netherlands and in 1706 by Val-
dipped in an arsenical solution at 2-week intervals. lisnieri in Italy. Emperor Francis 1 of Austria ordered
Quarantines were used to prevent the movement Vincent Kollar to publish his work on the role of
of infested cattle into areas that had been cleared. natural enemies insuppressing pests. Kollars great
By 1943, after 37 years of grueling effort, the ticks work appeared in1837 and the English translation
had been eliminated entirely from the United appeared in Londons Gardners Magazine in 1840.
States for a total cost of about $40 million dollars, E. F. Knipling has analyzed the potential
or the equivalent of the annual losses suffered contributions of parasitoids to area-wide pest
before the program was initiated. Quarantines suppression. Parasite augmentation could be an
have been effective in preventing these ticks from especially desirable preventive measure because the
becoming re-established from their populations in release of host specific parasites poses no danger to
Mexico. A broadly shared vision sustained this humans, beneficial organisms, or the environment.
program in spite of war and the great economic Highly misleading conclusions have been drawn
depression. from past augmentation experiments, because the
experiments were done in small non-isolated areas.
Most pest arthropods and parasites or predators are
Contributions of Natural Enemies highly mobile. Therefore, meaningful results can be
obtained only if augmentation experiments are
Area-wide pest management began to be practiced conducted over large areas. Even though many
widely during the nineteenth century using natural species of natural enemies have developed effi-
enemies. During the eighteenth and nineteenth cient host finding by following odor plumes of

1907 1915

1935 1943

Area-Wide Insect Pest Management, Figure 76 Progress in eradicating Boophilus ticks in the United
States, 19061943.
278
A Area-Wide Insect Pest Management

kairomones emanating from the host, under natu- c lassical biological control program in history. In
ral conditions the level of parasitization does not 1973, cassava near Brazzaville and Kinshasa was
threaten the host with extinction. Augmentation found to be attacked by the cassava mealybug,
utilizes the host resources in nature to produce large Phenacoccus manihoti (Matile-Ferrero). In a few
numbers of parasite progeny. If done properly, par- short years immature crawlers were dispersed by
asite augmentation for several generations can wind throughout sub-Saharan Africa.
become a self-perpetuating suppression measure. The cassava mealybug created starvation
Augmentation causes progressive increases in the and hardship for many of the 200 million people
rate of parasitism with each succeeding parasite for whom cassava had become a staple crop. In
generation, provided that the initial rate of parasit- 1981, an excellent parasitoid, Epidinocarsis lopezi
ism is above 50%. In addition, a host-dependent (DeSantis), found in Paraguay by A.C. Bellotti,
species will tend to distribute itself proportionally proved capable of bringing the cassava mealy-
to the distribution of its host. No other method of bug under control. The parasite was mass-reared
insect control has the characteristic of concentrat- and released by aircraft over 38 countries
ing its suppressive action where it is most needed. (Fig.77) of sub-Saharan Africa (an area much
larger than the combined area of the United
States, Mexico and India) with excellent results.
Lasting Suppression of Cottony Cushion This singular accomplishment required strong
Scale by Vedalia Beetle and imaginative leadership and action by IITA,
generous funding by donors, and brilliant scien-
That classical biological control can provide area- tific and technical work by Herrens team and
wide solutions was dramatically illustrated against their cooperators in Africa, Europe, and the
an exotic pest in California in 1888 and 1889. At Americas.
that time an introduced pest, the cottony cushion
scale, Icerya purchasi, was killing hundreds of thou-
sands of citrus trees. However Albert Koebele Area-Wide Conservation of Predators
was able to introduce a scale predator, the vedalia ofthe Brown Planthopper
beetle, Rodolia cardinalis (Mulsant), from Australia
and New Zealand. Less than 11,000 vedalias were In many cases, natural enemies are effective only if
distributed, but they spread throughout the entire most smallholders in an area work to conserve
citrus growing area of southern California and saved them. Because both pests and natural enemies are
the industry. The vedalia beetle continues to effec- mobile, their populations distribute themselves
tively protect citrus in California, and nothing needs throughout the region in which their food sources
to be done other than to avoid the use of certain are available. Even smallholders who do not par-
insecticides, which would decimate this invaluable ticipate in the conservation program receive some
natural enemy. of its benefits. They get a free ride, and for them
this is a positive externality of the program. On the
other hand, the movement of natural enemies off
Lasting Suppression of Cassava Mealybug the property of the participating farmer to that of
by Epidinocarsis lopezi the free rider is a negative externality.
The brown planthopper, Nilaparvata lugens
Almost exactly 100 years after the great vedalia (Stl), has been the scourge of rice production in
success, a team led by Dr. Hans Herren of the southeast Asia for many years. However, during
International Institute for Tropical Agriculture the 1980s, Indonesia (with technical assistance
(IITA) successfully implemented the largest from FAO and Germanys GTZ) simultaneously
 Area-Wide Insect Pest Management
A 279

Libya
Egypt Quatar
Western Sahara Algeria
Saudi Arabia
Oman
Mauritania
Mall
Niger
Eritrea Yemen
Chad
Gambia, Th Burkina Faso Sudan
Djibouti
Benin Nigeria Ethiopia
Ghana Central
Togo African Republic
Somalia
Gabon
Uganda
Kenya
Congo
Rwanda
Zaire Burundi
Tanzania United Republic of

Cassava Mealybug Angola

Zambia
Epidinocarsis lopezii
Parasite
Zimbabwe Mozambique
Madagascar
Botswana
Namibia
Casava Belt
Swaziland

South Africa

Area-Wide Insect Pest Management, Figure 77 Biological control of the cassava mealybug in
sub-Saharan Africa by mass rearing a parasite from Paraguay and distributing it by air over 38 countries.

achieved substantial increases in rice production When 70% of smallholders participate, they
and major reductions in insecticide use. Generally, gain almost 60% and the free riders gain about 40%,
brown planthoppers are effectively controlled by and when 90% participate, they gain about 83%
indigenous spiders and other predators. Moreover, ofthe potential benefit, while the free riders gain
since insecticides have a greater impact on the 66%. Clearly, a conservation program is almost
predators than on the pest, the brown planthopper futile until about one-half of the smallholders
populations are able to resurge after being sprayed. participate, and the program becomes progres-
In the past, farmers induced resurgence by begin- sively more beneficial as the percent participation
ning to spray at 40 days after transplanting the increases toward 100.
rice. However, cage studies showed that the small-
holder who delays spraying until 65 days after
transplanting saves two insecticide applications, Bark Beetles
and realizes a yield increase of about two tonnes,
for a total benefit of US $588 per hectare. Dendroctonus pine bark beetles are dangerous
It is possible to model what happens when pests in forestry because of their mass attacks on
some smallholders delay spraying to conserve nat- healthy trees. During the first decades in the twen-
ural enemies but others do not. If about 10% of tieth century, foresters focused on destroying the
smallholders conserve natural enemies, they gain developing broods of potentially destructive
only one-fifth of the potential benefit. If 30% of beetles before they could emerge and attack valu-
smallholders conserve natural enemies, they gain able trees. This was implemented by felling dead
only one-quarter of the potential benefit, and the trees, peeling and burning the bark or by storing
free riders gain about 7%. When 50% of small the infested logs in millponds until they could be
holders conserve natural enemies they gain one- sawed into lumber. The futility of such attempts by
third of the potential benefit, and the free riders focusing directly on killing beetles became appar-
gain about 18%. ent when, in 1932, an extremely cold winter
280
A Area-Wide Insect Pest Management

occurred and destroyed at least 80% of the beetles In 19711973, a large pilot field experiment
in western North America. The destruction of the to assess the feasibility of eradication was cen-
beetle broods by frost was more complete, exten- tered in southern Mississippi. The eradication
sive and uniform than could be accomplished by zone was surrounded by three buffer zones. Very
forest managers. Yet, within 2 years the beetle intensive suppression was implemented in the
populations had resurged and were again killing two inner zones, and farmers were expected to
ponderosa pine on a vast scale. practice diligent control in the outer zones,
However, forest entomologists recognized although some grew cotton simply to qualify for
that the most vulnerable trees were those that government payments and with no intention to
lacked vigor or were in decline. Thus, in 1937 con- harvest a crop. Only one application of the sup-
trol of bark beetles based on susceptibility of trees pressive system was made, because of a shortfall
to attack was pilot tested in California by a pro- in appropriations. Nevertheless, the boll weevil
gram called sanitation-salvage logging. In this was suppressed below detectable levels in 203 of
approach, up to 20% of trees at highest risk of bee- 236 fields in the eradication zone. All of the 33
tle attack were removed and sawed into lumber. lightly infested fields were located in the north-
During the first year following the removal of the ern one-third of the eradication zone and less
most vulnerable trees, losses to bark beetles were than 40 km from substantial populations farther
reduced by 90%, and losses remained low for at north. In the southern two-thirds of the eradica-
least 10 years after the selective logging. tion zone, no reproduction could be detected in
any of the 170 fields. Knipling and some others
concluded that the available technology was suf-
Boll Weevil Eradication in the USA ficiently effective to achieve eradication. Their
experience with the screwworm indicated that
E. F. Knipling, with the support of the National eradication could be accomplished iteratively,
Cotton Council, was determined to eradicate the following an application of the suppressive sys-
boll weevil from the United States because the wee- tem that clears the pest from most of the target
vil necessitated the use on cotton of one-third of the zone. Next, surviving populations are delimited
insecticides used in U.S. agriculture. Also, highly and similar suppressive measures are applied to
insecticide-resistant boll weevil populations had them. In this iterative fashion, the aggregate range
emerged. Newsom and Brazzel, at Louisiana State occupied by the pest is progressively reduced
University, had discovered that in the fall of the year toward zero. However, some felt that the technol-
the boll weevil enters a reproductive diapause and ogy was not adequate to mount an eradication
hibernates in trash along the edges of cotton fields. campaign, unless a single application of the sys-
Brazzel showed that the number of weevils surviv- tem of suppression eliminated all weevils in the
ing the winter is reduced 90% if insecticides are target zone.
applied just before diapausing weevils leave the A Cotton Study Team appointed by the
fields. Moreover, Kniplings analysis showed that if National Academy of Sciences drafted a very
insecticide sprays were targeted also to kill the gen- negative interpretation of the results. Because
eration producing individuals going into diapause, Knipling was a member of the Academy, he had
then the number overwintering would be reduced access to this draft, and he wrote a strong rebut-
by more than 99%. Kniplings model was verified, tal. Therefore, the Cotton Study Team wrote a
and this ignited great interest in actually eradicating toned down statement that continued to express
the boll weevil. An effective pheromone-baited trap strong reservations about the feasibility of eradi-
was developed for detection. Weevils were sexually cating the boll weevil, but concurred to conduct a
sterilized with the anti-leukemia drug, busulfan. new trial eradication program in North Carolina.
 Area-Wide Insect Pest Management
A 281

Grudgingly the Academy team legitimized the geographical areas clearly defined by biologically
concept of continuing large-scale eradication based criteria. D. A. Lindquist wrote: An area-
experiments, but with the caveat that they would wide insect control program is a long-term
probably fail. planned campaign against a pest insect popula-
The new trial program, started in 1978 in tion in a relatively large predefined area with the
Virginia and North Carolina, was highly successful. objective of reducing the insect population to a
Subsequently, piece-meal programs, each run by a non-economic status.
separate foundation, have removed the boll Both of these definitions have considerable
weevil from about 5 million acres in Virginia merit and they fit the majority of area-wide pro-
and the Carolinas, Georgia, Florida, south Alabama, grams. However, slightly different definitions may
California, and Arizona. These programs have be needed to describe programs on the conservation
caused significant reductions in pesticide usage, of natural enemies (which can tolerate some free-
and the eradication efforts are continuing. Thus, the riders) and on classical biological control where the
job is about half done. However, the corrosive effect adaptation of the introduced biological agent to all
of the Academys report persists. The US Congress new environments cannot be known in advance of
reduced the share of federal funds from the tradi- making releases. Also, in programs to contain an
tional 50 to <30% of the cost. However, such cost invasive pest population, it may not be possible to
sharing is no longer guaranteed, and in 1997 the US clearly define the boundary of the pest population.
Department of Agriculture initiated a program of In the similar vein, A. T. Showler stated: Locust
making loans to officially recognized boll weevil swarms can be highly variable, influenced by many
eradication foundations. Moreover, the process of factors, including geography, vegetative conditions,
eradication is being conducted piece-meal with a land-use patterns, environmental sensitivity, avail-
minimum of technology. Pheromone traps are used ability of resources and tactics, prevailing winds,
to delimit infestations, and the attack begins with insecure areas, and rainfall patterns. Reliance on a
insecticides applied late in the growing season single control strategy is therefore unrealistic. A more
against weevil still reproducing and those entering appropriate approach would be to develop specific
diapause. As many as 15 insecticide applications per strategies that will fit with projected scenarios,
year are made against dense persistent populations. mostly by harmonizing them with national contin-
Planting by all growers is synchronized and delayed, gency plans. The common thread that runs through
short season varieties are grown, harvested as soon all area-wide pest management programs is the
as possible, and stalks are destroyed immediately strong emphasis on preventing the existence of any
after harvest. Eradication is usually accomplished places of refuge or foci of infestation from which
by the end of the third growing season. recruits can come to re-establish damaging densities
of the pest population in areas of concern.

Attempts to Sharply Define the

Area-Wide Pest Management Benefit-Cost Assessment and
Strategy Discounting Net Returns

A few scientists have attempted to sharply define Usually, investments in area-wide programs are
the area-wide pest management strategy. Knipling made with the expectation that program benefits
stated: Area-wide pest management is the sys- will accrue over a multi-year time horizon.
tematic reduction of a target key pest(s) to prede- Therefore, we must discount future benefits to bal-
termined population levels through the use of ance them against present or near term expendi-
uniformly applied control measures over large tures. The stream of discounted annual benefits
282
A Area-Wide Insect Pest Management

and costs for many years of an undertaking can be many developing countries, then it seem unlikely
summed up and expressed as a single value, known that vector control programs in these countries
as the present value net benefits (PVNB). The would ever be launched.
formula for calculating the PVNB for a 15-year
project is as follows:
Kniplings Imperative
PNVB = NB1 + w2NB2 + w3NB3 + w4NB4
+ w5NB5 + w6NB6 + wtNBt + w15NB15 When the World Food prize was awarded to
Knipling and Bushland, Knipling stated: If major
where NBt represents the net benefits in year t, advances are to be made in coping with most of
and wt represents the weighting factor for year t. The the major arthropod pest problems, then the
weighting factors are a function of a discount rate (r): tactics and strategies for managing such insects,
ticks and mites must change. They must change
1 from the current, limited scale, reactive, broad-
wt =
(1 + r)t spectrum measures to preventive measures that
are target-pest specific and rigidly applied on an
The discount rate is the opportunity cost of area-wide basis. Great and enduring strides can
the money, or the interest value that money could be made by adopting the strategy of area-wide pest
earn if allocated to the best alternative use. This management to help meet world food, health and
rate may be established by subtracting the national environmental challenges.
inflation rate from the bank interest rate for sav-
ings. In normal times, this procedure will generally
produce a figure around 4 or 5% in developed References
countries. This represents the reasonable persons
discount on the future, because people put their Klassen W (1989) Eradication of introduced arthropod pests:
money in the bank to gain this premium, and oth- theory and historical practice. Miscellaneous Publica-
erwise they would spend it now. So, the benefit of tions of the Entomological Society of America 73:129
Klassen W (2000) Area-wide approaches to insect pest inter-
eradication next year is worth 5% less if it is brought
ventions: history and lessons. In: Teng-Hong Tan (ed)
back to the present. Benefits in 20 years are only Joint Proceedings of the FAO/IAEA International Con-
worth 37% of their face value when brought back ference on Area-Wide Control of Insect Pests, May
to the present. In riskier economic environments, 28June 2, 1998, and the Fifth International Symposium
on Fruit Flies of Economic Importance, June 15, 1998.
discount rates will be much greater, so the calcu- I.A.E.A, Penerbit Universiti Sains Malaysia, Pulau,
lated net present value of future benefits may be Pinang, Malaysia, pp 2138
insignificant. However, for programs involving Klassen W, Lindquist DA, Buyckx EJ (1994) Overview
vectors of human diseases, the futures of groups of oftheJoint FAO/IAEA Divisions involvement in fruit
fly sterile insect technique programs. In Calkins CO,
people are at stake, and it does not seem appropri- Klassen W, Liedo P (eds) Fruit flies and the sterile insect
ate to discount benefits in the manner appropriate technique. CRC Press, Boca Raton, FL, pp 2138
for private investments. The health of the human Knipling EF (1979) The basic principles of insect population
suppression and management. USDA agriculture hand-
population 30 years in the future seems just as
book 512. Washington, DC, 659 pp
important as the health of the population at pres- Knipling EF (1992) Principles of insect parasitism analyzed
ent. Nevertheless, investments in vector control from new perspectives: practical implications for regu-
programs must be subjected to critical analysis in lating insect populations.USDA agricultural handbook
693. Washington, DC, 337 pp
the interest of efficient and sound management. Reichelderfer KH, Carlson GA, Norton GA (1984) Economic
However, if high discount rates (e.g., 25%) are guidelines for crop pest control. FAO plant production
selected commensurate with economic risk in and protection paper 58. FAO, Rome, Italy, 93 pp
 Argasid (Soft) Ticks (Acari: Ixodida: Argasidae)
A 283

Argasid (Soft) Ticks (Acari: most argasid ticks increase their body mass after
Ixodida: Argasidae) feeding by only 36-fold. The blood feeding time
of argasid ticks is much shorter than that of ixo-
igor uspensky dids, taking from several minutes to 12 h, and
The Hebrew University of Jerusalem, Jerusalem, male gorging taking 1.52 times less than that of
Israel females. In contrast, nymphal argasids feed in
much the same manner as ixodids; this is explained
The family Argasidae is second to the family Ixodidae by their capacity to create new cuticle during feed-
with regard to its medical and veterinary significance ing. Thirdly, adult ticks can gorge blood several
and the number of species. According to the novel times during their life, and can oviposit after each
classification based on a phylogenetic analysis of feeding. The maximal number of possible feedings
relationships at the generic to subgeneric level, the is unclear, though as many as nine feedings have
argasid ticks comprise four genera and about 185 been documented.
species, among which three genera are represented
by a large number of species: Carios (87 species),
Argas (57 species) and Ornithodoros (36 species, one Ecology
of which consists of three subspecies). The fourth
genus (Otobius) is represented by three species. Not Argasid ticks are spread over all continents (with
all researchers fully agree with the currently pro- the exception of Antarctica) but have been studied
posed systematic groupings of the family. This clas- very unevenly; in particular, there is insufficient
sification has its weaknesses but is considered information on this group in South America and
superior to traditional classifications. In any case, Australia. Both in the Palaearctic and the Nearctic,
further molecular taxonomic study is necessary. soft ticks inhabit regions with a hot climate, mainly
The main morphological difference between deserts, semi-deserts and southern savannas
argasid and ixodid ticks is the lack of the scutum (steppes, veldts, prairies), but some species pene-
in argasids; thus, they are called soft ticks. The trate as far north as 5055N. The maximum num-
lack of the scutum leads to the absence of such a ber of species and their greatest abundance are
clear sexual dimorphism in the adult stage of this known in foothill areas (300900 m above sea
family compared with ixodid (hard) ticks. The level), but some ticks can be found at higher eleva-
integument of the Argasidae looks wrinkled and tions (a maximum of 2,900 m above sea level for
leathery. The mouthparts are located on the ven- the cave tick Ornithodoros tholozani (Fig.78) in
tral side of the body, covered by the frontal margin the Pamirs).
of the body, and are invisible from above. Almost all species of argasid ticks are nidi-
There are a number of significant biological colous, i.e., they live in or near shelters of various
differences between soft and hard ticks. Firstly, kinds. Ornithodoros transversus is an exceptional
argasid ticks have several nymphal stages (instars), species that spends its entire life on the giant
varying from 2 to 8, usually from 3 to 6. The num- tortoises of the Galapagos Islands. Endophilous
ber of instars is not constant, and is controlled nidicoles inhabit bird and rodent nests, mammal
by exogenous factors such as the size of the burrows, and caves as well as stalls, poultry houses
blood meal and the ambient temperature during and farms. Harborage-infesting parasites live near
development. Secondly, nymphs and adults of nests or burrows, very often in rock or stone ledges
argasid ticks cannot engorge as much blood as as well as in human dwellings and temporary
ixodid ticks. The integument of adult argasids is human-made cabins in places of resting, hunting
strongly folded and capable of stretching during or fishing. In such shelters, ticks inhabit all kinds
feeding, but does not grow at that time. Females of of cover: cracks and crevices on walls, sandy or
284
A Argasid (Soft) Ticks (Acari: Ixodida: Argasidae)

number of eggs in each batch may fluctuate

widely. After each complete blood feeding, they
lay off-host from 50 to 200 eggs. If blood feeding
is not complete, the number of eggs laid dimin-
ishes proportionally. During its entire life, a
female can lay up to 1,200 eggs. Female oviposi-
tion depends on their insemination, which
occurs off-host, and can take place either before
or after feeding. Some cases of female insemina-
tion several months after feeding, followed by
oviposition, have been described. One mating is
sufficient for several ovipositions. Multiple
gonotrophic cycles have been recorded among
the Argasidae. There are some exceptions from
gonotrophic harmony when a female lays eggs
without feeding, using nutritional reserves
remaining after nymphal feeding.

Feeding Behavior

Argasid (Soft) Ticks (Acari: Ixodida: Argasidae), Several feeding nymphal instars and repeated
Figure 78 The cave tick, Ornithodoros tholozani. feedings in adult females allow us to describe the
Argasidae (with a few exceptions) as multi-host
dusty soil surface of burrows and caves, spaces ticks, though consecutive feedings may take place
between nest fibers, etc. Ambient conditions, such on the same host. Most argasid species feed on
as air temperature, relative humidity and light specific groups of hosts and, in a broad sense, can
intensity, are more uniform and suitable for ticks be considered specialists. Ticks of some subgenera
in shelters than in the surroundings; this enables of Argas parasitize birds available to them during
tick survival in extremely unfavorable areas. Being nesting or resting. The genus Carios contains
dependent on the hosts living in the shelters, the nearly all bat-associated argasids. When the ticks
ticks have developed different patterns of adapta- are offered unusual hosts, they either do not feed
tion, the main one being their unusual ability to at all or have some abnormalities in their meta-
persist without feeding. This is especially charac- morphosis after such feeding. An extreme special-
teristic of nest and burrow inhabitants because ization was observed in Cuban Carios natalinus
death of the host or migration to another habita- and C. tadaridae, which parasitize only bats of the
tion are common phenomena, whereas active genera Natalus and Tadarida, respectively. In con-
migration between shelters is not typical for most trast, such ticks as Ornithodoros erraticus, O. tarta-
argasid ticks except in several species parasitizing kovskyi, or O. tholozani must be considered
ungulates and hares. Under laboratory conditions, generalists. They can feed on any mammals, birds
unfed adult O. tholozani survived without feeding and reptiles available to them. Among exceptions
for more than 10 years and unfed adult Argas laho- are the one-host Ornithodoros transversus and the
rensis for as long as 18 years. two-host Otobius megnini and A. lahorensis. The
As a rule, females of argasid ticks are char- latter species demonstrates some characteristics of
acterized by gonotrophic harmony, though the exophilic ticks which are followed by adaptations
 Argasid (Soft) Ticks (Acari: Ixodida: Argasidae)
A 285

to hot xeric environments. This tick has an iapause also occurs in ticks parasitizing bats,
d
extremely high critical temperature of the epicu- which hibernate in cool caves. Photoperiod seems
ticle (61C in contrast to 42 to 54C in other spe- to be the main but not the only factor regulating
cies studied) and minimal water loss under low the induction and termination of diapause. A
RH. Among other adaptations are the develop- prolonged hunger is not considered diapause
ment on the host from larval attachment until even when it continues for several years.
engorgement of nymphs of the last instar with a The abundance of argasid ticks in their shel-
constant number of nymphal instars (3) and ters can be extremely high. A single cave inhab-
nymphal feeding at each instar for several days ited by bats may contain hundreds of thousands
which increases the blood meal size and, hence, of bat-parasitizing argasids. Cases have been
the number of eggs laid (300500). documented when seabirds abandoned their
A capacity of unfed argasid ticks to parasitize nests in the middle of the breeding season
and feed on engorged specimens of the same spe- because of enormous tick density. Especially high
cies presents an interesting phenomenon called tick density has been noted in abandoned habita-
homoparasitism (homovampirism, in Russian lit- tions of Central Asia. Such constructions are even
erature). Usually, unfed nymphs and males para- more dangerous than dwellings; the longer ticks
sitize engorged nymphs of late instars and females. are without hosts and the hungrier they become,
Unfed ticks prick the integument and gut walls of the more aggressively they attack occasional visi-
engorged specimens, and suck the gut contents. As tors. In past centuries special bug traps full of
a rule, such an operation is not followed by the hungry argasids were used by Central Asian rul-
death of the victim, so that this phenomenon can- ers for the torture of prisoners who died from
not be called cannibalism. This phenomenon has exsanguination by thousands of ticks. The capa-
been documented many times for a number of bility of argasid ticks to migrate varies depending
species of both Argas and Ornithodoros under on the habitation of a particular species. Endo-
laboratory conditions, but there are also a few philous nidicoles inhabiting nests, burrows and
observations from the field. Apart from this, feed- caves are usually considered non-migratory spe-
ing of unfed ticks on engorged specimens of other cies because the distance to the host is very short.
species has also been recorded. Harborage-infesting species can migrate over
Depending on the conditions of tick habi- larger distances measured in many meters. As in
tats, ticks have different forms of seasonal activ- the hard ticks, the migration toward a host is
ity. The seasonality is absent or weakly pronounced influenced by a spectrum of factors, such as CO2,
in ticksinhabiting shelters with a relatively stable host body heat, various odors, etc. However, the
microclimate. In the tropical zone, ticks attack effect of a single stimulus is weaker than for hard
hosts, feed and oviposit all year round according ticks, and the maximal effect has been observed
to observations on the African tampan Orni- when all stimuli worked together.
thodoros moubata. A similar pattern of activity Evolutionarily, the Argasidae are more primi-
was recorded on O. erraticus inhabiting the Nile tive than the Ixodidae. This primitivism is exem-
grass rat burrows in Egypt. In the subtropical and plified by a number of characteristics, such as
especially temperate zones, the seasonality in tick rather narrow ecological patterns, low capacity
activity is much better defined. Ticks feed and foractive migrations, existence of many nymphal
oviposit during the summer and have one or two instars, and slight morphological difference
gonotrophic cycles during this period. In the between the last nymphal instar and the adult
winter months, a morphogenetic diapause in the stage. These characteristics are considered typical
form of ovipositional delay takes place in argasid for more primitive forms among different groups
species that parasitize migratory birds. Such of the Arachnida.
286
A Argasid (Soft) Ticks (Acari: Ixodida: Argasidae)

Medical Importance are the main vectors of the African swine fever
virus, an acute contagious disease affecting
The medical significance of argasid ticks is mainly domestic pigs and several wild representatives of
determined by their participation in transmission the family Suidae. Epidemics of this disease have
of many species of Borrelia pathogenic to humans. occurred in many African countries, as well as in
These closely related bacteria are causative agents of some southern European-Mediterranean coun-
tick-borne relapsing fevers. Each species ofBorrelia tries, but also in Brazil and Central America
is transmitted by its specific tick vector. Borrelia (Cuba, Dominican Republic, Haiti). Ornithodoros
duttoni and its vector Ornithodoros moubata were coriaceus transmits Borrelia coriaceae, the caus-
the first combination of such kind recognized in ative agent of epizootic bovine abortion in the
Africa in the very beginning of the twentieth cen- western United States. Cattle, and especially sheep,
tury. The disease occurs in the central, eastern and densely parasitized by Argas lahorensis, may suf-
southern parts of the continent and humans are the fer from large losses of blood and often die. Some
primary reservoir host, which is unusual because in representatives of the genus Argas that are closely
other combinations, mammals, especially rodents, connected with poultry transmit destructive dis-
are the main reservoir hosts. More than 15 combi- eases of domestic birds. Fowl (or avian) spiro-
nations of Borrelia with particular species of argasid chetosis caused by Borrelia anserina affects
ticks are recently known worldwide. They occur in chickens, geese, ducks, turkeys, pheasants and
North, Central and South America, Africa, and the some other fowl and decorative birds. The fowl
Mediterranean area, including some European tick, A. persicus (Fig.79), the most important cos-
countries, the Caucasus, Asia from the Near East to mopolitan poultry parasite, is the main vector of
western China. In the western and southwestern the pathogen. The pigeon tick A. reflexus (and,
United States the following combinations have been
identified: B. hermsi-Ornithodoros hermsi, B. parkeri
-O. parkeri, B. turicatae-O. turicata, B. mazzottii-
Carios talaje. The ticks are capable of transovarial
and transstadial passage of Borrelia for many gen-
erations, as well as of prolonged preservation of
pathogens, even during prolonged hunger. The pas-
sage of pathogens from hungry to engorged speci-
mens as a result of homoparasitism has been proved
experimentally. Because tick vectors are nidicolous,
the human infection depends on human closeness
to tick habitation. Tick species inhabiting human
dwellings, such as Ornithodoros moubata and
O. tholozani, are especially dangerous vectors. In
other cases the infection takes place only when
humans intrude into tick shelters or settle them-
selves nearby.

Veterinary Importance

Some argasid ticks are also of veterinary importance. Argasid (Soft) Ticks (Acari: Ixodida: Argasidae),
Ornithodoros porcinus porcinus and O. erraticus Figure 79 The fowl tick, Argas persicus.
 Argasid (Soft) Ticks (Acari: Ixodida: Argasidae)
A 287

perhaps, other species from the A. reflexus group) increased dramatically during past decades. Such
also participates in transmission of the disease. reactions are typical for other members of Argas
The mode of transmission is unique for tick- reflexus group (e.g., for A. latus in Israel).
borne borrelioses, by contamination from infec- The most severe form of tick toxicosis is tick
tious tick feces. Transovarial passage of the paralysis, which only occurs after prolonged
pathogen has been proved. Fowl spirochetosis is feeding. In argasid ticks, the known cases of tick
spread worldwide: in North, Central and South paralysis were described only for larvae charac-
America, Europe, Australia and many regions of terized by prolonged feeding. Larvae of several
Asia and Africa. Argas persicus is also responsible Argas species cause paralysis of fowl with total
for transmission of a rickettsia, Aegyptianella pul- recovery after all larvae drop off the host. Paraly-
lorum, infecting some fowl. The disease is espe- sis and death of sheep and cattle caused by Argas
cially destructive for young chickens. Argas lahorensis has been reported from some Euro-
walkerae, whose adults transmit this disease in pean countries, Caucasus and Central Asia after
South Africa, also causes paralysis in chickens attachment of 100200 nymphal ticks of the
when its larvae feed on them. slow-feeding third instar.
A number of other human and animal patho-
gens have been isolated in nature from some species
of argasid ticks, but there is not enough data to Management of Tick Populations
consider such ticks as competent vectors. On the
other hand, some argasid ticks have been Personal prophylaxis is the basis of human protec-
successfully infected by different pathogens in the tion from argasid ticks. It is necessary to avoid rest-
laboratory, and maintained the pathogens for some ing and overnighting in sites where tick attacks are
time, but this also does not constitute proof of the possible. The most efficient method of tick eradica-
tick importance in transmission of the disease. tion in human dwellings is the improvement of
Nevertheless, the involvement of argasid ticks in dwellings so that ticks are deprived of possible
the transmission of other diseases is very possible. shelter. The maintenance of good sanitary condi-
tions in poultry houses and farms with limited use
of acaricides should maintain the abundance of
Human Response to Tick Feeding fowl ticks at a low level. The acaricidal treatment of
domestic animals infested by argasids is an effec-
Human skin reacts to argasid bites, sometimes tive mode of tick control. Some animal diseases,
rather severely. People are often insensitive at the such as African swine fever, can be eradicated either
time of the tick bite but later a strong itch appears by very severe quarantining of the infected herds
followed by scratching and the appearance of or by destroying the infected herds together with
ulcers. The strength of the human reaction the ticks infesting the animals. Only a small num-
depends on the tick species. Evidence of Orni- ber of pathogens, parasites and predators of argasid
thodoros tholozani bites may be in evidence for ticks are known, thus it is impossible to estimate
many months. Argas ticks living in towns and the prospects of their use for argasid tick control.
parasitizing pigeons often inhabit human
dwellings, even some apartments in many-story
buildings, and may cause allergic responses and References
toxicoses in humans. Many cases of anaphylactic
Balashov YS (1972) Bloodsucking ticks (Ixodoidea) vectors
reactions (sometimes even with fatal results)
of diseases of man and animals. Miscellaneous Pub
caused by bites of A. reflexus have been reported lications of the Entomological Society of America
in European towns where pigeon populations 8:163376
288
A Argentine Ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae: Dolichoderinae)

Filippova NA (1966) Argasid ticks (Argasidae). Fauna S.S.S.R.

Paukoobraznye, 4(3). Nauka, Moskva-Leningrad, p256.
(in russian)
Hoogstraal H (1985) Argasid and Nuttalliellid ticks as para-
sites and vectors. Adv Parasitol 24:135238
Horak IG, Camicas J-L, Keirans JE (2002) The Argasidae, Ixo-
didae and Nuttalliellidae (Acari: Ixodida): a world list of
valid tick names. Exp Appl Acarol 28:2754
Klompen JSH, Oliver JH Jr (1993) Systematic relationships in
the soft ticks (Acari: Ixodida: Argasidae). Syst Entomol
18:313331
Mans BJ, GotheR, Neitz AWH (2004) Biochemical perspec-
tives on paralysis and other forms of toxicoses caused by
ticks. Parasitology 129:S95S111
Obenchain FD, Galun R (eds) (1982) Physiology of ticks. Argentine Ant, Linepithema humile (Mayr),
Pergamon Press, Oxford, UK, 509 pp (Hymenoptera: Formicidae: Dolichoderinae),
Sonenshine DE (1991) Biology of ticks, vol 1. Oxford
University Press, New York, NY, 447 pp Figure 80 A foraging Argentine ant, Linepithema
Sonenshine DE (1993) Biology of ticks, vol 2. Oxford humile.
University Press, New York, NY, 465 pp
an unusually robust mesosoma, longer than the
gaster, that bears a distinctly concave posterior prop-
Argentine Ant, Linepithema odeal face.
humile (Mayr) (Hymenoptera: Much of the early literature about this species
Formicidae: Dolichoderinae) is found under the name Iridomyrmex humilis. The
change to current nomenclature occurred when
alex wild recent phylogenetic research revealed a number of
University of Arizona, Tucson, Arizona, USA new world dolichoderine species, including the
Argentine ant, to be unrelated to true Iridomyrmex,
Identification and Taxonomy a strictly Indo-Australian group.
Argentine ants belong to the subfamily Dolichoder-
inae, or odorous ants, characterized in the worker
caste by the presence of a single constricted peti- Distribution
olar segment, the lack of a sting, and a transverse
slit-like anal orifice. Worker ants (Fig.80) of the The natural distribution of Linepithema humile
genus Linepithema can be further recognized by (Fig.81) extends in the south from the Buenos
the combination of the anterior clypeal margin Aires province across Paraguay to the Pantanal in
bearing a medial concavity and a distinct mandib- the north, and is closely associated with major
ular dentition bearing a series of larger teeth inter- waterways in subtropical South Americas Paran
spersed with two to three small denticles. River drainage. This species typically inhabits
The Argentine ant is distinguished from all lowland forests and grasslands in the Paran and
other Linepithema species in the worker caste by a Paraguay floodplains.
lack of erect setae on the mesosomal dorsum, the In the eighteenth century, L. humile began to
presence of dense pubescence on the mesopleuron, appear elsewhere in the world, arriving on
large compound eyes comprised of 80110 omma- the Atlantic island of Madeira in the 1850s and
tidia, and the long antennal scapes that are as long or inthe southern United States and in Portugal inthe
slightly longer than head length. Worker ants are 1890s. In spite of its humid subtropical provenance,
uniformly reddish brown to dark brown and are this insect has been most successful invading Med-
between two and three millimeters in length. Linepi- iterranean climates. Thriving introduced popula-
thema humile males are unmistakable as they have tions are now found in California, Mexico, Hawaii,
 Argentine Ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae: Dolichoderinae)
A 289

Argentine Ant, Linepithema humile (Mayr), (Hymenoptera: Formicidae: Dolichoderinae),

Figure 81 Current distribution of Argentine ant, Linepithema humile.

Ecuador, Colombia, Chile, Peru, South Africa, Argentine ants possess a number of life his-
Japan, temperate Australia, New Zealand, numer- tory traits that facilitate colonization and possibly
ous Pacific islands, and throughout the Mediterra- pre-adapt this species as a globally successful
nean region. Occasional populations persist invader. First, Argentine ant colonies have a large
indoors in northern Europe and North America. number of fertile queens, in some colonies run-
Microsatellite evidence suggests that atleast some ning into the thousands. This polygyny increases
of these introduced populations originated in the chance that an isolated nest fragment will
Argentina near the port city of Rosario. contain a queen and be able to grow into a suc-
cessful colony. Second, colony reproduction
occurs by budding. Argentine ants do not have to
Biology pass through the high mortality bottleneck at col-
ony founding endured by haplometrotic species
Like most ant species, Argentine ants are haplodip- that found new colonies with single queens draw-
loid and eusocial. They live in colonies composed ing on body reserves. Indeed, L. humile queens
largely of sterile female workers and a smaller without workers are incapable of founding new
number of fertile queens and males. Unlike most colonies, but propagules as small as 10 workers
ants, queens of L. humile do not fly, mating instead with a queen or even female brood can mature
in the nest. Genetic evidence suggests that queens into populous colonies. Finally, Argentine ants
are singly mated. For reasons that remain obscure, cope with frequent disturbance of nesting sites.
up to 90% of queens in a colony are periodically Nests tend to be superficial and transitory, occu-
executed by the workers. Males are present in early pying the top level of soil or litter. The ants move
summer and disperse by wing at dusk. As for all among existing nests and establish new nests fre-
Holometabola, metamorphosis is complete. quently in response to changes in moisture and
Development time is dependent on temperature temperature. In their native range colonies will
and has been estimated at 445 degree-days above a climb trees to escape rising flood waters.
16C threshold for workers. Under field conditions, Argentine ant colonies can reach extraordi-
the process from egg to adult can take several weeks nary sizes, inhabiting a diffuse system of inter-
to several months. connected nests spanning a few meters to several
290
A Argentine Ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae: Dolichoderinae)

hundred kilometers or more. While colony net- especially problematic in orchards and greenhouses
works in the native range are restricted to at most where they confound biological control efforts.
a few thousand square meters, introduced popu- The extent of Argentine ant invasion is likely
lations normally comprise unicolonial supercol- limited by a combination of abiotic conditions and
onies on the scale of landscapes or even interactions with other ant species. Invasions are
continents. Supercolonies are thought to arise facilitated in arid regions by development-related
following population bottlenecks at introduction increases in moisture from irrigation and run-off.
that produce genetic homogeneity among descen- Highly competitive local ant communities may
dents. Such colonies are normally diagnosed limit the spread of the Argentine ant. In the south-
using aggression assays and have been docu- eastern United States, for example, Argentine ant
mented to cover coastal Chile, California, most numbers declined following the introduction of
of Southern Europe, and parts of Australia. the fire ant Solenopsis invicta.
Argentine ants, like all Linepithema species,
are trophic generalists. They predate and scavenge
a wide variety of protein sources, often arthropods, Management
and display a high affinity for honeydew. Argen-
tine ants recruit quickly to food sources using The diffuse network structure of Argentine ant col-
chemical communication and are often seen run- onies renders control more difficult than for many
ning in active foraging trails. The trail pheromone other ant pests, as extirpated nests are readily
is (Z)-9-Hexadecenal, produced by the Pavans replenished from neighboring areas. Effective con-
gland at the tip of the abdomen. trol is unlikely to be gained with any single strategy,
and pest managers may have to experiment with
different approaches to treat an infestation. Treat-
Effects ment of Argentine ants around homes should
include cleaning indoor ant trails when they appear,
Introduced populations of L. humile penetrate removal of potential water and food sources, and
both human-disturbed and natural habitats. They sealing the ants entry points into the house. Con-
disrupt ecosystem processes both through active trol using toxic baits is often effective, and boric
predation and exploitative competition. Commu- acid-based liquid baits are generally more palatable
nity diversity is often reduced following invasion, to the ants than most commercially available ant
and Argentine ants have been documented dis- baits. As a last resort, appropriate perimeter insecti-
placing native arthropods in California, Hawaii, cides or repellents may be applied. For agricultural
Japan, South Africa, and Spain. Long term effects infestations, chemical or physical barriers applied
of Argentine ant invasions have included changes to individual plants have reduced ant damage.
in South African fynbos plant community struc- No specialized natural enemies are known
ture via displacement of native seed-dispersing forthe Argentine ant, but this insect has received
ants, and local extinction of Phrynosoma lizards relatively little research in its native range and
inCalifornia following the decline of their native some may yet be discovered. Recent work suggests
ant prey. that native populations may be held in check by
Damage to agriculture stems largely from the intraspecific competition among colonies and
ants association with honeydew-producing pests. interspecific competition with species such as
The ants protect their insect symbionts from attack Solenopsis invicta, also native in the Paran drain-
by predators and transport them to uninfested age. If this is the case, long-term strategies for lim-
plants, leading to outbreaks in populations of aphids, iting the effects of Argentine ants may include the
scale insects and mealybugs. Argentine ants are maintenance of robust native ant communities.
 Army Cutworm, Euxoa auxiliaris (Grote) (Lepidoptera: Noctuidae)
A 291

References Army Ants

Human KG, Gordon DM (1996) Exploitation and interfer- Ants that display group predatory and nomadic
ence competition between the invasive Argentine ant, behaviors. The nest site is changed at regular
Linepithema humile and native ant species. Oecologia
intervals, and workers forage in groups.
105:405412
Soeprono M, Rust MK (2004) Strategies for controlling Ants
Argentine ants (Hymenoptera: Formicidae). Sociobiol-
ogy 44:669682
Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in Army Cutworm, Euxoa auxiliaris
biological invasions dominated by long-distance jump
dispersal: insights from Argentine ants. Proc Natl Acad
(Grote) (Lepidoptera: Noctuidae)
Sci USA 98:10951100
Tsutsui ND, Case TJ (2001) Population genetics and col- This insect is found in the Great Plains and Rocky
ony structure of the Argentine ant (Linepithema Mountain regions of the United States and Canada. It
humile) in its native and introduced ranges. Evolution
55:976985 has been recorded from all states west of the
Wild AL (2004) Taxonomy and distribution of the Argentine Mississippi River, and as far east in Canada as Ontario,
ant Linepithema humile (Hymenoptera: Formicidae). but attains high densities only in semiarid areas, espe-
Ann Entomol Soc Am 97:12041215
cially along the western edge of the Great Plains.

Argidae
Host Plants
A family of sawflies (order Hymenoptera, subor-
der Symphyta). Army cutworm has been reported to feed on a large
Wasps, Ants, Bees and Sawflies number of plants. It is known principally as a pest
of small grains, perhaps because these crops domi-
nate the landscape where army cutworm occurs. It
Argyresthiidae damages such field crops as alfalfa, barley, clover, flax,
rye, sanfoin, sunflower, sweet clover, timothy, vetch,
A family of moths (order Lepidoptera). They and wheat. Among vegetable crops, it has been
commonly are known as shiny head-standing reported to damage beet, cabbage, celery, corn, onion,
moths. pea, potato, radish, rhubarb, tomato, and turnip.
Shiny Head-Standing Moths Other crops injured include such fruit crops as apple,
Butterflies and Moths apricot, blackberry, cherry, currant, gooseberry,
peach, plum, prune, raspberry, and strawberry. Army
cutworm also feeds on noncultivated plants such as
Arista
bluegrass, Poa spp.; bromegrass, Bromus spp.; buffa-
lograss, Buchloe dactyloides; grama grasses, Bouteloua
A large hair or bristle on the antennae of flies.
spp.; field pennycress, Thlaspi arvense; dandelion,
Antennae of Hexapods
Taraxacum officinale; lambsquarters, Chenopodium
album; and lupine, Lupinus spp.
Armored Scales
Members of the family Diaspididae, superfamily Natural Enemies
Coccoidae (order Hemiptera).
Bugs Many natural enemies have been found associated
Scale Insects and Mealybugs with army cutworm, and both hymenopterous
292
A Army Cutworm, Euxoa auxiliaris (Grote) (Lepidoptera: Noctuidae)

parasitoids and disease have been documented to before adults appear. Adults first become active in
cause considerable mortality. In the central Great April-May in southern locations such as Kansas
Plains, mortality studies over a 20-year period and Texas, whereas in more northern locations
demonstrated parasitism levels of up to 33% and such as Alberta and Montana they may not appear
disease incidence of up to 57%. Not surprisingly, until June-July. The moths migrate from the plains,
incidence of disease was greatest at high army- where the larvae develop, to higher elevations in
worm population densities. In a 3-year study in the Rocky Mountains, where the adults feed on
Oklahoma, researchers found that <12% of larvae nectar from flowers. The adults return to the plains
were parasitized, with most parasitism due to two in August-September.
species, Meteorus leviventris (Wesmael) and Apan-
teles griffini Viereck (both Hymenoptera: Braconi-
dae). A polyembryonic wasp, Copidosoma bakeri Egg
(Howard) (Hymenoptera: Encyrtidae), causes lar-
vae to consume more food, to become larger, and Eggs are deposited singly or in small clusters just
live longer; this can result in the appearance of beneath the soil surface on a solid substrate. The
artificially high rates of parasitism, which some- eggs are a slightly flattened sphere, measuring
times exceeds 50%. about 0.6 mm in diameter and 0.5 mm in height.
Among the other parasitoids known from army The egg is white to yellow initially, becoming gray
cutworm are such wasps as Apanteles marginiventris to brown as the embryo matures. The egg is marked
(Cresson), A. militaris Walsh, Chelonus insularis Cres- with about 18 very narrow ridges that radiate from
son, Macrocentrus incompletus Muesebeck, Micropli- the apex. Survival of eggs is reported to be affected
tis feltiae Muesebeck, M. melianae Viereck, Rogas sp., by moisture, and above-average rainfall in late
Zele melea (Cresson) (all Hymenoptera: Braconidae); summer and autumn tends to assure good insect
Campoletis flavicincta (Ashmead), C. sonorensis survival and damaging populations the subsequent
(Cameron), Diphyus nuncius (Cresson), Exetastes year. Field-collected females were reported to pro-
lasius Cushman, and Spilichneumon superbus (Pro- duce 200300 eggs, with the potential to produce
vancher) (all Hymenoptera: Ichneummonidae). Flies about 500 eggs.
known to parasitize this species include Bonnetia
comta (Fallen), Euphorocera claripennis (Macquart),
Mericia spp., Peleteria sp., Periscepsia cinerosa Larva
(Coquillett), P. helymus (Walker), and P. laevigata
(Wulp) (all Diptera: Tachinidae). The eggs hatch in the autumn or early winter but the
Several viruses are known to infect army cutworm, larvae are usually not noticed until spring when they
including entomopox, granulosis, and nonoccluded increase in size and begin to consume considerable
viruses. The relative importance of each is uncertain, foliage. There are 67 instars, with head capsule
but the granulosis virus is unusually pathogenic. widths of 0.260.30, 0.400.45, 0.650.72, 1.041.21,
1.702.10, and 2.903.40 mm, respectively, for
instars 16 among larvae with only 6 instars. Addi-
Life Cycle and Description tional instars apparently occur when larvae feed on
less suitable host plants. The body color of the larvae
There is a single generation per year throughout is (Fig.82) grayish brown, but bears numerous white
the range of this insect. Eggs are deposited on and dark brown spots. There usually is evidence of 3
soilin August-October. Eggs hatch in autumn or weak light-colored dorsal stripes. Laterally there
early winter, and larvae overwinter, feeding actively tends to be a broad dark band, and the area beneath
in the spring. Pupation occurs about a month the spiracles is whitish. The head is light brown with
 Army Cutworm, Euxoa auxiliaris (Grote) (Lepidoptera: Noctuidae)
A 293

Army Cutworm, Euxoa auxiliaris (Grote)

(Lepidoptera: Noctuidae), Figure 82 Larva of army
cutworm Euxoa auxiliaris.

dark spots. Larvae attain a length of about 40 mm.

They usually are found beneath the surface of the Army Cutworm, Euxoa auxiliaris (Grote)
soil, emerging in late afternoon or early evening to (Lepidoptera: Noetuidae), Figure 83 Army cutworm
feed. On cloudy days, however, they may be active adult, light form.
during the daylight hours. Larvae will assume a
migratory habit when faced with food shortage, and bearing bean-shaped and round spots but lacking
large numbers will proceed in the same direction, bands and stripes. In all cases, the hind wings are
consuming virtually all vegetation in their path. It is brownish with dark veins, and darker distally. The
this dispersive behavior that is the basis for their brown body of the moth is quite hairy.
common name, and larvae have been observed to As previously noted, the adults are migratory,
disperse over 4 km. dispersing from the plains to the mountains annu-
ally. In transit and in the mountains they feed on
nectar from flowering plants. They are nocturnal,
Pupa and seek shelter during the daylight hours. They
have the habit of aggregating in houses, automo-
Pupation occurs in the soil, in a cell prepared by the biles, and other sheltered locations where they
larva. The walls of the cell are formed with salivary become a nuisance, soil walls, and induce allergic
secretion, which hardens and provide a degree of reactions among some individuals. They also may
rigidity. The depth of pupation varies according to aggregate in natural shelters in mountainous
soil and moisture conditions, but may be any depth regions, where they become prey for bears. In the
up to 7.5 cm. The larva spends about 10 days in the Rocky Mountain region they are commonly called
cell prior to pupation. Duration of pupation is 2560 miller moths.
days. The pupa is dark brown in color, and measures
about 1722 mm in length and 6mm in width.
Damage

Adult These insects principally are pests of small grain

crops grown in arid regions, although a number of
The adults measure 3550 mm in wingspan. They irrigated crops also are at risk. Larvae readily climb
are quite variable in appearance, with five named plants to consume foliage, eating holes in vegetation
subspecies, but moths generally assume two basic initially, and eventually destroying the entire plant.
forms. One common form has the leading edge of Although they burrow into the soil during the day-
the forewing marked with a broad (Fig.83) yellowish light hours they do not normally feed below-ground.
stripe, and the remainder of the wing blackish but However, when succulent food is in short supply
marked with white-rimmed bean-shaped and they will follow the plant stem down into the soil.
round spots, and a light transverse line. In another When food supplies are exhausted large numbers of
common color form the forewing is mottled brown, larvae may disperse in search of additional food.
294
A Armyworm, Pseudaletia unipuncta (Haworth) (Lepidoptera: Noctuidae)

Management Armyworm, Pseudaletia unipuncta

(Haworth) (Lepidoptera:
Adults can be captured in light traps and phero- Noctuidae)
mone traps. However, males are attracted to the
sex pheromone only during the autumn flight. john l. capinera
Pheromone traps positioned at a height of 1 m or University of Florida, Gainesville, FL, USA
lower are more effective than those place higher.
Larvae can be recovered from soil by raking Armyworm also occurs in many areas of the
through the top 57 cm. world,including North, Central and South America,
Persistent insecticides can be applied to veg- southern Europe, central Africa, and western Asia.
etation to kill army cutworm larvae when they It is known principally as a grain pest. It does not
emerge from the soil to feed; Bacillus thuringiensis overwinter in northern latitudes, but disperses north-
is not effective. Larvae also will accept bran bait ward each spring, and then southward during the
containing insecticide. autumn. Because it is found widely, it has acquired
Cultural manipulations are not generally several common names, including true armyworm,
effective to prevent oviposition because moths rice armyworm, and American armyworm.
will deposit eggs on barren soil. Delayed planting
of crops can be effective, however, as larvae
complete their development on weeds or starve Life History
before crops are planted. If larvae are dispersing,
creation of deep ditches with steep sides, or filled Although not surviving year-round in cold winter
with running irrigation water, may prevent inva- areas, larvae apparently overwinter at intermediate
sion of fields. levels, and in warm weather areas all stages may be
To protect plants grown in the home garden, found during the winter. The number of generations
barriers are sometimes used to reduce access by varies among locations, but in North America two
cutworms to seedlings. Metal or waxed paper generations occur annually in Ontario, Canada,
containers with both the top and bottom removed whereas in the USA there are 23 generations
can be placed around the plant stem to deter in Minnesota and New York, 45 are reported in
consumption. Aluminum foil can be wrapped Tennessee, and 56 in southern states. A complete
around the stem to achieve a similar effect. generation requires 3050 days.
Because larvae will burrow and feed below the Females deposit eggs in clusters consisting of
soil line, the barrier should be extended below two to five rows, in sheltered places on foliage, often
the soil surface. between the leaf sheath and blade, especially on dry
Wheat Pests and their Management grass. Often females seem to deposit large numbers
in the same vicinity, resulting in very high densities
of larvae in relatively small areas of a field. Neverthe-
less, the eggs are very difficult to locate in the field.
References
The eggs are white or yellowish, but turn gray imme-
diately before hatching. Eggs are spherical, and mea-
Burton RL, Starks KJ, Peters DC (1980) The army cutworm.
Oklahoma Agricultural Experiment Station Bulletin sure about 0.54 mm (range 0.40.7 mm) in diameter.
739:135 The egg surface appears to be shiny and smooth, but
Capinera JL (2001) Handbook of vegetable pests. Academic under high magnification fine ridges can be observed.
Press, San Diego, 729 pp
Kendall DM, Kevan PG, LaFontaine JD (1981) Nocturnal
The egg clutches are covered with an adhesive secre-
flight activity of moths (Lepidoptera: Noctuidae) in tion that is opaque when wet but transparent when
alpine tundra. Can Entomol 113:607614 dry. As the adhesive material dries it tends to draw
 Armyworm, Pseudaletia unipuncta (Haworth) (Lepidoptera: Noctuidae)
A 295

together the foliage, almost completely hiding the but soon assumes a mahogany brown color. The tip of
eggs. Mean duration of the egg stage is about 3.5 days the abdomen bears a pair of hooks. Duration of the
at 23C, and 6.5 days at 18C, but the range is 324 pupal stage is 714 days during summer but longer
days over the course of a season. Hatching rates are early and late in the season, sometimes lasting 40 days.
affected by temperature, with cool weather more The adult is a light reddish brown moth with
favorable for embryonic survival. In Tennessee, about a wing span measuring about 4 cm. The forewing
98% egg hatch occurs in early spring and autumn, is fairly pointed (Fig.84), appearing more so
with hatching rates dropping to less than 30% during because a transverse line of small black spots
the summer; this probably accounts for the evolution terminates in a black line at the anterior wing tip.
of the dispersal behavior in this species. The forewing is also marked with a diffuse dark
Larvae normally display 6 instars, though up to area centrally containing one or two small white
9 instars have been observed. Mean head capsule spots. The hind wings are grayish, and lighter
widths (range) are 0.34 (0.300.37), 0.55 (0.490.63), basally. Adults are nocturnal. Mating commences
0.94 (0.831.12), 1.5 (1.291.70), 2.3 (2.082.56), 13 days after moths emerge from the soil, and
and 3.3 (3.043.68) mm, respectively, for instars 16. usually 47 h after sunset. Eggs are normally depos-
Head capsule widths increase slightly with increased ited within a 45 day period (range 110). Females
temperature up to about 30C. Larvae attain a body produce an average of 4.9 egg masses (range 116).
length of 4, 6, 10, 15, 20, and 35 mm, respectively, Reproductive capacity varies, with authors report-
during instars 16. Except for the first instar, which ing mean egg production anywhere from 500 to
is pale with a dark head, the larvae of armyworm are 1500 per female. Feeding is necessary for normal
marked with longitudinal stripes throughout their oviposition. Mean longevity at warm temperatures
development. The head capsule is yellowish or yel- is about 9 days in males and 10 days in females
low-brown with dark net-like markings. The body (range 325) whereas at cool temperatures mean
color is normally grayish green, but a broad dark longevity of males is 19 days and females 17 days.
stripe occurs dorsally and along each side (Fig.85). Armyworm generally prefers to oviposit and
A light subspiracular stripe often is found laterally feed upon plants in the family Gramineae, includ-
beneath the dark stripe. Development time varies ing weedy grasses. Thus, such grain and grass crops
with temperature. During summer larvae complete as barley, corn, millet, oats, rice, rye, sorghum,
their development in about 20 days, but this is sugarcane, timothy, and wheat may be consumed,
extended to about 30 days during the spring and as well as wild or weed grasses. During periods of
autumn, and greatly prolonged during winter. Instar- abundance larvae feed more generally, damaging
specific development times recorded during early such crops as alfalfa, artichoke, bean, cabbage, car-
summer in Tennessee are 23, 23, 24, 23, 45, rot, corn, celery, cucumber, lettuce, onion, parsley,
and 710 days for instars 16, respectively. The lar-
vae tend to disperse upward following hatching,
where they feed on tender leaf tissue. If disturbed,
they readily extrude silk and spin down to the soil.
Larvae in instars 36 are active at night, seeking
shelter during the day on the soil beneath debris or
clods of soil.
Larvae pupate in the soil, often under debris, at
depths of 25 cm. Pupation occurs in an oval cell that
contains a thin silken case. The pupa is moderate Armyworm, Pseudaletia unipuncta (Haworth)
in size and robust, measuring 1317 mm long and (Lepidoptera: Noctuidae) Figure 84 Adult of
56 mm wide. The pupa is yellowish brown initially, armyworm, Pseudaletia unipuncta (Haworth).
296
A Armyworm, Pseudaletia unipuncta (Haworth) (Lepidoptera: Noctuidae)

parsnip, pea, pepper, radish, sugarbeet, sweet potato, Damage

watermelon, and others. Adults feed on nectar of
various flowers and sometimes feed on other sweet Larvae initially skeletonize foliage, but by the third
foods such as ripe and decaying fruit. instar they eat holes in leaves, and soon afterwards
The importance of natural enemies, especially consume entire leaves. Larvae of armyworm (Fig.85)
parasitoids, has been studied, though nearly all are notorious for appearing out of nowhere to inflict
data are derived from periods of high armyworm a high level of defoliation. This occurs for several
density, which is not typical for this insect. Over 60 reasons: a highly clumped distribution of young
species of wasp and fly parasitoids are known, and larvae, with most of the crop uninfested until larvae
vary considerably from time to time and place to are nearly mature and highly mobile; a tendency by
place in importance. larvae to feed on grass weeds preferentially, only
Predators readily consume armyworm larvae. moving to crops after the grass is exhausted; occur-
Ground beetles (Coleoptera: Carabidae) are espe- rence of a preponderance of feeding, about 80%, in
cially effective because larvae spend a great deal the last instar; the nocturnal behavior of larvae,
oftime in association with soil, but various preda- which makes them difficult to observe during the
tory bugs (Hemiptera: various families), ants day; and the gregarious and mobile behavior of
(Hymenoptera: Formicidae), and spiders (Araneae: mature larvae, which form large aggregations or
Lycosidae and Phalangiidae) also feed on army- bands (hence the common name army worm). As
worm. Avian predators are often credited with previously noted, grasses and grains are preferred,
destruction of armyworms. The bobolink, Dolicho- but as these plants are consumed larvae disperse,
nyx oryzivorus (Linnaeus), prospers during out- often in large groups, to other plants. During out-
break years and has sometimes been called the breaks, few plants escape damage.
armyworm bird in North America. Other birds of
note include the crow, Corvus brachyrhynchos
Brehm, and starling, Sturnus vulgaris Linnaeus. Management
Diseases commonly infect armyworms, espe-
cially during periods of high density. Bacteria Adults can be captured with blacklight traps, and a
and fungi, particularly the fungus Metarhizium sex pheromone has been identified and can be
anisopliae, are reported in the literature. Nema- used for population monitoring. It is advisable to
todes are sometimes considered to be important examine crop fields for larvae, especially if moths
mortality factors. However, undoubtedly the most have been captured in light or pheromone traps.
important diseases are viruses; several granulosis, Fields should be examined at dawn or dusk,
cytoplasmic polyhedrosis, and nuclear polyhedro- because larvae are active at this time. If it is neces-
sis viruses often kill virtually all armyworms dur- sary to check fields during the day, it is important
ing periods of outbreak, especially when larvae are to sift through the upper surface of the soil and
also stressed by lack of food or inclement weather. under debris for resting larvae.
Armyworm attains high densities irregularly,
often at 520 year intervals. The exact cause is
unknown, but outbreaks often occur during un
usually wet years and are preceded by unusually dry
years. Armyworm is not well adapted for hot tem-
perature; survival decreases markedly when temper-
atures exceed about 30C. Consequently, at southern Armyworm, Pseudaletia unipuncta (Haworth)
latitudes populations are higher early and late in the (Lepidoptera: Noctuidae), Figure 85 Larva of
year, but at northern latitudes it is a mid season pest. armyworm, Pseudaletia unipuncta (Haworth).
 Arnett, Jr., Ross Harold
A 297

Larvae will consume wheat bran or apple earned a B.S. degree in 1942. That same year, he
pomace baits treated with insecticide, but foliar married Mary Ennis, spent a short time working for
and soil-applied insecticides are also effective, and the New York Conservation Department, then
used frequently. joined the U.S. army. His army duties had him con-
Cultural practices have limited effect on army- trolling mosquitoes in Florida, and then teaching
worm abundance due to their highly dispersive mosquito taxonomy in Panama. In October 1945,
behavior. However, grass weeds are a focal point of he was d ischarged by the army, and returned to Cor-
infestation, and should be eliminated, if possible. nell University as a graduate student. He received his
Not surprisingly, no-till and minimum tillage fields masters degree in 1946, having studied medical and
experience greater problems with armyworm, rela- aquatic entomology. For his doctoral research, he
tive to conventional tillage fields. Proximity to small returned to his early interest in beetles, beginning a
grain crops is considered to be a hazard due to the taxonomic revision of the North American Oede-
preference of moths for such crops, and the suit- meridae, and he received his Ph.D. in 1948. He was
ability of grains for larval development. In Virginia, employed (19481954) by the U.S. Department of
destruction of winter cover crops by herbicide Agriculture as a taxonomist at the U.S. National
application is more favorable to armyworm survival Museum, 19541958 as professor of biology at Saint
than is mowing of cover crops, apparently because John Fisher College in New York state, 19581963
predators are more disrupted by herbicide treat- as professor of biology at the Catholic University of
ment. Prior to the availability of effective insecti- America (in Washington, DC), 19661973 at Pur-
cides, deep furrows with steep sides were sometimes due University (Indiana), and 19731979 at Siena
plowed around fields to prevent invasion by dis- College (New York state). Thereafter, he left aca-
persing armyworm larvae. Although this approach demic life and derived his income from publishing.
remains somewhat useful, it is rarely practiced. His research interests were in the family Oedemeri-
Turfgrass Insects and their Management dae. (false blister beetles), on which he published
Wheat Pests and their Management several scientific papers. However, it is as a teacher
(he guided several graduate students in taxonomy
of Coleoptera) and author of books and journals
References and publishing projects that entomologists knew
him best. His Beetles of the United States. A man-
Breeland SG (1958) Biological studies on the armyworm, ual for identification was the standard identifica-
Pseudaletia unipuncta (Haworth), in Tennessee (Lepi-
doptera: Noctuidae). J Tennessee Acad Sci 33:263347 tion reference from its publication in 1962 until its
Capinera JL (2001) Handbook of vegetable pests. Academic replacement by the two-volume American Beetles
Press, San Diego, 729 pp (volume 1: 2000, volume 2: 2002) that he began. In
Guppy JC (1961) Life history and behaviour of the armyworm,
1947 he founded The Coleopterists Bulletin and
Pseudaletia unipuncta (Haw.) (Lepidoptera: Noctuidae),
in eastern Ontario. Can Entomol 93:11411153 was for years its editor (it was later and ungram-
Guppy JC (1969) Some effects of temperature on the imma- matically renamed by others The Coleopterists Bul-
ture stages of the armyworm, Pseudaletia unipuncta letin). In 1985 he founded the journal Insecta
(Lepidoptera: Noctuidae), under controlled conditions.
Can Entomol 101:13201327
Mundi, which is now published by the Center for
Systematic Entomology, of Gainesville, Florida, as a
low-cost outlet for taxonomic publications on
insects. He published a book on Coleoptera collec-
Arnett, Jr., Ross Harold tions of North America, which later was greatly
expanded to become The insect and spider collec-
Ross Arnett was born on April 13, 1919, in the state tions of the world (1986) and still later (1993) was
of New York. He attended Cornell University and revised, and another (Entomological Information
298
A Arolium

Storage and Retrieval, 1970) on documentation, Arrhenogenic

both of which were ahead of their time. He was
author or coauthor of books on botany, on How to A sex determining system, in which females pro-
know the beetles, of Simon and Schusters Guide to duce male progeny only. Found in the blow fly
Insects, and of two volumes on The Beetles of Chrysomya rufifacies (Calliphoridae).
northeastern North America. His American
Insects (1985) won the R.R. Hawkins award from
the American Association of Publishers, but coleop-
Arrhenophanidae
terists would argue that his works on Coleoptera
were far greater. He was the founder of a short-lived
journal featuring colored photographs (hitherto A family of moths (order Lepidoptera). They also
rarely seen in entomology because of cost, yet com- are known as tropical lattice moths.
mon in everyday advertisements for commercial Tropical Lattice Moths
products) called Insect World Digest, and of two Butterflies and Moths
publishing companies (Flora and Fauna publica-
tions, and Sandhill Crane Press), which helped ento-
mologists and other biologists to publish their works.
He was the instigator in the 1970s of the North Arrhenotoky
American Beetle Fauna Project, whose ambition was
to catalog and document all of the North American A form of parthenogenesis in which an unfertil-
Coleoptera. He was the greatest proponent of North ized egg develops into a male by parthenogenesis
American coleopterology for over 50 years. He died and a fertilized egg develops into the female.
on July 16, 1999, in Gainesville, Florida, survived by Arrhenotoky is found in many Hymenoptera.
his devoted wife, Mary Ennis Arnett, who died on
January 3, 2002, and eight children.

References Artematopididae

Gerberg EJ (1999) Ross Harold Arnett, Jr. Am Entomol

A family of beetles (order Coleoptera). They com-
45:191192 monly are known as soft-bodied plant beetles.
Thomas MC (1999) Ross H. Arnett, Jr. Coleopterists Bull Beetles
53:300

Arolium
Artheneidae
A pad or pads found between the tarsal claws or at
the base of the tarsi. A family of bugs (order Hemiptera, suborder
Legs of Hexapods Pentamorpha).
Bugs

Arrestant
Arthropleidae
A factor that causes an insect to aggregate at the
site of the factor, but not a factor facilitating long- A family of mayflies (order Ephemeroptera).
distance orientation (i.e., not an attractant). Mayflies
 Arthropod-Associated Plant Effectors (AAPEs): Elicitors and Suppressors of Crop Defense
A 299

Arthropod-Associated Plant herbivore, corn (Zea mays), and host-seeking

Effectors (AAPEs): Elicitors and parasitic wasps (Cotesia marginiventris). In corn,
Suppressors of Crop Defense this rapidly induced increase in volatile emission
could not be stimulated by mechanical damage
hans t. alborn, eric a. schmelz alone yet was readily mimicked by the application
USDA ARS CMAVE, Gainesville, FL, USA of beet armyworm oral secretions to wounded
leaves. In 1997 the fatty acid-amino acid conjugate
Interactions between plants and insects have played N-17-hydroxylinolenoyl-L-glutamine, termed volicitin,
a significant role in the evolution of both groups of was discovered in the oral secretions of beet
organisms. In response to herbivory, plants have armyworm. This elicitor of corn leaf volatiles
evolved the ability to perceive and defensively marked the first AAPE isolated and identified
respond to insect herbivores (or potential herbi- from insects.
vores), either directly, by inducing biochemical During arthropod feeding or oviposition,
changes that impede pest growth or indirectly, by mechanical wound responses in the plant can
promoting advantageous interactions with benefi- be greatly amplified by the presence of elici-
cial organisms, often through the release of volatile tors. Elicitors are specific bioactive chemicals
signals. These volatile signals indicate to parasitic present at the plant wound-site that may be
and predaceous insects the location of potential derived from the insect, the plant, or from
prey. Insects may also partly inhibit these induced the interactions between organisms. The
plant responses by limiting the accumulation of mode of action of elicitors may vary, but
defense-related biochemicals at the feeding site. We increasingly some classes are predicted to act
collectively refer to substances that either nega- as ligands that bind plant receptors (likely
tively or positively alter plant responses to attack as membrane-bound extracellular leucine-rich
arthropod-associated plant effectors (AAPEs). repeat receptor kinases) initiating a complex
Those effectors that increase a plants defense cascade of signal transduction leading to
against an arthropod pest are termed elicitors while induced plant responses. Typically, over the
those that reduce a plants defense are suppressors. course of a few hours, elicitors will cause a
Research on arthropod-associated elicitors rapid induction of defense-related phytohor-
and suppressors of plant responses traces its roots mones, including jasmonic acid, ethylene,
to the 1972 discovery by Clarence Ryan and col- and salicylic acid which serve as both mark-
leagues that feeding by Colorado potato beetle ers and signals for subsequent plant defense
(Leptinotarsa decemlineata), as well as mechani- responses. In contrast to elicitors, suppres-
cal damage to tomato plants, rapidly increases sors of plant defense may act through direct
the concentration of leaf protease inhibitors. This insect-derived protein/enzyme interactions
ultimately led to the discovery of systemin, an 18 within the plant. The majority of recently
amino acid peptide, and established the existence identified AAPEs described below act as
of peptide signals in plants. In 1988, Marcel Dicke e licitors of plant defense; however, glucose
and colleagues demonstrated that herbivory by oxidase acts as a suppressor of plant defense.
spider mites (Tetranychus urticae) induced plant
volatiles in lima bean (Phaseolus lunatus) leaves,
which in turn served as attractants for predatory Volicitin
mites (Phytoseiulus persimilis). Shortly thereafter,
Jim Tumlinson and colleagues demonstrated In 1997, Hans Alborn and colleagues isolated
similar volatile-mediated tritrophic interactions and identified volicitin from the larval oral secre-
among the beet armyworm (Spodoptera exigua) tions of the beet armyworm (BAW), Spodoptera
300
A Arthropod-Associated Plant Effectors (AAPEs): Elicitors and Suppressors of Crop Defense

exigua. Subsequently, other analogous fatty acid isoprenoid pathways. Fatty acid amides seem
amide elicitors have been identified in the oral to have activity on a broad range of plants,
secretions of several other species of Lepi- although some clear exceptions exist (see
doptera. This class of elicitors consists of plant inceptin below). A significant release of vola-
fatty acids, typically linolenic, linoleic, and oleic tiles can typically be detected a few hours after
acid, or their 17-hydroxy analogs, conjugated an application of about 10 pmol volicitin/corn
with glutamine or glutamic acid. They were seedling.
initially thought to be specific for Lepidoptera
but recently they have also been found in
k atydids, crickets and fruit flies. Thus far, three Caeliferins
herbivore-produced fatty acid-amino acid
elicitors, volicitin, N-linolenoyl-L-glutamine In the early 1990s, when working on the isolation of
and N-linolenoyl-L-glutamate (Fig.86), have volicitin, the Tumlinson group observed that not
been demonstrated to have significant activity only feeding by lepidopteran larvae but also feeding
in inducing plants to produce and release vol- by the American grasshopper (Schistocerca ameri-
atile organic compounds that are synthesized cana) induced corn seedlings to release volatile
by several different biosynthetic pathways, organic compounds. This led to the recent discov-
including the lipoxygenase, shikimate and ery of a new type of elicitor named caeliferins. These

Arthropod-Associated Plant Effectors (AAPEs): Elicitors and Suppressors of Crop Defense,

Figure 86 Structures of some elicitors.
 Arthropod-Associated Plant Effectors (AAPEs): Elicitors and Suppressors of Crop Defense
A 301

compounds are comprised of saturated and mono- the emission of large amounts of volatile organic
unsaturated, sulfated alpha-hydroxy fatty acids compounds. However, inceptin has additional roles
(with fatty acid chains of 1520 carbons) in which in direct plant defense including upregulation of
the omega carbon is functionalized with either a protease inhibitor transcripts and reduced growth
sulfated hydroxyl or a carboxyl conjugated to gly- of larvae on induced tissues. Similar to established
cine via an amide bond. In the oral secretions of the peptide signals with known plant receptors, such as
American grasshopper, the 16-carbon analogs are systemin and flg22 (derived from bacterial flagellin),
predominant and also most active in inducing inceptin is also believed to act as a ligand that spe-
release of volatile organic compounds when applied cifically binds a plant receptor initiating these
to damaged leaves of corn seedlings. It appears that responses. In cowpea and beans, insect gut proteol-
caeliferins, which are the first non-lepidopteran ysis following herbivory generates inappropriate
elicitors of volatiles identified in insect herbivores, fragments of an essential metabolic enzyme that
might be present in most, if not all, grasshoppers enables plant non-self recognition.
(members of the suborder Caelifera), but not in
crickets or katydids (suborder Ensifera). Interest-
ingly, oral secretions of at least some crickets and Bruchins
katydids contain some of the same glutamine and
glutamic acid-based fatty acid amides that are found The first beetle-derived elicitor of physical plant
in Lepidoptera larvae. Preliminary results indicate defense was described from the cowpea weevil
that the activity of caeliferins might be restricted to (Callosobruchus maculatus F.). Oviposition of
monocotyledons where the response mimics that pea weevil (Bruchus pisorum L.) on pods of spe-
of volicitin. The typical lowest active dose is about cific varieties of pea (Pisum sativum L.) promotes
100 pmol/corn seedling. neoplastic cellular growths that impede entry of
neonate weevil larvae into the pod and increase
the probability of predation, parasitism and
Inceptin and Related Peptides dehydration. This class of elicitors, collectively
named bruchins, represents long-chain ,-diols,
In cowpea (Vigna unguiculata) and beans (Phaseo- partly or entirely esterified with 3-hydroxypro-
lus vulgaris), herbivory by fall armyworm (Spodo- panoic acid. Like the inceptin peptide, bruchins
ptera frugiperda) larvae and applications of oral exhibit potent biological activity with as little as 1
secretions elicit phytohormone changes and induce fmol (0.5 pg) inducing neoplastic growth on pea
volatile emission due to the presence of a disulfide- pods. Supportive of a role for specific plant recep-
bridged peptide termed inceptin. Inceptin and tors, only pea plants harboring the yet uncloned
related fragments are derived from the -subunit of Np allele exhibit these responses.
chloroplastic ATP synthase (cATPC) present in leaf
tissue. As a result of insect gut proteolysis, the oral
secretion of larval fall armyworm contains a mix- Glucose Oxidase
ture of related peptides derived from cATPC, includ-
ing additional amino acids at the N terminus and The first demonstration of a suppressive effect of
also C-terminal truncations. Inceptin is the one of AAPEs came from studies of the corn earworm
the most potent AAPEs known to date, and has (Helicoverpa zea) feeding on leaves of tobacco
measurable elicitor activity starting at 1 fmol/leaf. (Nicotiana tabacum). During herbivory larvae
Inceptin elicits a rapid and sequential induction of secrete the salivary enzyme glucose oxidase (GOX)
defense-related phytohormones, such as jasmonic from the spinneret which reacts with glucose to
acid, ethylene and salicylic acid, and also stimulates form hydrogen peroxide and gluconic acid. GOX
302
A Arthropod-Associated Plant Effectors (AAPEs): Elicitors and Suppressors of Crop Defense

levels in labial glands vary considerably dependent Significance of AAPEs

upon larval diet and host plants. Insect secretion
of glucose oxidase limits the wound-induced accu- Many insect herbivores are vulnerable to preda-
mulation of the toxic alkaloid nicotine following tors and other natural enemies only during narrow
herbivory. As a product of GOX, hydrogen perox- developmental windows. For example, the parasi-
ide may either directly or indirectly inhibit wound- toid wasp Cotesia marginiventris must locate hosts
induced nicotine accumulation but this hypothesis before the end of the caterpillars second instar.
awaits confirmation. Long range attraction to the hosts is mediated by
herbivore-induced plant volatiles, yet the amount
of mechanical damage caused by first instar larvae
Other Systems for Consideration is low. Elicitors, whether plant-or arthropod-pro-
duced, serve an important ecological function in
Enzymatic activity consistent with -glucosidase amplifying plant signal transduction cascades
has been found in larvae of the cabbage white such that a significant response (i.e., release of vol-
butterfly (Pieris brassicae). Applications of -gluco- atile organic compounds) is generated from a very
sidase preparations from almonds have been modest initial injury.
reported to promote volatile emission in excised Photosynthetic organisms have had to cope
leaves of Brussels sprouts (Brassica oleracea L. var with biotic stress in the form of microbes long before
gemmifera) that have been additionally wounded. the existence of insects. A significant component of
Curiously, the role of -glucosidase as an elicitor plant pathology research focuses on the molecular
of plant volatile emission has not been followed up aspects of how plants recognize pathogens and the
on in over a decade nor demonstrated outside of mechanisms by which pathogens avoid recognition.
the aforementioned experimental system. Many Emphasis on this area of inquiry arose from neces-
lytic enzymes have the potential to influence plant sity and the microscopic nature of the interactions.
physiological responses; however, clear and care- Entomologists have additional levels of complexity
ful experimentation is required prior to demon- to confront including insect behavior, multiple
strating a substance to be a relevant effector. instars of development and complex multitrophic
Alkaline phosphatase activity has been demon- interactions. Studies involving these visible markers
strated to exist in the salivary glands of adult white- have historically been more numerous than molecu-
flies (Bemisia tabaci B biotype, syn. B. argentifolii) lar level investigations. Plant breeders strive to main-
and is also secreted into artificial diets. This enzyme tain insect resistance in new crop cultivars, ideally
exists as a candidate AAPE but at this time no spe- one step ahead of emerging insect biotypes that
cific action on plant physiology has been shown. overcome these defenses. Currently, numerous
Alternatively, the pore-forming peptide alamethicin examples of genes responsible for plant resistance to
and larger polypeptides from preparations of cel- insects are being identified as receptor kinases. These
lulysin, originating from the fungus Trichoderma receptors are not directly toxic and by themselves do
viride, are potent inducers of plant defense responses. not result in plant resistance. Instead, ligand (i.e.,
These bioactive substances have been demonstrated elicitor) binding to receptors triggers induced plant
to have activities similar to known AAPEs yet responses that result in resistance. In plant pathol-
they are not known to exist in the secretions of ogy research, some virulent pathogens lack key bio-
arthropods at meaningful levels. Many additional chemicals or possess slightly modified protein
plant-insect systems, such as the plant response to sequences enabling evasion of receptor-mediated
oviposition of insect eggs,have been clearly demon- plant recognition. We can fully expect the same
strated to involve putative AAPEs, yet the majority interactions to be occurring in insect pests that are
of these await detailed characterization. specialized on specific crops.
 Arthropods
A 303

Once basic insect recognition systems are host-searching parasitic wasps. Proc Natl Acad Sci USA
92:20362040
understood in plants at molecular and mechanis-
Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin
tic level, strategies will be tractable to transgeni- G, Murphy JB, Felton GW (2002) Herbivory: caterpillar
cally modify and promote a plants ability to induce saliva beats plant defences A new weapon emerges in
rapid defense responses. Some examples of future the evolutionary arms race between plants and herbi-
vores. Nature 416:599600
research on insect biotypes that overcome plant Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J,
resistance will likely demonstrate mechanisms Chourey PS, Alborn HT, Teal PEA (2006) Fragments of
involving the alterations of receptor-ligand binding ATP synthase mediate plant perception of insect attack.
interactions. Currently not a single plant-insect Proc Natl Acad Sci USA 103:88948899
Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of
interaction involving AAPEs is understood at this herbivore-induced plant odors by host-seeking parasitic
level. This research direction is essential for further wasps. Science 250:12511253
progress. Understanding the chemistry of the
AAPEs that mediate these interactions is more
than just a research curiosity. AAPEs represent
literal and figurative keys to induced plant defense Arthropods
and resistance to insect pests.
Allelochemicals Those members of the phylum Arthropoda. Ani-
Tritrophic Interactions mals with jointed legs. The principal arthropod
Plant Resistance to Insects taxa of interest to entomologists are:
Phylum Arthropoda
Subphylum Trilobita Trilobites (these are
References extinct)
Subphylum Chelicerata
Alborn HT, TurlingsTCJ, Jones TH, Stenhagen G, Loughrin Class Merostomata Horseshoe crabs
JH, Tumlinson JH (1997) An elicitor of plant volatiles
from beet armyworm oral secretion. Science 276:
Class Arachnida Arachnids (scorpions,
945949 spiders, ticks, mites, etc.)
Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson Class Pycnogonida Sea spiders
JH, Schmelz EA, Teal PE (2007) Disulfooxy fatty acids Subphylum Crustacea Crustaceans
from the American grasshopper, Schistocerca americana,
elicitors of plant volatiles. Proc Natl Acad Sci USA (amphipods, isopods, shrimp, etc.)
104:1297612981 Subphylum Atelocerata
Dicke M, Sabelis MW (1988) How plants obtain predatory Class Diplopoda Millipedes
mites as bodyguards. Netherlands J Zool 38:148165
Class Chilopoda Centipedes
Doss RP, Oliver JE, Proebsting WM, Potter SW, Kuy SR,
Clement SL, Williamson RT, Carney JR, DeVilbiss ED Class Pauropoda Pauropods
(2000) Bruchins: insect-derived plant regulators that Class Symphyla Symphylans
stimulate neoplasm formation. Proc Natl Acad Sci USA Class Entognatha Collembolans, pro-
97:62186223
Green TR, Ryan CA (1972) Wound-induced proteinase
turans, diplurans
inhibitor in plant leaves possible defense mechanism Class Insecta Insects
against insects. Science 175:776777 In addition, the Phylum Onychophora is
Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT sometimes considered to be arthropods, but it is
(2001) Molecular interactions between the specialist
herbivore Manduca sexta (Lepidoptera, Sphingidae) best considered to be a separate phylum, evolu-
and its natural host Nicotiana attenuata. III. Fatty acid tionarily intermediate between arthropods and
amino acid conjugates in herbivore oral secretions are annelids.
necessary and sufficient for herbivore-specific plant
Centipedes
responses. Plant Physiol 125:711717
Mattiacci L, Dicke M, Posthumus MA (1995) Beta-Glucosidase Diplurans
an elicitor of herbivore-induced plant odor that attracts Entognatha
304
A Articulation

Millipedes separation of species. These characteristics include

Mites ascospore shape, size, color and arrangement, as
Pillbugs and Sowbugs well as the size, color, etc., of sporocysts. The loca-
Proturans tion (i.e., subcuticular, external) of the cysts also
Scorpions can be relevant in identification, although it has
Spiders been reported that cysts of A. apis can occur
Springtails beneath the integument in carpenter bee larvae.
Ticks Ascosphaera spores can initiate infection in
healthy bee larvae either by breaching the external
cuticle or through the digestive tract. Chilling
Articulation appears to facilitate the infection process, and the
peripheral brood, where the temperature may be
A connection or joint between two sections of the lower, is therefore more easily infected. Some spe-
cuticle, or structures. Articulations take many forms, cies of the fungus can infect solitary insects; for
ranging from membranous or lightly sclerotized example, A. aggregata commonly occurs in alfalfa
area between two plates, to a ball and socket joint. leafcutting bees. The infection is initiated only by
ingestion of the spores. The hyphae invade the
midgut wall and hemocoel, and eventually replace
Ascalaphidae most of the larval tissues. This species of Asco-
sphaera does not readily digest chitin, so that
A family of insects in the order Neuroptera. They sporulation is subcuticular, in contrast to A. apis
commonly are known as green owlflies. in which the mummified surfaces usually are cov-
Lacewings, Antlions and Mantidflies ered with white mycelia and darkened cysts. When
sexual reproduction in A. aggregata is complete,
and the mature ascospores are formed, the fungal
Ascosphaera apis mat becomes dark brown and is hard and dry. This
species requires a complex medium for in vitro
One of the best-known ascomycetous insect growth and thus appears to be a true obligate
pathogens is Ascosphaera (Plectomycetes). Asco- parasite. Other species are considered to be oppor-
sphaera apis causes chalk-brood disease mainly in tunistic since they can grow saprophytically, or
honey bees, a condition that may not necessarily only infect stressed insects.
be serious depending upon the hygienic behavior
of the insects; colonies from which diseased brood
is removed by worker bees appear to be resistant References
to the disease. The fungus is usually heterothallic,
and during sexual reproduction the trichogyne Gilliam M, Lorenz BJ, Buchmann SL (1994) Ascosphaera apis,
(receptive female hypha) fuses with a nutriocyte, the chalkbrood pathogen of the honey bee, Apis
an inflated part of the ascogonium. The nutrio- mellifera, from larvae of a carpenter bee, Xylocopa cali-
cytes develop asci and ascospores that form into fornica arizonensis. J Invertebr Pathology 63:307309
Gilliam M, Taber III S, Lorenz BJ, Prest DB (1988) Factors
tightly packed spheres called spore balls. The affecting development of chalkbrood disease in colonies
chambers that encase the spore balls are termed of honey bees, Apis mellifera, fed pollen contaminated
the sporocysts, and these appear as dark specks on with Ascosphaera apis. J Invertebr Pathol 52:314325
McManus WR, Youssef NN (1984) Life cycle of the chalk
mummified larvae. Enzyme analysis has been used
brood fungus, Ascosphaera aggregata, in the alfalfa
to identify strains of Ascosphaera, whereas cer- leafcutting bee, Megachile rotundata, and its associated
tain morphological characteristics can facilitate symptomatology. Mycologia 76:830842
 Ash-Gray Leaf Bugs
A 305

Vandenberg JD, Stephen WP (1983) Pathogenicity of produced by infected cells that undergo an apop-
Ascosphaera species for larvae of Megachile rotundata. J
totic-like cleavage. In vivo, infected larvae have
Apic Res 22:5763
been observed to discharge infectious virus from
the eversible gland. The vesicles, when fed to neo-
nate larvae, resulted in erratic infection patterns
Ascoviruses (285%). However, challenge with a minutin pin
dipped in virus suspensions resulted in 100%
The members within the proposed Ascoviridae infection rates. As few as ten vesicles are infec-
family are characterized by the accumulation of tious when delivered into the insect hemocoel.
virion-containing vesicles (asco=sac, or bladder) Research has demonstrated that ascoviruses can
in the hemolymph of host noctuid larvae. The be mechanically transmitted from infected larvae
membrane-bound vesicles (110 m) contain to healthy larvae during oviposition by parasi-
hundreds of enveloped allantoid shaped virus toids. The ascoviruses are able to outcompete the
particles that are 300400 nm in length and 130 developing parasitoid and successfully infect host
nm in diameter. The outer surface of the bilayer larvae. It has been suggested that the incidence of
viral envelope possesses a characteristic reticulate ascovirus in noctuid populations, ranging from 1
pattern. Purified ascoviruses contain a complex of to 25%, may be associated with the presence of
12 structural proteins ranging from 11 to 200 larval parasitoids.
kDa. Ascoviruses encapsidate a circular dsDNA
(140180 kbp) having a G+C ratio of 60%. Com-
parative sequence analysis of the DNA polymerase References
genes suggests that ascoviruses and iridoviruses
shared a common ancestor. Presently, ascoviruses Federici BA (1983) Enveloped double-stranded DNA insect
have been detected in several noctuids including virus with a novel structure and cytopathology. Proc
Autographa californica, Trichoplusia ni (TAV), Natl Sci Foundation 80:76647668
Spodoptera frugiperda (SAV), Heliothis virescens Federici BA, Vlak JM, Hamm JJ (1990) Comparative study of
virion structure, protein composition and genomic
(HAV), Heliocoverpa zea (HZV), and Scotogramma DNA of three ascovirus isolates. J Gen Virology
trifolii (STV). Southern blot hybridization studies 71:16611668
have demonstrated that the SAV genome (140 kbp) Bigot Y, Stasiak K, Rouleux-Bonnin F, Federici BA (2000)
Characterization of repetitive DNA regions and methyl-
differed from the closely related TAV and HAV
ated DNA in ascovirus genomes. J Gen Virol 81:
genomes (180 kbp). Histological examinations 30733082
revealed that TAV and HAV both replicated in the
nuclei of epidermal and mesodermal insect tis-
sues, whereas SAV replication was restricted to fat
body tissue. Asexual
Ascovirus infections normally retard growth
and development of diseased larvae. This virus, Lacking separate sexes, and reproducing by
originally identified as a Rickettsial-like organ- parthenogenesis.
ism, is slow acting, causing larval death after a
prolonged period (2030 days) of arrested larval
growth. These viruses infect a limited number of Ash-Gray Leaf Bugs
cells within a particular tissue. Examination of
the milky infected hemolymph under light Members of the family Piesmatidae (order
microscopy revealed the presence of numerous Hemiptera).
virion-containing vesicles. These vesicles are Bugs
306
A Ash Whitefly, Siphoninus phillyreae (Hemiptera: Aleyrodidae)

Ash Whitefly, Siphoninus in size, off color, and having objectionable flavor. In
phillyreae (Hemiptera: Southeast Asia, mandarins and oranges are the
Aleyrodidae) main citrus trees planted in commercial groves, and
they are the most susceptible cultivars. Liberobactor
This species affects citrus and other shrubs and asiaticum is a phloem-limited, gram-negative bac-
trees. See also, Citrus Pests and their Management, terium which also can be readily transmitted by
Hemiptera. grafting and propagating with infected plant mate-
Citrus Pests and their Management rial. Both the nymph and adult can transmit the
greening agent in 15 min acquisition feeding time.
The incubation period in the vector is about 3
Asian Citrus Psyllid, Diaphorina weeks. The infectious vector can retain the patho-
citri Kuwayama (Hemiptera: gen for life.
Psyllidae) The length of the life cycle of Asian citrus psyl-
lid varies from 27 to 117 days, depending on rearing
temperature and host plants. The average develop-
james h. tsai mental time for the immature stages is from 14 to 49
University of Florida, Ft. Lauderdale, FL, USA days within 1528C. D. citri nymphs undergo five
instars. The adult longevity averages from 34 to 88
The Asian citrus psyllid Diaphorina citri, is of Far days within the temperature range of 1530C. The
Eastern origin and is also called the oriental maximal longevity of individual females is 117 and
citrus psyllid. Its known range of distribution 51 days at 15 and 30C, respectively. The individual
covers tropical and subtropical Asia including female may lay more than 748 eggs at 28C. A total
India, Burma, Thailand, Nepal, Sikkim, Hong of 1,378 eggs have been reported to be deposited by
Kong, Ryukyn Islands, the Philippines, Malaysia, a single female on grapefruit. Asian citrus psyllid
Indonesia, Ceylon, Pakistan, Afghanistan, can feed and breed on most citrus spp., two species
Reunion, and Mauritius. It is also found in Saudi of Murraya and three genera of Rutaceae. The devel-
Arabia in the Near East, and Brazil in South opmental time of immature stages on various host
America. This insect was first discovered in the plants varies significantly, ranging from 69 days on
United States in 1998, and is now widespread in sour orange to 85 days on grapefruit. The average
southern Florida. adult longevity on rough lemon is significantly lon-
Diaphorina citri causes severe damage to citrus ger than those on orange jassamine, grapefruit and
by: (i) withdrawal of a large quantity of sap from the sour orange. However, the females preferentially lay
foliage, affecting the overall growth of citrus, and more eggs (averaging 858 eggs/female) on grape-
promotion of sooty mold on honeydew secreted fruit than the other hosts mentioned above. The egg
onto leaves, which results in reduction of photosyn- incubation period is about 4 days regardless of host
thesis; and (ii) efficient transmission of greening plants. Eggs are deposited within 2 cm lengths of
bacterium (Liberobacter asiaticum) by D. citri. The terminal tissue, including leaf folds, petioles, axillary
greening disease (Huanglungbin) is a limiting fac- buds, upper and lower surfaces of young leaves and
tor in citrus production in the Far East, though it tender stem. The egg is anchored on a slender stock-
does not occur in Florida. Citrus infected by the like process arising from the plant tissue. The egg is
greening agent initially shows leaf mottling and elongate, with a broad basal end and tapering
chlorosis symptoms, followed by stunted growth, towards its distal and curved end. The average size of
unseasonable bloom and leaf and fruit drops. Even- egg measures 0.31 mm long and 0.14 mm wide.
tually, branch dieback and a general decline will Freshly deposited eggs are light yellow, turning
result. Fruits from infected trees are small, uneven bright orange with 2 distinct red eye spots at maturity.
 Asian Citrus Psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae)
A 307

First and 2nd instar nymphs mostly aggregate and metathoracic wing pads extend to 4th abdominal
feed on the inside of folded leaves, the terminal stem segment. In some mature nymphs, the abdominal
and between the axillary bud and the stem of tender color turned bluish green instead of pale orange.
shoots. Young nymphs are quite docile and they only Adults of D. citri (Fig.87) are often found to
move when disturbed or overcrowded. The nymphs rest on the terminal portion of plants, especially
continuously secrete a copious amount of honeydew on the lower side of the leaves, with their heads
from the anus, and thread-like waxy substance from pointing to the leaf surface at a 30 angle. When
the circumanal glands, resulting in the growth of disturbed, they readily take flight to a short dis-
black sooty mold on the lower leaves. The average tance. The females only oviposit on the tender
size of 1st instars measures 0.30 mm in length and shoots. In the absence of suitable tissue, oviposi-
0.17 mm in width with light pink body and a pair of tion ceases temporarily. The average size of the
red compound eyes. The measurement of 2nd instars adult female is 3.3 mm in length and 1.0 mm in
averages 0.45 mm long and 0.25 mm wide. The rudi- width; the mean size of the adult male is 2.7 mm
mentary wing pads are visible on thoracic dorsum. long and 0.8 mm wide.
The average size of 3rd instars is 0.74 mm long and Control of Asian citrus psyllid can be achieved
0.43 mm wide. The wing pads are well developed by insecticide application. It is advisable to target
and the segmentation of antenna is evident. The 4th the nymphs, (Fig.88) as they are less mobile and
instar averages 1.01 mm long and 0.70 mm wide. concentrated on terminal tissue. However, other
The wing pads are well developed; the mesothoracic non-chemical control methods have been widely
wing pads extend towards 1/3 of compound eyes and accepted; they include the use of such natural
the metathoracic wing pads extend to 3rd abdominal enemies as syrphids, chrysopids, coccinellids and
segment. The 5th instar averages 1.60 mm long parasitic wasps. The success in Reunion of using the
and 1.02 mm wide. The mesothoracic wing pads eulophid (Tamarixia radiata Waterston) to control
extend towards the front of compound eyes; the Asian citrus psyllid is a good example of biological

Asian Citrus Psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), Figure 87 Adult Asian citrus
psyllid, Diaphorina citri (photo J. Tsai).
308
A Asiatic Garden Beetle, Maladera castanea (Coleoptera: Scarabeidae)

Asian Citrus Psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), Figure 88 Nymphs of Asian
citrus psyllid (photo Lucy Skelley, University of Florida).

control. Other control measures, such as injecting with tree diseases in China. In: Hiruki C (ed) Tree
mycoplasmas and mycoplasma disease. The Uni-
infected trees with tetracyline antibiotics, establish- versity of Alberta Press, AB, Canada, pp 69240
ing disease free nursery and monitoring and remov- Tsai JH, Liu YH (2000) Biology of Diaphorina citri
ing diseased trees from the grove are also known to (Homoptera: Psyllidae) on four host plants. J Econ
Entomol 93:17211725
be effective.
Tsai JH, Wang JJ, Liu YH (2000) Sampling of Diaphorina citri
(Homoptera: Psyllidae) on orange jassamine in south
Florida. Fla Entomol 83:446459
References

Liu YH, Tsai JH (2000) Effects of temperature on biology

and life table parameters of the Asian citrus psyllid
Diaphorina citri Kuwayama (Homoptera: Psyllidae). Asiatic Garden Beetle, Maladera
Ann Appl Biol 137:201206 castanea (Coleoptera:
Mead FW (1977) The Asiatic citrus psyllid, Diaphorina citri
Kuwayama (Homoptera: Psyllidae). Florida Department
Scarabeidae)
of Agriculture and Consumer Services, Division Plant
Industry, July 1977 A native of Asia, this insect was accidentally intro-
Pande YD (1971) Biology of citrus psyllid, Diaphorina citri duced to northeastern North America where it
Kum (Hemiptera: Psyllidae). Israel J Entomol 5:
307311
became a turf pest. See also, Turfgrass Insects and
Tsai JH, Chen ZY, Shen CY, Jin KX (1988) Mycoplas- their Management.
mas and fastidious vascular prokaryotes associated Turfgrass Insects and their Management
 Asparagus Aphid, Brachycorynella asparagi (Mordvilko) (Hemiptera: Aphididae)
A 309

Asilidae into stem mothers (fundatrices). Fundatrices move

to asparagus spears and give birth to about 18
A family of flies (order Diptera). They commonly nymphs. Subsequent generations may be apterous
are known as robber flies. (wingless) or alate (winged). Sexual forms are pro-
Flies duced in the autumn, mate, and the females deposit
Robber Flies eggs on the asparagus plant. Duration of a com-
plete generation is about 1519 days at 25C.
The eggs initially are green in color, but turn
Asiopsocidae shiny black within 12 days. Females produce, on
average, 10.5 overwintering eggs during their life
A family of psocids (order Psocoptera).
span. The elliptical eggs are deposited in the lower
Bark-Lice, Book-Lice or Psocids
one-third of the asparagus canopy.
The grayish green nymphs exhibit four instars,
Asiopsocidae the durations of which are about 2 days each,
regardless of the morph or sex. Thus, nymphal
A family of psocids (order Psocoptera). development time averages about 89.5 days. Each
Bark-Lice, Book-Lice or Psocids female produces about 55 nymphs at 23C, but only
27 and 9 at 14 and 32.5C, respectively.
Both the alate and apterous adult viviparous
Asparagus Aphid, Brachycorynella aphids are present throughout the summer
asparagi (Mordvilko) (Hemiptera: months, and reproduce parthenogenetically. The
Aphididae) adults are relatively small, measuring 1.21.7 mm
in length, and with short antennae. They are elon-
john l. capinera gate oval in shape, and green or gray-green in
University of Florida, Gainesville, FL, USA color, often covered with a whitish waxy secre-
tion. They blend in well with asparagus foliage,
Asparagus aphid is found widely in eastern Europe but impart a slightly bluish gray tint when the
and along the Mediterranean Sea. It invaded North infestation is heavy. The most important charac-
America about 1969, where it was first detected in ter for distinguishing viviparous asparagus aphid
New York. It dispersed (or was dispersed) quickly, from other asparagus-infesting species is the
attaining North Carolina in 1973, British Colum- inconspicuous cornicles and long cauda of
bia in 1975, Missouri and Washington in 1979, B.asparagi. Egg-producing females survive up to
Alabama,Georgia, Oklahoma and Idaho in 1981, about 20 days.
and California in 1984. Although it is abundant This aphid feeds only on species of Asparagus.
across the northern portions of North America, In addition to garden asparagus, Asparagus officina-
andvery abundant along the west coast including lis, it is known to feed on ornamental Asparagus spp.
southern California, it is uncommon in the humid A large number of native predators, parasitoids,
southeastern states. and insect diseases affect asparagus aphid. Among
the most important are ladybirds (Coleoptera: Coc-
cinellidae), green lacewings (Neuroptera: Chrysopidae),
Life History and a parasitoid of many aphid species, Diaeretiella
rapae (MIntosh) (Hymenoptera: Braconidae).
Oviparous aphids deposit overwintering eggs on Other species of some importance are brown lace-
asparagus ferns in September or later. Beginning wings (Neuroptera: Hemerobiidae), the predatory
in about March, eggs hatch into aphids that develop midge Aphidoletes aphidimyza Rondani (Diptera:
310
A Aspergillus Spp. Fung

Cecidomyiidae), flower flies (Diptera: Syrphidae), research has also been done to demonstrate the
and other wasps (Hymenoptera: Braconidae and possibility of delivering insecticides to asparagus
Aphelinidae). Natural enemies are reported to keep through the irrigation system.
the population in check in eastern North America, Several cultural practices for suppression of
but once attaining the arid western regions of North asparagus aphid were investigated. Autumn and
America asparagus aphid developed into a severe spring tillage reduce aphid overwintering but also
pest, and was seemingly little influenced by natural reduce subsequent spear production. Mowing and
enemies. This suggests that climate plays a signifi- herbiciding within asparagus fields can destroy
cant role, perhaps in conjunction with weather-sensi- early season aphids and delay the buildup of dam-
tive natural enemies such as fungi. aging populations. However, destruction of wild
(volunteer) asparagus is the most important cul-
tural practice available because it eliminates over-
Damage wintering sites and limits invasion of aphids into
commercial, aphid-free fields. Herbiciding, burning
Aphids feed on the new growth, causing shortening
and removal of asparagus crowns by digging are all
of the internodes, rosetting, dwarfing, and reduced
viable options to eliminate volunteer asparagus.
root growth. Asparagus aphids deplete the sugars,
particularly in the roots, and to a greater degree than
some other aphids. Heavily infested plants have a References
bushy or bonsai-like appearance. Aphid infestation
can kill seedlings or small plants in a relatively short Capinera JL (2001) Handbook of vegetable pests. Academic
time. Older, well established plantings may show Press, San Diego, CA, 729 pp
Hayakawa DL, Grafius E, Stehr FW (1990) Effects of tem-
damage and even death in the year following infesta- perature on longevity, reproduction, and development
tion by aphids, especially following a particularly cold of the asparagus aphid (Homoptera: Aphididae) and
winter. Freezing and aphid infestation are synergistic; the parasitoid, Diaeretiella rapae (Hymenoptera:
Braconidae). Environ Entomol 19:890897
together they reduce survival and vigor of dormant
Tamaki G, Gefre JA, Halfhill JE (1983) Biology of morphs of
asparagus crowns greater than either aphid feeding or Brachycolus asparagi Mordvilko (Homoptera: Aphidi-
freezing alone. The threat of damage is much greater dae). Environ Entomol 12:11201124
in western areas than in eastern North America, and Wright LC., Cone WW (1986) Sampling plan for Brachyco-
rynella asparagi (Homoptera: Aphididae) in mature
it remains an infrequent pest in Europe. asparagus fields. J Econ Entomol 79:817821
Wright LC, Cone WW (1988) Population dynamics of Brachy-
corynella asparagi (Homoptera: Aphididae) on undis-
Management turbed asparagus in Washington state. Environ Entomol
17:878886
Egg hatch can be predicted from temperature Wright LC, Cone WW (1988) Population statistics for the
asparagus aphid, Brachycorynella asparagi (Homoptera:
models. Eggs can be separated from foliage by Aphididae), on different ages of asparagus foliage. Envi-
washing with petroleum cleaning solvent. Nymphs ron Entomol 17:699703
can be extracted from plants by heat or methyl
isobutyl ketone. Aphid distribution tends to be
clumped, with most aphids in basal regions of the Aspergillus spp. Fungi
plants. A sample of about 140 branches per field is
optimal for making management decisions. Aspergillus spp. fungi cause a disease in honeybees
Foliar insecticides can suppress aphids, but called stonebrood. Several species may be involved,
multiple applications may be necessary, especially although A. flavus and A. fumigatus are most com-
under high density conditions. Granular systemic monly implicated.
insecticides may provide long term control. Some Stonebrood
 Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae)
A 311

Aspirator and relationships between them remain unset-

tled. Subfamilies Harpactocorinae (about 2,000
A device used to collect small terrestrial arthro- species), Reduviinae (about 1,000 species), Eme-
pods. Although there are many variations in design, sinae (about 900 species), Stenopodinae (more
the principle behind the designs is the same air than 700 species) and Ectenodeminae (more than
current causes the insect to be sucked (aspirated) 600 species) together total more than 80% of
into a tube or tubing that leads to a container/ known reduviid species. An additional five minor
receptacle area. The key feature of the aspirator is subfamilies contain only 3 or 4 species. Ten gen-
that although the arthropod can be sucking into era contain between a hundred and two hundred
the container, it cannot be sucked further (inhaled species each.
in the case of mouth aspiration) because a fine
screen blocks its egress, so it is retained/captured.
The principal variables associated with aspirators Morphology
are the form of suction (mouth or mechanical),
length and shape of the tube/intake, and the size of Adult bugs vary greatly in body size, ranging from
the container/receptacle. This apparatus works well 3.5 mm in such reduviids as the genus Empicoris
for small and/or weakly flying insects. (Emesinae) to 40 mm in the genus Arilus (Harpac-
torinae). The body shape is also extremely vari-
able. Reduviidae may be robust and oval, as occurs
Assassin Bugs, Kissing Bugs and in the genus Reduvius, to elongate and thread-like,
Others (Hemiptera: Reduviidae) as in the genus Empicoris. Body coloration may be
cryptic or aposematic. Most species are dark in
eva ribes1, marta goula1, xavier jeremas2 color, with hues of brown, black, red, or orange.
1
University of Barcelona, Barcelona, Spain Others are masters of disguise and camouflage,
2
Museum of Natural Science (Zoology), colored to blend with their substrate or to resem-
Barcelona, Spain ble their prey. Many species are very hairy or spiny,
with varied body expansions.
The Reduviidae are a large, cosmopolitan, and Reduviidae can be distinguished from other
morphologically diverse family of predatory true bug families by their elongated head, with a trans-
bugs. They include assassin bugs (genera include verse groove behind the compound eyes, and the
Melanolestes, Psellipus, Rasahus, Reduvius, Rhiginia, short, prominent, apparently three-segmented
Sinea, and Zelus), wheel bugs (Arilus cristatus), rostrum curved (Figs.89 and 90) outwards from
kissing bugs (species of Triatoma, Rhodnius and the head. A characteristic of the family is that the
Panstrongylus), ambush bugs (genera Apiomerus tip of the rostrum, in repose, fits into that groove.
and Phymata), and thread-legged bugs (the sub- The head has a pair of large compound eyes,
family Emesinae, including the genus Emesaya). usually two ocelli, and a pair of four-segmented
antennae about the same length as the body. How-
ever, subdivision of antenna segments gives an
Taxonomy appearance of antennae with a larger number of
segments. The forewings (hemelytra) lack the
In 1843, Amyot and Serville recognized the costal feature, and the membrane usually has two
reduvids as a discrete group. In its present sys- elongated cells and a few veins emanating posteri-
tematic organization, the large family Reduviidae orly. Legs are usually long, normally with 3-seg-
contains around 25 subfamilies, about 930 genera mented tarsi, although the tarsal formula is
and 6800 species. Composition of subfamilies variable.
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A Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae)

the likelihood that they will enter inhabited struc-

tures and contact humans.
Reduviidae are well adapted for their physical
environment. They may pass through inclement
periods in the egg, nymphal or adult stage. Num-
ber of generations per year ranges from one to
several, but in other cases the completion of life
cycle may take more than 1 year. Longevity is also
very variable among species. Some Salyavatinae
live <2 weeks, whilst some Reduviinae live for
about 7 months.
Except for Triatominae, which are hematopha-
Assassin Bugs, Kissing Bugs and Others gous and feed on vertebrate blood, all reduviids
(Hemiptera: Reduviidae), Figure 89 A ventral prey on other insects. First step of attack is with the
view of the reduviid head, showing the curved legs, whose length allow a longer attack distance.
rostrum and a groove located ventrally. A Also, the legs of some of these bugs are covered in
characteristic of the family is that the tip of the tiny hairs that serve to make them sticky to grip
rostrum, in repose, fits into that groove. prey while they feed in the manner of flypaper.
Other assassin bugs (subfamily Apiomerinae) go
one step further and collect certain plant resins
The male genitalia are usually symmetric and which they spread over their front legs; these resins
the ovipositor of females is usually plate-like. Eggs are very attractive to insects, and to bees in particu-
have three or more micropyles. lar. Once the prey is grasped, the reduviid feeds by
puncturing it with sharp stylets in their rostrum,
injecting saliva which will paralyze the prey and
Biology liquify its tissues, to then finally sucking up the
body fluids. The saliva is commonly effective at
Despite their abundance and interest, reduviids have killing prey substantially larger than the predatory
been largely ignored, and we do not know much on bug itself. In contrast, the genus of the small
their biology. Triatominae are the exception, as their reduviid Ptilocerus uses chemical lures located in a
relationship with human diseases has stimulated special ventral abdominal gland to trap and prey
their study under laboratory conditions. on ants. The ants are very attracted by this secre-
Reduviidae may live in a variety of habitats in tion, which paralyses them. Also, reduviids that
the wild, and tend to occupy warm environments. tackle large and dangerous prey like wasps or bees
Sylvatic triatominae are found in burrows and tend to make the first stab near the victims head or
nests of wild vertebrates, among rocks, fallen tim- neck, thus ensuring that their toxic saliva has maxi-
ber, hollow trees, roots, palms and bromeliads. In mum effect in the shortest possible time.
the subfamily Emesinae, some species are caverni- In Triatominae, ingestion of blood is possible
colous, but lack the characteristics common to thanks to different enzymes present in the bug
many cave dwellers such as eyelessness or depig- saliva that counterbalances the hemostatic response
mentation. Among Emesinae and Triatominae, on the part of the vertebrate host. Bug saliva is pro-
some species are domestic or peridomestic, which vided with anticoagulants (preventing the coagula-
increase the medical importance of Triatominae tion of host blood in the insects suction apparatus),
as vectors of the protozoan Trypanosoma cruzi. apyrases, platelet antiaggregation factors, antisero-
The attraction of Triatominae to light also enhances tonin, antihistamine, tryalisine (lytic protein which
 Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae)
A 313

Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae), Figure 90 Some reduviids:
(a) Anterior view of a reduviid, showing their elongated head and the short, prominent, apparently
3-segmented rostrum curved outwards from the head; (b) adult wheel bug, Arilus cristatus. This is one
314
A Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae)

permeabilizes mammalian cells), emollient factors, 670 eggs of Harpactorinae. Eclosion and ecdysis
antithromboxane and a vasodilator. Blood is stored occur usually in daytime.
in the crop and stomach of triatomine. Several days Many species glue their eggs to the plants,
later, erythrocytes are lysed, and the accessible often in a group, sometimes covering the eggs with
hemoglobin is then digested. Blood ingestion is a gelatinous material. Ground-dwelling species
needed by nymphs to complete development, and may bury their eggs in the soil, and some species
by adults to perform reproduction, as cyclical egg of the subfamily Reduviinae have more well-de-
laying is related to blood meals. veloped ovipositors, suitable for the insertion of
Reduviids are generally polyphagous, but eggs into cracks.
there are also cases of prey specialization. For A few species are known to guard their eggs,
example, the subfamily Emesinae contains a num- and in this case, the males perform the guarding. In
ber of genera (Eugubinus, Ploiaria, Emesa, the genus Rhinocoris, the female lays a batch of
Stenolemus and Empicoris) in which elongate, eggs on the plant leaf immediately after copulating.
thread-legged member species feed on insects The male stands by and, when the female finishes
caught in spiders webs, or on the spiders them- laying, takes up his position aside the egg mass.
selves. These slender, slow-moving bugs never get Over the course of the next days the female lays
trapped in the spider silk, as they avoid the sticky additional egg batches. While the male is guarding
spirals and walk very carefully so that they are not he generally does not feed, unless an easily catch-
trapped in the spider silk. An extraordinary case able prey comes his way. However, when the eggs
of coprophagy is found in the Indian harpactorine have all hatched, he loses interest and moves away.
Lophocephala guerini, which feeds on fermenting Exceptionally, the guarding male may be relieved
cow dung. Its microhabitat is underneath stones, by a female that had copulated with him.
in association with the formicine ant Anoplolepis In the majority of nymphs and adults, the ros-
longipes, and it is always attended and guided by trum can be used to produce sounds (stridulation)
these ants. However, the trophic habits of most by being scraped along a medially located, ridged
reduviid species are still unknown. groove on the underside of the thoracic segments.
Courtship behavior is much like in other The aim of this acoustical communication may be
insects, although it has some characteristic fea- mate attraction, courtship and copulation. In other
tures. The sequential acts of mating behavior can cases, the aim is intimidation, and thus, some
be categorized into arousal, approach, riding over reduviids stridulate defensively. Non-receptive
(precopulatory riding of Harpactorinae), nuptial females may emit male-deterring vibrations.
clasp, extension of genitalia and connection, copu- Reduviids have an array of defensive and
lation, and postcopulatory acts. The fecundity var- offensive behaviors, accompanied by morphologi-
ies between 50 eggs of the Stenopodainae to the cal adaptations. These behaviors threaten other

of the largest and most easily recognized reduviids. It is found in North America and Central America,
where it feeds on numerous insects, but also inflicts a nasty bite when handled by humans; (c) nymphal
wheel bug, Arilus cristatus; (d) nymphal wheel bug, Arilus cristatus, feeding on a leaftier larva; (e) adult
Sinea diadema. This species is found through most of North America including Mexico, where it inhabits
meadows and crop fields. It often is reported to be an important predator of crop pests; (f) nymphal
Vibertiola cinerea, an African savanna-inhabiting species that is now found in the Iberian Peninsula. Its
host plant is the grass Hyparrhenia hirta, where it blends in well due to its elongated body; (g) Rasahus
sp. bugs are found p redominantly in the neotropics; (h) Zelus longipes is found throughout the western
hemisphere where its often found feeding on caterpillars (photo credits: f, Eva Ribes, University of
Barcelona; others Lyle Buss, University of Florida).
 Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae)
A 315

insects, aid escape from enemies and larger prey, as beneficial. They kill more prey than they need to
and give protection from cannibalism. Some satiate themselves. Reduviids exhibit a positive
nymphs and adults of different subfamilies (Redu- numerical response by killing more prey in terms
viinae, Cetherinae, Salyavatinae, Triatominae) will of available prey population per predator at a given
cover and camouflage themselves with debris, time, and by increasing their population through
including soil particles or the remains of dead higher fecundity and survival.
preyed insects, which are affixed by sticking objects In spite of their merits as beneficials, their
to the viscid secretions of specialized setae located potential as biocontrol agents of pests has been
on the dorsum. The elongated slender bodies of little studied. The better studied species in this area
Rhaphiodosoma and Vibertiola species (Harpac- focus on Rhinocoris fuscipes, R. kumarii, R. margi-
torinae) and stenopodaeines provide camouflage natus, Ectomocoris tibialis and Acanthapsis pedes-
among the elongated grasses where they live, tris. Other promising groups of predatory reduviids
imparting protection from vertebrate predators. are species of Sinea and Zelus, which may help
In other cases defense is active, as in harpactorine regulate insect pests on cotton. Recently, Amphi-
nymphs, which often fight to the death. bolus venator has been reported as a useful preda-
tor on last-instar larvae, pupae and adults of the
stored-product insect pest Trobolium confusum
Some Aspects of Distribution (red flour beetle [Coleoptera: Tenebrionidae]).
Amphibolus venator is commonly found in stored
The distribution of Reduviidae is nearly cosmo- product facilities, shipments of groundnuts, ware-
politan, though most taxa inhabit the tropical and houses or in rice milling facilities, and preys on
subtropical regions, where they are particularly other stored-product insect pests.
varied and abundant. Of the 6,800 species, 16% Because of their polyphagy, reduviids may
occur in Oceania, 37% in sub-Saharan Africa and not be useful as predators on specific pests, but
21% in the neotropics. Certain taxa with a wide they are a valuable help when a variety of insect
distribution suggest transport by humans and pests occur. The counterpart of that polyphagy is
their goods, or by migratory animals. that from time to time they may attack beneficial
arthropods. A few of them appear to specialize
on insects of some value; for example, several
Ecological and Economic apiomerine reduviids feed on bees of the genus
Significance Trigona, that are useful pollinators.
Unfortunately, assassin bugs interact with
As predators, Reduviidae play a role in biological human health negatively. They may become a nui-
control. Their worldwide distribution, abun- sance, as many assassin bugs have been known to
dance, diversity, large pest prey record, amenabil- bite humans when not handled carefully. For some
ity for mass culturing, ready synchronization and species the bite is known to be very painful, some-
freedom from hyperparasites and predators are times causing allergic reactions, and bites can
the merits of reduviids as potential biological become infected, as with any wound. Some of
control agents. them are known to produce toxic saliva contain-
More than 150 reduviids predators belonging ing powerful enzymes similar to those in snake
to 53 genera and seven subfamilies have been found venom. As with any severe allergic reaction in
preying upon a wide array of insect pests. Some humans, side effects of repeated bites may include
species have been known to feed on cockroaches shock and possible death. The fecal material of
or bedbugs (in the case of the masked hunter Redu- some reduviids can cause irritation of the eyes and
vius personatus) and are regarded in many locations nose and temporary blindness in humans.
316
A Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae)

Most important to human health are some additional species belonging to the three genera
blood-feeding triatominae species, also known as mentioned above can also act as disease vectors,
kissing bugs due to their habit of biting humans but they are more local in distribution so they are
in their sleep on the soft tissue of the lips and not as important, or as well known. Other genera
eyes. A number of these hematophagous species involved locally in transmission of HCD are Mec-
are able to transmit a potentially fatal trypanosome cus (Mexico), and Microtiatomba and Para-
disease known as human Chagas disease (HCD), belminus (Brazil). Infestation rates of triatominae
also named American trypanosomiasis, caused by Trypanosoma cruzi vary greatly from one area
by the protozoan Trypanosoma cruzi. These redu- to another. As examples, in Brazil, 41% of 2412
viids belong to genera Triatoma, Rhodnius and triatominae bugs were infested whereas in Pan-
Panstrongylus, and the three most important spe- ama, 68.8% of 740 Rhodnius pallescens were
cies in this regard are Triatoma infestans, T. dim- infested, but only 17.7% of 94 Triatoma dimidiata
idiata and Rhodnius prolixus (Fig.91). About 50 were. In Yucatan (Mexico), infection rates of

Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae), Figure 91 Kissing bugs or
bloodsucking conenoses, Triatoma spp.: (a) adult T. dimidiata; (b) immature of T. sanguisuga; (c) adult of
T. sanguisuga (photo credits: a, Ron Cave; others Lyle Buss, both University of Florida).
 Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae)
A 317

Triatoma dimidiata by T. cruzi ranged from 0% ral balance and habitats of T. cruzi, its triatomine
(in Tipoco) to 25% (in Tella). In Santander vectors, and its mammalian reservoirs.
(Colombia), 48% of T. dimidiata contained the Kissing bugs are strictly nocturnal, taking
protozoan, while in Guayaquil (Ecuador), 50% blood meal for 2030 min and inflicting no pain to
were infested. Once infested, a bug may be infec- the host. When they feed, the bugs leave (infected)
tive for about 2 years. In contrast with other excrement behind on the skin. Transmission of the
arthropod vectors (i.e., ticks), the protozoan can- protozoan occurs when people scratch their bites
not be transmitted to the offspring transovarially. and allow protozoa in bug defecations to infect
In 1909, the Brazilian doctor Carlos Chagas their blood. Other forms of transmission are pos-
discovered the disease, and reported both the vec- sible, though, such as ingestion of raw food con-
tor and the causative flagellate protozoan Trypano- taminated with parasites, blood transfusion, organ
soma cruzi. He recognized and described the disease transplantation and placental transmission (from
in humans but also investigated the life cycle and infected mother to fetus).
other aspects of the protozoan and its insect vector. The human disease occurs in three stages or
This disease is mostly found in rural areas, where phases: (i) the primary or acute phase, shortly after
the Triatominae can breed and feed on the natural the infection, with an incubation of 15 (direct
reservoirs, such as opossums, raccoons, and arma- bite)-40 days (blood transfusion infection); symp-
dillos. In fact, wild animals reported as infected toms are an inflammatory reaction, with necrosis
with T. cruzi belong to the Orders Marsupialia around the bug bite site; meningoencephalitis and
(opposums), Edenteta (armadillos, etc.), Chiroptera myocarditis are very severe consequences of this
(bats), Carnivora (cats, foxes, etc.), Lagomorpha stage in children under 10 years old; (ii) indetermi-
(rabbits), Rodentia (mice and rats, squirrels) and nate phase, 810 weeks after the acute stage and
Primates (monkeys). But, depending on the special which may last for years without any symptom; the
local interactions of the vectors and their hosts, main danger is that the individual is unaware of
other infected humans and domestic animals may being infested, acting as reservoir of T. cruzi; (iii)
act as reservoirs too. Among domiciliary and peri- chronic stage that may develop up to 10 years after
domiciliary reservoirs are Canis familiaris (dog), infection; the main signs are liver and heart dys-
Capra hyrcus (goat), Cavia porcellus (Guinea pig), functions, as well as, hypertrophy of the heart and
Felis domesticus (cat), Mus musculus (mice), Orycto- certain parts of the digestive and/or excretory sys-
lagus cuniculus (rabbit), Rattus novervegicus and tems. The parasite circulates in the bloodstream,
Rattus rattus (rats) and Sus scrofa (pig). and infects, multiplies and ultimately destroys
Trypanosoma cruzi may have both sylvatic and muscle and nerve cells all around the body, partic-
domestic cycles. The sylvatic cycle involves its cir- ularly in the heart and digestive system. The nega-
culation among wild small mammals and the Tri- tive effects of the disease are reflected in a
atominae. The sylvatic cycle usually does not affect progressive deterioration of health, associated to
humans unless they enter in the wild and disturb increasing apathy, a decreasing capacity to perform
the natural balance of wild fauna and flora. The work and a general reduction in the quality of life.
domestic cycle, which has evolved more recently, If no action is taken, disease is lethal.
involves humans, domestic mammals and a small The disease is distributed in the Americas,
number of Triatominae species that are able to live ranging from the southern United States to south-
in domestic or peridomestic habitats. Although ern Argentina, mostly in poor, rural areas of Cen-
some reports on Chagas disease date back to preco- tral and South America. Domestic infestation in
lumbian times, the real dispersion of the American very poor rural zones may be of 1,000 insects per
trypanosomiases occured as a result of European house. Human Chagas disease (HCD) has been
conquest and the resulting disturbance of the natu- spread into nonendemic urban areas by people
318
A Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae)

migrating to cities from rural areas. In most coun- efficient and permanent reduction of triatomine
tries where Chagas disease is endemic, testing of vectors in peridomestic areas. Also, several plant
blood donors is already mandatory, since this can extracts showed insecticidal activity against tri-
be an important route of transmission. Up to 18 atomines. As examples, plants belonging to genera
million humans were affected by this disease in Salvia, Annona, Neurolaena, Tagetes, Erythroxylon,
1990, but recently data suggests nine million peo- Cassia, Senna and Cabralea elicited an increase in
ple affected, after coordinated initiatives through- the mortality rate (1652%) of Rhodnius neglectus.
out the endemic HCD area. Of some 100 million Topical treatment of T. infestans with Achryrocline
at risk of acquiring the disease in 1990, now about extracts resulted in a 45% mortality of triatomine
60 million people are out of risk. About 200,000 bug. Five plant species (Aspidosperma macrocarpon,
new cases, and about 70,000 deaths are reported Talauma ovata, Guarea guidonia, Guarea kunthiana
annually. Rates of human infection in endemic and Simarouba versicolor) from the Brazilian biome
areas are very different, relating to different vector Cerrado, selected according to ethnobotanical
species or populations. In Zacapa (Guatemala), information, have been tested in the form of 24
where R. prolixus is the principal vector, 38.8% of plant crude extracts on Rhodnius milesi. Most prom-
373 people were infected. In contrast, in Santa ising results were obtained from ethanolic extract
Rosa (Guatemala), where T. dimidiata is the only of the root bark of S. versicolor (probably due to its
vector found, only 8.9% of the 428 people studied antifeedant growth regulating activity) and the
had the protozoan. The same trends were reported hexane extract of the root of G. guidonia (by a not
in Honduras, in relationship to HCD vectors. Out- yet clear activity). In addition to investigating new
side of the Americas, one genus and several bug methods to kill triatomine bugs, considerable
species occur in India, where theoretically they success has been made preventing bugs taking up
may transmit Chagas disease. residence in human domiciles.
Once infected, there are some pharmaceuticals However, the peridomicilium (considered to be
useful to fight infections, but they are very toxic and the area within 100 m proximity of human dwell-
have a lot of undesirable secondary effects. The best ings) has been shown to be crucial in management of
way to reduce HCD incidence is prevention, either HCD. Henhouses, pigpens, corrals, perches, piles of
by fighting the vector (Triatoma) or improving tiles, bricks, wood and straw have to be taken into
housing and sanitary conditions in the rural area. account. In research conducted in 121 peridomicili-
Vector insects may be eliminated by using sprays ary environments in rural areas of the state of Cear
and paints containing insecticides (synthetic pyre- (Brazil), triatominae (2670 specimens collected)
throids). Although resistance development is much were present in 30% of the environments, with 68.7%
lower than in mosquitos (due to long life-cycle and being shelters for domestic animals (mainly goat/
use of different insecticides), significant levels of sheep corrals, perches, henhouses and pigpens), and
resistance to deltamethrin and other pyrethroids 32.3% were piles of bricks, roofing tiles or wood. Also,
have been reported in Rhodnius proxilus (Venezu- palm trees growing near human habitations are of
ela) and Triatoma infestans (Brazil and Argentina). great importance in HCD, as Rhodnius species breed
Recently, oil-formulated Beauveria bassiana has in the crowns of many genera of palm trees. Specific-
been used against T. sordida and has proven to be ity among insect and palm tree species may be very
useful in peridomestic areas of central Brazil. This strict, as is the case of R. brethesi on Leopoldinia pias-
could lead to implementation of integrated control saba, or R. colombiensis on Attalea butyracea, but this
by alternating application of fungi in the rainy sea- is not always the case, as in R. pallescens or R. pictipes,
son with synthetic insecticides in the dry season, or which dwell in association with five host palm spe-
a combined application of fungi and insecticides in cies each, or R. prolixus, with 13 host palm species.
the rainy season. Those strategies could promote an Peridomestic palm trees, especially in the presence
 Assemblage
A 319

of bird nests, may be regarded as high-risk habitats. as T. cruzi and its wild reservoirs. Schools and hos-
In Ecuador, the palm seed endosperm (vegetable pitals (obstetrics, blood donors, organ transplanta-
ivory or tagua) and leaves of Phytelephas aequato- tion) are essential surveillance hot-spots where
rialis are used for handicraft manufacturing and infestations may be detected and controlled.
roof thatching; as a result, those palms, which are Bugs (Hemiptera)
the primary habitat of Rhodnius ecuadoriensis (a Trypanosomes
major vector of Chagas disease in Ecuador and Chagas Disease: Biochemistry of the Vector
Peru), are often found around dwellings. Area-Wide Pest Managment
For urban dwellers who spend vacations Chagas Disease or American Trypanosomiasis
outdoors or camp in the wilderness, or who sleep Parental care
at hostels or primitive houses in HCD-endemic Acoustical Communication
areas, a mosquito net is recommended to reduce
the risk of infection. If the traveler intends to References
travel to an area of HCD prevalence, he/she
should get information on the incidence of Cha- Ambrose DP (1999) Assassin Bugs. Science Publishers,
gas disease from traveler advisories, such as the Enfield, New Hampshire, 337 pp
USAs Communicable Disease Center (CDC). Ambrose DP (2000) Assassin bugs (Reduviidae excluding
Triatominae). In: Schaefer CW, Panizzi AR (eds) Het-
The Southern Cone Initiative against HCD was
eroptera of economic importance. CRC Press, Boca
launched in 1991, following a resolution of the Min- Raton, FL, pp 695712
isters of Health of Argentina, Bolivia, Brazil, Chile, Aukema B, Rieger C (eds) (1996) Catalogue of the Heteroptera
Paraguay and Uruguay. It focused on interruption of the Palaearctic Region, vol 2: Cimicomorpha I.
Netherlands Entomological Society, Amsterdam, The
of T. cruzi transmission by eliminating domestic Netherlands, 361 pp
vectors (particularly T. infestans), extending screen- Coll M (1998) Living and feeding on plants in predatory
ing of blood donors, and promoting maternal Heteroptera. In: Coll M, Ruberson JR (eds) Predatory
screening and specific treatment of infected new- Heteroptera in agroecosystems: their ecology and use
in biological control. Thomas Say Publications in Ento-
borns. Similar initiatives were launched in 1997 for mology, Entomological Society of America, Lanham,
Central America and the Andean Pact countries. MD, pp 89129
Those multinational initiatives, coordinated by the Garcia ES, Azambuja P, Dias JCP (2000) Triatominae (Redu-
viidae). In: Schaefer CW, Panizzi AR (eds) Heteroptera
Pan American Health Organization (PAHO)
of economic importance. CRC Press, Boca Raton, FL,
allowed that on June 9, 2006, at the 15th annual pp 539552
meeting, the Intergovernment Commission of the Maldonado CG (1990) Systematic Catalogue of the Reduvii-
Southern Cone Initiative against Chagas disease dae of the World. Special Publication, Caribbean Journal
of Science, Mayaguez, Puerto Rico, 694 pp
declared Brazil to be free of Chagas disease trans- Putshkov PV, Putshkov VG (1996) Family Reduviidae
mission due to Triatoma infestans. Also in Uruguay, Latreille, 1807 assassin bugs. In: Aukema B, Rieger
Chile, most of Argentina, Bolivia, Paraguay and C (eds) Catalogue of the Heteroptera of the Palae
parts of Central America, transmission has been arctic Region. Netherlands Entomological Society,
Amsterdam, The Netherlands, pp 148265
effectively eliminated. In 2004, a surveillance initia- Schofield CJ, Jannin J, Salvatella R (2006) The future of
tive was announced for the nine countries of the Chagas disease control. Trends Parasitol 22:583588
Amazon basin. To assure and increase the success Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera
Heteroptera): classification and natural history. Cornell
obtained in this 15-year initiative, surveillance and
University Press, Ithaca, NY, 335 pp
control of the disease and its vector are currently on
the agenda of all endemic countries. It is essential to
keep in mind the perennial need of surveillance, Assemblage
data assimilation and selective interventions, as tri-
atomines will always be present in the wild, as well The species within a particular taxon at a location.
320
A Associative Learning

Associative Learning Aster leafhopper is native to North America,

where it is nearly everywhere. It is most common,
The capacity to associate a stimulus, which itself however, in the central region of the continent.
has no positive or negative effects, with positive or Also, it overwinters poorly in cold areas. Most
negative effects. For example, bees can learn to areas with aster leafhopper problems are invaded
associate color with food sources. Insects com- annually by leafhoppers originating in the south-
monly display this ability. ern Great Plains. In the mild-climate northwest,
Learning in Insects however, leafhoppers are able to overwinter suc-
Habituation cessfully, and long-distance dispersal is not an
Latent Learning important factor.
Insight Learning

Life History
Assimilation Efficiency
This insect overwinters in the egg stage in north-
The proportion of energy ingested by an animal ern locations, and in the adult stage in warmer cli-
that is absorbed into the body. mates. In northern areas, there are three generations
per year, whereas up to five generations may occur
in more favorable midwestern locations. Because
Astatidae the generations overlap, and are initiated by both
overwintering eggs and migrating leafhoppers, it
A family of wasps (order Hymenoptera). is difficult to discern the generations. Total gen-
Wasps, Ants, Bees and Sawflies eration time requires about 2734 days.
Eggs are deposited in leaf, petiole, or stem tissue,
often near the juncture of the leaf blade and stem.
Asteiid Flies They are deposited singly, but often in short rows of
up to five eggs. They require a moist environment,
Members of the family Asteiidae (order Diptera). and perish if the foliar tissue desiccates. The eggs are
Flies translucent when first produced, soon turning white.
They average 0.80 mm in length (range 0.730.87
mm) and 0.23 mm in width. They are slightly curved,
Asteiidae with one side concave and the opposite side convex,
and taper to a blunt point at each end. The incuba-
A family of flies (order Diptera). They commonly tion period of the egg is about 78 days.
are known as asteiid flies. Newly hatched nymphs are nearly white, but
Flies soon become yellow and gain brownish markings,
including dark markings on the head. There are five
instars, the duration of which are about 34, 45,
34, 46, and 57 days, respectively, when reared at
Aster Leafhopper, Macrosteles 2125C. The body length measures about 0.61.0,
quadrilineatus Forbes (Hemiptera: 1.2, 2.0, 2.5, and 3.0 mm in instars 15, respectively.
Cicadellidae) As the nymphs mature, they gain spines on the hind
tibiae, the number increasing from about 67 to
john l. capinera 89. The tip of the abdomen also bears spines. The
University of Florida, Gainesville, FL, USA wing pads are indistinct through the third instar,
 Aster Leafhopper, Macrosteles quadrilineatus Forbes (Hemiptera: Cicadellidae)
A 321

but are apparent in the fourth instar, and overlap adult leafhoppers was found only in Texas, USA,
the abdominal segments in the fifth instar. although north of Texas eggs may overwinter. By
The adults (Fig.92) are small, the males about May, northward movement was evident, with adults
3.23.4 mm long, and the female 3.53.8 mm. present in Kansas, Nebraska, and South Dakota,
These insects are light green in color, with the fore- where no nymphs had been found previously. By
wings tending toward grayish green and the abdo- June the leafhoppers had progressed northward into
men yellowish green. There are six pairs of black Montana and North Dakota, and westward into Col-
spots, some of which are elongated almost into orado and Wyoming. Thus, northward migration
horizontal bands, starting at the top of the head occurs rather rapidly, and the leafhoppers are present
and extending along the front of the head almost during most of the growing season in these areas.
to the base of the mouthparts. The six pairs of Aster leafhopper has a wide host range. It tends
spots are the basis for the other common name of to overwinter on grains such as wheat and barley,
this insect, six-spotted leafhopper. Strong winds and on grasses, clover, and weeds, then dispersing
moving north in the spring transport adults into to other crops in the summer months. Several veg-
midwestern and northern crop production areas etable crops are damaged by aster leafhopper,
annually. Adults usually arrive in advance of egg including carrot, celeriac, celery, corn, lettuce, pars-
hatch by overwintering populations, and popula- ley, potato, and radish, but among vegetables only
tions of long-distance dispersants greatly exceed lettuce is consistently suitable for leafhopper repro-
resident leafhoppers. Arrival time in the north duction. Other crops fed upon are barley, clover, dill,
varies, but May arrival dates are common. field corn, flax, oat, rice, rye, sugarbeet, and wheat.
When dispersal was studied in the western In Washington, USA, studies indicated that
Great Plains of North America, the western edge of the most important breeding areas were mixtures
the principal migration path, overwintering of the of clover and pasture grasses, followed by clover,
sweet corn, oats, carrots, lawn grasses, rye, field
corn, and various weeds. Among the weeds favored
were fleabane, Erigeron spp.; ragweed, Ambrosia
spp.; dandelion, Taraxacum officinale; wild lettuce,
Lactuca canadensis; tumble mustard, Sisymbrium
altissimum; and lambsquarters, Chenopodium
album. Low, sparse, and young vegetation provided
the best habitat. In Minnesota, large crabgrass, Dig-
itaria sanguinalis; horseweed, Conyza canadensis;
barnyardgrass, Echinochloa crusgalli; fowl-meadow
grass, Poa palustris; and barley, wheat, and oats
were especially suitable for reproduction. Carrot,
dill, potato, and radish were important adult food
plants, but not good breeding hosts.
Natural enemies are not well known, or very
important in the population ecology of aster leaf-
hopper. The most important enemies are the parasi-
toidsPachygonatopusminimusFenton,Neogonatopus
Aster Leafhopper, Macrosteles quadrilineatus ombrodes Perkins, and Epigonatopus plesius Fenton
Forbes (Hemiptera: Cicadellidae), (all Hymenoptera: Dryinidae). The best known
Figure 92 Adult of aster leafhopper, Macrosteles among these is P. minimus, which has caused up to
quadrilineatus Forbes. 37% parasitism.
322
A Aster Leafhopper, Macrosteles quadrilineatus Forbes (Hemiptera: Cicadellidae)

Damage chemical-based disease suppression is feasible.

Insecticides are especially effective in the absence
Leafhoppers pierce leaf tissue of plants and remove of long-distance dispersal by leafhoppers. Systemic
the sap. The feeding punctures cause death and insecticides are often favored due to their persis-
discoloration of individual plant cells, resulting in tence, but contact insecticides can also be effective.
a yellow, speckled appearance in affected plants. Insecticides are often applied at 57 day intervals.
This feeding damage, while unsightly, is minor in Because it takes 1015 days for infected plants to
comparison to the damage caused to a great num- show signs of infection, it is not necessary to treat
ber of vegetable crops by transmission of aster yel- plants just prior to harvest.
lows by leafhoppers. Crop varieties differ in their susceptibility to
Aster yellows is a plant disease caused by a infection with aster yellows; this is well studied
mycoplasma-like organism (MLO), and is trans- both for carrots and lettuce, two of the more sus-
mitted almost exclusively by aster leafhopper. Such ceptible crops. Cultural manipulations can also
crops as carrot, celery, cucumber, lettuce, potato, enhance resistance. In studies conducted in Min-
pumpkin, and squash are affected. Losses of 50 nesota, very significant reductions in disease inci-
100% are reported due to this disease. MLO- dence were shown where aluminum foil mulch was
infected plants are discolored, stunted, and used. Straw mulch was equally effective. Row cov-
deformed. On carrots, for example, the symptoms ers, where economically feasible, should provide
are red or yellow foliage and excessively hairy, bit- good protection against leafhoppers and disease
ter-tasting roots. On lettuce, symptoms are chloro- transmission. Destruction of weed species known
sis, stunting, and lack of head formation. to harbor aster yellows is desirable.
Aster leafhopper acquires the MLO by feed-
ing on infected perennial or biennial weeds or
Management crop plants. Acquisition requires a prolonged
period of feeding, usually at least 2 h, before the
Leafhoppers are sampled with sweep nets, espe- leafhopper is infected. Usually <2% of dispersant
cially from grasses and grain fields. Yellow sticky leafhoppers become infected. There is evidence
traps are also useful and easy to use, and light traps that the MLO multiplies in the body of the leaf-
equipped with fans for suction also have been used hopper, and there is an incubation period of about
effectively to capture leafhoppers. 2 weeks in nymphs, and 610 days in adults, before
In addition to sampling for leafhopper abun- the insects are capable of transmitting aster yel-
dance, it is also desirable to determine the propor- lows. Leafhoppers remain infective for the dura-
tion of leafhoppers that harbor the MLO. Formulas tion of their life, but the MLO is not transmitted
based on both insect number and disease inci- between generations through the egg stage. Thus,
dence, called the aster yellows index, have been there is ample time for insecticides to interrupt
developed to trigger control measures before the disease transmission.
pathogen is widely transmitted to susceptible crops.
Leafhoppers are collected before they enter an area,
fed on aster plants, and the plants read for disease. References
This works effectively to alert large areas, such as
entire states, but is not useful for local prediction. Capinera JL (2001) Handbook of vegetable pests. Academic
Insecticides commonly are used to kill leaf- Press, San Diego, CA, 729 pp
Hagel GT, Landis BJ (1967) Biology of the aster leafhopper,
hoppers, and thereby minimize disease transmis-
Macrosteles fascifrons (Homoptera: Cicadellidae), in
sion. Because there are protracted acquisition and eastern Washington, and some overwintering sources of
incubation times associated with this disease, aster yellows. Ann Entomol Soc Am 60:591595
 Attelabidae
A 323

Hoy CW, Heady SE, Koch TA (1992) Species composition,

phenology, and possible origins of leafhoppers (Cicadel-
Asymmetric Competition
lidae) in Ohio vegetable crops. J Econ Entomol
85:23362343 Competition between two individuals or species in
Nielson MW (1968) The leafhopper vectors of phytopathogenic which one is more severely affected than the other.
viruses (Homoptera: Cicadellidae). Taxonomy, biology, and
virus transmission. USDA Technical Bulletin 1382, p 386

Asymmetric PCR
Asterolecaniidae
Single-stranded DNA produced by providing an
A family of insects in the superfamily Coccoidae excess of primer for one of the two DNA strands.
(order Hemiptera). They sometimes are called pit Asymmetric primer ratios are typically 50:1100:1.
scales. Single-stranded DNA produced can be sequenced
Bugs directly without cloning.

Aster Yellows Asynchronous Muscle

This is an important insect-vectored disease that Muscle in which the frequency of contraction is
affects many plants. See also, Transmission of Plant not controlled directly by nervous impulses, with
Disease by Insects. the contraction frequency a property of the mus-
Transmission of Plant Diseases by Insects cle. Asynchronous muscle produces several to
many contractions in response to a single nervous
stimulation. (contrast with synchronous muscle)
Ateluridae
A family of silverfish (order Zygentoma). ATP
Silverfish
Adenosine triphosphate is the primary molecule
for storing chemical energy in a cell.
Athericid Flies
Members of the family Athericidae (order Diptera).
Flies
Atrophy
Decrease in size of a tissue, organ, or part after full
Athericidae development has been obtained. In pathology, a
condition in which the affected cells undergo
A family of flies (order Diptera). They commonly degenerative and autolytic changes, become
are known as anthericid flies. smaller, and have a lessened functional capacity.
Flies

Attelabidae
Astrotaxis
A family of beetles (order Coleoptera). They com-
Taxis response with respect to the sun, moon, stars monly are known as leaf-rolling weevils.
or polarization of light. Beetles
324
A Attenuation

Attenuation having a bitter taste are broken down to mustard

oils (isothiocyanates) and other substances by
The process of decreasing the virulence of a enzymes which are known as myrosinases.
microorganism. Isothiocynates, in general, have hot and pun-
gent odors. However, those which have a bigger
molecule lose pungent odor and have more sweet
Attractant and mild odors. For example, 2-propenyl isothio-
cyanate (allyl isothiocyanate, C3H5NCS), which is
An odor, or the material producing an odor, that (Fig.93) split from sinigrin, has a very pungent
attracts insects. odor; however, 2-phenylethyl isothiocynate
(C6H5CH2CH2NCS), which is derived from gluco-
nastrutiin, has a sweet odor.
Attraction of Insects to Organic E. Verschaffelt, a botanist from the Nether-
Sulfur Compounds in Plants lands, first noticed the relationships between
insects and glucosinolates early in the twentieth
yoshiharu matsumoto century. He found that the host plants of the large
University of Tokyo, Tokyo, Japan and small white butterfly larvae, Pieris brassicae
and P. rapae, were limited to the plants containing
Among the secondary plant metabolites, two types glucosinolates. By smearing sinigrin on leaves
of organic sulfur compounds are of considerable which had been rejected before, the larvae came to
importance: glucosinolates and cystein derivative readily attack and feed on some of these. Half a
amino-acids, and their respective breakdown century later, this result was verified and devel-
products. These compounds, in various ways, oped by Thorsteinson and his group in Canada
influence the diversity of organisms associated with the diamondback moth, Plutella xylostella,
with plants bearing these compounds. using artificial agar diet containing a known quan-
tity of glucosinolate. Sinigrin, sinalbin, glucochei-
rolin, and progoitrin stimulated larval feeding in
Glucosinolates the presence of glucose. After these important
works, the stimulation of feeding by glucosino-
Glucosinolates (=mustard oil glycosides) occur lates, mainly sinigrin, was shown in a variety of
predominantly throughout the order Capparales, specialist herbivores feeding on cruciferous plants:
consisting of Brassicaceae (=Cruciferae), Cappa- the cabbage aphid, Brevicoryne brassicae, the
raceae, Moringaceae, Resedaceae, Tovariaceae, cabbage fly, Delia brassicae, the cabbage beetle,
and sporadically in some other families (e.g., Cari- Phaedon cochlearia, and P. brassicae. The gravid
caceae, Limnanthaceae, and Tropaeolaceae). female white butterflies tap the leaf surface with
About 50 different glucosinolates are found in their forelegs (called drumming) when they
Brassicaceae, and over 100 glucosinolates through- attempt to oviposit on leaves. They receive chemical
out the plant kingdom. Several to about twenty
glucosinolates occur in each cruciferous species.
For example, in leaves there are 14 glucosinolates
in cabbage, 12 in cauliflower, 11 in Brussels sprouts,
7 in broccoli and Chinese cabbage. In roots, there
are 18 glucosinolates in turnip and 8 in kohlrabi. Attraction of Insects to Organic Sulfur
In oilseeds, there are 9 glucosinolates in rapeseed Compounds in Plants, Figure 93 Chemical
and turnip rape, and 5 in mustard. Glucosinolates structure of sinigrin.
 Attraction of Insects to Organic Sulfur Compounds in Plants
A 325

stimulation from glucosinolates in leaves via the attraction by isothiocynates are observed in
sensilla on their tarsal undersurface. Glucobrassi- specialist herbivores on Brassicaceae. Contrarily,
cin (3-indolylmethyl glucosinolate) is effective at unfavorable effects such as feeding and oviposi-
106 M, 1,000-fold more effective than sinigrin tion inhibition and repulsion are observed in non-
(2-propenyl glucosinolate), in initiating oviposi- adapted herbivores, such as the bertha armyworm,
tion by P. brassicae. Each crucifer plant has a few or Mamestra configurata, Colorado potato beetle,
many glucosinolates so that they seem to work Leptinotarsa decemlineata and the desert locust,
together. Schistocerca gregaria.
In Japan during the 1950s, the olfactory stimu- Plant breeding strategies have concentrated
lation of insect by isothiocynates was first proven on reducing the glucosinolate content of rape
by Sugiyama and Matsumoto with both of adults seeds because of reducing the risk of causing goi-
and larvae of the vegetable weevil, Listroderes ter and organ abnormalities in livestock animals.
costirostris. This species is a typical generalist, However, the response of insects to the glucosino-
feeding on over 120 species in 28 plant families, in late and/or isothiocynate content is not so simple.
which Brassicaceae are among the important host A worker reported that Phyllotreta cruciferae and
plants. Each allyl-, 1-butyl-, 2-butyl-, phenyl-, ben- P. xylostella larvae fed at equal rates on Brassica
zyl-, 2-phenylethyl isothiocynate evoked every step juncea and its low-glucosinolate lines, indicating
of the chain reaction of host selection behavior in that these species are insensitive to sinigrin.
adults, consisting of the orientation (=attraction), Another group of workers reported that the feed-
antennae tapping and final continuous biting ing activity, such as the proportion of time feeding
(=feeding) against the odor-material in the absence and area damaged, by P. xylostella larvae is higher
of any taste substances or nutrients. For newly on the lines with low myrosinase activity than on
hatched larvae, nine isothiocynates, methyl-, ethyl- the lines with high mirosinase activity. In contrast,
to 2-phenylethyl, 1-naphtyl isothiocynates indi- the feeding activity of the southern armyworm,
cated a significant attractiveness, increasing with Spodoptera eridania, a generalist, is not related to
an increasing number of CH2 groups. These results myrosinase activity. Relative growth rates of both
clearly show that not only the specialist herbivores, insect species are lower on cotyledons of lines with
but also the generalist herbivores, use plant odors high glucosinolate content, but are not related to
as the token stimuli for their host selection behav- myrosinase activity in the lines. Thus, glucosino-
ior. In Germany, the attraction of the flea beetles, late reduction is not always promising for protect-
Phyllotreta crucifera and P. striolata, by allyl isothi- ing crops against the insects.
ocynate was first shown in field trapping. Thereaf-
ter, allyl-isothiocynate was proven to be effective in
attraction to the cabbage root fly, Delia radicum, Organic Sulfur Compounds in
the turnip root fly, D. floralis, D. brassicae adults, Allium Plants
and also in stimulation of oviposition by P. rapae
and P. xylostella females. The cabbage seed weevil, V. G. Dethier first proposed investigation of behav-
Ceutorhynchus assimilis, is attracted by isothiocyn- ioral reactions of typical allium-feeders to organic
ate mixtures similar to the composition of odor sulfur compounds, which seemed to be character-
chemicals in oilseed rape plants. However, omis- istic of odor in allium plants. During the late 1950s
sion of two isothiocynate, 3-butenyl isothiocynate to early 1960s, the fast progress of instrumental
and 4-pentenyl isothiocynate from the mixture analysis brought forth the component data of
significantly reduces the attractiveness. onion volatiles. Allium plants produce very spe-
In general, favorable effects such as feeding cific sulfur compounds. Cysteine derivative amino
and oviposition stimulation by glucosinolates and acids are converted by enzymatic splitting into
326
A Audinet-Serville, Jean-Guillaume

sulfenic acids and thiosulfinates, which evolve into have been found to favor the host finding by an
numerous substances. This results in production allium specialist, but to deter the approach and
of odorous substances consisting mostly of mono-, attack to the plant by generalists. This is similar as
di-, tri-sulfides, and n-dipropyldisulfide (n-DPDS, in glucosinolates.
n-C3H7SSC3H7) and 1-propanethiol (1PTH,
n-C3H7SH), which are reported to be the main
components of onion odor. The attraction and ovi- References
position stimulation of female onion fly, Delia anti-
qua, by these two compounds was first demonstrated Dethier VG (1947) Chemical insect attractants and repellents.
by Matsumoto and Thorsteinson in laboratory Blakiston, Philadelphia, Pennsylvania, and Toronto,
Canada
experiments and field trapping in Manitoba, Canada
Fenwick GR, Heaney RK, Mullin WJ (1983) Glucosinolates
in 19631964. However, no attraction nor oviposi- and their breakdown products in food and food plants.
tion stimulation was observed to di-methyldisulfide CRC Critical Rev 18:123201
(DMDS). Newly hatched larvae also were shown to Finch S (1981) Chemical attraction of plant feeding insects to
plants. Appl Biol 5:67143
be attracted to over 20 compounds of various mono-, Matsumoto Y (1970) Volatile organic sulfur compounds as
di-sulfides and alkyl-thiols, including DMDS. The insect attractants with special reference to host selec-
larvae are likely to be less strict in the selection of tion. In: Wood DL, Silverstein RM, Nakajima M (eds)
odor chemicals. Control of insect behavior by natural products.
Academic Press, New York, NY, UK
Over 10 years later, the analysis of green onion- Miller JA, Stricker KL (1984) Finding and accepting
seedling odor was conducted in Canada and Japan host plants. In: Bell WJ, Card RT (eds) Chemical
independently, so that nine alkyl di- and trisulfides e cology of insects. Chapman and Hall, New York, NY,
pp 128157
including n-DPDS and 1PTH were found. A pro-
Stdler E (2000) Secondary sulfur metabolites influencing
pylthio (n-C3H7S) moiety was shown to be essen- herbivorous insects. In: Rennenberg H, Brunold C, Stu-
tial for a compound to induce attraction and len I, Dekok L (eds) C et al (eds) Sulfur nutrition and
oviposition stimulation activities. The compounds sulfur assimilation in higher plants. Paul Haupt, Bern,
Switzerland, pp 187202
having butylthio (n-C4H9S) or amylthio (n-C5H11S) Thorsteinson AJ (1960) Host selection in phytophagous
moiety also were reported to be attractive, although insects to plants. Ann Rev Entomol 5:67143
these compounds were not found in volatiles from Verschaffelt E (1910) The cause determining the selection of
onion. The green onion seedlings of susceptible food in some herbivorous insects. Proc Royal Acad
Science, Amsterdam 13:536542
cultivars give a larger quantity of propylthio com-
pounds than those of resistant cultivars, because
the allinase activity is higher than in the resistant
cultivars. Audinet-Serville, Jean-Guillaume
Host finding by the leek moth, Acrolepiopsis
assectella, an allium specialist, is also controlled by Jean-Guillaume Audinet-Serville was born in Paris
sulfur compounds, with propylpropanethiosulfi- on November 11, 1775. The family wealth was lost
nate (n-C3H7SOSC3H7) the most attractive. The during the French revolution, and Jean-Guillaume
adults of Diadromus pulchellus, an endoparasitoid was sent to work in a coal store. The wife of the
of the young larvae of A. assectella and P. xyllostera, director of the store, Mme. de Tigny, author and
use the volatiles from the frass excreted by their correspondent of several notable entomologists,
hosts, and from the plant leaves fed by their hosts. influenced him to collect and study insects. He
In the volatiles from the frass of both moths, the married, and had three children before losing his
same three disulfides (dimethyl, dipropyl, and wife. Latreille asked him to continue a work that
methyl propyl) are the most abundant substances. Palisot de Beauvois had left incomplete due to the
Thus, volatile sulfur compounds in allium plants death of that entomologist. Thus, the 15th (last)
 Augmentative Biological Control
A 327

part of Insectes recueillis en Afrique et en not build a personal collection of insects. He also
Amrique was written by Audinet-Serville and published on applied entomology with a book
published in 1819. Another famous work, Oliviers (1842) Insectes nuisibles la vigne. With
Encyclopdie mthodique, was likewise incom- Brongniart and Dumas he founded the journal
plete, and here again Latreille persuaded Audinet- Annales des Sciences Naturelles. He died in Paris
Serville, with help from Lepelletier de St. Fargeau on November 9,1841.
and Latreille, to write volume 8, published in 1825.
A third work,Faune franaise was also completed
by Audinet-Serville in 1830, when he wrote the Reference
natural history of Coleoptera. Then, in 1831, he
began publishing his own studies, first on the genus Fauvel A (1868) Biographie et bibliographie. In: Faune gallo-
rhnaneColoptres. vol 1, pp 59130
Pirates, and then Revue mthodique de l ordre
des orthoptres, both in the pages of Annales
des Sciences Naturelles. Other works followed, of
Augmentation
which a notable one in 1839 was on Orthoptres
and formed a supplement to Buffons series of
The practice of rearing and releasing biological
volumes Histoire naturelle. He died on March
control agents to effect pest suppression. This is
27, 1858. His collections were broken up and sold
also called augmentative biological control.
to various collectors.
Augmentative Biological Control

Reference
Augmentative Biological Control
Amyot CJB (1858) Notice necrologique sur Audinet-Serville.
Ann Soc Entomol France 6:343351 marjorie a. hoy
University of Florida, Gainesville, FL, USA

Augmentation involves efforts to increase popula-

Audouin, Jean-Victor tions or beneficial effects of natural enemies (para-
sitoids, predators, pathogens, entomopathogenic
Jean-Victor Audouin was born in Paris on April 2, nematodes) of pest insects, mites and weeds.
1797. He began to study law, but turned instead to Various techniques can be employed in augmenta-
medicine. His (1826) thesis was on the chemistry, tion, but augmentation typically involves releases
pharmaceutical uses, and medical effects of can- of natural enemies or environmental manipulation
tharides (cantharidin), and on the beetles that to enhance effectiveness of naturally occurring
produce it. He was made assistant to Latreille, and natural enemies. Environmental manipulation may
then succeeded Latreille as chairman of entomol- involve providing alternative hosts or prey, food or
ogy at the Musum National d Histoire Naturelle, nesting sites or modifying cropping practices to
and reorganized and enriched the collections. In favor natural enemies.
1829, he coauthored a book with Milne Edwards Periodic releases may be labeled inundative or
on natural history of Crustacea. His (1834) book inoculative, depending upon the numbers of natural
Histoire naturelle des insectes was of several enemies released and the time interval during which
volumes. He contributed some of his work to they are expected to provide control. The distinction
Cuviers Rgne animal In 1838, he was elected between inundative and inoculative augmentative
a member of the Academie des Sciences. He did releases may become blurred. Inundative releases
328
A Augmentative Biological Control

involve releasing large numbers of natural enemies control house flies, Musca domestica, on dairy
with the goal of achieving an immediate effect on farms can be effective if conducted as part of an
pest populations. In essence, the natural enemies integrated pest management program.
are living pesticides. Pathogens and nematodes are Augmentative releases are extensively emplo-
commonly released inundatively. Parasitoids or yed in European glasshouses (or greenhouses).
predators are less often released in this manner Releases of parasitoids or predators are made to
because it is more difficult to mass produce high control spider mites, whiteflies, leafminers, aphids
quality natural enemies inexpensively. For inocula- and other pests on cucumbers, tomatoes and sweet
tive releases, relatively small numbers of natural peppers. For example, greenhouse whiteflies, Tri-
enemies are released early in the cropping season aleurodes vaporariorum, are controlled by releases
and it is assumed that they will multiply and provide of a pathogenic fungus, Aschersonia sp. or a para-
control of the target pest later in the season. sitoid wasp, Encarsia formosa. Several aphids can
be controlled with releases of the cecidomyiid
predator Aphidoletes aphidimyza, and the aphid
Examples of Augmentative Releases Myzus persicae can be controlled by releases of the
parasitoid Diaeretiella rapae. Leafminers, Liro-
Augmentation is an appropriate tactic to consider myza sp., can be controlled by releases of several
if indigenous natural enemies cannot suppress commercially available parasitoids. The two-spotted
pest populations to an adequate level because the spider mite, Tetranychus urticae, a major pest of
natural enemy population lags behind that of the both ornamental and vegetable plants, is controlled
pest, or if the natural enemies cannot persist over by releases of the phytoseiid mite Phytoseiulus
winter. Releasing natural enemies into crops that persimilis. Much of the information developed for
are sprayed with pesticides that are toxic to the releasing natural enemies in European glasshouses
natural enemies is unlikely to be effective unless can be adapted to control glasshouse pests else-
the sprays are applied in a selective manner. where because these pests are widely distributed.
Examples of augmentative releases include
releases of Cryptolaemus montrouzieri, a coccinel-
lid predator of mealybugs into California citrus Controversies about Augmentative
groves. This ladybird beetle has established perma- Releases
nently only in a narrow coastal area of California
and does not overwinter elsewhere, so releases of Some augmentative release programs are contro-
1020 Cryptolaemus beetles per tree at the begin- versial. For example, egg parasitoids of the genus
ning of the summer can result in control of the Trichogramma attack eggs of many Lepidoptera.
mealybugs during the growing season. Periodic These tiny wasps have been mass reared and released
releases of the parasitoid Aphytis melinus are made against moth pests on millions of hectares of crops
to control California red scale on citrus grown in around the world. However, their efficacy rarely has
the coastal citrus region of California; approxi- been documented. It is suspected that efficacy may
mately 200,000400,000 wasps per acre are be less than expected because the wasps usually are
released. Several species of phytoseiid predatory reared, for economic reasons, on host eggs other
mites have been released to control the two-spot- than those of the target pest. Parasitoids produced
ted spider mite, Tetranychus urticae, in strawber- on alternative host eggs may be of lower quality
ries in California. Releases became essential and (small in size or with crumpled wings). Effective
cost effective after this spider mite developed resis- Trichogramma releases may require releasing as
tance to the pesticides used previously to control it. many as 150,000500,000 wasps per hectare every 2
Releases of the parasitoid Muscidifurax raptor to weeks during the growing season. Other elements
 Augmentative Biological Control
A 329

of effective Trichogramma releases include collect- the crops are of high value, the natural enemies are
ing the species or biotype (specific strain) that reliably available at competitive prices, and guide-
attacks the target pest in the target crop for mass lines on release methods, rates and timing are avail-
rearing. Reestablishing colonies on an annual basis able. However, relatively few predators and
using field-collected material has been recom- parasitoids (probably <50) have been evaluated for
mended in order to maintain high quality. efficacy, reliability and economic feasibility.
Some augmentative releases of natural ene- Augmentative releases can be hampered if high
mies have appeared to be effective because they quality parasitoids and predators are not be avail-
induced the farmer to stop pesticide applications. able at the right time. Mass rearing of parasitoids
However, the released natural enemy may not have and predators is restrained by high costs, lack of
provided control, which was actually provided by effective artificial diets, ineffective or limited quality
naturally occurring parasitoids, predators and controls and an inability to stockpile or store natural
pathogens. Knowingly using augmentative releases enemies during periods when they are not needed.
as a placebo effect, in which the pest control is Typically, parasitoids or predators are reared on
achieved by native natural enemies which are no insect hosts or prey, which are themselves reared on
longer disrupted by pesticide applications, is plants, making the rearing system complex and
considered unethical because the consumer pays expensive. Maintaining pure and vigorous colonies
for unnecessary natural enemies. of both hosts and natural enemies, as well as dis-
Other releases of natural enemies may be of ease-free plants, requires skill and resources. If
little direct benefit to the consumer purchasing effective artificial diets could be developed for addi-
them. For example, releases of some predators tional natural enemies, costs could decline and
(such as some species of lady beetles or lacewing availability could increase. Although artificial diets
adults) may provide limited benefit at the release for some arthropods are available, many diets are
site because these predator species may be geneti- less effective than natural foods in producing high
cally programmed to fly long distances prior to quality natural enemies. Concerns have been raised
settling down to feed and reproduce. as to whether parasitoids or predators reared in
Another, more recent, issue that has been raised is insectaries are less fit than desired. For example, sex
whether some natural enemy species released in aug- ratios in parasitoid populations reared in the labo-
mentative biological control programs could become ratory often change due to inbreeding. Optimal
permanently established in the environment. If the methods for maintaining quality and genetic vari-
natural enemy is not native, some have questioned ability need to be developed to increase the effec-
whether the natural enemies could have unintended tiveness of natural enemies reared for augmentative
effects on nontarget species in natural environments, releases in biological control programs.
perhaps reducing biodiversity. In the USA, importa- Relatively few microbial products are available
tion of nonnative natural enemies, whether for classi- for pest management programs despite the fact
cal biological control or for augmentative releases, that it may be easier and less expensive to produce
must be approved by the U.S. Department of Agricul- viruses, bacteria or fungi than to rear parasitoids or
ture after undergoing risk analysis. predators. The commercial production of micro-
bial pesticides involve a series of steps, including:
isolating a suitable pathogen by screening a large
When and Where are Releases number of isolates to identify those which show
Made? activity against the target pests; conducting labora-
tory and greenhouse tests to evaluate the efficacy
Augmentative releases are most likely to offer prac- of potential agents and to determine what environ-
tical alternatives to pesticides in situations where mental issues could affect their effectiveness;
330
A Augmentative Biological Control

producing commercial scale quantities of the prod- augmentative releases of natural enemies. Some
uct, which usually involves fermentation; develop- natural enemies, such as some lady beetles, are
ing the correct formulation of the microbe so the generalists and will eat many species of aphids.
product can be stored, handled and applied effec- However, even generalist lady beetles may not eat
tively in the field; conducting efficacy trials of the all species of aphids because the aphids are repel-
agent under field conditions using commercial lent or contain toxic chemicals. Many pests require
types of formulations. Microbial pest control prod- specific natural enemies to achieve control. For
ucts are expected to increase in popularity, but are example, a predatory mite that is known to feed on
not expected to replace synthetic organic pesti- spider mites may not consume other plant-feeding
cides. These microorganisms often are not patho- mite species such as rust mites or tarsonemid
genic to predators and parasitoids, which can allow mites. Many parasitoids have a very limited host
these agents to be compatible. range, sometimes limited to one or a few species.
Several problems limit the use of microbial Thus, a taxonomic identification of the pest to
pesticides. Microbial products are not always species or strain may be required.
reliable under field conditions due to limita- Next, the best natural enemy(ies) for that target
tions in both formulation and the microorgan- pest need to be identified. Companies provide lists
ism itself. The activity of the microorganism of pests against which their products may be applied,
may be too specific, which can be a disadvan- but these may be less than reliable. Consult your
tage when there are multiple pests in the crop- land grant university extension service, the U.S.
ping system. Most microbial products have a Department of Agriculture or licensed pest control
short residual activity in the field (especially in advisors for additional information as to which nat-
comparison to synthetic organic pesticides), ural enemies are appropriate for your target pest.
which makes it necessary to make multiple One of the most difficult questions to answer
applications which increases labor and product is how many do I have to purchase for release ?
costs. Microbial products may act slowly, mak- This question should be answered after careful
ing them appear ineffective or allowing exces- consideration; if too few natural enemies are
sive damage to occur in the crop. released, the releases will be ineffective and the
funds used to purchase the natural enemies will
be wasted. Furthermore, the additional damage
Some Logistical and Ethical Issues to the crop caused by the pest could reduce yield
or quality.
Augmentative biological control with releases of There are some common rules of thumb in
natural enemies requires that the user (grower, release rates: for example, releasing 1 predatory
farmer, home owner) have considerable informa- mite for each 10 or 20 spider mites will provide
tion. Consumers need to be informed before using relatively rapid pest population suppression.
augmentative biological control or consult with a However, even this release rate is inadequate if the
knowledgeable pest control advisor. Some aug- 10 or 20 spider mites have caused economic dam-
mentative releases should be considered experi- age to the plant prior to the release; an average of
ments because necessary information is lacking. It ten mites per leaf results in different levels of
is possible that the release rates and timing may damage than an average of ten mites per plant.
not have been evaluated under the specific cli- Thus, information about the damage the plant can
matic conditions and crop production conditions tolerate is needed. Different cultivars of a crop
at the release site. may vary in sensitivity to feeding by pests, so
Detailed information about the pest species release rates and timing may have to be tailored to
you wish to control is usually required for effective the specific crop cultivar.
 Augmentative Biological Control
A 331

To calculate the number of natural enemies Ideally, augmentative releases will be planned
required in an augmentative release program, the prior to the start of the growing season and a
number of pests should be estimated by an effec- monitoring program will be implemented so that
tive sampling scheme. For example, it may be use- releases can be scheduled as soon as the target pest
ful to estimate the mean number of spider mites population appears.
per leaf, the mean number of leaves per plant and
the mean number of plants per acre or hectare to
calculate the total number of mites present and, Costs of Releasing Natural Enemies
thus, the number of predators to order. Do not
forget to allow for a continued population Costs of releasing natural enemies depend on the
increase between the time you calculate the pest number that must be released. It is often the case
population density and the time you receive the that too few natural enemies are released and, as a
natural enemies (typically several days to a week result, in inadequate control occurs. In California
later). The sooner the releases occur the less dam- strawberries, it was estimated to cost approximately
age will accrue to the crop plant. US $600 per acre to release predatory mites to con-
Once the natural enemies arrive, follow the trol two-spotted spider mites in strawberries. This
directions on how to store them before releasing cost was accepted because the spider mites were
them, monitor the containers to be sure the natu- resistant to the currently registered pesticides and
ral enemies are healthy, and follow the directions no other effective control method was available.
on how to release them. Once the releases have Furthermore, the high value of strawberries
occurred, know how to monitor the release site to (approximately $30,000 per acre) made this con-
be sure the natural enemies are performing as trol cost feasible. In lower value crops, augmenta-
expected. tive releases might not be economically justifiable.

What is the specific pest you need to control?

Time is of the Essence Which natural enemies are known to perform well
on that specific pest species under similar climatic
Because natural enemies are relatively expensive, and geographic conditions?
it is desirable to release them as early as possible How many pests do you have? Per leaf? Per plant?
in a pest population outbreak so that fewer natu- How many plants per row or acre? How many
ral enemies are required to perform the job. acres?
Waiting until the pest population is abundant What is the effective release rate for that natural
increases costs and reduces the likelihood that enemy? For example, should the natural enemy
the natural enemies will perform effectively. be released in a ratio of one natural enemy to
Many natural enemies arrive from commer- each 10 pest individuals? If so, the earlier the
cial producers as adults, and they may have been releases can be conducted, the less expensive
stressed during shipment. As a result, they may such releases will be. For example, If hundreds
require a lag time before they feed or reproduce of spider mites are present on each plant, then it
on the target pest. Furthermore, many natural is expensive and difficult to release sufficient
enemies, such as predatory mites, typically live as predators to suppress them; it would be better to
adults less than a week; if we assume that the make releases when less than one spider mite
adults were collected immediately after emerging per leaf is present.
for shipping and the shipping process takes 1 day, Calculate the number of natural enemies needed
such individuals will still have lost approxi- based on release rate, area to be covered and abun-
mately 2 days in their potential effectiveness. dance of the pest per plant, row, acre.
332
A Augmentative Biological Control

Are multiple releases needed over days or weeks should be considered experiments and conducted
to achieve the necessary level of pest on a relatively small scale initially until it is clear
suppression? that the necessary information is available and
How should the natural enemies be stored and appropriate for the new situation.
handled after your receive them from the
commercial producer to reduce mortality and
enhance effectiveness after release? Future of Augmentation
When should releases be conducted (time of day,
temperature conditions) and in what manner? For Pests in greenhouses in Europe, in which egg-
example, do natural enemies disperse readily or plants, cucumbers and tomatoes are grown, are
should they be released on each plant or each leaf. often under complete biological control due to
How can you monitor the results of the releases to augmentative releases of natural enemies. There
know if the natural enemies are performing as are several moderately large companies that
expected? produce natural enemies for this market, provide
Does the commercial producer provide informa- information on release rates and timing, and pro-
tion on release rates, timing, methods, and guar- vide other information. Control of pests of orna-
antee quality of the natural enemies during mental plants in Europe is less often achieved by
shipping? augmentative biological control because damage
to foliage or flowers reduces quality. Greenhouse-
grown crops in other geographic areas may be
Key Research Needs limited due to difficulties in obtaining natural
enemies in a timely fashion, differences in pest
Additional resources committed to improving and disease complexes, and differences in climatic
augmentative releases of natural enemies could conditions.
increase the use of this pest management tactic. Citrus growers in California have developed
These include research to develop adequate qual- grower-owned cooperatives to produce natural
ity control tests so that only high quality natural enemies. This approach has proven successful for
enemies are shipped from the commercial pro- over 50 years, suggesting that grower-owned coop-
ducers. Appropriate tests should be conducted to eratives might be a useful model for increasing the
confirm that the correct natural enemy species is use of augmentative releases in other crops in other
shipped, that it is disease free, vigorous and viable. geographic areas.
Research should also be devoted to developing Augmentative releases can be an effective
improved methods for producing natural enemies pest management tool for many pests in a diverse
at peak demand times, or for storing natural ene- array of crops. However, augmentative biological
mies without a loss in quality, so that adequate control requires that the pest manager have
numbers are available when needed. High quality, considerable information on pest and natural
but inexpensive, artificial diets could reduce pro- enemy biology, an understanding of pest-natural
duction costs. Shipping and storage methods could enemy dynamics, and the availability of adequate
be improved; many natural enemies arrive stressed numbers of high quality natural enemies for
or, even, dead. Finally, accurate information on release at the right time. Thus, it is an information-
release rates and timing could be improved and intensive and logistically critical management
developed for additional geographic regions and approach.
climates. Augmentation has the potential to become a
Because data are not available for all situations, more dominant component of pest management
many augmentative releases of natural enemies programs if sufficient resources are devoted to
 Augmentative Biological Control
A 333

Some natural enemies considered suitable for augmentative biological control

Natural enemy Pest
Predators
Amblyseius barkeri Thrips tabaci, Frankliniella occidentalis
Amblyseius cucumeris and A. degenerans Thrips tabaci, Frankliniella occidentalis
Anthocorus nemorum Thrips
Aphidoletes aphidimyza Aphids
Cryptolaemus montrouzieri Mealybugs and some scalaes
Chrysoperla carnea Aphids
Hippodamia convergens Aphids
Metaseiulus occidentalis Tetranychus urticae, T. pacificus
Orius sp. Frankliniella occidentalis
Phytoseiulus persimilis Tetranychus urticae
Parasitoids
Aphelinus abdominalis Macrosiphum euphorbiae
Aphidius colemani Aphis gossypii
Dacnusa sibirica Liriomyza bryoniae, L. trifolii, L. huidobrensis
Diglyphus isaea L. bryoniae, L. trifolii, L. huidobrensis
Encarsia formosa Trialeurodes vaporariorum, Bemisia tabaci
Eretmocerus californicus Bemisia tabaci
Leptomastix dactylopii Planococcus citri
Metaphycus helvolus Scales
Opius pallipes Liriomyza bryoniae
Trichogramma spp. Lepidopteran eggs
Pathogens
Bacillus thuringiensis Lepidopteran larvae
NPV-virus Spodoptera exigua
Trichoderma harzianum Fusarium spp.
Verticillium lecanii Aphids
Entomopathogenic nematodes
Heterorhabditis spp. Otiorrhynchus sulcatus
Steinernema spp. Sciaridae

obtaining the necessary information and improve- An Important Website: http://www.cdpr.ca.

ments in rearing and deployment. gov/docs/ipminov/bensuppl.htm, which provides a
Natural Enemies important in Biological list of commercial suppliers of natural enemies in
Control North America. A variety of natural enemies are
Culture of Natural Enemies on Factitious produced commerc ially for the control of green-
Foods and Artificial Diets house and other pests.
Rearing of Insects
334
A Auricular Openings

References References

Flint ML, Dreistadt SH (1998) Natural enemies handbook. The Common IFB (1973) A new family of Dacnonypha (Lepi-
illustrated guide to biological pest control. Publication doptera) based on three new species from southern
3386. University of California, Division of Agriculture and Australia, with notes on the Agathiphagidae. J Aust
Natural Resources, Oakland, CA Entomol Soc 12:1123
Hoy MA, Nowierski RM, Johnson MW, Flexner JL (1991) Nielsen ES, Kristensen NP (1996) The Australian moth
Issues and ethics in commercial releases of arthropod family Lophocoronidae and the basal phylogeny of
natural enemies. Am Entomol 37:7475 the Lepidoptera-Glossata. Invertebr Taxonomy 10:
Parrella MP, Heintz KM, Nunney L (1992) Biological control 11991302
through augmentative releases of natural enemies: a
strategy whose time has come. Am Entomol 38:
172179
Ridgway RL, Vinson SB (eds) (1977) Biological control by Australian Lappet Moths
augmentation of natural enemies. Plenum Press, New (Lepidoptera: Anthelidae)
York, NY
Sullivan DJ (1987) Efficacy of inundative releases. Ann Rev
Entomol 22:515531 john b. heppner
van Lenteren JC, Woets J (1988) Biological and integrated pest Florida State Collection of Arthropods, Gainesville,
control in greenhouses. Ann Rev Entomol 33:239269 FL, USA

Australian lappet moths, family Anthelidae, total

Auricular Openings 100 species, all from Australia. There are two sub-
families: Munychryiinae and Anthelinae. The
Lateral, slit-like openings to the insect heart by family is in the superfamily Bombycoidea (series
which blood is admitted into the dorsal vessel. Bombyciformes), in the section Cossina, subsec-
These are also known as ostia or incurrent ostia. tion Bombycina, of the division Ditrysia. Adults
medium size to very large (22166 mm wing-
span), with head vertex scaling (Fig.94) rough;
Australian Archaic Sun Moths haustellum absent (sometimes short or more
(Lepidoptera: Lophocoronidae) rarely long); labial short and mostly upcurved but
some more porrect; maxillary palpi vestigial;
john b. heppner antennae bipectinate (serrate to filiform in some
Florida State Collection of Arthropods, Gainesville, females); body robust. Wings broadly triangular
FL, USA

Australian archaic sun moths, family Lophocoro-

nidae, have six known species in Australia. The
family comprises its own superfamily, Lophocor-
onoidea, and is the only member of the infraorder
Lophocoronina, of the suborder Glossata. Adults
small (1015 mm wingspan), with head rough-
ened; labial palpi 3-segmented; haustellum short
and vestigial mandibles are present; maxillary
palpi are long and 4-segmented. Maculation is Australian Lappet Moths (Lepidoptera:
pale monotone with some darker spotting. Biolo- Anthelidae), Figure 94 Example of Australian
gies and larvae remain unknown, but adults are lappet moths (Anthelidae), Munychryia senicula
crepuscular in eucalyptus sclerophyll woodlands. Walker from Australia.
 Australian Sheep Blowfly, Lucilia cuprina Wiedemann (Diptera: Calliphoridae)
A 335

and rounded (rarely somewhat acute or even fal- short. Maculation is darkened with some darker
cate); hindwings rounded (rarely somewhat forewing spots. Biologies and larvae remain
acute); rarely with micropterous females. Macula- unknown.
tion mostly shades of brown with few markings,
but some more marked or lighter. Adults noctur-
nal, but at least one species with diurnal males.
Reference
Larvae are leaf feeders and generally colorful.
Kristensen NP (1978) Observations on Anomoses hylecoetes
Host plants recorded in several plant families, (Anomosetidae), with a key to the hepialoid families
including Casuarinaceae, Gramineae, Legumino- (Insecta: Lepidoptera). Steenstrupia 5:119
sae, and Myrtaceae, among others. Some species
have urticating larval setae.
Australian Realm

References The zoogeographic region of Australia and nearby

islands. It is characterized by a preponderance of
Common IFB, McFarland N (1970) A new subfamily for marsupials, large flightless birds, and parrots, as
Munychryia Walker and Gephyroneura Turner (Lepi- well as an absence of mammals.
doptera: Anthelidae) and the description of a new spe-
cies from Western Australia. J Aust Entomol Soc 9:1122
Zoogeographic Realms
Hulstaert PG (1928) Lepidoptera Heterocera. Fam. Anthelidae.
In: Genera Insectorum, vol 191, P. Wystman, Brussels, pp
113, 1 pl
Mills MB (1954) Observations on the life history of the moth
Anthela xantharcha (Meyrick) (Anthelidae). Western Australian Sheep Blowfly, Lucilia
Aust Nat 4:8690 cuprina Wiedemann (Diptera:
Seitz A (ed) (1925) Subfamilie: Anthelinae. In: Die Gross- Calliphoridae)
Schmetterlinge der Erde, vol 10. A. Kernen, Stuttgart,
364375, pl 46, 5658
Turner AJ (1921) Revision of Australian Lepidoptera Hypsi- john l. capinera
dae, Anthelidae. Proc Linn Soc New South Wales University of Florida, Gainesville, FL, USA
46:159191
Sheep in many areas of the world are plagued by
fly problems, but Australia, with 103,000,000 sheep,
Australian Primitive Ghost Moths has the most severe fly problems. The problem
(Lepidoptera: Anomosetidae) starts when wool becomes excessively wet. Con-
tinually wet wool is irritating to the sheeps skin,
john b. heppner and a condition called fleece rot develops. Fleece
Florida State Collection of Arthropods, rot results in skin inflammation and the secretion
Gainesville, FL, USA of serum from the irritated skin. Such a site is soon
teeming with bacteria. The wet, serum-containing
Australian primitive ghost moths, family Anomo- wool is attractive to ovipositing flies, and soon the
setidae, comprise a single genus with 1 known maggots hatching from those eggs feed not only
species from Australia. The family is in the super- on the fleece, serum, and bacteria, but the underly-
family Hepialoidea, of the infraorder Exoporia. ing skin. The problem is exacerbated by the pres-
Adults small (18 mm wingspan), with head rough- ence of urine, feces, sweat or other animal
scaled; haustellum short and vestigial mandi- secretions, all of which are attractive to flies. The
bles present; labial palpi short, 3-segmented; attack of flies on sheep in this manner is called
maxillary palpi minute, 2-segmented; antennae flystrike, and this condition can result in the
336
A Australian Sheep Blowfly, Lucilia cuprina Wiedemann (Diptera: Calliphoridae)

death of animals or the expense of treatments to alternative to crutching and mulesing is chemi-
prevent or cure this fly-based problem. The prob- cal protection, though this also requires repeated
lem is greatest in environments where warmth and treatment. Other alternatives include limiting
moisture occur frequently, and the cost for fly sheep raising to regions that are too dry or cool
treatments and loss of sheep due to flies is esti- for optimal fly population growth. Some breeds
mated at $100150 million annually in Australia. of sheep, such as Merino sheep, are particularly
The principal problem fly is Lucilia cuprina, known prone to problems because the are very wrinkled
in Australia as Australian sheep blowfly or primary and have a very dense wool. Historically, Merino
green blowfly. It is responsible for over 90% of the is the preferred sheep in Australia.
flystrike in Australia, but other flies can be Over 90% of the flystrikes in Australia are
involved. initiated by Lucilia cuprina, an introduced spe-
Beginning in about 1988, L. cuprina first cies. As is generally the case with blowflies, the
appeared in New Zealand, greatly exacerbating primary hosts are carrion, but when sheep are
the flystrike problem with sheep there, and afflicted with fleece rot or have thick mats of wet
extending flystrike attacks into a nearly season- wool, female flies will deposit eggs on live sheep.
long problem. In recent years, about half of the The presence of even a few flies (710 per hect-
flystrike incidents in New Zealand were caused are) is enough to cause severe problems if sus-
by L. cuprina, but the proportion attributable to ceptible sheep are present. The adults are metallic
this fly seems likely to grow as it continues to blue or green in color, and about 9 mm long.
spread. Flies initiate oviposition only after completing a
Sheep producers can take several actions to protein meal, which enables egg production, and
reduce or prevent flystrike. The mechanical then up to 250 eggs can be deposited in a single
removal of the wool around the tail, anus and batch on soiled wool. Each female typically pro-
vulva (in ewes) is called crutching, and helps duces two to three egg clusters during her life
prevent flystrike because these sites are most span of 23 weeks. The eggs hatch within 824 h,
likely to stay wet and soiled, and thus attractive and the maggots feed and grow to a length of
to ovipositing females. However, the wool grows 1015 mm in about 3 days. They then drop to the
continuously, so repeated removal of wool is soil, usually during the night or early morning,
necessary for this process to be effective, and is and pupate. About a week after pupation, the
not cost-effective for large producers of sheep. A adults emerge and start the cycle again. Thus an
more permanent treatment is the surgical entire life cycle is completed in about 2 weeks.
removal of skin around the anus and vulva, They reproduce best under warm (at least 18C),
resulting in wrinkle-free and wool-free tissue in wet conditions, but cannot tolerate high (over
these areas, which tend to remain clean and free 38C) temperatures, so fly populations may
of flies. This surgery is called mulesing, and is decrease during the middle of the summer in
normally conducted on lambs a few weeks after hot areas. Thus, peak blowfly populations tend to
birth. It takes about 4 weeks for the wounds to occur in spring, and late summer or autumn, in
heal, and should be conducted before flies are Australia.
active, or they will be attracted to the wounds, Sheep producers have several options when
making the problem worse. Mulesing is quite it comes to control of sheep blowfly. Producers
controversial because it is painful for the sheep, can apply organophosphate insecticides for rapid
and is being phased out in Australia. The tails of fly control, but these products tend not to be
lambs also can be docked to reduce the tendency very persistent (24 weeks), and resistance to
of the anal region to remain soiled and wet, and some organophosphates is known. Insect growth
this practice evokes less opposition. A common regulators take longer to take effect, but persist
 Australian Sheep Blowfly, Lucilia cuprina Wiedemann (Diptera: Calliphoridae)
A 337

longer (up to 14 weeks). Other products are pesticide residues. Avoidance of pesticides with
available, of course, and confer different advan- a history of fly resistance is important.
tages. Resistance to pyrethroid insecticides is Some of the other calliphorid species associ-
widespread in Australia. The insecticides are ated with sheep in Australia, and their local com-
sometimes applied by hand, which is advanta- mon names, include:
geous because they can be directed to the areas Lucilia sericata Meigen, the European green blow-
of the animal most susceptible to flystrike. To fly. This invader is the principal sheep blowfly in
reduce labor costs, automated (walk-through) the United Kingdom, but only a minor pest in
sprayers are sometimes used, but such applica- Australia. It is virtually identical to Lucilia cuprina
tions are less directed and commonly less in appearance.
effective in their coverage of sheep. Applications Calliphora stygia (Fabricius), the eastern gold-
are most common soon after shearing, and if enhaired blowfly. This fly is native to Australia.
applications are delayed, unacceptable insecti- It is brown and about 13 mm long. It prefers
cide residues on the sheep may result. cooler weather, disappearing in the summer
In addition to chemical treatment, growers months.
have recently adopted the practice of trapping Calliphora augur (Fabricius), the lesser brown or
flies. Traps consist of buckets with special lids bluebodied blowfly. This native fly is a secondary
containing entrance cones that allow the blowfly species, not usually attacking sheep until other spe-
to enter but not leave the trap. Each bucket con- cies have attacked. It is mostly brown, but has a
tains a number of chemical lures that mimic the metallic blue patch on its abdomen. It is about 11
odors of fleece rot, urine, feces, and animal car- mm long. It is found commonly in the summer. It
casses. Once trapped inside the bucket, the flies differs from most other blowflies in depositing lar-
die from dehydration. Traps are distributed at a vae rather than eggs.
rate of one trap per 100 sheep, and they are rec- Chrysomya rufifacies (Macquart), the green hairy
ommended to be used early in the season when maggot blowfly. This is another native, secondary
the fly population in naturally at its lowest. In species. It is metallic green, and can be distin-
addition to removing flies from the population, guished from Lucilia by the broad bands on its
and thereby reducing the rate of flystrike, the abdomen and its black forelegs. The adult is
traps are useful for monitoring population about 9 mm long. The larvae are distinctive,
densities. bearing sharp spines (the hairs) over its dark
Optimal management of sheep blowfly is body. It also is known to feed on other maggots.
accomplished with implementation of an inte-
grated or multi-faceted approach. This involves
reducing the attractiveness of sheep to flies by References
docking lambs tails, and by shearing, crutching
or mulesing all sheep. Keeping the flocks sepa- Armstrong R, Knights G, Urech R, Green P, Ward M.
rated helps reduce the movement of flies from Undated. Sheep parasites. The LuciTrap sheep blowfly
flock to flock. Regular inspection of the flock is trapping system. Queensland Government, Depart-
desirable, and catching and shearing of sheep, ment of Primary Industries and Fisheries, DPI&F
note, 4 pp
and spot treatment of sheep with fly infestations Heath ACG, Bishop DM (2006) Flystrike in New Zealand: an
is desirable. Trapping and monitoring of adult overview based on a 16-year study, following the intro-
fly populations with fly traps are helpful. Treat- duction and dispersal of the Australian sheep blowfly,
Lucilia cuprina Wiedemann (Diptera: Calliphoridae).
ment of the entire flock may be necessary if the
Vet Parasitol 137:333344
fly population becomes high, but timing needs Joshua E, Evans I (1999) Sheep blowflies. New South Wales
to be optimized to avoid contamination with Agriculture, Agnote DAI-70, 3 pp
338
A Australian Silkworm Moths (Lepidoptera: Carthaeidae)

Levot G (2000) Common blowflies that strike sheep in NSW, Larvae are leaf feeders, with numerous clubbed
Australia. New South Wales Agriculture, Agnote DAI-
152, 4 pp
setae. Host plants are only in Proteaceae.
Wilson K, Armstrong R (2005) Sheep parasites. Management
of blowflies. Queensland Government, Department of
Primary Industries and Fisheries, DPI&F note. 5 pp References

Common IFB (1966) A new family of Bombycoidea (Lepi-

Australian Silkworm Moths doptera) based on Carthaea saturnioides Walker from
(Lepidoptera: Carthaeidae) Western Australia. J Entomol Soc Queensland 5:2936
Common IFB (1990) Family Carthaeidae. In: Moths of
Australia. Melbourne University Press, Melbourne,
john b. heppner pp 401403
Florida State Collection of Arthropods, Heppner JB (2003) Carthaeidae. In Lepidopterorum
Catalogus, (n.s.). Fasc. 105. Association for Tropical
Gainesville, FL, USA Lepidoptera, Gainesville, p 8

Australian silkworm moths, family Carthaeidae,

are a monobasic relict family in Bombycoidea with
a single species from western Australia. The family Austrophasmatidae
is in the superfamily Bombycoidea (series Bomby-
ciformes), in the section Cossina, subsection Bom- A family of gladiators (order Mantophasmatodea)
bycina, of the division Ditrysia. Adults large Gladiators (Mantophasmatodea)
(75100 mm wingspan), with head scaling rough-
ened; haustellum developed; maxillary palpi small,
3-segmented; antennae bipectinate, or apparently Autecology
tripectinate (serrate in females); body robust.
Wings broad and triangular but termen rounded; The ecology of individuals, or the effects of the phys-
forewing with somewhat acute apex (Fig.95). Mac- ical and chemical environment on individual organ-
ulation gray with large dark eyespot medially on all isms (rather than on populations or communities).
wings and band of gray-brown at base and along Synecology
termen; hindwing reddish at apex with blue in eye-
spot. Adults are nocturnal (usually after midnight).
Autocidal Control
The use of insects for self destruction, normally
through release of sterile or genetically altered
insects into a natural population.

Autoecious Life Cycle

A life cycle in which the insects (generally aphids)
are host plant specific, living on a single host or
Australian Silkworm Moths (Lepidoptera: some closely related hosts throughout the year.
Carthaeidae), Figure 95 Example of Australian This is also called monoecious (contrast with
silkworm moths (Carthaeidae), Carthaea heteroecious life cycle).
saturnioides Walker from Australia. Aphids
 Austremerellidae
A 339

Attevidae s ubsection Cossina, of the division Ditrysia. Adults

small (1030 mm wingspan), with head scaling
A family of moths (order Lepidoptera). They are average; haustellum absent; labial palpi short;
commonly known as tropical ermine moths. maxillary palpi absent; antennae filiform (thicker
Tropical Ermine Moths in males). Body robust. Wings elongated and
Butterflies and Moths rounded. Maculation somber hues of gray, with
mainly a single forewing marking (one species is
yellow and black). Adult activity uncertain but
Aulacidae may be crepuscular. Larvae flattened, with lateral
protrusions; highly evolved as parasites of leaf-
A family of wasps (order Hymenoptera). hoppers, scale insects, or psyllids (Hemiptera) in
Wasps, Ants, Bees and Sawflies early instars, and then as predators of ant larvae.
The ants tolerate the predatory larvae, keep them
in their nests and care for them, since they give the
Aulacigastrid Flies ants desirable exudates. Eggs are laid on plants fre-
quented by likely hemipteran hosts and young lar-
Members of the family Aulacigastridae (order
vae then search for a suitable host to parasitize
Diptera).
upon hatching; eggs are tended by protective ants.
Flies

References
Aulacigastridae
Common IFB (1990) Family Cyclotornidae. In: Moths
A family of flies (order Diptera). They commonly of Australia. Melbourne University Press, Carlton,
are known as aulacigastrid flies. pp 306309
Flies Epstein ME (1996) Epipyropidae Dyar, 1903 and Cyclotorni-
dae Meyrick, 1912. In: Revision and phylogeny of the
limacodid-group families, with evolution ary studies on
slug caterpillars (Lepidoptera: Zygaenoidea). Smithso-
Australembiidae nian Contributions to Zoology 582:1102
Hinton HE (1951) Cyclotornidae. In Myrmecophilous
A family of web-spinners (order Embiidina). Lycaenidae and other Lepidoptera a summary, 167168.
Proceedings of the South London Entomological and
Web-Spinners
Natural History Society 194950:111175
Nielsen ES, Common IFB (1991) Cyclotornidae. In: Lepi-
doptera (moths and butterflies), Insects of Australia.
Melbourne University Press, Carlton, pp 879880
Australian Parasite Moths
(Lepidoptera: Cyclotornidae)
Australimyzidae
john b. heppner
Florida State Collection of Arthropods, Gaines- A family of flies (order Diptera).
ville, FL, USA Flies

Australian parasite moths, family Cyclotornidae, Austremerellidae

include only five known species from Australia.
The family is in the superfamily Cossoidea (series A family of mayflies (order Ephemeroptera).
Limacodiformes) in the section Cossina, Mayflies
340
A Austroniidae

Austroniidae Autosomes

A family of wasps (order Hymenoptera). All chromosomes except the sex chromosomes.
Wasps, Ants, Bees and Sawflies Each diploid cell has two copies of each
autosome.

Austroperlidae
Autotomy
A family of stoneflies (order Plecoptera).
Stoneflies Self-amputation which functions as an escape
mechanism. Under some circumstances, body
parts are deliberately shed to avoid capture by
predators. Arthropod legs are shed readily, and
Austropetaliidae
when this occurs early in life they can be regener-
A family of dragonflies (order Odonata). ated, in whole or in part.
Dragonflies and Damselflies

Autotroph
Autogenic Succession Organisms that obtain energy from the sun and
other materials from inorganic sources (contrast
A temporal succession of species that is driven by
with heterotroph).
processes within the community (contrast with
allogenic succession).
Auxiliary Vein
Autogenous A supplementary vein. The subcosta is often con-
sidered to be auxiliary.
Among blood-feeding insects, the ability to pro- Wings of Insects
duce eggs without a prior blood meal.

Auxiliae
Autoradiography
Small plates beneath the base of the pretarsal
A method for detecting radioactively labeled mol- claws, bearing the pulvilli (if present). These are
ecules through exposure of an x-ray sensitive pho- sometimes known as auxilliary sclerites.
tographic film. Legs of Hexapods

Autoregulatory Control Avermectins

Regulation of the synthesis of a gene product by Macrocyclic lactones derived from a soil-dwelling
the product itself. In some systems, excess gene microbe, the actinomycete Streptomyces avermitilis.
product behaves as a repressor and binds to the They are chloride channel agonists. These materials
operator of its own structural gene. are considered to be broad spectrum, slow acting,
 Avian Malaria, Bird Malaria
A 341

natural pesticides, and display activity against helm- parasites multiply in all of these tissues. Later gen-
inths, insects, mites, and nematodes. They are used erations of the parasites are less selective in host
widely to treat animals for parasitic organisms, but cell preference and the parasites may be found in
also for insect and mite pests in agriculture. They various other tissues. In the chronic phase the par-
degrade readily and lack persistence and mobility, so asite causes little harm. Several species of mosqui-
are valued in integrated pest management programs toes belonging to genera Anopheles, Culiseta,
and even in some organic agriculture situations. Mansonia, Aedes, Armigeres and Culex are found
Common commercial products include Abamectin, to be experimentally susceptible to different Plas-
Agrimek, Avert, Avid, and Vertimec. modium species that infect birds, but the natural
Insecticides vectors are mostly Culex and rarely Aedes species.
The life cycle of Plasmodium (Huffia) h ermani,
a parasite of wild turkeys (Meleagris gallopavo L.)
Avian Malaria, Bird Malaria that was described (Fig.96) from Florida in 1975,
will serve as an example. This parasite was discov-
jai k. nayar ered after specialized subinoculation technique of
University of Florida, Vero Beach, FL, USA blood (heparinized or citrated) from chronically
infected wild older turkeys into young poults of
Avian malaria is an infectious disease and it is broad-breasted-white domestic turkeys. In turkeys
found all over the world, especially in tropical and (both wild and domestic) the malaria parasite infec-
temperate areas. It produces a wide range of effects tion causes anemia, splenomegaly, and reduced
in avian hosts, from no apparent clinical signs to weight gains in poults. Natural infection of the
severe anemia and death. It has served as an exper- young turkey poults begins with the bite of an
imental model for human malaria during the early infected culicine mosquito. Sporozoites introduced
history of malaria research. Avian malaria is not with the salivary gland secretions are carried to the
one disease, but many and is caused by distinct reticular cells of the splenic Malpighian body. After
species of a protozoan blood parasite, Plasmodium, a minimum of three generations of exoerythrocytic
that is transmitted by mosquitoes. It belongs to development in these cells that takes about
Class Sporozoa, Subclass Telosporidia, Order Coc- 1014 days, the stage of parasite called merozoites
cidiomorphida and Suborder Haemosporidina, may spill over in the blood circulation and invade
and Genus Plasmodium. There are about 30 spe- basophilic cells of the erythrocyte series, or may
cies of Plasmodium parasites recognized that infect continue asexual reproduction. These merozoites
birds world-wide and they are grouped into four after invasion of basophilic cells of the erythrocyte
subgenera depending on the shape and size of the series transform into trophozoites (uninucleated,
parasite in erythrocytes and presence or absence either elongate or round), schizonts (rounded with
of schizogony: Haemamoeba species have round 614 nuclei arranged peripherally as a rosette)
gametocytes; Huffia species have elongate gameto- and finally elongate slender gametocytes (male and
cytes and schizogony in primitive red cells; Gio- female) with irregular margins in mature eryth-
vannolaia species have relatively large asexual rocytes. Time required may vary from 2 to 4 days.
stages and no schizogony; and Novyella species In general erythrocytic avian merozoites appear
have small asexual stages and no schizogony. to be able to choose among four possible fates.
Plasmodium parasites in birds are primarily Most may continue schiozgony in erythrocytes,
blood parasites, but in the acute phase they do but some may become micro- and macro-gameto-
infect a variety of other tissues, the lungs, endothe- cytes (male or female gametocytes, respectively)
lial cells of capillaries in the brain, and the reticu- or they may re-initiate asexual reproduction in
lar cells of the splenic Malpighian body. The the tissues as phanerozoites. Northern bobwhites
342
A Avian Malaria, Bird Malaria

Life cycle of avian (bird) malaria

Infected

0 1 2 3 4 cm
Control
Normal and
infected spleen

Early stages of P. hermani

in blood cells
Final host
and Reservoir

Mature gametocytes
in infected bllod cells

Sporozoites
Ingestion of mature
gametocytes

Oocyst 3
Oocyst 2 Sporozoites
Gametocyte
Ookinete
Oocyst 1

Salivary gland
Infected midgut

Lm
Sporozoites Hphy

Lb
Intermediate host
Developmental stages in mosquito

Avian (Bird) Malaria, Figure 96 Life cycle of Plasmodium hermani. Stages of avian malarial parasite in
mosquitoes: o ocyst 1=young oocyst about 4 days old, oocyst 2=about 7 days old, oocyst 3=about
10 days old. Lm=labium, Lb=labrum, and Hphy=hypopharynx.

(Colinus virginianus) in Florida is also a natural and infect young chicks (Gallus domesticus). Three
experimental host of P. hermani. additional species of turkey malaria have been
Natural and experimental vector for P. her- reported from other parts of the U.S.A. These are
mani in wild turkeys and northern bobwhites in P. hexamerium-like from Texas, P. lophurae from
Florida is Culex nigripalpus, but experimental Wisconsin, and P. kempi from Missouri, Wiscon-
studies indicate that other culicines (Cx. salinar- sin, Minnesota and North Dakota. Natural vec-
ius and Cx. restuans) may be involved to a lesser tors of these species of avian malaria are
degree. Plasmodium hermani is not transmitted presumably also culicines although they have not
by Cx. quinquefasciatus in Florida and it does not been determined. Experimental studies have
 Avian Malaria, Bird Malaria
A 343

shown that Cx. tarsalis and Cx. pipiens pipiens can P. elongatum from 3 raptors species (red-tailed
be infected with P. kempi. Other species of Aedes, hawk, bald eagle and eastern screech owl) in Flor-
Culiseta and Wyeomyia can be experimentally ida and Cx. restuans was shown to be the experi-
infected with avian malarias, but their contribu mental vector of P. forresteri n. sp., from several
tion in natural transmission of the parasite is species of raptors from Florida and Georgia.
unknown. In some of the experimental mosquitoes Normally epizootics of avian malaria are rare.
that are not natural vectors, a defense reaction Several species of avian malaria, e.g., P. gallinaceum,
occurs and development of oocysts in the mos- P. juxtanucleare and P. durae are the most danger-
quitoes is compromised by intracellular melaniza- ous for poultry, producing up to 90% mortality. In
tion of the developing oocysts. addition, there are a few documented cases where
The developmental cycle of the avian malar- avian malaria has been shown to either eliminate
ial parasite within the susceptible mosquito is or reduce bird populations. Until 1826, birds were
similar in all vector species and begins with the plentiful in Hawaii and mosquitoes were absent
ingestion of erythrocytes (blood cells) contain- from the region. Introduction of Culex pipiens
ing male and female gametocytes from the from ships traveling to Hawaiian Islands intro-
infected bird. As the blood meal passes into the duced a lethal form of avian malaria, which elimi-
gut, the change in the environmental factors nated indigenous bird populations. In another
induces gametocytes to emerge from the eryth- case, it is suggested that an abnormally early rainy
rocytes (within 46 h). The microgametes (male season over a 2-year period in southern Florida in
gametocytes) begin the prefertilization process the 1960s resulted in a widespread malaria epi-
by undergoing exflagellation. Soon thereafter zootic in wild turkey populations, which caused a
individual microgametes are released, which significant decline in the wild turkey population.
swim actively to the macrogametes (female In recent years, avian malaria has caused severe
gametes) and penetrate them culminating in fer- mortality in exotic bird populations, especially
tilization. This results in the formation of a penguins, in zoos across the U.S.A.
zygote, which elongates and undergoes cytoplas-
mic changes and forms motile ookinetes (within
24 h). The mature ookinetes migrate intracellu- References
larly through the midgut cells and move into the
outer wall of the midgut facing the hemocoel, Atkinson CT, Drake BM, Shema NP (2001) Pathogenicity,
where the ookinetes form a tumor like body, or serological responses, and diagnosis of experimental
and natural malarial infection in native Hawaiian
oocyst. Within 812 days, the timing depending
thrushes. Condor 103:209218
on temperature and species of the parasite, Forrester DJ (1991) The ecology and epizootiology of avian
schizogony within the oocyst produces hun- pox and malaria in wild turkeys. Bull Soc Vector Ecol
dreds, or even thousands of sporozoites. Sporoz- 16:127148
Garnham PCC (1966) Introduction to the avian subgenera, Hae-
ites are spindle-shaped organisms measuring mamoeba, Giovannolaia, Novyella and Huffia. Chapter
about 89 m in length and about 1 m wide. XVII. In: Malarial parasites and other Haemosporidia.
These are liberated into the body cavity by rup- Blackwell Scientific Publications, Oxford, UK, pp 514741
ture of the oocyst wall, and some find their way Huff CG (1965) Susceptibility of mosquitoes to avian malaria.
Exp Parasitol 16:107132
into the salivary glands, where they mature in Nayar JK, Knight JW, Telford SR Jr (1998) Vector ability of
12 days. A bite of an infected mosquito causes mosquitoes form isolates of Plasmodium elongatum
infection in young turkey poults and starts the from raptors in Florida. J Parasitol 84:542546
Seed TM, Manwell RD (1977) Plasmodia of birds. In Para-
life cycle all over again.
sitic protozoa. vol III. Gregarines, Haemogregarines,
Recently, Cx. nigripalpus, Cx. restuans and Cx. Coccidia, Plasmodia, and Haemoproteids. Academic
salinarius were shown be experimental vectors of Press, New York, NY
344
A Axenic

Telford SR, Jr Forrester DJ (1975) Plasmodium (Huffia) her- Axillary

mani sp. n. from wild turkeys (Meleagris gallopavo) in
Florida. J Protozool 22:324328
Telford SR, Jr Nayar JK, Foster GW, Knight JW (1997) Plas- This refers to the point of origin of a structure,
modium forresteri n. sp., from raptors in Florida and often a junction or angle. Thus, the axillary
southern Georgia: its distinction from Plasmodium region of the wing is the wing base, and the
elongatum morphology within and among host species
and by vector susceptibility. J Parasitol 83:932937 axillary lobe in Diptera is the sclerite covering
the base of the wing.

Axenic Axon

Free from associated organisms. Including inter- A portion of the nerve cell that transmits nerve
nal symbionts. impulses away from the cell body to a synapse.
This also is called nerve fiber.
Nervous System

Axenic Culture
Azadirachtin
Culture of insects in the complete absence of other
species (usually of microorganisms), including This is a triterpenoid derived from the neem tree,
internal symbionts. Azadirachta indica. It is found in many parts of
the tree, but is particularly concentrated in the
seeds, from which it is extracted as used as an
insecticide. It also has other properties, including
Axiidae medicinal. Although azadirachtin is a principal
factor in insecticidal products, it is not the only
A family of moths (order Lepidoptera) also known active property, and is not especially useful as a
as gold moths. feeding deterrent, though crude extractions of
Gold Moths the tree contain feeding deterrents.
Butterflies and Moths Neem
B

Babesia Bacillus sphaericus

A genus of Protozoa that is transmitted to animals colin berry

by ticks. Cardiff University, Cardiff, Wales, United
Babesiosis Kingdom
Piroplasmosis
The bacterium Bacillus sphaericus is best-known
to entomologists because of the toxicity of some
Babesiosis strains to the larval stages of mosquitoes. This tox-
icity will be examined below but first, some con-
Several related diseases caused by infection sideration of the taxonomic group that is known
with Babesia protozoans, and transmitted by as Bacillus sphaericus is necessary.
ticks.
Piroplasmosis
Taxonomy

Identification of a bacterium as a B. sphaericus iso-

Bacillary Paralysis late is based on relatively few morphological fea-
tures (e.g., the possession of a spherical terminal
A disease of silkworm larvae caused by ingestion
spore) and a limited number of biochemical tests
of spores and parasporal crystals of Bacillus
(e.g., inability to ferment sugars). As a result, the
thuringiensis.
classification contains a heterogeneous collection
of strains and it has been shown that, at the DNA
level, these can be divided into five major homol-
Bacillus larvae (=Paenibacillus ogy groups (groups I-V), each of which could be
larvae; Bacteria) considered as a separate species. All of the insecti-
cidal strains of B. sphaericus are found within a
The bacterium responsible for causing American subdivision of one of these groups Group IIA;
foulbrood in honey bees; it is now known as however, not all strains that fall within this group
Paenibacillus larvae. are insecticidal. It is the insecticidal strains of
American Foulbrood B. sphaericus and their properties that will be con-
Paenibacillus sidered further below.
346
B Bacillus sphaericus

Target Range The Insecticidal Toxins

Bacillus sphaericus is toxic to a small range of dip- Insecticidal strains of B. sphaericus owe this
teran target insects, principally mosquitoes (with property to the fact that they produce protein
some possible activity against Chironomus spe- toxins. To date, several different types of toxins
cies). Within the mosquitoes, B. sphaericus is often have been identified. The names of these toxins,
seen as most active against Culex species with along with notes on their mechanisms of action,
lower activity against Anopheles, Mansonia and are given in the table below.
Psorophora and lowest activity against Aedes spe- All the toxins except sphaericolysin exert
cies. However, these generalizations should be their effects on the gut of the aquatic larval form
treated with caution as some Aedes species are as of the mosquito after ingestion of the bacterium.
sensitive as Culex species so that susceptibility The binary toxin (Bin) is produced on sporula-
must be judged at the species level and not by tion whereupon it is deposited in spore-associ-
genus. In addition, activity of a B. sphaericus toxin ated crystal As shown in the figure of B.
has been reported against the German cockroach, sphaericus, (Fig.1) the spore is the round body at
Blattela germanica. the top, the crystal is the grey, rhomboid body in
the center, and both are contained within the
elongated exosporium. Once eaten by a mos-
quito larva, the crystal dissolves and its two com-
Field Use ponent proteins (BinA -42 kDa and BinB -51
kDa) are able to bind to specific receptors in the
Bacillus sphaericus strains have been used in gut before lysing the cell by pore formation.
control programs worldwide to suppress mos- Note: although the Bin proteins form a spore
quito populations that are of nuisance or public associated toxin crystal, they are not related to
health importance. For this purpose, only strains the majority of the crystal-associated Cry and
showing high-level, spore-associated toxicity Cyt toxins of Bacillus thuringiensis. Most highly
are used (e.g., VectoLex and Spherimos from toxic B. sphaericus strains produce only the Bin
Valent BioSciences, or Sphaerus from Bthek toxin in association with spores (Mtx toxins are
Ltda). For production of maximum toxicity, as produced only in vegetative cells and in very low
well as for ease of production and storage, such quantities). The existence of only one toxin in
formulations are produced from fully sporu- spores applied in mosquito control programs in
lated B. sphaericus cultures that can be sprayed the field can lead to resistance in target popula-
or applied as blocks or granules that disperse in tions. A few strains of B. sphaericus can over-
the aqueous habitats. come this resistance in Culex mosquitoes. These

Bacillus sphaericus, Table 1 Toxins of Bacillus sphaericus

Toxin (molecular wt.) Mechanism of action Reference
Bin (51 and 42 kDa) Pore formation Oei et al. (1992), Schwartz et al. (2001)
Mtx1 (100 kDa) ADP-ribosylation Thanabalu et al. (1993)
Mtx2 (31.8 kDa) Pore formation Thanabalu and Porter (1996)
Mtx3 (35.8 kDa) Pore formation Liu et al. (1996)
Cry48/Cry49 (136 and 53 kDa) Pore formation Jones et al. (2007)
Sphaericolysin (53 kDa) Pore formation Nishwaki et al. (2007)
 Bacillus sphaericus
B 347

References

Ahmed I, Yokota A, Yamozoe A, Fujiwara T (2007) Proposal of

Lysinibacillus boronitolerans gen. nov. sp. nov., and trans-
fer of Bacillus fusiformis to Lysinibacillus fusiformis comb.
nov. and Bacillus sphaericus to Lysinibacillus sphaericus
com. nov. Int J Syst Evol Microbiol 57:11171125
Jones GW, Nielsen-Leroux C, Yang Y, Yuan Z, Dumas VF, Mon-
nerat RG, Berry C (2007) A new Cry toxin with a unique
two-component dependency from Bacillus sphaeriucs.
FASEB J 21:41124120
Krych VK, Johnson JL, Yousten AA (1980) Deoxyribonucleic
acid homologies among strains of Bacillus sphaericus.
Int J Syst Bacteriol 30:476484
Liu J-W, Porter AG, Wee BY, Thanabalu T (1996) New gene
from nine Bacillus sphaericus strains encoding highly
conserved 35.8-kilodalton mosquitocidal toxins. Appl
Environ Microbiol 62:21742176
Nielsen-LeRoux C, Rao DR, Murphy JR, Carron A, Mani TR,
Hamon S, Mulla MS (2001) Various levels of cross-
resistance to Bacillus sphaericus strains in Culex pipiens
(Diptera: Culicidae) colonies resistant to B. sphaericus
strain 2362. Appl Environ Microbiol 67:50495054
Nishiwaki H, Nakashima K, Ishida C, Kawamura T, Matsuda K
(2007) Cloning, functional characterization, and mode
of action of a novel insecticidal pore-forming toxin,
sphaericolysin, produced by Bacillus sphaericus. Appl
Environ Microbiol 73:34043411
Oei C, Hindley J, Berry C (1992) Binding of purified Bacillus
sphaericus binary toxin and its deletion derivatives to
Culex quinquefasciatus gut: elucidation of functional
binding domains. J Gen Microbiol 138:15151526
Schwartz J-L, Potvin L, Coux F, Charles J-F, Berry C,
Humphreys MJ, Jones AF, Bernhart I, Dalla Serra M,
Bacillus sphaericus, Figure 1 Bacillus sphaericus.
Menestrina G (2001) Permeabilization of model lipid
(Photo courtesy of Dr. J.F. Charles.) membranes by Bacillus sphaericus mosquitocidal binary
toxin and its individual components. J Membr Biol
184:171183
Silva-Filha MH, Nielsen-LeRoux C, Charles J-F (1999) Iden-
strains produce a novel toxin pair, Cry48/Cry49, tification of the receptor for Bacillus sphaericus crystal
which are deposited as crystals outside the exo- toxin in the brush border membrane of the mosquito
sporium. The Cry48 protein is related to 3-do- Culex pipiens (Diptera: Culicidae). Insect Biochem Mol
Biol 29:711721
main Cry toxins of B. thuringiensis while Cry49 Silva-Filha M-H, Regis L, Nielsen-LeRoux C, Charles JF
is related to the Bin proteins. Both components (1995) Low-level resistance to Bacillus sphaericus in a
are required for toxicity to Culex larvae and do field-treated population of Culex quinquefasciatus (Dip-
not appear to kill other insects (including Anoph- tera: Culicidae). J Econ Entomol 88:525530
Thanabalu T, Berry C, Hindley J (1993) Cytotoxicity and
eles and Aedes mosquitoes). ADP-ribosylating activity of the mosquitocidal
Despite reports of resistance developing in toxin from Bacillus sphaericus SSII-1: Possible roles
mosquito populations, careful use of this bacte- of the 27- and 70-kilodalton peptides. J Bacteriol
175:23142320
rium is likely to enable the continued favorable
Thanabalu T, Porter AG (1996) A Bacillus sphaericus
use of this product for integrated control programs gene encoding a novel type of mosquitocidal toxin
in the field. of 31.8 kDa. Gene 170:8589
348
B Bacillus thuringiensis

Yuan Z, Zhang YM, Cai QX, Liu EY (2000) High-level field farms. Additional B. thuringiensis isolates have been
resistance to Bacillus sphaericus C341 in Culex
detected in various insectaries, stored product envi-
quinquefasciatus from Southern China. Biocontrol Sci
Technol 10:4149 ronments, and grain processing facilities. Studies
have suggested that B. thuringiensis is a normal
inhabitant of the foliage of plants. However, the soil
Bacillus thuringiensis habitat has been the primary source for isolating
novel B. thuringiensis isolates. Whether or not B. thu-
Bacillus thuringiensis was initially described early ringiensis undergoes saprophytic development in
in the 1800s as the causal agent of the sotto bacil- soil is unclear. Many bacilli considered to be close
lus disease of the silkworm Bombyx mori. Later relatives of B. thuringiensis are known to inhabit
studies by Aoki in 1915 demonstrated that this hypogean environments. Presently, it has been esti-
bacterial agent produced a crystalline toxic mate- mated that over 60,000 isolates of B. thuringiensis are
rial at sporulation. In 1911, Berliner isolated the being maintained in culture collections worldwide.
type species Bacillus thuringiensis var. thuringien- Members of B. thuringiensis are rod-shaped
sis from the flour moth in the province of Thurin- (1.01.2 by 35 microns), gram positive, facultative
gia, Germany. Following this report, a series of anaerobes which utilize carbohydrates as preferred
papers demonstrated that B. thuringiensis could energy sources. Classification based on 16S rRNA
infect and kill a variety of lepidopteran host insects. sequence data clusters B. thuringiensis with B. cereus,
Until the 1970s, all B. thuringiensis isolates were B. mycoides, and B. anthraxis within the B. subtilus
characterized as being toxic to immature insects group. Bacteriological tests define B. thuringiensis
within the order Lepidoptera. However, today var- isolates as being closely related to B. cereus. In fact, the
ious B. thuringiensis subspecies have been identi- ability of B. thuringiensis to produce the crystalline
fied which are lethal to lepidopterans, dipterans, inclusion is the major feature that separates it from
coleopterans, and/or nematodes. B. cereus. Acrystalliferous strains of B. thuringiensis
Historically, Bacillus thuringiensis has been iso- generated by plasmid curing are nearly identical to
lated from environments associated with insect B. cereus. The growth of B. thuringiensis on relatively
populations and/or plant material. For example, B. simple media (0.1% glucose, 0.2% NH2SO4, 0.2%
thuringiensis was discovered initially in silkworm yeast extract) is biphasic and involves both a

Bacillus thuringiensis, Figure 2 Electron micrograph of thin section of sporulating cell of

Bacillus thuringiensis. Note the thick-walled endospore and endotoxin-containing crystalline
inclusion.
 Bacillus thuringiensis
B 349

v egetative cell division phase and a sporulation B. thuringiensis resistance is the same as that
phase. During sporulation, B. thuringiensis pro- required for resistance to the neurotoxic insectides:
duces both the (Fig.2) endospore and crystalline a multigenerational (continuous) exposure of the
inclusions. The endospore, highly resistant to envi- host to the mortality agent. With B. thuringiensis,
ronmental stress, provides a mechanism for long- this may be achieved either by a conventional
term survival of B. thuringiensis. This mesophilic spray program or by a contiguous planting of B.t.-
bacterium can be produced easily on solid media or transgenic plants.
under submerged fermentation conditions. The Early work on the mode of action of the
rapid growth and sporulation of B. thuringiensis in -endotoxin addressed the effect of extracted
relatively inexpensive media under submerged fer- inclusions on lepidopteran larvae. Initial symp-
mentation conditions have been key factors in its toms, occurring within one hour of ingestion of
successful development as a biopesticide. Many of inclusions, include a cessation of larval feeding
the advances made in the fermentation industry and gut paralysis. The endotoxin-induced gut
over the past three decades have improved the paralysis retards passage of ingested plant material
quality of B. thuringiensis products. and spores, allowing spores to germinate and
Initially, it was presumed that the B. thuringi- undergo vegetative development. At later stages,
ensis was an infectious agent and much effort was intoxicated larvae display a general paralysis
spent on maximizing the delivery of bacterial followed by death within one to two days post-
spores to host insects. Early field experiments in challenge. Histological studies demonstrated that
the 1960s involving applications of spore-based the toxins released from inclusions and proteolyti-
formulations against pest insect populations cally activated in the gut lumen specifically target
produced erratic results. By the 1970s, it was dem- the midgut columnar cells. Examination of midgut
onstrated that the primary insecticidal activity of tissue dissected from treated larvae initially
B. thuringiensis against lepidopteran hosts was due revealed that columnar cells are slightly swollen
to the -endotoxins comprising the crystalline but over time goblet and columnar cells become
inclusions. These endotoxins are extremely potent heavily vacuolated. At the late stages, midgut cells
and are toxic to target insects at picomole concen- dislodge from the basement membrane and are
trations. However, with certain insects such as the sloughed off. At subcellular levels, the -endotoxins
larvae of the Indian meal moth Plodia interpunc- produce pores in the membrane. The activated
tella, the addition of spores synergizes the activity toxin recognizes specific cell membrane receptors
of the -endotoxins. Potentially, this synergism is and then generates small pores in the cell mem-
due either to additional toxins in the spore coat or brane. The subsequent depolarization of the
to the outgrowth of vegetative cells from ingested columnar cell stimulates the closure of the gap
spores. Many commercial formulations contain- junctions, causing an increase in intracellular pH
ing high levels of -endotoxin have proven to be as and cell hypertrophy. Without a functional colum-
effective as chemical insecticides yet exhibit high nar cell, the K+ pump in goblet cells ceases to func-
specificity to target pests without detrimental tion. Intoxicated cells, due to increases in internal
effects on beneficial insects and animals. By the pH and loss of ion transport, become osmotically
1990s, B. thuringiensis-based products represented sensitive and lyse.
more than 90% of the biopesticides used world- Importantly, the -endotoxins are primary
wide. Until the 1980s, it was proposed that micro- translation products of bacterial genes and are
bial-based products such as B. thuringiensis, unlike amenable to genetic engineering techniques. By
their chemical pesticide counterparts, did not the early 1980s, U.S. and European laboratories
select for resistance in treated insect populations. had successfully isolated, cloned, and character-
The critical element required for the selection of ized genes coding for -endotoxins. During the
350
B Backswimmers

past two decades over 90 different protoxin genes Bacterial Conjugation

containing representatives of both Cry and cyt
classes have been cloned and sequenced. The A temporary union between two bacteria, during
technology developed to study the structure and which genetic material is exchanged. All or some
function of the -endotoxin has provided the of the chromosomes are transferred from the
foundation for the genetic engineering of this class donor to the recipient
of biopesticides.In several respects,the -endotoxin
gene has played a pivotal role in agricultural
biotechnology. The -endotoxins derived from Bacterial Wilt of Corn
recombinant bacteria represent the first group of
genetically engineered products released into agri- This is an important insect-transmitted disease of
cultural systems. To date, recombinant microbes corn (maize).
expressing -endotoxin genes have been field Transmission of Plant Diseases by Insects
tested worldwide in numerous agricultural sys-
tems. Secondly, the -endotoxin genes have been
used as models for optimizing the gene expression Bacterial Wilt of Cucumbers
in transgenic plants. Over the past decade,
researchers have manipulated the -endotoxin This is an important insect-transmitted disease of
gene and have altered the protoxin profile as well cucurbit crops.
as the toxicity and specificity of individual Cry Transmission of Plant Diseases by Insects
toxins. Significantly, Cry gene expression in trans-
genic plants has provided protection against insect
herbivory Bacteremia
The presence of bacteria in the hemolymph or blood
References of invertebrates and other animals without produc-
tion of harmful toxins or other deleterious effects
Aronson A (2002) Sporulation and -endotoxin synthesis by
Bacillus thuringiensis. Cell Mol Life Sci 59:417425
Fieltelson JS, Payne J, Kim L (1992) Bacillus thuringiensis and
beyond. Bio/Technology 10:271276 Bacteriophage
Knowles BH, Dow JA (1993) The crystal endotoxin of Bacil-
lus thuringiensis: models for their mechanism of action A virus whose host is a bacterium
on the insect gut. Bioassays 15:469476
Maagt RA, Bravo A, Crickmore N (2001) How Bacillus thur-
ingiensis has evolved specific toxins to colonize the
insect world. Trends Genet 17:193199
Whiteley HR, Schnepf HE (1986) The molecular biology of Bacteriophage Wo
parasporal crystal body formation in Bacillus thuringi-
ensis. Annu Rev Microbiol 40:549576
jason m. meyer, marjorie a. hoy
University of Florida, Gainesville, FL, USA

Backswimmers Bacteriophages are obligate intracellular viruses

that infect and kill bacteria. These viruses are ubiq-
Members of the family Notonectidae (order uitous and shape aspects of bacterial population
Hemiptera). ecology in almost every environment on earth.
Bugs Bacteriophage WO infects the alpha-proteobacterium
 Bacteriophage Wo
B 351

Wolbachia, which is commonly associated with appears that both Wolbachia and bacteriophage
insects, mites, nematodes, and terrestrial isopods. WO are horizontally transmitted between different
Wolbachia is notorious for causing reproductive arthropod species by unknown mechanisms. This is
alterations in its hosts such as feminization, male supported by evolutionary studies showing incon-
killing, cytoplasmic incompatibility, and parthe- gruence between phylogenetic trees constructed
nogenesis. The diversity of Wolbachia strains and using DNA sequences from Wolbachia and bacterio-
their influence on host biology has stimulated phage WO. Interestingly, some insects host multiple
research encompassing broad topics including strains of Wolbachia that are infected with different
genetics, ecology and evolution. In addition, types of bacteriophage WO, and even individual
removing obligate Wolbachia infections from strains of Wolbachia can harbor multiple phage types.
filarial nematodes has provided a novel treatment Wolbachia has a broad and dynamic host range that
for human disease. The significance of both basic may be facilitated by the horizontal transfer of
and applied research involving Wolbachia has made virulence factors it acquires from bacteriophage WO.
it one of the most well understood endosymbiont- In 2000, the first bacteriophage WO was
host associations. completely sequenced using DNA isolated from
Virus-like particles (bacteriophage WO) were the Mediterranean flour moth Ephestia kuehniella
discovered inside Wolbachia cells in the reproduc- Zeller (Lepidoptera: Pyralidae) infected with
tive tract of the mosquito Culex pipiens using Wolbachia. A total of 33 open reading frames were
electron microscopy in 1978. Bacteriophage WO detected among a genome of approximately
particles are approximately 40 nm in diameter 25,000 base pairs of DNA. The open reading
with short tails, contain linear double-stranded frames represent the DNA coding information
DNA, and are found near the Wolbachia cell mem- that dictates the construction and assembly of
brane. Since its discovery, researchers have focused proteins. Some of the putative proteins identified
on characterizing the basic biology, distribution, were related to proteins known from a diverse
and evolution of bacteriophage WO. group of other bacteriophages, while others
Bacteriophage WO has both a lysogenic phase, showed no significant similarities to known phage
where its genetic information is integrated into proteins. Additional bacteriophage WO types
the Wolbachia chromosome as a prophage, and a have since been sequenced using DNA isolated
lytic phase, where the virion resides in the from Wolbachia infecting the almond moth,
cytoplasm and can lyse Wolbachia cells. Little is Cadra cautella Walker (Lepidoptera: Pyralidae),
currently known about what triggers the virus to and from Wolbachia infecting Drosophila mela-
kill Wolbachia. Bacteriophage WO may prevent nogaster Meigen (Diptera: Drosophilidae).
excessive proliferation of Wolbachia, and this may Using the polymerase chain reaction (PCR),
have evolutionary implications for long-term the putative minor capsid protein gene, orf7, is
maintenance of the association with the host. commonly used to detect bacteriophage WO in
Bacteriophage WO is transmitted transovarially Wolbachia strains infecting arthropods. More
inside arthropod eggs along with its host Wolbachia than 100 orf 7 sequences of bacteriophage WO
cells. This transmission mechanism provides an have been deposited in GenBank as of May 2007.
efficient and stable means for Wolbachia and its The orf 7 gene has been detected in many, but not
associated bacteriophage WO to infect arthropod all, Wolbachia-infected arthropods. Using species
populations at a high frequency. This notion is representing multiple orders of arthropod hosts,
substantiated by the similarity of the G+C content between 70 and 100% of the Wolbachia strains
and codon usage of phage and Wolbachia genes, tested are PCR-positive for bacteriophage WO.
indicating a long-term evolutionary tie between However, multiple Wolbachia-infected species
bacteriophage WO and Wolbachia. However, it also of parasitoids in the genus Trichogramma
352
B Baculoviridae

(Hymenoptera: Trichogrammatidae) and the Baculoviridae

parasitoid Diaphorencyrtus aligarhensis Shafee,
Alam and Agarwal (Hymenoptera: Encyrtidae) A family of insect pathogenic viruses known as
lack bacteriophage WO. In addition, the nema- baculoviruses.
todes Dirofilaria immitis, Litosomoides sigmodon- Baculoviruses
tis, Setaria equine and Brugia malayi, and a
population of the predatory mite Metaseiulus
occidentalis (Nesbitt) all had Wolbachia infec- Baculoviruses
tions but lacked bacteriophage WO, based on
PCR analysis of the orf7 gene. The insect baculoviruses, the nucleopolyhedrovi-
In vitro cultures of Wolbachia must be ruses (NPVs) and the granuloviruses (GVs), are
maintained using insect cell cultures because the most intensely studied insect viruses. Histori-
the endosymbiont is intracellular. Currently, no cally, the first reports of a baculovirus-induced
methods have been developed to transform viremia were associated with the silkworm
(genetically modify) Wolbachia that would Bombyx mori. The spread of sericulture from Asia
provide a tool to study its interactions with to Europe led to the introduction of the affiliated
arthropods in detail. Bacteriophage WO has the diseases grasserie or jaundice disease (NPV), as
potential to be developed as a vector to geneti- well as flacherie (non-occluded virus, bacteria),
cally modify Wolbachia because it integrates into the silk-producing regions. In the sixteenth
into the Wolbachia genome and its genes are century poem titled De bombyce, Marco Vida
actively expressed. describes the rupture of tissues and the release of
Sex Ratio Modification by Cytoplasmic Agents fluid from diseased silkworm larvae. It is presumed
Symbionts of Insects he is describing the last stages of B. mori NPV-
induced jaundice. In 1856, the Italian scientist
Maestri made the first scientific observation of
References the causal agent of jaundice. With the aid of the
compound microscope, he described the presence
Braquart-Varnier C, Grve P, Flix C, Martin G (2005)
of polyhedral bodies (Fig.3) or occlusions in the
Bacteriophage WO in Wolbachia infecting terrestrial
isopods. Biochem Biophys Res Commun 337:580585 fluid and tissues of diseased silkworm larvae
Fujii Y, Kubo T, Ishikawa H, Sasaki T (2004) Isolation and By the late 1890s, J. Bolle reported that the
characterization of the bacteriophage WO from Wolbachia, polyhedral bodies were proteinaceous crystals
an arthropod endosymbiont. Biochem Biophys Res
Commun 317:11831188
resistant to various solvents but sensitive to
Masui S, Kamoda S, Sasaki T, Ishikawa H (2000) Distribution alkaline solutions. Bolle reported that healthy
and evolution of bacteriophage WO in Wolbachia, the silkworms that fed on the polyhedral bodies con-
endosymbiont causing sexual alterations in arthropods. tracted jaundice. The intracellular inclusions
J Mol Evol 51:491497
Masui S, Kuroiwa H, Sasaki T, Inui M, Kuroiwa T, Ishikawa H described initially by Bolle as Microsporidium
(2001) Bacteriophage WO and virus-like particles in polydricum were named later by Prell as Crystal-
Wolbachia, an endosymbiont of arthropods. Biochem loplasma polyhedricum. Glaser and Chapman, who
Biophys Res Commun 283:1099-1104
in 1916 reported that the infectious agent was a
Gavotte L, Henri H, Stouthamer R, Charif D, Charlat S,
Boultreau M, Vavre F (2007) A survey of the bacterio- filterable agent of dimensions much smaller
phage WO in the endosymbiotic bacteria Wolbachia. than the micron-sized polyhedral bodies, ques-
Mol Biol Evol 24:427435 tioned the infectious nature of the polyhedral bodies.
Hoy MA, Jeyaprakash A (2005) Microbial diversity in the preda
tory mite Metaseiulus occidentalis (Acari: Phytoseiidae)
They and others proposed that the polyhedral
and its prey, Tetranychus urticae (Acari: Tetranychidae). bodies were metabolic by-products and not causal
Biol Control 32:427441 agents of the disease. The nature of the polyhedral
 Baculoviruses
B 353

Baculoviruses, Figure 3 Scanning electron micrograph of occlusion bodies of the nucleopolyhedrovirus

depicting their three dimensional shape.

bodies and capsules finally was resolved in the similar disease in the larvae of the variegated cut-
1940s by the German scientist G. Bergold. He and worm, Peridroma margaritosa, the first report of
co-workers examined alkali-treated baculovirus this disease outside of France. To date, granulosis
inclusions under the newly developed electron viruses have been found to infect only lepidopteran
microscope and described the occluded, rod-shaped hosts. These viruses are considered to be among
virus particles. the most specific insect viruses, capable of infecting
In the late 1930s, the French scientist A. Paillot a single species or species within the same genus
described a new type of viral disease in the Prior to their identification, baculoviruses
cabbage butterfly, Pieris brassicae, that, unlike the were recognized as important natural regulators
NPVs, produced numerous minute capsules of various lepidopteran defoliators. At the end of
(granules). Using high-speed centrifugation, Paillot the nineteenth century in central Europe, nun
and co-workers determined that the infectious moth (Lymantria monacha) populations were
entities were associated with the granules in the decimated periodically by a wilt disease. Prior
high-speed pellets. Paillot observed that this viral to death, infected insects migrated to the tops
disease, termed pseudo-grasserie, multiplied in (Wipfeln) of the trees, attached by their prolegs,
the fat body and caused infected larvae to exhibit and died. Upon death, the body disintegrated and
a whitish coloration. In the early 1930s, he released infectious fluid. Initially, the causal agent
described a similar disease in the cutworm Euxoa of the disease, known as Wipfelkrankheit, was
segetum that caused nuclear hypertrophy of described as a bacterium, then later as a protozoan
infected fat body cells followed by the formation within the genus Crystalloplasma. Although it was
of the granules. In 1947, Steinhaus discovered a not properly named, a great deal was learned from
354
B Baculoviruses

these early studies of this disease agent. Experi- of a baculovirus. In Canada, the European pine
ments showed that the infectious material resisted sawfly, Neodiprion sertifer, was introduced and
putrification and was stable for 3 years when stored became established as a major forest defoliator.
in a dry state. Furthermore, the disease agent In the early 1950s, T. Bird (Canadian Forest Ser-
persisted in the soil and could be extracted from vice) reported that a sawfly virus imported from
washings using differential centrifugation. This Sweden was highly virulent to N. sertifer larvae.
agent was transmitted per os; the fluid released The introduction of this virus resulted in wide-
from the cadavers was highly infectious to healthy spread epizootics that spread through the sawfly
larvae. Finally, it was reported that the infectious population and provided a natural control of
agent displayed specificity to certain insect species. this defoliator. This virus, unlike the lepidopteran
For example, the fluid released from diseased nun baculoviruses, was transmitted easily from
moth larvae was infectious to the related gypsy infected adults to the egg stage. The combination
moth, Lymantria dispar, but was harmless to of its high virulence and ability to be vertically
silkworm larvae. Throughout the 1920s, a program transmitted were responsible for its ability to
in Europe promoted the spread and distribution provide effective long-term control of this pest
of the causal agent into disease-free areas. This insect. The natural occurrence of baculovirus
involved a variety of tactics, including the use of epizootics and their potential to be manipulated
mortars to deliver infectious material into the tree as biological control agents against key pest
canopy. The field studies on the nun moth NPV insect defoliators served as the catalysts for bac-
suggested that this disease operated as a density- ulovirus research during the past 30 years. Dur-
dependent disease agent ing this period more than 4,000 research papers
In the United States, a similar scenario was have been published on baculoviruses, of which
observed in populations of the gypsy moth, an more than 3,000 have focused on the nucleopo-
imported defoliator of deciduous hardwoods. This lyhedrovirus group. In the 1970s and early 1980s,
insect, originally imported as an alternative silk the major focus was studying the effects of wild-
producer, escaped into the oak forests and spread type baculovirus strains on insect population.
throughout southern New England. In the early From the mid-1980s to the present, the emphasis
1900s, collapses of gypsy moth populations were has been directed at the biochemistry and molec-
attributed to the natural occurrence of wilt or ular biology of these viruses. This work, in addi-
flacherie disease. At this time, Glaser and Chapman tion to providing detailed insight into the
initiated a series of key studies on this disease. workings of this complex virus, has provided the
Microscopic examination revealed that this virus scientific community with a highly efficient
replicated initially in the tracheae then spread to eukaryotic expression vector system that is being
virtually all the insect tissues. Infected cells were used commercially to produce various protein
recognized by the large number (Fig. 4) of intra- products. Lastly, the basic research has provided
nuclear occlusion bodies. In 1913, Glaser and a means to engineer the baculovirus, which in
Chapman reported that the filterable agent, the future years may provide highly efficacious
causal agent of gypsy moth wilt disease, was recombinant strains for managing insect pest
sensitive to sunlight and to heat treatment. In 1916, populations (Table 2).
it was determined that the occlusions could be Nucleopolyhedroviruses are horizontally
disrupted readily when placed in alkaline solu- transmitted to susceptible insects per os; larvae
tions and could be re-formed by neutralization of become infected by ingesting foliage contami-
the alkaline solution. nated with occlusions. In limited cases, chroni-
One of the classic examples of biological cally infected adults may disseminate baculovirus
control of insects has involved the introduction onto the chorion surface during oviposition,
 Baculoviruses
B 355

Baculoviruses, Figure 4 Transmission electron micrograph of a thin section of the multiply embedded
nucleopolyhedrovirus, not the crystalline protein matrix within which are embedded membrane bound
rod shaped virus particles. Ingestion of these occlusions by host insects results in the digestion of the
matrix protein and release of occluded virus.

resulting in a vertical transfer of the pathogen to role in both the initiation and maintenance of
progeny caterpillars. Not all baculoviruses cause natural virus epizootics. During the epizootic
lethal infections; latent infections can persistently phase the primary route of baculovirus transmis-
infect insect colonies in which the virus is trans- sion is per os. Ingested viral occlusions are dis-
mitted within the egg stage. At present, very little rupted by the action of alkaline proteases in the
is known about the frequency and impact of such midgut lumen. The types and amounts of gut
persistent baculovirus infections on natural proteases produced by an insect influence the
insect populations. The initiation of baculovirus processing of ingested occlusions. Increased
epizootics has been attributed mainly to insects feeding rates, as displayed by mature larvae, may
contacting and ingesting overwintering virus result in the rapid passage of ingested food con-
inocula that are associated with plant and/or soil taining intact or only partially digested occlu-
substrates. It is likely that latent infections play a sions, thereby preventing contact with the midgut
356
B Baculoviruses

Baculoviruses, Table 2 Examples of baculoviruses production of a well-defined peritrophic mem-

isolated from different insect hosts brane. The ODVs do not orientate to the
Baculovirus Host microvilli in any particular fashion, suggesting
Nucleopolyhedrovirus that the anti- receptors, if present, are distrib-
uted throughout the ODV envelope. The viral
AcNPV Lepidoptera: Autographa
californica membrane fuses to the microvillar membrane
and the nucleocapsids are released into the cyto-
AgMNPV Lepidoptera: Anticarsia
gemmatalis plasm. Nucleocapsids are transported to the
LdMNPV Lepidoptera: Lymantria
nucleus and attach to the nuclear pores of the
dispar columnar epithelial cells. In addition to directly
SeMNPV Lepidoptera: Spodoptera infecting the columnar cells, investigators have
exigua reported that parental nucleocapsids can tra-
CfMNPV Lepidoptera: verse the columnar cells and infect underlying
Choristonuera fumiferana regenerative cells. Viral development in the
TnSNPV Lepidoptera: columnar epithelial cells may be aborted by the
Trichoplusia ni preferential sloughing off of infected cells and by
BmSNPV Lepidoptera: Bombyx the removal of the midgut layer at larval molt.
mori Therefore, the ability of a baculovirus to infect
TpSNPV Diptera: Tipula paludosa the regenerative cells may play a key role in
CnSNPV Diptera: Culex nigripalpus maintaining a systemic infection.
The naming of the different viruses includes
NsSNPV Hymenoptera:
Neodiprion sertifer the initial letter of the host species followed by
Granulovirus
mnv (multiply embedded nucleopolyhedrovirus),
Snpv (singly embedded nucleopolyhedrovirus) or
TnGV Lepidoptera: Gv (granulovirus).
Trichoplusia ni In the midgut cells, viral particles either
PiGV Lepidoptera: Plodia attach to the nuclear pore and uncoat, or enter
interpunctella the nucleus and uncoat. The release of the viral
CpGV Lepidoptera: Cydia genome into the nuclear region marks the initia-
pomonella tion of the primary replication phase. In various
lepidopteran hosts the majority of baculoviruses
produce only the non-occluded virus; occlusions
tissue. Alternatively, the ingestion of plant mate- are not normally synthesized in either virus-
rial that either buffers gut alkaline conditions or infected columnar or regenerative cells. Unlike
contains endogenous protease inhibitors or anti- other enteric viruses (e.g., Cypoviruses), the
viral allelochemicals may reduce the susceptibil- virus released from the infected columnar cells
ity of an insect to baculovirus infection. do not horizontally spread to adjacent midgut
The released occlusion derived virus (ODVs) cells but can infect adjacent tracheal cells or
must bypass the peritrophic membrane in order migrate to the basal face of the midgut. However,
to access the initial target midgut cells. The the basement membrane, comprised of exocel-
peritrophic membrane is a dynamic structure lular matrix proteins, surrounds the basal face of
that varies among different species and between the midgut and is believed to act as a barrier to
the different developmental stages. As insects prevent the large-scale release of baculoviruses
mature they often display a developmental resis- into the hemocoel. The virus that has penetrated
tance to infection that is related in part to the the tracheal cells can undergo a complete
 Baculoviruses
B 357

r eplication cycle and may then infect neighbor- massive numbers of the ODV phenotype and
ing tracheal cells. Utilizing the host tracheal sys- associated occlusion bodies. The very late stage
tem as a conduit, the virus can access and infect of NPV development is characterized by the
other susceptible insect tissues. In addition to presence of hypertrophied, infected nuclei
being disseminated via the tracheal conduit, becoming filled with highly refractile occlu-
NPV-infected hemocytes also can spread the sions. Virtually all host tissues become infected
virus to healthy tissues and larvae are extremely fragile. Frequently,
During baculovirus replication, various NPV infected larvae will disintegrate into a
viral proteins are produced which modulate the puddle of occlusion bodies. This wilting symp-
host at the cellular as well as organism level. tom is believed to result in part from the
Baculoviruses may contain genes that code for production of virally encoded hydrolases hav-
proteins with anti-apoptotic activities that block ing either proteolytic or chitinolytic activities.
the internal cell suicide program. Premature cell The production of this enzyme, detected in cul-
death would abort the production of viral prog- ture supernates at 12 h post-infection, is under
eny particles. Baculovirus replication also has the regulation of a late gene promoter. This
been observed to disrupt the developmental enzyme, stable between pH 3 and 10, is believed
program of host insects. For many years it has to be partially responsible for the liquefication
been known that baculovirus infection retards of baculovirus-infected insects. The disintegra-
larval development and prevents the larval-to- tion of infected insects also is aided by the pro-
pupal molt. In the late 1980s baculoviruses were duction of various viral proteases. A variety of
found to contain a gene (egt) which codes for a viral, host, and environmental factors determine
ecdysteroid UDP-glucosyl transferase (egt). The the rate and level of occlusion formation in a
egt gene encodes for a 57 kDa polypeptide with baculovirus-infected insect. Regardless, the bio-
506 aa. The egt holoenzyme, an oligomer of 35 magnification of baculoviruses in their respec-
subunits, catalyzes the transfer of glucose or tive lepidopteran hosts is phenomenal. Neonate
galactose from UDP-glucose or UDP-galactose, larvae may be infected by ingesting as few as
respectively, to ecdysteroids producing inactive 110 occlusions, succumb to viremia within
sugar conjugates of this steroidal hormone. 412 days, and then release 107 occlusions into
Expression of the egt gene inhibits the molting the environment.
process and maintains the host in the larval
stage. This gene is non-essential, deletion
mutants retain their ability to infect and to rep-
licate both in cell culture and in host insects. References
However, egt expression alters host ecdysone
titers, results in a massive reprogramming of Clem RJ, Fechheimer M, Miller LK (1991) Prevention of
apoptosis by a baculovirus gene during infection on
host tissues, and disrupts larval molting and insect cells. Science 254:13881390
pupation. The prolongation of the larval stage Granados RR, Federici BA (eds) (1986) Biology of the bacu-
results in increased viral yields. Alternatively, loviruses. CRC Press, Boca Raton, Florida
the disruption of pupation due to viral infection Maramorosch K, Sherman KE (1985) Viral insecticides for
biological control. Academic Press, Orlando, FL, 809 pp
reduces the likelihood of viral-infected adult Miller LK (1996) Insect Viruses. In: Fields BN, Knipe DM,
insects. Since the initial report in AcMNPV, Howley PM (eds) Fundamentals of virology. Lippincott-
homologous genes have been detected in vari- Raven Publishers, Philadelphia, PA, pp 401424
Miller LK (1984) Exploring the gene organization of baculo-
ous NPVs.
viruses. Methods Virol 7:227258
In non-midgut tissues, NPVs, in addition to Rohrmann GF (1992) Baculovirus structural proteins. J Gen
producing the baculovirus phenotype, produce Virol 73:749761
358
B Baetidae

Baetidae families in the past). The family is part of the

superfamily Tineoidea, in the section Tineina,
A family of mayflies (order Ephemeroptera). subsection Tineina, of the division Ditrysia. Adults
Mayflies minute to medium size (460 mm wingspan), with
very rough head scaling; haustellum vestigial and
naked; labial palpi reduced, 1 to 2-segmented but
fused together (rarely 3-segmented); maxillary
Baetiscidae palpi; antennae usually bipectinate. Maculation
mostly dull colored, but sometimes with clear
A family of mayflies (order Ephemeroptera).
wings or translucent wing spots; some are spotted;
Mayflies
rarely colorful. Adults are mostly diurnal or
crepuscular. Larvae are mostly leaf feeders or feed
on lichens, all making distinctive types of larval
Bagworm Moths (Lepidoptera: cases, or bags. Pupation is within the larval case
Psychidae) and females often remain there in a wingless or
larviform shape, using pheromones to attract the
john b. heppner winged males. A number of species are economic
Florida State Collection of Arthropods, and many are general plant feeders.
Gainesville, FL, USA

Bagworm moths, family Psychidae, total 1,001

known species, mostly Palearctic and African, with
References
only 88 known for the New World; actual fauna
Betrem JG (1952) The genotypes of the Indo-Australian
likely (Fig.5) exceeds 1,200 species. The family is Psychidae (Lepidoptera). Tijdschrift voor Entomol
now divided into six subfamilies, although vari- 95:331340
ous tribes are sometimes elevated as additional Dalla Torre KW, von Strand E (1929) Psychidae In: Bryk F
subfamilies: Lypusinae, Naryciinae, Taleporiinae, (ed) Lepidopterorum catalogus, vol 34. W. Junk, Berlin,
211 pp
Penestoglossinae, Psychinae, and Oiketicinae (most Davis DR (1964) Bagworm moths of the Western Hemisphere
of the subfamilies have also been treated as separate (Lepidoptera: Psychidae). Bull US Natl Mus 244:1233
Httenschwiler P (1997) Psychidae Sachtrger. In: Schmet-
terlinge und ihre Lebensrume: Arten Gefhrdung
Schutz. Schweiz und angrenzenden Gebiete, 2:165308,
pp 47.Pro Natura-Schweizerische Bund fuer Naturschutz.,
Basel
Kozhanchikov IV (1956) Nasekomye Chechuekrulye. Chechlo
nosye Meschechnitsky (sem. Psychidae). In Fauna USSR.
Insects. Lepidoptera 3(3):1516. Moscow [Engl transl: 1969.
525 pp, Smithsonian Institution, Washington]

Bait
A food or food-like substance that is used to attract
Bagworm Moths (Lepidoptera: Psychidae), pests. It often is combined with an insecticide to
Figure 5 Example of bagworm moths (Psychidae), poison insects, slugs, snails and rodents.
Eumeta pryeri (Leech) from Taiwan. Food-Based Baits
 Banana Pests and Their Management
B 359

Balanced Mortality Hypothesis so when viewed on a larger scale. Clearly, eco-

logical stability is scale-dependent, and broad-
The belief that the level of reproduction is scaled scale stability (metastability) usually exists only
to the probability of survival, with insects living in at the meta-scale.
hostile environments having higher levels of
reproduction than those occurring in more benign
environments References

Egerton FN (1973) Changing concepts of the balance of

Balance of Nature nature. Q Rev Biol 48:322350
Wu J, Loucks OL (1995) From balance of nature to hierarchi-
cal patch dynamics: a paradigm shift in ecology. Q Rev
This is the idea that in nature there exists an inher- Biol 70:439466
ent equilibrium founded on the interactions of
plants and animals, resulting in a stable, continuing
system of life on Earth. This belief is fundamental
to many cultures, though Carl Linnaeus is often Banana Pests and Their
credited with popularizing it (oeconomia Management
naturae) in his writings of 1749. Sometimes this
natural order was attributed to divine providence, william tinzaara,1 clifford s. gold2
but at other times maintained by nature. Once a 1
Bioversity International-Uganda, Kampala
popular notion, it no longer is popular with Uganda
ecologists. 2
CIAT-Uganda, Kampala Uganda
Some elements of balance exist, such as the
adaptations of different elements in a natural Bananas are among the most important food crops
ecosystem such that resource production and use in the world. Despite their importance, banana
are commonly balanced and optimized. However, yields are continuously declining due to attack by
the so-called balance is continually upset by insect pests. Insects attack the banana rhizome,
natural events and by the activities of humans. pseudostem, leaf and fruit. The most serious insect
Outbreaks of insects are an example of the dis- pest on a global basis is the banana weevil. Other
equilibrium that calls into question the notion of pests include the sugarcane weevil, pseudostem
balance. However, the resistance of systems to weevil, banana scab moths, banana skipper, banana
perturbation, the resiliency (rapidity of return to thrips and banana aphids. Pests of minor or local-
equilibrium after perturbation) of both producer ized importance include the spiraling whitefly,
and consumer organisms, and the persistence mealybugs, big-headed ant, chinese rose beetle
(tendency of organisms to persist even when and coconut scale. Thrips cause cosmetic damage
faced with catastrophic changes in abundance), directly to the fruit, reducing marketability. Most
can be construed as supportive of the balance pests do not attack the bunch and cause indirect
hypothesis, or at least supportive of the idea of damage. For example, banana weevils attack the
continuance or constancy. rhizome and pseudostem causing yield reductions
Much of the disagreement about the bal- through plant loss, delayed maturation and bunch
ance of nature is due to differences in scale. weight reduction. Some pests, such as Pentalonia
Ecosystems are mosaics of patches, and envi- nigronervosa, are vectors of serious diseases. In
ronmental stochasticities or biological feed- this article, the pest status, distribution, biology
backs that appear to be destabilizing or and control options of major pests of banana are
catastrophic on a local scale may be much less discussed.
360
B Banana Pests and Their Management

Banana Weevil, Cosmopolites morphological features and all show extreme

sordidus (Germar) (Coleoptera: variation in color. The adults are 914 mm long
Curculionidae) black adults with red or yellow markings. The base
of the elytra is one-half to one-third red or yellow
The banana weevil is the most important insect on a black background. The pronotum and venter
pest of banana and plantain. Its host range is are black to red and black. This species can be
restricted to wild and cultivated clones of Musa confused with Metamasius calligsona which
(banana, plantain, abaca) and Ensete. The insect infests bromeliads. M. hemipterus adults are active
originated in southeast Asia and has spread to all fliers (unlike C. sordidus).
important banana and plantain growing areas. It is
not normally a pest in its area of origin.
Because of its importance, detailed treatment of Biology
this insect is provided elsewhere in the Encyclopedia.
Banana Weevil, Cosmopolites sordidus The three subspecies of M. hemipterus have simi-
lar biology. The adults are most often found in
moist, dark places. They are attracted to, and ovi-
Sugarcane Weevil, Metamasius posit in, healthy banana pseudostems, rotting
hemipterus sericeus (Coleoptera: banana plants, banana residues, damaged or
Curculionidae) stressed sugarcane stalks, ripe fruit (i.e., pineapple,
mango, papaya), or palm sheaths or stems. More
The sugarcane weevil Metamasius hemipterus is known about the oviposition habits of
sericeus (Olivier) (Coleoptera: Curculionidae: Dry- M. hemipterus on sugarcane than on banana. The
ophthorinae) primarily infests banana, plantain, weevil is attracted to stalks damaged by either
sugarcane and, less commonly, ornamental palms. mechanical cultivation, harvesting equipment,
The insect is endemic to the America tropics. It has rats, borers, disease or natural growth cracks. In
been found on plantain in West Africa but has not some cases, Metamasius females prefer to deposit
been reported from East Africa. eggs on sugarcane that has been damaged by Dia-
The importance of M. hemipterus as a pest of traea (Lepidoptera: Pyralidae). In Colombia, this
banana is disputed but it is considered more seri- type of damage is known as the Diatraea-Meta-
ous than the banana weevil, Cosmopolites sordidus, masius complex. Metamasius hemipterus has also
in the banana growing areas of western Colombia. been observed infesting canes used as seed pieces.
In this region, M. hemipterus is known to transmit The females lay their eggs in cracks and
Erwinia chrysanthemi pv paradisiaca causing rot- damaged areas of bananas and sugarcane, or in
ting of the banana pseudostem. Some authors petioles and crown shafts of certain species of
argue that M. hemipterus is unimportant or only a healthy palms. The adult can live up to 60 days
secondary pest of banana. during which time the female can deposit 400
There are three recognized subspecies, all of 500 eggs. This contrasts with the biology of
which attack banana: M. h. hemipterus (L.) is dis- C. sordidus, which is longer lived but produces
tributed from Puerto Rico through the Lesser far fewer eggs. As with C. sordidus, M. hemipterus
Antilles and into most of South America; M. h. places single eggs in holes made in the host by
sericeus (Olivier) is found in the Greater Antilles, the insects rostrum.
southern Florida (USA) and from Nicaragua to The oval egg is 1.21.5 mm in length and
Ecuador; while M. h. carbonarius (Chevrolat) creamy-white. The egg stage is 37 days. The cream-
occurs from Mexico to El Salvador and Hondu- color, yellowish larvae are typical legless weevil
ras. The three subspecies have similar external grubs and similar in most aspects to other members
 Banana Pests and Their Management
B 361

of the Rhynchophorinae. Fully developed larvae are Trapping and Monitoring

1.32.0 cm. The larval stage lasts 5060 days.
Metamasius hemipterus larvae can be differ- Trapping of adults is often used to monitor weevil
entiated from those of Cosmopolites by color numbers, although interpretation of trap captures
(creamier coloration), behavior (more active), is difficult. The use of a sandwich trap using
and morphological features (stigmata, cranial banana pseudostem as an attractant has been sug-
sutures, and structures on the labium and gested. A maximum of ten weevils per trap per
clypeum). Mature M. hemipterus larvae construct week have been captured using banana pseu-
a fibrous pupal case (similar to that of the giant dostem disc traps, although the number of weevils
palm weevil, Rhynchophorus palmarum) and collected at these traps was consistently too low to
pupation takes place mostly within the banana accurately assess weevil density. Fermenting sug-
pseudostem. The pupal stage is 1020 days. Thus, arcane has also been used to attract M. hemipterus.
depending on temperature, the life cycle is com- An average of 30 weevils per trap using pieces of
pleted in 6386 days. bamboo filled with pieces of fermenting cane have
been captured. Tests conducted on different trap
designs and the response of adults to semiochemi-
Pest Status cals demonstrated that weevil counts increased
with combinations of ethyl acetate, sugarcane and/
Damage in banana is caused by the larvae, which or the aggregation pheromone metalure, com-
feed in the upper part of the pseudostem. The lar- pared with the use of any compound alone. The
vae bore into the stem causing extensive physical major male-produced aggregation pheromones
damage and, in heavy infestations, can kill the and host kairomone compounds have identified
plant. The first symptoms of M. hemipterus attack the trap designs and protocols that can be used for
are yellowing of the lower leaves and consequent enhanced monitoring of weevil populations in the
rotting of the pseudostem. In cases of extensive field. In addition, it has been demonstrated that
damage to the pseudostem, the plants cannot resist pheromone and host-baited traps can be used to
the weight of fruit, increasing the likelihood that mass trap M. hemipterus infesting banana and
the plants may double and eventually die. The pest sugarcane in Costa Rica.
has also been reported to attack the banana rhizome Control Measures
and cause damage similar to that of C. sordidus.
Moreover, there are reports that M. hemipterus did
not show any preferences between rhizome and Chemical Control
pseudostem tissue of the cultivars Gross Michel
(AAA) and Bout Rond. Unfortunately, there are no Labeled rates of acephate, carbofuran, chlorpyri-
yield loss data for M. hemipterus in banana. fos, cyfluthrin, disulfoton, imidachloprid, isofen-
Larvae of M. hemipterus can seriously affect phos, lindane and vydate have been demonstrated
the ornamental palms Phoenix canariensis, Pty- to kill adults of M. hemiperus. The data suggest
chosperma macarthurii, Ravenia rivularis, and that poisoned sugarcane traps may be adequate for
Roystonia. Larval tunneling in palms starts in the control of M. hemipterus, although inadequate
petioles, wounds in petioles, crown, stem and then control with chemical insecticides has also been
extends into healthy leaf or stem tissue. Affected reported. Moreover, chemically based pest con-
palms are often characterized by the production of trols represent short term and questionable strate-
an amber-colored, gummy exudate in the stem, gies for resource-poor farmers in developing
crown shaft or petioles, and galleries in the leaves, countries, along with accompanying health and
petioles and stems. environmental concerns.
362
B Banana Pests and Their Management

Cultural Control M. hemipterus larvae, but not adults. However, the

authors concluded that chemical insecticides and
Sanitation of residues harboring the weevil has entomopathogenic nematodes would need to be
been recommended. This procedure is done by applied frequently and over a long period of time
cutting up pseudostems and allowing them to dry for effective management because of the weevils
up. No data are available on efficacy. high reproductive potential and the cryptic habitat
of the immature stages.

Biological Control
Natural Enemies
Both entomopathogens and naturally occurring
biological control agents affect sugarcane weevil. Reported predators of M. hemipterus include labi-
durids, histerids, staphylinids, carabids, cicindelids,
formicids and reduviids. Little is known on the con-
Entomopathogens trol potential of predators. In Florida, Colombia and
Ecuador, surveys for predators and parasitoids of
The use of entomopathogens provides a promising, M. hemipterus sericeus have been unsuccessful.
yet still expensive means of control of M. h. sericeus. There are reports that trials with the tachinid
The entomogenous fungi Beauveria bassiana Microseromasia sphenophori failed. However, the
(Balsamo) Vuillemin and Metarhizium anisopliae tachinid Admontia spp, observed parasitizing
(Metchnikoff) Sorokin have gained considerable Metamasius quadrilineatus in Honduras, could be
attention as potential control for weevils. For example, tested as a possible parasitoid of M. hemipterus.
studies have demonstrated that naturally occurring Thus, to date, very little research has been done on
B. bassiana was an important mortality factor to parasitoids of M. hemipterus in the neotropics, so it
adults of M. hemipterus in Florida. Beauveria is unclear whether or not effective biological control
bassiana infection increased up to 70% between will be possible.
March and April 1991 when more than ten weevils
were captured per trap. In Brazil, B. bassiana and
M. anisopliae caused high death rates of adults Banana Pseudostem Weevil,
applied under laboratory conditions. Odoiporous longicollis (Coleoptera:
Applying fungal formulations to traps made Curculionidae)
from banana pseudostems was considered the
most effective delivery system, while applica- The banana pseudostem weevil, Odoiporous
tions outside traps were deemed impractical. It longicollis (Olivier) (Coleoptera: Curculionidae) is

was observed that M. hemipterus adults were considered a minor to important pest of banana and
more susceptible to infection by both fungi than Manila hemp in parts of India, Nepal, Burma, Sri
C. sordidus adults. In Cuba, a strain of B. bassi- Lanka, Thailand, Indonesia, China and elsewhere in
ana from the sweet potato weevil, Cylas formi- Asia. The weevil bears a superficial resemblance to
carius elegantulus, which is reported to be highly the banana weevil, Cosmopolites sordidus (Germar),
pathogenic to M. hemipterus and C. sordidus was but is slightly larger and its elytra do not completely
isolated. More information is needed on the cover the abdomen. The color of the adult weevil
effect of these fungi before pest management varies with age from reddish-brown to black. Sexing
decisions can be made. of adults is based on punctuation of the rostrum.
The nematode Steinernema carpocapsae Males also tend to be smaller than females. The sex
has been demonstrated to be effective against ratio ranges from as 1:1.2 (male:female) to 1:1.5.
 Banana Pests and Their Management
B 363

Biology The larvae attack the pseudostem and stem of

banana plants, although they will occasionally feed
The weevil is characterized by long life span, within the rhizome. This contrasts with the banana
negative phototropism, thigmotropism, gregari- weevil, which attacks the rhizome and uncom-
ousness, hydrotropism and death mimicry. Most monly enters the pseudostem. As such, pseudostem
adults live 610 months, although some can borer damage may be clearly visible, while banana
survive for more than 2 years. In contrast to the weevil damage can only be observed by dissection
banana weevil, the adult readily flies, although it of the rhizome. The pseudostem borer will attack
has been described as a poor flyer. Still, it has suf- both living plants and harvested stumps.
ficient capability to move between proximal Larval damage can lead to the rotting of
banana stands. In spite of being negatively photo- pseudostem tissues and breakage in the wind.
trophic, diurnal flight occurs. Breakage of damaged plants is potentially a serious
Oviposition is in the leaf sheaths of living plants problem, although such losses are rarely quantified.
or residues. The weevils are especially attracted to, Thus although the weevil has been described as an
and readily oviposit in, cuts in banana material. important pest, there are no available data on plant
Some authors have suggested that ovipositing loss and/or yield reductions. Further work in this
females prefer stressed plants, while others observed area is required for the development of any integrated
greater oviposition in residues than in living pest management program.
plants. The greatest oviposition has been found in
pseudostems with a girth of 2550 cm, with little
oviposition in plants less than 25 cm or more than Control Measures
75 cm in girth. The eggs are placed singly in cham-
bers made with the females rostrum. The egg stage Cultural Control
has been reported as 34 days and 512 days.
The larvae pass through four instars. The first There is limited information available on control
instar remains near eclosion sites in the same leaf of banana pseudostem weevil. Selecting new and
sheath. Subsequent instars bore into the inner leaf clean sites, use of clean planting material, crop
sheaths or pseudostem. The mature larvae may be sanitation (e.g., burying infested residues), rogue-
twice the size of those of banana weevil. The larval ing of infested plants, crop rotation (to rid fields of
stage has been reported by several authors to be weevils), and trapping by placement of residue
14 days, 36 weeks and 2668 days. slices on the ground has been recommended.
The prepupa forms a pupal chamber within Because the weevil flies and its dispersal capacity
the host plant. Pupation is within a cocoon formed has not been determined, it is unclear how effec-
out of plant fibers. The prepupal stage lasts 39 days, tive the use of these cultural methods might be.
while the pupal period has been reported as 320 One scientist reportedly collected more than 2
days. Following emergence, the adults may pass million weevils in traps over a 4-month period,
extended periods and even mate within the host but did not provide information on the effect of
plant. The pre-oviposition period lasts 1 month. this trapping program on weevil populations.

Pest Status Chemical Control

The adult weevils feed on living and decomposing Swabbing of the pseudostem and weevil holes with
banana leaf tissues, but eat little and are not con- insecticides has also been recommended. No data
sidered pests. Damage is done by the larval stage. are available on efficacy.
364
B Banana Pests and Their Management

Host Plant Resistance Pest Status

Host plant resistance has been suggested to be Banana scab moth females lay eggs on the outside
effective in reducing weevil infestations. In India, one of the banana flower bracts or on nearby leaves as
variety was found to be completely free of the weevil, the flower first emerges. Upon hatching, the larvae
while two others appeared resistant. In screened enter the flower and feed on the developing fruits
banana germplasm studies, six varieties were found within. Feeding results in irregular dark brown to
to be severely infested, three heavily infested, four black corky blotches on the fruit skin. Light dam-
moderately infested, and 27 lightly infested. age may be superficial and confined to the upper
end and outer side of the curved fingers. Heavier
infestations can scar the entire fruit, cause deformed
Banana Scab Moth, Nacoleia fingers, or penetrate into the flesh of the fruit.
octasema (Lepidoptera: Pyralidae)

Banana scab moth, Nacoleia octasema (Meyrick) Control Measures

(Lepidoptera: Pyralidae), is a serious pest of bananas
in the Samoan Islands and elsewhere in the south- Uses of biological control, resistant varieties, or
western Pacific. The pest also attacks Heliconia cultural controls have not proven effective for
spp. and Pandanus spp. Other moths that attack managing banana scab moth.
banana but are considered of minor importance
include Opogona sacchari and Othreis fullonia.
Chemical Control

Biology Chemical control works well when used properly.

Because the larvae begin damaging the developing
Banana scab moth females lay eggs on banana fruits when they are still enclosed inside the flower,
flower bracts or leaves as the inflorescence emerges. the best control can be achieved by injecting an
Larvae hatch, enter the flower, and feed on the insecticide into the flower after it first becomes
developing fruits within. The feeding results in visible, but before it starts bending over from the
rough and irregular scars (brownish-black) on vertical position. A single injection at this stage,
fruit skin. Large infestations can scar the entire applied about 1/3 of the way down from the flower
fruit and cause deformed fingers. tip, will percolate down to protect all the hands
Eggs are laid singly or in small, flattened, almost inside. This protection will last until the bracts
transparent clusters of a few to over 20 eggs. The eggs begin to fall away and no more egg laying occurs.
hatch in 34 days and the larvae enter the banana Some growers prefer to lift or remove the
lower, where they feed. The larval period is 1119 flower bracts and dust or spray insecticide onto the
days. Pupation is inside a loose silken cocoon, often fruits after the flower has bent over. This method
placed between banana fingers, in folds of the dead can stop some of the damage, but not all of it,
leaves still attached to the pseudostem, or in litter because by this stage feeding has already begun.
near the base of the plant. Adult moths emerge in Flowering is more or less continuous in banana
810 days and are short-lived, dying after about 310 plantations in American Samoa, and the stage at
days. Females lay approximately 80120 eggs during which insecticide must be applied lasts only a few
their lifetime. The moths are rarely seen, because they days for each plant. Therefore, it is important to
hide among dead leaves and vegetation during the check the plantation frequently to ensure that all
day and are active only during the early night. emerging inflorescences are treated.
 Banana Pests and Their Management
B 365

Biological Control are more common after a drought and in wind

protected areas.
Several kinds of natural enemies attack the banana The banana skipper is a large brown Hesperiid
scab moth, but in general they do not provide with large yellow spots on the forewings above.
sufficient control to reduce damage to acceptable Adults are less often seen although the caterpillars
levels. Spiders and ants may prey on the immature can be quite common on the host plants. This may
stages of banana scab moth. Parasitic wasps may be due to the fact that the butterfly is only active
also help reduce banana scab moth numbers. In during the early morning hours and just before
the Samoan Islands, the most common parasitoid dusk. It is sometimes attracted to the lights of
is Chelonus sp. (Hymenoptera: Braconidae), which dwellings and flies towards the lights in the
lays its egg inside the egg of the scab moth. The evenings.
Chelonus larva then develops inside the scab moth The caterpillars can be found where the banana
egg and larva. It finally emerges from the nearly plants (Musa spp.) are cultivated. Occasionally, an
full grown scab moth larva to spin a cocoon nearby infestation is severe enough for the species to be
in which it pupates. considered one of the banana farmers pests. The
characteristic rolled up portions of the banana
leaves are a dead giveaway to the presence of the
Host Plant Resistance caterpillars. Pupation takes place in a rolled up leaf
as well, and the adult butterfly emerges after about
Some banana varieties appear to be less suscep- 7 days. The caterpillar swings from side to side
tible to scab moth damage. Left untreated, these when disturbed, and exudes a greenish fluid. The
varieties may produce a satisfactory product for pupa also wriggles violently when disturbed.
markets that can tolerate some damage.

Biology
The Banana Skipper, Erionota thrax
(Lepidoptera: Hesperiidae) The adult butterfly lays bright yellow eggs singly or
in groups of up to 25. Oviposition is mostly on the
The banana skipper, Erionota thrax (Linnaeus) lower leaf lamina midway between the midrib and
(Lepidoptera: Hesperiidae) is a minor to severe the outer edge. Eggs turn bright red and the pale
pest of bananas and Musa textilis in Southeast green larvae hatch after about 58 days. The larvae
Asia and Papua New Guinea. Damage has also move to the outer leaf lamina where they com-
been reported from bamboo, coconut and other mence feeding and then produce loose rolls by
plants although it has been suggested that other cutting the leaf and rolling the lamina towards the
species may be responsible for the records on midrib. Larvae feed and grow within the rolls,
palms and bamboo. Banana clumps in isolated commencing a new roll once the midrib is reached.
villages in Java had a very patchy damage distri- The second and subsequent three instars are cov-
bution, ranging from severe defoliation to nil on ered in a white waxy powder that provides protec-
clumps growing within close proximity. Heavy tion from drowning during high rainfall. The
rainfall and strong winds are unsuitable for larval stage lasts 2030 days, depending on tem-
banana skipper. Entry of water into the leaf rolls perature. Pupation occurs within the leaf roll and
drowns the larva (particularly the first instar) lasts 812 days. Adults emerge in the afternoon
and wind-torn leaf laminae are unsuitable for and are most active in the evening and early morn-
the production of leaf roll shelters. For these ing when they actively fly around banana plants to
reasons, outbreaks in Malaysia and Indonesia mate and oviposit.
366
B Banana Pests and Their Management

Pest Status result in splitting of the peel with subsequent

development of secondary rots. Usually only fruit
Direct fruit production losses is only significant grown commercially requires treatment with
following heavy defoliation since banana plants prophylactic pesticides. In Australia, chemical
can withstand at least 20% leaf lamina loss before treatments are routinely applied to prevent the
production is affected. Nonetheless, bananas in rusty brown discoloration caused by the pantropi-
Southeast Asia are grown for aesthetic value and cal banana rust thrips C. signipennis. The closely
for culinary purposes where even minor infesta- related C. orchidii (Moulton) causes similar dam-
tions would be detrimental. age in Central and South America. The banana
flower thrips T. hawaiiensis, a widespread and
polyphagous flower feeder in Oriental and Pacific
Control Measures regions, damages fruit at flowering as it oviposits
and feeds on fruit during and immediately after
The banana skipper is adequately controlled by a emergence of the inflorescence. The slightly raised,
range of beneficial insects such that other control silvery grey lesions caused by these thrips are
measures are seldom required. In Indonesia, egg locally referred to as corky scab.
parasitoids, including Ooencyrtus erionotae, Agi- In Mexico, Frankliniella parvula prefers to ovi-
ommatus sp. and Anastatus sp., can parasitize 50 posit in the epidermis of young banawna fruits and
70% of the eggs. Young larvae are attacked by less frequently in the flower parts. In Yemen, Scirto-
Apanteles erionotae while older third instar larvae thrips aurantii and Thrips pusillus cause fruit spot-
are preferred by Scenocharops sp. The pupal para- ting on bananas. Small circular spots first appear on
sitoids Brachymeria sp., Xanthopimpla sp. and the surface of the fruit, gradually enlarge, blacken,
Pediobius sp. also contribute to biological suppres- and develop into oily, water soaked lesions.
sion of E. thrax. If unusually heavy outbreaks In Australia, T. hawaiiensis causes a superfi-
occur, the collection and destruction of leaf rolls cial skin injury locally referred to as corky scab.
may reduce subsequent damage. Adults are attracted to the emerging inflorescence.
Female oviposition and subsequent nymphal and
adult feeding cause damage on the developing
Banana Thrips (Thysanoptera: fruit while the bunch is wrapped closely in the
Thripidae) bracts. Oviposition punctures result in localized
raised pimples which disappear as the fruit
Species of thrips that attack and damage banana develops, while the superficial grazing by the
include Chaetanaphothrips orchidii (Moulton), C. thrips develops into the slightly raised silvery-grey
signipennis, Caliothrips bicinctus, Frankliniella areas of corky scab. This damage is more prevalent
parvula, Heliothrips haemorrhoidalis (Bouch), during dry periods and is more commonly associ-
Hercinothrips bicinctus (Bagnall), Thrips hawai- ated with fruit fingers on the lower bunch hands,
iensis (Morgan), and Tryphactothrips lineatus. the rachis and attacked cushion.
The banana thrips H. bicinctus (Bagnall), C. bicinc-
tus, C. orchidii, C. signipennis, T. hawaiiensis and
T. lineatuss are the most important peel-blemish- Biology
ing insects, producing a range of damage symp-
toms on immature fruit. Eggs are inserted into the plant tissues including
Thrips cause superficial skin blemishes on fruit, pseudostem and leaf petioles, depending on
immature and developing banana fruit. Damage is species. Surfaces that are in close contact are pre-
primarily cosmetic although severe attacks may ferred for oviposition and development. The eggs
 Banana Pests and Their Management
B 367

hatch in 12 weeks. Nymphs are clear to straw- flowers after the fruits are formed, removal of
colored and, like the adults, shun sunlight, quickly alternate host plants, and covering banana bunches
dispersing when disturbed from their cryptic hid- with a bag impregnated with insecticides have
ing places between adjacent fruit or from under leaf been recommended. There are no known useful
bracts on the pseudostem. Pupation takes place on natural enemies of banana thrips. Reportedly there
the plant or in the soil near the base of the plants, is a lack of effective predators for C. signipennis in
depending on species. Banana rust thrips (C. signi- north Queensland, Australia, although a number
pennis) may spend part of their life cycle in the soil, of generalist predatory bugs, coccinellids and
while banana flower thrips stages all occur on the chrysopids feed on flower thrips and can reduce
host plant. For example, in Australia, the entire life their numbers.
cycle of T. hawaiiensis is spent on the fruit or other Chemical control methods consist of enclosing
parts of the plant. During summer months, the the bunch inside an insecticide-treated bag. This
period from egg to adult for this species is 3 weeks. practice, once widespread, is still recommended in
South America. A single pesticide injection into the
emerging inflorescence, a treatment specifically
Pest Status aimed at the banana scab moth, is also efficacious
against T. hawaiiensis and helps protect from early
Thrips can scar, stain, or deform banana fruits by C. signipennis infestation. Attaching a piece of
feeding on the fruit skin. Thrips are small, winged chlorpyrifos impregnated ribbon to the upper bunch
insects that feed on banana flowers and/or the ten- stalk also provides extended protection against C.
der green skin of developing fruits. The two fac- signipennis. Untreated polythene bunch covers sig-
tors of feeding site and species determine the type nificantly reduced damage compared to uncovered
and extent of fruit damage. Thrips outbreak can fruit, while bunch covers impregnated with 1% chlo-
occur during periods of dry weather. Thrips cause rpyrifos provided almost total protection.
superficial skin blemishes on immature and devel-
oping banana fruit. Damage is primarily cosmetic
although severe attacks may result in splitting of The Banana Aphid, Pentalonia
the peel with subsequent development of second- nigronervosa (Hemiptera:
ary rots. Usually only fruit grown commercially Aphididae)
requires treatment with prophylactic pesticides.
Most of the species are found in the inflores- The banana aphid, Pentalonia nigronervosa
cences or between fruits. The skin of severely Coquerel, (Hemiptera: Aphididae) is present world-
infested fruit may crack, allowing secondary inva- wide where banana (Musa spp.) is grown. The aphid
sion of pathogens. In Brazil, injury by T. lineatus is is a serious problem on banana because it is a vector
regularly observed on 30-day old fruits, or fruits of Banana Bunchy Top Virus (BBTV), the most
larger than 32 mm in diameter. damaging virus disease of bananas. The preferred
host of this aphid is banana but also may infest
many tropical and subtropical food and ornamen-
Control Measures tal plants, including Alpinia purpurata (floral red
and pink ginger), Xanthosoma (ape or elephant
Cultural control methods, such as clean cultiva- ear), cardamom, Heliconia, tomatoes, taro, Calla,
tion and removal of trash, promote the exposure Costus, kahili ginger, torch ginger, and Zingiber.
of pupae to desiccation, but do not provide effec- The banana aphid is present just about every-
tive control. In Brazil, use of chemical control as where banana is grown. It has been reported
soon as the flowers are formed, elimination of throughout tropical Africa, Atlantic Islands,
368
B Banana Pests and Their Management

Australia, California, Florida and Hawaii (USA), bracts of the ginger stem. The entire inflorescence
Central America, Cook Islands, Egypt, Fiji, Kiribati, may be infested. Small colonies occasionally occur
India, Indonesia, Malaysia, Madagascar, Marshall on the leaf blade. Ants are associated with the banana
Islands, Mauritius, Mexico, Micronesia, the Middle aphid. The ants feed on the honeydew secreted by
East, Mozambique, New South Wales, Papua New the aphid and, in turn, establish new aphid colonies
Guinea, the Philippines, Runion, Samoa, northern and ward off natural enemies. Winged adults often
South America, Taiwan, Tokelau, Tonga, Tuvalu, develop after 710 generations of wingless individu-
Vanuatu, Wallis Island, and much of the West Indies. als. Dispersing winged adults establish new colonies
on other new host plants. Although they are not
strong fliers, they may be carried considerable
Biology distances by light winds. Flight activity peaks
between 9:0011:00 A.M. and 5:00 P.M. to dusk.
Reproduction in the banana aphid is entirely
parthenogenetic (without mating). Females give
birth to live female young. Males are not known Pest Status
for this species. The life cycle (nymph to adult) is
completed in 916 days. The adult life span ranges The banana aphid is a phloem feeder that uses its
from 8 to 26 days; there could be as many as 30 long stylets to pierce plant tissues to suck the sap
generations produced per year in Hawaii. directly from the vessels. This can cause plants to
There is no egg stage. Young are born live. Like become deformed; the leaves become curled and
most other aphid species, the banana aphid has shriveled, and in some cases galls are formed on
four nymphal stages. Newborn nymphs are oval at the leaves. Young plants may be killed or their
first and become slightly elongated. They are red- growth checked if there is sufficient feeding by the
dish brown, with four segmented antennae, and banana aphid. However, direct damage by this
measure 0.1 mm in length. The second stage aphid is generally negligible.
nymphs are similar in appearance and measure The insects do far more harm as vectors of
approximately 0.7 mm long. The third nymphal numerous viruses, including bunchy top. The aphid
stage individuals are light brown, measuring about picks up the virus while feeding on a sick plant,
0.9 mm in length; the compound eyes are more then spreads it to healthy banana plants in subse-
noticeable beginning with this stage, and the quent feedings. Both wingless (apterous) and
nymphs have five-segmented antennae. The fourth winged (alate) aphids are able to transmit viruses.
stage nymphs have six-segmented antennae, are Transmission is usually in a non-persistent manner
light brown in color, and are 1 mm long. The first, where the virus is taken up into the aphids
second, third, and fourth nymphal stages last 24, mouthparts while feeding on an infected plant and
34, 24, and 24 days, respectively. transferred to a healthy plant during subsequent
Adult banana aphids are small to medium feedings. In non-persistent transmission, the virus
sized aphids (12 mm), shiny, reddish to dark brown reproduces in the plant, and aphids simply aid in
or almost black. They have six-segmented antennae transporting the virus. With these types of virus-
that are as long as the body. Alates have prominent, vector associations, the aphid acquires the virus
dark (brown or black) wing veins. Adults start pro- and is only able to transmit the virus temporarily.
ducing young one day after reaching maturity. They Once all the infective charge is reduced by feeding
can give birth to four aphids per day with an aver- or the passing of time, the aphid is unable to trans-
age production of 14 offspring per female. mit the virus until it feeds on infected tissue again.
Colonies of the banana aphid are commonly Symptoms of banana bunchy top disease
found in the upper leaf sheaths and lower flower include bunched, yellow leaves at the top of the
 Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae)
B 369

plant, dark green streaks on the leaves and mid- Hippodamia convergens, Scymnodes lividigaster,
ribs, progressively smaller leaves, leaf curling, and iomus notescens (Coleoptera: Coccinelidae), and
D
small, distorted fruits. Since the aphid harbors the Nesomicromus navigatorum (Neuroptera: Hemero-
virus only temporarily, it needs a regular diet of biidae). The larvae, as well as the adults, of ladybird
infected plant tissue to remain infective. beetles and lacewings are very active aphid feeders,
and have been found, along with syrphid fly larvae,
in floral red ginger in Hawaii.
Control Measures An entomopathogenic fungus, Acremonium
sp., was also observed on banana aphids. The fungus
Farmers typically manage banana bunchy top dis- observed to reduce reproduction, development and
ease by destroying infected plants, which serve as a population of banana aphid, Pentalonia nigronervosa,
reservoir for the virus, and controlling aphids with a vector of bunchy top virus diseases of banana.
insecticides. A wasp that is a known parasitoid of the Banana Weevil, Cosmopolites Sordidus
aphids and ladybird beetles that prey on them was Tropical Fruit Pests and Their Management
introduced in Hawaii as biological control agents.
However, none will control banana aphid adequately
enough to prevent the transmission of BBTV. References

Botha J, Hardie D, Power G (2000) Banana scab moth (Naco-

Chemical Control leia octasema): exotic threat to Western Australia. Fact
sheet No. 45/2000. Hortguard TM Initiative AGWEST,
Department of Agriculture, Australia
Chlorpyrifos and acephate foliar sprays have been Giblin-Davis RM, Pea JE, Oehlschlager AC, Perez AL (1996)
effective in reducing aphid populations and the Optimization of semiochemical-based trapping of
Metamasius hemipterus sericeus (Olivier) (Coleoptera:
attending ants. Immersing flowers and foliage in
Curculionidae). J Chem Ecol 22:13891410
hot water at 49C for 10 min kills banana aphids. Gold CS, Pinese B, Pea JE (2002) Pests of banana, pp 1356
This treatment is safe for many commodities, but In: Pea JE, Sharp JL, Wysoki M (eds) Tropical fruit
preconditioning may be required. pests and pollinators. CABI, Oxford, UK, 448 pp
Scot C, Nelson R, Ploetz C, Kepler A (2006) Musa species
(banana and plantain). Species profiles for Pacific Island
Biological Control agroforestry. Traditional tree initiative, Version 2.2.
(www.traditionaltree.org)
Sosa O, Shine J, Tai P (1997) West Indian cane weevil
Introductions of the braconid Lysiphlebius testaceipes (Coleoptera: Curculionidae): a new pest of sugarcane in
were made in 1923, 1953, and 1965 by the Hawaii Florida. J Econ Entomol 90:634640
Department of Agriculture to combat aphids. The
sources of the introduced wasps include Japan,
Cuba, California, and Mexico. This parasitoid is
established on all populated Hawaiian Islands and Banana Weevil, Cosmopolites
is a known parasitoid of the banana aphid. sordidus (Germar) (Coleoptera:
Biological control experts from the Hawaii Curculionidae)
Department of Agriculture have introduced ladybird
beetles to the islands to control insects. Coccinella clifford s. gold1, william tinzaara2
7-punctata var. brucki was brought in from Okinawa 1
CIAT, Kampala Uganda
in 1958 and is established on the major islands, and 2
Bioversity International, Kampala Uganda
is listed as a banana aphid predator. Other predators
that have been successfully introduced to combat The banana weevil is the most important insect
aphids are Coelophora inaequalis, C. pupillata, pest of banana and plantain. Its host range is
370
B Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae)

restricted to wild and cultivated clones of Musa contribution of M. acuminata and M. balbisiana.
(banana, plantain, abaca) and Ensete. The insect Cooking, roasting, dessert and brewing types are
originated in Southeast Asia and has spread to all grown. Production systems range from kitchen
important banana and plantain growing areas. It is gardens and small, low input stands to large-scale
not normally a pest in its area of origin. export plantations.
Banana weevil larvae bore in the corm, damag-
ing the root and vascular system, reducing nutrient
and water uptake, and weakening the stability of the Biology and Life Cycle
plant. Attack in newly planted banana stands can
lead to crop failure. In established fields, weevil Adult Stage
damage can result in plant loss (death of suckers,
toppling, snapping), reduced bunch weights, mat Adults are uniform black or dark brown and
disappearance (following failure to produce suckers), average 12.513 mm in length. The sex ratio is 1:1.
and shortened stand life. Damage and yield losses Males can be distinguished from females on the
increase over time. Yield losses may exceed 50% in basis of small pits on the rostrum extending
ratoon crops. Stand life can be reduced from more beyond the point of insertion of the antennae and
than 30 years to less than five. by greater curvature of the last abdominal sternite.
Banana weevil pest status is affected by clone Males are on average 20% smaller than females in
selection, ecological conditions, and management size and weight.
system. Highland bananas (AAA-East Africa) and The banana weevil displays a classical K
plantains (AAB) are most susceptible. Other clonal selected life cycle with long life span and low
groups, including export dessert bananas (e.g., fecundity. Adults may live 4 years though most live
Cavendish, AAA), tend to be moderately to highly less than 1 year. They are free living but closely
resistant. Ensete is susceptible, but usually grown associated with banana mats and cut residues. They
above the pests upper elevation threshold and there- are usually hidden during daylight hours and most
fore escapes attack. often observed at traps. The adults feed on rotting
banana tissues and can survive months without
food. They require moist environments and die
The Host Crop within days if maintained on dry substrates. Banana
weevils are attracted to their hosts by volatiles,
Banana is an herbaceous perennial that is propa- especially those released from damaged corms.
gated through lateral buds giving rise to new plants Males produce an aggregation pheromone attrac-
(suckers). The plant consists of an underground tive to both sexes.
corm and a pseudostem composed of overlapping Banana weevils are negatively phototrophic
leaf sheaths. The true stem emerges from the corm, and most active between 2100 and 0400 h
grows through the pseudostem, and bears the Temperature thresholds for activity are 1518C.
inflorescence. The plant dies after the bunch Flight is uncommon. Dispersal by crawling is limited;
matures. A group of plants sharing a common fewer than half move 50 m in a year. The banana
corm comprise a mat. Suckers may be detached weevils narrow host range and limited dispersal
from the mat and planted elsewhere. capability preclude immigration of adults into
Edible bananas are ultimately derived from isolated stands. Dissemination is primarily through
two wild progenitors, Musa acuminata and M. bal- movement of infested planting material (suckers).
bisiana. Banana clones (or cultivars) are assigned Ovipositing weevils prefer flowered plants and
to genome groups (e.g., AB, AAA, AAB, ABB, crop residues but accept all plant stages. Females
AAAA) based on ploidy and the relative genetic are attracted to freshly cut corms, making suckers
 Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae)
B 371

detached from banana mats especially vulnerable; and resistant clones and will accept any clone
a single larva can kill a young plant if it damages for oviposition. A male aggregation pheromone
the growing point. Oviposition rates are usually (sordidin) is attractive to both sexes. This has been
0.54 eggs per week, although averages of 14 eggs synthesized and is commercially available as lures.
per week have been observed. Low fecundity con- The attraction range of semiochemicals is unlikely
tributes to the slow build-up of weevil populations to exceed 10 m and may be much less.
over time.

Monitoring
Immature Stages
Accurate assessment of banana weevil population
Eggs (0.52 mm) are cylindrical and laid in the levels and damage are necessary for understanding
corm and base of the leaf sheaths. Eggs are depos- pest status, screening germplasm and evaluating
ited singly in holes (12 mm deep) excavated by the impact of intervention strategies. The insects
the female with her rostrum. Eclosion rates are biology makes assessment and control difficult.
80100%. Larvae emerging in leaf sheaths usually
move to the corm, although feeding in the true
stem and, rarely, the pseudostem also occurs. In Damage Assessment
the corm, the larvae prefer cortical tissue to the
central cylinder. The larvae pass through 58 The reclusive behavior of the adults and the
instars. Pupation is in a bare chamber near the difficulties in measuring larval damage in the inte-
plant surface. rior of the corm has resulted in a multitude of
In West Africa, developmental thresholds and scoring and evaluation systems. These include
thermal requirements were 12C and 89 degree- monitoring adult numbers through trapping;
days for eggs, 8.8C and 538 degree-days for larvae, measuring damage to the corm periphery; and
and 10.1C and 121 degree-days for pupae. Under measuring internal corm damage through cross
ambient tropical conditions, stage duration is 68 and longitudinal sections. Some of these methods
days for eggs, 2155 days for larvae, and 68 days are subjective, making results hard to interpret or
for pupae. In addition to temperature, larval stage compare. Moreover, sites of banana weevil attack
duration is affected by clone, plant stage, size of may differ among clones. In Uganda, for example,
corm, and weevil density. The data suggest the dessert banana Ndiizi (AAB) had similar levels
extended periods of low night-time temperatures of damage to the corm surface as that of highland
(e.g., at higher elevations) are bottlenecks for cooking banana (AAA-EA), but only 16% as much
immature development and/or adult survival. The internal damage within the corm.
banana weevil is rarely important at elevations Damage to the corm interior is better related
above 1,600 m. to yield loss than damage to the corm periphery,
while damage to the central cylinder is more
important than damage to the corm cortex.
Semiochemicals Measuring larval damage in cross sections at
the collar (corm-pseudostem junction) and 10 cm
Both males and females are attracted to hosts by below the collar in recently harvested plants is
kairomones containing mono- and sesquiter- recommended. A common method is to visually
penes. Attraction to corm material is greater than estimate percentage cross section surface area con-
to pseudostems. Field observations suggest that sumed by weevil larvae in the central cylinder and
banana weevils are attracted to both susceptible cortex, respectively.
372
B Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae)

Yield losses tend to increase over time. In one populations may be as much as 2.5 times higher in
trial, yield losses increased from 9% in the plant mulched than in unmulched plots because of more
crop to 48% in the third ratoon. In Ghana, weevil favorable soil moisture conditions.
damage in plantain stands was often low in spite of
susceptible germplasm, favorable temperatures and
low management levels. Shifting agricultural systems Pest Status
predominated with most plantain abandoned after
two crop cycles. As such, short plantation life The pest status of banana weevil was once controver-
precluded adequate time for weevil populations to sial as many clones are resistant and attack in some
build up to damaging levels. Weevil problems (e.g., Cavendish, AAA) is often realized on crop
became evident in the few plantations maintained residues where damage has no effect on yield.
beyond two cycles. Meaningful yield losses have now been demonstrated
in highland banana (AAA-EA) and plantain (AAB)
systems. The banana weevil has also been shown to
Population Densities be an important component of yield decline leading
to the disappearance of highland bananas in its
Adult populations may be monitored using traps traditional growing areas in East Africa.
made from corm or pseudostem residues. How- Crop establishment may be impeded if plant-
ever, interpretation of trap data is difficult as a ing is in an already infested field or if planting
multitude of factors (e.g., materials, size, number, material carries eggs and larvae. Plant loss of up
location, weather) influence trap catches. There- to 40% has been recorded in newly planted
fore mark and recapture studies (using pseu- highland banana and plantain stands. In fields
dostem traps) are recommended for estimating with minor initial infestations of banana weevils,
population densities. Weevils are marked by population build-up is slow and problems may
scratching the elytra. In Uganda, densities not appear for several years. In a highland banana
among proximal farms ranged from 850 adults/ha trial in Uganda, damage to the central cylinder
(1.5 per mat) to 149,000 adults/ha (240/mat), while increased from 4% in the plant crop to 17% in the
in Cameroon density estimates for subplots third ratoon. Similarly, in surveys of plantain
ranged from 10 to 337 adults/mat. systems in Ghana, damage increased from 2% in
This within-site variability suggests that man- the plant crop to 7% in the second ratoon. Damage
agement plays an important role in regulating will have a greater effect on yield if the same mat
weevil populations. Weevil pressure is widely has sustained heavy attack in preceding crop
believed to be associated with clonal susceptibility, cycles. Thus, single cycle yield loss trials may
management levels, bad drainage, acid or low underestimate weevil importance. For example,
fertility soils, weedy fields, inadequate sanitation, yield losses in several highland banana trials
extended droughts and nematode infestations. went from negligible in the plant crop to 4860%
However, on-farm and on-station studies have within a few years.
failed to find strong relationships between weevil Yield loss is reflected in plant loss, reduced
damage and management factors or plant stress. bunch weights and dying out of mats. Plant loss
Moreover, only a modest relationship (r=0.22) attributable to banana weevil attack in two high-
existed between weevil adult density and damage land banana trials increased from 4% in the plant
across 50 farms within one watershed. Population crop to 29% in the third ratoon, while heavily
estimates may be a poor indicator of economic damaged plants suffered reductions in bunch
status if a high population reflects build-up on weights of 2045%. In another trial, 35% of
residues rather than maturing plants. Also, adult banana mats died out in 5 years in plots infested
 Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae)
B 373

with weevils, compared to 2% mat loss in con- the time of planting. Once established in the field,
trols. This suggests that the weevil can severely it is unclear whether tissue culture plants are
reduce stand life. Farmers in central Uganda more or less susceptible to banana weevils than
reported that banana weevil had contributed to plants grown from suckers. Paring (removal of
reductions in highland banana stand life from >30 the outer corm surface) eliminates most eggs and
years to 4 years, while in Colombia the weevil first instar larvae, and exposes weevil galleries,
reportedly reduced plantain stand life to two to allowing farmers to reject heavily damaged
three crop cycles. suckers. Paring cannot remove larvae that have
penetrated below the corm surface. Suckers may
be dipped in pesticide solutions or pesticides
Integrated Pest Management may be applied to the planting hole. Alternatively,
Beavueria bassiana formulations can be applied
Current research results suggest that no single to planting holes to reduce weevil attack of
control strategy will provide complete control suckers. None of these methods assure elimina-
for banana weevil. Therefore, a broad integrated tion of weevils. Adults may already be in the field
pest management (IPM) approach, combining a from a previous planting or may invade from
range of methods, might offer the best chance nearby plantations. As a result, the benefits of
for success in controlling this pest. The compo- clean planting material may be limited to a few
nents of such a program include cultural control crop cycles.
(habitat management), biological control, host Selected cropping systems: Mixed cropping
plant resistance, botanicals and (in some cases) systems often result in lower insect pressure by
chemical control. reducing immigration rates, interfering with host
plant location and increasing emigration rates.
However, banana weevils are sedentary insects
Cultural Control (Habitat Management) that live in perennial systems with an abundant
supply of hosts. Coffee intercrops and residues
Cultural controls for banana weevil include clean (e.g., husks) may repel banana weevils but this
planting material, selected cropping systems, requires further study. Otherwise there is little
improved agronomic practices to promote plant evidence that intercrops or insect-repellent green
vigor, crop sanitation (destruction of crop residues) manures (Canavalia, Mucuna, Tephrosia) have
and trapping with crop residues. meaningful effects on banana weevil populations.
Clean planting material: Infested suckers
provide the principal entry point of banana weevils
into newly planted fields. Thus, clean planting Crop Sanitation
material eliminates the most important source of
infestation in new plantations. The insects low Banana residues serve as adult refuges and ovipo-
fecundity and slow population growth suggest that sition sites and contribute to population growth.
a reduction in initial infestation level can retard In Uganda, 2532% of adult weevils were associ-
pest build-up and damage for at least several ated with prostrate (cut or fallen) residues, while
cycles. The use of clean planting has been widely another 1012% was found in standing stumps. In
recognized and promoted. Australia, 60% of adults emerged from residues.
Recommended methods include the use of For some clones, banana weevil damage is much
tissue culture plantlets, paring and selection of higher on residues than on growing banana plants.
weevil-free suckers, pesticides, and entomo- It is widely believed that destruction of crop
pathogens. Tissue culture plants are insect-free at residues (splitting of harvested pseudostems
374
B Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae)

and/or removal of corms) lowers overall weevil Biological Control

populations and reduces damage on standing
plants in susceptible clones. In Ugandan field Biological control efforts against banana weevil
surveys, sanitation level had more impact on have included the use of exotic natural enemies
weevil pest status than any other management (classical biological control), endemic natural
practice. In on-farm trials, increasing sanitation enemies and microbial control (e.g., entomo-
level from low to high for 3 years reduced adult pathogens, entomophagous nematodes). Micro-
population density from 52,000 to 13,000 ha1, bial control agents may require repeated
lowered corm damage by 41% and increased applications as biopesticides and entail application
yield by 70%. costs on the part of the farmer.

Trapping Classical Biological Control

Traps exploit banana weevil attraction to crop Introduced pests, unimportant in their areas of
residues. The most common are split pseudostem origin, often reach damaging levels when released
traps (3060 cm lengths split longitudinally and from the control of co-evolved natural enemies.
placed flush on the soil surface at the base of The banana weevil appears to fit this pattern.
banana mats) and disk-on-stump traps (a piece of Searches in southeast Asia identified histerids
cut corm placed on top of a banana stump). Inclu- (Plaesius javanus Erichson and Hololepta spp.),
sion of corm material in a trap increases its attrac- staphylinids (Belonuchius ferrugatus Erichson and
tivity to weevils. Thus disk-on-stump traps tend Leptochirus unicolor Lepeletier), a hydrophilid
to have higher weevil catches than pseudostem (Dactylosternum hydrophiloides MacLeay), a cucu-
traps. However, pseudostem trapping is more jid (Canthartus sp.), and a leptid (rhagionid) fly
often recommended for systematic trapping (Chrysophila ferruginosa (Wied.)) as predators of
studies because a single harvested plant can only banana weevil. Of these, P. javanus appeared most
support one disk-on-stump trap (fixed in space), important. Between 1913 and 1959, 45 attempts
while the same plant can provide material for were made to introduce eight natural enemies
many pseudostem traps (placed where the farmer from Asia to other banana growing regions in the
deems most useful). The effect of trapping on world. P. javanus, for example, was released in
weevil populations will, in part, reflect trap den- Australia, Oceania, Latin America and Africa.
sity and trapping frequency. Intensive trapping in In most cases, the predators did not establish and
established fields results in a gradual decline in in no case did they provide control. Recent searches
weevil numbers with a lag time required before for egg and larval parasitoids in Indonesia came
effects are manifested in reduced damage. In a up empty handed. Classical biological control of
1-year study in farmers fields in Uganda, weevil banana weevil, therefore, remains an elusive
numbers declined by 61% in farms with intensive objective.
trapping (1 trap/mat/month), 53% with moderate
trapping (0.30.6 traps/mat/month) and 38% in
farms without trapping. Trapping success was Indigenous Natural Enemies
affected by management level and weevil immi-
gration from neighboring farms. Although Reported arthropod predators of banana weevil
farmers were convinced that trapping was bene immatures include nabids, cydnids, capsids, redu-
ficial, adoption was low due to resource and viids, mirids, thrips, rhagionids, sarcophagids,
labor requirements. histerids, carabids, hydrophilids, staphylinids,
 Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae)
B 375

t enebrionids, labiids, carcinophorids, and formi- penetration through the insects cuticle. The fungi
cids. Ants appear to be the most promising while can kill the insect through direct attack on the
other predators seem of little importance. In insects nutrients or through toxic metabolites.
Cuba, the myrmecine ants Pheidole megacephala Dead insects kept in moist environment quickly
and Tetramorium guineense (Mayr) reduced developed surface growth of mycelia. Beauveria
banana weevil populations and damage by bassiana can invade the haemocoel where it
5469% following artificial establishment of ant produces a toxin, beauvericin, that reduces
colonies in plantain stands. In Uganda, Pheidole competition with bacteria and weakens the
sp. and Odontomachus troglodytes were most immune system. Strain virulence is often related
effective in reducing weevil egg and larval popu- to toxin production.
lations in pot experiments. Both species readily Natural rates of infestation are normally
entered and removed larvae from galleries in crop low (i.e., <5%). Nevertheless, numerous strains of
residues. B. bassiana and M. anisopliae have been demon-
strated to kill >90% of banana weevils when applied
topically in the laboratory or in pot trials. In Ghana,
Microbial Control B. bassiana applications to planting holes reduced
damage to suckers, while in Brazil, Colombia, Costa
Microbial agents tested against the banana weevil Rica, Cuba and Uganda, applications B. bassiana at
include entomopathogenic fungi (e.g., Beauveria the base of established mats in banana or plantain
bassiana and Metarhizium anisopliae) and ento- stands reduced weevil populations and/or increased
mopathogenic nematodes (e.g., Steinernema spp. yields. In Uganda, transmission from infected to
and Heterorhabditis spp.). Entomopathogenic uninfected weevils under field conditions was 13%.
fungi and nematodes are most often used to kill While these studies demonstrate field potential,
adult weevils. Beauveria bassiana has been estab- cost-effective production and delivery systems still
lished as an endophyte, although its potential need to be developed. However, field establishment
against banana weevil immatures is not yet clear. of B. bassiana tends to be low, so repeated applica-
Although a number of strains of entomo- tions are usually necessary.
pathogenic fungi and entomopathogenic nema- Entomopathogenic nematodes in the genera
todes have shown promise in the laboratory and in Steinernema and Heterorhabditis have been tested
preliminary field studies, efficient and economi- against banana weevil, most notably in Australia.
cally viable mass production and delivery systems Infective juvenile nematodes enter through natural
still need to be developed, while the performance orifices (Steinernema) or interskeletal membrane
of microbial control agents against banana weevil (Heterorhabditis). After entering the host, the nema-
under different agro-ecological conditions is not todes penetrate mechanically into the haemocoel
well understood. Only in a few sites have entomo- and release Xenorhabdus bacteria which cause
pathogens been reported to establish following septicemia and death within 12 days. In Brazil,
applications in banana fields. Without adequate entomopathogenic nematodes were widespread in
establishment, entomopathogens will require plantain stands, but naturally occurring mortality of
repeated applications as a biopesticide. This will banana weevils was low and, as with entomo
entail continued production, distribution and pathogenic fungi, viable delivery systems are an
storage costs that will be passed on to the farmer. important consideration. The cryptic habitat of
The conidia of Beauveria and Metarhizium weevil larvae within living plants makes delivery
enter the insect through its spiracles or digestive against these stages difficult; therefore, applications
system or by producing extracellular proteolytic, of entomopathogenic nematodes should target
chitinolytic and lipolytic enzymes which facilitate adult weevils.
376
B Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae)

The most effective entomopathogenic nema- Antixenosis (nonpreference) is of little impor-

tode delivery system, developed in Australia, tance. Laboratory and field studies suggest that
capitalizes on the weevils attraction to cut corms banana weevils (i) appear to be attracted equally
and damaged plants. This system employs conical to susceptible and resistant clones, and (ii) will
shaped cuts in residual corms, i.e., a cone is cut and accept all clones for oviposition. Clonal attraction
removed, and then loosely replaced into the corm. and acceptance (i.e., number of eggs) were not
These cuts attracted adult weevils and provided related to damage. In one field trial, oviposition
thigmotactic stimuli that encouraged them to remain was similar on resistant Pisang awak (ABB) and
at the infection sites. The holes also buffered the susceptible five highland bananas (AAA-EA),
delivery site against temperature extremes and pro- while subsequent damage was 525 times higher
vided excellent conditions (high humidity, moderate on the highland clones. Thus, antibiosis appears to
temperatures, protection against ultraviolet light) for be the most important in conferring host plant
nematode persistence. The nematodes were released resistance to banana weevil.
at a density of 250,000 per hole in a formulation Antibiotic factors are those which negatively
including a polyacrylic gel (to reduce water build-up influence larval performance (i.e., poorer survivor-
and incidence of nematode drowning) with an adju- ship, slower development rates, reduced fitness).
vant of 1% paraffin oil (to encourage the weevils to These factors may be physical (e.g., sticky sap and
raise their elytra, exposing the first spiracle for latex, corm hardness), antifeedants, toxic secondary
nematode entry). However, controls based on plant substances and nutritional deficiencies. To test
entomopathogenic nematodes are more costly than these factors, banana weevil larvae are commonly
pesticides in Australian commercial banana systems. reared on potted plants or excised corm material.
One difficulty in this system is that resistant factors
may quickly break down after harvest or ex situ.
Host Plant Resistance For example, Pisang awak (ABB) is highly resis-
tant to banana weevil in Indonesia; larvae freely
Highland bananas (AAA-EA) and plantains (AAB) feed without problems in its residues. Similarly,
are most susceptible to banana weevil attack. Some Yangambi- Km5 is highly resistant to banana
variability exists among clones within these weevil, often showing no damage in screening trials,
genome groups. Among highland bananas, for yet larvae may be successfully reared on excised
example, Atwalira and Kisansa displayed weevil corm material taken from this clone.
damage scores two to three times higher than Nevertheless, screenhouse and laboratory
those for Mbwazirume and Nakyetengu, while the studies have shown that immature banana weevils
degree of penetration into the central cylinder was may have higher mortality, extended develop-
greatest for Nakitembe, Namwezi and Musakala. mental periods and lower pupal weights on
In screening trials, Ensete appeared to be highly resistant clones. Corm extracts from resistant
susceptible. However, in Ethiopia where the crop is Pisang awak placed on corm material of suscep-
most widely grown, Ensete escapes attack because tible highland banana clones severely inhibited
most production is above the weevils upper eleva- larval feeding while extracts from other clones did
tional threshold. Export Cavendish dessert bananas not. A bioassay-guided separation process of the
(AAA) are generally considered resistant, although Pisang awak extract was then undertaken using
serious banana weevil problems may occur in some chromatographic techniques. Two of the 16 frac-
areas (e.g., southeastern coast of South Africa). A tions obtained were found to be very active against
wide range of other banana dessert and brewing weevil larvae. However, the compounds respon-
types (AB, AAA, AAB, ABB) are moderately to sible for activity against banana weevil have not
highly resistant to banana weevil. been identified.
 Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae)
B 377

To date, there have been no attempts to breed Botanical Control

bananas or plantains for resistance to banana
weevil. Conventional breeding of banana is a dif- In Kenya, varying formulations of neem
ficult and complicated procedure as the most (Azadirachta indica) seed derivatives (neem
widely used clones are triploids and sterile. This seed powder, neem kernel powder, neem cake
entails crossing wild diploid and highly fertile and neem oil) applied to banana material greatly
males to female triploid clones followed by exten- (i) reduced adult settling on corm pieces, (ii)
sive hybrid selection. Nevertheless, there does reduced oviposition rates, (iii) reduced eclosion
appear to be useful sources of resistance within the success, (iv) increased larval penetration time,
available germplasm. The wild diploid Calcutta-4 (v) extended larval development, (vi) increased
(AA), Yangambi-Km5 (AAA) and the hybrid larval mortality, (vii) reduced larval weights,
FHIA-03, for example, show high levels of resistance (viii) impeded population build-up in field tri-
and might be exploited in breeding programs. Corm als, and (ix) reduced damage in pot and field
hardness has been shown to be a key resistance experiments. Neem kernel powder and neem oil
mechanism and screening for this trait may assist in appeared toxic to the banana plants and may
weevil improvement. Secondary metabolites found have interfered with nutrient and water uptake,
in resistant clones also appear to be important. whereas neem seed powder and neem cake dis-
Transgenic approaches (i.e., biotechnology) played phytotoxic effects only at very high
are also being used to develop resistant clones by application rates. Neem applications in farmers
transforming banana through insertion of foreign fields in Tanzania also resulted in reduced dam-
genes, in particular cysteine proteinase inhibitors age. In spite of these encouraging results, neem
(cystatins) from rice and papaya and toxins derived has not been widely adapted by farmers due to
from the bacterium Bacillus thuringensis (Bt). availability and costs.
Cysteine proteinases are mid-gut enzymes that
many beetles, including banana weevil larvae, use
in the digestion of dietary proteins. Cysteine Chemical Control
proteinase inhibitors are defensive compounds
produced by some plants in response to insect Chemical pesticides for control of banana weevil
attack or wounding. These inhibitors impede diges- may be applied to protect planting material
tion resulting in protein deficiency and stunted (through dipping of suckers or applications in
development. Bt has been used as a biopesticide planting holes), periodically applied at the base of
in the control of several insect pests. More recently, the mat after crop establishment, and/or applied
Bt toxin genes have been inserted into crop plants to pseudostem traps to increase trap catches.
to improve resistance. There have been numerous studies on the relative
Successful incorporation of cysteine protei- efficacy of different insecticides under different
nase inhibitors from rice and papaya into banana formulations and application rates, persistence
tissue reduced banana weevil larval body weights and the appearance of insecticide resistance in
by 60% in 10 d. Current efforts are to insert the banana weevils. At least 45 pesticides have been
genes into banana plants. In preliminary bioassays, used at one time or another against banana
incorporation of the Cry3A Bt toxin into artificial weevil. Insecticide resistance in banana weevil
diets resulted in 30% mortality of banana weevil has been documented in Australia, Latin America
larvae. It is believed that high rates of mortality can and Africa for a range of chemicals including
ultimately be achieved by pyramiding cysteine cyclodienes, organophosphates, and carbamates.
proteinase inhibitors and Bt toxins. Research in Cross-resistance has also been demonstrated.
this area is on-going. Nevertheless, chemicals remain an important part
378
B Band

of banana weevil control although costs often Band

make them prohibitive for subsistence farmers.
Pesticides remain the fastest action method that A transverse line, usually wide, crossing the body.
can be used to bring a weevil outbreak under This term often is confused with stripe, a term
control. used to designate a longitudinal line running the
Tropical Fruit Pests and Their Management length of the body. The term band is also used to
describe an aggregation of insects, usually immature
grasshoppers or caterpillars, dispersing in the same
direction.
References

Collins PJ, Treverrow NL, Lambkin TM (1991) Organophos- Band Application

phorous insecticide resistance and its management in
the banana weevil borer, Cosmopolites sordidus (Germar)
(Coleoptera:Curculionidae), in Australia. Crop Protect An application in which an insecticide (or other
10:215221 chemical) is applied in strips, usually to the
Gold CS, Pea JE, Karamura EB (2001) Biology and integrated planting bed or seed row.
pest management for the banana weevil, Cosmopolites
sordidus (Germar) (Coleoptera:Curculionidae). Integr
Pest Manag Rev 6:79155
Gold CS, Ragama PE, Coe R, Rukazambuga NDTM (2005) Banded Thrips
Selection of assessment methods for evaluating banana
weevil Cosmopolites sordidus (Germar) (Coleoptera:
Curculionidae) damage on highland cooking banana
Members of the family Aeolothripidae (order
(Musa spp., genome group AAA-EA). Bull Entomol Res Thysanoptera).
95:115123 Thrips
Kiggundu A, Gold CS, Labauschagne MT, Vuylsteke D,
Louw S (2003) Levels of host plant resistance to banana
weevil, Cosmopolites sordidus (Germar) (Coleoptera:
Curculionidae), in Ugandan Musa germplasm. Euphyt- Bandwinged Grasshoppers
ica 133:267277
Kiggundu A, Pillay M, Viljoen A, Gold C, Tushemereirwe W,
A subfamily (Oedipodinae) of grasshoppers in the
Kunert K (2003) Enhancing banana weevil (Cosmopolites
sordidus) resistance by genetic modification: a per- order Orthoptera: Acrididae.
spective. Afri J Biotechnol 2:563569 Grasshoppers
Nankinga CM, Moore D (2000) Reduction of banana weevil Katydids and Crickets
populations using different formulations of the entomo-
pathogenic fungus Beauveria bassiana. Biocontr Sci
Technol 10:645657
Pavis C, Lemaire L (1997) Resistance of Musa germplasm Banks Grass Mite, Oligonychus
to the banana weevil borer, Cosmopolites sordidus
Germar (Coleoptera: Curculionidae): a review. Info-
pratensis (Banks)
musa 6:39
Tinzaara W (2005) Chemical ecology and integrated mana A mite (Acarina: Tetranychidae) pest of grasses,
gement of the banana weevil Cosmopolites sordidus including wheat.
in Uganda. Ph.D. Thesis, Wageningen University,
Wheat Pests and Their Management
Wageningen, UR, 184 pp
Treverrow NL (1994) Control of the banana weevil borer,
Cosmopolites sordidus (Germar), with entomopatho-
genic nematodes, pp 124138. In: Valmayor RV, Barb
Davide RG, Stanton JM, Treverrow NL, Roa VN
(eds) Proceedings of Banana Nematode/Borer Weevil
Conference, Kuala Lumpur, 1822 April 1994INIBAP, Any of a number of sharp projections armed with
Los Banos, Philippines teeth or hooks. Insects sometimes have spines or
 Bark Beetles in the Genus Dendroctonus
B 379

setae equipped with projections pointed backward Bark Beetles

(to the base, or away from the point) that cause them
to remain imbedded once contact with them is made. Some members of the subfamily Scolytinae (order
Presumably they function in defense, especially Coleoptera, family Curculionidae).
against vertebrate predators. Structures bearing such Beetles
projections are said to be barbed, and the occurrence Bark Beetles in the Genus Dendroctonus
of numerous setae is sometimes described as barbate.
A small barb is called a barbule.
Bark Beetles in the Genus
Dendroctonus
Barber, Herbert Spencer
barbara j. bentz
Herbert Barber was born in South Dakota on April U.S. Department of Agriculture Forest Service,
12, 1882. His father, an engineer, encouraged his Logan, UT, USA
sons interest in natural history. At the age of 16 he
was given employment as an insect preparator at the The genus Dendroctonus (Coleoptera: Curculioni-
U.S. National Museum. He worked at such tasks as dae, Scolytinae), originally described by Erichson in
arranging the Hubbard and Schwarz collection of 1836, currently includes 19 species that are widely
Coleoptera, but including a collecting trip with distributed. Seventeen species occur between Arctic
Schwarz to Arizona and New Mexico. Although he North America and northwestern Nicaragua, and an
was employed continuously at the museum until additional two species are in northern Europe and
retirement, his pay was, after some years, and until Asia. Dendroctonus species attack and infest conifer
his retirement, provided by the U.S. Department of hosts (Pinaceae) in the genera Larix, Picea, Pinus,
Agriculture. In time, by association with entomo and Pseudotsuga. Species within the genus can be
logists and through experience, he began to publish identified by the host species they attack, egg gallery
results of his own studies. His publications eventually patterns, population behavior, and morphological
amounted to some 90 papers. One of the most distinctions. The smallest species is D. frontalis (male
intriguing was on his discovery of the strange life his- length 2.03.2 mm) and the largest is D. valens (male
tory of Micromalthus (Coleoptera: Micromalthidae) length 5.38.3 mm). Members of the Dendroctonus
in which there are several forms of larvae, and that genus, which means tree killers, are noted as the
some larvae may produce eggs and larvae. He died most economically and ecologically significant spe-
in Washington, DC, on June 1, 1950. cies affecting forest ecosystems in western North
America. Tree mortality resulting from Dendrocto-
Reference nus outbreaks can adversely affect timber manage-
ment, forest planning, and recreational opportunities.
Mallis A (1971) Herbert Spencer Barber, pp 281283. In: In contrast, disturbance events caused by native bark
American entomologists. Rutgers University Press, New beetle species are important drivers of forest succes-
Brunswick, NJ, 549 pp sion, foster heterogeneity and biodiversity, promote
biomass recycling, and play a critical role in the fire
ecology and overall health of many ecosystems.
Barberry Whitefly, Parabemisia Dendroctonus beetles are monogamous, and
myricae (Kuwana) spend the majority of their lifecycle in a cryptic
habitat beneath the bark of host trees where larvae
A whitefly (Hemiptera: Aleyrodidae) pest of citrus. feed within the inner bark or phloem. Relative to
Citrus Pests and Their Management the length of their life cycle, only a short time is
380
B Bark Beetles in the Genus Dendroctonus

spent as an adult moving from tree to tree. The commonly used, often with traps, for monitoring
majority of the species in this genus is capable of and control of many economically important
killing the host tree in one generation. In fact, death species in the genus. The complexity of the signal
of the host is often a requirement for successful for interruption of aggregation has made it difficult
brood production. Although most of the species to identify the chemical makeup of compounds, as
are capable of attacking and killing standing, well as, the specific biological action of the
vigorous trees, recently fallen trees are favored by compounds within the population ecology of
some species. The female is the colonizing sex in many Dendroctonus species. Consequently, the
the majority of Dendroctonus species. After attack current use of synthetic interruptive aggregation
of a new host, mating typically occurs in a nuptial chemicals is limited.
chamber beneath the bark and an egg gallery is As with most poikilothermic organisms, tem-
initiated. Adults of a few species, however, mate perature is a strong driving force of Dendroctonus
before emerging from the brood host. Eggs are laid population dynamics and an important controller
either singly along the sides of the gallery, or in of seasonality. Diapause, which is often tempera-
clumps. Egg galleries may be either vertical or ture related, is typically considered the universal
sinuous, and larvae mine and feed horizontally in adaptation of insects for maintaining seasonality.
the phloem, either singly or en mass, depending on However, with the exception of an adult reproduc-
the species. Pupation takes place in individual tive diapause in D. rufipennis and D. pseudotsugae,
niches within the phloem or in the outer bark of and a prepupal diapause in D. rufipennis, this
the host tree. Upon adult emergence, which is usu- physiological timing mechanism appears to be
ally temperature dependent, beetle dispersal to a absent in the Dendroctonus genus. Instead,
new host occurs and the process begins again. Dendroctonus seasonality appears to be under
Aggregation, which facilitates host selection direct temperature control. Life cycle duration in
and mating, is an important life history strategy of the genus is variable depending on the species,
most, although not all, Dendroctonus species. latitude, elevation, and microclimate of the popu-
Aggregation is often a response to chemicals lation. Species in the south can have as many as
produced by the host tree, adults from the same or seven generations per year, whereas in the north,
a different species attacking the host tree, microbes, or at high elevation some species require up to 3
or a combination of these factors. Aggregation on years to complete a single generation. Intraspecific
a single host tree allows for a mass attack by latitudinal differences in many temperature-
conspecific beetles, thereby overcoming the resin associated life history traits exist as well. Global
defensives of the conifer hosts. To overcome the climate warming will undoubtedly have significant
defenses of healthy, vigorous hosts, many beetles impacts on the distribution and seasonality of the
must attack within a short time (13 days). Con- Dendroctonus species.
versely, trees of poor health may be overcome by Many Dendroctonus species carry spores of
fewer beetles (e.g., endemic population levels). symbiotic fungi either passively on the exoskele-
Because a single tree is a limited resource, some ton or in specialized structures of the integument
Dendroctonus species have evolved a response to a called mycangia. The fungi are disseminated
series of chemicals that interrupt aggregation. among host trees via adult Dendroctonus beetles.
These chemicals act to space beetle attacks along a Although little research has been conducted on
single tree and signal incoming beetles to begin fungal associations of the majority of Dendrocto-
attack on another, nearby tree. Synthetic forms of nus species, the work that has been done shows
both attractive and interruptive aggregation chem- both a benefit and a detriment to the beetle,
icals have been developed for many Dendroctonus depending on the particular fungal associate.
species. The attractive aggregant chemical(s) are Benefits gained include protecting the beetle brood
 Bark-Lice, Book-Lice or Psocids (Psocoptera)
B 381

from other antagonistic associates, aiding beetles Office, Forest Service, U.S. Department of Agriculture.
USDA Forest Service, Rocky Mountain Research Station,
in overcoming host tree defenses through patho-
General Technical Report RMRS-GTR-62
genic action of the fungi, altering the moisture Seybold SJ, Bohlmann J, Raffa KF (2000) Biosynthesis of
composition of the phloem, and providing or coniferophagous bark beetle pheromones and conifer
concentrating nutrients essential for reproduction isoprenoids: evolutionary perspective and synthesis.
Can Entomol 132:697753
or development. Wood SL (1982) The bark and ambrosia beetles of North and
Native Dendroctonus bark beetles play signifi- Central America (Coleoptera: Scolytidae), a taxonomic
cant roles in long term forest ecosystem function monograph. Great Basin Naturalist Memoirs, Number 6
and structure. However, forest conditions in many Brigham Young University Provo, UT, 1359 pp
parts of the Dendroctunus range in North America
have changed from conditions that existed prior to
pre-European colonization. The result is large Bark-Gnawing Beetles
landscapes vulnerable to Dendroctonus outbreaks
which are often in conflict with current land use Members of the family Togossitidae (order
objectives. The formulation of effective manage- Coleoptera).
ment strategies for Dendroctonus populations Beetles
requires careful consideration of all aspects of land
use including timber production, the urban/wild-
land interface, wilderness, watershed, recreation Bark-Lice, Book-Lice or Psocids
and wildlife. Synthetic attractive and interruptive (Psocoptera)
aggregation chemicals and silvicultural options
are available for some species to aid in the preven- arturo baz
tion and suppression of large scale outbreaks. Any Universidad de Alcal, MadridSpain
action, including no action, should be tightly tied
to the management objectives for the landscape The insects of the order Psocoptera (=Copeog-
under consideration. Restoration of the landscape natha, Corrodentia) are commonly called psocids,
to reestablish ecological integrity after an outbreak although outdoor species living on tree trunks and
is also important for maintaining long-term branches have been called bark-lice, whereas
ecosystem health. indoor species, sometimes found in old books,
Mountain Pine Beetle have been called book-lice. The Psocoptera are a
Douglas-Fir Beetle small order of paraneopteran insects (near 4,000
Roundheaded Pine Beetle species have been described around the world)
which are found in a wide range of terrestrial eco-
systems throughout the world. Most psocids
References inhabit trees and shrubs, some others occur in
ground litter, others are found on rocks and in the
Coulson RN, Witter JA (1984) Forest entomology, ecology nests of birds and mammals. Some live on herbs
and management. Wiley, New York, NY, 669 pp and grasses, and a few in moss, whereas others are
Mitton JB, Sturgeon KB (1982) Bark beetles in North
American conifers, a system for the study of evolution-
found in caves. Lastly, several species are found in
ary biology. University of Texas Press, Austin, TX domestic habitats. The Psocoptera share certain
Schowalter TD, Filip GM (1993) Beetle-pathogen interac- morphological features with the lice (orders Mal-
tions in conifer forests. Academic Press, London, UK. lophaga and Siphunculata; Phthiraptera of some
252 pp
Samman S, Logan J (2000) Assessment and response to bark authors), and these taxa are grouped together in
beetle outbreaks in the rocky mountain area. Report to the superorder Psocodea by some authors. Fossil
Congress from Forest Health Protection Washington insects identified as psocids have been reported
382
B Bark-Lice, Book-Lice or Psocids (Psocoptera)

from as far back as the Permian period in Kansas, epicraneal suture

ocelli
Russia and Australia. These, together with Jurassic
material from Germany and Russia, differ in many antenna

ways from more recent forms. So, although these

fossils are quite psocid-like, some doubts exist compound
eyes
about their ordinal placement. The earliest unques-
tionable fossil psocids are those from Cretaceous
amber. These Cretaceous forms are essentially postclypeus
modern and do not show any clear connections anteclypeus
with the older fossils of doubtful assignment. labrum

Morphology
maxillary
Psocoptera are free-living exopterygote insects palpi
ranging in body length from 0.6 to 25 mm, Bark-Lice, Book-Lice or Psocids (Psocoptera),
although rarely exceeding 10 mm. Figure 6 Head of Stenopsocus stigmaticus in
frontal view.

cutting edges
Head

The head capsule is large compared to the rest of the

body, with a large bulbous postclypeus. The anten- grinding
edges
nae are long and filiform with 1150 flagellomeres.
The eyes commonly are large and globose, varying
from multi-faceted structures down to the complete
reduction in a cavernicolous species. Three ocelli Bark-Lice, Book-Lice or Psocids (Psocoptera),
are usually present in winged forms, but absent in Figure 7 Mandibles of Cerobasis guestfalica.
apterous species. The Y-shaped epicraneal suture is
prominent. The mouthparts (Figs.610), although Thelabium has reduced one- or 2-segmented palpi,
retaining a chewing function, are specialized. The and the chitinous mentum is divided apically into
mandibles are asymmetrical, and each has both lateral halves (paraglossae) by a small protuberance
grinding and cutting edges. In the maxillae the (glossa) representing the opening of the salivary
cardo is not differentiated; the galea is a large, fleshy glands to the exterior. The labrum is simple, with
lobe, whereas the lacinia is a narrow, sclerotized rod the distal margin bearing two groups of setae: an
(the pick). The lacinia is perhaps the most special- anterior group of 410 sensilla, and a posterior
ized and characteristic psocid structure. The lacinia group which has some taxonomic value. The palatal
may be used to scrape food from the substrate, but lining of the labrum and the anteclypeus is the
such has not been directly observed. Some authors hypopharynx, which has a characteristic structure.
inferred that the lacinae may be used as picks, The lingua bears a pair of ventral sclerites (lingual
because psocids move laciniae vertically in a man- sclerites) which are connected to the median sitophore
ner which suggests this may be so. Also, they appear sclerite by ligaments; these lingual sclerites when
to be used to support the head whilst feeding and protruding are capable of taking up water fromthe
may act to regulate the depth of feeding on the atmosphere (Fig.11). The sitophore sclerite is situated
substrate. The maxillary palpi are 4-segmented. on the ventral surface of the base of the cibarium. On
 Bark-Lice, Book-Lice or Psocids (Psocoptera)
B 383

stipe

maxillary palp

lacinia galea

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 8 Left maxilla of Cerobasis guestfalica.

mentum of both winged and apterous psocids is clearly

separated from the other thoracic segments. Legs
are slender, and hind legs are longer, which allows
them to carry out small jumps. The coxae of hind
paraglosses
legs are modified in many species by having
labial palp cuticular projections of various kinds. The most
Bark-Lice, Book-Lice or Psocids (Psocoptera), usual are a small blister-like projection on the
Figure 9 Labium of Cerobasis guestfalica. inner surface, an ovoid rasp bearing rows of small
denticles; in some cases near the rasp, a rounded
lingual sclerites area of similar size can be found. These structures
are called coxal organs or Pearmans organs
(Fig.12) and the function is unknown, although it
has been suggested that they are stridulatory. The
small trochanters are articulated with the coxae
but their junction with the femora is usually
immovable. The femora are simple, but sometimes
lingua filament markedly convex on their outer surface. Tibiae
sitophore
may have a row of characteristic ctenidiobothria
Bark-Lice, Book-Lice or Psocids (Psocoptera), (setal sockets, having four to ten conspicuous
Figure 10 Hypopharynx. teeth, with each bearing a simple spine) along the
ventral surface. The tarsi are of either two or three
the dorsal surface of the cibarium wall (opposite the segments (all the immatures possess two segments
sitophore) is a knoblike process that is believed to and this character remains in some adults); all
move against the sclerite in the manner of a mortar and except the apical segment have apical spines, and
pestle and facilitate the grinding up food. ctenidiobothria may be present on the basal or all
segments. The tarsus terminates in a pair of claws;
the base of each claw usually has two ventral
Thorax projections: the proximal one is setiform and the
distal (the pulvillus) is of various forms. Some
The thorax unites to the head with a membranous pulvilli are greatly expanded, whereas others are
and flexible neck. In a general way, the prothorax slender or narrow. Expanded pulvilli can act as a
384
B Bark-Lice, Book-Lice or Psocids (Psocoptera)

filament sitophore
labrum

labium

lingual sclerite

hypopharynx

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 11 Mechanism of absorption of atmospheric water.

coxa

Pearmans organ

trochanter
femur

tibiae b
rasp

ctenidiobothria

c pulvillus

claw

d
claws
tarsi

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 12 Metathoracic leg (a); Pearmans organ of
Psococerastis gibbosa (b); ctenidiobothria from a metathoracic tibia (c); detail of a metathoracic
tarsus (d).
 Bark-Lice, Book-Lice or Psocids (Psocoptera)
B 385

sucker, enabling the insect to walk on smooth sur- posterior border of pterostigma. The radial sector
faces. Most foliage-frequenting psocids have a pul- (Rs) terminates in an apical fork, named the radial
villus of this type, whereas most bark-frequenters fork, which is composed of R2+3 and R4+5, and
have a narrow pulvillus. Two pairs of wings contacts the median (M) in the middle of the wing.
(Fig.13) are found in many psocids, although one At this junction, the two veins (Rs and M) may
or both pairs may be reduced in size, showing meet in a point, be linked by a short crossvein or
various states of reduction (brachyptery, microp- be fused for a short length. M usually has three
tery) and sometimes absent (aptery). Some species branches (M1, M2, M3). The first cubital vein (CU1)
are dimorphic, with macropterous individuals of reaches the posterior border of the wing, sometimes
one sex (usually males) and apterous or micropter- simply, but in many psocids it is two-branched,
ous individuals of opposite sex (usually females). forming a cell known as areola postica (AP),
The anterior wings are larger than the hind pair. At which is bordered by CU1a and CU1b. The presence
rest they are held rooflike over the body. The fore and shape of the areola postica vary considerably
and hind wings are coupled during flight and at in different groups of psocids, and it may be joined
rest. Most psocids have simple venation, with few to the median, or fused with it or completely free.
crossveins. The second cubital vein (CU2) is morphologically
In the forewing, the costa (C) forms the wing distinct from the more anterior veins. It is simple
margin. The subcosta (Sc) is often greatly reduced and unbranched. Behind this is one anal vein (1A),
to a small vein at the base of the wing (the basal which reaches the wing margin near the same
sector) and a short vein closing basally the point as CU2. When the vein 1A reaches the margin
pterostigma (the distal sector). The radius (R) runs at the same point as CU2 it forms the nodulus. In
more or less parallel to the costa and forms the a few groups a small second anal vein (2A) is

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 13 Wings of Stenopsocus stigmaticus.

386
B Bark-Lice, Book-Lice or Psocids (Psocoptera)

Fore wing
Cu2

1A
nodulus

stigmapophysis
b
a
Hind wing

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 14 Stigmapophysis from the ventral surface of the
forewing in Cerastipsocus sp (a); joining system of the wings of Lachesilla sp. (b).

resent. The cells take the name of the vein imme-

p Underside the forewing the distal end of Cu2 pos-
diately anterior to them. The one exception is the sess a hook which engages the hind costa in flight.
large discoidal cell bordered by M and Cu1, and
present in the forewing of the family Psocidae and
others forms in which AP is joined to M. In the Abdomen
hind wing the venation is more reduced. Sc is often
vestigial, R1 reduced and simple, Rs forked in two The abdomen consists of ten segments and the
branches as in the forewing, M usually simple but terminal region (telson) formed by three lobes: the
sometimes having two branches, both cubital veins epiproct which is dorsal and the paraprocts which
are simple, and one small anal vein is usually are lateral. In many psocids the last tergite (tg 9+10)
present. As in the forewing, the form of the R-M and the distal half of tergite eight are strongly sclero-
junction can be variable. Of particular interest is tized, forming a structure called the clunium. The
the fact that in the families Lepidopsocidae and epiproct is, normally, a very simple structure, of
Amphientomidae the forewings are typically covered rounded, trapezoidal or triangular shape in both
by scales, and give the insect the appearance of a sexes. In some species, the male epiproct bears rows
small moth. In this case, the shapes of scales are or fields of hooks or denticles. The paraprocts are
sometimes of specific value. Psocids possess two variable in shape. On the dorsal basal region there is
independent methods of wing coupling. At rest, often a well-defined area (sensorial field) containing
some species have a protrusion at the base of the long setae each rising from a sunken rosette-like
pterostigma on the underside of the forewing, socket. These setae are called trichobothria and are,
formed from modified trichia and tracheolar rings presumably, involved in the orientation in flight or
of R1; this projection (known as stigmapophysis) air currents. Near the apex of the paraprocts of the
engages the costal vein of the hind wing in repose Trogiomorpha is a long, thickened spine (anal spur).
(Fig.14). Similar structures for coupling wings in Male genitalia comprise a hypandrium (male
repose can be found in the family Lepidopsoci- subgenital plate) and a phallosome (copulatory
dae, where it is composed of a row of comb-like apparatus). The hypandrium is an expansion of
teeth on Sc or R1. When they fly, many psocids the 9th sternite, defining a cavity in which lodges
have another mechanism for coupling wings. the phallosome. The hypandrium varies from a
 Bark-Lice, Book-Lice or Psocids (Psocoptera)
B 387

broad shield, varying from slightly convex and resembles it in appearance. The external valvulae
weakly sclerotized to a strongly convex and heavily are attached to the surface of the base of the dorsal
sclerotized, and bearing apophyses of different valvulae, and commonly are broad and setose. The
kinds. The phallosome (Figs.15 and 16) comprises spermapore (female gonopore) opens between
the endophallus, the parameres and the aedeagus. the gonapophyses in the 9th sternite. Sometimes
The endophallus is a membranous structure which the cuticle around the spermapore is heavily scle-
is everted during copula. Its surface is adorned rotized to form a distinct plate (spermapore plate).
with small sclerites (radulae). The parameres are The internal structure of psocids resembles
symmetrical, sclerotized structures with small that of other insects. The tracheal system usually
pores sensilla on the distal end. From each opens to the exterior by means of two pairs of
paramere an inner branch often protrudes; these thoracic and eight pairs of abdominal spiracles.
branches are fused apically, forming a sclerotized Four Malpighian tubules are attached at the posterior
arch (the aedeagus). end of the midgut. The nervous system is very simple
Female genitalia comprise, in the majority of and comprises the following ganglionar centers: brain,
species, a subgenital plate, one pair of gonapophyses subesophageal ganglion, prothoracic ganglion,
from the 8th segment (ventral valvulae), two pairs pterothoracic ganglion and the abdominal ganglion.
of gonapophyses from the 9th segment (dorsal val- The reproductive system in females comprises two
vulae and external valvulae), the modifications of ovaries, each with three to five polytrophic ovarioles,
the 9th sternite around the spermapore, and the lateral oviducts which open into a larger median
spermatheca or receptaculum seminis (Fig.17). duct, and a spermatheca. In the males the testes are
The subgenital plate is a extension of the 8th stern- round or three-lobed.
ite; commonly it is a large broad plate having the
apical margin rounded. However, in many groups a
pronounced median posterior lobe is present Systematics
which has (Fig.17) been termed the egg guide.
The ventral valvulae are shorter than the others, Living Psocoptera are divisible into three well-
glabrous, and apically pointed. The dorsal valvulae defined suborders: Trogiomorpha, Troctomorpha
run parallel to the ventral valvulae, and sometimes and Psocomorpha. The earliest fossils from the

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 15 Male terminalia of Mesopsocus unipunctatus.

388
B Bark-Lice, Book-Lice or Psocids (Psocoptera)

Lower Permian of Kansas, regarded as Psocoptera

by some authors, differ from modern species in
wing venation and mouthpart characters. Thus,
they have been placed in a distinct suborder,
Permopsocina. The Trogiomorpha contain the
most primitive forms, and the Psocomorpha the
most advanced.

Suborder: Trogiomorpha

Diagnostic characters of Trogiomorpha are as

follows: antennae with more than 20 segments;
hypopharyngeal filaments separate, never fused
Bark-Lice, Book-Lice or Psocids (Psocoptera), on midline; tarsi of the adults 3-segmented; labial
Figure 16 Phallosome of Elipsocus sp. palps 2-segmented; pterostigma not thickened

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 17 Female terminalia of Metylophorus nebulosus in

lateral view (a); detail of the gonaphyses of Metylophorus nebulosus (b); detail of the subgenital plate of
Metylophorus nebulosus (c).
 Bark-Lice, Book-Lice or Psocids (Psocoptera)
B 389

or absent; and paraprocts with strong posterior (Psyllipsocidae) are exclusively found in domestic
spine. situations. Lastly, the Prionoglarididae are a small
This suborder (Fig.18) contains five families family containing three genera (Prionoglaris from
into two family groups: Atropetae (Lepidopsocidae, the Palaearctic, Speleketor from the United States
Trogiidae and Psoquillidae) and Psocatropetae (Psyl- and Sensitibilla from Namibia) and seven species.
lipsocidae and Prionoglarididae). Lepidopsocidae The members of these families live almost exclu-
(the major family of the suborder) form a primar- sively in caves or under stones.
ily tropical group of bark- and leaf-litter inhabit-
ing forms recognized by their moth-like appearance
caused by the scales that cover their body and Suborder: Troctomorpha
wings. Trogiidae comprise species with reduced
wings (apterous or brachypterous); this cosmopoli- Characters of Troctomorpha (Fig.19) are: antennae
tan family includes several domestic species, in par- with 1415 segments, rarely with fewer segments
ticular Lepinotus sp., which causes great infestations (the only exception is the Palaearctic genus Nephax
in granaries and warehouses. Psoquillidae and Psyl- which possess antennae of 13 segments), the flagellar
lipsocidae are both small and widely distributed fami- segments beyond the fifth usually with secondary
lies. Psoquillids are commonly found on bark annulations; hypopharynx with filaments separated
whereas Psyllipsocids occur in caves or leaf-litter. only in distal region; tarsi 3-segmented; labial palps
Both families include some domestic species; for 2-segmented; forewing, when present, lacking scle-
instance, some species of the genus Dorypteryx rotized pterostigma.

Bark-Lice, Book-Lice or Psocids (Psocoptera),

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 19 Liposcelis bostrychophila
Figure 18 Trogium pulsatorium (Trogiomorpha). (Troctomorpha).
390
B Bark-Lice, Book-Lice or Psocids (Psocoptera)

This suborder contains eight families in two

family groups: Amphientometae (Musapsocidae,
Troctopsocidae, Manicapsocidae, Compsocidae
and Amphientomidae) and Nanopsocetae (Lipos-
celididae, Pachytroctidae and Sphaeropsocidae).
The largest families in this suborder are the
Liposcelididae (near 150 species), Amphiento
midae and Pachytroctidae. The Liposcelididae are a
cosmo-politan group of apterous psocids (although
a few species possess reduced wings) whose mem-
bers are recognized by their small size (12 mm)
and their greatly enlarged hind femora. The family
includes a number of common booklice (Liposcelis
spp.) found in houses, warehouses and ships holds
where they may cause measurable weight loss and
quality deterioration in stored grain. Some authors
concluded that Liposcelis spp are secondary pests of
grain whose diet is supplemented by mold. Outdoor
species occur in leaf-litter and under bark. The
other families are mainly tropical, occurring in both
the Old and the New World. Bark-Lice, Book-Lice or Psocids (Psocoptera),
Figure 20 Lachesilla pedicularia (Psocomorpha).

Suborder: Psocomorpha
S tenopsocidae and Amphipsocidae. The Caecil-
This suborder is characterized by possessing ante- iusidae are one of the largest families of Psocop-
nnae with 13 or fewer segments, never with secondary tera, with nearly 400 known species. It is a family
annulations. The labial palpus is 1-segmented, of worldwide distribution, in which most species
lacking-basal segment. The hypopharynx has are foliage dwellers. Amphipsocidae (150 species)
chitinous filaments separated in posterior region. are a large family widely distributed in the Old
The forewings usually are present, with sclerotized World (a few species can be found in the
pterostigma. Adults have 2- or 3-segmented tarsi. Americas); these psocids are generally found on
This very large suborder contains nearly 80% broad-leaved foliage. The group Homilopsocidea
of all known species of Psocoptera. It consists of was erected to hold those families which could
23 families, in four family groups: Epipsocetae not easily be associated with families in the other
(Epipsocidae, Dolabellopsocidae, Ptiloneuridae family groups. The result is a heterogeneous
and Cladiopsocidae). Epipsocidae are the largest assemblage of 11 families (Lachesillidae, Ectopso-
family of this group with 133 described species, cidae, Peripsocidae, Calopsocidae, Pseu-docaeciliidae,
mostly tropical and subtropical in distribution. Bryopsocidae, Trichopsocidae, Elipsocidae,
In some species, females are apterous or brac- Philotarsidae, Mesopsocidae and Archipsocidae).
hypterous. Most species live in particularly damp Most of these families are of cosmopolitan
situations: under stones, in caves, on dead distribution and can be found forming part of the
branches in humid forests, or in damp leaf litter. psocid faunas around the world. Lachesillidae
The family group Caeciliusetae comprises the consist of more than 250 species (most of them
following families: Asiopsocidae, Caeciliusidae, living in the Americas), primarily found in dry
 Bark-Lice, Book-Lice or Psocids (Psocoptera)
B 391

foliage. Some species (e.g., Lachesilla pedicularia) Simultaneously, males vibrate the wings or, in
are widely distributed, occurring in granaries, apterous species, vibrate the antennae. Courtship
warehouses and human habitations, occasionally requires a variable time (220 min) and is followed
in great numbers. Ectopsocidae and Peripsocidae by mating. The male approaches the female from
are two closely related families, and are cosmo- the side or from behind, passes over her in a
politan in distribution (although Peripsocidae forward direction, then backs underneath, and
are more diverse in the Oriental region). Some copulation ensues. The copulation has a variable
species of Ectopsocidae (Ectopsocus briggsi) and duration, ranging from the 510 s (as observed in
Trichopsocidae (Trichopsocus clarus) are commonly Stenopsocus stigmaticus) to 24 h in the Trogiidae.
found on fruit-bearing trees, and possibly are Copulation length depends on the degree of
involved in the transmission of pathogenic fungi. complexity of the genitalia, and the sperm trans-
Pseudocaeciliidae and Archipsocidae are mainly mission mode. In the species with extremely short
tropical groups. Some species of Archipsocidae copulation, the terminalia are very simple and
live in massive aggregations under sheets of little sclerotized in both sexes. Also, the spermato-
webbing that may cover an entire tree. Philotar- phore is directly deposited on the atrium from
sidae live on bark or low vegetation. Members which the sperm is transferred to the spermatheca.
of this family can be found around the world In other species the coadaptation of the genital
but are especially common in the Oriental apparatus is more intense, which explains the long
region. Elipsocidae and Mesopsocidae are bark duration of copulation. In the Atropetae and the
inhabitants, and also may be found in many Amphientometae, sperm are transferred in a liquid
types of bushes. Both families are abundant in medium into the spermatheca within a structure
temperate regions. called a sperm packet. This structure apparently
Lastly, the family group Psocetae consists of is formed by glandular secretions of males and
four families (Psocidae, Psilopsocidae, Myopsoci- females, a process that lengthens the duration of
dae and Hemipsocidae). Psocidae are the largest the copulation.
family in the order with near 600 known species.
It is a cosmopolitan group of psocids which are, in
a general way, darkly colored and live on bark or, Eggs, Oviposition, Hatching, Viviparity,
occasionally, on the ground or under stones. Parthenogenesis
Myopsocidae (near 150 species) are large, tropical
Psocoptera living on bark. The members of this Eggs of Psocoptera are often simple, elongate
family usually have densely spotted brown wings. ovoids or cylinders without a micropyle, and usually
are smooth, lacking any conspicuous sculpture. In
the more primitive psocids, however, eggs have
Reproductive Biology pronounced areolate folds or a crest on the upper
surface. Observations on psocid eggs allow us to
Courtship and Mating recognize four categories of egg deposition:

Many observations of courtship in various species 1. Eggs laid bare: (a) webbed, (b) not webbed.
of psocids show that elaborate behavior patterns 2. Eggs encrusted with material from the digestive tract:
may be involved, and that behavioral differences (a) webbed, (b) not webbed.
may constitute effective isolating mechanisms for
closely related species. In a general way, mating it There is a systematic and an ecological basis for
is preceded by the male nuptial dance, in which the pattern of egg deposition. Thus, species which
the male describes circles around the females. are open bark inhabitants (as Psocidae) lay
392
B Bark-Lice, Book-Lice or Psocids (Psocoptera)

unwebbed encrusted eggs, whereas leaf inhabiting dance by the males, which eventually results in
species (Caeciliusidae, Pseudocaeciliidae) usually copulation. Meanwhile, the parthenogenetic
lay bare, webbed eggs. females remain indifferent. This incompatibility
Batch size varies considerably, but egg number of the races within the same species could be the
is constrained by the fact that two follicles mature rule in all Psocoptera possessing such biologic
in each ovariole at once, thus imposing a maximum races, driving reproductive isolation of the races.
batch size (for example, 12 eggs in Graphopsocus; This ultimately can be responsible for speciation.
16 in Caecilius and Stenopsocus, and 20 in Ectopsocus More recently, in the common domestic psocid
briggsi). However, larger batches are occasionally pest Liposcelis bostrychophila dense concentra-
laid by such species (32 eggs in the first batch of an tions of small bacterial inclusions have been
individual of Graphopsocus cruciatus). This is a found. These bacteria are tentatively identified as
rare phenomenon, but occurs because the presence Wolbachia, a genus implicated in changes in
of two eggs in an ovariole does not inhibit matura- reproductive function (in which parthenogenetic
tion of further follicles. reproduction is included) in many other insect
Hatching is accomplished with the aid of a groups.
specialized egg burster on the frontal region of the
pronymph. This egg burster has the form of a blade
or tooth, or a row of several spines. By pushing Postembryonic Development
this structure against the egg cuticle, the pro-
nymph creates a hatching orifice, and the nymph The juvenile instars of psocids (nymphs) gener-
is partially extruded through this orifice. The first ally resemble adults in body form and markings.
instar then emerges from the pronymphal cuticle They lack functional ocelli, never have more than
attached to the hatching orifice. two tarsomeres, and early instars have fewer
Viviparity is an unusual habit in the psocids. flagellomeres than adults of their species.
Only a few species are known as viviparous. In the Nymphs of some genera of the families Troctop-
best-known viviparous genus of psocids (Archip- socidae, Psocidae and Myopsocidae have gland
socopsis), females lack gonapophyses and the hairs, which in some cases retain bits of debris,
abdomen may contain more than a dozen embryos thus forming a camouflaging coat over the body
in different stages of development. Eggs remain in surface. The usual number of nymphal instars in
the ovarian tubules and pass down the common psocids is six for the two sexes, but this can be
oviduct to the exterior. reduced to five (micropterous form of Psyllipsocus
Parthenogenesis in psocids is widespread. The ramburii), four (apterous females of Embidopsocus
usual form of parthenogenesis is obligatory enderleini) or, more rarely, three (apterous males
thelytoky, although a few examples of facultative of Embidopsocus enderleini). The reduction of
thelytoky are known. This mode of reproduction instars number is frequently associated with alary
is known in at least 12 families, representing all polymorphism, in which some species with sexual
three suborders. However, the situation actually is alary dimorphism differ in instar number between
more complex, as demonstrated by Caecilius sexes: the apterous sex having one less instar
flavidus and Psocus bipunctatus (two European than the macropterous one. Also, the reduction
species). These species consist of two races, one of the number of larval stages is generally
bisexual and other parthenogenetic. Females of regarded as a case of neoteny, and associated
the parthenogenetic race in the presence of males with the reduction of other characters (lack of
of the bisexual race provoke no reaction from the ocelli, only two tarsomeres and reduction in
males, whereas the introduction of a female of the numbers of ctenidiobothria and paraproct
bisexual race is immediately followed by a nuptial trichobothria).
 Bark-Lice, Book-Lice or Psocids (Psocoptera)
B 393

Feeding various psocid species of the genera Lachesilla,

Lepinotus, Liposcelis, Ectopsocus or Rhyopsocus.
Psocids are herbivores or detritivores, feeding on Other organisms parasitizing psocids are
microflora and organic debris on the surface of nematodes that live in the abdominal cavity, and
vegetation and other substrates. They are among fungi of the order Entomophtorales (species of the
a relatively small number of insects that actively genus Erynia).
exploit these food resources (according to some
authors, the psocids together with the Collem-
bolans constitute the guild of epiphyte grazers). Parasitoids
The primary components of their diet are green
algae of the genus Pleurococcus, lichens (espe- The parasitoids of psocids are Hymenoptera
cially corticicoles and lapidicoles) and fungal attacking both eggs and nymphs.
spores and hyphae. Although it is common to Parasitic Hymenoptera that attack the eggs
find pollen grains in their alimentary tract belong to the genus Alaptus (Mymaridae), and
(mainly of coniferous trees), detritus of all types include several species. In general, only a few eggs
and even remains of dead arthropods (probably of each batch are parasitized, and each egg contains
already in decomposition) are consumed. A few only a single individual of Alaptus. Some studies
psocids are partial predators, taking insect eggs reveal that the proportion of parasitized eggs
and possibly scale insects. The differences in the varies between 610% although in some species of
diet depend on the habitat occupied by the Mesopsocus, proportions of 2070% have been
species. For example, the bark-inhabiting psocids observed. Parasitic Hymenoptera attacking the
feed on pleurococcine algae and lichens. Leaf- nymphs belong to the genus Leiophron (Braconidae:
inhabiting psocids feed primarily on small leaf Euphorinae). The proportion of parasitized
fungi, and often ingest small amounts of leaf nymphs is sometimes 5060%, as has been
tissue with the fungal hyphae. Domestic psocids reported in some populations of Caecilius flavidus
feed on mold that develops on the organic matter studied in England.
found on furniture in dwellings, and on the rotted
wood and the old papers found in basements.
Psocids that live in the kitchens of houses become Ectoparasites
consumers of stored food (flour, cereals, rice,
bags of tea, etc.). The presence of larvae of Acari (genus Hauptman-
nia) living as ectoparasites on psocids has been
mentioned. Some phoretic Acari (Phytoseiidae)
Natural Enemies attached to larvae of psocids have also been
described.
Parasites

The intestine of most species contains gregarines Predators

(Protozoa) fixed to the intestinal wall. These
gregarines are also found in the feces, and can The main predators of psocids are arthropods and
infect other individuals. vertebrates. Among the arthropods, numerous spe-
Psocids have been mentioned occasionally cies that feed on eggs, nymphs or adult psocids have
as intermediary hosts of tapeworms (Cestoda). been reported. For example, several arachnids
Cestode larvae of the genera Thysanosoma, (Acari, spiders, Opiliones, pseudoscorpions) and
Thysaniezia and Avitellina, have been found in numerous representatives of various orders of
394
B Bark-Lice, Book-Lice or Psocids (Psocoptera)

insects (Dermaptera, Heteroptera, Neuroptera, Some authors suggest the existence of mim-
Hymenoptera [ants], Diptera and Coleoptera) are icry in some species. The best example is the case
known. The main vertebrate predators on psocids of Chelyopsocus garganicus, which resembles a
are birds. Many bird species include psocids in their beetle, a less consumable species.
diet, although they represent only a small fraction
of the total insect captures: 1.5% in the diet of swifts
(Apus pallidus) that hunt flying insects, or 3.6% in Dispersal
the diet of treecreepers (Certhia) and nuthatches
(Sitta) that hunt on the trunks of trees. Interchange of psocids between different habitats,
Occasionally, predation by reptiles has been and extension of habitat or geographical range,
mentioned, as in the case of an arboricolous occurs frequently and may result from one or more
lizard in Chile. of three interrelated forms of dispersal. These are:

1. Aerial dispersal by flight, as revealed by the abundance

Defense Mechanisms and frequency of catches in aerial traps (suction traps or
Malaise traps).
Most psocids possesses features or develop 2. Passive dispersal. Psocids, like many other small
behaviors to avoid parasites and predators. These insects, frequently become incorporated in the ae-
defense mechanisms can be included in several rial plankton after active take-off, and may be trans-
categories: ported over considerable distances. On the other
First, defense by hiding is called crypsis. Among hand, phoresy of psocids on vertebrates has been
psocids, many examples can be recognized: eggs observed. Psocids have been recovered from the
covered with silk and detritus helps reduce detec- plumage of several species of birds, and from rats,
tion, nymphs with glandular hairs covering the body chinchillas, puppies and humans.
surface to which detritus adheres, and both adults 3. Hitchhiking in vehicles or cargoes. This method is pro-
and nymphs with color patterns matching the sub- bably responsible for the broad occurrence of many
strate where they live. Protective coloration has been domestic species. In fact, most of them are cosmopoli-
well studied in British populations of the species tan despite being flightless.
Mesopsocus unipunctatus, providing a case of indus-
trial melanism for this species (the darker individu-
als are more frequent on trees near industrial areas Ecology
as a consequence of differential predation by birds).
On the other hand, some cases of mechanical Habitats
defenses are known: the ability of the Liposcelidiidae
to run backward swiftly, the surprising jumping Psocids occupy a wide range of habitats,
abilities of some species (Dorypteryx, Psocathropos, although the various habitat categories of psocids
and the females of Cyrtopsochus), or the partial intergrade substantially. The following ecological
autotomy of the antennal flagellum as have been categories hold for a great majority of psocids:
observed among some species, such as Prionoglaris
stygia. Some species combine two defense methods.
For example, Hemineura bigoti blend in well with Trees and Shrubs (Foliage-Frequenting and
dried Genista bushes, but H. bigoti also shows a Bark-Frequenting Psocids)
hiding behavior that consists of revolving around
the Genista shoots, thereby keeping out of sight of Most psocids live on trees and bushes, but not all
possible predators. occupy the same parts of the plant. So, in a general
 Bark-Lice, Book-Lice or Psocids (Psocoptera)
B 395

way, we can consider two categories of psocids: towards alary polymorphism. The principal
foliage-frequenting and bark frequenting. psocid group of this category is the family
The foliage-frequenting habitat has been Liposcelididae.
adopted by relatively few species, but some groups
use this habitat. Some of them contains species
that live on live leaves. The claws of most of these Low Vegetation
species lack a preapical tooth, and the pulvillus is
broad. With the aid of this pulvillus, psocids moves Some species have a clear preference for low
without problems onto flat leaf surfaces. Also, the vegetation (herbaceous or woody). This fauna is
presence of abdominal vesicles in some species typically found in those ecosystems where low
guarantees adherence that is particularly effective vegetation predominates (heathers, brooms, gorses,
against the action of the wind. Other psocids that thyme, grasses and herbs). Some examples of true
can also be considered foliage inhabitants are grass-frequenting psocids are Asiopsocus meridi-
those that live on dead leaves, including those that onalis in semi-arid regions of Spain, Peripsocus
remain attached to the trees, as well as those that alboguttatus on heaths in southern Britain, or Cae-
fall to the ground. This habitat (the dead leaves) cilius antillanus in Brazil.
harbors an epiphytic microflora that is attractive
to some psocids (members of the families Lache-
sillidae and Ectopsocidae). For example, several Litter
Brazilian Lachesilla species appear to be closely
associated with palm foliage, and their numbers Psocoptera are a small portion of the active
are considerably greater on dead foliage than on mesofauna of litter and are encountered in litter
living fronds. In general, psocid abundance tends habitats in many parts of the world. However,
to be greater on dead foliage than on living foliage distribution of litter Psocoptera is extremely vari-
if the two types are available together. able. For example, in northern temperate regions
Most of the psocids living on trees are bark- only a small part of the total psocid fauna is
frequenters. In fact, in some areas, psocids are the found in this habitat, whereas in the southern
most abundant animals found feeding on bark temperate zone of South America (Chile), edaphic
surface microfloral communities. Some families Psocoptera may be more diverse than arboreal
are almost exclusively found on this habitat (Pso- species. Traditionally, the litter psocid fauna has
cidae, Myopsocidae, Mesopsocidae, Peripsocidae been included in three ecological categories:
and Philotarsidae). In these species, the shape of
the claws is different: the claws possess a preapical 1. Primary litter dwellers. These species spend their
tooth and the pulvillus is, in general, setiform and entire life in the litter, and do not frequent other
with the apex pointed, which favors the attach- habitats. Species typical of this category are Lepino-
ment to a surface more or less rough. Among the tus reticulatus and many species of Liposcelis.
psocids living in barks and trunks, an important 2. Secondary litter dwellers. These species have ge-
group is the subcortical psocids, which live under nerations in two distinct habitats each year, with
the bark, where they find food and protection. at least one being in the litter. Some species that
They show morphological adaptations for could be included in this category carry out seaso-
subcortical existence: extreme dorsoventral nal local migrations from the litter onto trees and
flattening with legs inserted laterally, apterism or vice versa. For example, in a Mediterranean species
somewhat thickened forewing held flat on the (Hemineura sclerophallina) the edaphic populations
abdomen (rather than in a more vertical position are composed only of nymphs, with a peak during
of other arboreal psocid) and a strong tendency July, while the nymphal populations on trees have a
396
B Bark-Lice, Book-Lice or Psocids (Psocoptera)

peak during October (adults are found exclusively Bird and Mammal Nests
on plants). The edaphic populations are restricted
to the dry season when the humidity conditions are, Psocids frequently have been reported from mam-
presumably, more suitable for psocids in leaf litter mal and bird nests. For ground-nesting mammals,
than in trees. the psocids are primarily leaf-litter species, while
3. Casual litter dwellers. These species do not normally for tree-nesting species the psocids usually are
breed in litter, but are present intermittently as a re- those occurring on bark. Psocids are common
sult of falling from trees. inhabitants of bird nests, because psocids find
favorable conditions in the bird nests. The associa-
Generally, the bulk of primary litter dwellers tion between psocids and the birds in the nest is
belong to the more primitive suborders, while not parasitic because the psocids feed on the
Psocomorpha are relatively rare in this role. microflorae that grow on the nest material. Most
species of psocids living in bird nests are apterous
or micropterous and are members of the families
Rock Surfaces Trogiidae, Liposcelididae and Ectopsocidae. Less
frequently, some psocids species live inside the
A few psocids appear to have become specialized nests of other insects. For example, Liposcelis
for dwelling on the surface of rocks. This category formicaria and Liposcelis myrmecophila occur in
includes species that are located under the stones ant nests, Lachesilla pedicularia is found in nests of
on soil, as well as species living on the stones of wasps of the genus Polistes, and numerous species
walls (for example, on the walls of old houses). In of psocids have been reported in the hives of
Europe, members of the families Psocidae, Myo- honey bees.
psocidae, and Peripsocidae such as Psocus bipunc-
tatus, Neopsocus rhenanus, Myopsocus eatoni and
Peripsocus subfasciatus are habitually found in this Domestic Habitats
habitat type, although most of such species have
broader habitats, either in the litter or on bark with Among the Psocoptera, a considerable number of
similar lichen or algal associations. species (predominantly Trogiomorpha and Troc-
tomorpha) occur in houses and other buildings,
Caves feeding mainly on fungal hyphae, spores of
molds, and on green algae. Psocids are common
Nymphs and adults of psocids are regularly found inhabitants of domestic environments such as
in caves. Psyllipsocidae (in Europe the most humid rooms, basements, damp walls and room
common psocid in caves is Psyllipsocus ramburii) partitions. Psocids are commonly associated with
and Prionoglarididae are perhaps particularly char- products in food stores, granaries, warehouses,
acteristic of caves. Some authors hypothesize that railway boxcars and ships holds. Many species
the hypogean fauna (from caves and similar habi- seem to be exclusively domestic, including some
tats) had a remote origin in Cretaceous tropical for- species of the genus Dorypteryx, Ectopsocus and
ests. These forests disappeared during the early Liposcelis (Liposcelis mendax is frequently encoun-
Tertiary, as a consequence of climatic change, and tered in rice). Psocids are usually not seriously
the fauna moved to colonizing some subterranean unhygienic, causing only minor problems of
habitats. In the case of psocids, it has been suggested contamination and allergies. Their principal dam-
that the Psyllipsocidae (an ancient group) may have age to buildings is their effect on property values:
survived by avoiding competition with more recent lawsuits resulting from the presence of psocids
forms by inhabiting caves or similar habitats. often prove costly. For example, in a Spanish
 Bark-Lice, Book-Lice or Psocids (Psocoptera)
B 397

coastal town, three species of psocids were involved Substrates and Plant "Preferences"
in spreading infestation of the alga Pleurococcus
on recently constructed buildings, and were the Psocids are not strictly phytophagous because they
basis of a legal conflict. feed on the microflora that grows on the plants.
However, occasionally they show a certain speci-
ficity toward their substrate plant. In a general
Ecological Distribution way, this specificity refers to groups of plants. For
example, among the foliage-frequenting psocids, a
Altitudinal Distribution marked division exists among those that live on
conifers and those that live on broad-leaved trees.
Although some psocid habitats are distributed Also, they are more frequent on plants with rough
over a wide altitudinal range, many of the psocids leaves (Ulmus spp.), or with small leaves that are
present are usually limited to a part of this range. easily moved by the wind (Betula spp.). However,
In the most comprehensive work concerning alti- among the bark-frequenting species this specific-
tudinal distribution of psocids, only two of 53 spe- ity is less marked. The ecological conditions of a
cies of psocids found on mango (Mangifera indica) site that favors a type of vegetation can be more
in Jamaica were found throughout the plants alti- important for psocids than the presence or absence
tudinal range of 1501,200 m. An altitudinal zona- of certain substrate plants. In central Spain, some
tion of psocids has also been observed in central well defined psocid communities have been found,
Spain between a range of 9001,700 m. In this in particular those that live in the Spanish juniper
case, of the 15 species studied, three showed pref- forests (Juniperus thurifera) and in the Scots pine
erences for the low altitude, four were distributed forests (Pinus sylvestris), suggesting that changes
mostly at high altitudinal levels, while the remain- in structure and composition of psocid communi-
der were distributed throughout the altitudinal ties can be determined by both climate and vege-
range. The same has been observed in Swiss tation types. Psocid faunas inhabiting different
National Park; only 14 of 55 species were taken in plant species are affected by taxonomic related-
the upper alpine zone (above 1,900 m) and 24 were ness and by architectural similarities among the
not found above the montane level (to 1,500 m). substrate plant species. For example, there are dis-
So, from the available data, psocids can be classi- crete faunal communities on shrublands (Cistus
fied into three altitudinal groups: sp., Rosmarinus sp., and Genista sp.), junipers
(Juniperus thurifera, J. sabina, J. comunis is J. oxyce-
1. eurytopic species, found over most of the range. drus), pines (Pinus pinaster, P. nigra, P. halepensis,
2. low altitude stenotopes, restricted to lower eleva- P. sylvestris) and oaks (Quercus faginea, Q. pyrena-
tions. ica, Q. rotundifolia).
3. high altitude stenotopes, found at higher elevations
only.
Humidity
Although data are not available from most parts of
the world, it seems that individuals at the upper The thinness of the integument of psocids (partic-
end of an altitudinal gradient may be larger than ularly in the nymphs) is responsible for the fact
those lower down. In Jamaica, there was a linear that most psocids are very susceptible to desicca-
increase in the size of females of Pseudocaecilius tion. This means that relative humidity is a limit-
citricola and Hemipsocus roseus with increasing ing factor to psocids and that, therefore, high
altitude. This tendency is probably due to temper- humidity is desirable. Psocids can ingest water
ature gradients. with the food or, exceptionally, as liquid, but it is
398
B Bark-Lice, Book-Lice or Psocids (Psocoptera)

generally insufficient to prevent desiccation. How- particularly favorable (namely Lepinotus and Lipo-
ever, psocids are able to actively take up water scelis). In general, they have been assumed to cause
from the atmosphere. This process (this is not little damage, but the observations on some spe-
exclusive of psocids because it is also found in cies of Liposcelis that cause primary damage to
some Mallophaga) is carried out with the mouth- stored grain indicate that some species may cause
parts. The lingua bears a pair of ventral sclerites) direct economic loss. On the other hand, although
which are connected to the median sitophore domestic psocids are generally only contaminants,
sclerite by ligaments; these lingual sclerites are the appearance of some species in large numbers
capable of taking up water from the atmosphere can cause a direct damage to insect collections,
and driving it by means of the tubular filaments herbaria, older books and animal products. Most
into the alimentary tract. of these species (genus Liposcelis) are difficult to
eliminate because they can survive without food
and tolerate unfavorable conditions of tempera-
Psocids and Humans ture and relative humidity, recovering their nor-
mal activity once the environmental conditions
In general, psocids are of little economic and become favorable. Also, as a consequence of the
health importance to man. Occasionally they may parthenogenetic mode of reproduction in many of
cause human health problems such as skin dis- these species, they are able to multiply in an explo-
eases or scalp infestations. The dead bodies of sive way and to expand their population very
some domestic psocids in household dust are quickly. Some authors suggest maintenance of rel-
responsible for allergies and asthmatic attacks. ative humidity of less than 50% with temperatures
Also, several species of psocids serve as intermedi- of 15C or less, in order to retard development and
ate hosts of some cestodes, particularly of the slow the increase in populations. However, though
fringed tapeworm of sheep. Psocids also have such measures may be feasible in temperate
been revealed to be disease vectors on plants. For regions, they are likely to prove extremely difficult
example, Ectopsocus briggsi may occasionally in many tropical areas. Other control measures
disseminate fungal pathogens on fruit-bearing include the use of insecticides in varied forms; one
trees by leaving viable spores in feces deposited on of the most widely used is pyrethrin dust.
uninfected sites. As mentioned previously, three
species of psocids were involved in spreading
infestation of the alga Pleurococcus on recently References
constructed buildings.
Some species of psocids can be considered to Lienhard C (1998) Psocoptres Euro-mditerranens. Faune
be pests. Among the psocids occurring out-of- de France, 83. Federation Franaise des Socits de
doors, the large webs of Archipsocidae have occa- Sciences Naturelles (ed) Paris, France, 517 pp, 11 plates
Mockford EL (1993) North American Psocoptera (Insecta).
sionally required removal due to their unsightliness. Flora and fauna handbook 10. Sandhill Crane Press,
Those of Archipsocus nomas in Florida, for exam- Gainesville, FL, 455 pp
ple, are sometimes removed by scrubbing larger New TR (1987) Biology of the Psocoptera. Oriental Insects
branches and trunks of trees with oil emulsions. In 21:1109
Smithers CN (1972) The classification and phylogeny of the
Europe, the species Lachesilla pedicularia can form Psocoptera. Aust Mus Memoir 14:1351
dense clouds that are a temporary nuisance. How- Smithers CN (1990) Keys to the families and genera of Pso-
ever, most of the psocid species that become pests coptera (Arthropoda: Insecta). Tech Rep Aust Mus
2:182
are domestic species. Most of the domestic pso-
Smithers CN, Lienhard C (1992) A revised bibliography of
cids occur in large numbers in houses or stored the Psocoptera (Arthropoda; Insecta). Tech Rep Aust
products when the environmental conditions are Mus 6:186
 Bates, Henry Walter
B 399

Thornton IWB (1985) The geographical and ecological distri- Bat Bugs
bution of arboreal Psocoptera. Ann Rev Entomol
30:175196
Members of the family Polyctenidae (order
Hemiptera).
Barley Thrips, Limothrips Bugs
cerealium (Haliday)

A thrips (Thysanoptera) pest of some grasses,

including wheat. Bates, Henry Walter
Wheat Pests and Their Management
Thrips Henry Bates was born in Leicester, England, on
February 8, 1825, and developed an early interest
Basal in entomology. At the age of only 17 or 18 he
published notes on Coleoptera in the Zoologist.
A term used to refer to the base or point of attach- At about the age of 20, he met Alfred Russel Wal-
ment, or the portion of the appendage nearest the lace, who was then teaching English in a school
main body. in Leicester and had an interest in botany.
Through the influence of Bates, Wallace began to
collect beetles. In 1847, Wallace proposed a trip
Basalare to Par, Brazil, to collect insects and other natu-
ral history objects, having read W.H. Edwards
A small section above the principal pleuron, anterior Voyage up the Amazon. These two explorers,
to the wing, to which flight muscles are inserted. together with Bates brother, sailed from Liver-
pool for Par in April 1848. They intended to
Base Pair (bp) support themselves by the sale in Europe of natu-
ral history objects that they expected to collect in
Two nucleotides that are in different strands of Brazil. Many hardships followed. These included
nucleic acid and whose bases pair by hydrogen his affliction with yellow fever, the death of Bates
bonding. In DNA, adenine pairs with thymine and brother, and the loss at sea of Wallaces first col-
guanine pairs with cytosine. lection of natural history objects. Nevertheless,
he persevered (Wallace traveled separately after
the first 2 years, and departed from Brazil years
Basement Membrane sooner than Bates), and assembled large collec-
tions, including over 14,500 species of insects, of
A noncellular layer that separates the epidermal
which 8,000 were new to science during the 11
cells from the hemolymph. This membrane is the
years that he spent in Brazil. He returned to Eng-
innermost layer of the integument.
land, worked on the specimens he had collected,
Epidermis
and published. In 1861 his paper Contributions
Cuticle
to an insect fauna of the Amazon Valley; was
read before the Linnean Society. It explained
Basic Reproductive Rate mimicry (see Batesian mimicry). In 1863, his
two-volume book A naturalist on the river Ama-
(R0) The average number of offspring produced by zons; was published by John Murray with an
a population of individuals over the entire course introduction by Charles Darwin, to great acclaim.
of their life. These works resulted in his being offered the job
400
B Batesian Mimicry

of assistant secretary to the Royal Geographical environmentalism. His books include (1949) The
Society in 1864. This at last freed him from finan- natural history of mosquitoes, (1950) The nature
cial worry, but reduced the time available for him of natural history, and (1955) The prevalence of
to work on his Amazonian insects. He later con- people. He died on April 3, 1974.
tributed (18811889) volumes to the series
Biologia Centrali-Americana;, published
numerous other works, and was twice president References
of the Entomological Society of London. He died
on February 16, 1892. Anon (2002) Marston Bates. Available at http://www.
netwalk.com/~vireo/bates.html. Accessed Aug 2002
AN Marquis Company (1968) World whos who in science.
AN Marquis Company, Chicago, IL
Today in Science History (2002) Marston Bates. Available
References at http://www.todayinsci.com/7/7_23.htm. Accessed Aug
2002

Sharp D (1892) Henry Walter Bates, F.R.S. Entomologist

25:7780
Woodcock G (1969) Henry Walter Bates. Naturalist of the
Amazons. Fader and Fader, London, 269 pp
Bat Fleas

Members of the family Ischnopsyllidae (order

Siphonaptera).
Fleas
Batesian Mimicry

Resemblance of a palatable insect to a less palat-

able one, a process that benefits the palatable Bat Flies
mimic by reducing predation.
Mimicry Members of the families Streblidae and Nycteribi-
idae (order Diptera).
Flies
Bates, Marston

Marston Bates was born in the state of Michigan, B Chromosomes

USA, on July 23, 1906. He graduated from the
University of Florida with a B.S. degree in 1927. B chromosomes are non-vital supernumerary
He worked for the United Fruit Company in chromosomes found in many organisms. They are
19281931. He entered Harvard University and thought to be derived from normal chromosomes,
was awarded an A.M. degree in 1933 and Ph.D. in and often transmitted at higher rates than expected,
1934. In 19351937 he worked as a research assis- thus exhibiting drive.
tant at Harvard. In 19371952, he worked at vari-
ous laboratories of the Rockefeller Foundation,
and his studies of mosquitoes in northern South Beach Flies
America contributed to an understanding of epi-
demics of yellow fever. In 19521971 he was a fac- Members of the family Canacidae (order
ulty member of the University of Michigan. He Diptera).
contributed much to ecology of mosquitoes and to Flies
 Beauveria
B 401

Beaded Lacewings is the discovery that a 25 million-year-old worker

ant embedded in amber was covered with a fun-
Members of the family Berothidae (order gus similar to present day B. bassiana isolates.
Neuroptera). The infective propagules, the conidia of Beau-
Lacewings, Antlions and Mantidflies veria, are dry, hyaline (colorless), and globose to
oval in shape (Figs.21 and 22). The conidiophores
can occur singly or can be grouped in irregular
Beak clusters or in whorls; the base of the conidiophore
is inflated or flask-shaped, with conidia borne on
A prolongation of the head, usually referring to a distinctive apical zigzag extension (rachis). Like
the snout of weevils. This term also is used to other entomopathogenic hyphomycetes, B. bassi-
describe the jointed piercing-sucking, or sucking, ana conidia initiates infection of host insects at
mouthparts of Hemiptera. the outer integument, although invasion through
the alimentary tract has been reported in certain
ants and termite hosts. Successful infection by
B. bassiana by cuticular penetration depends
Beauveria upon a number of factors. For example, younger
insects are usually more easily infected than older
Jacqulyn c. pendland, Drion g. boucias larvae. Specific Beauveria strains are infectious to
University of Florida, Gainesville, FL, USA adult insects such as grasshoppers, as well as to
insects undergoing a molt. The type of plants that
The genus Beauveria (Deuteromycota) includes the target insects consume is also important since
several entomopathogenic species, the most some plants produce compounds inhibitory to
notable being B. bassiana. Beauveria has a fungal growth. Conidial germination on a suscep-
worldwide distribution and has a wider host tible host requires optimal temperature and
range than the other Deuteromycetes infect- humidity (>75%). Conidia, for example, will not
ing insects from most orders. In addition to infect overwintering adult Colorado potato bee-
B. bassiana, three other species, including tles because the soil is too dry and cool; however,
B. brongniartii (=tenella), B. relata, and B. amor- post-emergent beetles can become infected later
pha have been identified. The latter two species in the spring when conditions are more favorable.
are South American isolates from Lepidopteran Even if conditions are optimal for the germina-
larvae and Coleoptera, respectively. Beauveria tion and penetration processes, B. bassiana
brongniartii (B. tenella), found predominantly conidia must first bind to the host cuticle after
in soil-inhabiting insects, has been described as contact has been made. Attachment, as in the case
a naturally occurring pathogen of mosquito of other fungi that produce dry conidia, is likely
larvae. Beauveria bassiana, the white muscar- due to the hydrophobicity of both the conidial
dine fungus, was observed around 900 a.d. in and cuticular surfaces. In B. bassiana, conidial
silkworms in Japan. Insects mummified by hydrophobicity can be attributed, at least in part,
B. bassiana also were used for medicinal pur- to the presence of a hydrophobin-type protein
poses, e.g., as an antiseptic for wounds and sore in the outermost rodlet layer. In addition to
throats. Importantly, itwas through a study of attachment, conidial surface hydrophobicity may
this fungus that the germ theory of disease (i.e., prevent desiccation of the propagules and aid
the idea that microorganisms could cause infec- in their dispersal. Fungal enzymes may help to
tious disease in animals) was postulated by consolidate attachment of B. bassiana conidia
A. Bassi in 1834. Also ofhistorical significance to host cuticle.
402
B Beauveria

Beauveria, Figure 21 Adult mole cricket, Scapteriscus vicinus, infected with Beauveria bassiana. Note the
external conidiospores emerging from the head, thorax, and leg regions.

Beauveria, Figure 22 Scanning electron micrograph of the conidiophore of Beauveria bassiana.

Under the proper conditions, germination of enzymes. There are several classes of enzymes
B. bassiana conidia occurs within hours. Studies produced by B. bassiana during germination,
have shown that different strains of B. bassiana including proteases, chitinases, and lipases that
produce different amounts of cuticle-degrading function in the breakdown of host cuticle.
 Beauveria
B 403

Penetration of insect cuticle (e.g., Helicoverpa tospores show both a reduction in the overall
zea) by B. bassiana germ tubes usually does not number of immunocompetent granular hemo-
involve the formation of appressoria. Once the cytes and a suppression in their abilities to spread
germ tubes penetrate the cuticular and epidermal and form filopodia.
regions, the fungus grows towards the hemocoel, In addition to being a ubiquitous soil ento-
where blastospores become evident at about 48 h mopathogen, certain strains of B. bassiana have
post-infection. In vivo produced blastospores, been reported to be endophytic and colonize
unlike in vitro cells, lack a formal cell wall and plant tissue. Unlike most insect mycopathogens,
contain a thin fibrillar layer on the plasma mem- B. bassiana has been associated with fatal respi-
brane. In Heliocoverpa zea, there is very little tis- ratory infections in some cold-blooded animals,
sue damage until 6070 h post-infection, when including tortoises, crocodiles and American
the fat body may show some signs of deteriora- alligators. One strain causes the rupture and/or
tion. The gut and Malphigian tubules can become death of fish embryos due to attachment of the
affected at 67 days, when death and mummifica- conidia to the chorion with subsequent germi-
tion also occur. However, the gut, muscle, silk nation and penetration of the fungus. A second
glands, and tracheae can remain intact during the strain tested also caused teratogenic responses,
entire infection process. Death is likely due to including abnormalities in embryos. As a result
nutrient depletion, dehydration, and/or toxin of these tests, there is some concern that large-
production by the fungus. scale applications of B. bassiana conidia could
Host response to Beauveria invasion varies, be harmful to aquatic ecosystems. Infections in
of course, depending upon the insect and its sus- the lungs and nasal passages of mammals have
ceptibility to the particular isolate used. Melanized been reported but are rare since the fungus
patches (dark spots) can occur on the cuticle at probably does not grow well at 37C; however,
the penetration site, thus indicating the induc- B. bassiana can cause allergic reactions in some
tion of phenoloxidase activity in the insect. In people.
grasshoppers injected with B. bassiana conidia, Beauveria conidia from field-collected
levels of phenoloxidase in the hemolymph were cadavers can be inoculated onto mycological
found to increase by 24 h post-treatment. After media such as SMY agar or broth and main-
topical application with conidia and penetration tained in culture by transfer at regular intervals
of the cuticle, as the fungus reaches the hemo- to fresh media. Beauveria, less fastidious than
coel, host immunoreactive hemocytes may sur- Nomurea rileyi, can be grown on oatmeal agar
round the hyphal tip and further melanization or potato dextrose media, and stored at ultra-low
reactions can occur. If B. bassiana cells become temperatures (-70C). Isolation of Beauveria
surrounded by hemocytes either via phagocytic from a soil environment may require the
and/or nodulation or granuloma-type mecha- selective media containing antibiotics such as
nisms, the fungus can still remain viable as an streptomycin, tetracycline, gentamycin and
intracellular parasite, and later emerge from the cycloheximide to eliminate bacterial growth
insect blood cells to continue growth and replica- and N-dodecylguanidine acetate (dodine) to
tion in the hemocoel and tissues. Thus, B. bassi- inhibit growth of other soil fungi.
ana can overcome host cellular defense response Due to its broad host range, including mem-
even if it has already been initiated, and as bers within the orders Lepidoptera, Coleoptera
mentioned earlier, some toxins produced by the and Hemiptera, and to the fact it is cultured eas-
fungus appear able to suppress such responses ily on inexpensive media, B. bassiana has long
(phagocytosis, nodulation) entirely. Spodoptera been targeted as a potential biocontrol agent.
exigua larvae injected with B. bassiana blas- Insect pests such as the Colorado potato beetle,
404
B Beck, Stanley Dwight

Leptinotarsa decemlineata; European corn borer, in a lumber mill for a year to save money to pay
Ostrinia nubilalis; codling moth, Laspeyresia for a university education. With those funds, he
pomonella; Japanese beetle, Popillia japonica; entered Washington State University to study
European cockchafer, Polyphylla fullo; chinch biology, and earned a B.S. degree in 1942. He
bug, Blissus leucopterus; and the European cab- then served 3 years in the U.S. navy. From 1945
bageworm, Pieris brassicae, are susceptible to to 1950 he was a graduate student at the University
B. bassiana. However, the inability to produce of Wisconsin at Madison, earning an M.S. degree
and formulate fungal propagules that are stable in 1947 and a Ph.D. in zoology in 1950. At the
and provide consistent mortality rates in con- same university, he was appointed assistant
stantly changing biotic and abiotic conditions professor in 1950, a full professor in 1964, and
has restrained large-scale development of this a distinguished professor in 1969. He taught a
mycopathogen. For example, over the years both course on insect physiology. His research inter-
B. bassiana and B. brongniartii have been targeted ests were in host-plant resistance to pests, and
to control some soil-inhabiting insects, but due insect nutrition and metabolism. His publica-
to this hypogean environment, Beauveria is tions were 138 scientific papers and several
placed in direct contact with the antagonistic books including (1963) Animal photoperiod-
soil microfauna that can be lethal or can inhibit ism and (1968) Insect photoperiodism. He
its growth. received several awards, was elected to the U.S.
National Academy of Sciences in 1988, and
served as president of the Entomological Soci-
References ety of America. His accomplishments were the
more remarkable because by 1952 he was essen-
Bing LA, Lewis LC (1992) Endophytic Beauveria bassiana tially paralyzed by poliomyelitis and was con-
(Balsamo) Vuillemin in corn: the influence of the plant
growth stage and Ostrinia nubilalis (Hbner). Biocontr fined to a wheelchair for the rest of his life. He
Sci Technol 2:3947 died on July 8, 1997, in Madison, Wisconsin,
Boucias DG, Pendland JC (1991) Attachment of mycopatho- survived by his wife, Isabel, and three of his four
gens to cuticle. In: Cole GT, Hoch MC (eds) The fungal
daughters.
spore and disease initiation in plants and animals.
Plenum Press, NY, pp 101127
Hung S-Y, Boucias DG (1992) Influence of Beauveria
bassiana on the cellular defense response of the beet
armyworm, Spodoptera exigua. J Invert Pathol
60:152158
Reference
Middaugh DP, Genthner FJ (1994) Infectivity and teratoge-
nicity of Beauveria bassiana in Menidia beryllina Wedberg J (1998) Stanley D. Beck. Am Entomol 44:127
embryos. Arch Environ Contamin Toxicol 27:95102
Pendland JC, Hung S-Y, Boucias DG (1993) Evasion of hose
defense by in-vivo produced protoplast-like cells of the
insect mycopathogen Beauveria bassiana. J Bacteriol
175:59625969 Bed

In modern agriculture, a raised area of soil into

which crops are planted (planting bed). Beds are
Beck, Stanley Dwight bounded by furrows which sometimes are used
to deliver irrigation water to the beds. In tradi-
Stanley Beck was born in the state of Oregon on tional agriculture, a bed (seed bed) is also an area
October 17, 1919, but grew up in the adjoining used to grow seedlings for later transplant into
state of Washington. As a young man he worked fields.
 Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)
B 405

Bed Bugs (Hemiptera: Cimicidae: caves where humans began their cohabitation
Cimex spp.) with the ancestral bed bug. As humans began to
practice agriculture (80005000 b.c.) within the
dini miller fertile crescent (present day Iraq), people
Virginia Tech University, Blacksburg, VA, USA moved from their cave dwellings into villages
near their agricultural fields. It has been specu-
The Cimicidae are obligate blood feeding ecto- lated that bed bugs were transported into these
parasites of humans and other animals. There are newly civilized environments, thus becoming
74 species of cimicids, including the human bed permanently associated with humans and human
bugs, bat bugs, chicken bugs, swallow bugs, and dwellings.
pigeon bugs. Cimicids are organized into 22 gen-
era and 6 subfamilies. Of the 22 genera, 12 have
evolved to feed exclusively on bats while another 9 Morphology
genera feed exclusively on birds. There is only one
genus, Cimex, which contains species that feed on Adult bed bugs are easily identified by their brown-
multiple hosts, typically specializing on birds, bats, ish red color and their lack of wings. The body is
or humans. Of all the cimicid species only three broadly flattened and ovoid, typically 58 mm in
feed on humans. These include Leptocimex boueti length and about 4 mm wide. Because the adults
Brumpt, a West African species that feeds on only have wing pads, the first 11 dorsal abdominal
humans and bats; Cimex hemipterus F. (tropical segments are usually easy to see when the body is
bed bug), found in both the new and old world not engorged.
tropics feeding on humans and chickens; and The morphology of the bed bug head is very
Cimex lectularius L. (common bed bug), which is similar to that of other cimicids. The multifac-
found all over the world and feeds on humans, eted eyes of the bed bug look like small knobs
chickens and bats. protruding from the sides of the head. The anten-
Cimicids that feed on humans get their com- nae of the bed bug are 4-segmented and project
mon name bed bugs from their long history of forward from a small protuberance between the
harboring in human dwellings, particularly in eye and clypeus. The third and forth segments of
those locations where the host would come to rest the antennae are thinner than either the basal or
at night (bed or bedding). By harboring in the second segment.
bed, the bugs could feed undisturbed while the The most prominent feature on the head is
host was asleep. the labrum. The labrum extends out from the
While the origin of the bed bug is unknown, clypeus at the extreme anterior of the head and
it is thought that human bed bugs were originally is marked with a labral suture. The labium arises
ecto-parasites of bats. When humans moved into just below the labrum, at the anterior margin of
caves and either lived with the bats or removed the head, and has three segments. When the
them, the bat parasites adapted to the presence of labium is held at rest (under the bed bug head),
the new host. Those bat bugs that survived and the ventral side of the labium contains a longi-
proliferated on human blood continued to inhabit tudinal groove which holds a fascicle of man-
human environments. dibular and maxillary stylets. Between the
The exact geographic origin of human bed maxillary stylets are a large food canal and a
bugs is also unknown, but both Neanderthal smaller salivary canal. The food canal and the
man (100,000 years ago) and, later, Cro-Magnon stylet fascicle are connected with the cibarial
man (12,000 b.c.) populated caves in the Middle pump inside the head of the bed bug. The 3-seg-
East. It is most likely in these Middle Eastern mented labium, including the maxillary and
406
B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)

mandibular stylets and the food and salivary Life Cycle

canals, are collectively referred to as the ros-
trum (Fig. 23). The rostrum pierces the hosts The bed bug life cycle is unique in that it begins
skin and the cibarial pump is used to pump the with an unusual form of copulation known as
blood from the host into the head of the traumatic insemination. Unlike other hemipter-
bedbug. ans, Cimex males never insert their copulatory
The pronotum of the bed bug is very distinct organs into those of the female. Instead the male
and the shape or hairiness of the dorsal side is awkwardly mounts the females back and wraps
often used for species identification. In general his abdomen around the right side of her body.
the pronotum is broad, surrounding the base of He then punctures her body wall, wounding the
the head within the concave anterior margin. female as he inserts his copulatory organ into her
The sides of the pronotum extend up around the paragenital sinus or Organ of Berlese to inject
base of the head in a wing-like fashion. his sperm. Mating usually lasts for several min-
The abdomen of the adult bed bug consists utes but can last up to half an hour in some cases.
of 11 segments and is completely sclerotized. Within 2 h of mating the male spermatozoa pass
However, the sclerotized abdomen is capable of from the female Organ of Berlese into her
enormous expansion due to the wide interseg- abdominal cavity. Once in the hemocoel, the
mental membranes and the hunger folds (ven- spermatozoa accumulate at the base of the
tral membranous sections) located within the oviducts, moving into the seminal conceptacles
second and fifth abdominal segments. The within 12 h.
female reproductive organs (gonapophyses) are After mating, a female held at 23C will begin
homologous to the ovipositor found in other to produce eggs within 3 days. Several sources
species and are located on the ventral side of the have indicated that female bed bugs, when fed reg-
8th and 9th abdominal segments. The female ularly, are able to produce viable eggs for 57 weeks
spermalege or paragenital sinus appears as a after a single mating. However, mated females will
notch located on the ventral side of the abdo- usually cease oviposition after about 11 days with-
men between the 5th and 6th segments. The out an additional blood meal. Under laboratory
genitalia of the male bed bug also originate on conditions (23C and 75% RH) a typical female
the ventral side of the abdomen near the apex. that has been fed and mated regularly can produce
The male abdomen is narrower at the apex than 34 eggs every day averaging more than 200 eggs
that of the female and the 9th segment is longer total over her entire lifespan. Under natural condi-
and asymmetrical. The male paramere is tions fecundity can be quite variable, depending
strongly curved to the left and lies in a groove not only on the availability of mates but also tem-
within the 9th segment. perature and nutrition. Egg production is closely
Immature bed bugs differ from adults in their correlated to ambient temperature, the weight of
morphology in several ways. First, they lack the the unfed female, and size of the female blood
characteristic reddish color of the adults. Nymphs meal. An increase in temperature from 17 to 23C
are typically translucent white, making their inter- has been shown to produce as much as a ten-fold
nal structures visible after a blood meal. Nymphs increase in weekly egg production among well fed,
also differ from adults in that not all of their mated females. The mean weight of unfed females
abdominal segments are sclerotized, particularly also influences egg production. As expected, larger
on the ventral surface of the abdomen. Nymphs females produce more eggs. Also, because larger
also have a 2-segmented tarsus while the adult females tend to take larger blood meals, the size of
tarsus is 3-segmented. Finally, immature bed bugs the blood meal has also been shown to result in
lack any structures associated with reproduction. increased egg production.
 Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)
B 407

Bed Bugs (Hemiptera: Cimicidae: Cimex spp.), Figure 23 The common bed bug, Cimex lectularius:
(a) ventral morphology of adult bed bug head showing the rostrum, pronotum, and antennae; (b) adult
female bed bug; (c) engorged adult and early instar bed bugs; (d) partially fed first instar bed bug with
egg cap on head; (e) first instar bed bug emerging from egg.
408
B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)

Oviposition occurs 36 days after mating. extended to 4 months or more depending on the
The bed bug eggs are about 1 mm in length, ambient temperature and the availability of
white, elongate, and slightly bow shaped. Upon regular blood meals.
oviposition, eggs are coated with sticky cement
that dries quickly causing them to adhere to the
substrate on which they were deposited. The eggs Behavior
are typically laid in cracks and crevices near a
harborage site and take 610 days to hatch, Bed bugs are thigmotrophic and seek out har-
although temperature variation may alter hatch borages where their bodies can be in direct con-
time. As a first instar bed bug emerges from the tact with surrounding surfaces. They are often
egg, anti-peristaltic movements of the gut drive found aggregating in cracks and crevices of
fluid into the head, deploying hatching spines to homes and other structures, or wedged into
dislodge the egg cap. After hatching, most first mattress tufts or staple holes where they can
instars will stay near the egg capsule until they remain undisturbed. In hotel rooms they are
leave in search of their first blood meal. Several often found behind removable headboards or
studies have indicated that bed bug survivorship picture frames hanging on the wall. They can
is closely linked to the amount of energy they also be found hiding in the wood frames of the
have to expend searching for a host. This is par- box springs or the stuffing. In some heavy infes-
ticularly true for first instars. While quite ambu- tations, the best harborages are already filled so
latory for their size, first instars are at great risk many bed bugs will take up residence along
of dehydration compared to the older life stages. baseboards, behind posters on the wall, or under
Therefore, we can assume that many first instars the carpet tacking. Bed bugs will typically avoid
are lost before they ever consume their first locations exposed to air movement but may be
blood meal simply because they hatched too far seen aggregating in the open on the ceiling or at
from a host. the ceiling/wall junction if no other space is
Bed bugs have five nymphal instars, each available. The stimulus that prompts bed bugs
requiring a blood meal to complete develop- to leave their harborages is not well understood
ment. Each nymphal stage can feed within 24 h but obviously they have to leave in order to feed.
after molting and all bed bugs are typically After feeding, bed bugs will return to these same
stimulated to feed at slightly less than weekly harborages after their meal and remain there
intervals. At higher temperatures (27C), the while digesting. The digestion period after feed-
feeding interval can be reduced to every 3 days, ing results in the accumulation of fecal material
and all nymphal instars molt more quickly when (black spots of dried blood) in preferred har-
exposed to warmer temperatures. In studies borage locations.
conducted on nymphal stages 15, it was found Bed bugs are nocturnal, usually avoiding the
that the mean number of days between the light. Studies have indicated that bed bugs are most
blood meal and molting ranged between 2.1 active after 3:00 a.m., a time when the host would
days at 35C and 26 days at 15C. Ordinarily, most likely be in a deep sleep. However, bed bugs
nymphal bed bugs will feed once per instar, will feed during the daylight hours if they are hun-
with each instar lasting 35 days at optimal gry and a host is available. The question regarding
temperatures (23C). If insufficient blood meals how these nocturnal insects are able to navigate
are taken, secondary blood meals will be neces- between the host and their harborage is quite con-
sary before molting can occur. So although the troversial. Little is known about bed bug vision,
average time from egg to adult is often reported but it is suspected that they do not see well because
as about 1 month, that time period can be of their nocturnal and parasitic lifestyle. Bed bugs
 Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)
B 409

are thought to use pheromone and odor cues for treatment, and may have had some potential for
navigation. However, bed bugs have been tested repelling bed bugs away from the sleeping host.
repeatedly and have never been observed to detect However, the snap bean (Phaseolus vulgarius) has
heat sources or host odors over distances >12 cm. demonstrated true potential for bed bug control.
Several researchers have suggested that bed bug In the Balkans, the leaves of this bean plant were
searching behavior in the natural environment placed under the beds in infested rooms. Foraging
must be completely random. However, others bed bugs would become entangled in the hairs on
claim that random searching would be too costly the bean leaves during the night. In the morning,
for bed bugs to have achieved their obvious repro- the leaves were simply swept up and burned to
ductive success. Regardless of how bed bugs detect destroy the bed bugs. While the practice of sleep-
their food source, there is no question that they ing over bean leaves most likely provided at least
have evolved to take advantage of the diurnal some bed bug relief, the ancient remedy of hang-
nature of the human host. They feed at night when ing the feet of a dead stag or rabbit at the foot of
the host is unconscious, thereby increasing their the bed (as host decoy), probably had little effect.
chances of feeding to repletion. After feeding they Another folk method of bed bug prevention that is
quickly abandon the host and return to their har- still used today is to place the legs of the bed frame
borage where they remain during the daylight in pans of water or kerosene. Although this method
hours, thus decreasing their chances of being is thought to work, there have been many anec-
detected. dotal references to bed bugs circumnavigating
these barriers by crawling up the wall and drop-
ping onto the sleeping host from the ceiling.
Bed Bug History In spite of all of the recorded history of cohab-
itation with humans, bed bugs are still the bug
References to the bed bug as the bane of human that nobody knows. The reason for this bed bug
existence appear in some of the earliest recorded denial is that there is a social stigma associated
history. Aristotle made reference to bed bugs in his with bed bug infestations. Many people believe
Historia Animalia (384322 b.c.), and many other that bed bugs only infest overcrowded or unsani-
historical texts document the presence of bed bugs tary housing. Therefore, you can only get bed bugs
in Greece in 499 b.c., Italy in 77 a.d., and in China if you visit or live in these poor conditions. This
by 600 a.d. Because bed bugs have co-existed with has never been true. Bed bugs do not discriminate
humans for centuries, many common names and between human hosts and infest every social class
folk remedies have been created regarding them. and nation across the globe. The bed bugs ability
Bed bugs are known by over fifty common names to infest any human environment has been con-
in a number of different languages. The English firmed by the resurgence of bed bug infestations
language names include wall-louse, red coat, in industrialized nations over the past decade.
pursuer, crimson rambler, wall flounder, and the During the 1990s, new bug infestations appeared
mahogany-flat. In addition to the various com- first in five star hotels and other expensive tourist
mon names, there are several folk sayings that are locations within the United States, Australia,
related to bed bugs, including crazy as a bed bug Singapore, and Europe.
or snug as a bug in a rug.
Bed bugs have long been a target of folk rem-
edies. Some remedies may have been somewhat Geography of the Bed Bug
effective while others, though creative, were prob-
ably useless. The plant Actaea cimicifuga or bug- Today, Cimex hemipterus F. (tropical bed bug) and
bane has long been regarded as viable bed bug Cimex lectularius L. (common bed bug) are by far
410
B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)

the two most important and widespread cimicid C. lectularius was compromised in the presence of
parasites of humans. Both are thought to have C. hemipterus. Specifically, it was found that in
originated from the Old World but are now found mixed populations, C. lectularius females laid only
all over the globe. Colonies of C. hemipterus sterile eggs when C. hemipterus accounted for
have been cultured from such diverse locations as >75% of the individuals. However, the potential
Vietnam, Taiwan, Panama, Uganda, Venezuela, negative impacts (if any) of C. hemipterus males
Cuba, India, and Florida in the United States. on C. lectularius females living in mixed popula-
Although C. hemipterus has a worldwide distribu- tions have yet to be fully determined.
tion, its range rarely extends beyond the tropics,
therefore it has been described as strictly a
tropico-politan species. Public Health Importance
C. lectularius is a truly cosmopolitan bed bug
and has expanded its range with humans through- Because bed bugs are blood feeders and have typi-
out Europe and into the Americas. Records of cally been associated with poor living conditions,
C. lectularius have been collected from all over the they have long been suspected of being potential
world with the exception of Antarctica. However, vectors of human disease. In fact, studies prior to
Antarctica will no doubt have C. lectularius by the the 1960s identified many diverse disease organ-
end of the decade due to the eco-tourist industry isms that were collected from the bed bug gut,
that has recently developed on that continent. body and feces. These pathogens included those
In many tropical locations, the distribution of responsible for plague, murine typhus, smallpox,
C. hemipterus and C. lectularius overlap. Yet, unlike poliomyelitis, yellow fever and at least 20 other
C. hemipterus, C. lectularius is able to survive in diseases. However, there has been no conclusive
both tropical and temperate climates. Interestingly, evidence that bed bugs transmit any of these
C. lectularius does not typically occur where pop- diseases to humans. More recently, bed bugs have
ulations of C. hemipterus are well established. been evaluated for their ability to become infected
Some authors have speculated that the reason with and transmit Human Immunodeficiency
for this absence is that C. lectularius is suscepti- Virus (HIV) and Hepatitis B. HIV has been found
ble to fungal infection in tropical locations of to survive in bed bugs for several days after ingestion,
high humidity while C. hemipterus is not. A more but there has been no epidemiological evidence
interesting suggestion is that the distribution of indicating that HIV could be transmitted from an
C. lectularius is limited by the fact that interspe- infected bed bug to a host during the feeding pro-
cific copulation is common between the two spe- cess. While Hepatitis B cannot be transmitted from
cies and yet has a deleterious effect on C. lectularius. bed bugs to humans via the taking of a blood meal,
For example, one older study suggested that there is evidence to suggest that the Hepatitis B
sperm fluid of C. hemipterus males was toxic to virus may be mechanically transmitted to humans
C. lectularius females. Later research indicated that in bed bug feces or when bed bugs are crushed
the deleterious effects of interspecific copulation during the feeding process. However, as of this
were due to the fact that attempts of C. hemipterus writing there is no medical record of such a trans-
males to mate with C. lectularius females resulted mission ever taking place.
in female mortality. The reason suggested for Disease transmission is not the only health
this mortality was that the paragenital sinus of the issue associated with bed bugs. In many cases,
C. lectularius female was not suited to accommo- the number of bed bug bites or reactions to the
date the C. hemipterus paramere. The most recent bites has been cause for concern. When a bed
study regarding the viability of mixed bed bug bug bites, the mandibles and maxillae form a
populations determined that the fecundity of compact bundle (fascicle) that is rapidly injected
 Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)
B 411

into the hosts skin. During the act of piercing, around the bite site and the delayed response
the toothed mandibles move in a rapid alternat- may last for longer than a week. Perhaps the worst
ing motion slicing their way through the skin scenario for sensitive people who experience the
tissues slightly ahead of the maxillae. After the delayed reaction is to inadvertently spend several
tissues are breached, the fascicle probes in all nights sleeping in an infested location. Only with
directions, backwards and forwards, often cut- the onset of the delayed immune response, do
ting across or entering small capillaries and they realize that they have been subjected to
larger vessels. The probing can result in numer- hundreds of bed bug bites.
ous small hemorrhages throughout the tissues. Fortunately, the suffering caused by receiving
The bed bug fascicle probes for a vessel of suit- hundreds of bed bug bites typically has no long
able size from which to begin feeding. Blood term physiological effects, provided the person is
vessels that are too large or too small are ignored. able to leave the infested area or have the bed bugs
Once the fascicle finds a suitable vessel, the max- eliminated. Today, the most common medical
illae enter the blood vessel and inject the saliva consequences of bed bug bites are secondary bac-
(anticoagulant). The pressure in the vessel causes terial infections that can occur from vigorous
the hosts blood to rush up the food canal into scratching and excoriation. Yet historical records
the bed bug head, allowing for feeding to be indicate that excessive bed bug feeding has been
completed in a matter of minutes. However, the known to cause iron deficiencies among infants
destructive nature of the probing coupled with in India.
the injection of the bed bug saliva can produce a Although bed bug bites do not produce any
wide variety of reactions within the host. long-term physiological problems, the psycholog-
It has been well documented that many peo- ical aftermath of dealing with a bed bug infesta-
ple do not react to bed bug bites; however, some tion may be significant. Many people suffer from
people can suffer severe skin reactions that last for stress and anxiety after an encounter with bed
several days. There have been many reports of bugs and are fearful that bed bugs may be infest-
married couples staying in infested hotel rooms ing their homes or living on their bodies. Most
where the wife or husband was made miserable by people who suffer from bed bug anxiety have had
hundreds of itching bed bug bites while their an infestation in their home or have been bitten
spouse experienced nothing at all. It has also been severely while traveling. Still other sufferers have
suspected that hypersensitive individuals living never had an encounter with bed bugs, but have
with large populations of bed bugs may actually been told about bed bugs or have had it suggested
suffer asthma attacks after being bitten repeatedly that their itching skin may be the result of bed bug
by bed bugs. The reactions of people who are sen- bites. Regardless of whether they have encoun-
sitive to bed bug bites vary widely in severity and tered real bed bugs or not, people who suffer from
may be immediate, delayed or both. bed bug anxiety have great difficulty sleeping for
Bed bug saliva contains many proteins that fear that bed bugs are crawling on them. They
trigger the bodys immune response. The imme- often get up several times a night to check them-
diate immune response usually involves the selves or their children for bed bugs. Some people
development of an inflamed reddish weal that have moved several times and discarded most of
will start to itch within a couple of hours and their furniture and other belongings. Many have
may continue to itch for 12 days. People who also paid thousands of dollars for repeated bed
experience the delayed response are typically bug exterminations that have not worked to their
unaware that they have been bitten for several satisfaction. Another characteristic of these suffer-
days. They then begin to experience localized ers is that they often withdraw from family and
itching and swelling (sometimes very severe) friends and spend hundreds of hours on the
412
B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)

c omputer researching bed bug cures and partici- Current Pest Status
pating in internet-based bed bug support groups.
Although not everyone who suffers from In the early 1990s pest management professionals
bed bug anxiety has experienced a real infesta- began to receive complaints about new bed bug
tion, the potential for bed bug infestation is very infestations within the United States. By 2001,
real. Bed bugs have enjoyed a long history of many pest control firms were reporting tenfold
infesting human environments and it was only increases in bed bug calls every year. While new
within the last century that certain developed infestations were found to be particularly com-
nations have enjoyed a brief respite from these mon in hotels, bed bugs were increasingly being
noxious pests. reported in homes, apartments, retirement com-
munities, health care facilities, college dormito-
ries, youth camps and used furniture outlets. The
resurgence of the bed bug after its supposed eradi-
Control History cation has presented a number of unique chal-
lenges to a variety of commercial industries which
At the turn of the twentieth century the bed bug in their own way have contributed to the bed bug
was a common household pest in the United problem.
States and the world. Bed bugs were frequently First, within the pest management industry,
encountered in quality hotels and motels, laun- most pest management professionals are too
dromats, movie theaters, city buses, and taxis. young to have had any personal experience with
Bed bugs were easily transported home via a bed bug control. This lack of experience has
travelers clothing, vehicle, or luggage. Once resulted in many incomplete and ineffective bed
inside the home, bed bugs could find harborage bug treatments since the bed bug resurgence
in furniture, cracks and crevices in the floor or began. Second, the medical profession has had
walls, behind wallpaper, or under carpeting. The very little experience with bed bugs, so many bite
easy transportability of the bed bug coupled with complaints were misdiagnosed, allowing bed bug
the war-time movement of people in the United infestations to continue in homes where they
States and Europe (19141945) led to millions of might have been treated had they been correctly
homes and other structures becoming infested. identified. Leaders in the hospitality industry were
However, the importance of the bed bug as a also slow to admit that bed bugs were a problem in
household pest began to diminish in the 1940s hotels. Therefore, the hoteliers did not readily
and 1950s with the use of pyrethrum insecticides develop bed bug prevention or treatment plans
and DDT. These insecticides were applied liber- because they failed to recognize the potential dam-
ally to all walls, floors, mattresses, bed frames, age that bed bugs could cause their industry. For
curtains, cupboards, and any other surface that example, when bed bugs were first (re)discovered
could be occupied by bed bugs. Complete control in the United States, it was in five-star hotels in
was usually obtained within a matter of days, and cosmopolitan locations like Los Angeles and New
with the use of DDT, the residual activity was so York City. The hotel industry was immediately
long that the sprayed areas remained toxic and faced with million dollar lawsuits initiated by cli-
bed bug free for months. Therefore, in the latter ents who had been bitten while staying in their
half of the twentieth century the bed bug was facilities. These lawsuits received extensive press
almost eradicated in the United States and coverage and immediately associated the hotel
Europe, with only a few persistent populations brand name with bed bug infestations. It was only
surviving in locations where living conditions after a number of these bed bug cases were reported
were exceptionally poor. that the hospitality industry began to address the
 Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)
B 413

expanding bed bug problem. Finally, an unantici- that the increasing population pressure has led to
pated source of bed bug proliferation has been the the widespread dissemination of bed bugs
rapidly growing organic foods industry in the throughout the world.
United States. Organic poultry farms house thou- Historical records indicate that bed bugs
sand of chickens that are being raised for either developed resistance to a number of the insecti-
meat or eggs. There have been several documented cides used for their control. These chemicals
infestations within these organic facilities where included DDT, methoxychlor, dieldrin, aldrin,
bed bugs have been found cohabitating with and carbaryl, Malathion and other organophosphates.
feeding on the chickens. Because these facilities Many of these older chemistries have been banned
are pesticide-free, the bed bugs in these facilities by the US Environmental Protection Agency and
number in the millions, causing stress to both the are no longer available for bed bug treatment.
chickens and migrant workers. While the trans- However, because bed bugs have not been a prob-
port of these bed bugs to other locations has not lem in the USA for over 40 years, few of the exist-
been documented, there is the potential for these ing pesticide products are labeled for bed bug
bed bugs to be shipped all across the nation via the control and many of these products have the same
thousands of delivery trucks that bring eggs and type of active ingredients. The majority of insecti-
other poultry products to food distribution centers cide products that are labeled for the treatment of
every day. bed bugs are either natural pyrethrins, or pyre-
While the exact cause of this recent, world- throids. Because these active ingredients have been
wide increase in bed bug activity is not known, used for decades all over the world, and because
there are several factors that may have contributed they are from the same chemical class, it has been
to the resurgence of bed bugs in the USA. It has suspected that the newly emerging bed bug popu-
been suggested that international travel from lations might already be resistant to pyrethroids.
developing nations has increased the distribution As of 2007, bed bug resistance to a number of
of bed bugs throughout the world. However, inter- pyrethroids has been documented. Field popula-
national travel has been common for many decades tions of bed bugs have been found to have variable
and bed bugs have only recently (1990s) become levels of resistance to permethrin, deltamethrin,
recognized as a widespread problem. Another beta-cyfluthrin, and lambda-cyhalothrin. In some
possibility for the bed bug increase has been the cases, the resistance of field collected bed bugs
reduction in residual insecticide use indoors. exposed to specific active ingredients was found to
Because of concerns about human exposure risk, be 1,000 times that of susceptible laboratory strain
routine interior applications of spray insecticide bed bugs. Likewise, the time to mortality for bed
have been greatly reduced in favor of integrated bugs confined on dried pyrethroid product resi-
pest management (IPM), where pesticides are dues was found to be significantly greater than
applied only on an as needed basis. IPM also that of the laboratory strain bed bugs. For exam-
uses insecticide baits as the primary method for ple, the time it took to kill 50% of the laboratory
controlling crawling insects. However, pesticide strain bed bugs (LT50) confined on panels treated
baits have no effect on blood sucking parasites. with a formulation of deltamethrin (0.06%) was
Thus, it is thought that in the absence of the resid- 61 min. However, when testing bed bugs collected
ual sprays, bed bug populations have been able to from an infested apartment in Arlington, Virginia,
establish unchecked. One final possibility that the LT50 for deltamethrin was 19 days and 2 h.
deserves consideration is that bed bug populations Interestingly, in tests evaluating the potential
across the world have become resistant to insecti- repellency of pyrethroids to bed bugs, it was docu-
cide products used in developing nations and the mented that neither the field nor the laboratory
USA. If this is the case, it is reasonable to suggest strain bed bugs found pyrethroids repellent. In
414
B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)

choice tests where bed bugs could aggregate on infested site by a qualified professional. In many
either a panel treated with a pyrethroid product or cases, infested rooms will be taken completely
a panel treated with water, there was no significant apart and all personal belongings inspected for
difference as to where the bed bugs chose to aggre- live bed bugs, bed bug eggs and fecal spots. Per-
gate. In fact, many bed bugs remained in contact sonal belongings are then bagged for treatment,
with the pyrethroid treated panels until they died, laundering, or disposal. Because clutter provides
even though they could leave the panel to aggre- numerous harborages for bed bugs and makes
gate somewhere else at any time during the test. insecticide applications very difficult, a bare
In addition to pyrethroid resistance, these walls approach is generally required to provide
resurgent bed bug populations are not readily sus- adequate control. After all clutter and personal
ceptible to the non-pyrethroid products labeled for belongings have been removed, the infested room
their control. For example, pyrethroid dusts usually and furniture can then be treated.
take several days to kill resistant bed bugs. Desic- A back-pack vacuum cleaner with HEPA
cant dusts like silica aerogel, diatomaceous earth or filter is recommended for the removal of live bed
limestone and corn bran dusts can also take days or bugs and their cast skins. The removal of live bed
even weeks to kill bed bugs confined on the bugs and their debris will not only reduce the
material. Because bed bugs do not groom, stomach bed bug numbers but will aid the pest manage-
toxicants like boric acid have no effect on bed bugs. ment professional in identifying incipient infes-
Even crack and crevice sprays containing pro- tations in future inspections. Once vacuuming is
insecticides like chlorfenapyr may take longer than completed, the vacuum cleaner bag must be
a week to kill bed bugs, thus allowing them to sealed in a plastic bag and removed from the
reproduce prior to suffering any toxic effects. The structure immediately. It should be noted that
insect growth regulator hydroprene, which has although the vacuum cleaner will be able to
been a widely used juvenile hormone analogue for remove the majority of live bed bugs it will not
cockroach control, has been found to function as a be able to remove the bed bugs eggs which are
chitin synthesis inhibitor in bed bugs, disrupting typically cemented to the surfaces on which they
the final molt. Yet, although hydroprene kills close are laid. Therefore, additional treatment(s) will
to 50% of exposed bed bugs during the final molt, be necessary.
the surviving adults are not sterilized and produce A frequently used method of reducing bed
a greater number of viable offspring than unex- bug harborage sites is the use of sealants and caulk.
posed bed bugs after taking their first adult blood Because early instar bed bugs are capable of occu-
meal. Finally, non-toxic mattress treatments pying extremely small cracks it is important to
containing isopropyl alcohol, sodium laurel sulfate inspect the walls and ceilings very carefully for
or protein degrading enzymes typically kill over bed bug harborages around switch plates, wallpa-
80% of bed bugs that are directly sprayed with per seams, electrical outlets, inside nail holes and
these products. However, these treatments have no screw heads, around window frames, and in sta-
residual activity once the product is dry, and like ples holes. Caulking and sealing these harborages
most insecticides, these non-toxic mattress treat- will force bed bugs to wander in search of new
ments have no effect on bed bug eggs. harborage space, causing them physical stress and
increasing their chances of exposure to insecticide
residues.
Current Management Practices Steam cleaning is rapidly becoming a widely
used method of bed bug control. Professional
Because of their cryptic lifestyle, bed bug manage- steam cleaners can be used to kill bed bugs hiding
ment begins with a thorough inspection of the in baseboards, under carpeting, in mattress seams
 Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)
B 415

and in the wooden components of box springs. Because bed bugs are susceptible to high
Professional cleaners that produce dry steam at temperatures, heat fumigation is being used to
temperatures >60C (140F) are preferred because eradicate bed bugs from large commercial
they produce enough heat to compensate for the facilities. Using the heat fumigation technology
insulating properties of mattresses and other developed for the treatment of grain silos, fans
upholstered furniture which might otherwise are used to blow air in from the outside to raise
prevent bed bugs from reaching their thermal the atmospheric pressure inside the facility. The
death point. When purchasing a steamer for bed air is then heated and monitored to make sure that
bug control, it is important to select a machine all locations inside the building reach the appro-
with a steam head large enough to disperse the priate temperature (bed bug thermal death
steam at a low velocity. The small steam head of point) and pressure. The heat treatment is then
some machines will disperse the steam with such maintained for a period of hours to ensure that
force that the bed bugs and eggs are blown off the all bed bugs and bed bug eggs are killed. Although
treatment areas into other parts of the room. heat fumigation is an effective bed bug treat-
Although steaming bed bugs is a slow and laborious ment, the cost, like that of chemical fumigation,
task, steam cleaning is one of the most effective is often prohibitively expensive for the average
methods for killing both bed bugs and their eggs. consumer.
After steaming, the treated mattress and box Exposing bed bugs to cold temperatures will
springs should both be placed inside a bite proof, kill bed bugs but the duration of exposure is often
escape proof mattress cover. A variety of products too long to be practical. For example, the thermal
are available for covering mattresses, however, death point for adult bed bugs exposed to cold
most were not designed to function as a bed bug temperatures for 1 h is 18C (1F). Yet, most
prevention tool. Many tear easily or have zipper conventional freezers have a minimum tempera-
casings that are large enough for bed bugs to crawl ture of 0C (32F), thus requiring that the bed bugs
through. However, there are mattress covers that be frozen long enough to achieve 100% kill.
have been tested to ensure that bed bugs cannot Attempting to kill bed bugs at 0C will take several
get inside the cover and any bed bugs already days at least, and if the bed bugs are insulated in
trapped inside the cover cannot escape or bite clothes or bedding it may take several weeks of
through the fabric. Although mattress covers exposure to ensure that all bed bugs are killed and
cannot prevent a future bed bug infestation, they bed bug eggs are no longer viable.
do keep the client from having to throw the mat- Although increased sanitation and exclusion
tress away. techniques are necessary to remove bed bug har-
All bedding and any clothing articles that are borages, these techniques alone will not control an
suspected of being infested with bed bugs must be established infestation. Therefore, chemical meth-
laundered. Both clothing and bedding should be ods must also be employed as part of a compre-
bagged and marked so that they are not mixed with hensive bed bug management program. As stated
uninfested articles during the cleaning process. All earlier, most modern pesticides will not control
items should be laundered at a temperature >49C bed bug infestations when used individually. How-
(120F) for more than 10 min with laundry deter- ever, combinations of products with different for-
gent. Bed bugs, like all insects, are very susceptible mulations and modes of action have been evaluated
to drowning when exposed to soap, so the addition in the field and have been found to produce satis-
of laundry detergent will ensure a quick kill. Plac- factory control. These products must be applied
ing bed clothes in a dryer at 60C (140F) for 20 according to the product label and the treatment
min or longer is also recommended to make sure area must be regularly monitored to make sure
that no bed bug eggs survive. that the products are working. Field evaluations
416
B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)

have determined that microencapsulated products complete vacuuming of all carpeting and furni-
containing pyrethroids are an effective residual ture, steam cleaning of upholstered furniture
spray because the micro capsules stick to the bed and mattresses to kill bed bugs and their eggs,
bug body allowing for enough exposure time to and treatment of the mattresses and box springs
kill resistant bed bugs. These products can be used with a non-toxic mattress treatment (preferred)
for application into cracks and crevices where bed or a labeled residual insecticide. After treating
bugs hide and also along baseboards or ceiling/ the mattress, both the mattress and box springs
wall junctions where bed bugs will often harbor should be encased in bite proof, escape proof
when the infestation levels are high. In addition to mattress covers. The infested room should be
the crack and crevice applications, products treated with a combination of residual insecti-
labeled for upholstery treatment can be applied to cide spray and an insect growth regulator. These
infested furniture as well as to the mattress and products should be applied according to the
box springs. Some mattress products have residual label to cracks and crevices, baseboards, and any
activity (pyrethroids) while other non-toxic other bed bug harborage locations. The infested
products do not. The non-toxic products that room and all adjoining rooms should then be
contain isopropyl alcohol or sodium laurel sulfate inspected (and/or treated) weekly to determine
as the primary killing agent will kill bed bugs on the efficacy of the treatment products and to
contact. Yet, these products evaporate almost make sure that the bed bug population is being
immediately after application and bed bugs that eliminated.
survive the treatment will continue to bite and
reproduce. Residual dusts are particularly useful
in the frame of the box springs and wood compo- Summary
nents of the other furniture because they stay
within the application site and have a very long Most entomologists and pest management pro-
residual. Residual dusts containing pyrethroids fessionals believe that the resurgence of human
also adhere to the bed bugs body allowing for the bed bugs (both Cimex lectularius and Cimex
long exposure period (possibly days) necessary to hemipterus) presents the single greatest indoor
kill resistant bed bugs. Non-toxic desiccant pest management challenge in decades. Since the
dusts will also kill bed bugs but they too may take bed bugs widespread reappearance in the 1990s,
several days to work. Baseboard, and crack and the common bed bug has become a full blown
crevice treatments with insect growth regulators epidemic with new infestations reported in most
are useful in that they will kill many immature European countries and in all 50 states in the
bed bugs during the final molt. However, there is United States. Likewise, the tropical bed bug has
no evidence that insect growth regulators will spread throughout the tropics in the last 10 years
kill or sterilize adult bed bugs. Although aerosols increasing its range to infest Australia and rees-
and foggers are frequently used for bed bug tablishing populations in Singapore and other
elimination, they are not effective control prod- tropical nations where they had been previously
ucts because they do not penetrate into bed bug eradicated. Because these insects have never
harborages. completely disappeared from developing nations
Overall, a complete bed bug treatment they have been continuously treated with many
should include the removal of infested items insecticide products over the last 50 years. This
for either treatment or disposal, the laundering continuous pesticide pressure has selected for
of infested clothes and bedding, the elimination bed bug resistance, particularly to pyrethroids.
of clutter, the sealing of all small cracks and These pyrethroid resistant populations present a
holes that might provide bed bug harborage, a unique problem in developed nations where
 Bee Louse, Bee Fly, or Braulid, Braula coeca Nitzsch (Diptera: Braulidae)
B 417

public opinion and federal legislation has elimi- Newberry K (1989) The effects on domestic infestations of
Cimex lectularius bed bugs of interspecific mating with
nated entire classes of insecticides from indoor
Cimex hemipterus. Med Vet Entomol 3:407414
use due to their perceived toxicity. Pyrethroids Potter M (2006) The perfect storm: an extension view on bed
have been one of the few chemical classes bugs. Am Entomol 2:102104
that remain available for indoor use due to Usinger S (1966) Monograph of Cimicidae. Thomas Say
Foundation Vol. VII. Entomological Society of America,
their low mammalian toxicity. As a result, pyre- Lanham, MD, 585 pp
throids are the most frequently used class of Vall Meyers M, Hall A, Inskip H, Lindsay S, Chotard J
chemistry for bed bug control in the United (1994) Do bed bugs transmit hepatitis B? Lancet
States today. However, with increasing bed bug 343:761763
Webb P, Happ C, Maupin G, Johnson B, Ou C (1989) Potential
resistance these products will gradually become for insect transmission of HIV: experimental exposure
less effective at controlling new infestations. of Cimex hemipterus and Toxorhynchites amboinensis
Because of the prevalence of bed bug resistance to Human Immunodeficiency Virus. J Infect Dis
160:970977
many researchers believe that the bed bug
e pidemic will become much more severe in
the future.
The key to bed bug control in developed Bee Bread
nations will ultimately be education. People will
have to accept that bed bugs exist and learn how A pollen and honey mixture fed to bee larvae by
to avoid transporting bed bugs to their homes worker bees
(from hotels, taxis, air planes, camp cabins,
movie theaters, laundromats, day care centers,
multiple unit housing, etc.) during the course of Bee Flies
their daily activities. The ability of the average
citizen to identify bed bugs and bed bug evi- Members of the family Bombyliidae (order
dence will be critical for them to successfully Diptera).
protect themselves and their home from bed Flies
bug infestations.

Bee Lice
References
Members of the family Braulidae (order Diptera).
Cooper R, Harlan H (2004) Bed bugs and kissing bugs. In: Flies
Hedges S (ed) Mallis handbook of pest control, 9th edn. Bee louse
GIE Publications, Cleveland, OH, pp 494529
Doggett S, Geary M, Russell R (2004) The resurgence of bed
bugs in Australia: with notes on their ecology and con-
trol. Environ Health 4:3038 Bee Louse, Bee Fly, or Braulid,
Harlan H (2006) Bed bugs importance, biology, and control Braula coeca Nitzsch (Diptera:
strategies. Armed Forces Management Board Technical
Guide No. 44. http//:www.afpmb.org/pubs/tims/TG44/
Braulidae)
TG44.htm
Johnson CG (1942) The ecology of the bed-bug, Cimex jamie ellis
lectularius L in Britain. J Hyg 41:345361 University of Florida, Gainesville, FL, USA
Moore DJ (2006) Evaluation of multiple insecticidal products
for control of the common bed bug (Cimex lectularius,
(L.)). Unpublished M.S. thesis, Virginia Tech University, The bee louse, Braula coeca Nitzsch (Diptera:
Blacksburg, VA, 118 pp Braulidae), is a wingless fly that lives as a
418
B Bee Louse, Bee Fly, or Braulid, Braula coeca Nitzsch (Diptera: Braulidae)

c ommensalist in western honey bee (Apis mellif-

era L.) colonies. Not much is known about the
bee louse as its biology has been studied only
irregularly since the 1920s. The fly is presumed
to be harmless to its host, although this point is
debatable. It is found in many countries, and
because no true e conomic damage can be
attributed to the fly, it probably poses a mini-
mal threat to bees.

Bee Louse Life Cycle and Behavior Bee Louse, Bee Fly, or Braulid, Braula coeca
Nitzsch (Diptera: Braulidae), Figure 24 An adult
Adult bee lice (Fig.24) are small (<1.5 mm long) Braula coeca (photo by James Ellis, University
and are covered in spine-like hairs. They are round of Florida), and its worldwide distribution (from
in shape and unlike most flies, have neither wings Ellis, Munn (2005) The worldwide health status of
nor halteres. They are reddish-brown in color, honey bees. Bee World 86(4):88101).
which often leads to their misdiagnosis as varroa
mites, Varroa destructor. Structurally, physically,
and their location on the adult bee all are similar While on the head of its host, the fly will
or the same for varroa. One noticeable difference steal food from the mouth of its host as the host
between the bee louse and varroa is the presence is fed, or is feeding another bee. There is some
of six legs on the bee louse while varroa has eight. evidence that bee louse adults can induce regur-
Further, the adult bee louse has a raised appear- gitation from the bees. They accomplish this by
ance while varroa are flatter and more oval than scratching the upper edge of the bees labrum
the bee louse. Despite this, both are very small and until the bee extends its tongue, at which time
difficult for most people to distinguish with the they will feed on food or other secretions that
naked eye. the bee offers.
The eyes of adult bee lice are located just Bee louse eggs are white, oval shaped, and
above the antennae. They occur as pale spots on have two lateral flanges. The flanges are flat and
the surface of the cuticle and are surrounded by extend parallel to each other toward the long axis
pigmented chitinous rings. The terminal joint of a of the egg. The eggs range from 0.780.81 mm
bee louses 5-segmented tarsi is divided and modi- long and 0.280.33 mm wide without the flanges.
fied with comb-like teeth, an adaptation that allows Including flanges, the eggs average 0.840.42 mm
the fly to cling to bees. The thorax is very short. (l x w). Female bee lice can oviposit a number of
When viewed dorsally, it is less than half as long as places in the bee nest (empty cells, brood cappings,
the head, resembling an abdominal segment. The debris on the floor) but only eggs oviposited on
scutellum is absent. honey cappings hatch. The incubation period of
Presumably, bee louse adults feed on nectar the egg can range from 27.4 days, depending on
and pollen, as well as food and other excretions the season.
passed between adult bees trophallactically. After the incubation period, larvae emerge
Regarding the latter, bee louse adults often are from the eggs oviposited on the waxy cappings of
found on the heads of workers, drones, and espe- honey comb. Upon emergence, the larvae con-
cially queens. More than 180 bee louse adults have struct a tunnel under the cell cappings. This is the
been found on a single queen. most noticeable damage attributed to the bee
 Bees (Hymenoptera: Apoidea: Apiformes)
B 419

louse. Larvae tunneling under the cell cappings Bee Mites

can visually taint the waxy cappings. Although
some consider this damage, it is of minor eco- Some species of mites (Acarina) can be serious
nomic importance. Regardless, the intersecting pests of honey bees.
tunnels are a common sign of bee louse presence. Varroa Mites, Tracheal Mite, Mites
Many beekeepers have seen this damage but few
recognize it for what it is. It is believed that bee
lice larvae feed on honey and pollen residues
encountered while tunneling under the cell cap- Bees (Hymenoptera: Apoidea:
pings. There is a modicum of control suggestions Apiformes)
for the bee louse, largely because it is not consid-
ered a major pest. However, many of the synthetic james h. cane
pesticides used against varroa also demonstrate USDA-ARS Bee Biology and Systematics
activity against the bee louse. Laboratory, Utah State University, Logan,
Larvae of the bee louse have three larval UT, USA
instars, ranging from 7.110.8 days. Following this
time, the larvae become prepupae, a stage that can Bees essentially are wasps that turned to pollen for
last from 12.7 days. During this time, the prepupa dietary protein. A combination of distinctive fea-
has a creamy-white appearance. The developing tures, taken together, make bees unique among
pupa is enclosed in the larval skin. The white/yel- insects. (i) Sociality, characterized by overlapping
lowish pupae are 1.41.7 mm long0.50.75 mm generations, cooperative brood care and a repro-
wide. The life cycle begins again as the adult fly ductive division of labor between fertile queens
emerges. and sterile female workers, has evolved multiple
times within the bee lineage. Presumptive interme-
diate stages of sociality are represented by at least
several living species, and thus are available for
Reference observation, evolutionary study, and experimental
manipulation. (ii) Bees, unlike most other herbivo-
Morse RA, Flottum K (eds) (1998) Honey bee pests, preda- rous insects, dine solely on pollen and nectar or
tors, and diseases, 3rd edn. A.I. Root Company, Medina, floral oils. This dietary transition from their car-
OH, 718 pp
nivorous ancestors was accompanied by the evolu-
tion of branched body hairs which aid bees in
picking up pollen, plus modification of the hind
legs or ventral abdominal surface for carrying large
Bee Milk loads of pollen. These features typically distinguish
bees from wasps. (iii) Unlike most insects, each
Also called royal jelly, this is a substance that is adult female of every non-parasitic bee species,
secreted by Apis nurse bees from a gland on whether social or not, rears her young in a nest.
their head (the hypopharangeal gland), mixed Thus, all food and shelter needs of bee larvae are
with crop contents, and fed to bee larvae. All provided by their mother, or one or more sisters if
bees are fed bee milk for the first 3 days, but lar- the species is social, or the host female if the species
vae destined to become queens are fed this is parasitic. (iv) From the central nest, females daily
material throughout their larval development venture forth repeatedly on spatially extensive
whereas future workers are switched to nectar foraging trips to acquire floral resources for their
and pollen. brood. These trips require remarkable navigational
420
B Bees (Hymenoptera: Apoidea: Apiformes)

skills equaled by few other insect taxa. (v) As a con- Circle. Only social bees achieve maximum diver-
sequence of their extensive foraging at flowers, bees sity in lowland tropical rainforests. Non-social (or
have become the primary biotic agents of pollina- solitary) species are most diverse in drier, more
tion for continental floras worldwide. No other seasonal biomes of the world s temperate zones.
animal group so dominates this, or the other great These include the Mediterranean Basin and areas
plant-animal mutualism, seed dispersal. of similar climate around the world (e.g., western
South Africa, southern California, central Chile
and Argentina, much of Australia) and the more
vegetated,warm deserts (e.g.,Sonoran,Chihuahuan
Evolutionary History and Colorado deserts of the southwestern U.S. and
adjacent Mexico). Warmer grasslands also can be
Bees (Hymenoptera: Apoidea: Apiformes) likely productive, such as the Great Plains of the U.S. In
arose in the Cretaceous, perhaps 120 million these regions, several hundred bee species can be
years ago, when they diverged from the carnivo- easily expected in any given locality.
rous habits of their closest relatives, the sand
wasps (Hymenoptera: Apoidea: Spheciformes).
Flowering plants (angiosperms) had made their
debut by this time. Most paleontological material Development and Life Cycle
consists of bees entombed in amber (polymer-
ized tree resins) millennia later. Specimens from Like other insects with complete metamorphosis,
the Eocene (40 million years ago) are common. bees pass through four discrete life stages (Fig.25).
They are typically workers of the stingless bees Bee eggs are sausage-shaped. Those of the solitary,
(Meliponini) that probably became mired while non-parasitic species can be proportionally huge
gathering resin to seal their nest cavities. These for an insect; eggs of some large carpenter bees
represent highly evolved social genera that (Xylocopa) are 16 mm long. Non-social bee spe-
remain extant today, suggesting a much earlier cies are much less fecund than most insects, lay-
origin for bees. Tantalizing casts of much earlier ing only 1025 eggs in their lifetimes, averaging
fossil nest cells are also reported, but their identity one to two per day. As with other Hymenoptera,
remains controversial. progeny sex is determined by egg fertilization:
male eggs remain unfertilized and are thus, hap-
loid. Bee larvae are gently curved, soft, white,
blind, largely immobile and defenseless grubs.
Diversity and Distribution Only specialized instars of some cleptoparasitic
species are mobile and armed with powerful
There are more species of bees today than the sum mandibles, adaptations that they use to assassi-
total of mammals, reptiles, amphibians and birds; nate host larvae before consuming the host s
17,000 species of bees have been described, per- provision masses.
haps another 10,000 await discovery. They are dis- Larvae of nearly all solitary species and most
tributed among only seven families. The largest eusocial species receive an individual cache, or
genus (Andrena) has 1,400 described species; mass provision, of pollen moistened with nectar,
many have more than 100. Bees are native to all or occasionally, floral oils. Provision shape and
continents but Antarctica. Few species are found consistency varies from firm, spherical pellets to a
on isolated oceanic islands, but ranges of some soupy gruel on which the larva actually floats.
hardy species extend well north of the Arctic Larvae pass through four molts (so five instars) to
 Bees (Hymenoptera: Apoidea: Apiformes)
B 421

Bees (Hymenoptera: Apoidea: Apiformes), Figure 25 Bee life cycle, illustrated using the alkali bee,
Nomia melanderi (Halictidae): (top left) egg atop a completed provision mass. Note the
polished waterproof cell lining applied to the soil matrix; (top right) third instar larva feeding
on remaining provision; (lower left) prepupa, the post-feeding larval resting stage; (lower right) two
pupae (removed from their nest cells) (photos by William Nye).
422
B Bees (Hymenoptera: Apoidea: Apiformes)

accommodate their rapid growth, consuming Other bee species nest above ground, excavating
theirprovision mass in a few weeks. Larvae do not pithy stems of plants or adopting abandoned
defecate until they are mature. Once the provision tunnels chewed by wood-boring larvae of beetles
mass is consumed, larvae of many (but not all) and some other insects. Some carpenter bees
species then spin a cocoon. The final larval stage is (Xylocopa) can chew tunnels directly into sound
the prepupa, which is more robust and resistant to wood. The highly social honey bees and stingless
desiccation than the earlier instars, but still grub- bees often build their nests in hollow tree cavities.
like. This is the typical resting, or diapause, stage Free-standing nests are made by a few paleotropi-
for those temperate-zone species whose single cal honey bees (pendant wax combs) and a few
adult generation flies later in spring or summer. other bees (mostly orchid bees and some
Unlike most other insects, bees do not weather megachilids that use clay or resin).
inhospitable seasons as pupae. Rather, bee pupae
are quite delicate, resembling waxen versions of
the adult. If a bee species is one that flies in the Mating Biology
early spring (allowing little warmth for further
development), then the pupal stage lasts only a few Male bees do not contribute to nesting (excava-
weeks, yielding an adult that will remain in the tion, foraging, defense) (Fig.26). With few excep-
cocoon (or nest cell) to overwinter. Some tions, males are not welcome in the nest. They
halictids (sweat bees), as well as bumble bees, spend their days patrolling for receptive conspe-
emerge as adults, mate, and then disperse before cific females, and their nights sleeping on flowers
overwintering. or vegetation, or in shallow burrows underground.
Males of various species enhance their encounter
rates with females using one or more search and/
Nesting or advertisement strategies employing scent and
vision. Among non-social species, males are often
All larval bees live in a nest selected, constructed, protandrous, emerging some days before females
maintained, defended and provisioned by their of the year. Males of floral specialists may patrol
mother, sisters (social species) or host (parasitic preferred floral hosts, especially if females of their
bee). A genus of bee often can be recognized by its species mate repeatedly during their lifetimes.
nesting substrate and nest architecture. Most bee Males also may patrol nesting sites; among species
species nest underground, typically excavating a whose females mate but once and whose nests are
central, cylindrical tunnel that is either partitioned aggregated, males may compete intensively to find
into nest cells, or from which lateral tunnels branch freshly emerged virgin females, guided by the
that terminate in nest cells. Soil cliffs as well as virgin females scent. Conversely, males may apply
more horizontal surfaces are used. Excavated soil scent-marks to attract females to a sort of trapline
on horizontal surfaces is often heaped in a small that males patrol. These can sometimes extend for
cone or delta of irregularly sized pellets, the hundreds of meters. Honey bees, some bumble
tumulus. Nest depths differ among species, rang- bees and large carpenter bees maintain aerial ter-
ing from a few centimeters to several meters if in ritories. Some orchid bees reportedly form leks
sandier soils. Cells are often egg- or barrel-shaped, perfumed with scents synthesized from floral oils
just large enough for a mother bee to fit with her of orchids. A few recent cases report flightless
assembled provision mass. Cell walls are com- males that linger in their natal nests to mate with
monly smoothed, even polished, usually with the their sisters. In general, courting and mating are
addition of a secreted waxy or membranous brief affairs for bees. Most species are monandrous,
waterproof lining, or alternatively, plant resin. each female mating but once in her lifetime. All
 Bees (Hymenoptera: Apoidea: Apiformes)
B 423

Sociality

Bees have lineages representing all degrees and

hypothesized evolutionary steps of sociality, includ-
ing reversion to solitary habits. Populations of a
few species range from solitary to social depending
on ecological circumstance. Less social arrange-
ments include: communal species, wherein repro-
ductive females sometimes share in a single nests
construction and defense but otherwise act soli-
tarily; semisocial colonies founded by a group of
(likely) sisters; subsocial species in which mothers
actively care for growing daughters, that in turn
may linger as adults to aid their mother; and several
other much rarer arrangements. Many non-social
species, especially ground-nesters, will nest
gregariously (Fig.27) in populous aggregations of
hundreds to many thousands of individuals.
During adult activity, these bee cities can be
dramatic, with a dense traffic of foragers and patrol-
ling males producing a loud, daylong hum.
The hallmarks of higher sociality (eusocial-
ity) are an overlap of generations (mothers and
daughters), cooperative brood care by workers,
and reproductive division of labor (queens and
workers). Workers are rarely, if ever, mated, and so,
if they lay eggs, these are male. For primitively
eusocial species (some sweat bees and carpenter
bees, nearly all bumble bees), nests are founded in
the spring by a single, mated female (gyne), as with
solitary species. In rare cases, there are several
foundresses. This mother bee builds a nest and
prepares cells. Each cell receives a ball (Figs.28 and 29)
Bees (Hymenoptera: Apoidea: Apiformes), Figure 26 of pollen moistened with nectar and a single egg.
Mating adults (above), male atop female (photo by The cell is then sealed. Emerging daughters remain
William Nye); aggregation of males (center) sleeping with the nest rather than dispersing, helping their
together atop plant stem (photo by William Nye); mother construct, provision and defend her nest.
female at nest entrance (below). (photo by The original foundress, mother to the nest, then
James Cane). becomes the colonys primary egg-layer (queen).
The more eusocial species have morphologically
female bees are able to store live sperm to varying distinct queens and workers. Primitively eusocial
degrees; at the extreme, queens of social species colonies grow to, at most, a few hundred workers.
store live male sperm for months or even years. Late in the summer or early autumn, reproduc-
Hence, sperm often outlive the male bees that tives are produced, and mate; only the future
produce them. queens pass the winter in diapause.
424
B Bees (Hymenoptera: Apoidea: Apiformes)

CORE
TUMULUS

SCARAB BURROW

4.0 cm

FILL

5
4
3

FECES

6
8
POLLEN

7 FOOD LOAF

Bees (Hymenoptera: Apoidea: Apiformes), Figure 27 Gregarious nesting (above left) showing dark soil
tumuli atop a square meter of soil surface (photo by James Cane); core (1 cu. ft.) of nesting soil (above
right) from alkali bee nesting aggregation, showing numerous white prepupae in their individual nest
cells (photo by William Nye); schematic (below) of an excavated subterranean nest of the neotropical bee
Tapinotaspis tucumana (Apidae). Nests and enlarged views of three nest cells (Reproduced with permis-
sion from the American Museum of Natural History. Artwork by Jerome Rozen, Jr.).
 Bees (Hymenoptera: Apoidea: Apiformes)
B 425

Bees (Hymenoptera: Apoidea: Apiformes), Figure 28 Laboratory nest of the bumble bee Bombus
morrisoni (Apidae) (above left) showing nest cells and honey pots clustered amid insulative cotton
batting; Nest of a Brazilian Melipona sp. (Apidae)(above right). The thin pliable sheets of the involucrum
(i) have been peeled back to reveal the topmost tier of horizontal combs (c). Between the involucrum
and the wall of the cavity are the large pollen pots and honey pots (h). Honey is visible in those pots
that remain open (Photo by James Cane); adult female of the cleptoparasitic bee, Triepeolus dacotensis
(Nomadinae) (lower left). Note paucity of hairs, lack of pollen-transporting structures, and the e xserted
sting; first instar assassin larva of Triepeolus dacotensis (Nomadinae) (lower right). Note its long
recurved mandibles, which are used to grip and kill the host egg or young larva. Subsequent instars
resemble normal bee larvae (photos by William Nye).

Only the stingless bees (Meliponini) and i ndividuals of cleptoparasitic species, it is only for
honey bees (Apis) are highly eusocial. Most reside self-maintenance and sometimes mates. All other
in the humid tropics. Their colonies are tightly females seek, gather and transport nutritious
integrated and perennial, populated by thousands substances (typically pollen and nectar) and
of workers headed by long-lived queens that are sometimes, nesting materials for their progeny.
dependent on worker care. Their colonies repro- Species of honey bee size will regularly fly a kilo-
duce by fissioning, when swarms of workers meter or more to desirable bloom. Using the sun
accompany a queen to found a new colony. and local landmarks for navigation, they can then
fly directly home at 1525 kilometers per hour to
find a nest entrance that is often no bigger than
Foraging the bee, and, in the case of gregarious species, that
is imbedded in an aggregation of hundreds or
Except for queens and drones of highly eusocial thousands of like-looking entrances of their
species, all bees visit flowers. For males and conspecifics.
426
B Bees (Hymenoptera: Apoidea: Apiformes)

toxic. A retractable, complex proboscis allows bees

to sip or lap nectar. A bees access to nectar is
constrained by body size, tongue length, and the
flowers dimensions. Some carpenter bees, sting-
less bees and bumble bees regularly rob deep,
tubular flowers of their nectar by perforating the
corolla near its basal nectaries. Perhaps because
bees can readily assess nectar volume, sugar
constitution and its concentration, individuals and
species can and will compare nectar yields of
various flowering species, optimally choosing the
most rewarding species at any given time. Some
flowers, mostly tropical, secrete calorically rich
oils rather than nectar. These are mopped or wiped
up by bee species that have pads and squeegees
of hairs specialized for the task, to be incorporated
into larval provisions and sometimes, nest cell lin-
ings. Some ground-nesting species and many
eusocial species synthesize and secrete their own
calorically rich substances that they blend into
progeny provisions.
Bees also seek pollen at flowers, which is their
key dietary source of proteins, fats, minerals and
sometimes starches, for themselves and their off-
spring. Pollen, of course, also contains the male
gametes of flowering plants, so it really serves two
reproductive purposes, plant ovule fertilization
and bee reproduction. No effective dietary substi-
tute for pollen has yet been devised for bees. Few
animals match the nitrogen assimilation efficiency
of bees, despite the indigestibility of the external
shell, exine, of pollen grains.
Pollen, in most cases, dusts the foraging bee as
Bees (Hymenoptera: Apoidea: Apiformes), Figure a powder that lodges in the vesture of branched
29 Cast of nest cell of Anthophora (Apidae) (above); hairs that envelop its body. Harvest may be
provisioned nest cell of ground-nesting Colletes enhanced by buzzing, biting, scraping and scrab-
(Colletidae), showing the thin, translucent membrane bling. Many specialized structures, hairs and
made of secreted polyesters (center); larvae of parasitic behaviors of foraging females then work in con-
Melittobia wasps (Hymenoptera: Eulophidae) in nest cert to efficiently groom and accumulate pollen
cell of an Osmia bee (below) (photos by William Nye). from the body for transport. Pollen is transported
in a brush of hairs called a scopa, often on the
Bees always take nectar at flowers. Nectar hind legs (or under the abdomen of megachilids).
powers bees flight and contributes carbohydrates A few taxa carry pollen internally in their crop
and water to larval diets. Typical nectar sugars are (e.g., Hylaeus). Bumble bees, honey bees, orchid
glucose, fructose and sucrose. Few nectars are bees and stingless bees carry pollen in a pollen
 Bees (Hymenoptera: Apoidea: Apiformes)
B 427

basket, or corbicula, on the hind leg, a smooth, Pollination

slightly concave surface surrounded by guard hairs
that holds a damp pollen pellet. Bees are the most important and cosmopolitan
Anthers of some flowers (e.g., tomato and biotic pollination agents in most continental
blueberry) shed their pollen through apical pores habitats, and for most prevalent plant families, such
or slits like a salt shaker. These require vibration to as the Asteraceae, Fabaceae, Lamiaceae, Orchidaceae,
dispense their content of pollen. Some bees shake Rosaceae and Solanaceae. Few nocturnal flowers
this pollen free by battering or stroking the anthers are pollinated by bees. Reciprocal co-evolution
with their legs, while others bite the anthers to between bees and their flowers seems, at best,
squeeze out pollen. Species of many genera can diffuse in nearly all cases, although adaptations
shiver their flight muscles while on the flower, that enhance attraction, resource extraction and
sonicating these anthers to eject their content of pollination are evident everywhere. Most collected
pollen. This buzzing is audible. The effect can be pollen ends up in a larval provision, not on a flow-
duplicated with a vibrating tuning fork. Bumble ers stigma, but bees are still vastly more efficient
bees frequently use this method of pollen extrac- than wind in moving pollen to receptive flowers.
tion, even for flowers with anthers of normal Bees are essential pollinators of some vegetable
morphology. crops (or their seeds), many prominent fruit and
Many bee species are floral generalists seed-oil crops, forage legumes and a few nut or
(polylectic), taking pollen from many taxa of fiber crops. Crops that contribute the starches and
flowers, a necessity for the long-lived colonies of refined sugars to the human diet are typically wind-
social bees. Foraging individuals often will display pollinated or vegetatively propagated. Home and
floral constancy, selectively visiting sequences of market gardeners benefit from pollination services
conspecific flowers on a given foraging trip, despite of wild bees. In large mechanized agriculture, how-
the availability of alternatives. Such preferences ever, only hived honey bees can generally supply
are labile, perhaps reflecting learning or memory the millions of inexpensive foragers needed for
constraints. In contrast, a third or more of the non- pollination. In the past half-century, though, a
social species in a community may be oligolectic. growing minority of tree fruit, forage seed and
This is a fixed species-specific predilection to greenhouse crops are benefiting from pollination
collect pollen from the same small subset of avail- services of managed solitary bees and bumble bees
able flowering species, commonly one or several (rather than honey bees), a trend that seems likely
related genera within a plant family. Such unwav- to continue, given their often superior pollination
ering fidelity is particularly common among desert efficiencies and the devastating effects of new pest
bee faunas and vernal bees of the temperate zone. problems suffered by honey bees.
The reason(s) for oligolecty are not fully under-
stood. In some cases, oligoleges seem to accumulate
at reliable pollen hosts that produce generous quan- Diseases, Parasites and Predators
tities of pollen (e.g., willow, sunflowers, creosote
bush, and blueberries). For other species, the associ- Among insects, the superior life expectancies of
ation seems to reflect phenological specializations bees result largely from superior maternal care of
(e.g., crepuscular flowers, early spring blooms) or offspring. Females actively deter predators and
more or less private floral resources eschewed by parasites by biting, stinging and by use of chemical
other species (e.g., oil flowers of Lysimachia and repellents. Nest cells are waterproofed and possibly
their associated Macropis bees). Unlike insect fumigated with applied glandular secretions or
herbivory, host chemical defenses rarely, if ever, plant resins. Despite such extensive maternal care
dictate floral specialization by bees. and defenses, bees are nonetheless plagued by
428
B Bees (Hymenoptera: Apoidea: Apiformes)

iseases, parasites and predators. Feeding larvae, in

d c onstructs that are extensive, monotonous and
particular, succumb to various viral, bacterial inhospitable (e.g., lawns, parking lots, wheat fields)
and fungal diseases. Microorganisms commonly fail to fulfill bees nesting and/or foraging needs,
spoil provision masses, too. Nematodes and mites although bees can readily fly through a finer patch-
(mostly external) are ubiquitous bee parasites. work mosaic of these features if interspersed with
Many larval insects devour the contents of bee favorable nesting and foraging habitats. Unlike
nests, including clerid and meloid beetles. Others accidental or misguided introductions of plants,
are internal or external parasitoids, including vertebrates and shellfish, exotic bees have generally
chalcidoid wasps, bombyliid flies and strepsipter- been of little ecological consequence, although
ans. The elaborate structural defenses of stingless ill-guided international trade (or smuggling) of
bee nests attest to the intense predation pressures honey bees and bumble bees has been disastrous
of ants and social parasites of the tropics. Adult in some recent cases. The greatest risk attending
bees are subject to the myriad predators of other intercontinental transport of live bees is likely to
mobile insects. be the inadvertent transport of diseases and pests,
Cleptoparasitic, or cuckoo bees, are analogous such as those that are currently devastating
to cowbirds and European cuckoos, surreptitiously apiculture, especially Varroa and tracheal mites.
inserting their eggs into the provisioned nest cells
of their bee hosts. There are thousands of clep-
toparasitic species, most associated with specific The Families of Bees
genera of host bees. They directly or indirectly
exterminate the host larva, ultimately consuming Seven families of bees are currently recognized.
its provision. Adult females spend much of the day The Colletidae, Halictidae, Andrenidae, Melittidae
searching for and evaluating host nests. They dis- and Stenotritidae are grouped as short-tongued
play numerous subtle adaptations to conceal their bees, while the Megachilidae and Apidae are long-
eggs from the host female and repair damage tongued bees. The five more common families are
incurred to nest cells during oviposition. Odor considered here.
concealment and mimicry may be practiced as
well. Social bee species (other than Apis) host their
own parasitic bees, often evolving from within Family Colletidae: Yellow-Faced,
their hosts genus. Psithyrus queens usurp bumble Masked and Plasterer Bees
bee nests, enslaving unwitting host workers to
produce parasite progeny. Robber genera among Distribution: Worldwide, but Greatest Diversity is
the stingless bees (e.g., Lestrimelitta) raid host in the Southern Hemisphere, Including Australia.
nests for honey and pollen. This is probably the oldest extant bee family. No
studied species nests socially. Pollen is transported
dry in hair brushes of the hind leg (e.g., Colletes)
Conservation or mixed with nectar and carried internally in the
crop (e.g., Hylaeus). Their tongue tips are
Human activities also can harm bees. Bees tend to distinctively bilobed. They nest underground, or
be sensitive to broad-spectrum insecticides, which rarely, in mortar and even sandstone (e.g., Colletes),
if used indiscriminately or carelessly by farmers or in pithy stems (e.g., Hylaeus), or adopt holes in
homeowners during bloom, can poison adults, or wood. The plasterer bees are so named for the
later, their progeny. No genetic resistance has been peculiar, secreted, transparent, polyester membranes
shown. Herbicides, when used to kill wildflowers, used to waterproof their nest cells; those of Hylaeus
remove available forage for bees. Habitats and contain silk strands. Hylaeus (=Prosopis) (570 species)
 Bees (Hymenoptera: Apoidea: Apiformes)
B 429

and Colletes (330 species) are the commonly sometimes in dense aggregations. The common,
encountered genera in the U.S. and Europe; cosmopolitan cleptoparasite genus in the family is
Leioproctus has 300+ species in Australia and Sphecodes (250 species). Halictids illustrate an
temperate South America; Nesoprosopis has radi- unprecedented diversity of social organization,
ated in the Hawaiian Islands, where many of its particularly among the 1,000+ species of
species appear to be endangered. This subgenus Lasioglossum.
contains the only cleptoparasites in the family. The alkali bee, Nomia melanderi, is the worlds
Hylaeus may be the most cosmopolitan of all bee only intensively managed ground-nesting bee. In
genera, found on all continents but Antarctica as regions of the western U.S., alfalfa (=lucerne) seed
well as many oceanic islands, their dispersal growers construct large subirrigated nest sites with
facilitated by their stem-nesting habits. salt-crusted surfaces. Densities of 400 nests/m2
over a hectare or more can be obtained with this
gregarious bee. Nest sites can remain populous for
Family: Andrenidae more than 50 years. Another effective alfalfa
pollinator, Rhophitoides canus, is less intensively
Distribution: Worldwide, Except Australia, Rare managed in regions of eastern Europe for alfalfa
in the Moist Tropics. Species of this family nest seed production.
underground. The family includes two enormous
genera: Andrena (1,400 species, ubiquitous in
north temperate regions) and Perdita (600 or Family Megachilidae: Leaf-Cutting
more species, mostly of the American Southwest Bees, Mason Bees, Carder Bees and
and northern Mexico). Perdita are small-bodied, Others
including the tiniest bee, Perdita minima (slen-
der, 2 mm long, 1/3 mg). A few species of Perdita, Distribution: Worldwide. The common names for
Andrena and Panurgus nest communally; no groups in this large family refer to the remark-
studied andrenid is social. There are no clep- able diversity of exogenous materials that they
toparasitic species in this family. Pollen is car- typically use to line or construct their nest cells.
ried on the hind legs, and in some species, is Many nest above ground in twigs, stems and
moistened with nectar. Probably all Perdita are wood, and will readily adopt drilled holes in these
oligolectic, as are the majority of Andrena and substrates (termed trap nests). A few even nest
species of other genera. in abandoned snail shells. Megachile and others
line their nest cells, and partition and cap their
nest tunnels, with strips and disks neatly cut from
Family Halictidae: Sweat Bees, leaves or petals; other species build with leaf pulp,
Alkali Bee, etc resin, nectar, mud, plant hairs, or pebbles. Forag-
ing females of non-parasitic species can be easily
Distribution: Worldwide. Most halictids are small recognized, as they are unique in (Fig.30) carry-
or medium sized. Some taxa are commonly known ing pollen in a scopa solely beneath the abdomen.
as sweat bees because they alight on peoples skin Nearly all species are solitary. There are several
to lap up sweat for the salts that it contains. Many cleptoparasitic genera (notably Coelioxys, 300 spe-
halictids are darkly colored, others are a brassy or cies). Megachile is a cosmopolitan genus (900+
brilliant emerald green. Some Nomia have striking species); Osmia (300 species) are common in the
pearly green or orange abdominal bands. Pollen is Northern Hemisphere. The worlds longest bee is
carried on the hind legs, typically dry. Their nests Megachile pluto at 39 mm. Many megachilids are
are burrows in soil, or occasionally, rotting wood, important pollinators, especially for plants in the
430
B Bees (Hymenoptera: Apoidea: Apiformes)

pea and clover family (Fabaceae). The cavity-nesting

species are the most successful stowaways in
transoceanic travel.
The alfalfa leaf-cutting bee, Megachile rotun-
data, came to the U.S. from the Near East as a stow-
away before 1937. Burgeoning feral populations of
this bee prospered in the semi-arid western U.S.
The species value as an alfalfa pollinator soon
became apparent. A multimillion-dollar industry
developed in North America for cheaply mass rear-
ing of this species for sale to alfalfa seed growers.
Wooden or foam boards, each with several thou-
sand nesting holes, are placed in shelters in alfalfa
fields. Each shelter receives 50,000 or more females.
This bee is versatile, pollinating other crops too,
such as hybrid canola and various vegetable seeds.
Several species of mason bees in the genus
Osmia are more recently being managed in Japan,
the U.S. and Europe to pollinate tree crops in the
rose family, such as apples, plums, sweet cherries and
almonds. One of these species has been dubbed the
blue orchard mason bee. Only 250300 blue orchard
bees are needed to pollinate as many apple or cherry
flowers as two to three hives of honey bees.

Family Apidae: Carpenter Bees,

Orchid Bees, Bumble Bees,
Stingless Bees, Honey Bees

Distribution: Worldwide. This family is large, eco-

Bees (Hymenoptera: Apoidea: Apiformes), logically diverse and continues to be taxonomically
Figure 30 Nest of Osmia (Megachilidae) in reed, perplexing. One or more tribes of this family is most
split open to reveal partitioned nest cells each closely related to the lineage that evolved into todays
occupied by a single larva with its mass provision of highly eusocial Apinae. Many cleptoparasitic species
pollen moistened with nectar (above); three nests are included (1,600 species). This unwieldy group is
of a leaf-cutting bee (Megachile: Megachilidae), best recognized by its constituent tribes, of which
consisting of a linear series of cells each wrapped there are many. Select ones are treated here.
with cut leaf pieces (center); female of the alfalfa leaf
cutting bee, Megachile rotundata, visiting alfalfa
flowers (below). Note the pollen load carried dry in Subfamily Nomadinae: Cuckoo Bees
a scopa of hairs beneath her abdomen. To the right
is a "tripped" flower, the staminal column pressed Distribution: Worldwide. This is the largest group
against the banner petal. Good alfalfa pollinators of cleptoparasitic bees (Nomada alone has 800
trip the flowers frequently (photos by William Nye). species). Most species are glossy, quite hairless
 Bees (Hymenoptera: Apoidea: Apiformes)
B 431

and wasp-like with a rugged exoskeleton. They orchid flowers and, in the process, pollinate the
can commonly be seen patrolling low over the orchids. The orchids provide no food, but rather
ground for host nests. produce scents which male euglossines collect
and place in a glandular pocket of their enlarged
hind legs. These perfumes attract mates. Several
Subfamily Xylocopinae: Carpenter species have intricate male displays. These large
Bees bees are flying jewels, sporting metallic emerald,
cobalt, violet and bronze colors as well as red,
Distribution: Worldwide. Carpenter bees typically orange and yellow. They are important pollinators
excavate nests above ground in pithy stems or even of many endangered tropical orchids and proba-
bore into sound wood. Cells are unlined. Most bly the Brazil nut, too.
species are solitary, but some are subsocial or even
primitively eusocial. Females overwinter as mated
adults; they can be very long-lived. The large car- Tribe Bombini: Bumble Bees
penter bees (Xylocopa) are primarily tropical. They
can resemble bumble bees, but have a smooth, Distribution: The Americas, Europe, Asia, North
glossy dorsal abdomen and transport their pollen Africa. Bumble bees (Bombus) are large, furry,
dry. Xylocopa pollinate commercial passion fruit; often black and yellow, orange or red bees. They
they are also adept nectar robbers. Males of some are common in the worlds cooler climates, follow-
Xylocopa hover for hours in aerial territories, pur- ing mountain ranges into the tropics. Few species
suing any and all small airborne objects. The small live in deserts or rainforests. They nest shallowly
carpenter bees (Ceratina) nest in dead stems of underground, often in abandoned rodent nests, or
roses, sumac, elderberry and some grasses. sometimes above ground, either in tree cavities or,
less commonly, beneath a leaf heap on the forest
floor. They actively brood larvae to warm them,
The Corbiculate Apinae: Orchid and fan their wings at the colony entrance to cool
Bees, Bumble Bees, Stingless Bees, its contents. Few other bees can fly in cooler
Honey Bees weather. Bombus consists of primitively eusocial
species and a lesser number of social parasites.
Distribution: Worldwide. This quartet of tribes They are important pollinators in alpine, boreal
contains all of the highly eusocial bees, as well as and subarctic habitats. Queens of species such
the primitively eusocial bumble bees and the as B. nevadensis and B. dahlbomi are the worlds
mostly solitary orchid bees. All secrete wax, which most massive bees, weighing a gram or more (the
they incorporate into their nest structures. They weight of a raw almond).
carry pollen on a specially adapted, smooth region Bumble bees are important pollinators of
of the hind leg referred to as the pollen basket or several crops, especially red and crimson clover.
corbicula. Taxonomists formerly grouped these The honey bee proboscis is too short to probe such
four tribes as a separate family. deeply tubular flowers. Bumble bees, having longer
tongues, work these flowers efficiently. Bumble
bees have been imported into New Zealand and
Tribe Euglossini: Orchid Bees Chile for clover pollination. They aid in the
pollination of several other crops like alfalfa, and
Distribution: New World Tropics, from Central several fruits, especially blueberries, cranberries
Mexico into Argentina. The orchid bees are so and kiwi. A multimillion-dollar global business has
named because the males collect scents from emerged from Europe for year-round propagation
432
B Bees (Hymenoptera: Apoidea: Apiformes)

of disposable bumble bee colonies to pollinate Colony fission is unlike Apis, because for meli-
greenhouse vegetables like tomatoes, peppers, egg- ponines, the new home is selected and furnished
plants and squashes. Introduction of these few before the swarm issues from the parent colony.
managed species outside of their native ranges can Workers assemble a complete new nest using mate-
lead to feral populations that pose problems for rials transported from the parent colony. Only then
native Bombus and perhaps other bees. does a group of workers and new queen fly to the
new nest. The old queen is too large to fly and
remains with the parent colony and its workers.
Tribe Meliponini: Stingless Bees Workers of some stingless bees recruit nest-
mates to food sources, but in ways different from
Distribution: Old and New World Tropics. The Apis. Scouts of some species scentmark trails from
stingless bees are highly eusocial, and as a group, productive flowers to the nest, depositing mandib-
exhibit a sweeping diversity of adaptations and ular gland secretions on surfaces every few meters.
natural history traits. Their permanent colonies Returning to the nest, this scout buzzes loudly; the
can be populous, containing between 300 and longer the buzz, the greater the distance of the food
80,000 workers. Although stingless, many can from the colony. The scouts behavior excites others
defend their nests with irritating bites sometimes which follow the odor trail to the resource. This
accompanied by caustic secretions. Queens are method of recruitment communicates not only the
morphologically distinct from workers, their direction and distance of food from the nest, but
status sometimes determined genetically, in other can lead other foragers directly to the food at any
cases as an individual larvas reproductive gamble. height by means of the odor trail. This three-di-
Of the 260 known species, 70% are found in mensional road map is especially adaptive in tow-
Central and South America. They are the most ering tropical forests where flowers are frequently
common insects in Dominican and Baltic amber. found high in the leafy canopy.
Stingless bees usually build nests in tree Stingless bees benefit people in several ways.
hollows, although some species nest on exposed In the Neotropics, Melipona colonies are cultured
surfaces, in underground cavities, or in termite for honey in special wooden hives, although yields
or ant nests. Workers fashion a hard shell of are meager (25 pounds per year). Stingless bees
batumen for the nest, consisting of wax blended pollinate numerous tropical crops, but their eco-
with resin, mud or vegetation. Intricate nest nomic impact has not been widely estimated.
entrance platforms and tubes are fashioned from Stingless bees are promising pollinators for green-
wax, resin, or even plant latex. Within this shell, house crops.
honey and pollen are stored in large irregular
waxen pots. These rim the brood chamber, whose
exterior is delineated by layers of pliable, delicate
sheets of the involucrum, made of insulative wax Tribe Apini: True Honey Bees
imbued with resin. Within this chamber are the
waxen combs dedicated to brood rearing, grouped Distribution: Europe, Asia, Africa, Now Intro-
in horizontal tiers supported by thin pillars, remi- duced to all Continents Except Antarctica. There
niscent of nests of hornets or yellow-jacket wasps. are 11 currently accepted species of true honey
Cells are typically mass provisioned with pollen, bees, all of the genus Apis. These are very different
honey, and in some genera, glandular secretions from all other bees, such that their evolutionary
(in a few cases, consisting of digested carrion). origins and ancestry remain unresolved. The genus
Some genera (e.g., Lestrimellita) rob nests of other is largely restricted to tropical Asia. Taxonomic
stingless bees for their honey and pollen stores. diversity is centered in Indonesia, Malaysia and
 Bees (Hymenoptera: Apoidea: Apiformes)
B 433

the Philippines, where new species continue to be food, which together with the uniform comb dimen-
discovered. Only the familiar western honey bee sions, yields adults of very consistent size.
or hive bee, A. mellifera, is also native to Europe, Species of Apis can be assigned to one of three
northern Asia, and most of Africa. Its colonization groups, based on body size and nesting habits. Two
of cooler regions was facilitated by its honey stor- dwarf honey bees, exemplified by A. florea, have
age habits that fuels the workers warming of their small colonies of a few thousand small workers
brood. Because we value this species for honey, that construct beneath a branch a single exposed
wax and pollination, and can manage it in trans- comb the size of a waffle. The top of this comb is
portable hives, it has been further introduced broadened horizontally; recruitment dances per-
throughout most of the world. formed on this surface are oriented simply in the
The western honey bee is among the most direction of the food source. Several giant honey
studied animals on the planet. Certainly their hall- bees (e.g., A. dorsata) also build a single exposed
mark behavior is the remarkable abstract dance vertical comb, often in conspicuous groups, but
language performed by foragers and scouts for beneath a stout branch or cliff. Living curtains of
precisely communicating distance, direction and the huge workers envelop the massive comb; when
quality for resources, translating the direction of disturbed, they pour off en masse to assail any
gravity into celestial bearings. Once thought intruder. They are nonetheless robbed for honey.
unique to Apis mellifera, this and other behaviors The remaining species of Apis build nests that con-
now have been observed and studied for some of sist of multiple wax combs housed in a hollow tree
the lesser-known species of Apis, too. or rock cavity. Cavities enhance defense and insu-
Colony activities of Apis require sophisticated lation, but present problems with ventilation for
coordination. Much of the information is commu- temperature, humidity and atmospheric control.
nicated olfactorily using pheromones. Like the The most familiar representatives of this group are
Meliponini, all Apis are highly eusocial, maintain- A. cerana and A. mellifera, which share many simi-
ing populous perennial colonies. Queens, drones larities, including their management in hives.
and workers are morphologically distinct. Among Honey Bees
bees, only worker Apis have a barbed sting that Alfalfa Leafcutting Bee
lodges in the skin and continues to pump venom Apiculture
even after the worker bee has been killed and Orchid Bees
swept away. Colonies reproduce by fissioning, Hymenoptera
again like stingless bees, but in Apis, it is the old Carpenter Bees
queen that departs with the swarm, whose work- Pollination by Osmia Bees
ers then scout out a suitable nesting site at which Pollination and Flower Visitation
they must construct their combs unassisted by the African Honey Bees
parent colony. This seems a riskier strategy, but it Cape Honey Bees
does allow swarms to disperse more widely. Honey
bees thermoregulate their colonies using evapora-
tive as well as convective cooling. Some tropical References
species undertake mass defecation flights to fur-
ther nest cooling. Only Apis produce the familiar Free JB (1993) Insect pollination of crops (2nd ed) Academic
waxen vertical combs of uniform hexagonal cells Press, New York, NY
that are reused over and over to house pollen, nectar Michener CD (2000) The bees of the world. Johns Hopkins
University Press, New York, NY
(as honey) or progeny, although the wax itself can- Michener CD, McGinley RJ, Danforth BN (1994) The bee
not be recycled. Very unusual for bees, larval honey genera of North and Central America (Hymenoptera:
bees are fed progressively rather than with a cache of Apoidea). Smithsonian Institution Press, Washington, DC
434
B Beesoniidae

Mller A, Krebs A, Amiet F (1997) Bienen: Mitteleuropische except for South America. Because it is a tropical
Gattungen, Lebensweise, Beobachtung. Weltbild Verlag,
insect, and lacks a diapause mechanism, it can
Augsburg, Germany
O Toole C, Raw A (1991) Bees of the world. Facts on file, New overwinter successfully only in warm areas or in
York, NY greenhouses. Daytime temperatures below 10C
Prys-Jones OE, Corbet SA (1991) Bumblebees, Revised edi- are deleterious, and it rarely overwinters in areas
tion. Cambridge University Press, Cambridge, UK
Roubik DW (1989) Ecology and natural history of tropical
where frost kills its host plants. Despite its inability
bees. Cambridge University Press, Cambridge, UK to overwinter in cold areas, beet armyworm nev-
Strickler K, Cane J (eds) (2003) Thomas Say publications in ertheless invades temperate areas annually. Despite
entomology: proceedings: for non-native crops, whence this invasive potential, however, it is not normally
pollinators of the future? Entomological Society of
America, Lanham, MD, 204 pp considered a threat in temperate areas, except
Westrich P (1989) Die Wildbienen Baden-Wrttembergs. sometimes in greenhouses.
Allgemeiner Teil: Lebensrume, Verhalten, kologie
und Schutz. Verlag Eugen Ulmer, Stuttgart, Germany

Life History
Beesoniidae
Seasonal activity varies considerably according
A family of insects in the superfamily Coccoidae to climate. In warm locations, all stages can be
(order Hemiptera). found throughout the year, although develop-
Bugs ment rate and overall abundance are reduced
during the winter months. The life cycle can be
completed in as few as 24 days, and six genera-
Beeswax tions have been reared during 5 months of sum-
mer weather in Florida. However, generation
Beeswax is produced by Apis bees. It is produced times of 50126 days have been observed, with a
only by young worker bees. Beeswax consists of total of five generations annually, in southern
fatty acids, esters, and hydrocarbons, and is secreted California.
from glands on the ventral surface of the abdomen. Eggs are laid in clusters of 50150 eggs per
The beeswax is used by the bees to construct hon- mass. Females may deposit over 1,200 eggs during
eycomb cells, in which their young are raised. After their lifetime, but normal egg production is about
removal of honey from the honeycomb, the wax is 300600. Eggs are usually deposited on the lower
purified and used for many products, particularly surface of the leaf, and often near blossoms and
candles, wood furniture polish, shoe polish, lubri- the tip of the branch. The individual eggs are cir-
cants, and skin treatments. cular when viewed from above, but when exam-
ined from the side the egg is slightly peaked,
tapering to a point. The eggs are greenish to white
in color, and covered with a layer of whitish scales
Beet Armyworm, Spodoptera that gives the egg mass a fuzzy or cottony appear-
exigua (Hbner) (Lepidoptera: ance. Eggs hatch in 23 days during warm weather,
Noctuidae) but the incubation period is extended to about 4
days when it is cool. The developmental threshold
john l. capinera for eggs is estimated at 12.4C.
University of Florida Gainesville, FL, USA Normally there are five instars, although addi-
tional instars are sometimes reported. Duration
Beet armyworm is a tropical insect, native to of the instars under warm (summer) conditions
Southeast Asia. It is now found around the world, is reported to be 2.3, 2.2, 1.8, 1.0, and 3.1 days,
 Beet Armyworm, Spodoptera exigua (Hbner) (Lepidoptera: Noctuidae)
B 435

respectively, and at constant 30C, instar develop- and soil particles held together with an oral
ment time was reported to be 2.5, 1.5, 1.2, 1.5, and secretion that hardens when it dries. The pupa is
3.0 days, respectively. Total larval development time light brown in color and measures about 1520
is also influenced by diet quality. The developmen- mm in length. Duration of the pupal stage is 57
tal threshold for larvae is estimated at 13.6C. Only days during warm weather.
1 mm long at hatching, the larvae attain a mean The moths are moderately sized, the wing
length of 2.5, 5.8, 8.9, 13.8, and 22.3 mm during span measuring 2530 mm. The forewings are
instars 15, respectively. Head capsule widths aver- mottled gray and brown, and normally with an
age 0.25, 0.45, 0.70, 1.12, and 1.80 mm, respectively. irregular banding pattern and a light colored bean-
The larvae are pale green or yellow in color shaped spot. The hind wings are a more uniform
during the first two instars, but acquire pale stripes gray or white color, and trimmed with a dark line
during instar 3. During instar 4, larvae are darker at the margin. Mating occurs soon after emergence
dorsally, and possess a dark lateral stripe. Larvae of the moths, and oviposition begins within 23
during instar 5 are quite variable in appearance, days. Oviposition extends over a 37 day period,
tending to be green dorsally with pink or yellow and the moths usually perish within 910 days of
color ventrally and a white stripe laterally. A series emergence.
of dark spots, dashes or triangles (Fig.31) is often This insect has a wide host range, occurring
present dorsally and dorsolaterally. Sometimes as a serious pest of vegetable, field, and flower
larvae are very dark in color. The spiracles are crops; even trees are sometimes attacked. Among
white with a narrow black border. The body is susceptible vegetable crops are asparagus, bean,
practically devoid of hairs and spines. It is easily beet, broccoli, cabbage, cauliflower, celery, chickpea,
confused with other caterpillar pests. corn, cowpea, eggplant, lettuce, onion, pea, pepper,
Initially the larvae of beet armyworm are gre- potato, radish, spinach, sweet potato, tomato, and
garious, feeding as a group and skeletonizing plant turnip. Field crops damaged include alfalfa, corn,
foliage. As they mature they become solitary and cotton, peanut, safflower, sorghum, soybean,
quite mobile, often traveling from plant to plant. sugarbeet, and tobacco. Weeds also are suitable
Cannibalism may occur when larvae are at high for larval development, including such common
densities or feeding on food low in nitrogen. plants as lambs-quarters, Chenopodium album.;
Pupation occurs in the soil. The larva gener- mullein, Verbascum sp.; pigweed, Amaranthus
ally constructs a pupal chamber near the soil spp.; purslane, Portulaca spp.; Russian thistle,
surface, digging only about one cm beneath the S alsola kali; parthenium, Parthenium sp.; and
surface. The chamber is constructed from sand tidestromia, Tidestromia sp. Although the host
range is wide, there are significant differences
in suitability even among hosts considered to
be suitable.
Numerous natural enemies have adapted to
this pest. Among the most common parasitoids
are braconid wasps, and the tachinid Lespsia
archippivora (Riley) (Diptera: Tachinidae). Preda-
tors frequently attack the eggs and small larvae;
among the most important are minute pirate bugs,
Orius spp. (Hemiptera: Anthocoridae); bigeye
Beet Armyworm, Spodoptera exigua (Hbner) bugs, Geocoris spp. (Hemiptera: Lygaeidae); dam-
(Lepidoptera: Noctuidae), Figure 31 Mature larva sel bugs, Nabis spp. (Hemiptera: Nabidae); and a
of beet armyworm, Spodoptera exigua (Hbner). predatory shield bug, Podisus maculiventris (Say).
436
B Beet Armyworm, Spodoptera exigua ((Hbner)) (Lepidoptera: Noctuidae)

Pupae are subject to attack, especially by ants. the need for crop treatment with insecticides.
Fungal diseases, Erynia sp. and Nomurea rileyi, Regular monitoring of crops, probably about
and a nuclear polyhedrosis virus also inflict some twice per week, is recommended because adults
mortality. The important mortality factors vary frequently invade from surrounding crops or
among crops, and among geographic regions. weeds.
None except the nuclear polyhedrosis virus are The relatively high abundance of beet army-
highly specific to beet armyworm, which may worm has stimulated frequent application of
explain why they are not especially effective. Virus insecticides. Chemical insecticides and Bacillus
is considered to be the most important mortality thuringiensis are commonly applied to foliage to
factor in Mexico. protect against defoliation. Insecticide resistance
is a major problem in management of this insect,
possibly because it attacks crops such as flowers,
Damage cotton, and vegetables crops that are treated
frequently with insecticides. Beet armyworm
Larvae feed on both foliage and fruit. Young lar- abundance is favored by frequent insecticide use,
vae feed gregariously and skeletonize foliage. As and it is considered to be a secondary or induced
they mature, larvae become solitary and eat large pest in some crops. Also, intensive use of insecti-
irregular holes in foliage. They also burrow into cides for beet armyworm control in vegetables
the crown or center of the head on lettuce, or on such as celery has stimulated outbreaks of other
the buds of cole crops. As a leaf feeder, beet army- pests, principally American serpentine leafminer,
worm consumes much more cabbage tissue than Liriomyza trifolii (Burgess).
diamondback moth, Plutella xylostella (Lin- Host plant resistance in several crops has been
naeus), but is less damaging than cabbage looper, studied for its contribution to beet armyworm pest
Trichoplusia ni (Hbner). This insect is also management. In tomato, for example, resistance is
regarded as a serious pest of celery in California, correlated with total glycoalkaloid concentration
and damage is directly correlated with abundance in the fruit tissue. However, leaf tissue does not
of late instar larvae late in the season. However, have any effective antibiotic chemistry, so larvae
damage to foliage and petioles (stalks) during the are able to develop on plants even if they have
first half of the growing season is of little conse- unsuitable tomato fruit.
quence because these plant parts are removed at Several insect pathogens may prove to
harvest. Tomato fruit is most susceptible to injury, be useful for suppression of beet armyworm.
especially near fruit maturity, but beet armyworm A nuclear polyhedrosis virus isolated from beet
is not considered to be as threatening to tomato armyworm is fairly effective as a bioinsecticide
as is corn earworm, Helicoverpa zea (Boddie). under greenhouse conditions, where inactivation
Larvae not only damage tomato fruit, but may by ultraviolet light in sunlight is not a severe
appear as c ontaminants in processed tomato. problem. It is as effective as commonly used insec-
ticides, but presently is not commercially available.
Entomopathogenic nematodes (Rhabditida: Stein-
Management ernematidae and Heterorhabditidae) successfully
infect both larvae and adults of beet armyworm,
Pheromone traps can be used to detect the pres- and infected adults can fly short distances, helping
ence of adult beet armyworm. Visual sampling to spread the pathogens. Use of nematodes is simi-
for damage and larvae, combined with an action larly constrained by environmental conditions,
threshold of 0.3 larvae per plant, was used success- but these biological control agents are available
fully on cabbage in south Texas to determine commercially.
 Beetles (Coleoptera)
B 437

References Beetles are holometabolous insects which

have the front wings hardened and serving as
Ali A, Gaylor MJ (1992) Effects of temperature and larval diet protection for the hind wings which are used
on development of the beet armyworm (Lepidoptera: exclusively for flying. The front wings, or elytra, are
Noctuidae). Environ Entomol 21:780786
Brown ES, Dewhurst CF (1975) The genus Spodoptera
usually raised during flight; at rest, they meet in a
(Lepidoptera, Noctuidae) in Africa and the Near East. straight line along the back. When not in use, the
Bull Entomol Res 65:221262 hind wings are folded longitudinally and trans-
Capinera JL (2001) Handbook of vegetable pests. Academic versely and hidden under the elytra. Beetles also
Press, San Diego, CA, 729 pp
Wilson JW (1932) Notes on the biology of Laphygma exigua possess chewing mouthparts, usually 11-seg-
Huebner. Fla Entomologist 16:3339 mented antennae, and the abdominal sternites are
Wilson, JW 1933. The biology of parasites and predators of usually more heavily sclerotized than the tergites.
Laphygma exigua Huebner reared during the season of
1932. Fla Entomol 17:115

Anatomy

Beetles (Coleoptera) The body of an adult beetle is composed, like all

insects, of three regions: head, thorax, and abdomen.
michael c. thomas What is visible in dorsal view in beetles, though, is
Division of Plant Industry, Florida Department of the head, prothorax, and elytra (singular, elytron),
Agriculture and Consumer Services Gainesville, which cover the meso- and metathorax, and usually
FL, USA all of the abdomen.
The head bears the eyes, chewing mouthparts,
The present era could with some justification be and usually 11-segmented antennae. The size and
called the Age of the Beetles. Members of the order placement of the compound eyes varies widely
Coleoptera comprise the largest order of life. One within the order, and eyelessness is fairly frequent,
out of every five species of living things on Earth is especially in soil and litter inhabiting beetles, and
a beetle. No one knows precisely how many beetle those which dwell in caves. The presence of ocelli
species have been described, but estimates start at occurs in only a very few small groups. Mouthparts
250,000. Beetles live in almost every habitat where may be borne on the end of a rostrum (most notably
insects are found but do not come to the attention in weevils, Curculionidae). Beetles exhibit almost
of the layperson as often as members of some other endless modifications of the mouthparts, especially
orders which are more conspicuous by virtue of of the mandibles, which may be the most striking
their size or habits. The majority of beetles are capa- feature of the individual, as in Lucanidae and some
ble of flight and some fly quite well, but none has Cerambycidae. The antennae in beetles range from
adopted the truly aerial lifestyle of butterflies and simply threadlike (filiform) or beadlike (monili-
dragonflies. Most spend the greater part of their form), to gradually (clavate) or abruptly (capitate)
lives in cryptic habitats under bark and in dead clubbed, or saw-like (serrate), or with the club seg-
wood, in soil and leaf litter, in the water of ponds, ments asymmetrically developed and capable of
lakes, and streams. Although some beetles are opening and closing like a fan (lamellate), or elbowed
among the largest insects, most are quite small; like an ants antennae (geniculate), or feathery (pec-
indeed, some are among the smallest of insects. tinate or flabellate). Although most beetles have
Nevertheless, beetles are unrivaled in their 11-segmented antennae, reduction in the number of
diversity of form and color and in the nearly segments (to only one or two segments in extreme
endless ways they have found to live, feed, and examples) is common, while an increase in the num-
reproduce. ber of segments is quite uncommon.
438
B Beetles (Coleoptera)

The thorax is composed of three parts: the pro- riassic. They were preceded by a group of
T
thorax bears the forelegs; the mesothorax gives rise beetle-like insects called the Protocoleoptera
to the forewings, or elytra, and the middle legs; the that arose in the Lower Permian. By the Jurassic,
metathorax bears the hind wings and hindlegs. The many modern families had arisen, and most of
legs are 5-segmented, composed of (from closest to the rest appeared during the Cretaceous, coinci-
the body) the coxa, trochanter, femur, tibia, and tar- dent with the rise of the flowering plants. Inter-
sus. The tarsus is composed primitively of five tar- estingly, many of the Cenozoic amber fossils can
someres, but this is often reduced and the tarsal be attributed to modern genera.
formula (the number of tarsomeres on the front,
middle, and hind legs) is important in beetle identi-
fication. The elytra generally completely cover the Classification
dorsal part of the metathoraz and abdomen, but are
secondarily short in many groups (Staphylinidae, Beetles were recognized as a distinct group of
Silphidae, Cerambycidae, etc.). They almost always insects as far back as the ancient Greeks, but the
meet in a straight line, one of the very few excep- classification within the group has been in a state
tions being the genus Meloe in the Meloidae. of flux up to the present day. The limits of the order
The dorsal part of the abdomen is usually soft, are well understood, with the only issue being
except in those groups with abbreviated elytra; the whether to include or exclude the twisted-wing
ventral surface of the abdomen is almost always parasites (Strepsiptera). Most now treat them as a
heavily sclerotized. separate order near Coleoptera, but some have
argued that their true affinities lie with the Diptera.
Within the Coleoptera, the general classification is
Life Cycle fairly well accepted but disagreement persists on
the ranking or placement of some family-level
Beetles undergo complete metamorphosis. The life groups. The classification presented here is that
cycle of the typical beetle includes egg, three to five used in the two-volume American Beetles (Arnett
larval instars, pupa, and adult. A few beetle families and Thomas 2000, Arnett et al. 2002), the most
have more complicated life histories: Micromalthi- recently published, major general work on beetles.
dae have multiple larval forms and paedogenesis There are 166 families of beetles in the world;
(reproduction by larvae); several families, e.g., Mel- 131 of those occur in America north of Mexico.
oidae, Ripiphoridae, Passandridae, undergo hyper- The order is divided very unequally into four
metamorphosis, with the first instar larva being suborders: Archostemata, Myxophaga, Adephaga,
considerably different from succeeding instars. The and Polyphaga.
length of the life cycle v aries widely within the
order, but generation length of most beetles falls
within a few weeks to 1 or 2 years. A few beetles, Archostemata
notably some Cerambycidae, under extraordinary
conditions can spend decades as larvae. Only four families comprise this primitive subor-
der. Beetles very similar to present-day Cupedidae
are known from the Lower Triassic. Two families,
Evolution Cupedidae and Micromalthidae, are known from
the Nearctic. Most are found in decaying wood.
It is generally agreed the beetles are most closely The sole member of Micromalthidae, Micromalthus
related to the neuropteroid orders. The first debilis LeConte, has an unusual and complex life
fossils of true Coleoptera date back to the history, including paedogenesis.
 Beetles (Coleoptera)
B 439

Myxophaga predominantly predacious and aquatic. The Histeri-

dae and Sphaeritidae are terrestrial and predacious.
Another four families have been assigned to this, Superfamily: StaphylinoideaThis family contains
the most recently recognized suborder. Two fami- six small or moderate-sized families and one huge
lies, Microsporidae and Hydroscaphidae, occur in one, the Staphylinidae, which has more than 4,100
the Nearctic. The few minute species are associ- species in the Nearctic and more than 46,000
ated with algae. worldwide. All the families occur in the Nearctic.
Staphylinids, or rove beetles, often are found
around decaying vegetable material and dead
Adephaga animals, where they feed on fly larvae and other
insects. Many staphylinids live in the nests of social
Nine families comprise this suborder, the only one insects, ants and termites primarily, and show
that is composed exclusively (except for one small many physical and behavioral adaptations to that
family of wood-inhabiting beetles, the Rhysodidae) way of life. Most staphylinids have very short elytra
of predacious beetles. Eight families occur in the and flexible abdomens.
Nearctic, the Carabidae or ground beetles, being
by far the largest family in the suborder, with 2,635
species and subspecies being recorded from the Series: Scarabaeiformia
Nearctic and about 40,000 for the world. Carabids
often are found on the ground under stones or This series contains only the single superfamily
logs, or in leaf litter, but many, especially in the
tropics, are arboreal. They are usually small to Superfamily: Scarabaeoidea
moderate in size. Most are darkly colored, but This superfamily contains 11 small or moderate-
many exhibit brilliant metallic colors. Most ground sized families and one very large one, the Scarabaei-
beetles are predacious, feeding on soft-bodied dae. There are more than 27,800 species of scarab
insects, but some are specialized predators of snails beetles in the world; about 1,700 occur in the Nearc-
and millipeds. A few are seed feeders. Beetles in tic. This superfamily includes the relatively small
most of the other families spend most of their lives but well-known Lucanidae (stag beetles) and Pas-
in fresh water. salidae (bess beetles). The Scarabaeidae include
some of the largest known beetles, such as the mem-
bers of the genera Dynastes and Megasoma in the
Polyphaga New World, and Goliathus in tropical Africa. Males
of many scarabs bear spectacular horns on the head
All the rest of the beetle families are assigned to and/or pronotum with which they battle each other
this suborder. It has been subdivided into several for females. Scarab beetles have extremely diverse
series and numerous superfamilies. feeding habits. Many feed on dung of mammals,
some being extremely specific on the kind of dung
they will accept. Dung beetles provision burrows
Series: Staphyliniformia with dung for their larvae, some rolling balls of
dung away for burying and sculpting the dung ball
This series is composed of two superfamilies. into special shapes. Some even tend the dung to
prevent the growth of mold on it. Many others feed
Superfamily: Hydrophiloidea in soil, humus, and decaying wood. Some, like the
Three families, two moderately sized and one small, Japanese beetle Popilia japonica Newman, feed on
comprise this superfamily. The Hydrophilidae are living plants and are economic pests of extreme
440
B Beetles (Coleoptera)

importance. Many others are found in nests of Superfamily: Elateroidea

social insects, primarily ants and termites. Fifteen rather diverse families comprise this
superfamily, all but three of which are found in
the Nearctic. The largest family is the Elateridae,
Series: Elateriformia or click beetles. There are about 10,000 species
of click beetles in the world, with 965 recorded
This series contains five mostly small superfamilies. from the Nearctic. Click beetles (and a few of
the other families) bear a click mechanism on
Superfamily: Scirtoidea the pro- and mesosternum that allows them to
Four families, three of which are found in the fling themselves into the air with some force
Nearctic, comprise this superfamily. Two families, if they are placed on their backs. Members of
Eucinetidae and Clambidae, contain small to one mostly tropical group of click beetles are
minute beetles that are found in leaf litter and luminescent. Other large or widely distributed
apparently feed on fungus. Scirtidae are aquatic as families include the Lampyridae, Lycidae, Can-
larvae and adults generally are found in wet tharidae, and Eucnemidae.
habitats.

Superfamily: Dascilloidea
Series: Bostrichiformia
Only two small families, Dascillidae and Rhipic-
eridae (Figs. 32 and 33) comprise this superfam-
The series includes two small superfamilies, plus
ily. Larvae of Rhipiceridae are hypermetamorphic
the Jacobsoniidae, which have not been placed in
and parasitic on immature annual cicadas
a superfamily.
(Heteroptera).

Superfamily: Buprestoidea Superfamily: Derodontoidea

Two families, Schizopodidae and Buprestidae, Only the Derodontidae are included in this super-
are included in this superfamily. The Schizopodi- family. They are found on slime molds.
dae are a small family, confined to the western
Nearctic. The Buprestidae are one of the larger Superfamily: Bostrichoidea
families of Coleoptera, with 788 species and sub- Four families are included here, Nosodendridae,
species recorded from the Nearctic and more Dermestidae, Bostrichidae, and Anobiidae. The
than 14,000 in the world. These often brilliantly last three including many economically impor-
colored beetles are mostly wood borers as larvae, tant pests of animal products such as wool, leather,
although some are leaf miners. A few are of eco- feathers, and silk (Dermestidae) and stored prod-
nomic importance. ucts and wood or wood products (Bostrichidae
and Anobiidae).
Superfamily: Byrrhoidea
There are 12 mainly small families assigned here;
most of the species are aquatic or subaquatic. All
but one of the families are found in the Nearctic. Series: Cucujiformia
The water penny beetles, Psephenidae, with their
remarkably flattened larvae, are found on rocks This huge series contains the rest of the Coleoptera,
in streams. arranged in six superfamilies.
 Beetles (Coleoptera)
B 441

Beetles (Coleoptera), Figure 32 Some representative beetles: top left, drugstore beetle, Stegobium
paniceum (Anobiidae); top right, lesser grain borer, Rhyzopertha dominica (Bostrichidae); second row
left, cowpea weevil, Callosobruchus maculatus (Bruchidae); second row right, Buprestis lineatus (Bupres-
tidae); third row left, Pasimachus sublaevis (Carabidae); third row right, banded hickory borer, Knulli-
ana cincta (Cerambycidae); bottom left, Trirhabda bacharidis (Chrysomelidae); bottom right, Cicindela
punctulata (Carabidae) (photos by Lyle Buss).
442
B Beetles (Coleoptera)

Beetles (Coleoptera), Figure 33 Some additional representative beetles: top left, Neorthopleura thoracica
(Cleridae); top right, Mexican bean beetle, Epilachna varivestis (Coccinellidae); second row left, eyed click
beetle, Alaus oculatus (Elateridae); second row right, maize weevil, Sitophilus zeamais (Curculionidae);
third row left, striped blister beetle, Epicauta vittata (Meloidae); third row right, a firefly, Photinus tanytox-
us (Lampyridae); bottom left, a rove beetle, Platydracus fossator (Staphylinidae); bottom right, Hercules
beetle, Dynastes titus (Scarabaeidae) (Dynastes and Epilachna by Jim Castner; other photos by Lyle Buss).
 Beetles (Coleoptera)
B 443

Superfamily: Lymexyloidea plants, although some attack living trees. Many

This superfamily contains only the ship-timber are of economic importance. Some very large
beetles, Lymexylidae, a small group of soft-bodied, forms occur in the tropics and are among the
wood-boring beetles. largest beetles. The leaf beetles, Chrysomeli-
dae, include about 35,000 species worldwide
Superfamily: Cleroidea and about 1,720 in the Nearctic. Chrysomelids
Three moderate-sized families of predominantly differ from cerambycids in usually being
predacious beetles comprise this superfamily. smaller, less elongate, and with shorter anten-
nae. Often they are brightly colored. Leaf bee-
Superfamily: Cucujoidea tles are associated predominantly with living
This is a large superfamily composed of 31 mostly plants, feeding on the foliage and roots. Many
small to moderate-sized families, ten of which do are economically important pests of agricul-
not occur in the Nearctic. Members of most of turally important crops. The seed beetles,
the families are associated with fungus, but some Bruchidae, often are combined with the leaf
are predominantly predacious, such as the largest beetles. Several are important pests of stored
and best-known family, Coccinellidae, and a few legume seeds.
(Bothrideridae and Passandridae) even contain
species which have parasitic larvae.
Superfamily: Curculionoidea
Superfamily: Tenebrionoidea The largest family of living organisms is included
among the eight families in this superfamily. The
This is the second largest superfamily with weevils, Curculionidae, contain more than 60,000
30 families, six of which do not occur in the species worldwide and about 2,400 in the Nearc-
Nearctic. Most of the families are small to moder- tic. As presently defined, the Curculionidae are
ate in size, but the Tenebrionidae are one of the restr-icted to curculionoids with geniculate
largest families of Coleoptera, with about 19,000 antennae. They are almost entirely herbivorous,
species worldwide and about 1,100 in the Nearc- attacking all parts of all kinds of plants. Many of
tic. Although the Tenebrionidae are found in all the worst agricultural pests are weevils. The Bren-
kinds of habitats, the family is especially well rep- tidae, or primitive weevils, are mostly tropical but
resented in deserts. They are usually sombre in one oak pest occurs in the eastern Nearctic. The
coloration, hence their common name of darkling Anthribidae, or fungus weevils, are associated
beetles, and often are found on the ground under with fungi of various kinds.
rocks and logs. Classification of the Order Coleoptera Lin-
naeus 1758.

Superfamily: Chrysomeloidea Suborder: ARCHOSTEMATA Kolbe 1908

Cupedidae Laporte 1836, The reticulated
The superfamily contains five families, two of
beetles
which are very large. The longhorn beetles,
Ommatidae Sharp and Muir 1912
C erambycidae, contains more than 20,000 spe-
cies worldwide and more than 900 in the Crowsonellidae Iablokoff-Khnzorian 1983
Nearctic. They are generally elongate, hand- Micromalthidae Barber 1913, The telephone-
some beetles with long to very long antennae. pole beetles
Most are associated with dead or dying woody Suborder: MYXOPHAGA Crowson 1955
444
B Beetles (Coleoptera)

Lepiceridae Hinton 1936 Staphylinidae Latreille 1802, The rove

Microsporidae Crotch 1873, The minute bog beetles
beetles Series: SCARABAEIFORMIA Crowson 1960
Hydroscaphidae LeConte 1874, The skiff Superfamily: SCARABAEOIDEA Latreille 1802
beetles Lucanidae Latreille 1804, The stag beetles
Torridincolidae Steffan 1964 Diphyllostomatidae Holloway 1972, The
Suborder: ADEPHAGA Schellenberg 1806 diphyllostomatid beetles
Rhysodidae Laporte 1840, The wrinkled bark Passalidae Leach 1815, The bess beetles
beetles Glaresidae Semenovrlan-Shanskii and Med-
Carabidae Latreille 1802, The ground beetles vedev 1932, The glaresid beetles
Gyrinidae Latreille 1810, The whirligig beetles Trogidae MacLeay 1819, The skin beetles
Haliplidae Aub 1836, The crawling water beetles Pleocomidae LeConte 1861, The rain beetles
Trachypachidae C. G. Thomson 1857, The false Geotrupidae Latreille 1802, The earth-boring
ground beetles dung beetles
Noteridae C. G. Thomson 1860, The burrowing Belohinidae Paulian 1959
water beetles Ochodaeidae Mulsant and Rey 1871, The
Amphizoidae LeConte 1853, The trout-stream ochodaeid scarab beetles
beetles Hybosoridae Erichson 1847, The hybosorid
Hygrobiidae Rgimbart 1878 scarab beetles
Dytiscidae Leach 1815, The predacious diving Ceratocanthidae Cartwright and Gordon
beetles 1971, The ceratocanthid scarab beetles
Suborder: POLYPHAGA Emery 1886 Glaphyridae MacLeay 1819, The glaphyrid
Series: STAPHYLINIFORMIA Lameere 1900 scarab beetles
Superfamily: HYDROPHILOIDEA Latreille 1802 Scarabaeidae Latreille 1802, The scarab
beetles
Hydrophilidae Latreille 1802, The water
scavenger beetles Series: ELATERIFORMIA Crowson 1960
Sphaeritidae Shuckard 1839, The false clown Podabrocephalidae Pic 1930
beetles Rhinorhipidae Lawrence 1988
Synteliidae Lewis 1882 Superfamily: SCIRTOIDEA Fleming 1821
Histeridae Gyllenhal, The clown beetles Decliniidae Nikitsky et al. 1994
Superfamily STAPHYLINOIDEA Latreille 1802 Eucinetidae Lacordaire 1857, The plate-thigh
Hydraenidae Mulsant 1844, The minute beetles
moss beetles Clambidae Fischer 1821, The minute beetles
Ptiliidae Erichson 1845, The feather-winged Scirtidae Fleming 1821, The marsh beetles
beetles Superfamily: DASCILLOIDEA Gurin-Mneville
Agyrtidae C. G. Thomson 1859, The primitive 1843
carrion beetles Dascillidae Gurin-Mneville 1843
Leiodidae Fleming 1821, The round fungus Rhipiceridae Latreille 1834, The cicada para-
beetles site beetles
Scydmaenidae Leach 1815, The antlike stone Superfamily: BUPRESTOIDEA Leach 1815
beetles
Schizopodidae LeConte 1861, The schizopo-
Silphidae Latreille 1807, The carrion beetles did beetles
 Beetles (Coleoptera)
B 445

Buprestidae Leach 1815, The metallic wood- Lampyridae Latreille 1817, The firefly beetles
boring beetles Omethidae LeConte 1861, The false firefly
Superfamily: BYRRHOIDEA Latreille 1804 beetles
Byrrhidae Latreille 1804, The pill beetles Cantharidae Imhoff 1856, The soldier beetles
Elmidae Curtis 1830, The riffle beetles Series: BOSTRICHIFORMIA Forbes 1926
Dryopidae Billberg 1820, The long-toes Jacobsoniidae Heller 1926, The Jacobsons
beetles beetles
Lutrochidae Kasap and Crowson 1975, The Superfamily: DERODONTOIDEA LeConte 1861
robust marsh-loving beetles Derodontidae LeConte 1861, The
Limnichidae Erichson 1846, The minute tooth-necked fungus beetles
marsh-loving beetles Superfamily BOSTRICHOIDEA Latreille 1802
Heteroceridae MacLeay 1825, The varie- Nosodendridae Erichson 1846, The
gated mod-loving beetles wounded-tree beetles
Psephenidae Lacordaire 1854, The water Dermestidae Latreille 1804, The skin and
penny beetles larder beetles
Cneoglossidae Champion 1897 Bostrichidae Latreille 1802, The horned
Ptilodactylidae Laporte 1836, The powder-post beetles
toe-winged beetles Anobiidae Fleming 1821, The death-watch
Chelonariidae Blanchard 1845, The turtle beetles
beetles Series: CUCUJIFORMIA Lameere 1938
Eulichadidae Crowson 1973, The eulichadid Superfamily: LYMEXYLOIDEA Fleming 1821
beetles
Lymexylidae Fleming 1821, The ship-timber
Callirhipidae Emden 1924, The cedar beetles beetles
Superfamily: ELATEROIDEA Leach 1815 Superfamily: CLEROIDEA Latreille 1802
Artematopodidae Lacordaire 1857, The Phloiophilidae Kiesenwetter 1863
soft-bodied plant beetles
Trogossitidae Latreille 1802, The
Brachypsectridae Leconte and Horn 1883, bark-gnawing beetles
The Texas beetles
Chaetosomatidae Crowson 1952
Cerophytidae Latreille 1834, The rare click
Cleridae Latreille 1802, The checkered
beetles
beetles
Eucnemidae Eschscholtz 1829, The false
Acanthocnemidae Crowson 1964
click beetles
Phycosecidae Crowson 1952
Throscidae Laporte 1840, The false metallic
wood-boring beetles Prionoceridae Lacordaire 1857
Elateridae Leach 1815, The click beetles Melyridae Leach 1815, The soft-winged
flower beetles
Plastoceridae Crowson 1972
Superfamily: CUCUJOIDEA Latreille 1802
Drilidae Blanchard 1845
Protocucujidae Crowson 1954
Omalisidae Lacordaire 1857
Sphindidae Jacquelin du Val 1860, The
Lycidae Laporte 1836, The net-winged
dry-fungus beetles
beetles
Brachypteridae Erichson 1845, The
Telegeusidae Leng 1920, The long-lipped
short-winged flower beetles
beetles
Nitidulidae Latreille 1802, The sap-feeding
Phengodidae LeConte 1861, The glowworm
beetles
beetles
446
B Beetles (Coleoptera)

Smicripidae Horn 1879, The palmetto Latridiidae Erichson 1842, The minute brown
beetles scavenger beetles
Monotomidae Laporte 1840, The root-eating Superfamily: TENEBRIONOIDEA Latreille 1802
beetles Mycetophagidae Leach 1815, The hairy
Boganiidae Sen Gupta and Crowson 1966 fungus beetles
Helotidae Reitter 1876 Archeocrypticidae Kaszab 1964, The
Phloeostichidae Reitter 1911 archeocryptic beetles
Silvanidae Kirby 1837, The silvanid flat bark Pterogeniidae Crowson 1953
beetles Ciidae Leach 1819, The minute tree-fungus
Passandridae Erichson 1845, The parasitic beetles
flat bark beetles Tetratomidae Billberg 1820, The polypore
Cucujidae Latreille 1802, The flat bark fungus beetles
beetles Melandryidae Leach 1815, The false darkling
Laemophloeidae Ganglbauer 1899, The beetles
lined flat bark beetles Mordellidae Latreille 1802, The tumbling
Propalticidae Crowson 1952 flower beetles
Phalacridae Leach 1815, The shining flower Rhipiphoridae Gemminger and Harold 1870,
beetles The wedge-shaped beetles
Hobartiidae Sen Gupta and Crowson 1966 Colydiidae Erichson 1842, The cylindrical
bark beetles
Cavognathidae Sen Gupta and Crowson 1966
Monommatidae Blanchard 1845, The
Cryptophagidae Kirby 1837, The silken opossum beetles
fungus beetles
Zopheridae Solier 1834, The ironclad beetles
Lamingtoniidae Sen Gupta and Crowson
1969 Ulodidae Pascoe 1869
Languriidae Crotch 1873, The lizard Perimylopidae St. George 1939
beetles Chalcodryidae Watt 1974
Erotylidae Latreille 1802, The pleasing Trachelostenidae Lacordaire 1859
fungus beetles Tenebrionidae Latreille 1802, The darkling
Byturidae Jacquelin du Val 1858, The beetles
fruitworm beetles Prostomidae C. G. Thomson 1859, The
Biphyllidae LeConte 1861, The false skin jugular-horned beetles
beetles Synchroidae Lacordaire 1859, The synchroa
Bothrideridae Erichson 1845, The dry bark beetles
beetles Oedemeridae Latreille 1810, The
Cerylonidae Billberg 1820, The minute bark pollen-feeding beetles
beetles Stenotrachelidae C. G. Thomson 1859, The
Alexiidae Imhoff 1856 false long-horned beetles
Discolomatidae Horn 1878 Meloidae Gyllenhal 1810, The blister beetles
Endomychidae Leach 1815, The handsome Mycteridae Blanchard 1845, The palm and
fungus beetles flower beetles
Coccinellidae Latreille 1807, The ladybird Boridae C. G. Thomson 1859, The conifer
beetles bark beetles
Corylophidae LeConte 1852, The minute Trictenotomidae Blanchard 1845
fungus beetles
 Behavior of Insects: Genetic Analysis by Crossing and Selection
B 447

Pythidae Solier 1834, The dead log bark Leaf Beetles

beetles Longicorn Beetles
Pyrochroidae Latreille 1807, The fire-colored Powderpost Beetles
beetles Riffle Beetles
Salpingidae Leach 1815, The narrow-waisted Rove Beetles
bark beetles Sap Beetles
Anthicidae Latreille 1819, The antlike flower Water Penny Beetles
beetles
Aderidae Winkler 1927, The antlike leaf
beetles References
Scraptiidae Mulsant 1856, The false flower
beetles Arnett RH Jr, Thomas MC (eds) (2000)American bee-
tles, vol 1: Archostemata, Myxophaga, Adephaga,
Superfamily: CHRYOMELOIDEA Latreille 1802 Polyphaga: Staphyliniformia. CRC Press, Boca Raton,
Cerambycidae Latreille 1802, The FL, 443 pp
long-horned beetles Arnett RH Jr, Thomas MC, Skelley PE, Frank JH (eds) (2002)
American beetles, vol 2: Polyphaga: Scarabaeoidea through
Bruchidae Latreille 1802, the pea and bean Curculionoidea. CRC Press Boca Raton, FL, 861 pp
weevils Crowson RA (1981) The biology of the Coleoptera. Academic
Megalopodidae Latreille 1802, The Press, New York, NY, 802 pp
megalopodid leaf beetles Lawrence JF (1982) Coleoptera. In: Parker SB (ed) Synopsis
and classification of living organisms, vol 2. McGraw-
Orsodacnidae C. G. Thomson 1859, The Hill Publishers, New York, NY, pp 482553
orsodacnid leaf beetles Lawrence JF (Co-ordinator). Chapter 34. Coleoptera. In: Stehr F
Chrysomelidae Latreille 1802, The leaf beetles (ed) Immature insects, vol 2. Kendall/Hunt Publishing,
Dubuque, IA, pp 144658
Superfamily: CURCULIONOIDEA Latreille 1802
Lawrence JF, Britton EB (1994) Australian beetles. Melbourne
Nemonychidae Bedel 1882, The pine-flower University Press, Carlton, Victoria, Australia, 192 pp
snout beetles Lawrence JF, Hastings AM, Dallwitz M, Paine TA, Zurcher EJ
Anthribidae Billberg 1820, The fungus (1999) Beetle larvae of the world: descriptions, illustrations,
and information retrieval for families and subfamilies.
weevils
CD-ROM, Version 1.1 for MS-Windows. CSIRO Pub-
Belidae Schnherr 1826, The primitive lishing, Melbourne, Australia
weevils Lawrence JF, Newton AF Jr (1995) Families and subfamilies
Attelabidae Billberg 1820, The tooth-nosed of Coleoptera (with selected genera, notes, references
and data on family-group names). In: Pakaluk J, Slip-
snout beetles
inski SA (eds) Biology, phylogeny, and classification of
Brentidae Billberg 1820, The straight- Coleoptera: papers celebrating the 80th birthday of
snouted weevils Roy A. Crowson. Muzeum i Institut Zoologii, Polska
Caridae Thompson 1992 Academia Nauk, Warsaw, Poland, pp 7791006

Ithyceridae Schnherr 1823, The New York

weevils
Curculionidae Latreille 1802, The snout Behavior of Insects: Genetic
beetles and true weevils Analysis by Crossing and
Bark Beetles Selection
Bess Beetles
Blister Beetles marjorie a. hoy
Darkling Beetles University of Florida, Gainesville, FL, USA
Fireflies
Ground Beetles Sometimes, as will be demonstrated in examples
June Beetles below, mutations in a single gene or a few major
448
B Behavior of Insects: Genetic Analysis by Crossing and Selection

genes will alter the behavior of insects. The genetic behavior. The behavior of their progeny (the F1
basis of this behavior can be assessed by tradi- generation) and the progeny produced by crosses
tional techniques. Traditional behavior-genetic between the F1 progeny and one of the original
analysis primarily employs one of two experimen- parental types (backcross progeny) is also evaluated.
tal appro-aches: crossing and selection. A third Ideally, the environment experienced by the paren-
traditional approach, which is limited to D. mela- tal, F1 and backcross generations is controlled so
nogaster, involves analysis of fate maps in genetic that all individuals experience the same conditions.
mosaics. This method allows the researcher to It is easiest to interpret the results of crossing
locate the anatomical site of abnormalities that experiments if the individual insects that are
affect behavior in D. melanogaster. In addition, crossed differ only with regard to a single behav-
molecular genetic methods are becoming impor- ioral attribute.
tant in the analysis of insect behavior, but are dis-
cussed in a separate entry.
Although a specific behavior sometimes can Selection Experiments
be altered by the mutation of a single gene in a
pathway leading to the behavior, an insects behav- Selection experiments provide a second tradi-
ior often is influenced by many genes. In such tional method to determine the degree to which a
situations, analyses of behavior have traditionally given behavior is determined genetically. Selec-
required the use of a statistically based approach tion experiments do not usually allow the
called quantitative genetics. researcher to resolve the mode of inheritance. In a
selection experiment, individuals with a specific
behavioral attribute are allowed to reproduce and
Crossing Experiments this process is repeated over succeeding genera-
tions until a plateau in the selection response is
Crossing experiments are used to assess the mode obtained. The behavior of the selected population
of inheritance of a particular behavior. The behavior is altered if genetic variation for the attribute is
(phenotype) of the F1 and backcross progeny present in the initial colony and the selection pro-
indicates whether the behavior under study is cedures have been appropriate. The response of
determined by a single gene or more than one the population to selection can be analyzed to
gene. The phenotype indicates whether there is estimate whether the trait is heritable. An example
dominance (a single copy of the gene is sufficient of a selection experiment is provided by the anal-
to determine the behavior under study), sex link- ysis of migratory behavior in the milkweed bug
age (the gene is located on a sex-determining Oncopeltus fasciatus.
chromosome) or maternal influences (the behav- Migratory and nonmigratory behaviors of
ior is determined by the behavior of the mother, Oncopeltus fasciatus were shown to be under
which suggests that the trait may be determined genetic control. Strains of O. fasciatus were selected
by factors in the cytoplasm rather than in the for two attributes: wing length and propensity to
chromosomes located in the nucleus). If the trait is fly. Bidirectional selection (selection for increased
determined by many genes, it is difficult to deter- or decreased wing length) on wing length was
mine the number of genes, their relationship to performed for 13 generations and the flight behav-
each other, or their location on specific chromo- ior of the selected individuals was monitored.
somes because most insect species lack sufficient Individuals also were selected for flight duration;
genetic markers. those whose flight times totaled 30 min were
A crossing experiment involves mating considered fliers, while those with the shortest
individual insects that differ in a particular kind of flight times were labeled nonfliers.
 Behavior of Insects: Genetic Analysis by Crossing and Selection
B 449

Response to selection on wing length was nonhygienic, indicating that the gene, or genes,
rapid, and flight tests of the long- and short- conferring the hygienic behavior are recessive.
winged insects indicated there was a positive Progeny produced by backcrosses to the
correlation between wing length and flight dura- pure hygienic strain yielded approximately 25%
tion. Selection after two generations for flight or hygienic worker progeny, which is consistent with
noflight likewise resulted in divergent responses, the hypothesis that hygienic behavior is determined
indicating a large genetic component to flight by two recessive genes. Under this two-gene model,
behavior. hygienic worker bees have two copies of each of
two genes, called u and r. Hygienic bees (uurr)
both uncap the cells (uu) containing dead brood
and remove them (rr).
Behavior Determined by One or a
As expected, worker bees that contain two
Few Genes
copies of u but only one copy of the gene for
removal (r) will uncap the cells, but not remove
How often are insect behaviors determined by one
dead brood. The workers that contain only one
or a few genes? How often are behaviors determined
copy of the uncapping gene (u) but two copies of
by many genes? The following examples provide
the removal gene (rr) do not uncap brood, but
some examples of behaviors determined by one or
will remove them if the cells are uncapped for
a very few genes.
them. Workers that contain only one copy each
of u and r (u+u, r+r) are unhygienic, and will nei-
ther uncap nor remove brood. Rothenbuhler s
Susceptibility to American Foulbrood in research on hygienic behavior became a classic
the Honeybee in textbooks of behavior genetics because it was
one of the first examples to demonstrate that
The genetic basis of susceptibility to foulbrood behavior was inherited. The model has been con-
disease caused by the bacterium Bacillus larvae in firmed, although one analysis of the data suggest
honeybees (Apis mellifera) originally was analyzed that three genes might be involved in this
by Walter Rothenbuhler. Differences in resistance behavior.
in different bee strains were attributed to differ- Research on hygienic behavior indicates it
ences in hygienic behavior in worker (sterile may be a general response to remove pathogens
female) bees. To understand the genetic basis of and parasites from the nest. It is clear that the
the hygienic behavior, two inbred honeybee strains expression of hygienic behavior also depends on
with differing levels of resistance were crossed and colony strength and composition of worker types
the behavior of the F1 and backcross progeny was within the colony. Analyses of the olfactory
characterized. This research was one of the first to responses of hygienic and non-hygienic bees to
show that a specific behavior was determined by a diseased brood indicates that hygienic bees have a
few genes. higher sensitivity to low concentrations of the
Hygienic workers consistently remove dead odor of diseased bee pupae. Such differences are
larvae and pupae from the brood nest at a high due to a lower stimulus threshold and not a direct
rate, thus slowing the spread of the bacteria result of age or experience of the bee, suggesting
through the colony by reducing contamination. that non-hygienic bees may be unable to detect
The hygienic behavior has two components: (i) the diseased brood readily.
uncapping of infected cells, and (ii) removal of the Understanding hygienic behavior in A. mel-
dead bee larvae. Crosses between hygienic and lifera has great practical importance in maintain-
nonhygienic bees yield F1 worker bees that are ing effective colonies of pollinators and honey
450
B Behavior of Insects: Genetic Analysis by Crossing and Selection

producers. Studies on hygienic behavior has Domesticity in A. aegypti is a complex phe-

resulted in practical recommendations to bee nomenon that includes a variety of behaviors,
keepers for selecting colonies resistant to chalk including a preference for ovipositing in man-
brood (a fungal disease) and the pest bee mite made containers, ability of larvae to develop in
Varroa. So far, no negative effects have been asso- drinking water stored in clay pots with a low nutri-
ciated with hygienic behavior and such colonies tional content, and preferences for feeding on man
produce as much honey as nonhygienic ones. (rather than birds) inside houses, as well as resting
and mating indoors. No doubt A. aegypti speciated
long before man began to build houses, but A.
House-Entering Behavior in Aedes aegypti has adapted rapidly to human habitats, and
aegypti the domestic form of A. aegypti is the only one
known that is entirely dependent on man.
The mosquito Aedes aegypti is an important
vector of human disease and understanding its
behavior could result in better management of Foraging in Drosophila
this pest. House-entering behavior by A. aegypti
from East Africa has been analyzed by crossing Drosophila melanogaster larvae feed on yeast grow-
different populations that exhibited different ing on fruit. Naturally occurring populations con-
behaviors, which were controlled by genes with tain individuals that vary in the distance the larvae
additive effects. One population of A. aegypti travel while foraging for food, a difference attrib-
commonly enters houses (domesticated or D), uted to a single gene called foraging. Natural popu-
while others rarely do so (one is called perido- lations comprise approximately 70% rovers (who
mestic [P]; and the other is a wild or feral [F]; forage long distances) and 30% sitters (short dis-
population). tance foragers). The rover behavior is dominant to
Three populations of A. aegypti were collected sitter, indicating a single-gene mode of inheritance.
either inside houses (D), near a village (P), or from Sitter larvae grow at a normal rate and are of nor-
tree holes in a forest (F). The populations then mal size. Both sitters and rovers are maintained in
were bred in insectaries and crossed to produce the field by natural selection. It appears that density-
hybrid (DP, PD, DF, FD, PF, FP) populations. The dependent selection can shift gene frequencies so
original and hybrid populations were then marked that rovers are selected for in crowded larval envi-
with different colored fluorescent powders and ronments and sitters in less crowded ones.
released near houses. Marked mosquitoes were The foraging gene codes for a cyclic guanos-
captured inside houses and in the village area. Of ine monophosphate (cGMP)-dependent protein
the mosquitoes entering houses, 45% were from kinase, and rovers have higher kinase activity than
the domestic (D) population, 14% from hybrids sitters. Thus, subtle differences in this kinase can
between the domestic and peridomestic popula- lead to naturally occurring variation in behavior.
tion (DP and PD), 10% from the peridomestic Another gene, Chaser, also may affect larval
population (P), and 6% were hybrids between the foraging by increasing foraging path length.
domestic and feral populations (DF and FD). Only
1.5 and 0.6% of the PF and FP hybrids were
collected in the house, and the feral population (F) Other Behaviors Influenced by One or a
entered the house with a frequency of only 0.6%. Few Genes
The recapture rates in the village area were in the
reverse order. These results clearly indicate that Crossing experiments have shown that a specific
the behavior is genetically determined. behavior is influenced by one or a few genes in the
 Behavior of Insects: Genetic Analysis by Crossing and Selection
B 451

flour moth Ephestia kuhniella (silk mat spinning Alterations in the brain affect behavior and
by larvae prior to pupation), the mosquito Aedes genes involved in the behavior can be analyzed by
atropalpus (egg maturation without an exogenous mutagenesis and mosaic analysis. For example,
source of protein such as blood), and the parasi- eight different genes affecting walking behavior in
toid wasp Habrobracon juglandis (flightlessness). Drosophila melanogaster strains were analyzed by
In the silkworm Bombyx mori, females with the chemical mutagenesis, histological analysis, and
piled egg gene deposit eggs in a peculiar manner. analysis of genetically mosaic flies. These eight
B. mori larvae with the Non-preference gene are genes caused structural defects in the central com-
unable to discriminate mulberry leaves from others. plex of the brain and affected walking motivation,
When two tephritid fly species (Procecidochares) fast response to light, and response to gravity.
were crossed that differ in their host preference Because the aberrant behaviors were associated
(each having only one host plant), the behavior of with changes in a portion of the insect brain called
their progeny segregated in a manner consistent the central complex, the mutant flies confirmed
with hypothesis that the control of host preference that the central complex controls behavior. The
is determined by a single gene. central complex also regulates other behaviors
A variety of mutants determined by major (flight, singing, preening, escape).
genes have been identified in D. melanogaster that Pheromone communication in the European
affect behavior, including Shaker, Hyperkinetic corn borer Ostrinia nubilalis is genetically determined.
and eag, which are expressed when the flies are Females of the E- and Z-strains of O. nubilalis pro-
anesthetized with ether. Hyperkinetic (Hk) causes duce different ratios of enantiomeric (molecules
a vigorous steady leg shaking, and mutations of that are chemically the same but mirror images of
Shaker cause vigorous and erratic shaking and a each other) molecules of their sex pheromone
strong scissoring of wings and twitching of the (a substance released by an organism that causes a
abdomen. The eag mutant flies (ether a-go-go) reaction by another individual of the same species,
are less vigorous in their shaking. The easily in this case it serves as a sexual attractant). Hybrids
shocked gene of D. melanogaster is one of the between these two strains produce an intermedi-
class of bang-sensitive paralytic genes. Flies ate pheromone blend. Analysis of the F2 and back-
with this mutated gene exhibit a transient cross progeny indicated the types of pheromones
paralysis following a brief mechanical shock. A produced are controlled by a single gene, although
temperature-sensitive recessive mutant gene one or more modifier genes controls the precise
(parats) causes D. melanogaster to become ratio of the isomers in hybrid females.
immobile above 29C. The couch potato locus Males of the two O. nubilalis strains are
causes flies to be less active and exhibit abnor- attracted to the appropriate pheromone blends in
mal responses to gravity and light, resulting in the field, but hybrid males respond preferentially
altered flight behavior. The couch potato gene is to the pheromone produced by hybrid females
unusually complex, spanning more than 100 kb rather than to the pheromones produced by the
and encoding three different messenger RNAs. two parental female types. The response of males
Many single gene mutants that affect the mor- to the pheromone is determined by a single
phology of D. melanogaster also affect behavior. sex-linked gene. The olfactory sensillae of the two
Some mutant flies exhibit abnormal behavior types of males are different, which is controlled by
because they are unable to perform the reaction to a an autosomal gene. Hybrid males give intermediate
stimulus due to altered morphology. Other mutants results when their antennae tested for their elec-
exhibit altered behavior because perception of cues trophysiological responses, with E- and Z- olfac-
is impaired. For example, flies with white eyes may tory cells yielding approximately equal responses,
exhibit abnormal courtship behaviors. suggesting that multiple genes are involved. The
452
B Behavior of Insects: Genetic Analysis by Crossing and Selection

genes determining variation in pheromone Morinda. The two species can be crossed and F1
production and organization of male olfactory hybrids are produced. The number of genes
sensillae are not closely linked and are probably involved in resistance was estimated to be three to
on different chromosome. five based on a biometric approach. An analysis
using marker genes suggests that all chromosomes,
except the Y and the small fourth, carry genes
Behaviors Determined by Multiple affecting resistance. Thus, resistance appears to be
Genes neither very simple nor highly polygenic.
D. sechellia is stimulated by Morinda to
Behavior is often controlled by multiple genes with produce eggs, but oviposition in D. simulans is
small additive effects. With such behaviors, the inhibited by this plant. In hybrid progeny, the
task of teasing apart the respective roles of genes inhibition observed in D. simulans is dominant. F1
and environment requires statistical methods of hybrids and backcross progeny exhibit intermediate,
analysis. Drosophila behaviors determined by mul- approximately additive, behavior. These differences
tiple genes include locomotor activity, chemotaxis result in isolation of the two species in nature,
(response to chemicals), duration of copulation, although they overlap geographically. Thus, their
geotaxis (orientation to gravity), host plant prefer- ecological niches are determined by tolerance to
ence, mating speed, phototaxis (response to light), toxic products (including octanoic and hexanoic
preening, and the level of sexual isolation within acids) in the ripe Morinda fruit, with D. sechellia
and between species. Multiple genes may influ- exhibiting a strong preference for Morinda fruits,
ence host plant adaptation and host preference in an ability to detect fragrant volatiles from Morinda
insects. Learning may affect host preference. Host over a long distance, and a stimulation of egg pro-
plant choice usually is a hierarchy of several duction by Morinda. By contrast, egg production
components. in D. simulans is inhibited by Morinda and octanoic
A particularly interesting example of genetic acid in the fruit is toxic to D. simulans.
analysis of host preference in insects is that of
Drosophila sechellia, which is endemic to the
Seychelles archipelago in the Indian Ocean and is Other Behaviors Determined by
morphologically almost identical to its cosmopol- Multiple Genes
itan sister species D. simulans and to the endemic
island species D. mauritiana. When crossed to Other insects in which specific behavioral
either of these species, D. sechellia produces fertile attributes have been shown to be complex
hybrid females and sterile hybrid males. D. sechellia include: Musca domestica (number of attempts
uses the fruit of Morinda citrifolia as its host, which to mate by males); Phormia regina (high and low
may have allowed it to escape competition with ability to learn to extend the proboscis to a
other species of Drosophila there. stimulus applied to the forelegs); hybrid crickets
(call rhythm of males; female response to calling
songs); Anopheles albimanus (ability to avoid
Host Plant Specialization in Drosophila pesticides); Apis mellifera (high and low collec-
sechellia tion of alfalfa pollen, and stinging behavior). The
propensity for cannibalism by larvae of Heliothis
Drosophila sechellia breeds only in Morinda virescens is determined by multiple genes. Most
citrifolia, which is toxic to other Drosophila species. of these behaviors were analyzed by selection
D. simulans breeds on a variety of plants in the experiments.
same geographic area but cannot survive on Behavior of Insects: Molecular Methods
 Behavior: Molecular Genetic Analyses
B 453

References available, it is easier to isolate specific genes

that could be involved in behavior. In addition,
Arathi HS, Burns I, Spivak M (2000) Ethology of hygienic the genetic modification of D. melanogaster by
behavior in the honey bee Apis mellifera L. P-element mediated transformation makes it
(Hymenoptera: Apidae): behavioral repertoire of possible to insert genes from one species of
hygienic bees. Ethology 106:365379
de Belle JS, Sokolowski MB (1987) Heredity of rover/sitter: Drosophila into the genome of another, and
alternative foraging strategies of Drosophila melano- their effect(s) on behavior can be determined.
gaster larvae. Heredity 59:7383 Transgenic D. melanogaster carrying markers
Osborne KA, Robichon A, Burgess E, Butland S, Shaw RA,
such as green fluorescent protein (GFP) also
Coulthard A, Pereira HS, Greenspan RJ, Sokolowski MB
(1997) Natural behavior polymorphism due to a cGMP- allow scientists to determine when and where
dependent protein kinase of Drosophila. Science specific genes are active.
277:834836 Molecular genetic analyses of learning and
Palmer JO, Dingle H (1989) Responses to selection on flight
behavior in a migratory population of milkweed bug
memory in Drosophila may provide a means to
(Oncopeltus fasciatus). Evolution 43:18051808 study one of the most challenging frontiers in
Kha R, Capy SP, David JR (1991) Host-plant specialization n eurobiology. Molecular genetic methods
in the Drosophila melanogaster species complex: a may identify some of the individual genes
physiological, behavioral, and genetical analysis.
Proc Natl Acad Sci USA 88:18351839 among the many involved in determining the
Rothenbuhler WC (1964) Behavior genetics of nest cleaning interesting and complex behaviors exhibited
in honey bees. IV. Responses of F1 and backcross gen- by insects.
erations to disease-killed brood. Amer Zool 4:111123
Analyses of insect behavior employ tech-
Trpis M, Hausermann W (1978) Genetics of house-entering
behavior in East African populations of Aedes aegypti niques from several disciplines, including anatomy,
(L.) (Diptera: Culicidae) and its relevance to speciation. biochemistry, ecology, ethology (study of animal
Bull Entomol Res 68:521532. behavior in the natural environment), genetics,
psychology, physiology and statistics. These
disciplines are required because an insect per-
Behavior: Molecular Genetic ceives the environment through its sensory
Analyses systems. The external sensory stimuli are trans-
duced into electrical information, which is then
marjorie a. hoy
processed and decoded, leading to a behavioral
University of Florida, Gainesville, FL, USA
response. Behavior can be divided into several
sequential steps: stimulus recognition, signal
Molecular genetic techniques are beginning to transduction, integration, and response or motor
provide powerful new methods to analyze insect outputs.
behaviors such as olfaction (response to odors),
learning, circadian rhythms (daily periodicity),
and mating behavior. Prior to the use of molecular The Insect Nervous System
methods, genetic analyses of behavior primarily
involved crossing and selection experiments to Behavior is based on the structure and function of
resolve whether the behavior was genetically the insect central and peripheral nervous systems.
determined and the mode of inheritance of the The insect brain contains around 105106 neurons.
gene(s) involved (e.g., the genes were dominant or It consists of three main divisions, the protocere-
recessive, sex-linked or autosomal, determined by brum, deutocerebrum and tritocerebrum. In each
single genes or more than one). of these divisions, different neuropil regions are
Now that the complete sequence of the located; a neuropil is a dense network of inter
genome of the fruitfly Drosophila melanogaster is woven axons and dendrites of neurons and
454
B Behavior: Molecular Genetic Analyses

euroglial cells in the central nervous system and

n genes for many of these neuropeptides have been
parts of the peripheral nervous system. identified, cloned and sequenced.
In the protocerebrum, higher sensory centers Neuropeptides are released as cotransmitters
are present that are associated with vision and and modulate fast transmission at neuromuscular
other sensory receptors (the mushroom bodies junctions. A given neuropeptide may occur at
and central complex). The superior protocere- several different sites, including central nervous
brum, with the pars intercerebralis, contains system circuits and peripheral synapses, and at
different sets of neurosecretory cells that supply peripheral targets (muscles and glands). Neuropep-
neurohemal organs in the corpora cardiaca and tides regulate behavior by coordinating temporal
corpora allata, which are located in the head or and spatial activity of many neuronal circuits. Each
prothorax in insects. The optic lobes flanking the of the circuits controlling behavior employs sets of
protocerebrum consist of the most well-organized sensory neurons, interneurons and motor neurons.
neuropils in the brain. Thus, multiple neural networks share neural ele-
Mushroom bodies in the brain are associated ments. Molecular genetic analysis is providing rapid
with olfactory pathways, including olfactory progress in understanding neuropeptide receptors
learning. Among the insects, mushroom bodies and second messenger pathways. Research on neu-
differ greatly in size and shape, with the number of ropeptides and their receptors indicates that they
cells ranging from 2,500 in Drosophila to 50,000 in have roles during embryonic development and as
the cricket Acheta, 170,000 in the honey bee and cytokines in the immune systems of insects.
200,000 in the cockroach Periplaneta Molecular genetic analyses are providing
The antennal centers are found in the deuto- significant advances in our knowledge of behavior.
cerebrum; in the tritocerebrum, neurosecretory Behavior is a complex phenotype to study
neurons and neurons associated with the control because it involves the functioning of the whole
of feeding and foregut activity are found. The brain organism, is dynamic, and changes in response to
is connected to the subesophageal ganglion via the environment. Molecular genetic methods are
connectives and to the thoracic and abdominal unlikely to replace traditional methods of behavior
ganglia, or ventral nerve cord. analysis, but the ability to identify, clone, and
Information is transmitted in the insect via sequence specific genes in D. melanogaster makes
nerves and by neuropeptides that coordinate the it possible to understand several behaviors
development and behavior of insects. Both neu- (including the periodicity of biological rhythms,
rosecretory cells and neurons use neuropeptides mating behavior, locomotion, and learning) that
as messengers. Many different types of neuropep- are influenced by single genes.
tides have been identified, including proctolin It is now possible to clone a gene from one
and adipokinetic hormone, that serve as both hor- Drosophila species, insert it into a P-element vector,
mones and neurotransmitters or neuromodulators. and introduce the exogenous gene into mutant
Neuropeptides range in size from three amino acid strains of D. melanogaster to confirm that the
residues (thyrotropin-releasing hormone) to more putative gene does, in fact, code for the behavior of
than 50 (insulin). They are generated from larger interest. Cloned genes from Drosophila can, in
precursor proteins, ranging from 90 to 250 amino some cases, be used as probes to identify genes
acids in length. A number of genes have been from other arthropods, which then can be sequenced
identified that code for neuropeptides, including and compared. The availability of the complete
bombyxin or prothoracicotropic hormone (PTTH), genome of D. melanogaster allows analyses of
eclosion hormone (EH), FMRFamide- related behavior that could not be conducted previously,
peptides, diapause hormone and pheromone as will be described in the discussion of olfaction
iosynthesis-activating neuropeptide (PBAN). The in D. melanogaster (see below).
 Behavior: Molecular Genetic Analyses
B 455

The Photoperiodic Clock mammals, and cyanobacteria. In Drosophila, the

genes called period, timeless, Clock, cycle, double-
The potential that molecular genetics offers is time and cryptochrome are now known to be
exemplified by the analyses conducted using the involved in the circadian clock.
period, and other clock genes, of D. melanogaster.
Most insects exhibit particular behaviors at a
specific time of the day, which due to the action of The Period (Per) Gene of Drosophila
a circadian (approximately 24 h) clock that allows
the insect to measure time. Circadian rhythms The period gene of Drosophila is located on the X
have a number of characteristics: (i) The clocks chromosome. When the wild type gene (called
that regulate such behavior usually are free running per+) is mutated, eclosion (emergence of adults
in constant environments and are not simple from the pupa), locomotor activity and the length
responses to changes in light or temperature. of the interpulse interval of the courtship song are
(ii) Although the rhythms are free running, an affected. Eclosion of wild type flies typically occurs
initial environmental signal is required to start around dawn, when the presence of dew and high
the clock. Among the cues that set the clock relative humidity increase their survival rate.
are alternating light and dark cycles, high and Locomotor activity then decreases during midday
low temperature cycles, or short pulses of light. and is followed by increased activity in the evening.
(iii) The circadian rhythm is relatively insensitive Three classes of per mutants exist; they either
to changes in temperature (temperature compen- shorten (per mutants have 19-h eclosion rhythms
sated). (iv) The clock can be reset by altering the instead of 24-h patterns), lengthen (perL mutants
cues that entrain the clock. have 29-h eclosion rhythms), or completely abolish
Drosophila melanogaster reared in constant circadian eclosion and locomotor activity rhythms
darkness exhibit circadian locomotor activity (per0 mutants). Flies with the per0 mutation eclose
rhythms as adults. However, the rhythms of the arrhythmically, but periodicity in eclosion can be
individual flies composing these populations are restored by P element-mediated transformation of
not synchronized with one another. Rhythms can arrhythmic flies using the wild type per+ allele.
by synchronized if dark-reared flies are exposed to The per gene is approximately 7 kb long and the
light treatments as first-instar larvae (or as later protein produced has a series of threonine-glycine
instars). Light treatments occurring prior to hatching (Thr-Gly) repeats in the middle of the gene. The
of the first-instar larvae fail to synchronize adult region encoding the Thr-Gly repeat is polymorphic
locomotor activity rhythms, indicating the clock in length within and between Drosophila species
functions continuously from the time larvae hatch and plays a role in the thermal stability of the
until adulthood. The rhythm can be advanced, circadian phenotype. For example, either 17, 20 or
delayed, or unchanged, depending on the phase of 23 repeats are found in D. melanogaster populations.
the cycle at which the cue is given. A clinal pattern occurs along a north-south axis in
Molecular genetic analyses of Drosophila Europe and North Africa, with the shorter sequences
clock mutants is providing a fundamental under- in southern Europe, suggesting that the length
standing of the mechanisms of the circadian clock. polymorphism cline is maintained by natural
Rapid advances have been made in the past few selection under different temperature conditions.
years in understanding the molecular aspects of A large number of tissues express the normal
circadian clocks in a variety of organisms. Circadian (per+) product, including embryonic, pupal and
rhythms are found in all organisms, probably adult nervous systems, as well as the esophagus,
evolved early, and common genetic elements are gut and ovaries. The per+ gene product (the PER
present in Drosophila, the fungus Neurospora, protein) is predominantly found in cell nuclei in
456
B Behavior: Molecular Genetic Analyses

adult Drosophila, and per+ messenger RNA levels ranges from a period of 56 ms in D. melanogaster
undergo daily fluctuations, producing a feedback and 3540 ms in D. simulans. D. melanogaster males
loop in which PER affects the oscillations of its with the perS mutation sing with 40-ms periods,
own messenger RNA. The fluctuations in per+ perL males sing with 76-ms periods, and per0 males
messenger RNA are due to fluctuations in gene are arrhythmic.
transcription because the per+ messenger RNA has The genetic basis of species-specific song
a relatively short half-life, which is consistent with instructions was confirmed by the transfer of the
the hypothesis that PER acts to regulate its own per+ gene from D. simulans into D. melanogaster
gene activity. via P element-mediated transformation. The
The per+ genes from Drosophila simulans, D. D. simulans per+ gene restored a rhythm in these
virilis, D. pseudoobscura and D. yakuba have been transgenic D. melanogaster and the transgenic
cloned and sequenced. Parts of the gene are con- D. melanogaster males had mean period lengths in
served among them and parts are highly diverged, their song cycles of approximately 35 ms, which is
which suggests that conserved regions may characteristic of D. simulans males. Thus, substitu-
encode basic functions common to all (clock-type tions in four or fewer amino acids in the per+ locus
functions), while the variable regions may affect was shown to be responsible for this species-specific
species-specific differences influencing love courtship behavior.
songs, locomotor activity and eclosion.
Two X-linked loci, Clock and Andante, are
components of the circadian clock, causing slightly Other Effects of Per
shortened and lengthened cycles, respectively. In
addition, other mutations on the autosomal The per alleles affect locomotion, cellular rhythms
chromosomes induce flies to emerge as adults and development time. Flies with perS develop
from the pupal stage early in a light-dark cycle; faster than wild type flies and perL flies develop
phase-angle flies emerge in the pre-dawn part of more slowly than the wild type.
the cycle instead of just after dawn while gate flies It has long been thought that circadian oscil-
to fail to eclose during this narrow time window. lations provided the clock for photoperiodically
The cryptochrome (cry) gene is an important clock induced diapause in insects. Diapause is a geneti-
component because it encodes a circadian photo- cally determined state of arrested development
receptor in Drosophila. The gene product, CRY, that is induced prior to the onset of detrimental
belongs to a family of blue light-sensitive proteins, conditions. Hibernal diapause, which allows
which includes photolyases and plant blue light insects to survive over winter, is often induced in
photoreceptors. Flies over expressing CRY are insects when insects develop during a period of
hypersensitive to light. The CRY protein is probably cool temperatures under a short daylength, which
the only dedicated circadian photoreceptor in means they must be able to measure light and dark
Drosophila. cycles. However, per+ appears to have no influence
on the photoperiodic clock in D. melanogaster.
Females of a wild-type strain of D. melano-
Song Cycle Behavior in Drosophila gaster (Canton-S) and strains with per mutations
were able to discriminate between diapause-in-
The courtship song is produced when males vibrate ducing short days and non-inductive daylengths.
their wings and consists of two components: D. melanogaster adult females exhibit an ovarian
(i) courtship hums, and (ii) a series of pulses with diapause when reared and held under short days
interpulse intervals, which can fluctuate between and low temperature (12C). Females exposed to
15 and 85 ms. The variation in interpulse intervals long days at the same temperature reproduce.
 Behavior: Molecular Genetic Analyses
B 457

The critical daylength (the photoperiod at which curve to an asymptote. (iii) The change in behavior
50% of the individuals enter diapause) for Canton-S accompanying experience declines in the absence
females at 12C is approximately 14 h of light of continued experience of the same type or as a
per 24 h. Photoperiodic response curves for the consequence of a novel experience or trauma.
perS, perL and Canton-S strains were almost Insect populations vary in their ability to
identical, although per0 flies showed shortened learn. Genetic variability within strains has been
critical daylengths. However, per0 females are used to analyze learning in Drosophila, Phormia
able to discriminate between a long day and a flies and the honeybee Apis mellifera. Drosophila
short day. melanogaster can be sensitized and habituated,
Many behaviors, including learning, involve learn associations with positive or negative rein-
temporally patterned events. The interval between forcement, and be classically conditioned. Droso-
presentation of the conditioned stimulus and phila melanogaster can learn to run away from
reinforcement is important in associative learn- specific odors that they previously experienced
ing. The conditioned stimulus must be presented with electric shock and hungry flies can learn to
before the unconditioned stimulus and the uncon- run toward odors previously associated with a
ditioned stimulus must follow the conditioned sugar reward. Flies can learn visual, tactile, spatial
within a relatively brief interval. It was thought and proprioceptive cues. Analyses of memory
that the per+ gene could be involved in learning, mutants in Drosophila, including the genes dunce,
based on the observation that perL males in one rutabaga, amnesiac, radish, zucchini, cabbage,
experiment did not exhibit normal experience- tetanic, turnip, linotte and latheo, indicate that
dependent courtship behavior. However, males memory consists of distinct phases: short-term,
with the wild type or perS and per0 alleles could be intermediate, long-term and anesthesia-resistant
conditioned normally. memory.
Genetic analyses of learning in Drosophila
melanogaster began in the mid-1970s in Sey-
Learning in Drosophila mour Benzers laboratory when D. melanogaster
was trained to avoid an odor associated with an
It is difficult to produce a single definition of electric shock. The learned avoidance lasted
learning. Learning can be defined as a change in only a few hours, but the odor avoidance test
behavior with experience, but this definition would was used to screen mutagenized flies for strains
not exclude responses such as growth and matura- that had normal olfaction and aversion to shock,
tion, or other processes that are triggered by events but an abnormally-low ability to associate odors
such as mating or feeding. Another definition is a with shocks. The mutants obtained were poor
reversible change in behavior with experience, but learners but each had different phenotypes. One
this excludes phenomena in which the modifica- mutant strain, amnesiac, had a nearly normal
tion caused by some experience is fixed and resis- learning ability but forgot rapidly. The dunce
tant to further change. Another definition is that flies had a shortened memory for several
learning is a more or less permanent change in different conditioned behaviors due to a defec-
behavior that occurs as a result of practice, but this tive gene for cAMP-specific phosphodiesterase,
definition is ambiguous. an enzyme that regulates levels of cyclic AMP
The following properties are characteristic of (cAMP). The dunce flies have elevated cAMP
learning in insects: (i) The individuals behavior levels; cAMP is part of a second messenger sig-
changes in a repeatable way as a consequence of naling pathway in nerve cells that help form
experience. (ii) Behavior changes gradually with associative memories. dunce flies have impaired
continued experience, often following a learning synaptic transmission because the excess of
458
B Behavior: Molecular Genetic Analyses

cAMP leads to hyper polarization of the synap- neurons, it was found that long-term memory
tic terminals, resulting in a chronically lowered requires the vertical lobes. Short-term memory was
availability of neurotransmitter. normal in flies lacking either vertical lobes or the
The dunce gene is one of the largest and most two median lobes.
complex identified in Drosophila, extending over Learning probably requires other brain
140 kb. It produces, by the use of multiple tran- centers, including the antennal lobes, the central
scription start sites and alternative splicing of complex and the lateral protocerebrum in insects.
exons and differential processing of 3 sequences, During metamorphosis, the nervous system of
at least eight to ten messenger RNAs ranging in holometabolous insects such as Drosophila changes
size from 4.2 to 9.5 kb. One unusually large intron significantly. A controversy has existed as to
(noncoding sequence inside the coding region) is whether flies retain learned behavior after
79 kb in length and contains at least two other metamorphosis from larvae to adults, but there is
genes (Sgs-4 and Pig-1) within it. This genes within no evidence that larval conditioning induces a
an intron arrangement is uncommon. One of the change in adult olfactory responses. This is not
contained genes, Sgs-4, is expressed in larval salivary surprising because larval sense organs undergo
glands and provides the glue used by larvae to histolysis during the pupal stage and adult sense
attach themselves to the surface for pupation. organs are formed de novo from imaginal discs.
Sgs-4 is transcribed in the same direction as dunce. The mushroom bodies of the fly brain are
The second gene, pre-intermolt gene, also is extensively rewired during metamorphosis.
expressed in larval salivary glands but is transcribed Drosophila carrying the mutant turnip have
in the opposite direction. Genes homologous to difficulty in olfactory discrimination, conditioning
dunce have been identified in mice, rats and of leg position, larval, visual and reward learning.
humans. The mammalian counterparts of dunce The turnip gene is located on the X chromosome
function in regulating mood. The dunce gene is and is associated with reduced protein kinase
expressed in the mushroom bodies in the brain of C activity. Specifically, the turnip mutant is defective
D. melanogaster. in phosphorylation of pp76, a membrane protein in
Mushroom bodies are important for olfactory head tissues. Protein phosphorylations have been
learning and memory. In D. melanogaster these implicated repeatedly in changes underlying learning
structures are paired and consist of about 2,500 and short term memory.
neurons that send dendrites into a neuropil just Additional genes, including radish, amnesiac,
ventral to the perikarya where inputs arrive from cabbage, latheo and linotte, are involved in
the antennal lobes and other centers of the brain. abnormal learning or memory of D. melanogaster.
Mushroom bodies receive olfactory information For example, flies with the X-linked radish
from the antennal lobes through their dendrites mutation initially learn in olfactory tests, but
located in the calyx, a region of the brain just their subsequent memory decays rapidly at
ventral to the mushroom body. Mushroom bodies both early and late times after learning. The
house part of the short-term memory for odors, radish flies show normal locomotor activity
are required for courtship conditioning memory and sensitivity to odor cues and electric-shock
and are necessary for context generalization in reinforcements used in the learning tests.
visual learning, as well as regulating the transition Anesthesia-resistant memory, or consolidated
from walking to rest. By analyzing a Drosophila memory, is strongly reduced in D. melanogaster
strain with alpha-lobes-absent, a mutation which with the radish phenotype.
causes flies to lack either the two vertical lobes of The rutabaga gene codes for an adenylyl
the mushroom body or two of the three median cyclase, is expressed in Drosophila mushroom
lobes which contain branches of the vertical lobe bodies, and is involved in olfactory short-term
 Behavior: Molecular Genetic Analyses
B 459

memory. Volado, which codes for an -integrin that receptor gene is expressed in 20 olfactory neurons,
mediates cell adhesion and signal transduction, is some receptor genes are expressed in only two to
expressed in mushroom body cells of Drosophila three neurons. Seven olfactory receptor genes are
and mediates short-term memory in olfactory expressed solely in the maxillary palp.
learning. Integrins have diverse biological roles, It is thought that there are fewer than 100 types
including cell-cycle regulation, cell migration and of odor receptors in insects, and perhaps as few as
cell death (apoptosis), functioning as mediators of 50 or 60. By contrast, mammals have more than
interactions between cells with the extra cellular 10,000 different receptor types. The approximately
matrix or with counter receptors displayed by their 5060 odorant receptor genes in insects encode a
cells. They can also transduce information across novel family of proteins with seven predicted
cell membranes bi-directionally membrane-spanning domains; these genes are
The enlightenment obtained from the unrelated to vertebrate or nematode chemosensory
study of these Drosophila learning mutants is receptors, suggesting the genes evolved in an
providing an understanding of learning in independent manner throughout evolution. Fur-
higher organisms. thermore, the Drosophila genes are poorly grouped
into subfamilies of similar sequences because they
are only 1730% similar to each other.
Functional Genomics of Odor
Behavior in Drosophila
Learning in Apis mellifera
The ability to respond to odors is essential for
survival and reproduction, allowing insects to Mushroom bodies in the Hymenoptera are much
select mates, find and choose food, and locate larger than those in Drosophila, which may reflect
appropriate oviposition sites. A beginning has been the importance of the mushroom bodies for
made in understanding the complex genetic basis functions underlying social behavior, learning and
of odor behavior in insects using D. melanogaster memory in the honey bee. Many Hymenoptera
as a model system. (ants, bees, wasps) have complex behaviors that
Odors are received by olfactory receptors include caring for their brood either as individual
located on the third antennal segments and the females or as a social group of females. Bee species
maxillary palps, which send their axons to the such as Apis mellifera feed, protect and nurse
antennal lobes in insect brains. Each third antennal larvae, store food and respond to adverse environ-
segment in D. melanogaster contains about 1,300 mental factors. They search for nectar and pollen
olfactory receptor cells and each maxillary palp at unpredictable sites, learn the celestial and
carries 120 chemosensory neurons. These terrestrial cues that guide their foraging trips over
neurons project to 43 glomeruli in the antennal long distances and allow them to find their nest
lobe of the brain. From there, processed olfactory sites once again. They learn how to respond to the
information is relayed to higher-order brain changing position of the sun, to a pattern of
c enters (the mushroom body and the lateral horn polarized light during the day, and to landmarks.
of the protocerebrum). Associative learning is an essential component to
D. melanogaster has approximately 1,300 foraging behavior and dance communication.
olfactory receptor neurons and D. melanogaster is Hive mates attending a dance performance learn
able to recognize and discriminate between a large the odor the dancing bee carries and seek out that
number of odorants. Each olfactory sensory neuron same odor when they forage for food.
responds to several odorants, but respond maxi- The complexity of bee behavior makes it an
mally to only one. While the average olfactory ideal organism to analyze to better understand
460
B Behavior: Molecular Genetic Analyses

learning, especially in response to odors. Associa- binding proteins) are small, soluble proteins that
tive olfactory learning in honey bees has several are concentrated in the sensillum lymph.
features similar to higher forms of learning in Genes and complementary DNAs encoding
vertebrates. odorant binding proteins of many insects have
been cloned. Analysis indicates that the binding
proteins of unrelated species have low levels of
Pheromones in Insects amino acid sequence similarity, although they do
have a conserved region with cysteines that may
Insects use chemical cues as signals to find mates, be important for function. It appears that there
food, oviposition and hibernation sites. Molecular has been gene duplication and divergence of odor-
genetic methods are now being used to study vari- ant binding protein genes, with moth proteins
ous aspects of pheromone response behavior. For belonging to one branch and the proteins of other
example, genes that code for proteins involved in insects not closely related.
the synthesis of pheromones, the perception of The molecular receptors in an olfactory
semiochemicals, and the processing of the signals system involve G-protein-coupled seven trans-
are being cloned and characterized. membrane proteins. Such proteins also are found
Pheromone biosynthesis appears to use one or in the mouse and rat, where the number of such
a few enzymes that convert the products of normal genes number approximately 1,000 or nearly 1%
primary metabolism into compounds that act as of the genome, indicating that odor reception is
pheromones. For example, pheromones arise from an important component of the mammalian
isoprenoid biosynthesis, or by the transformation genome. Sequencing the Drosophila genome has
of amino acids or fatty acids. A number of the genes allowed receptor similar proteins to be identified
encoding the enzymes involved in transforming in an insect. The receptors are in large multigene
metabolites into pheromones have been cloned families and expressed at different times during
and sequenced. The production of pheromones by antennal development. The receptor genes were
insects is regulated by three hormonal messengers: found by searching the Drosophila genome to
juvenile hormone III, ecdysteroids, and a neuro- identify sequences that might encode transmem-
peptide called PBAN (pheromone biosynthesis brane domains.
activating neuropeptide). Once an odor or pheromone has activated the
Perception of the volatile pheromone is olfactory receptors, it needs to be deactivated.
mediated by olfactory organs (sensillae) located Several enzymes have been found that appear to
primarily on the antennae. Receptor neurons on degrade odor stimulants, including esterases,
the antennae appear to respond to one particular oxidases, and glutathion transferases. Multielec-
chemical (specialist neurons) while others appear trode recording of the Manduca sexta antennal
to respond to a number of compounds (generalist lobe indicates that the relative timing of action
neurons). Pheromones are often perceived in potentials may convey information about odor
combination with other chemicals, including plant concentration and mixture. A large and diverse
volatiles. family of genes coding for taste receptors have
The detection of pheromones and other been identified in Drosophila that are expressed in
chemicals by insects involves proteins (odorant the proboscis.
binding proteins, OBPs) that carry the compounds Rapid advances in understanding olfaction
from the surface of the antennal sensilla through and gustation in insects, especially based on
the sensillum lymph to the G-protein-coupled molecular genetic analyses of D. melanogaster,
receptors and the olfactory neurons. The odorant promise to advance our understanding of how
binding proteins (which includes pheromone insects perceive chemical cues in their environment.
 Behavior: Molecular Genetic Analyses
B 461

Unfortunately, early evidence suggests an extreme of behavior. Est-6 was used to isolate a homolo-
divergence of receptors within D. melanogaster gous gene (Est-5) from D. pseudoobscura. Sur-
that make it difficult to use homology to isolate prisingly, Est-5 has a different function in D.
odor receptor genes from other insects. pseudoobscura. Approximately 40% of Est-5 is
expressed in the eyes of D. pseudoobscura, with
the remainder expressed in the hemolymph of
Divergent Functions of Est-6 and both sexes. Despite these different patterns of
Est-5 in Drosophila Species expression, Est-6 and Est-5 have similar protein
products, messenger RNA transcripts, and DNA
Evolutionary changes in gene regulation can be a sequences.
prerequisite for macro evolutionary change and When Est-5 from D. pseudoobscura was
species divergence. One case study involves an cloned into a P element and introduced into D.
analysis of the esterase 6 enzyme in Drosophila melanogaster, its activity and pattern of expression
melanogaster and its homologue (esterase 5) in D. in D. melanogaster matched those of D. pseudoob-
pseudoobscura. This gene influences behavior in scura. These results imply that regulatory sequences
D. melanogaster but has a very different function in Est-5 have been conserved since the divergence
in D. pseudoobscura. of the two species 2046 million years ago, sug-
Esterase-6 (Est-6) in D. melanogaster influences gesting that the enzyme in the common ancestor
male mating speed and rate of remating by females. of these two species had a more extensive expres-
Fast and slow variants of esterase 6 protein, as sion pattern. After the species diverged, regulatory
detected by electrophoresis, are produced in natural mutations may have occurred that enhanced Est-5
populations of D. melanogaster. More esterase expression in the eyes of D. pseudoobscura, while
6 protein is produced in adult males than in females. mutations in Est-6 led to increased expression in
The enzyme is highly concentrated in the anterior the male ejaculatory duct of D. melanogaster. Thus,
ejaculatory duct of males and is transferred to the use of homology to identify behavioral (and
females during the first 23 min of the 20min other) genes can lead to surprises.
copulation. Enzyme activity in females can be
detected up to 2 h after mating and influences the
timing of remating by females. Males transfer a Courtship Behavior in Drosophila
substance in the seminal fluid which is converted in
the females reproductive tract by esterase 6 into a Mating behavior of D. melanogaster is stereotypi-
pheromone that serves as an antiaphrodiasiac. The cal, with a fixed sequence of actions that are under
antiaphrodiasiac reduces the sexual attractiveness genetic control. Courtship involves visual stimuli,
and receptivity of females, reducing the likelihood acoustic signals, and pheromones. Male courtship
she will remate. Because the sperm from the most behavior involves six elements in the following
recent male takes precedence in fertilizing a females fixed order: orienting following wing vibra-
eggs, this behavior appears to encourage monogamy tion licking attempting to copulate
in D. melanogaster females. Est-6 also influences the copulation.
rate of mating of males in D. melanogaster. Males Sexual differentiation in Drosophila is
with the slow variant of the protein require 10.2 min controlled by a short cascade of regulatory genes,
to achieve copulation with females, while males with the expression of which determines all aspects of
the faster-moving protein require only 5.7 min. maleness and femaleness in the body and the cen-
Once the Est-6 gene was cloned, it was used tral nervous system, including complex behaviors.
as a probe to identify homologous genes in related Such sexual behavior is irreversibly programmed
species, which can provide clues to the evolution during a critical period as a result of the activity or
462
B Behavior: Molecular Genetic Analyses

inactivity of the major control gene tra+. Male the courting male a chance to lick the females
behavior is replaced by female behavior when tra+ genitalia allowing males to attempt copulation.
is expressed around the time of puparium Nonreceptive females leave the courting male, and
formation. if the male pursues her, she may kick him. Non-
Other genes indirectly affect courtship behav- receptive virgin females persistently repel male
ior in Drosophila, including genes that involve: approaches by lifting their abdomens up to block
general behavior (yellow, inactive, couch potato, physically any contacts with males. Nonreceptive
cuckold, minibrain, nerd); visual behavior (white, fertilized females lower their abdomen, extrude
optomotor-blind, no-receptor-potential-A); olfaction their ovipositors and eggs to repel males. Thus,
(smellblind); learning/memory genes (dunce, female receptivity varies with age, diet, hormonal
rutabaga, amnesiac, Shaker, ether-a-go-go); regu- condition and mating experience. The spinster
lating periodicity of behavior (period), courtship mutation affects female sexual receptivity through-
song mutants (cacophony, dissonance, croaker, out their lives, and spinster females continuously
fruitless); female receptivity (spinster). leave, kick, or fend off courting males.
The fruitless mutation is involved in both sex Both D. melanogaster and D. simulans females
determination and courtship behavior and is produce contact pheromones, which consist of
active in the central nervous system. Males with cuticular hydrocarbons that elicit wing displays by
the fruitless mutation may court both females males. These chemical signals have a low volatility,
and males without copulating. Male flies express- and thus act at a very short distance (a few mm)
ing this gene are unable to bend their abdomens and thus are perceived by contact rather than
in the presence of females they are courting smell. Flies from a given strain, sex, and age
because they lack a male-specific Muscle of Law- produce a reproducible pattern of cuticular
rence. Some fruitless mutations cause males to be hydrocarbons, the biochemical pathway of which
homosexual (they do not court females), while is under genetic control. The most important
others cause males to be bisexual (they court hydrocarbons involved in mate recognition or
both males and females). The fruitless+ gene is the stimulation are 7-tricosene and 7-pentacosene.
first gene in a branch of the sex-determination One mutation, Ngbo, influences the ratios of 7-tri-
hierarchy functioning specifically in the central cosene and 7-pentacosene in D. simulans. Another,
nervous system, with mutants of this gene affect- kete, reduces the amount of 7-tricosene and all
ing nearly all aspects of male sexual behavior. It is other linear hydrocarbons but does not affect the
at least 140 kb long and produces a complex array ratio. Flies homozygous for both kete and Ngbo
of transcripts by using four promoters and alter- have reduced viability and fertility, perhaps
native splicing; the male-specific transcripts are because they have very little 7-tricosene.
only expressed in a small fraction of the central Experiments were conducted to eliminate all
nervous system. known cuticular hydrocarbons in D. melanogaster
Another mutation, dissatisfaction, is necessary in order to determine how mating behavior would
for some aspects of sex-specific courtship behavior be modified. The results were surprising; contrary
and neural differentiation in flies of both sexes. to expectation that D. melanogaster females lacking
Mutant males are bisexual but, unlike fruitless males, cuticular pheromones would induce no courtship
attempt to copulate. Males with the dissatisfaction by males, such females remained attractive.
phenotype take longer to copulate with females Additional analysis indicated that undetermined
while females are unreceptive to male advances pheromone(s), probably also cuticular hydrocarbons,
during courtship and do not lay mature eggs. were present on both control and transgenic flies.
Mating behavior of females involves the These newly discovered pheromones could represent
following sequence: stopping moving offering ancestral attractive substances in D. melanogaster
 Behavior: Molecular Genetic Analyses
B 463

and its sibling species. An absence of inhibitory A recessive mutant (bubblegum) in D. mela-
pheromones leads to high levels of interspecific nogaster exhibits adult neurodegeneration similar
mating among Drosophila species, suggesting that to that seen in the human disease adrenoleu-
cuticular hydrocarbons are important in main- kodystrophy (ALD), otherwise known as the dis-
taining reproductive isolation. ease cured in the movie Lorenzos Oil;. In ALD,
high levels of very long chain fatty acids are pro-
duced that can be lowered by dietary treatment
Studies of Human with a mixture of unsaturated fatty acids; feeding
Neurodegenerative Diseases and the ALD flies one of the components, glyceryl tri-
Addictions in Drosophila oleate oil, blocked the accumulation of excess very
long chain fatty acids and eliminated the develop-
Drosophila is perhaps unique among eukaryotes in ment of pathology. Thus, bubblegum flies provide a
the variety and level of sophistication that can be model system for studying mechanisms of disease
applied to understand its neurobiology. Drosophila and screening drugs for treatment.
is being studied, as well, to gain knowledge about Drosophila also has been proposed as a
various neurodegenerative diseases in humans. model organism for studying the genetics of
Modeling diseases in simple invertebrate alcohol abuse and drug addiction in humans.
systems is attractive because genetic interactions Alcohol addiction and many types of drug addic-
can be used to define cellular cascades mediating, tions appear to share common mechanisms. For
for example, death of neurons in Parkinson disease, example, the dopamine hypothesis suggests
the second most common neurodegenerative that addictive drugs may activate certain areas
disorder in humans. Transgenic Drosophila con- of the human brain leading to an increase in
taining a mutant form of the human -synuclein dopamine neurotransmitter release. Elevation of
gene exhibit the essential features of the Parkin- dopamine probably provides a sense of well
sons disease in humans, making it possible to being, pleasure, or elation (positive reinforce-
study the function of -synuclein and determine ment). Dopamine is not the only neurotransmit-
the underlying pathogenic mechanisms in a genet- ter acting in alcohol abuse; glutamate, serotonin,
ically tractable animal. and GABA also are may be involved. Further-
The spongecake mutant of Drosophila shows more, four of the five circadian genes (period,
degenerative changes similar to that seen in clock, cycle, doubletime) identified in D. melano-
humans with Creutzfeld-Jakob disease, while the gaster influence the flys responsiveness to
eggroll mutant produces changes similar to those cocaine and suggest a biochemical regulator of
seen in humans with Tay-Sachs disease. The beta- cocaine sensitization.
amyloid protein precursor-like (Appl) gene of Dros- Selection of D. melanogaster for resistance to
ophila encodes a homolog of the human -amyloid ethanol was shown to be determined by multiple
precursor protein which gives rise to -amyloid, a genetic components. Mutant strains with different
major component of the plaques in the patients responses to ethanol and different responses to the
suffering from Alzheimers disease. Another pro- effects of acute ethanol exposure on locomotor
tein associated with human Alzheimers disease, behaviors are remarkably similar to those described
presenilin, has been found in Drosophila and stud- for mammals. Thus, study of Drosophila could
ies suggest it may also be involved in the develop- pave the way for an in-depth study of the genes
ment of the pathology. A Drosophila homolog was involved in acute and chronic effects of ethanol. In
identified for the human gene for copper/zinc Drosophila, as in mammals, dopaminergic pathways
superoxide dismutase; mutants of this gene are play a role in modulating specific behavioral
implicated in Lou Gehrigs disease. responses to cocaine, nicotine or ethanol.
464
B Behningiidae

Sleep even occurs in Drosophila and may be a but the disciplines of ethology, genetics, physiol-
model for understanding sleep in other animals. ogy, and molecular biology promise to revolution-
Flies that are resting are sleeping, which involves ize the field.
the flies choosing a preferred location, becoming
immobile for periods of up to 157 min at a particu-
lar time in the circadian day, and becoming rela- References
tively unresponsive to sensory stimuli. When rest is
prevented, the flies tend to rest despite stimulation Bellen HJ (1998) The fruit fly: a model organism to study
and then exhibit a rest rebound. Drugs that affect the genetics of alcohol abuse and addiction? Cell
93:909912
sleep in mammals alter rest in flies, suggesting Brady JP, Richmond RC (1990) Molecular analysis of
conserved neural mechanisms. During sleep, an evolutionary changes in the expression of Drosophila
animal cannot forage for food, take care of its young, esterases. Proc Natl Acad Sc USA 87:82178221
procreate or avoid the dangers of predation, indi- Costa RA, Peixoto A, Barbujani G, Kyriacou CP (1992) A lati-
tudinal cline in a Drosophila clock gene. Proc R Soc
cating that sleep must serve an important function. London B 250:4349
Sleep disorders in humans are common, but the Field LM, Pickett JA, Wadhams LJ (2000) Molecular studies in
genes underlying these disorders are unknown. insect olfaction. Insect Mol Biol 9:545551
Fortini ME, Bonini NM (2000) Modeling human neurode-
generative diseases in Drosophila. On a wing and a
prayer. Trends Genet 16:161167
Molecular Analyses of Complex Greenspan RJ, Ferveur JF (2000) Courtship in Drosophila.
Behaviors Annu Rev Genet 34:205232
Greenspan RJ, Tononi G, Cirelli C, Shaw PJ (2001) Sleep and
the fruit fly. Trends Neurosci 24:142145
The genetic basis of many behavioral attributes in Vosshall LB (2000) Olfaction in Drosophila. Curr Opin
insects is probably determined by many genes. Neurobiol 10:498503
Furthermore, behavior is determined, not only by Waddell S, Quinn WG (2001) Flies, genes and learning. Annu
Rev Neurosci 24:12831309
genetic composition, but also by the environment Yamamoto D, Jallon JM, Komatsu A (1997) Genetic dissec-
and can be influenced by learning. The effects of tion of sexual behavior in Drosophila melanogaster.
the environment may mask those of the genotype, Annu Rev Entomol 42:551585
making genetic analysis imprecise. While elabo-
rate statistical techniques have been developed for
quantitative genetic analyses, a thorough under- Behningiidae
standing of behaviors that are quantitatively deter-
mined has been slow to develop. A family of mayflies (order Ephemeroptera).
Understanding the mechanisms of behavior Mayflies
determined by single genes is hard work, but
relatively straight forward. Understanding the
mechanisms of behavior determined by many Beklemishev, Vladimir
genes requires ingenuity and extensive effort. Nikolayevich
However, such research offers many rewards. For
example, advances in understanding the molecu- inna ioffe-uspensky, igor uspensky
lar genetic basis of social behavior in bees and ants The Hebrew University of Jerusalem, Jerusalem,
could allow us to understand the evolution of Israel
female choice, kin recognition, reciprocal altruism,
and the organization of insect societies. V.N. Beklemishev was born on October 5, 1890,
Analysis of insect behavior using insect in Hrodna, then a portion of Poland incorpo-
molecular genetic approaches is still in its infancy, rated into the Russian Empire. He grew up in a
 Beklemishev, Vladimir Nikolayevich
B 465

large harmonious family with a high level of of different species of Anopheles. These
culture and education. From the family he fundamental works included the detailed study
received a good intellectual and moral education of mosquito morphology, mosquito behavior,
that strongly influenced him. He studied in the gonotrophic cycles, physiological age, etc. He
local grammar school which he left as the top wrote that any finding illuminating unknown
pupil. He was interested in natural history and he features in Anopheles biology would be important
collected insects and read books by Braem, Fabre for the success of malaria control. From mos
and other naturalists. In 1908, he entered the quitoes he moved to the study of other groups of
University of St.-Petersburg specializing in arthropods which allowed him to develop a
zoology. After graduating from the University concept of the life scheme of species, which is
(1913) he was kept there to prepare for the title considered as the total amount of species adapta-
of Professor. In 1918 he received his Masters tions to the environment. His concept is rather
degree in zoology and comparative anatomy with close to Hutchinsons concept of a fundamental
the right to lecture. However, because of terrible ecological niche, developed later. He liked and
famine and collapse after the October Revolution estimated the comparative analysis as the mostly
of 1917 he left St.-Petersburg (Petrograd) for fruitful approach in biological study. He was the
Perm (in the Ural Mountains) where he received founder of the comparative parasitology of
the position of an associate professor in the bloodsucking arthropods. Comparing the life
University of Perm. By 1920 he was approved as a schemes of bloodsucking arthropods, he distin-
full professor in the faculty of medicine. He guished main types of their parasitism. He con-
lectured in many general and special courses and sidered the origins and development of arthropod
carried out intensive research on the morphol- parasitism on terrestrial vertebrates. He devel-
ogy of invertebrates, biocenology and hydrobiol- oped well-balanced systems of relationships
ogy. The wide range of his interests and his between parasitic arthropods and their hosts and
excellent erudition in various fields of biology showed the role of such systems in biocenoses.
were of great importance when in 1924 he headed During the 1950s he worked intensively on the
an entomological study at the Malarial Station of problem of tick-borne encephalitis in the USSR
the Medical and Biological Institute of Perm. and significantly contributed to the understand-
Working on the ecology of Anopheles larvae, he ing of the structure of natural foci and epidemi-
studied hydrobiological characteristics of larval ology and epizootiology of this infection. All his
biotopes and the habitat distribution of mosquito ideas were not only theoretical constructions but
larvae. He evaluated the significance of water the result of laboratory studies and field expedi-
bodies in different landscapes not only from an tions to different areas of the USSR in which he
entomological but also from an epidemiological participated together with his younger fellows.
point of view. As a result, he formulated the His main publications include: Ecology of the
doctrine of landscape malariology which allowed malarial mosquito (Anopheles maculipennis
the planning of control measures based on the Mgn) (1944); The planning of settlements and
characteristics of a particular landscape. In 1932 the problem of malaria (1949); Manual of
he was invited to Moscow to head the Depart- medical entomology in two volumes (editor and
ment of Medical Entomology in the Tropical the author of many chapters) (1949); Key to
Institute (later the Martsinovsky Institute of arthropods injuring human health (editor and
Medical Parasitology and Tropical Medicine). the author of some chapters) (1958). He was also
The biology of adult mosquitoes was the main the editor of many proceedings and books.
aspect of his interest at that time. Together with Unfortunately, most of his papers were published
his followers he studied the population biology only in Russian. He was well known among world
466
B Belidae

zoologists as the author of his greatest work State College, M.A. in zoology in 1966 from the
Principles of comparative anatomy of inverte- University of Massachusetts, and Ph.D. in 1969
brates which had three editions in the USSR from the University of Pennsylvania. The subject
(1944, 1952, 1964) and was also published in of his Ph.D. research was the role of juvenile
Romania, Poland and the German Democratic hormone in vitellogenesis. Then followed a
Republic. In 1969 this monograph was published 1-year postdoctoral fellowship at the University
in English (Edinburgh). In recognition of his of Texas before he was appointed assistant pro-
works he was elected to the Academy of Medical fessor of entomology at the University of Kansas.
Sciences of the USSR, and twice he was awarded His career was spent in Kansas, and he was pro-
the USSR State Prize. He was elected to the Polish moted to full professor at the age of 33. He taught
Academy of Sciences. He was also much revered undergraduate and graduate classes and, between
by his numerous pupils many of whom became 1970 and 1996 had trained 18 Ph.D. and eight
well-known specialists. His interests were not M.A. students in his laboratory. His research
limited by biology only. He knew history, liked interests, begun with developmental biology,
and knew Chinese art and philosophy, and he expanded to reproductive physiology, chemo-
liked poetry, fine art and architecture. He wrote perception, and related behaviors, and began to
verses himself. He died on September 4, 1962. In include field work. He served as editor of Journal
1970 his pupils published a collection of his most of the Kansas Entomological Society (1982
important papers under the title Biocenological 1984), co-editor of Environmental Entomology
principles of comparative parasitology. (19841987), and as editorial board member of
Journal of Insect Physiology. He served as editor
of Journal of Insect Behavior, which he and
References Tom Payne founded, from 1988 until his death.
He published over 100 research papers and
Balashov YS (1991) The significance of V.N. Beklemishevs reviews, edited three books, and wrote two:
concepts of parasitic systems and life schemes of the (1981) The laboratory cockroach, and (1991)
species for the development of parasitology. Parazi-
tologiya 25:185195 (in Russian)
Searching behavior: the behavioral ecology of
Smirnov ES (1962) Scientific activity of V.N. Beklemi finding resources. He died on October 17, 1998,
shev. In: Problems of general zoology and medical after a long illness, survived by his one son and
parasitology. Medgiz, Moscow, USSR, pp 738 (in former wife.
Russian)

References
Belidae
Greenfield MD (1998) William J Bell 19431998. J Kans
A family of beetles (order Coleoptera). They Entomol Soc 71:12
Greenfield MD (1999) William J Bell. Am Entomol 45:59
commonly are known as primitive weevils.
Beetles

Bell, William J Belostomatidae

Bill Bell was born in Boston, Massachusetts, on A family of bugs (order Hemiptera). They some-
January 10, 1943. His B.S. degree in biology and times are called giant water bugs and toe biters.
education was earned in 1964 from Bridgewater Bugs
 Bertha Armyworm, Mamestra configurata Walker (Lepidoptera: Noctuidae)
B 467

Beneficials Importance

Organisms that provide a benefit to crop produc- The economic impact of bertha armyworm is
tion, especially natural enemies of pests and plant attributed to its importance as a major pest of
pollinators such as bees. canola crops. Young larvae consume the leaf foli-
age of canola and the plant generally compensates
for this damage. The fifth and sixth instars cause
Benthic Community the greatest damage because they feed on the
developing nutrient rich seedpods, adversely
The community of organisms inhabiting the affecting seed quality and lowering seed grade.
bottom of a body of water. Since 1922, bertha armyworm outbreaks have
occurred at intervals of varying length and persist
from one to three years. Since 1970, the increase in
the incidence of bertha armyworm outbreaks has
Bertha Armyworm, Mamestra been associated with the extraordinary increase in
configurata Walker (Lepidoptera: the number of hectares planted to canola. Most
Noctuidae) outbreaks are local and not synchronized with
those of other areas. Widespread outbreaks cost
peter g. mason producers $10s of millions in yield losses and
Agriculture and Agri-Food Canada, Eastern control costs.
Cereal and Oilseed Research Centre, Ottawa, ON,
Canada
Biology
The bertha armyworm, Mamestra configurata,
atta- cks canola (Brassica napus L. and Brassica Bertha armyworm has a univoltine life cycle
rapa L.) in the northern great plains of North requiring 68 weeks from egg to pupa, which
America. Other crops subject to damage by ber- overwinters. Adults emerge from the soil from
tha armyworm include flax, Linum usitatissimum early June to early August and are attracted to
L., sweet clover, Meliotus officinalis L., and alfalfa, canola fields that are in bloom. The moths are
Medigaco sativa L., although development is not nocturnal, and females copulate during the 2nd or
completed or progeny are undersized. Bertha 3rd night after emergence, remaining in copula for
armyworm is a Nearctic species, apparently about 17 h. Females lay single-layered masses of
restricted to dry grassland-type habitats in west- 20200 eggs on the underside of leaves of host
ern North America. It prefers the native weed plants, depositing 75% of their egg complement
Chenopodium album (lambs-quarters) but suc- during the first week after emergence and up to
cessfully develops on B. napus and B. rapa variet- 3,500 eggs during their lifetime.
ies with low isothiocyanate and glucosinolate Eggs are spherical, slightly flattened on the
levels (canola). Mamestra configurata has one ventral surface, about 0.45 mm in diameter and
North American relative, Mamestra curialis with a series of longitudinal ridges and depres-
(Smith). The larvae of the two species are difficult sions (sculpting) radiating from the upper mitotic
to separate but adults are distinguished by the pole. The white eggs develop for approximately
wing markings and by c haracters of the male gen- one week. As development takes place the eggs
italia. The two species also occupy different habi- become almost black. Just before they hatch, the
tats, M. curialis occurs primarily in forested areas black headed first instar larvae are visible through
while M. configurata is found in grassland areas. the chorion.
468
B Bertha Armyworm, Mamestra configurata Walker (Lepidoptera: Noctuidae)

First-instar larvae hatch and immediately and females are distinguished by the structure of the
isperse from the egg mass to feed on foliage. The
d terminal abdominal segments. Bertha armyworm
larvae feed at night and when disturbed they may pupae are not easily distinguished from other
drop off the leaves using a fine silk thread which cutworm pupae. The pupae undergo a facultative
they use to climb back onto the plant. Large larvae diapause, induced by temperature and photo-
may drop off the plants and curl up when disturbed, period cues experienced by 46 instar larvae. If fall
behavior typical of cutworms and armyworms. conditions are unusually warm some pupae continue
The first four instars feed on foliage and, although development and will emerge. Over-wintering
they prefer foliage, the final two instars feed on the mortality of pupae is important and is influenced
developing pods, the most nutrient-rich plant part by duration of exposure to temperatures near or
during this time of the growing season. The final below freezing.
instar larva consumes 7080% of the total food The adult is large with a wingspan of about
consumed by the six larval stages. The dark color 4 cm. The forewing is mostly grey with patches of
of the last two larval instars makes them noticeable black, brown, olive and white scales. The distin-
in the crop. At summers end the mature larvae guishing feature of the bertha armyworm moth is
drop to the ground and seek shelter in cracks the broad olive band adjacent to the subterminal
516 cm below the soil surface where they pupate. line, defined by white markings on the inner side
Larvae vary greatly in color, particularly the older of the forewing.
individuals. Outbreaks of bertha armyworm are sporadic,
Newly hatched first instar larvae have a yet consist of huge numbers of larvae infesting
distinct black head and are about 0.3 cm long and canola crops. Population monitoring is important
are covered with sparse but distinct setae. The next for determining the potential for damage. Adult
five instars have light brown head capsules and the bertha armyworm can be detected by close inspec-
body setae are less evident. The first four instars tion of lambs-quarters and canola plants where
are green, usually with distinct, narrow, whitish, they roost during the day on the underside of
stripes on their back, and a wider but indistinct leaves. Egg masses and early instar larvae are found
band on the side of the body. Most fifth instar by inspecting the underside of leaves. The dark late
larvae are green, others brownish green, or brown instar larvae are readily visible when feeding on
with darker markings. The sixth instar, about 4 cm developing seedpods on the tops of canola plants,
long, is commonly velvety black or brown with even at a distance. Area-wide pest management
conspicuous yellowish-orange stripes along programs use traps baited with a species-specific
each side and a green underside which contrasts sex pheromone to monitor bertha armyworm adult
with the dark dorsum. Individuals of the velvety numbers. The data are refined and mapped using
black form have three narrow, interrupted white geographical information systems (GIS) to provide
stripes along their backs. In nature, many variants an early warning of outbreak potential. Producers
are found, singly or in homogenous groups, and in areas of high risk are advised to regularly inspect
appear to represent different species, increasing the their crops to assess larval densities.
difficulty of accurate identification. Larvae may
exhibit limited local migration, typical of armyworms,
when their preferred food source is consumed. Management
Pupae are reddish, slender, 5.5 mm wide and
18.5 mm long, gradually tapering caudally with Chemical insecticides are registered for use against
flexible abdominal segments. The terminal spines are bertha armyworm. The decision to apply insecti-
stout, about 0.7 mm long, close set but slightly cides is based on the larval densities associated
divergent, and slightly out-curved at the tip. Males with the value of the crop and the cost of spraying.
 Bequaert, Joseph Charles
B 469

However, insecticides harm natural enemies, Mason PG, Erlandson MA, Youngs BJ (2001) Effects of
parasitism by Banchus flavescens (Hymenoptera: Ich-
particularly parasitoids of the bertha armyworm.
neumonidae) and Microplitis meditor (Hymenoptera:
Cultural control methods for reducing the Braconidae) on the bertha armyworm, Mamestra
impact of bertha armyworm include crop rotation configurata (Lepidoptera: Noctuidae). J Hymenopt Res
and tillage. Crop rotation has limited effectiveness 10:8190
Mason PG, Turnock WJ, Erlandson MA, Kuhlmann U,
because adult bertha armyworm are strong fliers Braun L (2001) Mamestra configurata Walker, bertha
and readily invade neighboring crops. Fall tillage armyworm (Lepidoptera: Noctuidae). In: Mason PG,
may increase the overwintering mortality of pupae Huber JT (eds) Biological control programmes in
and spring cultivation may injure the pupae but Canada 19812000. CABI Publishers, Wallingford, UK
pp 169176
these methods are not used where minimum Rempel JG (1951) A study of the embryology of Mamestra
tillage is practiced. configurata (Walker) (Lepidoptera, Phalaenidae). Can
Naturally occurring diseases, such as the Entomol 83:119
fungus Entomophthorales sp., a nuclear polyhe-
drosis virus (NPV), and the microsporidian
Nosema sp., are important larval mortality factors Berytidae
at high population densities and NPV infections
in up to 95% of local populations have been A family of bugs (order Hemiptera). They some-
recorded. Of the native parasitoids, only Banchus times are called stilt bugs.
flavescens Cresson (Ichneumonidae) and Athrycia Bugs
cinerea (Coquillett) (Tachinidae) cause significant
mortality in bertha armyworm populations.
During outbreaks, B. flavescens, which attacks early
instar larvae, is usually the most abundant parasi- Bequaert, Joseph Charles
toid, although A. cinerea occasionally is more
abundant. Parasitism significantly reduces food Joseph Bequaert was born in Thourout, Belgium,
consumption by bertha armyworm larvae. The on May 24, 1886. He earned a Ph.D. from
effect of arthropod predators on bertha armyworm Universiteit Gent in natural sciences in 1908. In
populations is unknown. Vertebrates, particularly 19101912, he worked for the Belgian sleeping
birds, may be important when population sickness commission, and in 19131915 in what
densities are high. How natural enemies regulate was then the Belgian Congo. He emigrated to the
bertha armyworm populations between outbreaks USA and became (19171922) an associate of the
is not known. American Museum of Natural History as ento-
mologist, malacologist, and botanist. He became
a U.S. citizen in 1921. In 19231925 he worked as
References an instructor in entomology at Harvard Medical
School (Massachusetts, USA), in 19251945 as
Bracken GK (1984) Within plant preferences of larvae of assistant professor, and in 19291956 as curator
Mamestra configurata (Lepidoptera: Noctuidae) feeding of insects in the Museum of Comparative Zoology
on oilseed rape. Can Entomol 116:4549 at Harvard University and in 19511956 as
Bracken GK (1987) Relation between pod damage caused by
larvae of bertha armyworm, Mamestra configurata A gassiz Professor of Z oology at the same
Walker (Lepidoptera: Noctuidae), and yield loss, shelling, institution. Then he moved to the University of
and seed quality in canola. Can Entomol 119:365369 Houston (Texas, USA) as professor of biology,
Mason PG, Arthur AP, Olfert OO, Erlandson MA (1998) The
moving to the University of Arizona in 1960. His
bertha armyworm (Mamestra configurata) (Lepidoptera:
Noctuidae) in western Canada. Can Entomol final move was to the University of Massachusetts.
130:321336 He married Frances A. Brown in 1927 and they had
470
B Beraeidae

two children. His interests were in entomology

(especially medical entomology) and malacology
(especially medical malacology); he published
major works in both areas and was president of
the American Malacologists Union in 1954. He died
in Amherst, Massachusetts, USA, on May 24, 1982.

References

Abbott RT, Young ME (eds) (1973) American malacologists:

a national register of professional and amateur
malacologists and private shell collectors and biogra-
phies of early American mollusk workers born between
1618 and 1900. Falls Church, Virginia, USA, American Berlese, Antonio, Figure34 Antonio Berlese.
Malacologists/ Philadelphia, USA: Consolidated/
Drake Press, 494 pp history and collected insects and mites. His
Clench WJ (1982) Joseph Charles Bequaert 18861982. Nau-
tilus 96:35 studies at Universit di Padova (the University of
Padua) resulted in a degree in 1884 in natural sci-
ences. He worked for a few months in a school of
human anatomy, but then accepted a post at Stazi-
Beraeidae one di Entomologia Agraria in Florence, which
Adolfo Targione Tozzetti had founded and then
A family of caddisflies (order Trichoptera). directed. Finishing a professional course in 1887,
Caddisflies he worked as Targionis assistant until 1890 when
he was nominated for a position as professor of
general and agrarian zoology at R. Scuola Superi-
Bergmanns Rule ore di Agricoltura di Portici, where he worked
until 1903. Then, he was nominated director of the
Among mammals and birds, individuals of a species R. Stazione di Entomologia Agraria in Florence,
occurring in colder climates tend to have a larger succeeding Targioni. He built up this station little
body mass, and a correspondingly lower surface to by little until it became one of the best-equipped
volume ratio, than members of the same species in Italy. From his first publication in 1880, he
living in warmer climates. This trend results from worked 47 years without interruption, producing
the need to conserve heat in cold climates but to a total of 275 publications. A large part of his work
eliminate excess heat in hot climates. A variant of was devoted to the study of mites, in which he
this is Allens rule. These rules do not apply to built a collection of 12,750 slide-mounted speci-
ectothermic animals such as insects. mens. Another major endeavor was his work on
Allens Rule olive fruit fly, and yet another on the scale Diaspis
Thermoregulation pentagona. His two-volume book Glinsetti, loro
organizzazione, sviluppo, abitudini e rapporti
colluomo with 2,187 figures, was published in
Berlese, Antonio parts, from 1904 to 1923. His awards included a
prize of 10,000 lire from the R. Accademia di Agri-
Antonio Berlese (Fig.34) was born in Padua on coltura di Torino, a gold medal from the province of
June 26, 1863. As a boy, he was interested in natural Venezia in 1913, an award of 75,000 lire from the
 Bernhauer, Max
B 471

council of the province of Udine in 1924, and hon- he obtained in 1899 was as doctor juris (doctor of
orary membership in the Socit Entomologique de law), not as a biologist. He worked as a notary in
France. He died in Florence on October 24, 1927. Austria. It was Ludwig Ganglbauer, in particular,
who instructed Max on Coleoptera. His first two
References papers were published in 1898. Because of the
dearth of people willing to study and identify
Paoli G (1928) Antonio Berlese. Memorie della Societ Staphylinidae, Max was soon presented with an
Entomologica Italiana 6:5584 endless flow of specimens collected from around
the world, and asked to identify them (cost free, of
course). For Max, this was a seemingly endless
Berlese Funnel opportunity to classify and describe the species of
the huge family Staphylinidae, and to build his col-
An extraction devise used to separate and extract lection. He collaborated with Karl Schubert and
small arthropods from leaf litter or similar material. Otto Scheerpeltz in producing a world catalog
A Berlese funnel normally consists of a funnel with (published by Junk-Schenkling as part of Coleopter-
a wire mesh insert that support the plant material orum Catalogus;), completed in 1926 and listing
above a reservoir containing alcohol or another 12,740 species, but expanded to 19,900 species by
preservative. As the arthropods move about, 1932 by Otto Scheepeltz and continuing to grow.
particularly as they move deeper into the funnel to The world total of Staphylinidae as of the year 2000
escape drying of the plant material, they slip down exceeded 45,000 species, and Max Bernhauer had
the funnel into the reservoir containing liquid described 5,251 of them, including 342 new genera,
where they are retained for identification. This tech- in his 285 publications, a spectacular achievement
nique is useful for many arthropods, but not for for an amateur coleopterist. Names of the vast
those that may fly to escape, or those that are very majority of the species that he described are still
fragile and perish from desiccation before they can considered valid, even though he was not in the
escape the plant material. A modern variant of the habit of providing illustrations or keys for identifi-
Berlese funnel is the Tullgren Funnel, which is cation, so that confirmation of identity of the spe-
simply a Berlese funnel with an incandescent light cies he described is often very difficult. He died on
suspended above the funnel to provide a source of March 13, 1946, in Horn, Austria. His collection was
heat and to extract the arthropods faster. Another sold, soon after his death, a negotiation achieved by
variant uses a cover to eliminate escape by insects Rupert Wenzel, to the Field Museum of Natural
capable of flight, and to more efficiently direct the History, Chicago, USA. There seems to have been a
heat generated by the light bulb. Most Berlese teacher-student train Erichson-Ganglbauer- Bern-
funnels now used are actually Tullgren funnels, but hauer-Scheerpeltz among the German-speaking
the distinction is not generally appreciated. students of Staphylinidae, which, unfortunately,
ended with Otto Scheerpeltz.

Bernhauer, Max References

Max Bernhauer was born in Mglitz, Austria Herman LH (2001) Bernhauer, Max. Bull Am Mus Nat
(otherwise known as Mohelnice, and now in the History 265:4344
Czech Republic) on September 24, 1866. His Puthz V (1980) Bibliographie der Publikationen Max Bern-
hauers (18661946) [a bibliography, not a biography].
education was in Olomonic (now in the Czech
Philippia 4:248261
Republic) and then at Universitt Wien (the Rambousek G (1916) Ein Lebensbild Dr. Max Bernhauers.
University of Vienna, Austria), but the final degree Coleopterologische Rundschau 5:7382
472
B Berothidae

Berothidae Bess Beetles (Coleoptera:

Passalidae)
A family of insects in the order Neuroptera. They
commonly are known as beaded lacewings. jack schuster
Lacewings, antlions, and mantidflies Universidad del Valle de Guatemala, Guatemala
City, Guatemala

Bess, patent-leather, or passalid beetles are

Bertram, Douglas Somerville common, primarily tropical insects. A few of the
approximately 600 species occur in temperate
Douglas Bertram was born in Glasgow in 1913. regions (China, Japan, Korea, Canada, U.S., and
His Bachelors degree was from Glasgow Univer- Tasmania, but not Europe, though the largest
sity, after which he did graduate research and collection in the world may be that of the Paris
was employed as a demonstrator in the Zoology Museum of Natural History). Five species have
Department of that university. In 1938 he moved been collected in the U.S. (Compare to Guate-
as Lecturer in Entomology to Liverpool School mala, the size of North Carolina, with 84 species!)
of Tropical Medicine, began insect cultures, and The most common, Odontotaenius disjunctus
performed research on fowl malaria. In 1940, he (Illiger), is known from the East Coast to the
enlisted in the British army and served in Egypt riparian forests of the eastern Great Plains north
and Greece, but was captured in Crete and to Manitoba and Ontario, and south to Texas and
remained a prisoner in Germany for the dura- Florida. Another species, O. floridanus Schuster
tion of the war. In 1946, he returned to Liverpool is known only from sand hills of Florida scrub
for two years and worked on cotton rat filariasis habitat which used to be islands during previous
and on control of warble fly. In 1948, he was interglacial times. Two other species, Passalus
appointed as Reader in the Department of Medi- punctiger Lepeletier & Serville and P. punctatos-
cal Entomology in the London School of Hygiene triatus Percheron, were collected at the beginning
and Tropical Medicine, later becoming head of of the twentieth century in eastern Arizona; they
the department. His research was directed to may have been brought from Mexico in wood
mosquitoes, especially their age-grading, and shipped by train. They havent been collected in
their transmission of viruses and fowl malaria, the U.S. since that time. A fifth species, Ptichopus
but extended to other biting families of biting angulatus (Percheron), was recently collected in
flies, and to biological control of triatomine bugs. Arizona. This has been expected; it occurs in
He traveled extensively to tropical countries to leaf-cutter ant nests just south of the Rio Grande
further his research. He was consultant in ento- in Texas.
mology to the British army, fellow of the Royal Flightless beetles tend to originate on islands
Entomological Society, of the Institute of Biol- or (in passalids especially) on isolated mountains,
ogy, and of the Royal Society of Tropical Medi- resulting in high levels of endemism (an endemic
cine and Hygiene. He died in 1988. organism is one found only in a given area, e.g.,
endemic to Guatemala, or endemic to Pikes Peak).
The distribution of endemic passalids correlates
with the distribution of other endemic organisms.
References Because passalids are relatively easy to find, they
can be used as indicator organisms for areas of
Busvine JR (1989) Obituary. Douglas Somerville Bertram. endemism, especially for cloud forests on tropical
Antenna 13:89 mountains. For example, eight areas of endemism
 Bess Beetles (Coleoptera: Passalidae)
B 473

have been identified for Guatemala and adjacent Passalids are in the superfamily Scarabaeioidea
Chiapas, Mexico, on the basis of passalid distribu- together with the more famous scarab beetles. They
tions. This is important for prioritizing areas for are large beetles (length 11 to more than 80 mm)
conservation. and are orange or reddish when they hatch from
Only one fossil passalid is known, similar, if the pupal case; most change to a shiny black color
not identical, to a species known from the lowland as they mature. Most have grooves (striae) in the
neotropical forests, today reaching only to north- elytra (wing covers). Many have a horn of some
ern Mexico. This fossil, from Oregon, implies the sort in the center of the head. In the Americas, most
presence of such forests there in the Oligocene, have three lamellae in the antenna, some four or
more than 25 million years ago. five; some Old World species have more lamellae.
The classification of the Passalidae is: Certain Old World passalids have an asymmetrical
Order: Coleoptera face; such asymmetry is rare among animals.
Superfamily: Scarabaeioidea Beetles of some other families look remark-
Family: Passalidae ably like passalids; indeed, one tenebrionid from
Subfamily: Passalinae Africa has the epithet passalioides. Tenebrionids
Subfamily: Aulacocyclinae and lucanids which resemble passalids also live in
The Aulacocyclinae are restricted to the area from rotting wood; however, certain carabids (e.g., Scarites)
India to Oceania and Australia. The Passalinae are are superficially similar to passalids, but live
mostly pan-tropical. This subfamily is divided into underground. Some scarabs resemble passalids,
two tribes: Proculini, restricted to the Americas, and but live in dung or underground as well.
Passalini, which is mostly pan-tropical. Eggs are placed in a specially constructed nest
Most passalids live in rotting wood; a few live of masticated wood pieces and feces (frass) and
in other habitats, such as leaf-cutter ant detritus are red. As they mature they change to brown,
chambers, termite nests or under the roots of then green when ready to hatch. The larvae are
epiphytic bromeliads all sites of decaying organic easy to recognize; they look like white grubs
matter. Those in wood prefer broadleaf trees; oak though not as curved and they have only four
is a favorite. Some occur in palms and a few in easily visible legs. Actually, they do have 6; the hind
pines, but few in other conifers. They are most pair is reduced to a scraping organ that is rasped
common and diverse in tropical lowland and against the base of the second pair of legs. This
montane wet forests; up to ten species may be produces a sound, the function of which is
found in a single log (in Brazil). Some, flatter unknown.
species, are specialized for living under the bark; The larvae (and adults) require frass for
others bore deep into the logs. They appear to be feeding; even adults will die if no feces are included
quite important as wood decomposers in forest in their diet. They apparently have an external
ecosystems. rumen, as do rabbits; they feed on the fungi and
An unusual number of species of other organ- bacteria and the products of microorganism
isms are associated with passalids, especially mites digestion that are in the feces.
and certain fungi, perhaps due to their boring in The larvae pupate in a specially constructed
wood (other groups with high mite diversity include cocoon of frass that the adults and larvae build
scolytid beetles, also wood borers). At least ten together. The fact that young adult siblings of a larva
species of mites are associated with O. disjunctus in will repair a damaged pupal case implies a high
the eastern U.S. Various animals attack passalids, level of subsocial behavior for these beetles. Adults
including vertebrates (birds and mammals, and live at least two years in nature and to at least 5 years
probably some reptiles and amphibians), nematode in the laboratory. Some species have large colonies
worms, tachinid flies, and reduviid assassin bugs. with many individuals; others seem restricted to a
474
B Beta Taxonomy

pair and perhaps their offspring. Generally, only Bet-Hedging

mature individuals migrate. Though adults may be
found flying or walking at many times of the year, Variable life history strategies within an insect
they appear to be most commonly migrating at the population resulting from genetic or phenetic
beginning of the rainy season in the tropics. polymorphism. Bet-hedging is manifested by
Adults stridulate as well, producing sounds by variation in diapause, wing development, rate of
rubbing the dorsal surface of the abdomen against development, rate of reproduction and other
the hind wings. In species that dont fly, the wings critical life history traits. Bet-hedging equips a
are reduced to thin straps, but with the stridulatory population to survive variable and unpredictable
area preserved. Passalids are known to produce up environments that may favor certain traits in one
to 14 different acoustical signals in one species, season and certain traits in others.
more than many vertebrates. Pheromones, chemical
communication, is also apparently used. Sounds
are used when fighting other individuals, usually of Bethylidae
the same species. Also, sounds are important in
courtship, which involves a dance that can last as A family of wasps (order Hymenoptera).
long as 12 h in the laboratory. At least in some Wasps, ants, bees, and sawflies
species, copulation occurs in the tunnels of a log;
however, O. disjunctus has been observed copulating
during flight! At least in the laboratory, copulation Bias
begins venter to venter, a rare position for insects.
In sampling, an unidirectional deviation of an
References estimate from the true mean or variance of a
population.
Reyes-Castillo P (1970) Coleoptera, Passalidae: morfologia y Sampling Arthropods
division en grandes grupos; generos americanos. Folia
Entomologica Mexicana 2022:1240
Schuster J (1983) Acoustical signals of passalid beetles:
complex repertoires. Fla Entomol 66:486496 Bibionidae
Schuster J (2002) Passalidae. In: Arnett R Jr, Thomas M (eds)
American beetles vol 2. CRC Press, London, UK A family of flies (order Diptera). They commonly
Schuster J, Schuster L (1997) The evolution of social behavior
in Passalidae (Coleoptera). In: Choe J, Crespi B (eds) The are known as March flies.
evolution of social behavior in insects and arachnids. Flies
Cambridge University Press, Cambridge, UK, pp 260269
Schuster J, Cano E, Cardona C (2000) Un metodo sencillo para
priorizar la conservacion de los bosques nubosos de
Guatemala, usando Passalidae (Coleoptera) como organ- Bicaudate
ismos indicadores. Acta Zoologica Mexicana (n.s.)
80:197209 Having two cauda, or filamentous tail-like pro-
cesses, at the posterior end of the body.

Beta Taxonomy
Biddies
The arrangement of species into higher categories
of classification. A family of dragonflies in the order Odonata:
Alpha Taxonomy Cordulegastridae.
Gamma Taxonomy Dragonflies and Damselflies
 Biocenology (Biocoenology)
B 475

Biennial second is the species, and is not capitalized. Both

words are italicized. The authors name (the person
A plant that completes its life cycle in two years who first provided a technical description of the
and usually does not flower until the second grow- species) often follows the scientific name. If the
ing season. genus name has been changed since the organism
was named by the author, then the authors name
is placed in parentheses to indicate that a change
Bifid has been made. When several species in the same
species are discussed together, then species may
This refers to a structure that is forked, or divided be abbreviated spp. For example, in discussing the
into two parts or lobes. More commonly it is genus Spodoptera, we might refer the members as
described as bifurcate. Spodoptera spp. On the other hand, a single species
is indicated as sp.

Bifurcate
Binomial Sampling
This refers to the division of a structure into two
parts, as when it is forked; it is also called bifid. The A sampling method that involves recording only the
point where the division occurs is called the presence or absence of members of the population
bifurcation. being sampled (such as an insect pest) in a sample
unit (such as a leaf), rather than counting the
numbers of individuals. This is a type of presence-
absence sampling. (contrast with enumeration
Big-Headed Flies sampling).
Sampling Arthropods
Members of the family Pipunculidae (order
Diptera).
Flies Biphyllidae
A family of beetles (order Coleoptera). They
Bilateral Symmetry commonly are known as false skin beetles.
Beetles
This refers to symmetry of the body in which one
side is a mirror image of the other side. When
divided along the main axis, insects are almost Bioassay
always bilaterally symmetrical, with the left and
right halves being mirror images. The use of a living organism to determine the
effect of any chemical (or biological agent), such as
a semiochemical, upon the organism.
Binomial Nomenclature

A system of naming organisms with two names, Biocenology (Biocoenology)

the genus and species. This binomial is also known
as the scientific name, and is in Latin. The first of Study of the organization and functioning of
the two names is the genus, and is capitalized. The communities, particularly a descriptive analysis of
476
B Biocenosis (Biocoenosis)

assemblages of interacting populations within a Decreased insecticide use helps preserve natural
particular area. This term is most popular in enemies, reduces insecticide residues in crops,
Europe; elsewhere it is referred to as synecology or and delays the development of insecticide resis-
community ecology. In some respects, it is the tance. Other benefits are the conservation of
opposite of autecology. petroleum products, increased safety to farm
Biocenosis workers, local residents and the environment.
Additionally, models of insect biotic potential
and life cycle timing can increase the precision
Biocenosis (Biocoenosis) of sampling and monitoring programs, and
application of biological control procedures.
An association of interacting, living creatures in More complex bioclimatic assessment models
an area. The environment or habitat is usually have been designed to predict the potential
uniform, and the community self-sufficient. This establishment and distribution of insect species,
term is most popular in Europe; elsewhere it is often to assess the risk of invasion into areas
referred to as an ecological community. where they are not normally found.
Biocenology

Temperature Models
Biocides
Of all the climate variables that directly affect
Chemicals that kill a wide range of living organisms. insects, temperature has the greatest influence.
Insecticides The influence of temperature on insect develop-
Acaricides ment rate, growth and fecundity has been quan-
tified for many species. The relationship often
observed in laboratory conditions between
Bioclimatic Models in Entomology insect development rate and temperature (see
development rate figure, Fig.35) is well used by
susan p. worner applied entomologists to predict timing and
National Centre for Advanced Bio-Protection phenology of insect life cycle events. The rela-
Technologies, Lincoln University, Canterbury, tionship is usually nonlinear throughout the
New Zealand range of temperatures in which a species can
survive; however, a number of mathematical
Because climate has such a profound effect on functions, both linear and non-linear, have been
the distribution and abundance of invertebrates, used to describe it. Such functions comprise
quantification of climatic influences on insects simple models for prediction of timing or pheno
has been of considerable interest to entomolo- logy of life cycles, or can form the basis of more
gists for well over a century. While simple pre- complex bioclimatic models.
dictive models were developed early on, easier There are three basic approaches to modeling
access to computers in the 1970s resulted in the insect development in relation to temperature.
development of computer based models to pre- The oldest and most widely used model is a sim-
dict the biotic potential of insects in relation to ple linear description of insect development in
climate. Simple bioclimatic models are often relation to temperature (see development rate
used to predict population events so that control figure). The linear model forms the basis to the
methods can be more precisely applied, reducing well known thermal summation or degree day
costs to the grower as well as insecticide use. (DD) approach to timing prediction. Degree days
 Bioclimatic Models in Entomology
B 477

0.06 of the fly larvae or pupae, and by applying the

particular relationship between temperature and
0.05
development for the fly species, the forensic
Development rate

0.04 entomologist can often determine the time of death

of the unfortunate person. Of course, when investi-
0.03
gating a suspicious death, things are not usually
0.02 that easy and many factors that influence the
temperature experienced by the flies need to be
0.01
taken into account. For example, whether the body
0.00 is found inside a building, a vehicle, shallow grave
10 20 30 40 or other enclosed space, or whether it is found out-
Mean temperature (degrees celsius)
doors exposed to the elements is of importance.
Bioclimatic Models in Entomology, Figure35 Even the heat generated by the maggots could
Generalized nonlinear (solid line) and linear influence the rate of development of the flies.
development rate curves. Notice that the linear model is confined to the
more linear portion of the development rate curve
(see development rate figure). Intrinsic to the use
are also called thermal units, heat units, or grow- of the linear model is the assumption that devel-
ing degree days. Degree days are simply the num- opment is proportional to temperature. This means
ber of degrees above a threshold temperature that the reciprocal of the slope (1/slope) of a
required for growth. If temperatures are held con- regression line fitted to the developmental data
stant in the laboratory, for example at 20C, and if obtained at constant temperatures gives the DD
the lower threshold, T0, for growth or develop- required for development. The linear regression
ment of the insect life stage of interest, is 5C, then equation can also be used to calculate the lower
degree days per day or the amount of influential threshold (T0) for development which is defined
heat to which the insect is exposed is 205C=15 as a/b, where a, is the intercept and b is the slope
DD. Degree days per day are accumulated over of the regression line. The thermal optimum
the time it takes the particular life stage to com- (if required) is often estimated by visual inspec-
plete development. For example, if that life stage tion of the development rate curve.
takes 10 days to complete development, that time The linear or degree day model is easy to
is converted to physiological time by 15 DD10 develop and use. While the linear model is clearly
days=150 DD required for development. To pre- wrong in the sense that the lower and upper
dict events in the field, some meaningful point or curvilinear portions of the development rate curve
biofix from which to start degree day accumula- are ignored, this may not matter when field
tion and some method to calculate degree days temperatures lie within the developmental extremes,
from the daily diurnal temperature curve are but inaccurate predictions will result when temper-
required. There is a large amount of literature on atures stray too often beyond these points.
application of this method in applied entomology The second approach to predicting insect
and plant growth studies. phenology in relation to temperature encom-
Of special interest is how the relationship passes the many non-linear mathematical
between insect development and temperature is descriptions or functions used to describe non-
used in forensic entomology. As gruesome as it linear development of insects. These functions
might be, species of blowflies are often the first can range from a simple sine-curve fitted to the
to find a dead body, on, or near which, they lay nonlinear data to more complex biophysical
their eggs. By judging the age of the life stages models or equations. Non-linear models require
478
B Bioclimatic Models in Entomology

rate summation for timing prediction. Rate sum- that is available and that may dictate the level of accu-
mation can be described as: racy that is achievable. In many cases when great
accuracy is not necessary (or achievable) the simple
D = r(T(t))dt degree day approach may be all that is required.
Obviously, other climate variables have poten-
where development D is a function of temperature tial to influence insect population processes, and
T which in turn is a function of time t, r is the therefore the distribution and abundance of insect
development rate and dt is the time increment. For species in any locality. Models that incorporate
good precision the time increment should be other climate variables to predict insect distribu-
hourly. While these models provide a more accu- tion and abundance range from simple graphical
rate description of the developmental relationship approaches called climatographs or climographs to
they are more difficult to develop and complicated more complex models that are process orientated.
to apply in practice. The graphs use a combination of climatic factors to
predict areas that are suitable for establishment of
a particular species and allow quick comparisons
Distributional Models between sites. The simplest climatograph is a plot
of the profiles of mean monthly temperatures and
The third approach to life stage development in rainfall totals for a locality. A much more useful cli-
relation to temperature is represented by distribution mate diagram or climatograph, however, can be a
models of insect phenology that include tempera- plot of mean monthly temperatures against mean
ture dependant development as well as variation in monthly rainfall totals or humidity such that the
development rates within the population at any points for the 12 months of the year are joined to
particular temperature. Such models require consid- create a polygon. At a glance one can see different
erable research investment but can give important shaped climate diagrams may or may not overlap
information about the uncertainty of prediction and indicating times of the year where different regions
good estimates of limits to development in regions may or may not have similar climatic conditions
where the species is not normally found. In general, (see climatograph figure, Fig.36).
however, complexity does not ensure more accuracy,
and a comparative approach is often required. Addi-
tionally, there are also differences in the performance Multivariate Models
of phenological models under variable temperature
conditions that need to be taken into account. Other bioclimatic approaches include the use of
The biological realism or practicality of each multivariate statistical models to predict insect dis-
approach to phenological prediction has been widely tribution and abundance in relation to climatic
debated. Unfortunately, that debate is not helped by variables. Multivariate approaches such as principal
the fact that the appropriateness of a model is often components analysis (PCA) and discriminant
judged on how well it fits the observed data rather analysis can overcome the limited dimensions that
than on rigorous validation using independent data. constrain graphical models. Alternatively, multi
Rigorous validation requires that a model is vali- variate methods can help reduce large amounts of
dated against an adequate sample of the real world. environmental data to a few important variables,
One or two sites or seasons are clearly not enough. and are often used to pre-process data to reduce the
Currently, no model provides an accurate number of input variables to improve subsequent
description of development in all circumstances, analysis by other statistical methods or models.
especially under fluctuating conditions. Clearly, we Because the relationship between insects and
are limited by the accuracy of the temperature data their environment can be complex there have
 Bioclimatic Models in Entomology
B 479

15
Iceland ( )
Macquarie Is.()
10

Campbell Is.()
0

10 Deception Is.( )

15
Casey station( )

20
0 20 40 60 80 100 120 140 160
Rainfall (mm)

Bioclimatic Models in Entomology, Figure36 Climatographs for sites in the Antarctic region compared
with Iceland. Graphs were compiled to determine how likely insect species that have invaded and
established in some areas of the Arctic could survive the climatic conditions in representative sites of the
Antarctic and sub-Antarctic regions.

been many other attempts to characterize their and rainfall for several thousand sites throughout
response to a range of abiotic and biotic factors. the world.
Such models are called bioclimatic envelope At the second level of complexity the CLIMEX
models and are a type of species distribution program is designed to predict the potential
model wherein the current geographical distri distribution of the species by calibrating its
bution of the species is related to local climatic biological responses to the climate of its current
variables to enable prediction of survival or estab- distribution. The species responses are modeled
lishment in new areas or climates. The most well by a series of stress indices that include cold, hot,
known and well used model that combines insect dry and wet parameters that define particular
species response to a number of climate variables environmental limits to the sustained growth and
into meaningful, manageable indices, is called development of the population. These indices are
CLIMEX. CLIMEX is a computer based system then combined in an Ecoclimatic index that
that provides two levels of analysis. First is a describes the overall favorability of geographic
simple match function that can be used to find locations for that particular organism. There are
climates elsewhere in the world that are analogous many examples of bioclimatic assessments of
to, or match, within a specified level of similarity, insect species using CLIMEX particularly for
the area of interest. Given further information on quarantine or risk assessment purposes. Despite
insect biological parameters, CLIMEX can give being relatively easy to use, CLIMEX, like many
estimates in the form of simple indices of the models, should not be used as a black box, it
favorability of particular geographic region for requires a level of expertise or training to opti-
insect population growth and development. mize its use and to ensure correct interpretation
CLIMEX includes detailed long term weather of results.
data, comprising maximum and minimum There are now many examples of biocli-
temperatures, evaporation or relative humidity matic models that have been applied to a range
480
B Bioclimatic Models in Entomology

of taxa. Some of the most well known are weights of the network connections over many
STASH, BIOCLIM, CLIMATE, HABITAT, GARP hundreds or thousands of iterations to minimize,
and DOMAIN. In fact, the number of computer- by least squares, the difference between the
based models, statistical approaches and machine observed values and its own output values. The
learning techniques applied to bioclimatic predic- unique algorithm and structure means an ANN
tion continue to increase, apparently driven by can learn to fit extremely complex functions and
research interest in the distributional changes of therefore is very useful for predicting species
species in response to climate change. presence or absence based on a number of cli-
mate variables. Another advantage of machine
learning approaches is that correct procedure
Computational Intelligence involves training (fitting) but also testing and
validation of the models. This procedure assesses
More recently, applied computational intelligence how well the model can generalize to new data
models such as artificial neural networks (ANN) and as a result, over-fitting, the scourge of more
and other machine learning techniques have been conventional approaches, is avoided.Of all the
successful for bioclimatic assessment of insects as modeling and statistical methods described
well as other species. Such models have the advan- above, none can answer all the questions con-
tage that they can model complex nonlinear data cerning insect species biotic processes in rela-
and they are not constrained by the distributional tion to climate. The seemingly broad range of
characteristics of data as more conventional approaches can complicate the choice of model.
parametric statistical models may be. In some Interestingly, when different models are com-
comparative studies, ANN have been shown to be pared over many re-organizations of the data
better than other methods for modeling species used to create them (Fig.37), some models can
distribution in response to climate. The most com- perform better than others on a particular data
mon ANN used for prediction is the multi-layer set, but can perform worse than the others when
perceptron or MLP. using a different data set. That means it is impor-
ANN were first designed to mimic the ver- tant to compare the efficacy of new methods
tebrate brain and consist of a network of pro- with more standard approaches. While the bio-
cessing elements called neurons in usually three climatic models described here cannot replace
layers; the input layer, the hidden layer and the more detailed modeling of individual species
output layer. All neurons of each layer are con-
Processing of
nected to all the neurons of the adjacent layer. As the information
in the animal nervous system, each processing
element in the network receives input from many Dendrite
others in the network. Each of the inputs or Soma
Axon
independent variables (U) is multiplied by its
associated weight or coefficient and this dictates Inputs from Synapse
the strength or size of each input. The modified outside or
other neurons Outputs to the
u1 w1
inputs are summed and the result is further u2
exterior or
other neurons
w2 N
modified by what is called a transfer function, a=( ujwj)- x=f(a) x
uj wj
which is usually a sigmoid function, but can be j=1

Gaussian or even a simple linear function. The uN wN

result is either fed forward to other neurons in

the network or becomes the networks output. Bioclimatic Models in Entomology, Figure37
The complex network algorithm adjusts the Comparison of a biological and artificial neuron.
 Biogeography
B 481

responses to climate, they can provide important rganized into two sub-disciplines, historical
o
information to guide and inform decisions when biogeography and ecological biogeography,
more detailed data are lacking. Additionally, although there is overlap between the two. His-
many approaches, if correctly applied, have torical biogeography is big picture biogeogra-
potential for knowledge discovery that will phy. It is concerned with explaining patterns in
increase our scientific understanding of how a the distributions of organisms (usually at higher
range of abiotic variables can influence the dis- taxonomic levels) using the geological history of
tribution and a bundance of insects. the Earth. Historical biogeography often involves
large, even global, areas, and frequently deals
with extinct taxa. Ecological biogeography, on
References
the other hand, examines interactions among
organisms and their environment to explain spa-
Worner SP (1998) Some problems and approaches to
modelling insect phenology. In: Baumgrtner J, tial distribution patterns, usually at species and
Brandmayr P, Manly BFJ (eds) Important aspects in sub-specific levels. The spatial and temporal
p opulation ecology. Proc 20th Int Congr Entomol, scales are generally smaller in scope than is the
Florence, Italy, August 2531, 1997, A. A. Balkema,
The Netherlands, pp 8998
case with historical biogeography. As the above
Heikkinen RK, Luoto M, Arajo MB, Virkkala R, Thuiller W, definitions suggest, biogeography is a highly
Sykes MT (2006) Methods and uncertainties in biocli- interdisciplinary science, drawing on evolution-
matic envelope modelling under climate change. Prog ary biology and systematics, ecology, and the
Phys Geog 30:127
earth sciences. Biogeography is a young disci-
pline, first beginning to coalesce into a distinct
science in the mid-1900s. The first scientific peri-
Biocontrol odical devoted to the discipline, the Journal of
Biogeography, first appeared in 1973. The num-
An abbreviation for biological control. ber of books and journal articles devoted to some
aspect of biogeography has increased dramati-
cally in the last few decades. But while it only
recently emerged as a distinct science, biogeogra-
Biogeographic Realms phy as a field of endeavor has been practiced for
centuries, and many of the greatest scientists of
Dissimilar distributions of animals (and therefore
their time were biogeographers, though they may
best called zoogeographic realms). The animals
not have referred to t hemselves as such.
are usually isolated geographically and defined by
Questions about the diversity of life and its
continents, but sometimes separated by mountain
distribution across the world have been asked
ranges or other physiographic features.
since the time of the ancient Greek philosophers,
Zoogeographic Realms
and probably before. But the flowering of
eighteenth century exploration greatly expanded
knowledge of biological diversity and led to a
Biogeography corresponding increase in attempts to explain
the patterns seen in this diversity. At that time,
kenneth w. mccravy explanations were hindered by the prevailing lit-
Western Illinois University, Macomb, IL, USA eral acceptance of the Bible, and Carolus Lin-
naeus (17071778) himself wrestled with the
Biogeography is the study of spatial patterns contradictions between present-day patterns of
of biological diversity. Biogeography is often global biodiversity and biblical literalism.
482
B Biogeography

For instance, Linnaeus hypothesized a paradi- selection developed by Charles Darwin (18091882)
siacal mountain to explain the spread of species and Alfred Russel Wallace (18231913) was criti-
from Noahs point of landing. This mountain cal in providing an explanation for the adaptation
would have all the d ifferent environments of the and diversification of organisms across time and
Earth at different latitudes, which were colonized space. Wallace would devote his life to the study of
by the different animals as they left the Ark. biogeography, and would become known as the
These animals would then be well-suited to colo- father of zoogeography. He wrote three seminal
nize their respective habitats as they migrated books, and developed detailed maps of the Earths
throughout the world. While these ideas may biogeographic regions. He was also the first to note
seem naive in hindsight, Linnaeus logic was the sharp division between Southeast Asian and
astute, and his efforts in recording the type of Australasian faunas in the East Indies, a division
environment in which each species was found that is now known as Wallaces line. Many of the
can be considered a precursor of the sub- principles proposed by Wallace are still active
discipline of ecological biogeography. areas of current research among todays biogeo
The French naturalist Georges Buffon graphers. It is difficult to overestimate the contri-
(17071788) was among the earliest to seriously butions of Alfred Russel Wallace to the science of
consider that the earths climate, species, and even biogeography. British zoologist Philip Lutley
the position of the continents were not fixed, but Sclater (18291913) was also an important figure
mutable. He observed that environmentally similar in early efforts to define the Earths biogeographic
but separated regions have distinct faunas, an realms. Earlier attempts to define biogeographic
insight that became known as Buffons Law. regions were based to a great extent on artificial
Attempts to explain Buffons Law would occupy boundaries, and Sclater felt that these maps were
the attention of naturalists for decades, and would too arbitrary. His goal was to develop a system
require an acceptance of the dynamic nature of reflecting the most natural primary ontological
the Earth and its species. The German botanists divisions of the Earths surface, based on biotic
Johann Reinhold Forster (17291798), Karl similarity and dissimilarity. Being an ornithologist,
Willdenow (17651812), and Alexander von he based his system on passerine birds. His system
Humboldt (17691859) collected innumerable of biogeographic regions, with some revisions, is
plant specimens from around the globe, and found still in use today (Fig.38).
that Buffons Law applied to plants as well as Despite the efforts of these and other early
animals. Von Humboldt is generally recognized as biogeographers, explanations of the disjunct
the father of phytogeography. The Swiss botanist distributions of many plant and animal groups,
Augustin de Candolle (17781841) recognized particularly in the southern hemisphere, remained
distinct phytogeographic regions, and was the first elusive. This was due in large part to the fact that
to coin the word endemic. biogeographers were preoccupied with mecha-
New discoveries in geology and paleontology nisms by which the organisms themselves might
would provide a framework for further advances have dispersed across the continents. But the idea
in biogeography. The eminent geologist Charles that continents might move, or drift, relative to
Lyell (17971875) and others used the fossil record one another over geological time was even more
as evidence of the mutability of the Earths climate difficult for the scientific community to accept.
and sea levels, and asserted the antiquity of the This was despite the fact that much geological,
Earth. The biblically based time frame of a paleontological, and biogeographical evidence
few-thousand-years-old Earth was difficult to supported a dynamic Earth with moving conti-
reconcile with observed biogeographic patterns. nents. For instance, the disjunct southern distri-
The revolutionary theory of evolution by natural butions of groups such as the temperate ground
 Biogeography
B 483

beetle tribe Migadopini were difficult to explain ispersalist models, which were considered less
d
using dispersal models or short-lived land bridges, testable than the vicariance models.
but fit well with a Gondwanaland scenario. Famed evolutionary biologist Ernst Mayrs
Based on evidence from a variety of fields, the (19042005) studies of geographic distributions
German meteorologist Alfred Wegener (18801930) and speciation were instrumental in fostering a
developed the theory of continental drift in the synthesis between evolutionary biology and
early 1900s. However, his ideas were largely biogeography, as was the work of German
rejected by scientists initially. There were a variety entomologist Willi Hennig (19131976). Hennig
of reasons for this, the most important being the developed the methods of phylogenetic system-
lack of a known mechanism by which continents atics, or cladistics, which provided a rigorous
could move. But the overwhelming evidence for framework for testing hypotheses of evolution-
seafloor spreading and plate tectonics amassed by ary relatedness. Cladistics adheres strictly to
the 1960s vindicated Wegener by providing just classifications reflecting natural phylogeny, based
such a mechanism. on the sequence of branching as reflected by
During the last half-century, the study of shared derived character states. This approach
historical biogeography has been bolstered by fits well with vicariance-based biogeographical
increased methodological rigor in biogeographical methods. Development of molecular-based
analysis. Botanist Leon Croizat (18941982) approaches and their application to biogeograph-
developed the method of panbiogeography ical problems has also led to significant advances.
largely in response to what he believed was an The 1980s saw the development of the field of
over-reliance on difficult-to-test dispersal models phylogeography, which has revolutionized bio-
of geographic distributions. Croizat connected the geographical analysis. This approach seeks to
known distributions of taxa with lines, or tracks explain recently occurring evolutionary relation-
and then combined corresponding tracks into ships and geographical patterns at the level of
generalized tracks. Croizat asserted that it would species and species complexes, using molecular
be unlikely that several taxa, with different disper- approaches to produce gene trees that reflect
sal capabilities and ecological requirements, would the spread of lineages.
exhibit the same dispersal patterns. He reasoned Probably the most influential work in ecologi-
that these distributions were established before cal biogeography in the last half-century was
being interrupted by geographic barriers such as Robert H. MacArthur (19301972) and Edward O.
oceans. These explanations required hypothetical Wilsons theory of island biogeography, unveiled in
land bridges and drifting of islands, which most the 1960s. Interestingly (and sadly), an earlier form
biogeographers considered unrealistic. Further- of this seminal theory was independently devel-
more, Croizat never really accepted Wegeners oped by lepidopterist Eugene G. Munroe in the
theory of plate tectonics, even though it would 1940s but, for a variety of reasons, Munroes work
have provided reasonable explanations for many in this area has remained virtually unnoticed. The
of the patterns Croizat observed. Although theory of island biogeography questioned the
Croizats panbiogeography never gained a wide long-held view that species diversity and distribu-
following among biogeographers, he was a pioneer tions on islands necessarily changed slowly, over
in emphasizing the importance of geographic evolutionary time. MacArthur and Wilson asserted
isolation, or vicariance, in speciation. General that the number of species found on islands was a
acceptance of the theory of plate tectonics by the result of more proximal factors rates of immigra-
biogeographical community gave a further boost tion and extinction, which in turn are affected
to the importance of vicariant events in explaining by island size and distance from the mainland.
geographic distributions, at the expense of These ideas provided a much needed theoretical
484
B Biogeography

f ramework for the study of biota not only on oce- Insect Biogeography
anic islands, but on isolated terrestrial habitat
islands as well. The theory of island biogeography Many important contributions to our biogeo-
has also had a profound effect on the field of con- graphical knowledge base have been made by
servation biology. David Quammens excellent entomologists. Many of these contributions
book, Song of the Dodo: Island Biogeography in revolve around applications in pest insect control,
an Age of Extinctions, provides insight into the such as studies of the migration patterns of the
development of the theory and its implications African migratory locust and range expansions of
for conservation biology, as well as criticisms of the gypsy moth, Africanized killer bees, and fire
the theory. For some fascinating ideas in the area ants in the United States. In addition, many
of human biogeography and the geographical pat- dramatic range contractions and extinctions,
terns of wealth and power, see Jared Diamonds involving a variety of plant and animal groups,
Guns, Germs, and Steel: The Fates of Human have been caused by introduced insect vectors of
Societies and Collapse: How Societies Choose to plant and animal diseases, or introductions of the
Fail or Succeed. causative agents themselves. The introduction of

2
1

4
10

7 8
11

12
0 2000 mi

0 2000 km
9

Biogeography, Figure38 Global biogeographic kingdoms and regions based on modern biogeographic
analyses. This is more detailed than the original Sclater-Wallace portrayals and is not yet widely used.
Numerical designations: 12, Holarctic kingdom (=Laurasia); 1, Nearctic region; 2, Palearctic region; 36,
Holotropical kingdom (=eastern Gondwana); 3, Neotropical region; 4, Afrotropical region; 5, Oriental
region; 6, Australotropical region; 712, Austral kingdom (=western Gondwana); 7, Andean region; 8,
Cape or Afrotemperate region; 9, Antarctic region; 10, Neoguinean region; 11, Australotemperate region;
12, Neozelandic region (after Morrone 2002, J Biogegr 29:149152).
 Biogeography
B 485

mosquito-borne avian malaria in Hawaii has not appear to correlate with obvious human impacts
devastated many species of lower-elevation birds such as habitat alteration. However, surveys of this
there. The American elm, once a prominent part of species have shown that local extinctions have taken
North American landscapes, has been virtually place primarily at low-altitude and low-latitude
extirpated by Dutch elm disease. The introduced locations, as would be expected if increased
smaller European elm bark beetle is a primary temperatures were an important cause.
vector of the Dutch elm fungus. As mentioned earlier, some of the most
Other studies have a strong insect conserva- important theoretical advances in biogeography
tion slant, such as analyses of the range collapse of have involved entomologists and the study of
the American burying beetle. This insect was insects. Willi Hennig, the founder of phylogenetic
distributed over most of the eastern United States systematics or cladistics, was a dipterist who pro-
until the mid-1900s, but is now restricted to a few duced many important works in the area of fly sys-
widely separated locations in Nebraska and South tematics. Hennig was drafted into the German army
Dakota, Oklahoma and Arkansas, and the northeast during World War II, and did some of his system-
(Fig.39). Evidence for impacts of global climate atics work while held as a prisoner of war. Another
change on biotic distributions has been provided entomologist, Lars Brundin (19071993), studied
through analyses of insect distributions, such as southern hemisphere chironomid midges. He was
that of Ediths checkerspot butterfly, a species that a pioneer in the use of cladistics in biogeographical
ranges along the coast of western North America analysis. Brundin produced a cladogram reflecting
from Canada to Mexico. Declines of this species do the evolutionary relationships of his chironomid

Biogeography, Figure39 Range decline of the American burying beetle, Nicrophorus americanus
(Coleoptera: Silphidae). The original range is indicated by dark shading, the existing range by the small
unshaded areas designated by arrows.
486
B Biogeography

species. He then inserted the name of the continent the most isolated island had the fewest species,
on which each species is found. This resulted in a and the lowest recolonization rate. However, other
taxon-area cladogram. The sequence of diver- studies have not supported the theory, and the
gence of the chironomid species corresponded well theory has been criticized for a variety of reasons,
with the sequence of the separation of Gondwana such as lack of consideration for the biology of the
into the southern continents (Africa was the first organisms and their ecological and evolutionary
continent to break away, and the African species interactions. For instance, it has been suggested
were the first to diverge, etc.). Thus, systematic and that very small organisms, such as many insects,
biogeographical evidence reinforced each other. would be unlikely to reach saturation population
Among other things, this work showed that geological levels on any but the smallest of islands. So, for
information could be used to suggest which of several most islands within the size range that humans
plausible cladograms is likely correct. consider important, the theory may only apply to
Ecological biogeography has also benefited organisms of larger size, such as vertebrates.
greatly from entomological research. Ecologist As is the case in other sciences, biogeogra-
Robert MacArthur and entomologist Edward phers are constantly searching for patterns in
O. Wilson developed the groundbreaking theory nature. Many have been discovered, and, often,
of island biogeography. The major tenets of the insects play important roles in providing data in
theory, in highly simplified form, are: (i) an island support of, or as exceptions to, these patterns. It
will contain an equilibrium number of species, has been observed in many groups of plants and
(ii) this equilibrium number is a function of the animals that species diversity increases as one
balance of two processes, immigration and extinc- progresses from the higher latitudes to the tropical
tion, and (iii) immigration and extinction rates are regions. Several theoretical explanations for this
in turn a function of the size of the island, and pattern have been proposed. Many insect groups
the distance of the island from the mainland. fit this pattern. However, some do not. These
MacArthur and Wilson reasoned that small islands exceptions include two huge families of parasitic
will have higher extinction rates than large islands, wasps, the Ichneumonidae and Braconidae, as well
because populations of species on smaller as the sawflies and aphids. There are many possible
islands will be smaller and thus more likely to reasons for these exceptions. It has been suggested
become extinct. Likewise, islands far from the that aphids are more diverse in temperate regions
mainland will have lower immigration rates than because many aphid species are specialist feeders
islands near the mainland. Therefore, small, far that have difficulty locating suitable host plants
islands will have low equilibrium numbers of species, from long distances. Therefore, they should fare
and large, near islands will have larger equilibrium better in regions where plant species are clumped,
numbers of species. such as the agricultural lands of temperate regions,
Wilson, with his student Daniel Simberloff, than in tropical regions where plant assemblages
also provided an early rigorous test of the theory consist of many species that are each present at
through experimental defaunation studies on low densities. As is often the case, it is the excep-
small mangrove islands in the Florida Keys. In this tions to the rule that provide the most interesting
study, methyl bromide was used to kill all insects research questions.
and other terrestrial arthropods on the islands. Another interesting biogeographical pattern
Follow-up surveys were then done to monitor has been termed geographic parthenogenesis.
recolonization of the islands. Several aspects of Parthenogenesis is the production of offspring
the theory were supported. After defaunation, the from unfertilized eggs, usually with the asexu-
islands did eventually return to roughly their orig- allyproducedoffspring being female. Geographic
inal numbers of arthropod species. In addition, parthenogenesis refers to a pattern in which
 Biological Clock
B 487

arthenogenetic organisms occupy different geo-

p Lomolino MV, Riddle BR, Brown JH (2006) Biogeography,
3rd edn. Sinauer Associates, Sunderland, MA, 845 pp
graphic ranges than their closely related, sexually
Lomolino MV, Sax DF, Brown JH (eds) (2004) Foundations
reproducing relatives. The parthenogens are often of biogeography: classic papers with commentaries.
associated with what could be considered marginal University of Chicago Press, Chicago, IL, 1291 pp
habitats. These include more northerly latitudes, Quammen D (1996) The song of the dodo: island biogeo
graphy in an age of extinctions. Scribner, New York,
higher altitudes, disturbed habitats, islands or island- 702 pp
like patches of habitat, or dry environments. Such
patterns have been observed in many insect groups.
One interesting example is Pelecinus polyturator, a
parasitic wasp with a huge latitudinal geographic Bioinformatics
range that extends from eastern and central North
America, through the southwestern U.S. and Central Researchers in bioinformatics develop computer
America, down through South America to Argen- software applications that can store, compare and
tina. Pelecinus polyturator exhibits patterns consis- analyze the very large quantities of DNA sequence
tent with geographic parthenogenesis. In the data generated by the new genome technologies.
northern part of its range males are extremely rare, New bioinformatics tools can sift through a mass
but in tropical regions males are abundant and of raw data, finding and extracting relevant infor-
sexual reproduction is apparently common. Insect mation and their relationships.
species in other groups, including mayflies, aphids, Genomics
and stick insects, have also been found to exhibit Functional Genomics
geographic parthenogenesis. Structural Genomics
For centuries now, biogeographers have
provided fascinating insights into the patterns and
processes of the natural world. As human-caused Biointensive Pest Management
changes continue to affect global biodiversity, it
will be critical that we increase our knowledge of Biologically based pest management. Pest man-
the factors determining the geographic distri agement that depends on an understanding of pest
butions of organisms. The science of biogeography biology to prevent pests from causing damage, or
will continue to be at the forefront of these efforts. uses biological agents to suppress pests.
Zoogeographic Realms Integrated Pest Management
Pelecinid Wasps

Biological Amplification
References
The accumulation and increase in concentration
Avise JC (2000) Phylogeography: The history and formation
of species. Harvard University Press, Cambridge, MA,
of chemicals, usually insecticides or their metabo-
447 pp lites, in organisms at higher trophic levels.
Cox CB, Moore PD (2005) Biogeography: an ecological and Biomagnification
evolutionary approach, 7th edn. Blackwell, Malden, MA,
428 pp
Diamond JM (2005) Collapse: how societies choose to fail or
succeed. Viking, New York, 575 pp Biological Clock
Diamond JM (1997) Guns, germs, and steel: the fates of
human societies. W. W. Norton, New York, 512 pp
The biological/physiological timing device inside
Lomolino MV, Heaney LR (2004) Frontiers of biogeography:
new directions in the geography of nature. Sinauer an organism that allows it to establish regular
Associates, Sunderland, MA, 436 pp biological rhythms. It is self-sustained, but
488
B Biological Clock of the German Cockroach, Blattella Germanica (L.)

s ynchronized by natural biological patterns such self-sustained, endogenous clock is easily entrained
as light and dark cycles. (synchronized) by environmental signals such as
Biological Clock of the German Cockroach light-dark cycles, temperature cycles, and other
environmental changes, and allows an organism to
adapt to its environment properly in time. Such an
Biological Clock of the German environmental time signal has been called a Zeit-
Cockroach, Blattella Germanica geber (from the German for time-giver).
(L.) There are several lengths of rhythmic period
on earth, such as half-day tidal cycles, day-night
how-jing lee cycles, semilunar and lunar cycles, annual cycles,
National Taiwan University, Taipei, Taiwan and seasonal cycles that are caused by the move-
ments of sun, earth and moon. Since these predict-
Have you had a terrifying experience of seeing an able environmental changes are consistent events,
oily flat creature running for cover when you open organisms depend on their endogenous clocks to
a cupboard to look for a midnight snack? Even synchronize with the rhythmic changes of environ-
worse, while you are watching TV a cockroach ment. Among various lengthened environmental
runs swiftly under your feet to reach the other end cycles, the daily cycle is the most prominent and
of sofa! This tiny crawler is no stranger to us. It is universal environmental condition to influence the
our unwanted and unavoidable housemate, the survival of organisms. From primitive prokaryotic
German cockroach. single-cell cyanobateria to highly evolved eukary-
The German cockroach, Blattella germanica otic mammals, virtually all organisms possess an
(L.) is a cosmopolitan species and well-adapted to endogenous circadian clock (the term circadian is
human shelters such as houses, buildings, and fac- derived from the Latin for about a day). Therefore,
tories, and sometimes it is even found on public many scientists focus their research interests on
transportation. They feed on almost any organic circadian clocks.
matter. Although no life threatening disease is
transmitted by them, the existence of the German
cockroach poses a health threat to humans (allergy, Characters of Circadian Clocks
diarrhea) and represents deteriorating hygiene.
Since we live with the German cockroach The most important characteristics of a circadian
under the same roof, our daily life coincides with clock are: (i) a self-sustained oscillator with a
its activities. We rarely see them during daytime, period close to 24 h, (ii) a free-running rhythm
but we encounter them frequently at night. Do under constant environmental conditions (such as
they avoid their only natural enemy, humans, constant temperature and continuous light or dark
during the day, or is their activity schedule condition), and (iii) temperature-compensation.
controlled by a biological clock? The scientific evi- The first two characters are the essential ones that
dence shows that timing of its activity is scheduled should be used as the definition of the circadian
according to its endogenous biological clock. clock. When we remove all the environmental time
signals from an organism, it should follow its own
endogenous circadian clock and express an approx-
What Is a Biological Clock? imate, but not exact 24 h rhythm. Only when this
free-running rhythm is expressed under an artifi-
A biological clock is a timing device inside an cial, constant condition, can we definitely infer a
organism to give time signals so that an organism circadian clock in this organism. The third charac-
can perform proper behaviors at the right time. This ter is the key feature to allow the clock to run as
 Biological Clock of the German Cockroach, Blattella Germanica (L.)
B 489

accurately as possible in different seasons or and TIMELESS proteins in the cytoplasm of cells.
temperature conditions. Since the speed of all The phosphorylation of PERIOD enables it to bind
biochemical processes within an organism depends with TIMELESS to form a heterodimer, which in
on the temperature, the property of temperature turn translocates into the nucleus to inhibit
compensation can keep the molecular biological further transcription of period and timeless genes.
clock running in a constant pace regardless of When the diminishing concentration of PER-TIM
environmental temperature fluctuation. This heterodimer reaches a certain low level, the period
character is especially essential in ectothermal and timeless genes will be reactivated and cause
animals, those which depend on external conditions another cycle. This process takes about 24 h lag
to maintain their body temperature (Fig.40). time. Light can degrade the TIMELESS protein. If
there is reduced TIMELESS available to bind
PERIOD, then there is more delay of inhibition
Molecular Clock Mechanisms on the two clock genes, which prolongs the cycle
and changes the clock phase. This molecular
The biological clock operates in a negative feed mechanism explains the synchronization of cir-
back loop composed of various molecules. cadian clock phases with the light-dark cycles of
Although no universal scheme of molecular clock the environment(Fig.41).
exists in all organisms, the molecular clock mecha-
nisms in the fruitfly Drosophila melanogaster
underlie the clockwork of the German cockroach. Ecological Significance
The simplified molecular clock scheme includes
two clock genes, period and timeless, which are The ecological function of biological clocks is
activated and transcribed-translated to PERIOD the main reason these clocks occur in various

0 6 12 18 24

Age
(days)

10

15

Biological Clock of the German Cockroach, Blattella Germanica (L.), Figure40 The locomotor activities
of a male adult German cockroach at 28C, 12L:12D cycles for 5 days then switched to c onstant darkness
conditions. Each horizontal line shows 24 h, with each day attached below the p revious day. A vertical
line indicates the onset of locomotion. The shaded areas of the actogram represent darkness. The
superimposed line across the actogram represents the predicted onset time of the locomotion according
to its circadian period (DD=23.5 h) (modified from Lin and Lee, 1996).
490
B Biological Clock of the German Cockroach, Blattella Germanica (L.)

0 6 12 18 24

Age Age
(d.) (d.)

5 5

10 10

15 15

20 20

3.0 0.0 0 80
Length of oocytes (mm) Successful mating (%)

Biological Clock of the German Cockroach, Blattella Germanica (L.), Figure41 The locomotor activities
of a virgin female adult German cockroach at 28C, 12L:12D cycles for 5 days then switched to constant
darkness conditions. Daily development of ovaries represented by the length of oocytes is shown on
the left side of the actogram. The mating window for a virgin female is displayed on the right side of the
actogram. Other symbols as above (modified from Lee and Wu, 1994; Lin and Lee, 1996).

rganisms across five kingdoms. We can identify

o Natural selection has shaped the proper
the three most important ecological functions of a behaviors of organisms to act in the right place at
circadian clock: (i) the timing of each behavior is so the right time. Good timing is certainly involved
important that every organism within a species in life and death decision-making processes. An
should time each movement very accurately. This is endogenous circadian clock is definitely a key asset
the key function an endogenous circadian clock can to survive and prosper for the species.
provide. (ii) Although most environmental changes
are fairly rhythmic and predictable, some condi-
tions (such as continual raining, sudden cold or Biological Clock of the German
heat) might cause long lasting interruption on envi- Cockroach
ronmental rhythmicity. These unpredictable envi-
ronmental changes may last a few days and cause With some background information about
organisms to perform behaviors solely depending biological clocks, we can turn our attention to the
on their circadian clock for good timing. (iii) Every circadian clock of the German cockroach. Since it
day is a new challenge for an organism. The active would be difficult to actually see the working clock
tasks ahead require good preparation in physiologi- in a multi-cellular animal, a circadian rhythmic
cal conditions to overcome challenges. In order to behavior or physiological parameter can be
be well-prepared for the challenge, organisms selected and monitored as the overt expression of
depend on their circadian clock to trigger the whole the endogenous clock. The locomotor circadian
cascade of reactions. The physiological preparation rhythm is chosen as the focal point of this article.
in organisms occurs in the rest phase of the daily The German cockroach is a nocturnal insect,
cycles. A circadian clock can provide good timing and its locomotor activities mainly occur during
to start preparation and achieve survival in danger- the scotophase (dark phase) of the daily photope-
ridden environments. riod condition. Once the light-dark cycles are
 Biological Clock of the German Cockroach, Blattella Germanica (L.)
B 491

a rtificially changed to constant darkness condition, and that the locomotor pattern of female adults
a male adults free-running rhythm continues to does not display a circadian rhythmicity.
regulate locomotion for greater activity during the Since possessing a circadian clock is a genetic
time that would represent scotophase in light-dark trait for the species, female adults should also have
cycles. The circadian period of the male adult is a circadian clock underlying their arrhythmic
approximately 23.5 h. From this activity pattern, locomotion. When the ovaries are surgically
we know there is an endogenous clock driving its removed during the last instar, they express a loco-
locomotion in circadian rhythmicity. motor circadian rhythm of 23.6 h, the same as
When female adults are put into the same con- found in male adults (Fig.42). This circadian
dition, their locomotion does not show a circadian rhythmicity also can be seen in starving female
rhythm. Their locomotion is concentrated to the adults whose ovaries do not develop. The locomo-
few days before the formation of ootheca (egg tor circadian rhythm of females is masked by the
case), and activity is distributed relatively evenly endogenous development of ovaries. This masking
across the 24 h period. This locomotor pattern effect is a unique characteristic of the biological
coincides with the developmental cycles of ovaries. clock in the German cockroach.
When the ovaries reach at certain developmental A critical function of the circadian clock in
stage, female adults become active. Their locomo- reproductive behavior is to provide good timing
tion even occurs during the day, clearly counter to for bringing potential mates together. However,
the nocturnal nature of the species. In addition, why does the timing of mate-finding behavior not
this locomotor pattern coincides with the narrow synchronize between the sexes of the German
mating-window of the females. When the females cockroach? This question certainly implies that
become sexually receptive, their daily locomotion the masked circadian rhythm of female adults
increases significantly. Once the females mate, their does not impair the chances of meeting males. It
locomotion decreases immediately. We conclude requires a detailed analysis of the reproductive
that locomotion represents mate-finding activities strategies of the German cockroach to unveil the

0 6 12 18 24

Age
(days)

10

15

20

Biological Clock of the German Cockroach, B lattella Germanica (L.), Figure42 The locomotor activities
of an ovariectomized female adult German cockroach at 28C, 12L:12D cycles for 5 days then switched to
constant darkness conditions. The circadian period is calculated as 23.6 h. Other symbols as above
(modified from Lin and Lee, 1996).
492
B Biological Clock of the German Cockroach, Blattella Germanica (L.)

mystery of endogenous masking effects on the sexually mature females release sex pheromone to
locomotor circadian rhythm. attract males. Combining these two mechanisms,
Although German cockroaches are not social the female adults try to mate in time.
insects, they do live in groups. The groups are These complicated reproductive strategies
composed of immature and adult cockroaches of guarantee the survival and propagation of the
both sexes, and are maintained by an aggregation species. In fact, the high priority of reproduction
pheromone secreted by every individual. This style causes a unique masking effect on the mate-finding
of living provides easy opportunity for both sexes locomotion of the female. This arrhythmic loco-
to meet when they are sexually mature. Thus, the motion is the result of high demand on mate-finding
timing of mate-finding locomotion becomes less locomotion during the sexually receptive period
critical in comparison with solitary cockroach of female adults. Underneath this arrhythmic
species. The masked locomotor circadian rhythm locomotion, however, an endogenous circadian
does not handicap the chances of mating pair- clock paces daily locomotion.
formation. Random (Fig.43) mate-finding is
largely dependant upon group living and is the
primary strategy of the species. Conclusion
Since female adults produce an ootheca
regardless of their mating status, the nutrient-rich The biological clock of the German cockroach runs
oothecae is wasted when the females do not mate continuously in both sexes. It drives locomotion
during the narrow mating-window. The penalty to express circadian rhythm in male adults, but
for losing the mating opportunity is severe enough adult females fail to show circadian rhythmicity.
to drive female adults into locomotion to find An endogenous masking factor caused by the
mates regardless the time of the day. The masked developing ovaries obscures the overt rhythm of
locomotor circadian rhythm, therefore, reflects locomotion in females. Although this desynchro-
the high importance of mate-finding. In addition, nizing locomotion does not fit into the mode of

mating

male

mating
Increasing
male loc motion male

Calling behavior
(releasing sex pheromone)
female female

Primary strategy Secondary strategy

mating

Biological Clock of the German Cockroach, Blattella Germanica (L.), Figure43 Mating scheme for the
German cockroach (modified from Tsai and Lee, 1997).
 Biological Control by Neoseiulus Californicus (McGregor) (Acari: Phytoseiidae)
B 493

function for a circadian clock, the masked arrhythmic Biological Control by Neoseiulus
locomotion becomes part of reproductive strategy californicus (McGregor) (Acari:
that ensures a mating opportunity for sexually Phytoseiidae)
mature females.
norma e. snchez, nancy, m. greco, claudia
v. cdola
References Universidad Nacional de La Plata, La Plata
Argentina
Enright JT (1970) Ecological aspects of endogenous rhyth-
micity. Ann Rev Ecol Syst 1:221238 Neoseiulus californicus is a predator mite that pro-
Lee HJ (1994) Are pregnant females of the German cockroach
too heavy to run? Zool Stud 33:200204
vides an effective biological control of Tetranychus
Lee HJ, Wu YL (1994) Mating effects on the feeding and loco- spp. spider mites in strawberries, corn, grapes, roses,
motion of the German cockroach, Blattella germanica. fruit trees and ornamentals. It has a worldwide
Physiol Entomol 19:3945 distribution in arid and humid areas, including
Lin TM, Lee HJ (1996) The expression of locomotor circadian
rhythm in female German cockroach, Blattella german- semi-tropical and temperate South America, and arid
ica (L.). Chronobiol Int 13:8191 areas of southern California and southern Europe.
Lin TM, Lee HJ (1998) The parallel control mechanisms This predator is very small in size. The adult
underlying locomotor activity and sexual receptivity
measures 0.250.5 mm in length and is pear
of female German cockroach Blattella germanica (L).
JInsect Physiol 44:10391051 shaped and slightly orange in color. It passes
Scully AL, Kay SA (2000) Time flies for Drosophila. Cell through four developmental stages (egg, larvae,
100:297300 nymph and adult). Eggs are oval and translucent.
Tsai CW, Lee HJ (1997) Volatile pheromone detection and
calling behavior exhibition: secondary mate-finding
At 25C, the eggs hatch after two days. Larval and
strategy of the German cockroach, Blattella germanica nymphal (proto- and deutonymph) stages require
(L.). Zool Stud 36:325332 about three days to complete development. Then,
Tsai CW, Lee HJ (2000) Circadian locomotor rhythm masked it takes approximately five days to reach the adult
by the female reproduction cycle in cockroaches. Phys-
iol Entomol 25:6373 stage. Adult longevity is approximately 20 days,
Tsai CW, Lee HJ (2001) Analysis of specific adaptation to a and the oviposition period is 13.5 days. A female
domicile habitat: a comparative study of two closely can lay three eggs a day (Fig.44).
related cockroach species. J Med Entomol 38:245252
Neoseiulus californicus, as well as other predatory
Wen HW, Lee HJ (2000) Unequal coupling between locomo-
tor pacemakers of the German cockroach, Blattella mites (e.g., N. fallacis (Garman), Phytoseiulus persimilis
germanica (L.). J Insect Physiol 46:8997 Athias-Henriot and Mesoseiulus longipes (Evans)) is
commercially produced and used to control the
two-spotted spider mite, T. urticae Koch, in North
American and European greenhouse horticulture.
Biological Control A related species in the same genus, N. fallacis,
coexists with N. californicus in the Northern
The action of parasites, predators, or pathogens in Hemisphere. Both species are morphologically
maintaining another organisms population den- similar and have been rated as specialized predators
sity at a lower average level than would occur in of spider mites, but N. californicus seems to be
their absence. Biological control may occur natu- more generalist than N. fallacis. Pollen of different
rally in the field or result from manipulation or plants such as maize, almond, castor bean,
introduction of biological control agents. avocado, and some grasses, as well as thrips are
Augmentative Biological Control alternative food.
Classical Biological Control In South America, releases of predatory mites
Conservation Biological Control are not commonly used, and regular applications
494
B Biological Control by Neoseiulus Californicus (McGregor) (Acari: Phytoseiidae)

This predator seems to be a promising natural

enemy for controlling T. urticae through the imple-
mentation of conservation techniques. Taking into
account that the ability to tolerate acaricides is a
serious constraint on successful conservation of
phytoseiid predators, the reduction of unnecessary
acaricide treatments may enhance persistence of
predator mite populations.
At present, efforts are being made to reduce
the number of chemical applications through
monitoring of the prey/predator ratio and pest
population trend to avoid both unnecessary
pesticide applications and economic damage.
However, more field studies are needed to help
elucidate other factors that contribute to increase,
and to effectively preserve the natural populations
of this predator in annual as well as perennial
systems. Among these factors, plant diversity may
be a critical feature to increase natural enemy
persistence through: (i) provision of alternative
prey/host at times when the pest is scarce, (ii) pro-
Biological Control by Neoseiulus Californicus vision of supplementary food, and (iii) provision
(McGregor) (Acari: Phytoseiidae), Figure44 of refuge (for mating or overwintering).
Neoseiulus californicus (McGregor). It is also known that physical and chemical
characteristics of the food plants of prey can affect
of acaricides are made to control pest mites. How- natural enemy potential effectiveness. A good
ever, in commercial strawberry greenhouses in example of this is the negative way in which per-
Argentina, N. californicus is the main established sistence of N. californicus, plant colonization, and
enemy of the two-spotted spider mite. Although consumption of T. urticae are affected by tomato
this predator consumes fewer prey than other leaf glandular hairs. This finding reveals the risk of
phytoseiid species, it has longer survival under generalizing the effectiveness of N. californicus
starvation conditions. Moreover, the ability to feed from one crop to another.
on other food sources may contribute to its The implementation of conservation biological
persistence in the absence of spider mites. This control is still receiving inadequate consideration
trait may be of critical importance for the success in developing countries. The potential and utility
of conservation biological control. of N. californicus as a biological control agent is
Conservation biological control means the worth further investigation.
environmental manipulation to protect and enhance
natural enemies. This is an ecologically, environ-
mentally, and economically sound solution to pest
problems for growers of developing countries.
References
Recent studies in La Plata (Buenos Aires,
Greco NM, Liljesthrm GG, Snchez NE (1999) Spatial
Argentina) showed that T. urticae and N. californicus distribution and coincidence of Neoseiulus californicus
populations exhibit a high spatial coincidence and and Tetranychus urticae (Acari: Phytoseiidae, Tetrany-
the predator is very efficient in locating the prey. chidae) on strawberry. Exp Appl Acarol 23:567580
 Biological Control of Invasive Plants in Latin America
B 495

Ma W, Laing JE (1973) Biology, potential for increase and A frequently cited example of a successful
prey consumption of Amblyseiulus chilenensis (Dosse)
biological control project is the control of prickly
(Acarina: Phytoseiidae). Entomophaga 18:4760
McMurtry JA, Croft BA (1997) Life styles of phytoseiidae pear cactus, Opuntia stricta Haworth (Cactaceae)
mites and their roles as biological control agents. Annu in Australia by the pyralid moth Cactoblastis
Rev Entomol 42:291321 cactorum Bergroth (Lepidoptera: Pyralidae) intro-
Monetti LM, Croft BA (1997) Neoseiulus californicus
(McGregor) and Neoseiulus fallacis (Garman): larval
duced from Argentina in the 1920s. However, this
responses to prey and humidity, nymphal feeding drive is also a good example of conflicting interests, as
and nymphal predation on phytoseiid eggs. ExpAppl the invasive plant (cactus) is harmful in Australia
Acarol 21:225234 and biological control was needed. On the other
hand, it is useful as human and animal food, and
as an ornamental plant for people in other regions
Biological Control of Invasive (Mexico, Caribbean, southern regions of the USA).
Plants in Latin America Here, the successful biological control agent in
Australia, C. cactorum, threatens the native
julio medal1, maricela martnez 2 endemic cactus, so it is not regarded as a hero but
1
University of Florida, Gainesville, FL, USA as a pest, and control measures including the use
2
Instituto Mexicano de Tecnologa del Agua of natural enemies and the sterile insect technique
(IMTA), Jiutepec, Morelos, Mexico are being undertaken.
Other well-known examples of classical bio-
An invasive plant is an exotic that has been logical weed control include the effective control
introduced, intentionally or by accident, into a new of Klamath weed and alligator weed. Klamath
region where it successfully establishes, reproduces, weed or St. Johnswort, Hypericum perforatum L.
and spreads, eventually replacing the native vegeta- (Clusiaceae) was controlled in the western USA by
tion. Invasive plants or weeds, also called biological two European leaf-feeding beetles, Chrysolina
pollutants, threaten natural ecosystems and human- quadrigemina (Suffrian) and Chrysolina hyperaci
modified habitats by reducing biological diversity (Forster) (Coleoptera: Chrysomelidae), imported
and by causing significant reductions in crop yields from Australia in the mid 1940s. In Florida, USA,
and other harmful effects on property, humans, and complete biological control of alligator weed,
domesticated animals. The success of the exotic Alternanthera philoxeroides (Martius) Grisebach
plant to become invasive in a new geographical (Amaranthaceae) in aquatic environments was
region can be partially attributed to the fact that the achieved by the introduction of the flea beetle
exotic has been introduced without the arthropod Agasicles hygrophila Selman and Vogt (Coleoptera:
natural enemies and disease-producing pathogens Chrysomelidae) from Argentina.
that limit its reproduction in the area of origin. Interest in biological control of invasive plants
Manual removal and herbicides are the major using host-specific insects and pathogens has
invasive plant management practices currently increased in the last decade due to the publics
used in cultivated crops in Latin America. Biological concern about the negative effects of pesticides in
control, or the use of natural enemies such as the environment, a greater demand for pesticide-
arthropods, pathogens, and fish to reduce the free agricultural products, the reduction in the
population and reproduction of the exotic inva- number of pesticide registrations, the development
sive, has been traditionally practiced in developed of plant resistance to commonly used herbicides,
countries such as the United States, Australia, and the intensified oil crisis which increases the
Canada, South Africa, and New Zealand, primar- cost of using herbicides. A recent catalogue of
ily in rangeland situations, conservations areas, biological control agents and their weeds listed 949
and aquatic systems. releases involving at least 350 organisms against
496
B Biological Control of Invasive Plants in Latin America

133 target weeds as of 1996. Forty-one (31%) of Biological Control Activities

these weeds are considered under complete or Against Invasive Plants in Latin
substantial biological control. America
Biological control is not a panacea and is
not without an element of risk. The advantages The use of insects and pathogens as biological
of classical biological control over other invasive control agents of invasive plants in South America
plant control methods are that it is highly spe- has been quite limited. Compared with the
cific to the target plant, it has little or no impact advances achieved in biological control of arthro-
on non-target organisms, it does not pollute the pod pests for the same region, the use of insects
environment, it is relatively inexpensive, and it for control of invasive plants is in its infancy or
provides self-sustaining and permanent control initial stages of development. Chile can be consid-
of the invasive plant when it works. Among the ered a pioneer in this field, with biological control
disadvantages of biological control of invasive activities of invasive plants initiated in 1952 against
plants with introduced insects are that it is the non-native invasive Hypericum perforatum L.
unpredictable, and even if the insects establish, (Clusiaceae). This project has been a great success,
biological control may not suppress the invasive providing highly effective control of this weed.
plant population enough to achieve the desired Other biological control projects initiated in Chile
level of control. in the 1970s that had only moderate successes or
Several factors make biological control with have been ineffective include Galega oficinalis L.,
insects especially difficult in field crops. First, Ulex europaeus L. (Rosaceae), Rubus constictus
disturbance from planting, cultivation, and Lepeure & Mueller, and Rubus uifolius (Rosaceae).
pesticide applications is not conducive to the Research efforts using insects or pathogens for
establishment of the biological control agent. Sec- biological control of invasive plants in Chile
ond, because several species of invasive plants continue, with more intensity in the last decade
usually require control simultaneously, multiple due to enhanced funding provided by national
biological control agents are needed. Finally, rapid institutions. In Argentina, there is only one case
control (usually within one month of planting) is known of biological control, that of the invasive
necessary in order to prevent crop damage. Once aquatic plant waterhyacinth, Eichhornia crassipes
invasive plant-feeding insects establish, they are (Mart.) Solms (Pontederiaceae) in the province
unlikely to build up damaging populations in a of La Rioja located in the west-central part of
single field season. Highly specific plant patho- the country. The waterhyacinth-feeding weevil
gens may be better suited to control invasive Neochetina bruchi Hustache (Coleoptera: Curcu-
plants in field crop situations. Native plant lionidae) was introduced from the province of
pathogens can be formulated and applied as Buenos Aires and it was able to reduce the aquatic
bioherbicides, or exotic pathogens can provide plant infestation from 50% to 8%.
effective control of the invasive plants following Biological control of aquatic invasive plants
inoculative releases. Lastly is the conflicting in Mexico has been implemented with more inten-
interest issue mentioned previously. A plant sity during the last decade using a combination of
that is perceived as a nuisance by one group of insects and pathogens against waterhyacinth. Most
people can be considered a beneficial plant by of the current aquatic plants have been introduced
another group. Beekeepers are a good example by humans from their native habitats, and are free
of a special interest group that may object from their natural enemies and diseases. Invasive-
strongly to biological control because they may ness is a response to the high level of nutrients in
value the invasive plant as a source of nectar the urban, industrial and municipal wastewater.
and pollen. Aquatic invasive plants causes water loss through
 Biological Control of Invasive Plants in Latin America
B 497

plant evapotranspiration, displacement of native (Orthoptera: Acrididae), and Orthogalumna

species, public health risks, obstruction of channels t erebrantis (Wallwork) (Acari: Galumnidae).
and drains in irrigation systems, intakes to hydro- There is no evidence of them being native to
electric plants, restriction to tourist, recreational Mexico, and they could have arrived with
and fishing activities, and increasing sedimenta- waterhyacinth plants introduced in the past. The
tion with subsequent shortening of the useful life Brazilian weevil N. bruchi was introduced into
of the body of water. In Mexico, more than 62,000 Mexican quarantine from the USDA Aquatic
ha have been infested by aquatic invasive plants. Plant Management Laboratory in Fort Lauder-
The most important species are waterhyacinth, dale, Florida, USA. Although the Neochetina
followed by water fern (Salvinia spp.), pondweed species are well established in Mexico, the effec-
(Potamogeton sp.), cattail (Typha sp.), hydrilla tiveness of biological control requires the use of
(Hydrilla verticillata L. Royle), waterlettuce (Pistia additional agents to complement existing ones.
stratiotes L.), and duckweed (Lemma spp.). Several highly virulent waterhyacinth patho-
In 1993, the Aquatic Weed Control Program gens have been collected, identified, screened for
was initiated in Mexico by presidential mandate in plant host range, mass-produced, and field evaluated
response to the increasing need to control the in Mexico. After selecting two specific and highly
overwhelming presence of invasive plants in the virulent fungal pathogens, Cercospora piaropi
water sources. As part of this program, a biological Tharp., and Acremonium zonatum (Saw) W. Games,
control project was included. In Mexico, waterhya- the combined effects of the plant pathogens and
cinth is the most prolific invasive aquatic plant, the Neochetina weevils were evaluated in a seven
infesting an estimated 40,000 ha of water. This ha water reservoir in the central part of Mexico
plant was probably introduced in Mexico in the in the state of Morelos. A total of 9,800 weevils
early 1900s. Chemical and mechanical control were released and two applications of a mixture
methods have been used to manage waterhya- of the fungal pathogens were carried out. After
cinth, but these methods are expensive and several three months of the combined application of the
annual applications are needed. The difficulties in fungi and weevils, the reservoir was free of wate-
controlling this aquatic invasive are related to the rhyacinth. The dramatic reduction in waterhya-
plants rapid growth rate and its ability to reinfest cinth coverage was due to the increasing amount
via the seed bank or by flood-borne plants. For of a natural pathogen (C. piaropi) already present
these reasons, the only long-term and sustainable in the water reservoir, the introduction at the
solution is the application of an integrated same time of another highly virulent pathogen
approach to waterhyacinth management in which (A. zonatum) combined with the leaf feeding scars
biological agents play a key role. made by the Neochetina adult weevils and stem
The host-specific Brazilian weevils Neochet- damage by the Neochetina larvae. Weevil feeding
ina eichhorniae Warner and Neochetina bruchi allows the transmission of the pathogens, which
Hustache have been used in many countries results in increased disease incidence. This approach
worldwide to control waterhyacinth with relative of combining insects and pathogens to get a better
success. Neochetina eichhorniae was introduced control of an invasive aquatic plant is currently
to Mexico from the US in the late 1970s. How- implemented by the Instituto Mexicano de
ever, other reports indicated its presence in some Tecnologa del Agua in different regions of Mexico.
Mexican water bodies as early as 1967. Another In Honduras, a limited number of biological
three waterhyacinth insects that have been control activities against waterhyacinth were
observed occurring naturally in Mexican water initiated in the 1990s. The Neochetina weevils
bodies are Sameodes albigutalis (Warren) (Lepi- were introduced and released in a body of water
dopera: Pyralidae), Cornops aquaticum (Bruner) at the Pan-American Agricultural University
498
B Biological Control of Invasive Plants in Latin America

El Zamorano located 20 miles east of Tegucigalpa. world, mainly Australia, Canada, the continental
Control of waterhyacinth has been a complete United States and Hawaii, New Zealand, India, and
success in this body of water through the combined several African counties, principally South Africa.
effect of the Neochetina and manual removal of the The three countries from which most of the
fewer and smaller plants damaged by the feeding of biological control agents have been exported
the adult/larvae stages of the weevil. are Mexico (42 species or 33.1% of the total
In 2005, some biological control activities exported), Brazil (30 species or 23.6% of the
against aquatic invasive plants were initiated in total), and Argentina (20 species or 15.8% of
Nicaragua. Aquatic systems have been sampled to the total). This trend has continued into this
determine the arthropods fauna associated with century and is supported by local personnel and
waterhyacinth and waterlettuce, which invades institutions (e.g., USDA-ARS Biological Control
several lakes and rivers in Nicaragua, preventing Laboratory in Hurlingham, Argentina) established
fishing, navigation, and running of the hydroelectric by foreign countries that have invasive plants
plants that provide electricity to a large part of the native to South America.
country. A new species of Cornops sp. (Orthoptera:
Acrididae) was found feeding heavily on waterhy-
acinth, and host-specificity range studies are being Limitations on the Implementation
undertaken. of Biological Control of Invasive
The first biological control activity in Brazil Plants in Latin America
against a non-native invasive plant, Tecoma stans
(Bignoniaceae) was initiated in 2000. This medi- Among the main limitations to carrying out
um-size tree is originally from the southern USA, biological control projects against invasive plants
Mexico and Central America, and it is invasive in in South America is the limited number of
uplands and pasture areas in southern Brazil (the technical personnel with training in this disci-
states of Paran and Rio Grande do Sul) where it pline. Some efforts of training in this field were
replaces native vegetation. The rust fungus Prospo- initiated by the University of Florida in cooperation
dium appendiculatum (G. Winter) Arthur was with the Universidad Nacional Agraria of Nicara-
found attacking this plant in southern Brazil, and gua, the Instituto de Investigaciones Agropecuarias
no other potential specific agents has been found of Temuco, Chile, and the USDA-ARS South Ameri-
in field explorations conducted in recent years. can Biological Control Laboratory of Hurlingham,
Initial foreign exploration in the area of origin Argentina. Three intensive weed biological control
(Nicaragua, Costa Rica) of T. stans was conducted courses were given in Nicaragua during June 2002,
for several days in June 2006 and several potential 2004, and 2006 with 78, 51, and 46 participants,
natural enemies were collected on the plant. Addi- respectively. This kind of training is necessary to
tional field explorations are planned once funds prepare the personnel required for the implemen-
become available. tation of biological control programs in the
region.
Another important factor that limits the imple-
Exportation of Latin American mentation of invasive plant biological control
Biological Control Agents projects is the limited availability quarantine facilities
that exist in the region. However, most of the South
Contrary to the limited importation of biological American countries already have quarantine
control agents into Central and South American facilities for the introduction of parasites/predators
countries, as of the late 1900s, 127 insect species had for biological control of arthropod pests. These
been exported and used in other regions of the installations could be modified and adapted for the
 Biological Control of Invasive Plants in Latin America
B 499

introduction of biological control agents of invasive Bidens pilosa L. (Compositae; common name
plants. Countries that have quarantines to handle mozote); Coniza bonariensis (L.) Cronq., (Aster-
natural enemies of invasive plants include Brazil, aceae; common name varilla, distribution tropical
Argentina, and Chile. America); Cyperus rotundus L. (Cyperaceae; known
A third and very important limiting factor is as coyolillo in Central America, coquito in
the lack of funds. Economic resources for any Colombia); Desmodium tortosum (Swarts) Dc.,
type of agricultural research are scarce and (Fabaceae; known in Central America as pega-
competition for grants is highly competitive. The pega);Echinocloa colona (L.) Link (Poaceae; known
funding required to initiate a new project for as arroz de monte or arrocillo, plant originally
biological control of invasive plants is relatively from Eurasia and very common in South American
high. Nevertheless, the ecological and/or rice fields); Eichhornia crassipes (Pontederiaceae; com-
economic benefits that will be obtained if agents mon name jacinto de agua, lirio de agua, or lirio
become established and successful are quite acutico); Eragrostis plana Nees (Poaceae; common
substantial. name in Brazil capim annoni); Pistia stratiotes
(Araceae; known as lechuga de agua in Central
America and alfaa de agua in Brazil); Portulaca
Potential for Biological Control of oleraceae L. (Portulacaceae; known as verdolaga in
Invasive Plants in Latin America Central America), Richardia scabra L. (Rubiaceae;
common name botoncillo); Ricinus communis L.
The successes with biological control of invasive (Euphorbiaceae; highly toxic plant known in South
plants in conservation areas, agricultural situations, America as castor or higuerilla); Rottboellia
and aquatic systems obtained in other countries cochinchinensis (Lour) Chyton (Poaceae; known in
could be duplicated in Central and South America. Central America and in the Caribbean as la camina-
The diversity and complexity of the agricultural dora); Sida acuta Burn. f. (Malvaceae; known as
practices by South American farmers suggest that escobilla negra); Solanum torvum Swarts (Solanaceae,
management of invasive plants should be biologi- a spiny bush common in South America known as
cally based (biological control using native or lava platos or huevo de gato, a name also applied
introduced insects and/or pathogens) and inte- to various species of Solanum); Sorghum halepense
grated with conventional control methods. For (L.) Pers. (Poaceae; known as grama Johnson);
example, cultural practices (plant density, non- Taraxacum officinale Weber (Asteraceae; originally
tillage, intercropping, crop rotation, organic agri- from Europe and known in South America as
culture) that contribute to preservation of natural lechuguilla); Tecoma stans (L.) Kunth ex HBK.
enemies of the invasive plants should be encour- (Bignoniaceae, known as guabillo in Central
aged. Invasive plant pathogens can be integrated America, it is invasive in southern Brazil); and Ulex
with the more disruptive chemical and mechanical europaeus L. (Fabaceae; known in South America by
methods most commonly used for high-cash the common name tojo). These invasive plants
crops, or in situations where the availability of cause significant economic or ecological damage
manual labor is limited. in Central and South America and justify the
The twenty most important invasive plants in research and implementation costs of biological
Central and South America are shown in the control. In some cases, the costs for implementing
accompanying table: Amaranthus spinosus L. biological control programs in Central and South
(Amaranthaceae; common name spiny amaranth America can be reduced by making use of the
in the USA, bledo in Central America); Ambrosia existing technology that has been successful in
artemisiifolia L. (Asteraceae; common name other regions of the world, thus, biological control
Amargosa, distribution North and South America); with insects and/or pathogens could provide
500
B Biological Control of Invasive Plants in Latin America

Biological Control of Invasive Plants in Latin America, Table 3 The twenty most important invasive plants
in Central and South America
Scientific name Common name Family Origin
Amaranthus spinosus Bledo Amaranthaceae Tropical America
Ambrosia artemisiifolia Amargosa Asteraceae America
Bidens pilosa Mozote Compositae America
Conyza bonariensis Varilla Asteraceae Tropical America
Cyperus rotundus Coyolillo Cyperaceae India
Desmodium tortuosum Pega-pega Fabaceae Tropical America
Echinocloa colona Arroz de monte Poaceae Eurasia
Eichhornia crassipes Lirio acutico Pontederiaceae South America
Eragrostis plana Capim annoni Poaceae South Africa
Pistia stratiotes Lechuga de agua Araceae South America
Portulaca oleraceae Verdolaga Portulacaceae India
Richardia scabra Botoncillo Rubiaceae South America
Ricinus communis Higuerilla Euphorbiaceae Tropical Africa
Rottboellia cochinchinensis La caminadora Poaceae India
Sida acuta Escobilla negra Malvaceae Tropical America
Solanum torvum Lava platos Solanaceae Africa
Sorghum halepense Grama Johnson Poaceae Mediterranian
Taraxacum officinale Lechuguilla Asteraceae Europe
Tecoma stans Guabillo Bignoniaceae Mexico
Ulex europaeus Tojo Fabaceae Europe

e ffective, safe, and low-cost solutions to many of In: Charudattan R, Labrada R, Center TD, Nelly-Begazo
Central and South Americas most important C (eds) Strategies for water hyacinth control. A report of
a panel of experts meeting, Fort Lauderdale, Florida.
invasive plant problems. Table 3. Food and Agricultural Organization of the United
Biological Control of Weeds Nations, FAO, Rome, pp 125135
Classical Biological Control Holm LG, Plucknnett DL, Pancho JV, Herberger JP (1997)
The worlds worst weeds. University Press of Hawaii,
Invasive Species Honolulu
Julien MH, Griffiths MW (1998) Biological control of
weeds. A world catalogue of agents and their target
Reference weeds, 4th edn. CAB International, Queensland, Aus-
tralia, 223 pp
Charudattan R (1996) Pathogens for biological control of Martnez M, Charudattan R (1998) Survey and evaluation of
waterhyacinth. In: Charudattan R, Labrada R, Center TD, Mexican native fungi for potential biocontrol of water-
Kelly-Begazo C (eds) Strategies for water hyacinth hyacinth. J Aquat Plant Manage 36:145148
control. A report of a panel of experts meeting, Fort Martnez M, Gutirrez E, Huerto R, Ruz E (2001) Importa-
Lauderdale, Florida. Food and Agricultural Organization tion, rearing, release and establishment of Neochetina
of the United Nations, FAO, Rome, pp 9097 bruchi (Coleoptera: Curculionidae) for the biological
Gutirrez LE, Arregun CF, Huerto DR, Saldaa FP (1994) control of waterhyacinth in Mexico. J Aquat Plant
Control de Malezas Acuticas en Mxico. Ingeniera Manage 39:140143
Hidrulica en Mxico 9:1534 Martnez M, Gmez M (2007) Integrated control of Eichhor-
Gutirrez LE, Huerto R, Martnez M (1996) Waterhyacinth nia crassipes by using insects and plant pathogens in
problems in Mexico and practiced methods for control. Mexico. Crop Protection (in press)
 Biological Control of Weeds
B 501

Medal J (2004) Perspectives on biological control of invasive coevolved natural enemies to provide permanent
plants in Latin-America. In: Cullen JM et al (eds) Proc XI
control of the weed. Thus, classical biological control
Int Symp Biol ContWeed. Canberra, Australia, pp 425427
Medal J (2007) El control biolgico de malezas en Latinoa- can be defined as the planned introduction and
mrica: situacin actual y Perspectivas futuras. Vedalia release of undomesticated target-specific organ-
(in press) isms (usually arthropods, nematodes or plant
Norambuena H, Ormeo J (1991) Control biolgico de
malezas: fundamentos y perspectivas en Chile. Agricul-
pathogens) from the weeds native range to reduce
tura Tcnica (Chile) 51:210219 the vigor, reproductive capacity, or density of the
Norambuena H, Escobar S, Rodriguez F (2000) The bio target weed in its adventive range. The term
control of gorsse, Ulex europaeus in Chile: a progress adventive in this definition acknowledges the
report. In: Spencer NR (ed) Proc X Int Symp Biol
Cont Weed. Montana State University, Bozeman, MT fact that the arrival of a weed in a new geographical
pp 955961 area can occur by any means (e.g., immigration),
Norambuena H (2004) Exploraciones en el Extranjero, and is preferable to the term introduced, which is
Transporte, y Procedimientos de Cuarentena de los
restricted to actions taken by people. Biological
Agentes de Control Biolgico. In: Medal J, Norambuena
H, Gandolfo D (eds) Memorias del Segundo Curso weed control as it is defined here specifically
Latinoamericano de Control Biolgico de Malezas. excludes natural regulation (the action of organ-
Montelimar, Nicaragua. University of Florida-IFAS, isms without human intervention), cultural control
Gainesville, FL, pp 1621
practices (grazing management, crop rotation,
etc.), and plant competition (the deliberate use of
one plant species to competitively exclude another).
Biological Control of Weeds Although plant competition is not included in the
definition of biological weed control, it is an essential
james p. cuda component of the overall process that can affect
University of Florida, Gainesville, FL, USA the outcome of a biological control project.
Plant predation (or herbivory in the case of
Weeds are universally recognized as significant weed biological control) and plant competition are
pests worldwide because they interfere with entirely different ecological processes. An intro-
food and fiber production, and are considered duced natural enemy (arthropod, nematode, or
the most important threat to biodiversity after pathogen) damages or consumes portions of the
habitat destruction. Weeds cause 90% of weed, which rarely leads to plant death but results
agricultural losses, and herbicides account for in a loss of biomass or nutrients that weaken and
approximately half (47%) of the worlds agro- stress the plant. In plant competition, the weed and
chemical sales. The economic effect of weeds on its competitors are interfering with each other for
the U.S. economy is staggering. Weed-associated use of a common resource (e.g., light, water, nutrients
losses and costs in the mid 1990s were estimated or germination sites). It is the subtle interaction
to be in excess of $20 billion annually, with between these two distinct ecological processes that
non-native or invasive weed species accounting can lead to the permanent decline of a weed
for $13 billion, or 65%. population. An invasive weed is less likely to recover
An invasive weed is a non-native plant that from the effects of selective herbivory from biological
exhibits rapid population growth following its control agents if competition from desirable native
arrival in a new environment where it did not plant species is strong.
evolve. The success of the weed in its new habitat Classical biological control offers several
is due in part to the absence of the natural enemies advantages over other weed control methods: (i) it
that normally limit its reproduction and spread in provides selective, permanent control of the target
its native range. Classical biological control seeks weed; (ii) it is relatively inexpensive to develop
to reunite an invasive weed with one or more of its and implement compared to other methods of
502
B Biological Control of Weeds

weed control; (iii) introduced biological control Recent examples of successful biological
agents are self-replicating and will spread on their c ontrol of adventive weeds with introduced
own throughout the infested area; and (iv) because invertebrate organisms in the last 20 years are
they are living organisms, biological control agents shown above.
are biodegradable.
Some of the strengths of classical biological
control also contribute to its shortcomings: (i) once Procedures in a Classical Weed
biological control agents are established, they c annot Biological Control Project
be recalled if desirable species are attacked; (ii) con-
trol is not immediate and may require 510 years for From the beginning, weed biological control
agents to attain damaging levels; (iii) natural enemies s cientists have continued to develop and refine
for controlling every weed may not exist; and procedures for locating, screening, releasing
(iv) agent establishment and suppression of the and evaluating biological control agents (Sum-
target weed are not guaranteed. mary of steps, Table 5). All countries currently

Biological Control of Weeds, Table 4 Recent successes in classical biological control of weeds with
invertebrate organisms worldwide since 1980
Weed species Country
Aquatic and Wetland Weeds
Alligatorweed, Alternanthera philoxeroides (Martius) China, New Zealand, Thailand
Grisebach
Azolla, Azolla filiculoides (Lamarck) South Africa
Purple Loosestrife, Lythrum salicaria L Canada, USA
Water Fern, Salvinia molesta (D. S. Mitchell) Australia, Fiji, Ghana, India, Kenya, Malaysia,
Namibia, Papua New Guinea (PNG), South Africa,
Sri Lanka, Zambia
Water Hyacinth, Eichhornia crassipes (Martius) Australia, Benin, India, Indonesia, Nigeria, PNG,
Solms-Laubach South Africa, Thailand, Uganda, Zimbabwe
Water Lettuce, Pistia stratiotes L Australia, Botswana, Ghana, PNG, South Africa, Sri
Lanka, Zambia, Zimbabwe
Terrestrial Weeds
Annual Ragweed, Ambrosia artemisiifolia L Russia
Giant Sensitive Plant, Mimosa invisa (Martius) Australia, PNG
Leafy Spurge, Euphorbia esula L USA
Nodding Thistle, Carduus nutans L Canada, USA
Purple Sesban, Sesbania punicea (Cavanille) Bentham South Africa
Spinyhead Sida, Sida acuta (Burman) f Australia
Tansy Ragwort, Senecio jacobaea L USA, Australia

Sources: Julien MH, Griffiths MW (1998) Biological control of weeds. A world catalogue of agents and their target
weeds, 4th edn. CAB International, Queensland, Australia, 223 pp; McFadyen REC (1998) Biological control of weeds.
Annu Rev Entomol 43:369393; Spencer NR (ed) (2000) Proc X Int Symp Biol Cont Weed, Bozeman, Montana, USA,
414 July 1999. United States Department of Agriculture, Agricultural Research Service, Sidney, Montana, and Mon-
tana State University, Bozeman, MT
 Biological Control of Weeds
B 503

conducting weed biological control projects Because these host-specific natural enemies
follow this protocol in one form or another to reproduce only in the presence of their host plants,
ensure that candidate organisms are safe to they are able to regulate weed abundance by
introduce. operating in a self-sustaining, density dependent
manner.
Selecting organisms as candidates for classi-
Importance of Host Specificity cal weed biological control can be a complicated
and lengthy process because scientists must iden-
Host specificity is fundamental to biological weed tify those natural enemies that have developed a
control because it ensures that an introduced agent high degree of specificity with their host plants.
will not become a plant pest. Host specific, Scientists conduct various types of host range tests
coevolved natural enemies are considered good in the field and laboratory (oviposition, adult feed-
candidates as they are incapable of reproducing ing, and larval development) depending on the
on plants other than their weedy hosts, and have biology of the agent. Several screening tests usually
proven to be the safest to introduce because they are required to demonstrate with confidence the
are least likely to damage nontarget species. estimated host range of the agent. Candidate

Biological Control of Weeds, Table 5 Summary of steps involved in a classical weed biological control
project
Step Description
Target selection Review literature about target weed, related plants and known
natural enemies; identify and resolve conflicts of interest;
conduct cost-benefit analyses; seek approval and funding
Overseas and domestic surveys Locate native range of target weed and survey for natural
enemies; assess biocontrol potential of each organism in
country of origin; conduct faunal surveys in adventive range
Host specificity studies Examine host range of organisms in native range; compile list
of test plants and import promising candidates into quarantine
of country of introduction for further testing
Approval of agents Submit screening report to appropriate regulatory agencies to
obtain approval for release; respond to requests for additional
host testing or other concerns
Rearing and release Obtain release permit; mass rear biocontrol agent; identify and
implement most effective release strategy; release biocontrol
agent at various sites to increase likelihood of establishment
Evaluation Conduct field studies to confirm establishment and spread
ofbiocontrol agent on target and nontarget species; use
replicated manipulative experiments to determine effect of
biocontrol agent on target weed populations
Technology transfer Provide training to land managers and extension agents about
using biocontrol agents; collaborate with user groups to
determine best strategies for integrating biocontrol with other
control methods

Sources: Julien M, White G (eds) (1997) Biological control of weeds: theory and practical application, ACIAR Monograph
No. 49. ACIAR, Camberra, Australia; Luken JO, Thieret JW (eds) (1997) Assessment and management of plant invasions
504
B Biological Control of Weeds

organisms that fail the host specificity requirement Biological Control of Weeds, Table 6 Number of
are dropped from further consideration. Accord- weed species targeted and agent species released
ing to established guidelines, no organism can be in the five most active countries through 1990
introduced into a new environment before its host Country Weed species Agent
range is determined. species
United States 54 130
Australia 45 123
Taxa Used in Classical Biological
South Africa 28 61
Control of Weeds
Canada 18 53
Through 1996, there have been at least 1,150 New Zealand 15 15
deliberate releases of invertebrate organisms TOTAL 160 391
against invasive weed species in 75 countries. Five
of the countries shown here the United States, Source: Julien M, White G (eds) (1997) Biological control
Australia, South Africa, Canada and New Zealand ofweeds: theory and practical application, ACIAR
Monograph No. 49. ACIAR, Canberra, Australia
account for most of the activity, based on the
number of weed species targeted and agents
released. Biological Control of Weeds, Table 7 Invertebrate
A large number of families and species are taxa deliberately introduced between countries
represented in these releases, and they are listed by for classical biological control of adventive weeds
the taxonomic groupings shown on p. 307. The Group No. of families No. of species
taxa used in biological control projects worldwide INSECTA
are predominantly insects, but mites, nematodes,
Coleoptera 8 147
and fungi also have played an important role in
Lepidoptera 25 106
controlling adventive weeds in some cases. Overall,
Hemiptera 10 28
25% of all releases made before 1985 contributed
to the control of the target weed. Diptera 6 44
Thysanoptera 2 4
Hymenoptera 3 5
Classical Biological Control of Orthoptera 1 1
Weeds in Aquatic Habitats ACARINA 3 5
FUNGI 4 17
Compared to terrestrial weeds, biological control NEMATODA 2 2
of aquatic weeds with insects has been remarkably
Total 64 359
successful since it was first attempted in the United
States against alligatorweed (Alternanthera philox- Sources: Bellows TS, Fisher TW (eds) 1999 Handbook of
eroides (Martius) Grisebach) in 1964. Complete or biological control. Academic Press, San Diego, CA ;Julien
substantial biological control of several other MH, Griffiths (eds) (1998) Biological control of weeds: a
world catalogue of agents and their target weeds (4th ed)
aquatic weed species has been achieved in most
CABI Publishing, New York, NY
countries where it has been attempted. Although a
higher proportion of failures than successes has correlated with the growth form of the weeds, the
occurred in the field of weed biological control, taxa used as biological control agents, susceptibil-
the overall success rate for the aquatic weeds is ity to disease-causing pathogens, fluid nature of
extraordinary. A close examination of the various the aquatic environment, or some combination of
projects suggests this high success rate may be these factors.
 Biological Control of Weeds
B 505

The aquatic form of alligatorweed, water agents cannot develop damaging populations
yacinth (Eichhornia crassipes (Maritius) Solms-
h quickly enough to be effective against crop weeds
Laubach), water lettuce (Pistia stratiotes L.), salvinia because rapid control is needed to prevent the
(Salvinia molesta D. S. Mitchell), and water fern weed from overwhelming the crop. Finally, most
(Azolla filiculoides Lamarck) have been predictably crop weeds are multi-species assemblages of short-
controlled using classical biological control. An lived annuals that traditionally were not considered
interesting pattern emerges when the weed and amenable to biological control by introduced host-
insect attributes associated with these successes are specific organisms with the exception of fungi.
considered. (i) All of the aforementioned aquatic Several recent examples, however, have shown
weeds are either free-floating, or produce floating that classical biological control is feasible in some
mats in the case of alligatorweed. This plant growth intensively managed agricultural environments
form is susceptible to wave action and currents that where most of the problems are caused by one
are unique to aquatic environments. (ii) Reproduc- or two species of adventive crop weeds. Field
tion in these weeds is primarily by rapid vegetative bindweed (Convolvulus arvensis L.), which is
growth. High genetic uniformity usually associated native to Eastern Europe, is a serious pest of corn,
with vegetative reproduction was thought to be a cotton, sorghum, turf and wheat in much of the
necessary prerequisite for successful biological United States and Canada. An eriophyid mite
control. (iii) These floating weeds are highly suscep- (Aceria malherbae Nuzzaci), imported from Greece
tible to secondary infection. Aquatic plants that have in 1989, has proven to be effective in controlling
sustained damage by insects or disease will rot and field bindweed infestations in some parts of
disintegrate very rapidly. (iv) Beetles (Insecta: Texas and Oklahoma, and can survive repeated
Coleoptera) have been responsible for most of the mowing. The mite attacks the plants by producing
control, especially weevils. Coincidentally, most inver- galls onthe leaves, petioles, and stems that stunt
tebrate organisms released for classical biological new growth, deform the leaves, and limit seed
control of weeds worldwide have been beetles. production.
Puncturevines (Tribulus terrestris L. and
T. cistoides L.) are annual and perennial herba-
Classical Biological Control of ceous plants, respectively, native to the Mediter-
Weeds in Stable and Ephemeral ranean region and Africa. In the 1960s, these two
Habitats adventive weeds were serious pests of croplands
and pastures primarily in arid regions of the
Historically, only perennial weeds of relatively southwestern United States and Hawaii. Punc-
stable environments (e.g., pastures, rangelands, turevines were not only invasive but produced
and aquatic systems) were regarded as appropriate spiny burs, capable of penetrating tires, that were
targets for classical biological control with host injurious to livestock. Two weevils imported
specific introduced natural enemies. Habitat from Italy, a stem borer [Microlarinus lypriformis
stability coupled with minimal disturbance were (Wollaston)]; and a seed feeder [M. lareynii
thought to be necessary prerequisites for success- ( Jacquelin du Val)]; gave complete control of
ful biological control. Conversely, crop weeds were both puncturevines in Hawaii, and provided
deemed inappropriate targets for classical biological substantial control of the annual species in many
control with most of these organisms because of areas of the Southwest.
their vulnerability to conventional cultivation Three ragweeds that are native to North
practices (e.g., soil tillage, mowing) and the same America are adventive species in the former Soviet
pesticides used against crop pests. Also, there was Union where they have become invasive. One of
the belief that invertebrate biological control these ragweeds (Ambrosia artemisiifolia L.) caused
506
B Biological Insecticides

serious problems because it was infesting croplands Florida from Australia for biological control of
and was difficult to control using conventional melaleuca (Melaleuca quinquenervia (Cav.) S. T.
herbicides and cultural methods. A defoliating leaf Blake) are contributing to the successful integrated
beetle [Zygogramma suturalis (Fab.)]; obtained management of this invasive wetland tree weed that
from Canada and the United States, was released in is threatening the ecology of the Florida Everglades
the former Soviet Union in 1978. This leaf beetle Foreign Exploration for Insects That Feed on
built up enormous populations and provided Weeds
complete control of this ragweed under certain con- Host Specificity of Weed-Feeding Insects
ditions. On one farm, yields of alfalfa, sainfoin and Classical Biological Control
corn increased dramatically as the beetles completely
destroyed all the ragweeds in the infested fields.
More recently, the invasion of natural and
References
conservation areas by immigrant plant species or
Bellows TS, Fisher TW (eds) (1999) Handbook of biological
introduced ornamental plants that have escaped control. Academic Press, San Diego, CA
cultivation has generated considerable interest in Julien M, White G (eds) (1997) Biological control of weeds:
classical biological control as a weed management theory and practical application, ACIAR Monograph
tool. Invasive weeds of natural areas have been No. 49. ACIAR, Canberra, Australia
Julien MH, Griffiths (eds) (1998) Biological control of weeds:
called biological pollutants. Unlike other forms a world catalogue of agents and their target weeds
of environmental pollution whose effects are (4th ed). CABI Publishing, New York, NY
reversible once the source of the pollution is Luken JO, Thieret JW (eds) (1997) Assessment and
management of plant invasions. Springer, New York, NY
removed, invasive weeds pollute the environment
McFadyen REC (1998) Biological control of weeds. Annu Rev
after they become established by continuing to Entomol 43:369393
proliferate and spread causing potentially irrevers- Spencer NR (ed) (2000) Proc X Int Symp Biol Cont Weed,
ible ecosystem damage. Incipient populations of Bozeman, Montana, USA, 414 July 1999. United States
Department of Agriculture, Agricultural Research Ser-
adventive weeds often are indistinguishable from vice, Sidney, Montana, and Montana State University,
the native flora, and they usually avoid detection Bozeman, MT
until severe ecological harm already has occurred.
Eventually, these invasive natural area weeds change
the landscape by displacing more desirable native Biological Insecticides
plant species, altering fire regimes, increasing soil
Insecticides made with insect pathogens that are
erosion, contributing to the loss of wildlife habitat,
formulated to be applied like conventional chemi-
causing some plants and animals to become rare or
cal insecticides.
endangered, and diminishing the aesthetic value of
Insecticides
recreational areas. In some cases, invasive natural
Microbial Control of Insects
area weeds even cause human health problems.
Biological control offers an attractive alterna-
tive to conventional chemical and mechanical con- Biology
trol methods that are too costly and damaging to the
environment, especially on large tracts of public The study of life. This is an umbrella term that
lands set aside for nature preserves as well as state includes all aspects of the study of life, including
and national parks. Some recent examples of suc- biochemistry, genetics, and taxonomy. Some
cessful biological control programs against invasive taxonomic texts include a section with heading
weeds of agricultural as well as natural areas are Biology under which the authors assemble infor-
listed on p. 305. Although it has not been confirmed, mation about behavior and natural history, as if
there is every indication that insects introduced into taxonomy were somehow not part of biology.
 Biotechnology
B 507

Bioluminescence as inundative or augmentative biological control

agents.
Light produced by living organisms from a chemi- Microbial Control of Insects
cal reaction, usually involving the protein luciferin
and the enzyme luciferase.
Fireflies Biorational Pesticides
Fireflies: Control of Flashing
Glowworms Pesticides that are considered to be safe to humans
or the environment, and based on microbial agents
or naturally occurring chemicals (e.g., pheromones,
Biomagnification hormones). Because these are based on chemical
products rather than on living organisms, they are
Increase in the concentration of a persistent classified as chemical control rather than biological
chemical along a food chain, with the top-level control.
predators accruing the highest concentration. Pheromones
Biomagnification is of special concern with long- Microbial Control of Insects
lived pesticides, which can be retained in fat tissues Botanical Insecticides
rather than being excreted. Biomagnification is
also known as biological concentration and food
chain concentration.
Biosphere
Biological Amplification
The ecosystem that includes the entire earth.

Biomass

The mass of a living organism of a defined type Biosystematics

and from a defined area. Biomass, often expressed
as dry weight, is used to estimate abundance and The branch of systematics (classification) in which
to ameliorate the differences between a few large the genetic and evolutionary relationships between
individuals and many small ones. taxa are investigated.

Biome Biota

A large ecological unit or ecosystem defined by The species of plants and animals occurring within
vegetation, climate, and geography, though a biome a defined area.
can be found in more than one place. Examples of
biomes are salt marshes and steppe regions.
Biotechnology
Biopesticide The manipulation of organisms to provide desir-
able products. It has broader meanings, as well,
A product that consists of biological organisms, including all parts of an industry that creates,
usually microbial agents or their products, for develops and markets a variety of products through
pest suppression. Biopesticides usually are applied the molecular manipulation of organisms or using
508
B Biotic Disease

knowledge pertaining to the molecular biology of Bipectinate

organisms. In pest management, it is the use of
genetically modified organisms in the production The presence of comb-like structures on opposing
of crops or animals, including in the production of sides, usually used to refer to a form of antennae.
insect-suppressive agents. Antennae of Hexapods

Biotic Disease Bird and Rodent Fleas

Disease caused by a pathogen, such as a bacterium, Members of the family Ceratopsyllidae (order
fungus, or virus. Siphonaptera).
Fleas

Biotic Potential
Bird Cherry-Oat Aphid
The rate at which a species will increase in the
absence of limits. Wheat Pests and Their Management

Biotic Release Bird Lice

The escape of a population from the regulatory Members of the family Philopteridae (order
effects of its natural enemies, resulting in a popu- Phthiraptera).
lation increase or outbreak. Chewing and Sucking Lice

Biotope Bird Malaria

Avian (Bird) Malaria
An area of uniform environmental conditions
occupied by a similar community. This term is
most popular in Europe. It is essentially equivalent
to habitat, but although habitat is often used in Birnaviruses
conjunction with populations, biotope is used to
describe a community. The family Birnaviridae contains three genera, the
Avibirnavirus (infectious bursal disease of chick-
ens), the Aquabirnavirus (infectious pancreatic
Biotype necrosis virus of fish), and the Entomobirnavirus
(Drosophila X virus). Birnaviruses are icosahedral
A race or strain of an organism that differs in viruses and lack a viral membrane. Characterized
some way from the principal population, often as medium-sized viruses (60 nm diameter), they
in susceptibility to a pesticide or in association encapsidate two segments (A, B) of linear dsRNA
with a food plant. In the case of host plant asso- (total size 67 kbp). Unlike other dsRNA viruses
ciations, such biotypes are sometimes called (reoviruses), Birnavirus dsRNAs extracted from
host races. the viral capsid can serve as m-RNA; under in
 Br, Lajos
B 509

vitro conditions, the dsRNA molecules can bind to was then part of Hungary). He was the sixth
ribosomes and undergo translation. Segment A is child of a poor cabinetmaker. His father wanted
polycistronic and codes for three gene products, him to become a woodworker also, but young
whereas segment B is monocistronic and codes for Lajos had a keen interest in natural history.
one gene product. Thanks to his teacher, Ferenc Trk, he became
The Drosophila X virus (DXV), the type quite an expert in insect collecting and various
species of the Entomobirnavirus, was discovered other zoological preparation techniques. From
initially as a contaminant in insect cell lines. an early age he longed for the tropics but com-
Sequence analysis of DXV has revealed that ing from a poor family and living in land-locked
segment A contains two open reading frames Hungary, he could only dream about exotic
(ORFs) consisting of a 3096 bp and 711 bp countries and the exploration of their zoologi-
sequence. The 3096 bp ORF codes for the 114 kDa cal wonders. To satisfy his ambitions in discov-
polyprotein which is processed post-translation- ery and research, he built an extensive insect
ally by virus-encoded protease to generate VP-2, collection of Hungary and adjacent lands. To
VP-3, and VP-4. In most birnaviruses, the second become a university student was out of the
ORF codes for a small, arginine-rich peptide. question because of the familys financial
Segment B encodes for VP-1 putative viron asso- circumstances. The only way for him to obtain
ciate RNA polymerase. DXV is polytropic and can some sort of a tertiary education was to become
replicate in the cytoplasm of both the mesoder- a priest. He attended Protestant Theology but
mal and epidermal cells of D. melanogaster. DXV only for two years, as he couldnt develop a deep
replication results in extensive lysis of Drosophila religious belief and became a teacher. From his
cells within 26 h. Surviving cells maintain DXV in meager earnings he tried to save up for a tropi-
a repressed form (they are persistently infected) cal journey. At the same time his reputation as
and are immune to a second challenge with DXV. an entomologist grew and eventually he gained
Laboratory colonies of D. melanogaster infected government employment as grape phylloxera
with DXV exhibit anoxia sensitivity and do not inspector/consultant at the Entomological Insti-
recover after being anesthetized with CO2 or N2. tute in Budapest. The tragic death of Samuel
Fenichel prompted Br to take important steps
References towards the realization of his childhood dreams:
to grasp the emerging opportunity and embark
Chung HK, Kordyban S, Cameron L, Dobos P (1996) Sequence on a journey to New Guinea. To obtain the nec-
analysis of the bicistronic Drosophila X virus genome essary financial support, he sold his collection
segment A and its encoded polypeptides.Virology
225:359368
of over 20,000 specimens to the Hungarian
Nagy E, Dobos P (1984) Synthesis of Drosophila X virus National Museum and secured an agreement
p roteins in cultured Drosophila cells.Virology with its management for the purchase of the
134:358367 material he was to collect during the expedition.
He left Hungary on the 7th of November 1895
and arrived to Friedrich-Wilhelmshafen (today
Br, Lajos Madang) in Kaiser Wilhelm Land or German
New Guinea (today Papua New Guinea) on the
george hangay 1st of January 1896. During the following
Narrabeen, NSW, Australia 6 years, Br relentlessly worked towards his
goal to explore as much as possible of New
Lajos Br was born on the 29th of August 1856 Guineas insect fauna. He was a very ambitious
in Tasnd, Szilgy Shire, in Transylvania, (which and prolific collector. His activities were not
510
B Bisexual

restricted to insects alone as he also collected Biting Midges, Culicoides spp.

other zoological and ethnographical specimens (Diptera: Ceratopogonidae)
as well. The total number of his New Guinean
zoological collections exceeded 200,000 speci- alison blackwell
mens, while the ethnographical objects num- University of Edinburgh, Midlothian, Scotland,
bered over 6,000. These collections are still not United Kingdom
fully processed yet, although its study by many
researchers, including Br himself, generated Culicoides is the most important of four genera of
over 100 papers, describing 2,000 species new to the family Ceratopogonidae which feed on the
science. After his New Guinean years, Br con- blood of vertebrate animals. Culicoides includes
tinued his work as an entomologist, mainly more than 1,400 named species, and at least 50
focusing on Hymenoptera and Coleoptera. His are thought to be vectors of disease, spreading
greatest strength was evident in the field, where pathogens to man and animals.
his acute sense of observation and excellent col-
lecting methods yielded valuable information
and great numbers of specimens. He has con- Classification and Recognition
ducted fieldwork in many European locations,
including Turkey, Bulgaria, Crete, etc., and he Order: Diptera
was commissioned by the British Royal Geo- Suborder: Nematocera
graphical Society to train young zoologists in Infraorder: Culicomorpha
India and Burma. In recognition of his achieve- Superfamily: Chironomoidea
ments, in 1926 he was awarded an honorary Family: Ceratopogonidae
doctorate by the Ferenc Jzsef University of Sci- Subfamily: Ceratopogoninae
ence in Szeged (Hungary). Fellow workers Tribe: Culicoidini
named about 150 newly described species after Genus: Culicoides
him. He passed away in 1931 at the age of 75. The Ceratopogonidae as a whole is a family of
Br is considered today as one of the most small nematocerous flies, 24 mm in length with a
outstanding Hungarian field entomologists, wingspan of usually less than 2 mm. Although closely
who unselfishly served his nation and his related to the non-biting midges, or Chironomidae,
science. they are easily distinguished by the females biting
mouthparts, their short fore legs and characteristic
venation on their membranous wings. They are
most commonly known as biting midges but there
Reference are numerous geographical variations, including
sandflies,punkies,no-see-ums,no-nos,moose-
Balogh J, Allodiatoris I (1972) In Memoriam Lajos Br flies and biting gnats. Some names are particularly
and Smuel Fenichel. Acta Zool 42:12, Budapest, expressive, for example, the Gaelic name for the Scot-
Hungary
tish Highland midge is Meanbh-chuileag (tiny fly)
emphasizing its diminutive, 1.4 mm wingspan.
Culicoides are some of the smallest cerato
pogonids, 12 mm in length, partly distinguishing
Bisexual them from the other blood-feeding genera (Lepto-
conops, Austroconops and the subgenus Lasiohelea
The occurrence of males and females in different within the genus Forcipomyia). The small head has
members of the species. a large pair of compound eyes in addition to
 Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae)
B 511

ve-segmented maxillary palps, which are outside

fi The wings of Culicoides are often an immedi-
of the short set of sucking and piercing mouth- ate identification feature for the amateur, with
parts (in the female), held perpendicular to the the majority (but not all) having a series of dark
body axis. There is also a prominent pair of seg- and pale spots covering the wings, which are
mented antennae, with long mechanoreceptors on folded, scissor-like at rest or when feeding. Other
the male antenna, giving it a feathery appearance. genera, such as Austroconops, lack any pattern on
The dorsal thorax (mesonotum) is frequently cov- their wings. The wings have been a major taxo-
ered in a distinctive pattern of dark spots or other nomic feature of the Ceratopogonidae, with a
markings, accompanied at the proximal end by a number of admirable works detailing the degree
pair of small, elongate humeral pits, distinguish- and pattern of venation, wing color and mark-
ing Culicoides from other genera. The body is ings, and the degree of coverage by macrotrichia,
generally a variation of brown or black, but some which are fine, short hairs that often cover the
species are yellowish-brown/orange (Fig.45). wing surface (Fig.46).

Biting Midges, Culicoides Spp. (Diptera: Ceratopogonidae), Figure45 Female Culicoides nubeculosus.
512
B Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae)

In addition to the wing characteristics, further been carried out by molecular techniques, partic-
identification to species is best carried out from ularly species complexes, such as the C. imicola
slide-mounted specimens. For example, the third complex, where subspecies differentiation can be
segment of the maxillary palp contains a large pit difficult using morphological features alone
containing palpal sensilla. Some species have small (Figs.46 and 47).
pits, each bearing individual sensilla. These sen- Culicoides larvae are aquatic/semi-aquatic
silla are generally considered to be concerned with and swim with a distinctive eel-like motion. They
carbon dioxide (and hence host) detection in the are found in a variety of environments, such as
female midge, with smaller numbers found in the mud, salt-marsh, compost and leaf litter. Some of
non-blood-feeding male. The shape and size of the the most important veterinary species breed in
palpal pit, and the numbers of sensilla are often damp ground contaminated to a degree with
used as taxonomic tools. Likewise, the antennal animal excreta and other organic matter. The
sensilla are pivotal to species identification. The slender larvae are primarily pale, sometimes with
antenna consists of a small, flattened ring with a thoracic markings. The pharyngeal skeleton of the
triangular apex (thescape), a globular, cup-shaped sclerotized head capsule is a key taxonomic feature.
pedicel, which is enlarged in the male antenna to
accommodate a well-developed Johnstons organ
and the antennal flagellum, having 13 sub-seg- Distribution
ments. Culicoides antennae bear approximately
300350 (male) and 200250 (female) sensilla. Of Culicoides are the most widespread of the
greatest importance to the taxonomist is the num- Ceratopogonidae, occurring throughout the world,
ber and positions of the sensilla coeloconica and with the exception of the polar regions. The only
sensilla trichodea. Further taxonomic detail can large inhabited land masses from which they are
also be gained from both the male and female gen- known to be absent are New Zealand and the
italia. More recently, species differentiation has southern most areas of South America.

Biting Midges, Culicoides Spp. (Diptera: Ceratopogonidae), Figure46 Female Culicoides nubeculosus
showing separated compound eyes.
 Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae)
B 513

Biting Midges, Culicoides Spp. (Diptera: Ceratopogonidae), Figure47 Culicoides spp. maxillary palp,
3rd segment, showing different arrangements of the palpal sensilla: upper left, C. insinuatus; upper
right, C. nubeculosus; lower left, C. impunctatus; lower right C. pseudodiabolicus.

Ecology and Behavior down into the substrate, where they live as omni-
vores/detritivores. The larvae commonly remain
Life Cycle and Population Dynamics close to the substrate surface. In Scotland, more
The cylindrical or cigar-shaped Culicoides eggs than 50% Culicoides impunctatus larvae have been
(30200 per batch) are laid on the chosen sub- recovered from the top two cm of the soil surface.
strate surface, where they hatch (210 days C. impunctatus appears to show a weak photo-
depending on temperature) and the larvae move negative response, with a greater proportion in
514
B Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae)

deeper samples during the day than at night. This close to emergence sites, host-seeking females may
daily migration is far more marked in Culicoides move several kilometers from a breeding site. One
furens larvae, which live in the muddy banks of report suggests that Culicoides mississippiensis
mangrove channels. With vegetation often sparse, travels more than 3 km in 24 h, without wind
predation by birds is a serious threat during the assistance. When wind carriage does become
daylight hours, perhaps explaining the fact that important, midges can travel considerable distances
larvae feed on algae at the mud surface during the and increasing evidence suggests that disease
night and on nematodes deeper down in the mud outbreaks in areas where particular Culicoides-
during the day. In addition to a vertical compo- transmitted diseases are not endemic may start in
nent, the spatial distribution of Culicoides larvae this way. For example, the outbreaks of bluetongue
also appears to have a horizontal component. Even virus in Sardinia in 2000 and 2001 may have been
in apparently homogeneous environments such as caused by infected midges carried on the wind from
the Scottish Highlands, Culicoides larval distribu- Northern Africa.
tion can be directly correlated with soil conditions
(water and organic content) and key indicator Mating Behavior
plant species. A similar situation is seen with the
salt-marsh species Culicoides melleus, with larval Mating in Culicoides spp. has been studied for only
distribution related to soil pH and areas of a small number of species, and despite the general
Distichlis spicata (Gramineae). hypothesis that mating is initiated in male swarms
There are four larval instars, and the time (as in many other nematocerans), there are only a
required for larval development varies with tem- few records of Culicoides spp. swarms (including
perature. Development may be completed in 14 Culicoides nubeculosus and C. impunctatus). Since
days in warmer areas, with up to seven generations the conditions required for male swarming (still,
produced each year. In more temperate regions, warm and humid) can be rare in some temperate
this is reduced to one or two generations with the regions, it has been suggested that for species
final larval instar often acting as the over-wintering living in these areas (e.g., C. impunctatus in
stage, although some species will aestivate as eggs. Scotland), at peak emergence periods it may be
In Scotland, the over-wintering period for energetically more profitable for males to wait in
Culicoides lasts for up to 9 months, followed by two the vegetation for emerging females, i.e., some
adult generations during the summer. The pupal species may be facultative swarming species. Male
period lasts between 2 and 10 days. swarming can be stenogamic (swarming adjacent
Nightly trapping program can reveal signifi- to hosts on which females are feeding) or eurygamic
cant information on the structure of Culicoides (no host involved), depending on the species.
populations, including autogeny (e.g., females Distance and contact sex pheromones have been
laying their first egg batch without taking a blood- implicated in the mating of C. nubeculosus and
meal), protandry (e.g., males emerging before C. melleus, respectively. Both of these species have
females), in addition to reproductive and survival been the subject of detailed studies of the mating
rates, themselves allowing the calculation of a process, including mate selection by the female,
species vector competency (e.g., the likelihood of it spermatophore formation and sperm transfer.
being able to transmit a disease pathogen). In asso-
ciation with climate data, it is possible to construct
models of the influence of a range of climatic Host Finding and Feeding Behavior
conditions on midge flight and biting activity.
Records of midge dispersal rates vary enor- In addition to a bloodmeal, which is necessary for
mously. Whereas male midges appear to remain female Culicoides to develop their eggs (including all
 Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae)
B 515

egg batches laid after the first batch by autogenous host-seeking, with the production of a volatile
species), a carbohydrate source is also important for recruitment pheromone by parous, host-seeking
most species. Direct evidence of sugar feeding in females, possibly analogous to the invitation
the field, however, is rare. The small number of pheromone of some mosquito species. Variations
published records include C. mississippiensis feeding in these chemical cues between individuals may
from flowers of yaupon holly plants (Ilex vomitoria) account for some degree of intra-species selection
in Florida. by Culicoides.
The majority of Culicoides show some degree Visual cues are also important in bloodmeal
of host preference and this has been investigated host location by a range of blood-feeding insects
by a number of different techniques, including including both diurnal and crepuscular species.
precipitin tests, fluorescent antibody tests, latex Culicoides spp. appear to be no exception. Field
agglutination tests, ELISA tests and most recently, populations of C. impunctatus in Scotland were
DNA analysis by PCR. These tests help to refine attracted to solid-outlined, black, rectangular
the definition of a particular species such as, for targets and this response was enhanced in the
example, ornithophilic (bird-feeding) or mam- presence of CO2.
malophilic (mammal-feeding). Many species show Culicoides are pool-feeders, using their finely
further specialization within these broad classes. toothed mandibles and maxillae to pierce the skin,
For example, using an ELISA assay, single, working in a scissor-like fashion to create a pool of
blood-fed C. impunctatus were screened against blood from which the insect feeds. Prior to this
nine different potential bloodmeal hosts. The behavior, however, some midges display a degree
results showed that cattle, deer and sheep were the of choice concerning the area to feed from. This
primary hosts for this species. appears to be particularly the case with large
Culicoides spp. biting midges have a highly hosts, including cattle and horses. The size of
sensitive olfactory system, which is used in com- the Culicoides bloodmeal has been estimated at
bination with other senses to locate their blood- 4102 ml, with a process of rapid diuresis acting
meal hosts accurately. The olfactory system is to concentrate the blood.
based around the antennae and maxillary palps,
the morphology and ultrastructure of which has
been fully documented for a number of species.
Recent studies have used antennal responses as Biting Behavior: Implications
a screening tool to identify behaviorally active for Man and Animals
compounds. This has involved the development
of electrophysiological techniques, in particular Disease Transmission
the recording of electroantennograms (EAGs)
which, combined with behavioral studies and Culicoides spp. biting midges are most important
field trapping programs with active compounds, as vectors of a number of serious livestock patho-
has led to the identification of several semiochem- gens, including African horse sickness virus and
icals involved in the host location behavior of bluetongue virus (which cause OIE list A
Culicoides spp. For mammalophilic species, one diseases in their equine or ruminant hosts),
ubiquitous host-derived attractant is 1-octen-3- bovine ephemeral fever virus (which significantly
-ol, with others including acetone, butanone and reduces milk yields in cows and causes sterility
L(+) lactic acid. Responses to each of these can be in bulls), Akabane virus (which causes abortions
either enhanced or synergized by the addition of and congenital deformities in ruminants), Palyam
carbon dioxide. For one species, C. impunctatus, viruses (which cause abortion storms in cattle)
there is evidence of pheromone involvement in and epizootic hemorrhagic disease of deer virus
516
B Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae)

(which kills many species of deer and also causes in tropical and sub-tropical regions (e.g., Mansonella
disease in cattle). Each of these diseases has an ozzardie, transmitted by Culicoides phlebotomus in
established distribution, intricately linked with coastal North Trinidad) and a small number of
that of its vector. There are, however, increasing viruses, including Oropouche, which is strongly
examples of disease incursions into areas previ- pathogenic to man in parts of South America and
ously unaffected, perhaps as a result of relaxations the West Indies.
in international trade barriers, and a trend toward
more favorable climatic conditions in these areas.
For example, bluetongue virus (BTV) occurs as a Animal Welfare
clinical disease in Africa, the Middle East, the
Indian subcontinent, China, the USA, and Mexico The general irritation caused by midge bites can
where Culicoides are active throughout the year. occasionally also lead to serious health and
In December 1999, and January 2000, a BTV welfare conditions in both animals and man.
serotype 2 epidemic occurred in Tunisia, close to Deer herds are often forced off low-lying pastures
the Algerian border. This was the first time the onto higher, poorer slopes by midge attacks,
disease had been reported from North Africa. which has been suggested as the reason why Scot-
Further outbreaks followed in June 2000, matched tish red deer are weaker than their European
by outbreaks in contiguous coastal areas of counterparts. The distress caused by midges to
neighboring Algeria. From there it appears that cattle is also held to be responsible for reductions
infected vectors carried bluetongue to Europe, in milk yields. Horses can also suffer from a num-
with outbreaks reported by Italy (August: Sardinia, ber of allergic reactions to midge bites, including
November: Calabria and Sicily), France (October: sweet itch (also known as Queensland itch in
Corsica, for the first time) and Spain (October Australia and kasen in Japan), which is an
and November: Balearic Islands, last infected in acutely irritating dermatitis, primarily confined
1960). Although there are only a small number of to the mane and tail, although it may spread to
confirmed vectors for BTV (Culicoides variipen- the rest of the body. The horses skin becomes
nis and possibly Culicoides insignis in the New thickened, weals and pustules form, and much of
World, Culicoides imicola and possibly Culicoides the hair of the mane and tail breaks off or is
obsoletus in the Mediterranean and Middle East rubbed off, resulting in extensive damage and
and C. imicola and members of the Culicoides large sores in addition to financial loss. Causal
milnei and Culicoides schultzei groups in Africa), agents have been identified as Culicoides pulicaris
laboratory infections have demonstrated that (UK), C. obsoletus (Canada), Culicoides robertsi
a number of endemic species in officially (Australia), C. imicola (Israel) and Culicoides
unaffected countries will support virus multi- insignis, Culicoides stellifer and Culicoides venus-
plication following infection. tus (USA). Present methods of prevention include
Culicoides spp. also transmit a number of judicious stabling during the summer months
protozoans, most of which are avian parasites and a range of antihistamine, cortisone injections
(Haemoproteus, Hepatocystis and trypanosomes). and soothing ointments.
In addition, they transmit a variety of filarial
worms (including Onchocerca spp.), infecting a
range of animals, including birds, cattle and Human Annoyance
horses.
Overall, pathogen transmission to man by It is the biting attacks on humans, however, for
biting midges appears to be minimal, although which midges are most noted in a number of
they do transmit several species of filarial worms areas, including the Caribbean, California, Florida
 Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae)
B 517

and Scotland. The annoyance and discomfort potential for the development of resistant strains
they cause can influence outdoor activities from such wide applications of broad-spectrum
significantly and directly affect the local insecticides, precludes their use. Similar concerns
economies, particularly when they rely heavily are also associated with the use of pyrethroids,
on tourism. When bitten, the skin reaction of investigated for Culicoides larval control in the
humans is usually mild, including temporary 1980s with populations of C. varipennis and
burning and slight swelling. More sensitive indi- C.mississippiensis in the USA. For these reasons,
viduals, however, can develop weals, blisters and alternative larvicides based on naturally occurring
extreme inflammation of the skin. In a very few products, for example, neem-based products, are
cases, extreme allergies can lead to hospitaliza- being investigated following the growing trend
tion. Scarring and secondary infection may occur toward integrating botanical products into insect
if bites are scratched. pest-control programs.
Insecticide treatments of adult Culicoides
have met with less success than larvicidal
Control programs. A number of programs in the 1950s
and 60s were based on thermal insecticide fog-
Culicoides control programs have often been met ging, but the results were disappointing, most
with difficulties, due to a number of factors. These probably because the insects avoided contact with
include the fact that their breeding grounds are the insecticide by hiding beneath vegetation. In
often widely scattered, difficult to recognize and addition, there is the likelihood that a sprayed
often within environmentally sensitive areas, area would be reinvaded as soon as the insecti-
thereby limiting the application of control prod- cidal mist had cleared, requiring regular (and
ucts. The vast populations of adult midges and expensive) re-treatment.
their extreme mobility and potential for wind- Where Culicoides are responsible for out-
carriage also places limits on the use of chemical breaks of livestock disease, direct treatments of
control of adults. the animals with insecticides (e.g., pyrethroids
and ivermectin) have been partially successful.
Under serious virus challenge conditions,
however, permethrin failed to protect cattle
Chemical Control from bluetongue virus infection in a Californian
dairy.
Culicoides spp. are susceptible to the majority of
the major insecticide classes and most have been
used at some stage against both adults and larvae,
with varying degrees of success. Due to the diffi- Habitat Manipulation
culty of targeting adult midges, chemical control
programs have concentrated primarily on the Biting midge problems world-wide have been
larval stages. Early studies (from the 1950s to the partly alleviated through a variety of measures
1970s) involved the broadcast application of a aimed at altering the suitability of areas for both
number of persistent and broad-spectrum insecti- adult and larval midges. An example is the
cides, including members of the organochlorines impounding or flooding of areas in Florida and
(e.g., DDT) and organophosphates (e.g., chlorpy- the Caribbean to eliminate breeding sites of midge
rifos). Although partly successful, todays knowl- larvae which cannot survive in free-water.
edge of the significant environmental and health Alternative strategies have included draining or
risks associated with these products, as well as the land-filling breeding sites in salt marshes in Florida
518
B Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae)

to make them too dry for midges to breed. There concoctions marketed as insect repellents. These
are various other environmental manipulations, include oils distilled from a range of plants, includ-
such as stream flushing and shade removal, which ing lemon-grass, eucalyptus, cypress, lavender,
are in widespread use in the tropics to control pennyroyal and thyme. A common factor for most
mosquitoes. Such measures have never been used of these is that they contain a number of terpenoid
in more temperate regions. In fact, it has been compounds, such as citronellal and limonene.
suggested that it is doubtful that any attempt to There are a number of regional favorites. For
alter the landscape of localized areas would, in the example, in Scotland, the oil derived from the
long term, be successful against biting midges in leaves of Myrica gale (bog myrtle, sweet gale
Scotland. Considering the relatively high mobility Myricaceae), a deciduous shrub that grows widely
of these insects and the vast areas of potential in the Highlands of Scotland, has repellent prop-
breeding grounds, this is probably true. Addition- erties equivalent to DEET against Culicoides spp.
ally, these methods are often extremely expensive, In North America, even the US military consider
laborious and although they may make the the use of Avon Skin-So-Soft, as an alternative
environment less suitable for Culicoides, they to DEET to protect them from biting insects.
frequently destroy the habitats of other, non-target
organisms.
Traps

Repellents Traps are used mainly as population monitoring

devices for Culicoides spp., although over limited
The use of personal repellents can give a degree of areas, they can offer a degree of control. Traps vary
protection against biting midges and indeed, this from basic light-suction traps (with blacklights
is generally assumed to be the best line of defense. attracting more than whitelights), to more special-
In addition, repellents can be used to treat win- ized, odor-baited traps. The latter resulted in
dows and door screens and even clothing. A range increased and more specific Culicoides spp. catches.
of chemical repellents, in various formulations Carbon dioxide (often released from a dry ice
sold under a number of different trade names, are source) provides the most impressive increase in
currently available. The most widely used chemi- catch size, although its attractiveness can be
cal in insect repellents is DEET (N,N-diethyl-m- enhanced in combination with some of the
toluamide), forming the main active constituent in host-related kairomones that are gradually being
the majority of over-the-counter preparations, identified for Culicoides spp. For example, some
with concentrations varying from 10% to 90%. commercial traps use a combination of carbon
Since it was first marketed in 1956, DEET has dioxide and 1-octen-3-ol.
remained the most effective repellent against
midges, mosquitoes and other biting pests,
although there have been a number of concerns Biological Control
voiced regarding its safety, including a suggested
contribution of DEET usage to the psychological The possibility of employing biological control
effects associated with a number of combat situa- techniques for the control of Culicoides spp. has
tions. Although DEET toxicity from casual use is been little studied. Predators, parasites and
thought to be low and there are no definite reports pathogenic microbes suspected of being natural
that these products are not safe if used correctly control agents of Culicoides spp. were recorded
and sensibly, for those people preferring natural by Bacon in 1970, including viruses, rickettsiae,
products, there is no limit to the number of herbal bacteria, fungi, protozoa and nematodes. Few,
 Black Bean Aphid, Aphis fabae Scopoli (Hemiptera: Aphididae)
B 519

however, have been identified and studied in Biting Rate

relation to potentially reducing biting midge pop-
ulations. Nematodes of the family Mermithidae This is a measure of abundance of biting insects,
are known to be fatal parasites of Ceratopogoni- and is expressed as number of bites per person per
dae larvae, but have been found in only a few period of time. It is usually used in the assessment
species, including C. variipennis in dairy waste- of mosquito abundance, and rather than have
water ponds in California. The only report of a the insects actually bite before they are tabulated,
fungal pathogen of Culicoides spp. is for the insects are typically captured pre-feeding,
Culicoides molestus larvae in New South Wales, thereby alleviating stress to the census taker, and
Australia, in which infection rates with the alleviating the risk of disease transmission. Under
Oomycete Lagenidium giganteum of 162% were these conditions, then, it is actually the insect land-
recorded. Concerning microbial insecticides, ing rate that is being measured, and used as an
Culicoides spp. are virtually unaffected by com- index of the potential biting rate. Biting rate is also
mercial applications used frequently against used as a component of insect repellent assessment.
mosquito larvae, including Bacillus thuringiensis
var israelensis and Bacillus sphearicus.
Ceratopogonid midge species are regularly Bittacidae
infested with a variety of ectoparasitic mite spe-
cies. In particular, adult Culicoides have been A family of insects in the order Mecoptera.
found carrying phoretic instars of several families They commonly are known as hangingflies.
of mesostigmatid mites and ectoparasitic larvae Scorpionflies.
of the prostigmatid superfamily Trombidioidea.
The trombidioids are of additional interest
because, in their free-living adult stage, some Bivoltine
species have been seen feeding on larval cer-
atopogonids. The precise impacts of these mites The occurrence of two generation within a year.
on their hosts, however, is unknown. Information
is lacking on the basic biology of these mites, their
precise trophic relationships and perhaps their Bivouac
potential as vehicles and vectors of candidate
insect pathogens. Among army ants, the cluster of workers within
which the queen and brood are sheltered.

References
Blaberidae
Blackwell A (2001) The Scottish biting midge, Culicoides
impunctatus. Goetghebuer: current research status and A family of cockroaches (order Blattodea).
prospects for future control.Vet Bull 71:2R8R Cockroaches
Boorman J (1993) Biting midges (Ceratopogonidae). In: Lane
P, Crosskey RW (eds) Medical insects and arachnids,
723 pp. Chapman & Hall, New York, NY, pp 288309
Sebastiani F, Meiswinkel R, Gomulski LM, Guglielmino CR, Black Bean Aphid, Aphis fabae
Mellor PS, Malacrida AR, Gasperi G (2001) Molecular Scopoli (Hemiptera: Aphididae)
differentiation of the old world Culicoides imicola. spe-
cies complex (Diptera, Ceratopogonidae), inferred using
random amplified polymorphic DNA markers. Mol Ecol This is an important insect pest of several crops.
10:17731786 Aphids
520
B Blackburn, Thomas

Blackburn, Thomas Black Cutworm, Agrotis ipsilon

(Hufnagel) (Lepidoptera:
Thomas Blackburn was born at Islington near Noctuidae)
Liverpool, England, on March 16, 1844. Ordained a
deacon of the Anglican church in 1869, he was trans- john l. capinera
ferred to Hawaii in 1870. There, he collected insects University of Florida, Gainesville, FL, USA
of all orders. Next, he was transferred to Australia
and became rector of a church at Port Lincoln in The origin of black cutworm is uncertain, though
1882, then one at Woodville near A delaide, in 1886, it is now found in many regions of the world,
which position he held for the rest of his life. In Eng- being absent principally from some tropical
land, he and his brother J. B. Blackburn founded regions and cold areas. It is more widespread, and
The Weekly Entomologist which, after two years, damaging, in the northern hemisphere than the
was renamed Entomologists Monthly Magazine southern hemisphere. It annually reinvades
and is published to this day. In Australia, he collected temperate areas, overwintering in warmer or
beetles intensively, but specialized in Scarabaeidae. subtropical regions. It has acquired several other
He became the foremost Australian coleopterist, and common names, including greasy cutworm and
published descriptions of 3,069 Australian species. dark sword grass cutworm.
He died on May 28, 1912, at Woodville. Long distance dispersal of adults has long
been suspected in Europe, China, and North Amer-
ica. The basic pattern is to move north in thespring,
Reference and south in the autumn. Studies in the United
States demonstrated northward displacement of
Herman LH (2001) Blackburn, Thomas. Bull Am Mus Nat moths during the spring in the range of 1,000 km
Hist 265:4546 in 24 days when assisted by northward flowing
wind. Similar displacement to the south and south-
west has been documented in the autumn.
Black Carpet Beetle,
Atagenusmegatoma
(Fabricius)(Coleoptera: Life History
Dermestidae)
The number of generations occurring annually
This is an important pest of stored products, varies with weather conditions. In North America,
including stored grain. there are 12 generations in Canada but 24 in
Stored Grain and Flour Insects the United States. In Tennessee, USA, moths are
Stored Grain and Flour Insects and Their present in March-May, June-July, July-August, and
Management September-December. Based on light trap collec-
tions, moths are reported to be abundant in Arkansas,
USA (a warm climate) during May-June and Sep-
Black Citrus Aphid, Toxoptera tember-October, and in New York, USA (a cool
aurantii (Boyer climate), they occur mostly in June-July. However,
DeFonscolombe) light traps are not very effective during the spring
(Hemiptera:Aphididae) flight, and underestimate early season. Thus, the
phenology of black cutworm remains uncertain,
This is an important pest of citrus crops. or perhaps is inherently variable due to the
Citrus Pests and Their Management vagaries associated with long range dispersal.
 Black Cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae)
B 521

verwintering has been reported to occur in the

O reported to be 3.5, 5.36.2, 7, 10, 2030, 3045, 50,
pupal stage in most areas where overwintering and 50 mm for instars 18, respectively. Duration
occurs, but larvae persist throughout the winter in of the larval stage is normally 2040 days. Mean
Florida, USA, a subtropical environment. Pupae duration of instars 16 was reported to be 6.0, 5.0,
have been known to overwinter as far north as 4.6, 4.3, 5.6, 4.0 days, respectively, at 22C. Larval
Tennessee, but apparently are incapable of surviv- development is strongly influenced by tempera-
ing farther north. Thus, moths collected in the ture, with the optimal temperature about 27C.
central region of USA in March and April are Humidity is less important, but instars 15 thrive
principally dispersing individuals that are past best at higher humidities.
their peak egg production period. Nonetheless, In appearance, the larva is rather uniformly
they inoculate the area and allow production of colored on the dorsal and lateral surfaces, ranging
additional generations, including moths that from light gray or gray-brown to nearly black
disperse north into Canada. Duration of the life (Fig.49). On some individuals, the dorsal region is
cycle is normally 3560 days. slightly lighter or brownish in color, but the larva
The egg is white in color initially, but turns lacks a distinct dorsal band. Ventrally, the larva
brown with age. It measures 0.430.50 mm high and tends to be lighter in color. Close examination of
0.510.58 mm wide and is nearly spherical in shape, the larval epidermis reveals that this species bears
with a slightly flattened base. The egg bears 3540 numerous dark, coarse granules over most of its
ribs that radiate from the apex; the ribs are alternately body. The head is brownish with numerous dark
long and short. The eggs normally are deposited in spots. Larvae usually remain on the plant until the
clusters on foliage. Females may deposit 12001900 fourth instar, when they become photonegative and
eggs. Duration of the egg stage is 36 days. hide in the soil during the daylight hours. In these
There are 59 instars, with a total of 67 latter instars they also tend to sever plants at the soil
instars most common. Head capsule widths are surface, pulling the plant tissue belowground.
about 0.260.35, 0.450.53, 0.610.72, 0.901.60, Larvae tend to be cannibalistic.
2.12.8, 3.23.5, 3.64.3, and 3.74.1 mm for Pupation occurs belowground at a depth of
instars 18, respectively. Head capsule widths are 312 cm. The pupa is 1722 mm long and 56 mm
very similar for instars 14, but thereafter those wide, and dark brown. Duration of the pupal stage
individuals that display 89 instars show only is normally 1220 days.
small increments in width at each molt and even- The adult is fairly large in size, with a wingspan
tually attain head capsule sizes no larger than those of 4055 mm. The forewing, especially the proximal
displaying only 67 instars. Larval body length is two-thirds, is uniformly dark brown (Fig.48). The
distal area is marked with a lighter irregular band,
and a small but distinct black dash extends distally
from the bean-shaped wing spot. The hind wings
are whitish to gray, and the veins marked with

Black Cutworm, Agrotis ipsilon (Hufnagel) Black Cutworm, Agrotis ipsilon (Hufnagel) (Lepi-
(Lepidoptera: Noctuidae), Figure48 Adult of doptera: Noctuidae), Figure49 Mature larva of
blackcutworm, Agrotis ipsilon (Hufnagel). black cutworm, Agrotis ipsilon (Hufnagel).
522
B Black Cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae)

darker scales. The adult preoviposition period is Euphorocera claripennis (Macquart), Gonia longipul-
about 710 days. Moths select low-growing broad- villi Tothill, G. sequax Williston, Lespesia archippiv-
leaf plants preferentially for oviposition, but lacking ora (Riley), Madremyia saundersii (Williston),
these will deposit eggs on dead plant material. Soil Sisyropa eudryae (Townsend), and Tachinomyia
is an unsuitable oviposition site. panaetius (Walker) (all Diptera: Tachinidae). Preda-
Black cutworm has a wide host range. Nearly all tory ground-dwelling insects such as ground beetles
vegetables can be consumed, and this species also (Coleoptera: Carabidae) apparently consume
feeds on alfalfa, clover, cotton, rice, sorghum, straw- numerous larvae. Although studies in Florida, USA,
berry, sugarbeet, tobacco, and sometimes grains and indicated that 7580% of cutworms could be killed
grasses. In the midwestern USA it is considered to by a granulosis virus, there is surprisingly little infor-
be a serious corn pest. Among the weeds suitable for mation on epidemiology and of natural pathogens.
larval development are bluegrass, Poa pratensis; Rather, such pathogens as viruses, fungi, bacteria,
curled dock, Rumex crispus; lambs-quarters, Cheno and protozoa from other insects have been evalu-
podium album; yellow rocket, Barbarea vulgaris; ated for black cutworm s usceptibility; in most cases
and redroot pigweed, Amaranthus retroflexus. The only relatively weak pathogens have been identified.
preference by black cutworm for weeds is sometimes An entomopathogenic nematode, Hexamermis
quite pronounced, and crops will be attacked only arvalis (Nematoda: Mermithidae), is known to para-
after the weeds are consumed. Adults feed on nectar sitize up to 60% of larvae in the central USA.
from flowers. Deciduous trees and shrub such as
linden, wild plum, crabapple, and lilac are especially
attractive to moths.
Numerous species of natural enemies have Damage
been associated with black cutworm, but data on
their relative importance are scarce. However, in This species occurs frequently in many crops, and is
Missouri, USA, there are reports of 69% parasitism, one of the best-known cutworms. Despite the fre-
so natural enemies probably exact a significant toll quency of occurrence, however, it tends not to appear
on cutworm populations. Among the wasps known in great abundance, as is known in some other cut-
to attack this cutworm are Apanteles marginiventris worms and armyworms. Black cutworm is not con-
(Cresson), Microplitis feltiae Muesebeck, Microplitis sidered to be a climbing cutworm, most of the
kewleyi Muesebeck, Meteorus autographae Muese- feeding occurring at soil level. However, larvae will
beck, Meterorus leviventris (Wesmael) (all feed aboveground until about the fourth instar. Lar-
Hymenoptera: Braconidae); Campoletis argentifrons vae can consume over 400 sq cm of foliage during
(Cresson), Campoletis flavicincta (Ashmead), Hypo- their development, but over 80% occurs during the
soter annulipes (Cresson), and Ophion flavidus Brulle terminal instar, and about 10% in the instar immedi-
(all Hymenoptera: Ichneumonidae). Larvae parasit- ately preceding the last. Thus, little foliage loss occurs
ized by Meteorus leviventris (Wesmael) consume during the early stages of development. Once the
about 24% less foliage and cut about 36% fewer fourth instar is attained, larvae can do considerable
seedlings, so considerable benefit is derived from damage by severing young plants, and a larva may
parasitism in addition to the eventual death of the cut several plants in a single night. Plants tend to
host larva. Other parasitoids known from black outgrow their susceptibility to injury. Corn at the
cutworm include flies often associated with other one-leaf stage is very susceptible to damage, but by
ground-dwelling noctuids, including Archytas the 4- or 5-leaf stage plant yield was not reduced by
cirphis Curran, Bonnetia comta (Fallen), Carcelia larval feeding. Leaf feeding and cutting above the
formosa (Aldrich and Webber), Chaetogaedia mon- soil line are less damaging to corn than cutting at the
ticola (Bigot), Eucelatoria armigera (Coquillett), soil surface. Subterranean damage is very injurious.
 Black Cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae)
B 523

Management weeds also can be beneficial by supporting pro-

longed survival of parasitoids. In contrast, reduced
Adult populations can be monitored with both tillage cropping practices, which often produce
blacklight and sex pheromone traps. However, higher weed populations, seem to result in increased
light traps are not consistently efficient. Light traps abundance of black cutworm and higher levels
are most effective in the summer and autumn, of cutting in corn. This may be due, in part, to
butthe late season generations generally pose little the tendency of moths to oviposit on weeds;
threat to crops. Pheromone traps are more effective weedy fields tend to have higher cutworm
during the spring flight, when larvae present the populations.
greatest threat to young plants. Trap color affects Black cutworm populations also tend to be
moth capture rate, with white and yellow traps higher in wet areas of fields, and in fields that
capturing more than green traps. have been flooded. Black cutworm has been
Large larvae burrow in the soil, and are diffi- known, at times, as overflow worm, due to its
cult to observe. However, larvae can be sampled tendency to be abundant and damaging in
with bait traps, and this is most effective prior to fields that have been flooded by overf lowing
emergence or planting of seedlings. Various trap rivers.
designs have been studied, but many employ a In the home garden, barriers are sometimes
container sunk into the soil with the upper lip at useful to prevent damage to seedlings by cut-
the soil surface. The container is baited with fresh worms. Metal or waxed paper containers with
plant material and/or bran, and with vermiculite both the top and bottom removed can be placed
so the larvae can attain shelter. Larvae are effec- around the plant stem to deter consumption.
tively captured in baited containers if the vermic- Aluminum foil can be wrapped around the stem
ulite is not too near the surface, and catches are to achieve a similar effect. Because larvae will bur-
enhanced if a screen cylinder, which provides a row and feed below the soil line it is necessary to
visual stimulus to the cutworms, is suspended extend to barrier below the soil surface. Because
above the baited container. If plants are present in black cutworm moths, which easily circumvent
the field they compete with the bait in the traps, such barriers, are active during the growing season,
and trap efficiency declines markedly. The distri- this procedure alone may have little value. Use of
bution of larvae in the spring is random. netting or row covers, in addition to larval barri-
Persistent insecticides are commonly applied ers, should prove more effective.
to plants and soil for black cutworm suppression, Entomopathogenic nematodes (Nematoda:
but surface rather than subsurface soil applications Steinernematidae and Heterorhabditidae) will
are desirable. Larvae readily accept insecticide- infect and kill black cutworm larvae, but their
treated bran and other baits. Application of systemic populations normally need to be supplemented to
insecticides to seeds also provides some protection realize high levels of parasitism. Their effective-
against larval injury. Bacillus thuringiensis is not ness is related to soil moisture conditions.
usually recommended for cutworm control. Turfgrass Insects and Their Management
Black cutworm larvae feed readily on weeds, Vegetable Pests and Their Management
and destruction of weeds can force larvae to feed
exclusively on crop plants, exacerbating damage.
Thus, it is often recommended that weeds not be References
tilled or treated with herbicide until larvae have
Abdel-Gawaad AA, El-Shazli AY (1971) Studies on the
matured. Timing is important, however, because
common cutworm Agrotis ypsilon Rott. I. Life cycle and
prolonged competition between crop and weed habits. Zeitschrift fur Angewandte Entomologie
plants can reduce crop yield. Presence of flowering 68:409412
524
B Black Earwigs

Archer TL, Musick GL, Murray RL (1980) Influence of legs (Fig.50). The female possesses a long oviposi-
temperature and moisture on black cutworm
tor with which it deposits its eggs in small groups,
(Lepidoptera: Noctuidae) development and reproduc-
tion. Can Entomol 112:665673 beneath the scales protecting the ostiole (eye) of
Busching MK, Turpin FT (1976) Oviposition preferences of the syconium (fig fruit). Oviposition takes place
black cutworm moths among various crop plants, weeds, preferably in unripe figs, but ripening ones are also
and plant debris. J Econ Entomol 69:587590
Busching MK, Turpin FT (1977) Survival and development of
attacked. The larvae feed on the tissues of the syco-
black cutworm (Agrotis ipsilon) larvae on various species nium, destroying the fruit. Infestation of unripe
of crop plants and weeds, Environ Entomol 6:6365 figs usually results in premature fruit drop, which
Capinera JL (2001) Handbook of vegetable pests. Academic is frequently mistaken by the growers as due to
Press, San Diego, 729 pp
Harris CR, Mazurek JH, White GV (1962) The life history of physiological problems of the trees. The fly com-
the black cutworm, Agrotis ipsilon (Hufnagel), under pletes 45 generations per year and overwinters in
controlled conditions. Can Entomol 94:11831187 the pupal stage in the soil.
McCorcle, Robinson JF, Way MO, Wallendorf MJ, Goode-
Observations conducted in Chios island,
nough JL (1993) Mechanism of southward migration of
a noctuid moth [Agrotis ipsilon (Hufnagel)]: a complete Greece showed that the flies are attracted and feed
migrant. Ecology 74:23032314 mostly on sweet exudates of ripe figs, and on fresh
Schoenbohm RB, Turpin FT (1977) Effect of parasitism by or dry milky fig-tree sap exuded from injured plant
Meteorus leviventris on corn foliage consumption and
corn seedling cutting by the black cutworm. J Econ
parts. As many as 63 pupae were obtained from a
Entomol 70:457459 single infested, unripe fig, indicating multiple
Story RN, Keaster AJ (1982) Temporal and spatial distribu- oviposition. The parasitoid Pachycrepoideus
tion of black cutworms in midwest field crops. Environ vindemmiae Rondani (Hymenoptera: Ptero-
Entomol 11:10191022
malidae) emerged from S. adipata pupae.
Males were observed swarming in the afternoon
hours, an indication that the mating behavior
Black Earwigs is related to swarm formations. Hexanol, a
generally-occurring plant volatile chemical, is
Members of the earwig family Chelisochidae very attractive for the fly and selective, especially
(order Dermaptera). for females. Use of McPhail traps baited with
Earwigs hexanol is very effective for monitoring and pos-
sibly for control of this fly. Addition of 2%
ammonium sulphate in the trap water enhances
Black Fig Fly (Diptera: trap effectiveness. Proteinaceous bait sprays are
Lonchaeidae) recommended when better control is needed.

byron katsoyannos
Aristotle University of Thessaloniki,
Thessaloniki, Greece

The black fig fly, Silba adipata McAlpine, is a pest

of wild and cultivated figs, Ficus carica L.
(Moraceae), occurring in the Mediterranean coun-
tries and Iraq. This insect was studied extensively
by Silvestri in Italy at the beginning of the twenti-
eth century, although he misidentified it as
Lonchaea aristella Becker. The adult is glossy black, Black Fig Fly (Diptera: Lonchaeidae),
3.54.5 mm in length, with reddish eyes and brown Figure50 Adult black fig fly (after Silvestri, 1917).
 Black Flies (Diptera: Simuliidae)
B 525

References Approximately 260 species are known from North

America north of Mexico.
Katsoyannos BI (1983) Field observations on the biology and The taxonomy of the family is based primar-
behavior of the black fig fly Silba adipata McAlpine ily on features of the genitalia, legs, and wings of
(Diptera: Lonchaeidae), and trapping experiments.
JApplEntomol 95:471476
the adults; the cocoons and gills of the pupae; and
Katsoyannos BI, Guerin PM (1984) Hexanol: a potent attrac- the head capsule and pigmentation patterns of the
tant for the black fig fly, Silba adipata. Entomol Exp Appl larvae. Many species, however, are structurally
35:7174 similar, if not identical, and are known as sibling
Silvestri F (1917) Sulla Lonchaea aristella Beck. (Lonchaeidae)
dannosa alle infiorescenze e fruttescenze del caprifico e species. They are typically revealed by studies of
del fico. Bollettino del Laboratorio di Zoologia Agraria the banding patterns in the giant polytene chro-
in Portici 12:123146 mosomes of their larval salivary glands. Nearly a
Talhouk AMS (1969) Insects and mites injurious to crops in
quarter of the North American species, for exam-
middle eastern countries. Monographien zur ange-
wandte Entomologie 21:1239, Paul Parey Verlag, ple, were first discovered chromosomally.
Hamburg und Berlin, Germany The first three stages (egg, larva, pupa) of the
life cycle are completed in running water. All types
of flowing freshwater are exploited by black flies,
Black Flies (Diptera: Simuliidae) from the smallest trickles to the largest rivers.
Only a few species can tolerate polluted waters.
peter h. adler The female black fly typically deposits its eggs
Clemson University, Clemson, SC, USA either by dipping to the waters surface during
flight to release a few eggs at a time, or by crawling
Black flies are small, morphologically homoge- about on wetted vegetation and stones while
neous insects in the order Diptera, suborder Nem- releasing masses or strings of eggs. The eggs are
atocera, best known for their economic impact as bluntly triangular, and a female can carry from
biting and nuisance pests of humans and domestic about 20800, depending on the species. Larvae
animals. Adults are readily recognized by their hatch from the eggs within a few days to more
arched thorax, cigar-shaped antennae and strong than half a year. They hold onto objects in the
venation at the anterior margin of each wing. Black stream, such as rocks and leaves, by means of tiny
flies breed abundantly in flowing freshwater hooks at the end of the abdomen, which enmesh
rivers and streams throughout the world, from with a silken pad spun from the salivary glands
965 km north of the Arctic Circle to the southern- and applied to the substrate. The larval stage,
most tip of South America. Within this vast realm, including six or seven instars, lasts from about a
they are absent only from deserts and islands with- week to six months, depending on the species and
out flowing water. The immature stages often attain water temperature. Mature larvae are 315 mm in
large populations and play an important role in the length. Pupation occurs in flowing water, with a
food web of streams and rivers. silken cocoon anchoring the pupa to the substrate.
Worldwide, more than 1,700 species have Some species burrow slightly into the sand and silt
been formally named and described, with the of the streambed to pupate. The pupal stage gener-
expectation that this number will increase signifi- ally lasts no more than a few weeks. Some species
cantly as study of the family continues. The worlds are univoltine, completing only one generation
species are arranged in two subfamilies and about per year. Other species are multivoltine, producing
24 genera. The largest genus by far is Simulium, from two to about 15 generations in a year, depend-
which occurs worldwide. The greatest number of ing on the latitude and species.
species, more than one third of the known fauna, The majority of larval life is spent feeding.
inhabits the Palearctic Region, especially Russia. Most species feed primarily by filtering particulate
526
B Black Flies (Diptera: Simuliidae)

matter from the water column, using a pair of head bubble of air, buoyed to the surface with enough
fans, with one fan projecting from each anterior force to break free of the water. The freshly emerged
corner of the head. Food particles of an appropri- adult then flies to a resting spot where it tans and
ate size, those less than 350 m in diameter, often hardens its exoskeleton.
include diatoms, bacteria, protozoa, pollen, and Adults (Fig.51) are active during the day. They
organic debris. Most species also can obtain food typically live less than a month, during which time
by scraping it from the surface of stones and other they must mate and acquire food; females also
objects in the stream. About 1.5% of the worlds must return to a stream or river to oviposit. The
species do not have head fans and must obtain all adults of most species probably do not disperse
of their food by scraping. These species live in more than 10 km, although some species regularly
habitats, such as springs and glacial melt waters, travel more than 50 km in search of hosts. At least
where little organic matter is present in the water one species in Africa has been reported to disperse
column. Some species, in addition to filter feeding more than 500 km from the natal watercourses.
and scraping, also prey on small arthropods in the Mating usually takes place shortly after emer-
stream. gence. In many species, the males form aerial
Larvae often space themselves in characteris- swarms over or beside landmarks such as trees,
tic patterns depending on the species and water rocks, and waterfalls. Females fly into these swarms
currents. The larvae of some species space them- and are intercepted by males. The coupled pair
selves closely in moss-like clumps, others space quickly leaves the swarm. A small percentage of
themselves rather widely, and still others pack so species, about 2% in North America, mate on the
densely that they can exceed one million per square ground at their emergence sites. A similarly small
meter. For most of their lives, larvae remain percentage of females do not mate. These
attached to objects in the stream. When disturbed non-mating species consist of all-female, parthe-
or relocating they loop short distances, inchworm nogenetic populations, and they occur at northern
fashion, or release their hold of the silk pad and latitudes.
drift downstream either freely or moored to a silk Both male and female black flies feed on water
strand, eventually reattaching to a suitable substrate. and a source of carbohydrate, such as floral nectar
Drift is particularly frequent at sunset and during and honeydew, that fuel their flight activities. Only
the night, and is an important means of avoiding females feed on blood. The mouthparts of males are
predation by fish and predacious arthropods.
Larvae are susceptible to parasites and
pathogens, including mermithid nematodes,
protozoa, microsporidia, fungi, and viruses.
Only a small percentage, perhaps about 1%, of
a population is usually infected, although
p arasitized larvae often live longer than unin-
fected individuals and become more apparent
as the population ages and the healthy larvae
pupate. Most parasites kill the larvae, but some
pass through the pupae and into the adults,
typically sterilizing the adult.
Larvae of most species pupate singly, but
those of some species form large clusters of pupae. Black Flies (Diptera: Simuliidae), Figure51
The adult that has developed within the pupa Female black fly (from Cameron 1922; Canadian
forcibly splits the pupal cuticle and emerges in a Department of Agriculture Bulletin).
 Black Flies (Diptera: Simuliidae)
B 527

incapable of cutting skin. Females use their mandi- allergic reactions. More typical reactions include
bles to snip the skin of warm-blooded animals, itching welts at the site where the person was
while injecting various anesthetics and anti-clotting bitten. Outdoor industries and recreational activi-
factors. As the capillaries are severed, a pool of ties often are severely curtailed by both nuisance
blood forms, which is then imbibed. Not all species and biting species.
have females that feed on blood. In less than 10% of Black flies transmit numerous blood protozo-
the worlds species, the females have mouthparts ans, filarial worms, and perhaps a few viruses to
much like those of the males, too feeble to cut ver- mammals and birds. Human-borne pathogens are
tebrate flesh. These non-biting females typically transmitted by black flies only in Africa and parts
occur in northern environments such as the arctic of Central and South America. The most common
and are facultatively autogenous, meaning that by and serious human disease is onchocerciasis, or
necessity, they mature their eggs without the benefit river blindness, caused by a filarial worm. Filarial
of blood. The nutrient reserves for egg production worms also are transmitted to cattle, deer, moose,
are carried over from the larval stage. black bears, and ducks, but apparently cause little
Black flies use a wide range of hosts to acquire economic impact. The major avian pathogens
a blood meal although many species are quite transmitted by black flies are malaria-like blood
host- specific. For example, one species of black fly protozoans that cause a disease called leucocyto-
feeds only on loons. Other species feed only on zoonosis. In North America, turkeys, ducks, and
raptors, or only on small or large mammals. Still wild birds are affected. The consequences among
other species appear to be true generalists. To domestic birds can be grievous and include
locate their hosts, females use a series of cues such depressed immune systems, weight loss, decreased
as color, shape, size, and odor. Carbon dioxide is reproduction, and even death.
especially attractive. Species tend either to feed on Since the 1980s, the primary means of con-
birds (ornithophily) or mammals (mammaloph- trolling pest populations of black flies has been
ily). The bird feeders have a thumb-like lobe on with the bacterium Bacillus thuringiensis variety
their claws, whereas most mammal feeders have israelensis (Bti), which produces a toxin highly
simple or slightly toothed talons. specific to black flies and mosquitoes. When
By virtue of their requirement for blood, applied to streams and rivers, Bti is an environ-
black flies frequently become pests of humans mentally safe means of management, killing only
and domestic animals. Only a fraction of the spe- larval black flies. Management programs are
cies, about 15% in North America, actually causes operating in many parts of the world, including
economic problems. The majority of species are Pennsylvania, Quebec, sub-Saharan Africa, and
not attracted to humans and domestic animals Brazil. Some of these programs cost millions of
but, instead, feed only on wildlife. Some of the dollars to conduct every year.
pest species are primarily a nuisance, swarming
about the head and entering the facial orifices.
Those that take blood represent a more serious References
threat, either through exsanguination, injection
of toxic saliva (simuliotoxicosis), or the transmis- Adler PH, Currie DC, Wood DM (2004) The black flies
(Diptera: Simuliidae) of North America. Cornell
sion of disease agents. Some of the major cattle University Press, Ithaca, NY, 941 pp
and poultry pests can cause weight loss, reduced Crosskey RW (1990) The natural history of blackflies. Wiley,
egg and milk production, malnutrition, stam- Chichester, England, 711 pp
Kim KC, Merritt RW (eds) (1988) Black flies: ecology,
pedes, stress-related afflictions, and even death.
population management, and annotated world list.
Humans may develop fever, swollen eyes and Pennsylvania State University Press, University Park,
glands, headaches, nausea, or even more severe PA, 528pp
528
B Black Flies Attacking Livestock: Simulium arcticum Malloch and Simulium luggeri Nicholson & Mickel (Diptera: Simuliidae)

Laird M (ed) (1981) Blackflies: the future for biological allergic reaction can cause death. While S. lug-
methods in integrated control. Academic Press, New
geri do not have toxic saliva, they swarm in huge
York, NY, 399 pp
numbers around the head, causing livestock to
panic, often running into fences and being
injured. Bacteria that cause pinkeye may be
Black Flies Attacking Livestock: transmitted as black flies land to feed near the
Simulium arcticum Malloch and eyes of several hosts.
Simulium luggeri Nicholson &
Mickel (Diptera: Simuliidae)
Biology
peter g. mason
Agriculture and Agri-Food Canada Eastern Simulium arcticum has one or two generations per
Cereal and Oilseed Research Centre, Ottawa, ON, year, and attacks only cattle and related animals.
Canada This species prefers clean rocky locations in large,
fast-flowing, silt-laden rivers such as the Atha-
The livestock-attacking black flies, Simulium arcti- basca River in northern Alberta. Simulium arcti-
cum Malloch and Simulium luggeri Nicholson & cum formerly was the dominant species in the
Mickel, are important pests of cattle and wild Saskatchewan River but because of hydrological
ungulates in the northern great plains of Canada. changes caused by hydroelectric developments it
Other black fly species are pests of vertebrates ceased to be abundant
including humans in other parts of the world. Simulium luggeri has up to five generations
Females of S. arcticum and S. luggeri are greyish or per year and will attack humans as well as cattle.
brownish with the dorsum of the thorax uniformly This species prefers somewhat clear, flowing water
colored. They differ in appearance (the coloration of near the mouth of middle-sized rivers. The
the tibia of the hind leg is entirely dark in S. luggeri, human-induced hydrological changes to the Sas-
but the basal half is white in S. arcticum), and fea- katchewan River drastically reduced summertime
tures of the genitalia. river volumes, effectively modifying it from a fast-
flowing, silt-laden system to a slower-flowing,
clear system. The once deep and turbid river
became shallow, clear and slow flowing. This
Damage encouraged the growth of massive vegetation
beds on previously barren sand bars. This plant
Economic losses occur due to the massive attacks substrate served as suitable attachment sites
by female black flies seeking a bloodmeal needed allowing S. luggeri to replace S. arcticum as the
for production of eggs. Dispersal in search of dominant species. Both black fly species have four
hosts may be 150 km from the rivers where developmental stage, egg, larva, pupa, and adult.
emergence and oviposition take place. In parts The eggs, larvae, and pupae are restricted to rivers
of Saskatchewan and Alberta, black flies are lim- and streams.
iting to cattle production. Cattle harassed by Eggs are tiny and trapezoid-shaped. They are
attacking black flies become frightened and bombed on the water surface by gravid females
bunch together to escape the blood-seeking flying over the river. The eggs sink to the substrate
swarms. The cattle do not feed normally, result- where they become buried and pass the winter. In
ing in reduced weight gain and milk production. spring hatching commences about two weeks after
The saliva of S. arcticum is toxic to cattle and ice breakup.
 Black Flies Attacking Livestock: Simulium arcticum Malloch and Simulium luggeri Nicholson & Mickel (Diptera: Simuliidae)
B 529

Newly hatched larvae drift downriver and Larvicides are more effective than adulticides
attach to substrates such as clean rocks or vege- because larvae are concentrated in a relatively
tation in the swiftest flowing water. Larvae go definable location in rivers or streams and less
through seven instars or growth stages during insecticide is required to kill a substantial number
about three weeks. Larvae of S. arcticum are of pest individuals. Larvicide is only applied when
larger (0.9mm) than those of S. luggeri (0.74.3 and where pest populations are detected. Exclusive
mm). The brown or greenish-grey larvae feed by use of adulticide is ineffective because of the
filtering nutrients from the water using head extreme difficulty in implementing it; it requires
(cephalic) fans or by scraping algae from the sur- repeated (about every 10 days) applications of
face of rocks using their mouthparts. When mature, insecticide spray or fog over large areas of ground
the larva spins a cocoon and pupates within it. in affected communities. In addition, applying
Pupae of S. arcticum have paired respiratory insecticide directly to cattle via backrubbers,
filaments and pupation occurs within a boot- sprays, etc. has to be safe to the animals and
shaped cocoon. Respiratory filaments of S. luggeri consumers of animal products. Control of
pupae are grouped in threes and pupation occurs adults, however, can be useful as an additional
within a slipper-shaped cocoon. After a few days emergency measure, especially on cattle during
the adult escapes from the pupa and floats to the severe outbreaks. Bacillus thuringiensis israel-
surface in an air bubble. ensis is an effective biological insecticide, with
Adult male and female black flies feed on little environmental effect.
nectar and other plant juices to sustain their Disease agents are commonly associated with
energy requirements. Mating occurs soon after black flies but the life cycles are almost completely
emergence, and females of biting species then unknown, so knowledge of agent transmission
seek blood, which is required to produce eggs. between hosts is lacking. Mermithid nematodes
After locating a host, settling on its skin, and are one of the most promising biological control
inserting their blade-like piercing mouthparts, agents for black flies but their commercial devel-
the females suck blood until they become fully opment is hindered by a lack of basic ecological
engorged. After taking the blood meal they have information.
expanded to twice their normal size. Engorged
females seek suitable flowing water habitats in
which they lay eggs on particular substrates. Black
References
flies are active during daylight hours but their rate
of attack is highest during morning and afternoon.
Crosskey RW (1990) Natural history of black flies. British
On cloudy days or when storms are imminent Museum of Natural History, London, UK, 722 pp
black flies may attack viciously at any time of day. Kim KC, Merritt RW (eds) (1987) Black flies: Ecology, pop-
Winds can disperse large numbers of adults from ulation management and annotated world list. The
Pennsylvania State University Press, University Park,
breeding areas to surrounding regions, especially PA, 528 pp
open farmland, and shifting winds may disperse Laird M (ed) (1981) Blackflies: The future for biological meth-
black flies to other districts. Cold or rainy weather ods in integrated control. Academic Press, London, UK,
temporarily ends an outbreak. 399 pp
Mason PG, Shemanchuk JA (1990) Black flies. Agriculture
Canada Publication 1499/E, Minister of Supply and
Service Canada, Ottawa, Ontario, Canada, 8 pp
Management Mason PG, Boisvert M, Boisvert J, Colbo MH (2001)
Simulium spp., black flies (Diptera: Simuliidae). In:
Mason PG, Huber JT (eds) Biological control pro-
Control of black flies attacking livestock is achieved grammes in Canada 19812000. CABI Publishers,
most effectively through use of insecticides. Wallingford, UK, pp 230237
530
B Blackheaded Fireworm, Rhopobota naevena (Hbner) (Lepidoptera; Tortricidae)

Blackheaded Fireworm, Black Pod of Cacao

Rhopobota naevena (Hbner)
(Lepidoptera; Tortricidae) This is an important insect-vectored disease of
cacao.
A caterpillar pest of cranberries in North Transmission of Plant Diseases by Insects
America.
Small Fruit Pests and Their Management
Black Scale, Saissetia spp.
(Hemiptera: Coccidae)
Black Grain Stem Sawfly, Several species of soft scale in the genus Sais
Trachelus tabidus (Fabricius) setia, known as black scales, are pests of citrus
(Hymenoptera: Cephidae) crops.
Citrus Pests and Their Management
This is a pest of wheat in the northern hemisphere.
Wheat Pests and Their Management

Black Scavenger Flies

Members of the family Sepsidae (order Diptera).
Blacklegged Tick, Ixodes
Flies
scapularis Say (Acari: Ixodidae)

This is a common pest of mammals in North

America, and an important vector of Lyme Black Turfgrass Ataenius
disease.
Ticks Turfgrass Insects and Their Management

Blackwelder, Richard Elliot

Blacklight Trap
Richard Blackwelder was born on January 29,
An insect trap used for monitoring flying insects, 1909. His doctoral research was performed at
particularly moths, that come to the ultraviolet Stanford University, California. That research pro-
wavelengths produced by the black light source duced a (1936) monograph Morphology of the
associated with the trap. coleopterous family Staphylinidae in which he
Traps for Capturing Insects acknowledges the help of his advisor, G.F. Ferris,
and of R.E. Snodgrass. This work still is the fore-
most on its subject. Then he published short works
on the systematics of North American Tachypori-
Black Parlatoria Scale, Parlatoria nae (1936, 1938) and Paederini (1939). After
ziziphi (Lucas) (Hemiptera: graduation he became a Bacon Traveling Scholar
Diaspididae) for the Smithsonian Institution (19351938)
during which time he completed a 21-month col-
This is an important pest of citrus crops. lecting trip to many West Indian islands (June
Citrus Pests and Their Management 1935 through March 1937), returning with 50,000
 Blasticotomidae
B 531

specimens mostly collected by hand or with a net. and another Taxonomy in 1967. He died on
This culminated in his (1943) publication of a January 20, 2001.
Monograph on the West Indian species of the
family Staphylinidae, this work, which dealt with
the 91 genera and 468 species known to him, has Reference
not been bettered. In 19381940 he was Assistant
Curator of the American Museum of Natural His- Herman LH (2001) Blackwelder, Richard Elliot. Bull Am Mus
tory, and in 19401954 Assistant and Associate Nat Hist 265:4647
Curator of the Smithsonian Institution. During
these years he published short works on Lispinini
and Osoriinae (1942) and the staphylinid beetles Blaisdell, Frank Ellsworth
of the Cayman Islands (1947), and sundry other
Frank Blaisdell was born in New Hampshire on
papers including, with the help of his wife three
March 13, 1862, and moved with his parents and
supplements to the Leng catalog of North
siblings to California in 1870. Despite lack of a
American Coleoptera. His monumental works
high school education, in 1887 he entered Cooper
were (19441947, 1957) A checklist of the
Medical College in San Francisco, and graduated
coleopterous insects of Mexico, Central America,
two years later with the degree of Doctor of Medi-
the West Indies, and South America and (1952)
cine. He worked in California at first as a medical
The generic names of the beetle family Staphylin-
practitioner, and from 1900 as an academic at
idae. The first of these has been cited in just about
Cooper College and then at Stanford University
every subsequent biogeographic study including
(into which Cooper College was absorbed). Ulti-
neotropical Coleoptera and was of enormous
mately he became Professor of Surgery, from
importance. In the mid-1960s he explained to this
which post he retired in 1927. His hobby for
writer the reason for the much-delayed final part
decades had been the collection and study of
(1957), the bibliography, of the first work: that his
Coleoptera, especially the families Tenebrionidae
card index of bibliographic materials had
and Melyridae. After retirement from medicine he
disappeared during one of his absences from the
worked from the Department of Entomology at
Smithsonian Institution, and he had to rebuild it
the California Academy of Sciences, to which he
from his notes and reconsultation of the literature.
deeded his collection of almost 200,000 specimens.
The second undertaking, generic names, attempted
He published 95 papers in entomology. He died on
to apply the rules of the International Code of
July 6, 1946.
Zoological Nomenclature systematically across
the mishmash of usage; although it shook up the
established usage, it was largely correct and inevi-
table. Then he retired from life as a coleopterist
Reference
and researcher and became a teacher, employed
Mallis A (1971) Frank Ellsworth Blaisdell. In American ento-
first at St. John Fisher College in New York state mologists. Rutgers University Press, New Brunswick, NJ,
(19561958) and then at Southern Illinois Univer pp 278279
sity (19581977). His tremendous energy as a
researcher on Staphylinidae in his early years was
directed elsewhere by the late 1950s, although he Blasticotomidae
remained an active member of the Society of
Systematic Zoologists, published works on A family of sawflies (order Hymenoptera, subor-
systematics in Systematic Zoology and a book der Symphyta).
Classification of the animal kingdom in 1963 Wasps, Ants, Bees and Sawflies
532
B Blastobasidae

Blastobasidae another candidate was elected in 1910 as State

Geologist, Blatchley retired, and spent the rest of
A family of moths (order Lepidoptera). They com- his life working on subjects that appealed to him.
monly are known as scavenger moths. He traveled abroad, within the USA, and fre-
Scavenger Moths quently to Florida where in 1913 he bought a
Butterflies winter residence that later he occupied for
Moths months each year. With Charles Leng, he published
in 1916 Rhynchophora or weevils of northeastern
America; as sole author he published in 1920
Blastoderm TheOrthoptera of northeastern America, and in
1926 Heteroptera or true bugs of eastern North
The layer of cells in an insect embryo that sur- America. His books included several of a less tech-
rounds an internal yolk mass. The cellular blasto- nical nature but including observations on insects:
derm develops from a syncytium by surrounding (1899) Gleanings from nature, (1902) A nature
the cleavage nuclei with membranes derived from wooing at Ormond by the sea, (1906) Gleanings
the enfolding of the surrounding membrane. from nature, (1912) Woodland idylls, (1931) My
nature nook, (1932) In days agone, and (1934)
South America as I saw it. He died in Indianapolis
Blatchley, Willis Stanley on May 28, 1940, surviving his wife, Clara, by 12
years. His collection of insects, including 470
Willis Blatchley was born on October 6, 1859, in holotypes, was given to P
urdue University.
Connecticut, but he grew up on a farm in Indiana
that his parents bought in 1860. In 1879, after tak-
ing a six-week training course, he became a coun- Reference
try school teacher, and it was not until 1883 that
he entered Indiana University, majoring in natural A Mallis (1971) Willis Stanley Blatchley. In: American ento-
mologists. Rutgers University Press, New Brunswick, NJ,
science and graduating four years later. From 1887 pp 272278
to 1894 he worked as head of a high school science
department. In the first four years of that period
he conducted thesis research (a thesis entitled Blattaria
The Butterflies of Indiana) toward an M.A.
degree, awarded in 1891, again from Indiana Uni- An order of insects, also known as Blattodea. They
versity. His third degree was an honorary LL.D., commonly are known as cockroaches.
awarded in 1921 by the same institution. Schools Cockroaches
have long summer vacations, and Willis Blatchley
found summer employment with the Indiana State
Blattellidae
Geological Survey or with the U.S. Fish Commis-
sion. The first employment experience may have
A family of cockroaches (order Blattodea).
helped when in 1894 he won the elected position
Cockroaches
of Indiana State Geologist, and held it for 16 years.
His duties were not just as geologist, but also to
work on natural resources and natural history. The Blattidae
years 19061910 found him working on Coleop-
tera of Indiana as Bulletin 1 of the Indiana Depart- A family of cockroaches (order Blattodea).
ment of Geology and Natural Resources. When Cockroaches
 Blister Beetles (Coleoptera: Meloidae)
B 533

Blattodea the pro-, meso-, and metathoracic tarsi, respec-

tively. The color is variable; though often somber,
An order of insects, also known as Blattaria. They some are metallic. Body hairs often are absent but
commonly are known as cockroaches. Cockroaches sometimes dense. The pronotum of blister beetles
is narrower than the head and thorax. The legs are
long, and the body is unusually soft for a beetle.
Blephariceridae The body is often elongate, with the elytra flared at
the tips. However, body form varies considerably
A family of flies (order Diptera). They commonly and though wings usually are normal, some species
are known as net-winged midges. have short wings and elytra, and are flightless.
Flies The immature display hypermetamorphosis. Ovi-
position takes place on the soil, and young larvae
(triungulins) disperse to feed on grasshoppers
Blind Springtails eggs, or the eggs, larvae and provisions (usually
pollen) of ground-nesting Hymenoptera. Once
A family of springtails (Onychiuridae) in the order attaining a food supply, the larvae lose their
Collembola. mobility. When disturbed, the adults display reflex
Springtails bleeding, wherein cantharidin-containing blood is
released, principally from the femoral-tibilal joints.
Cantharidin is a toxic terpenoid that likely imparts
Blister Beetles (Coleoptera: some protection from predation, though it also
Meloidae) seems to have a role in communication. The bee-
tles also may display death feigning. Cantharidin
Blister beetles are an interesting group of insects,
is produced by larvae, but in the adult stage only
both because of their unusual larval development
by the males. It is transferred to females at mating,
and because of their toxic effects on humans and
and occurs in the eggs.
livestock. They are widely distributed, but are
absent from New Zealand and Antarctica. They
are most abundant in warm, dry climates. They
number about 3,000 species. Their classification is Life Cycle
as follows:
Order: Coleoptera Following is an account of black blister beetle
Suborder: Polyphaga development, which is typical of many species. In
Superfamily: Tenebrionoidae black blister beetle is a single generation per year,
Family: Meloidae with overwintering occurring in one of the larval
Subfamily: Eleticinae instars. The eggs are deposited within a cavity in
Subfamily: Meloinae the soil, in clusters of 100200 eggs. Because the
Subfamily: Nemognathinae likelihood of surviving is so small, blister beetles
Subfamily: Tetraonycinae produce very large numbers of eggs, sometimes up
to 10,000.
The larval instars of black blister beetle are
Characteristics quite varied in appearance, reflecting the unusual
biology of the insect, called hypermetamorphosis.
These are medium-sized beetles (usually 330 Unlike most insects, the ovipositing female does
mm, but some up to 70 mm) with 711 antennal not locate a food source for her offspring, appar-
segments. There are five, five and four segments on ently depositing her eggs randomly. Thus, when
534
B Blister Beetles (Coleoptera: Meloidae)

young larvae hatch they must dig to the surface larvae. Undoubtedly starvation of first instars is a
and disperse to find a host insect on which to feed. very important factor during most seasons, and
The first instar is thus quite mobile, and equipped cannibalism is prevalent among larvae. Antlike
with long legs with which to disperse. First instars flower beetles (Coleoptera: Anthicidae), false ant-
explore cracks, crevices, and depressions in the soil like flower beetles (Coleoptera: Pedilidae), and
as they search to find a host. Usually a single egg is some plant bugs (Hemiptera: Miridae) have been
adequate for complete development of the first implicated as mortality agents of blister beetles. The
instar. The number of instars is normally 67. The larva of the blister beetle Epicauta atrata (Fabricius)
larvae are creamy white or yellowish white in color, has also been shown to be predatory on eggs of
with brown head capsules. After the first instar the E. pensylvanica, and it is possible that other species
larva moves little, and the legs become relatively within the genus are predatory (Fig. 52).
shorter and shorter. The sixth instar does not feed,
instead digging 23 cm into the soil and preparing
a cell. The sixth instar may be followed by another Damage Caused by Blister Beetles
nonfeeding instar, or by the pupal stage. The sixth
and seventh instars bear only minute legs, and the Epicauta spp. and other blister beetles sometimes
head capsule is reduced in size and retracted into feed on crops, though few are commonly destruc-
the body. Black blister beetle larvae consume 2127 tive. In North America, black blister beetle,
eggs of Melanoplus differentialis Thomas during its Epicauta pensylvanica DeGeer, is usually the most
larval development. This grasshopper, and some common species, and occurs everywhere in the
other Melanoplus spp., produces 100 or more eggs, eastern United States and southern Canada west
allowing more than one blister beetle to develop. If to the Rocky Mountains. Immaculate blister bee-
blister beetle larvae encounter one another, how- tle, Epicauta immaculata (Say); spotted blister
ever, they fight and only one survives. Many grass- beetle, Epicauta maculata (Say); and striped blister
hoppers produce small egg pods, with less than 25 beetle, Epicauta vittata (Fabricius), are examples
eggs, thereby limiting the ability of blister beetles to of other common crop-feeding blister beetles
develop. The pupa resembles the adult beetle in Other genera of Meloidae occasionally affect
form, though the legs and wings are folded against crops, but incidents of damage are isolated. Among
the underside of the body, and there appears to be such occasional pests are Linsleya sphaericollis
no tendency for diapause in this stage. The adult (Say) in the Rocky Mountain region and west to
digs to the soil surface after pupation. the Pacific Ocean; Nuttall blister beetle, Lytta
Other blister beetles sometimes require more nuttalli Say, throughout the west and east to
than one year to complete a generation, or are Nebraska; and Meloe niger Kirby, which occurs
multivoltine, depending on the favorability of the throughout the United States and southern Canada
environment. The species feeding on bees differ in except for the southeastern states.
that the eggs may also be deposited on foliage, where Blister beetle adults are found on alfalfa, clover,
the young larvae are phoretic, attaching to adult bees soybean, and sugarbeet, as well as numerous
and are transported back to the nest of the bee. vegetable and flower crops, fruit trees, and broad-
leaf weeds. Adults often collect on goldenrod flow-
ers, Solidago spp., in the autumn. Indeed, flowers are
Natural Enemies often a preferred food of many species. Beetles tend
to aggregate, apparently in mating swarms, so
Surprisingly little is known concerning the natural damage can be severe in relatively small areas of a
enemies of blister beetles, reflecting their minor crop and absent or trivial elsewhere. consumption
status as crop pests and the subterranean habits of of foliage, in some instances they prefer blossoms.
 Blister Beetles (Coleoptera: Meloidae)
B 535

Blister Beetles (Coleoptera: Meloidae), Figure 52 Representative blister beetles: upper left, Epicauta
immaculata; upper right, Epicauta lemniscata; center left, Epicauta pensylvanica; center right, Epicauta
andersoni; lower left, Meloe laevis; lower right, Lytta sp.

Preference of blister beetles for blossoms is the drying and preservation of hay, but also can
most noticeable and potentially damaging in result in death of aggregations of blister beetles,
alfalfa, where beetles congregate mostly during and incorporation of their bodies into the hay.
periods of bloom. Aggregations of beetles can be Blister beetles, even dead individuals, contain a
incorporated into alfalfa hay when it is baled, vesicating substance called cantharidin which,
particularly if the stems are crushed as part of the when ingested, damages the digestive tract of
harvesting process. Crushing, or crimping, aids in animals. Cantharidin also causes blisters to form
536
B Blister Beetles (Coleoptera: Meloidae)

on the skin of sensitive humans who come into during, and immediately after, periods of grass-
contact with crushed beetles, and in formation of hopper abundance. The larvae of many blister
blisters in the mouths of livestock, particularly beetles, however, seem to feed principally on
horses. This blistering action is the basis for the ground nesting bees and the bees nest provi-
common name of the beetles. Cantharidin content sions. Their abundance fluctuates less, and they
varies among species, ranging from 5% cantharadin provide no known agricultural benefits. There is
in Epicauta immaculata to about 1% cantharidin even one instance in Canada where bee-feeding
in E. pensylvanica. Despite the relatively low toxin blister beetles interfered with alkali bees being
content in each beetle, large numbers can be managed for alfalfa pollination.
incorporated into hay, and horses can ingest
enough beetles to cause death. Cantharidin likely
serves as a feeding deterrent to most predators, Management
thereby protecting blister beetles and their eggs
from consumption. However, some insects are Blister beetles are not usually pests, though they
attracted to cantharidin, and this compound is may become quite abundant during and following
involved in the chemical communication among long-term grasshopper population increases.
blister beetles. Suppression of grasshoppers indirectly suppresses
In times past in Europe the so-called Spanish blister beetles by eliminating the food supply of
fly, Lytta vesicatoria, acquired the undeserved the blister beetle larvae. Direct suppression of
reputation as an aphrodisiac for horses. Likely blister beetles usually may not occur in conjunction
ingestion of this insect irritated the animals, mak- with chemical treatment of grasshopper popula-
ing them seem more restless and spirited. Thus, tions because the grasshoppers can occur earlier
the beetle was sometimes administered to horses, in the season, when blister beetles are still in the
and even sometimes to humans, but the effects can soil. Blister beetles are easily controlled by applica-
be quite deleterious. tion of common insecticides to crop foliage, and
small plantings can be protected with row covers
or screening. Because some blister beetle is highly
Beneficial Effects of Blister Beetles attracted to alfalfa, especially during periods of
bloom, large numbers of blister beetles may
The damage caused by Epicauta spp. blister bee- disperse to nearby crops following alfalfa harvest.
tles is offset, at least during periods of relatively Potato Pests and Their Management
low beetle density, by the predatory behavior of Beetles
blister beetle larvae. Epicauta spp. larvae feed on
the eggs of grasshoppers, including many crop-
damaging Melanoplus spp. During periods of References
grasshopper abundance the number of blister
beetles tends to increase substantially. Studies of Bologna MA, Pinto JD (2001) Phylogenetic studies of
egg pod destruction in western areas of the Meloidae (Coleoptera), with emphasis on the evolu-
tion of phoresy. Syst Entomol 26:3372
United States during a period of grasshopper
Pinto JD, Bologna MA (2002) In: Arnett RH Jr, Thomas MC,
abundance, for example, documented that 8.8% Skelly PE, Frank JH (eds) The American beetles, vol 2.
of pods were damaged by blister beetles. CRC Press, Boca Raton, pp 522529
Although the blister beetles eventually contrib- Pinto JD, Bologna MA (1999) The new world genera of
Meloidae (Coleoptera): a key and synopsis. J Nat Hist
ute materially to the suppression of grasshopper 33:569620
population outbreaks, the higher numbers of Selander RB (1991) On the nomenclature and classification of
blister beetles often cause greater crop injury the Meloidae (Coleoptera). Insecta Mundi 5:6594
 Blood Gill
B 537

Blister Beetle Antennal Twisting around the females antennae. The sexual behavior
Behavior of Meloidae has been studied in detail. However,
entwining of male and female antennae has not
yien-shing chow been reported before. The observed frequencies of
National Museum of Natural Science, Taiwan, right-handed and left-handed antennal pairs were
Republic of China 46.713.9% and 44.812.5%, respectively.
Blister Beetles
The blister beetle, Epicauta hirticornis, has an inter-
esting pre-copulating behavior. When a male dor- References
sally mounts a female, the male continuously waves
its antennae toward the females antennae. Eventu- Selander R (1964) Sexual behavior in blister beetles (Coleoptera:
ally, the males right or left antenna, or sometimes Meloidae). I. The genus Pyrota. Can Entomol 96:10371082
both, grasps the corresponding female antennae Pinto JD (1975) Intra-and interspecific courtship behavior in
blister beetles of the genus Tegrodera (Meloidae). Ann
and wraps around the female antennae (Fig. 53). Entomol Soc Am 68:275285
In northern Taiwan, blister beetles usually are
found aggregating on the leaves of blooming
glorybower tree, Clerodendrum cyrtophyllum Blood Gill
Turcz, and a novel sexual behavior was observed.
During their courtship, a male beetle mounts a A gill that lacks tracheae. In such gills, oxygen
female from behind and the males antenna winds passes directly into the blood instead of entering

Blister Beetle Antennal Twisting Behavior, Figure 53 Pre-copulating behavior of the blister beetle
Epicauta hirticornis. (a) A male mounts a female on the leaves of Clerodendrum cyrtophyllum. Their
antennae are twisted to the right. (b) Both male antennae are entwined with the female's antennae;
right-handed and left-handed structures are seen pointing backwards.
538
B Blow Flies

tracheae. Blood gills are found in some aquatic Bluetongue Disease

insects.
Tracheal System and Respiratory Gas Exchange walter j. tabachnick
University of Florida, Vero Beach, FL, USA
Blow Flies Bluetongue disease is an insect transmitted disease
that occurs primarily in sheep and wild ruminants.
Members of the family Calliphoridae (order
The bluetongue viruses that cause the disease are
Diptera).
members of a family of viruses called orbiviruses.
Flies
Although cattle in many regions of the world are
Myiasis
often infected with bluetongue virus, cattle rarely
show clinical signs of this disease.
Blueberry Maggot, Rhagoletis
mendax (Curran) (Diptera:
Tephritidae) Insect Vectors

This is an important pest of blueberry in North Bluetongue viruses can be found in the tropics and
America. subtropics throughout the world. The viruses are
Small Fruit Pests and Their Management transmitted by insect species within the genus
Culicoides, Family Ceratopogonidae. Various
species of Culicoides transmit bluetongue virus.
Bluebottle Flies Different regions of the world contain different
species of Culicoides involved in bluetongue virus
Members of the family Calliphoridae (order transmission. In South America, Culicoides insig-
Diptera). nis is the primary vector of bluetongue virus. In
Flies Africa, the primary bluetongue vector is Culicoides
Myiasis imicola, while in Australia the primary vectors are
Culicoides brevitarsis and Culicoides wadai. The
Culicoides vectors of the bluetongue viruses in
Bluegrass Billbug, Sphenophorus
parts of Asia include Culicoides imicola. However,
parvulus Gyllenhall (Coleoptera:
the Culicoides vectors in large parts of Asia have
Curculionidae)
yet to be identified. Bluetongue virus transmission
does not occur anywhere in the world in the
This is an important pest of turfgrass in North
absence of bluetongue-competent Culicoides vector
America.
species. The primary North American vector of the
Turfgrass Insects of the United States: Biology
bluetongue viruses is a member of the Culicoides
and Management
variipennis complex, Culicoides sonorensis.

Blues
The Disease
Some members of the family Lycaenidae (order
Lepidoptera). The most severe clinical signs of bluetongue
Gossamer-Winged Butterflies disease occur in sheep. Sheep with bluetongue
Butterflies disease show a rise in temperature lasting 5days.
Moths There can be swelling of the buccal and nasal
 Bluetongue Disease
B 539

mucosa, swollen tongue, profuse salivation, hem- has been essentially free of bluetongue virus
orrhages in the membranes of the mouth, and although there have been a few periodic outbreaks
hemorrhages in the bands of the hoof, which often in Spain and Portugal due to Culicoides imicola.
leads to lameness. Sheep may vomit because of Bluetongue outbreaks in sheep in Europe occurred
lesions in the esophagus and pharynx. This sign for the first time in 20012002 in Bulgaria, France
can lead to their aspirating the contents of their (Corsica), Italy (Sardinia) and Greece. The vectors
rumen, in pneumonia and frequently in death. of these outbreaks were not identified, although
Sheep mortality to bluetongue infection may range some appear to have involved Culicoides imicola.
from 5 to 50% of animals infected with virus.
Although clinical signs in cattle are rare, early
prenatal infection with bluetongue in cattle may lead Impact and Problems
to embryonic death. Cattle develop a very prolonged
viremia lasting several weeks where bluetongue The presence of severe bluetongue disease can
virus can be detected in blood and is available to have disastrous consequences on sheep popula-
infected susceptible Culicoides. As a result cattle tions. Consequently, in an effort to reduce the
are considered important reservoirs for the virus potential importation of a bluetongue-infected
and play an important role in infecting susceptible animal and the possibility of a bluetongue out-
Culicoides vectors and therefore in the disease break, many countries impose restrictions on the
transmission cycle in more susceptible ruminants. movement of livestock to their country from any
In the western and southern regions of the United country where bluetongue is prevalent. The Office
States where Culicoides sonorensis is present, there of International Epizootics is the international
are regions where it is not uncommon to find 50% agency responsible for developing regulations to
or more of the cattle to have once been infected with protect animals around the world. This agency
bluetongue virus. These animals are known to have develops regulations for animal trade between
once been infected because they contain antibody countries. In the case of bluetongue, the regula-
to one of the United States bluetongue viruses in tions in place provide for the safe movement of
their blood. The presence of antibody to a virus is livestock from bluetongue areas to bluetongue free
evidenceof a previous infection. areas. For example, the United States, where one of
five bluetongue serotypes may be found in cattle,
has restrictions imposed on its animal export to
The Viruses countries in the European Union that do not have
bluetongue virus. United States animal exports
There are 24 different serotypes of bluetongue virus must be tested and certified as being free of blue-
distributed throughout the world. The viral sero- tongue before they can be approved for shipment.
types are numbered 124 and, as with the different This results in lost trade opportunities for United
species of Culicoides vectors, the serotypes also are States animal exports. The worldwide result is that
found in specific regions of the world. There bluetongue is the cause of non-tariff trade barriers
appears to be an association with the particular costing millions of dollars in testing and lost
Culicoides vector species in a region and the trade opportunities on the international livestock
specific bluetongue virus serotypes found in the market.
geographic region. North America has five blue- The northeastern region of the United States
tongue serotypes (2, 10, 11, 13, 17), Australia has does not contain the bluetongue vector species,
eight serotypes (1, 3, 9, 15, 16, 20, 21, 23), Africa has Culicoides sonorensis. There is no evidence of
21 (119, 22, 24) Central America and the Carib- bluetongue virus transmission to livestock in this
bean region has eight (1, 3, 4, 6, 8, 12, 14, 17). Europe region. Such information is essential to declare a
540
B Boat Flies

bluetongue free region within a country that could very numerous insects is a daunting control chal-
result in improving the livestock trade opportuni- lenge. Outbreaks and problems with bluetongue
ties for the specific region despite restrictions on subside due to weather and climatic conditions
bluetongue transmission regions within the same that naturally reduce Culicoides populations.
country. The economic costs due to bluetongue Culicoides control has not been shown to interrupt
are considerable due to its impact on the interna- bluetongue transmission.
tional livestock market and may approach billions
of dollars.
Several different types of bluetongue virus References
vaccines are available for use in domestic livestock.
Unfortunately, each bluetongue serotype requires a Gibbs EPJ, Greiner EC (1989) Bluetongue and epizootic
specific vaccine for protection. These vaccines have hemorrhagic disease. In Monath TP (ed) The arbovi-
ruses: epidemiology and ecology. CRC Press, Boca
met with varying degrees of success. Some blue- Raton, FL, pp 3970
tongue vaccines are attenuated forms of the virus Tabachnick WJ (1996) Culicoides variipennis and
that were manufactured using techniques to reduce bluetongue-virus epidemiology in the United States.
their virulence in animals. Their advantage is that Ann Rev Entomol 41:2343
Walton TE, Osburn BI (eds) (1992) Bluetongue, African
they can provide protection after a single or booster horse sickness and related orbiviruses. CRC Press, Boca
injection, but unfortunately some have become Raton, Florida, 1042 pp
virulent in the animals or after they have been
picked up by blood feeding Culicoides. Killed virus
as vaccines has been used and these do not become Boat Flies
virulent, but often require more boosters to be
effective. Bluetongue vaccines have been perfected Members of the family Notonectidae (order
using molecular biology technology. Unfortunately, Hemiptera).
the commercial prospects for many bluetongue Bugs
vaccines have not been realized so that there has
been little commercial interest in their develop-
ment and use. In the United States, lack of interest Bodenheimer, Friedrich
in the commercial use of bluetongue vaccines is (Frederick) Simon
due to several factors. Use of bluetongue virus vac-
cines must face the challenge that naturally infected Friedrich Bodenheimer was born in Cologne on
animals must be readily distinguishable from vac- June 6, 1897. He was accepted into medical school
cinated animals. Undistinguished vaccinates would in 1914 in Munich, but soon volunteered for
not be acceptable for international movement, and service in World War I in the German army. He
vaccinated animals should not inhibit or mask served on the eastern front, realized the level of
naturally occurring infection that would prevent anti-semitism that existed, resolved eventually to
the early detection of an outbreak. Since only cattle emigrate to Palestine (now Israel), and decided to
used for export are impacted by bluetongue, there study entomology as a profession that would be
is little economic incentive for using the vaccine on useful in Palestine. He completed his studies at
the large numbers of United States cattle used for Universitt Bonn by 1922, and with a doctorate in
domestic purposes. This reduces the need and philosophy (and specialty in entomology). Before
commercial value for any vaccine. he left for Palestine, he visited the natural history
Although Culicoides control is an option to museum in Hamburg, and chose to spend time
prevent or interrupt a bluetongue virus outbreak in studying Coccoidea. His viewpoint was that every
domestic animals, the biology of these small and entomologist should have a thorough taxonomic
 Bogong Moth, Agrotis diffusa (Boisduval) (Lepidoptera: Noctuidae)
B 541

understanding of one group of insects. His choice Body Lice

of Coccoidea proved appropriate for his future
work in Israel. Next, and still before leaving Europe, Members of the family Pediculidae (order
he spent six months at the R. Scuola Superiore di Phthiraptera).
Agricoltura di Portici in Italy. There, he was able to Chewing and Sucking Lice
study with Grandi and Silvestri, in an environment Human Lice
similar to that of Palestine. He moved to Palestine
in 1922 and took up his appointment as head of
the Division of Entomology (in fact the only ento- Bogong Moth, Agrotis diffusa
mologist) of an Agricultural Experiment station (Boisduval) (Lepidoptera:
(in fact the yard of a high school) in Tel Aviv. Noctuidae)
His first task in Palestine was to inventory the
pest species. He did this as a book (1931) Die In most respects, Bogong moth is a typical cutworm,
Schdlingsfauna Palstinas. In 1923 he married and is one of the more important and widespread
Rachel Ussishkin, and enlisted her help in review- cutworms in Australia. However, it is distinguished
ing pre-Linnean entomological works to produce by its migratory tendencies: dispersal into the
his (19281029) Materialen zur Geschichte der Australian mountains for a period of aestivation
Entomologie bis Linn, a history of entomology. during the summer, followed by dispersal back to
In 1928, he moved to the Hebrew University in the plains in the cooler months. In this respect (as
Jerusalem as professor of zoology and was required well as morphology) it is quite similar to an American
to lecture to students. A difficulty was that he was species, Euxoa auxiliaris (Grote), also known as
required to lecture in Hebrew, that he did not army cutworm. However, bogong moth is an inter-
speak Hebrew, and there were no Hebrew texts for esting and well-known element in the culture of the
the subjects in which he was required to lecture; aboriginal people of Australia, where historically
eventually, he compiled the necessary textbooks, the moths were collected for human consumption,
publishing nine of them (and later four in Turkish so there is an unusual element of cultural anthro-
and one in French). He continued his interests in pology associated with this moth.
agricultural pests and published (1951) Citrus Bogong moth inhabits principally the pas-
entomology in the middle east, and (1957, with E. ture-land west of the Great Dividing Range of
Swirski) The Aphidoidea of the middle east. His eastern Australia (Victoria, New South Wales,
professorship in zoology and acquired knowledge Queensland), but during the summer months the
over 25 years in entomology and broader aspects moths migrate to higher country. In particular,
of zoology induced him to write (1958) Animal they aggregate near Mount Bogong in the Alpine
ecology to-day, in which he emphasized the National Park, which serves as the basis of their
importance of climate. He published more than common name. During the summer, they congre-
420 works. In 1948, although deemed too old for gate in caves and rock crevices until autumn,
military service, he nevertheless served in the when they return to the plains to deposit their
Israeli army, and was twice wounded. He died on eggs. They can accumulate in tremendous num-
October 4, 1959. He was a legendary figure, the bers on the floors and sides of the caves. The
founder of entomology in Palestine (Israel). moths are highly nutritious, and the Aborigines
traditionally have taken advantage of this resource
Reference and collected them by knocking them into bark,
kangaroo skin containers or nets, and then roast-
Harpaz I (1984) Frederick Simon Bodenheimer (18971959): ing them in the hot ashes of a fire to remove the
idealist, scholar, scientist. Ann Rev Entomol 29:123 wings and legs. The moth carcasses were mashed
542
B Bohart, Richard M

together into moth meat, which is said to have a Rocky Mountains. Perhaps the bogong moth also
nutty flavor resembling almonds or walnuts. They sustains itself during the summer by nocturnal
were formed into cakes, and if smoked, preserved feeding.
well for a week or longer. The fat content is 5060%,
and harvest of moths by aborigines early in the
twentieth century is estimated at several tons Economic Importance
annually. Some tribes harvested the moths for 23
months annually, so the moths were a staple of the Although bogong moth is an important food
aboriginal diet, not just a minor component. source for wild vertebrate animals and of the
indigenous people of Australia, it is also consid-
ered to be damaging to some crops. Larvae feed on
a variety of wild broad-leaf herbaceous plants such
Life Cycle and Description as cape weed, Cryptostemma calendula (Asteraceae),
but do not thrive on grasses. Among cultivated
Eggs are deposited at the base of plants near the plants damaged are alfalfa, linseed, cereal grains,
soil in the autumn after moths have descended cabbage, cauliflower, and English peas.
from the mountains. The eggs soon hatch and the These moths also can be a nuisance. Some-
winter months are passed in the larval stage. Lar- times strong wings carry the moths over the
vae initially are cream-colored, but later become mountains to the cities of the eastern seaboard of
green with pale and dark stripes, and dark spots. Australia, and great numbers invade cities such as
Overall, they are dark dorsally and pale ventrally, Canberra, Melbourne and Sydney.
with a dark head and prothoracic plate. They Army Cutworm
attain a length of about 5 cm. They hide in the Native American Culture and Insects
soil during the day, emerging at night to ascend Entomophagy: Human Consumption of Insects
plants and to feed. The larvae mature in spring,
pupate in the soil, and after about a month the
adults emerge to feed on nectar at flowers. The
References
adults are variable in color, ranging from brown
Common IFB (1952) Migration and gregarious aestivation in
to almost black. However, they typically bear a the bogong moth Agrotis infusa. Nature 170:981982
dark streak on each forewing that is interrupted Common IFB (1954) A study of the ecology of the adult
by a light circular spot and a light bean-shaped bogong moth Agrotis infusa (Boisd): (Lepidoptera:
light-colored spot. The hind wing is light brown Noctuidae). Aust J Zool 2:223263
Flood J (1980) The moth hunters. Aboriginal prehistory of the
with a darker border. The wingspan is about 5 cm. Australian Alps. Australian Institute of Aboriginal
The adults migrate to the mountains for the Studies, Canberra, Australia
summer months, returning to the lower pasture-
lands in the autumn. In the mountains, the moths
are reported to fly but not to feed. Interestingly, Bohart, Richard M
the American equivalent of bogong moth, army
cutworm moth, was until recently thought to aes- Born on 28 September 1913 in Palo Alto, California,
tivate during the summer months in the Rocky USA, Bohart became interested in insects as a young
Mountains, where aggregations are fed upon by child, and went on to earn three degrees in entomo
grizzly bears, but not by the indigenous people of logy at the University of California at Berkeley. He
the region. Army cutworm has since been shown taught at the University of California at Los Angeles
to feed at night on flowers at high altitudes of the (UCLA) from 1938 to 1941 before enlisting in the
 Boisduval, Jean-Baptiste Alphonse Dechauffour De
B 543

U.S. Navy. He joined the faculty of the University of him to travel and collect insects. In 1841, he was
California at Davis in 1946 and retired in 1980. appointed head of the entomological section of
Bohart is known for his contributions on the the natural history museum of Stockholm. He gave
systematics of wasps and mosquitoes. He authored his collection to the museum, and during the
over 200 publications, including six books. following 26 years he built the museums collec-
Foremost are Sphecid Wasps of the World (with tions considerably. His greatest published works
A.S. Menke) and The Chrysidid Wasps of the were his descriptions of new species in eight volumes
World (with L.S. Kimsey). Over the years, he of Schnherrs Genera et species curculionidum
acquired an outstanding collection of Nearctic (18331845), his Insecta Cafrariae (18381857)
Hymentoptera. He also acquired a number of and Monographia cassididarum (18541862). He
successful graduate students who went on the published about 50 important papers, and was the
populate museums, state departments of agriculture, describer of the boll weevil, Anthomonus grandis.
and universities. Indeed, his love of students was In 1867 he resigned from his position, but continued
said to be surpassed only by his affection for wasps. to work at the museum until just a few days before
He died on 1 February 2007, but will long be his death in Stockholm on November 2, 1868.
remembered as one of the worlds most important
hymenopterists.
References
Reference Stl C (1869) Notice ncrologique sur C.-H. Boheman.
Annales de la Socit Entomologique de France
9:105106
Garvey KK (2007) Richard M. Bohart. Am Entomol 53:5859.

Bohartillidae Boisduval, Jean-Baptiste

Alphonse Dechauffour De
A family of insects in the order Strepsiptera.
Stylopids Jean-Baptiste Boisduval (Fig.54) was born in
Normandy, France, on June 17, 1799. He was
employed by Dejean as curator of the latters
Boheman, Carl Heinrich insect collection. With Lacordaire as co-author,
he published (1835) Faune entomologique des
Carl Boheman was born in Jnkping, Sweden, on environs de Paris which follows the same
July 10, 1796. From the age of eight, he showed an theme as Fourcroys (1785) work. He became
interest in entomology. He asked permission of his one of the most famous lepidopterists of France,
father to study Latin, because Latin was necessary was one of the original members of the Socit
to read publications on natural history, although Entomologique de France, and an honorary
his father expected him to become a businessman. member in 1866. In 1860 he was awarded
In 1812, he became a student at the university of honorary membership in the Socit Ento-
Lund, and began to study law, but abandoned this mologique de Belgique. He collected not only
in 1813 to enter the Swedish army. His army career Lepidoptera (acquired not only from Europe
gave him spare time for his favorite occupation, but from North America too) but also Coleoptera
entomology, but he retired from the army in 1844 and Hemiptera, and published about 50 works.
with the rank of captain. His army career allowed He died in Normandy on December 30, 1879.
544
B Bokor, Elemr

XI., 1913, and Hrom j vakbogr Magyarorszg

faunjbl. Annales Musei Nat. Hung. XI., 1913). He
fought on the Russian Front in World War I as a
professional officer of the Austro-Hungarian army.
He suffered the life of a prisoner of war in Russia for
some years. On his return to Hungary in 1921 he
researched the arthropod fauna of 102 caves. In
1923 he surveyed the Abaligeti Cave and the result
of this work formed the basis for his doctoral disser-
tation. He received his doctorate in 1924. Elemr
Bokor devoted his life to the research of the Hungarian
caves. He has described several new species of cave
dwelling coleoptera. He was the president of the
Boisduval, Jean-Baptiste Alphonse Dechauffour Hungarian Speleological Society as well as the
De, Figure 54 Jean-Baptiste Boisduval. Entomological Society, providing great impetus to
the work of his colleagues.
His collection of Lepidoptera was sold in France,
his Elateridae are in the Natural History Museum References
(London), and the type specimens of his Curcu-
lionidae in Brussels. Balzs D (1993) Magyar utazk lexikona. Panorma, Budapest,
Hungary
Szkely K (1987) 100 ve trtnt. Karszt s Barlang. Budapest,
Hungary
References

Anon (1880) Jean-Baptiste Alphonse Dechauffour de

Boisduval. Entomologist 13:119
Bolitophilidae
Anon (1880) Dr. Boisduval. Entomologists Monthly Maga-
zine 16:235236 A family of flies (order Diptera).
Essig EO (1931) In A history of entomology. The Macmillan Flies
Company, New York, NY, pp 559562

Boll Rot of Cotton

Bokor, Elemr
This is an insect-transmitted disease of cotton.
george hangay Transmission of Plant Diseases by Insects
Narrabeen, NSW, Australia

Elemr Bokor was born on the 19th of January Boll Weevil, Anthonomous grandis
1887, at Storaljajhely, in the North- Eastern Boheman (Coleoptera:
corner of Hungary. As a young man he was already Curculionidae)
interested in entomology and in the beetles which
lived in caves. Although he received a military This insect, known also as the cotton boll weevil, is
education, he carried on with his nature studies, a very serious pest of cotton in the western
and in 1913 he published some important works hemisphere, and has had a significant effect on the
on the blind cave-dwelling beetles (j vakbogarak history of the United States. Little was known about
Magyarorszg faunjbl. Annales Musei Nat. Hung. it until about 1892 when it appeared in Texas,
 Boll Weevil, Anthonomous grandis Boheman (Coleoptera: Curculionidae)
B 545

aving moved northward from Central America or

h Description and Life History
Mexico. Once it reached the United States, it spread
rapidly to the north and east, and slowly to the Boll weevil is capable of completing its life cycle
west, eventually reaching California in 1982. In the in 25 days, so 810 generations are possible
early part of the twentieth century, little could be annually. The adult stage overwinters, emerg-
done to prevent damage by this insect, and the ing from beneath leaf debris, bark, trash and
agricultural economy of the southeastern United other protected places from March to June. It
States was seriously disrupted by this insect. begins to feed immediately and as squares
Numerous farms, cotton gins and related interests become available they begin production of eggs.
such as stores and banks ceased business because Females can produce from 100 to 300 eggs. The
the cotton crop was destroyed. On the other hand, white eggs are about 0.5 mm long. The eggs
the appearance of boll weevil in the southeast stim- hatch in 34 days, and the larva feeds within
ulated the diversification of the economy because the square or boll. The larva is white and l egless,
the residents could no longer depend exclusively with a brown head. It matures in about 9days
on cotton for their livelihood. Thus, the commu- and measures about 13 mm in length. There are
nity of Enterprise, Alabama erected a statue in rec- three larval instars, which can be distinguished
ognition of the beneficial side effects of this by head capsule width measurements (0.4, 0.6,
devastating pest (Fig. 55). Much later in the cen- and 09 mm, respectively for instars one to
tury boll weevil gained entry to South America. It three). At maturity, it forms a pupa within the
now infests cotton growing regions of Argentina, feeding cavity, and then the adult emerges in
Brazil, and Paraguay. about 5 days. The adult is gray or brown to
black in color, measures about 4 mm in length,
and bears a long snout. In the autumn the
weevils leave the crop for sheltered (Fig. 56)
areas and enter diapause. Diapause is a critical
period for boll weevils, and survival is enhanced
when weather is moister and above average in
temperature.).

Boll Weevil, Anthonomous Grandis Boheman Boll Weevil, Anthonomous Grandis Boheman
(Coleoptera: Curculionidae), Figure 55 Boll weevil (Coleoptera: Curculionidae), Figure 56 Adult
statue in Enterprise, Alabama (photo USDA, boll weevil feeding on a cotton boll (photo USDA,
Agricultural Research Service). Agricultural Research Service).
546
B Bombycidae

Host Plants insects has eliminated boll weevil over much of its
former range. Though initially costly, elimination
Boll weevil feeds exclusively on malvaceous host of this key pest brings substantial savings to gro-
plants, principally cotton but also okra, hollyhock, wers in the long run.
and hibiscus. Area-Wide Insect Pest Management

Damage References
Boll weevils cause injury when the adults chew Hunter WD, Hinds WE (1905) The Mexican cotton boll wee-
into the square (blossom) and boll (fruit) where vil. USDA Bur Ent Bull 51:4546
Hunter WD (1917) The boll weevil problem with special ref-
they feed and deposit eggs. The larvae also feed erence to means of reducing damage. USDA Farmers
within these structures, and little or no fiber is Bull 48:140
formed. Hunter WD (1922) The boll-weevil problem: methods of
reducing damage. USDA Farmers Bull 1262:131
Gaines RC (1959) Ecological investigations of the boll
weevil, Tallulah, Louisiana, 19151958. USDA Tech Bull
Management 1208:120
Palmer JO, Cate JR (1992) Overwintering survival of pre
reproductive and post reproductive boll weevils
Boll weevils are most effectively managed by a
(Coleoptera: Curculionidae) in central Texas. Environ
combination of approaches. Some of the approaches Entomol 21:117120
include:

1. Early destruction of plants in the field. Early har-

vest and destruction of crop residue kills many Bombycidae
weevils and deprives them of shelter.
2. Use of an early maturing cultivar. Early maturing A family of moths (order Lepidoptera). They com-
varieties produce blossoms before many weevils monly are known as silkworm moths.
are present, whereas late maturing varieties are Silkworm Moths
attacked by higher numbers of insects, thereby Butterflies and Moths
experiencing more damage. Proper agronomic
practices also encourage rapid growth and matu-
rity of the crop, hastening development before the
end of the season when weevils are most abun- Bombyliidae
dant.
3. Insecticide. Application of insecticide can allevi- A family of flies (order Diptera). They commonly
ate weevil injury. Applications are made early to are known as bee flies.
control weevils during blossom set and maturity. Flies
Applications may also be made late in the year to
reduce the number of weevils entering diapause,
and thereby reducing the number emerging in the
spring of the following year. Bonnet, Charles
4. Eradication. An eradication program is currently
under way in the United States. A combination of Charles Bonnet was born in Geneva in 1720 and
host destruction, insecticide application, trapping remained in Switzerland all his life. He received
with pheromone-based traps, and release of sterile training in law, and practiced it while deeply
 Borgmeier, Thomas
B 547

c ommitted to biological studies. His sight was said Bootstrapping

to have been so damaged by the age of 25 by his
constant use of microscopes that he could barely A statistical method based on repeated random
read or write thereafter. He was an observer and sampling with replacement from an original
experimenter rather than a taxonomist. In 1745 he sample to provide a collection of new estimates of
published Trait d insectologie, in which his a parameter, from which confidence limits can be
insectes were all the invertebrate animals except calculated.
molluscs, and the work contains results of his
observations on subjects such as parthenogenesis
in aphids, and respiration in caterpillars. His later
books included Contemplation de la nature Bootstrap Values
(twovolumes, 17641765) and Oeuvres d histoire
naturelle et de philosophie (8 volumes, 1779 A measure of the reliability of phylogenetic trees
1783). He died in 1793. generated using cladistic methods.

Reference Boreidae

Tuxen SL (1973) Entomology systematizes and describes: A family of scorpionflies (order Mecoptera). They
17001815. Smith RF, Mittler TE, Smith CN (ed) commonly are known as snow scorpionflies.
History of Entomology. Annual Reviews Inc., Palo Alto,
CA, pp 95117
Scorpionflies

Borgmeier, Thomas
Book-Lice
Thomas Borgmeier was born in Bielefeld, Germany,
Members of the insect order Psocoptera. on October 31, 1892. After graduation from the
Bark-Lice, Book-Lice and Psocids Gymnasium [high school] of Bielefeld, he
emigrated to Brazil and became a Franciscan monk.
From 19121914 he studied philosophy in Curitiba,
and from 19151918 theology in Petropolis. While
Boopidae he was a student, he became interested in entomol-
ogy, in 1917 befriending Hermann von Ihering. A
A family of chewing lice (order Phthiraptera). wealthy industrialist in Rio de Janeiro donated
They sometimes are called marsupial chewing money that allowed Thomas to buy von Iherings
lice. reprint library and a microscope. He was permitted
Chewing and Sucking Lice by the Franciscans to pursue an entomological career.
In 1924 he moved to the Museu Nacional in Rio de
Janeiro, and then transferred to the new Instituto
Biologico in So Paulo in 1928 as assistant in ento-
Boreal mology. In 1933 he retuned to Rio de Janeiro as head
of the entomological section of the Instituto de Bio-
A term used to indicate northern faunal regions, logia Vegetal in the botanical garden. He founded the
though boreal regions can extend southward at journal Revista de Entomologia, and edited and pub-
higher altitudes. lished it until 1951 when financial difficulties ended
548
B Boric Acid

it. Later he founded the journal Studia Entomologica. Normally, boric acid products are active only
About 1973 he retired from entomological activities when insects ingest the material (as a stomach
to a monastery in Rio de Janeiro. During his life, poison), though this can occur during grooming
Thomas published 243 papers on ants and on insects (cleaning the antennae and legs) as well as feeding.
associated with ant nests, especially the dipterous It is used in structures to control such urban pests
family Phoridae. He died on May 11, 1975. as cockroaches, ants, fleas, termites and silverfish.
It may be mixed into bait, particularly for cock-
roach and ant control, and is quite effective. It also
Reference is sprayed onto, or impregnated into, wood for
control of termites and wood boring beetles.
Herman LH (2001) Borgmeier, Thomas. Bull Am Mus Nat Application as a dust into wall voids, attics, and
Hist 265:4849 cracks and crevices harboring insects also is popu-
lar. Because cockroaches spend most of their time
in cracks and crevices, application of boric acid
into such harborages is advisable. The product is
Boric Acid normally blown in with a bulb duster, but must
be finely divided to achieve deep penetration.
john l. capinera Research has shown that crack and crevice treat-
University of Florida, Gainesville, FL, USA ment is superior to broadcast treatment for cock-
roaches. Boric acid is superior to borax for
This inorganic compound contains boron and cockroach control. Although it commonly takes
many other non-volatile elements, and has many several days for cockroaches to die from boric acid
useful properties. The chemical formula is H3 BO3 poisoning, boric acid is especially useful for sensi-
and its sodium salt, or borax, is Na2 B4 O210 H2O. tive areas like schools, pet shops and zoos. The
A more water soluble formulation is Na2 B8 O13 4 slow action can be an advantage for cockroach
H2O, known as disodium octaborate tetrahydrate. suppression because nymphs will feed on the feces
Formulations of borax and disodium octoborate of adults, so boric acid can be transported back to
tetrahydrate usually are known simply as borates. harborages. Similarly, cannibalism of boric acid-
Boric acid is used as a fungicide, bactericide, killed roaches can kill the scavengers.
antiseptic, and as an insecticide, but has several Boric acid is often formulated with diatoma-
other useful properties such as a flame retardant. ceous earth or silica gel (as desiccants) or tricalcium
Normally it is produced from borate minerals by phosphate (to reduce caking). Sometimes other
reaction with sulfuric acid. toxicants are included, including pyrethrins or
From a toxicological perspective, boric acid is sodium fluoride. Dusts can be repellents, and
a relatively nontoxic (to people and pets) insecti- although boric acid dusts tend to have low repel-
cide. Its oral toxicity is reported to be 2,660 mg/kg lency, inclusion of additives in boric acid formula-
in rats. Borax is even less toxic, with oral toxicity to tions increases the likelihood of the product being
rats estimated at 5,600 mg/kg. These chemicals are repellent. Thus, additives should be kept at low
not readily absorbed by skin. However, there is levels. Similarly, when incorporated into bait,
some risk associated with chronic exposure to boric acid concentrations should be kept low (usu-
aerosols, so respiratory protection is advised when ally 1%) so insects will not avoid ingestion. Boric
working around high concentrations. Also, acci- acid is sometimes mixed into cleaning solutions
dental ingestion of large quantities can be lethal. when floor mopping in cafeterias.
Use of goggles and gloves are recommended for Though very persistent and water soluble, boric
those applying these chemicals. acid is not readily impregnated deep into wood, so
 Botanical Insecticides
B 549

although the outside of structural timbers may be Botanical

protected, termites may burrow through incom-
pletely impregnated lumber. Formulations of borates A product derived from plants or plant parts. This
and penetrating agents such as ethylene glycol are term often is used to describe insecticides derived
used to improve wood penetration. The formulation from plants.
can be sprayed or painted onto untreated wood Botanical Insecticides
surfaces, or applied as a foam. Penetration is affected
by a number of factors, including moisture content,
and wood protection is best achieved when the Botanical Insecticides
wood is freshly harvested, or re-wetted to take
advantage of the solubility of the damp wood to murray b. isman
borates. Other factors affecting protection include University of British Columbia, Vancouver, BC,
thickness of the wood and thoroughness of applica- Canada
tion. For deep penetration, injection may be neces-
sary. Existing fence posts, mailbox supports, and Botanical insecticides are those products used to
other wood in contact with soil can be protected by kill or repel insects that consist of dried, ground
drilling a hole and inserting borate gel or rods, then plant material, crude plant extracts, or chemicals
sealing the hole. Boric acid products have herbicidal isolated from plants. The recorded use of plant
activity, however, so vegetation adjacent to treated material or plant extracts for insect control dates
wood can be affected. Overall, boric acid products back at least 200 years. Botanical insecticides were
are very useful for urban pest control, but should be important tools for crop protection prior to the dis-
used as a component of a broader management plan, covery of the insecticidal action of DDT; thesubse-
not as the sole component. quent development of inexpensive and highly
effective synthetic insecticides rendered botanicals
all but obsolete. However, botanicals are enjoying
References renewed interest as the popularity of organically-
grown food increases because botanicals are among
Quarles W (1998) Borates for wood protection. The IPM only a handful of natural insect control products
Practitioner 20(3):112 that can be used in organic agriculture.
Quarles W (2001) Boric acid, borates and household pests.
The IPM Practitioner 23(3):112
Although botanicals are products of nature,
they should not be considered absolutely safe or
non-toxic unless so demonstrated. The active
ingredients in certain botanical preparations used
Boridae as insecticides are relatively toxic to animals and
humans and several are toxic to fish. However,
A family of beetles (order Coleoptera). They com- most are used at very low concentrations of active
monly are known as conifer bark beetles. ingredients, minimizing the risk to humans and
Beetles wildlife from exposure. On the other hand, the
active principles in virtually all botanicals are
rapidly degraded in the environment, often by
Bostrichidae exposure to sunlight, and thus are considered non-
persistent. Apart from this generalization, the few
A family of beetles (order Coleoptera). They com- botanical insecticides in commercial use vary
monly are known as horned powder-post beetles. greatly in their sources, chemistry, toxicity and
Beetles other properties.
550
B Botanical Insecticides

Pyrethrum 1% rotenone at most. Owing to its moderate per-

sistence on foliage (35 days) and chronic effects
Pyrethrum is the most widely used botanical on laboratory animals, there are some concerns
insecticide. It is the oleoresin obtained by solvent about it potential health impacts on humans. It is
extraction of the fresh-picked flowers of the daisy especially toxic to fish, and in fact, more rotenone
Tanacetum cinerariaefolium (Asteraceae), native is used as a commercial fish poison (piscicide)
to the Balkan region of eastern Europe. Most of than for insect control. As a fish poison, rotenone
the world supply of pyrethrum in recent times has has been used for at least 300 years, and at least
come from Kenya, but large scale production is 150 years as an insecticide. In insects, rotenone is a
under way in Tasmania (Australia). The oleoresin slow-acting stomach poison particularly effective
contains six esters with insecticidal properties. against plant-feeding beetles (e.g., the Colorado
The most potent, pyrethrins I and II, typically potato beetle), but much less effective against
make up 20% of the resin by weight. The pyrethrins caterpillars.
are axonic poisons in insects and are characterized
by a fast knockdown time in flying insects. They
degrade rapidly in the presence of sunlight. In Neem
purity, the pyrethins have appreciable toxicity to
mammals, but given their concentration in the Neem is an extract of the seeds of the Indian neem
resin and the dosages normally used, pyrethrum tree, Azadirachta indica (Meliaceae). Native to the
has minimal toxicity to mammals. Pyrethrum is Indian subcontinent, it has been widely planted
a broad spectrum insecticide and has more throughout tropical and subtropical regions of
registered uses (in the U.S.A.) than any other the world. Dried neem leaves have traditionally
insecticide. Most products containing pyrethrum been used in protection against stored product
or pyrethrins as active ingredients are formulated pests. Neem has a diverse array of behavioral and
with a synergist, piperonyl butoxide, that prevents physiological actions against insects, most of
the metabolic degradation of the insecticide within which are attributable to the complex triterpenoid
the insects body, thus increasing potency. The azadirachtin. This chemical is reputed to be the
rapid environmental breakdown of pyrethrum most potent antifeedant to insects (it deters insect
created the impetus for the industrial development feeding in nanogram quantities), but is also a
of the synthetic pyrethroids, now the dominant potent disruptor of the insect neuroendocrine
class of agricultural insecticides. system. The most obvious manifestation of this
latter action is that azadirachtin inhibits the molt-
ing process in insects. As such, azadirachtin is a
Rotenone slow-acting insecticide and requires ingestion to
be effective. Another interesting property of
Rotenone is the ground roots or rhizomes of the azadirachtin is its systemic action in some plants.
tropical legumes Derris (southeast Asia) and Of primary importance, neem and azadirachtin
Lonchocarpus (South America, also known as cube are non-toxic to most non-target organisms,
root), or resins extracted from them. The name is including humans. Like pyrethrum, neem is rap-
also applied to the major insecticidal constituent, idly degraded in the environment by sunlight.
although each plant contains a number of related Neem became commercially available in the
isoflavonoids, most of which are insecticidal. U.S.A. in 1990, and is beginning to gain accep-
Rotenone is a mitochondrial poison in insects and tance for insect control in some agricultural
vertebrates. In purity it is quite toxic to mammals, commodities and especially in organic food
but most home and garden preparations contain production.
 Botanical Insecticides
B 551

Tobacco Schoenocaulon officinale, containing alkaloids that

are axonic poisons. Both are examples of plants
Water extracts of tobacco have been used to kill whose active principles, in purity, are relatively
insects for over 300 years. Nicotine (from Nico toxic to mammals, but for which the actual plant
tiana tabacum, Solanaceae), nornicotine (from preparations used have a wide margin of safety to
N. sylvestris) and anabasine (from Anabasis humans.
aphylla, Chenopodiaceae) are alkaloids that are Essential oils from certain plants have been
highly insecticidal. They poison both insects and used traditionally in some regions as insect
mammals through acommon mode-of-action, by repellents. The best known among these is oil of
mimicking the neurotransmitter acetylcholine citronella, obtained from lemongrass (Cym-
and causing over stimulation of nerve synapses. bopogon nardus, Poaceae), used as an alternative to
Unlike some other botanical insecticides, nicotine DEET for repelling mosquitoes and biting flies. In
is very toxic to humans, and poisoning can result addition, monoterpenes and phenols in clove oil,
not only from ingestion but from dermal expo- thyme oil, and various mint species have been
sure as well. As a consequence, nicotine is rarely recently shown to be insecticidal in a wide range
used for insect control at present, although it is of insects. As a result, several home and garden
still used as a fogging insecticide in some insect control products based on plant essential
greenhouses. oils have been developed and these materials
may have uses in agriculture (e.g., organic farming)
as well.
Other Botanicals Numerous other plant extracts have seen
regional traditional use, especially in developing
Other botanicals have seen some commercial use countries. Insecticides can be made from the seeds
in North America. These include ryania, the of chinaberry (Melia azedarach, Meliaceae), a r elative
ground stem wood of the Caribbean tree Ryania of the neem tree, although in some countries the
speciosa (Flacourtiaceae), containing alkaloids seeds contain substances that are toxic to animals. In
that poison neuromuscular junctions, and saba- the Peoples Republic of China, an insecticide is
dilla, the ground seeds of the South American lily made from the bark of M. toosendan, considered by

Botanical Insecticides, Table 8 Properties of some important botanical insecticides

Property Pyrethrum Rotenone Neem Essential oils Nicotine
Country of origin Kenya, Australia SE Asia, India Worldwide Worldwide
Venezuela
Active ingredients Pyrethrins (esters) Rotenoids Azadirachtin Monoter- Nicotine
(isoflavonoids) (limonoids) penes, simple (alkaloids)
phenols
Formulations Numerous Dusts, WPs ECs Numerous ECs, Dusts
% actives in 6% EC 1% Dust 5% WP 14.5% EC 35% EC 6% 40% EC
formulation Aerosol
Action on pests Contact/knock- Stomach poison/ Stomach Contact/ Contact/
down toxin cytotoxin poison/IGR/ knockdown knockdown
antifeedant toxin toxin
Persistence Very limited Limited Very limited Very limited Limited
Mammalian Minimal Moderate; very Non-toxic Non-toxic Very toxic
toxicity toxic to fish
552
B Bot Flies

some authorities to be taxonomically synonymous Bot Flies

with M. azedarach. The product, Toosendanin, is
reported to be effective against fruit and vegetable Members of the family Oestridae (order Diptera).
pests. The tropical trees Quassia amara and Ailan- Flies
thus altissima (Simarubaceae) contain insecticidal Myiasis
terpenoids that can be extracted from the wood and
used for insect control. Dried leaves of Haplophyton
cimicidum (Apocynaceae) have been used for centu- Bothrideridae
ries in Mexico and Guatemala to prepare cockroach
powder owing to a series of alkaloids in the foliage A family of beetles (order Coleoptera). They com-
of the plant. Seeds of the custard apple (Annona monly are known as dry bark beetles.
reticulata, Annonaceae), sweetsop (A. squamosa) Beetles
and soursop (A. muricata) contain potent insecti-
cidal acetogenins and have been used for insect con-
trol in many tropical countries in the Old and New Boutonneuse Fever
World. The dried, powdered flowers of Rhododen-
dron molle (Ericaceae) have a long history of use as This is a bacterial disease transmitted by ticks.
an insecticide in China. Ticks
Botanical insecticides are unlikely to displace
conventional synthetic insecticides in many pest
management contexts, but they should gain increas- Bovine Babesiosis
ing favor in situations where human exposure is
unavoidable and safety is of primary concern. This is a protozoon disease of cattle transmitted
Botanicals will also see continued use in developing by ticks.
countries where many of the plants from which Piroplasmosis
they are obtained can be readily grown and the
insecticidal preparations are a safer and less expen-
sive alternative to imported synthetic pesticides.
Alleochemicals Bovine Hypodermosis: Phenology
Chinaberry in Europe
Pyrethrum
Persian Insect Powder david reina, javier martnez, eantiago
Neem hernndez, ignacio navarrete
Universities of Extemadura and Crdoba,
Madrid, Spain
References
The life cycle and biology of the warble fly,
Arnason JT, Philogene BJR, Morand P (eds) (1989) Insecti- Hypoderma bovis, and of Hypoderma lineatum,
cides of plant origin. American Chemical Society, exhibit regional and local variation attributable to
Washington, DC, 213 pp
Isman MB (2000) Plant essential oils for pest and disease climatic and weather conditions (Fig. 57).
management. Crop Prot 19:603608 In Andalusia (southern Spain), it is possible
Isman MB (1995) Leads and prospects for the development of to find H. lineatum adults from the middle of
new botanical insecticides. Rev Pestic Toxicol 3:120
February to the beginning of May, first instar larvae
Koul O, Dhaliwal GS (eds) (2001) Phytochemical biopesti-
cides. Harwood Academic Publishers, Amsterdam, The (L1) in the esophagus from April to November, third
Netherlands, 223 pp instar larvae (L3) in the back from the middle of
 Bovine Hypodermosis: Phenology in Europe
B 553

while it is found in the rachis from the beginning

of October until the middle of February. Warbles
Eggs attached are found during much of the year, from October
to hairs in rows to March. In other studies, adults occur between
Adult Larvae March and August (the latter ones probably are
H. bovis), L1 is observed in the rachis and gullet
between July and December, and warbles occur
Migration
between September and February.
Pupa Warble on cattle On the other hand, there are significant
differences in phenology between northern and
southern Spain. In northwestern Spain (Galicia),
it is not possible to observe the first flies until the
Bovine Hypodermosis: Phenology in Europe,
middle of May, but after that they can be seen
Figure 57 Life cycle of Hypoderma spp. on cattle:
until the middle of September. First instar larvae
eggs (a) are deposited on the legs of the host;
are found from the middle of September to the
larvae (b) burrow into the animal and migrate
end of January, or from August to December.
through the animal, eventually reaching the back
Warbles are found from February until May. The
where a swelling (warble) is formed (d); the mature
phenology of Hypoderma in the north of Spain
larva drops to the soil to pupate (e) and an adult
is more similar to the countries of central Europe
emerges from the pupa.
than to the southern areas of the same country.
November to the end of March, and the mature In the central and eastern regions of France,
larva ready to commence pupation from the middle Hypoderma adults and eggs are found between
of January to the end of March. Adults of H. bovis the end of May and the middle of August. First
occur between May and June, L1 from November instars (the period of greatest risk due to local
to January, the period of warbles from mid- and systemic adverse reactions) occur from the
December to May, and the dropping of L3 from middle of August to the end of February. Warbles
mid-March to May. It is possible to find third are found in the backs of hosts during March to
instar larvae of H. lineatum in the back of bovines May, or possibly from March to July. It is likely
from October to early May. Adults are found during that the phenology is intermediate between the
April or May, although in some years some of them countries of central Europe and the southern
can be seen in March. First instar H. lineatum appear in Iberian peninsula. In Switzerland, the phenology
the gullet of bovines between September and is similar to that in France.
December. Hypoderma bovis is scarcer in western In Ireland, there is a delay in the presence of
and southwestern Spain, but display the same phe- warbles. Warbles appear in July and August rather
nology. In some areas of Portugal, such as the than in February and March. Ireland, together
Alentejo and Centro areas, phenology clearly is with the rest of United Kingdom, and also Holland,
similar to that of western Spain, which is logical are examples of locations where Hypoderma are
due to the geographic proximity of these regions. practically eradicated, at least from cattle.
The phenology (Table 9) is very similar in In eastern Europe, specifically Czechoslovakia,
northern Africa. In Morocco, it is possible to find extensive investigations have been conducted on
adults from February to the middle of May, and L3 H. bovis (throughout the country) and H. lineatum
in the back of the hosts from December to April. (in Slovakia). Warbles of H. bovis appear in heifers
In Algeria, adults are found between the end of from the end of March to June, and in cows in May
March and July. The L1 stage can be found in the to June. Dropping of larvae and pupation were
hosts esophagus between August and December, observed from early April to early July, while flies
554
B Bovine Hypodermosis: Phenology in Europe

Bovine Hypodermosis: Phenology in Europe, Figure 58 Warble being removed from beneath the
skin of host.

are present from early June to the beginning of As a general rule, H. lineatum occurs
September. For H. lineatum, the period of warbles e arlierthan H. bovis. The occurrence varies from
was earlier and shorter, from the second half of year to year, however, due to variation in envi-
February to the end of April. Pupation was observed ronmental conditions. They occur earlier when
from the end of March to the end of April, and flies it is warmer in the spring, summer or winter.
from May until the first days of July. Insouthwestern Spain,the mean annualmaximum
In countries such as Poland, warbles (Fig.58) temperatures are 2021C, with maximum sum-
have been detected in February, though normally mer temperatures averaging 2930C, and mean
the warbles do not occur until April.When occurring annual minimum temperatures of 89C. The
early, warbles are found in April, but when found cooler temperatures of eastern and central
normally, the warbles do not occur until May and Europe slow the biology of these pests.
June. It is possible to observe warbles until the end of To avoid damage caused by larvae, knowledge
July. In Romania, the period of activity of adults is of phenology is important. Before beginning a
May to September for H. lineatum, and between management or eradication effort, climatic varia-
August and September for H. bovis. The first warbles tion in Hypodermas must be considered.
produced by the second instar larvae appear in the
southern part of the country at the end of January or
References
early February. In the north, they occur from March
to April. The third stage larvae leave the hosts body
Boulard C, Argent G, Hillion E (1988) Hypodermis bovine:
from late April until the end of July (until August in description et incidence conomique. Le Point Vteri-
the northern part of Romania). Thus, the phenology naire 20 (111):1730
in Romania is similar to central Europe. Sometimes Martnez-Moreno FJ (1992) Estudio inmunolgico de la
hipodermosis bovina. Doctoral thesis. Crdoba, Spain
warbles are found in the back and lumbar regions of Minar J (1993) Cattle hypodermosis, its investigations
the host in September and as late as December; in and suppression in Czechoslovakia. Academia,
these cases the larvae are dead. Praha, 207 pp
 Brachelytry
B 555

Bovine Hypodermosis: Phenology in Europe, Table 9 Comparative phenology (chronobiology) of

Hypoderma species in some European ecological regions
Species Hypoderma lineatum Hypoderma bovis
Region Southwest Central East Southwest Central East
L1 AprilDecember SeptemberMarch September November JanuaryMay OctoberMay
April January
L3 OctoberApril FebruaryMay February December MayJuly MarchJune
April May
Mature JanuaryApril AprilJune MarchApril MarchMay MayAugust AprilJuly
larvae
Adults FebruaryMay MayJune MayJuly MayJune MaySep- June
tember September

Morrondo P, Lpez C, Panadero R (1995) Ciclo biolgico y no such comprehensive study appeared in print
epidemiologa de Hypoderma. Bovis 65:2738 until the second volume of F. C. Stehrs (1991)
Reina D, Martnez-Moreno FJ, Martnez-Moreno A, Molina
JM, Hernndez-Rodrguez S (1994) Present ststus of Immature Insects. Bving died in Washington on
warble fly in Extremadura (South-West of Spain). In: March 16, 1957.
Improvement in the control methods for warble fly in
cattle and goats. Commission of the European Commu-
nities, Brussels, Belgium, pp. 5964
Reference

Mallis A (1971) Adam Giede Bving. In: American entomol-

Bving, Adam Giede ogists. Rutgers University Press, New Brunswick, NJ, pp
431433

Born at Saby, Denmark, on July 31, 1869, Adam

Bving graduated from the University of Copen-
hagen in 1888. His interests included insect larvae, Brachelytry
and those of Donacia (Coleoptera: Chrysomelidae)
were the subject of his Ph.D. research. Then he was pierre jolivet
appointed Assistant Curator of Entomology at the Paris, France
Royal Zoological Museum in Copenhagen, and he
continued to study beetle larvae. Two years after Elytra are characteristic of Coleoptera, and
the death of his first wife, he moved to the United substantial thickening of the first pair of wings
States in 1913 and found employment with the U.S. (elytra) is uncommon among other orders of
Department of Agriculture. His work still revolved insects. The elytra are modified mesothoracic
around beetle larvae, but concentrated on those of wings, normally rigid and fitting over the abdo-
economic importance. He took an American wife men. Brachelytry is the possession of abbreviated
and citizenship. With F. C. Craighead as coauthor, wing covers or elytra. Brachelytrous insects are
he published in 19301931 in Entomologica commonly found among the Coleoptera, including
Americana, the work An illustrated synopsis of the Carabidae, Staphylinidae, Cerambycidae, His-
theprincipal larval forms of the order Coleoptera. teridae, Meloidae and Chrysomelidae. It seems
This major work has been much-cited by later most common among Galerucinae and is unusual
authors for the wealth of its informational content; among Alticinae. Both subfamilies are closely
556
B Brachelytry

related, as part of the Trichostomata. Alticinae, where the elytra become truncated, with the
Galerucinae (both Chrysomelidae) and Bruchidae apical part of the abdomen uncovered, includ
sometimes show only an exposed pygidium, with ing Hydroscaphidae, Histeroidea, Staphylinidae,
only a small shortening of the elytra. Some beetle Nitidulidae, Inopeplidae, etc. In all these groups,
families are exclusively brachelytral, as is the the elytra completely cover the folded wings. In
Lymexylidae, but they fly very well, as do most of some others, such as the myrmecomorph Ceram-
the myrmecomorphic Cerambycidae. Brachelytry bycidae and the Lymexylidae, the wings are left
should not be confused with physogastry (the free without any protection. The adaptive signifi-
swelling of the abdomen to an unusual degree due cance of this feature is not well understood.
to the hypertrophy of fat bodies, ovaries or both), Among the Staphylinidae, the main adaptive
which can result in a similar appearance. In that advantage of abbreviated elytra seems to be a
case, the abdomen is so big that it is protruding greater flexibility in the abdominal region, but
over the end of the elytra. Physogastry is common that does not explain the truncated elytra of
among certain Chrysomelinae (Gastrophysa) and Histeridae. Many beetles with truncate elytra and
Galerucinae (Agelastica) (both Chrysomelidae). with wings completely covered live on the ground,
Brachelytry occurs also in Dermaptera and and are saprophagous. But there are always excep-
Gryllidae. tions; among the Histeridae, for instance, some
Pseudophysogastry (artificial swelling of the genera have the elytra entirely covering the abdo-
abdomen) is also common among cavernicolous men. In the Staphylinidae, usually there are at
or termitophilous beetles. In many Meloidae least four abdominal segments exposed, some-
(Meloe), the elytra appear to fit badly, as among times six. There are, however, some Staphylinidae
physogastric beetles. The elytra overlap but the with the elytra not truncate.
beetle is apterous already as a pupa, as in Timarcha. There are also cases where the elytra are
This means a long history of apterism. In certain abbreviated and do not completely cover the
cases, brachelytry can be seen as a consequence of folded wings. In Atractocerus (Lymexylonidae),
apterism, but many macroelytrous (normal) bee- the elytra are very reduced and dont cover the
tles are alternatively brachypterous or apterous wings. There are also some myrmecomorphic
(Chrysolina banksi), or totally and permanently Cerambycidae, some Cantharidae (Malthinus
apterous (Timarcha). Often, in that case, the elytra and Malthodes), the male of Stylopidae, and
are fused. They are never fused among brache- several Rhipiphoridae, which are more-or-less
lytrous beetles. brachelytrous, with exposed wings. In male
A set of mutations is surely at the origin of Stylopidae, the elytra are peculiarly modified to
brachelytry, but macroelytrous and brachelytrous form balancing organs, like the halters of Diptera.
individuals do not occur in the same species. Often those beetles are free-living and flori-
Brachyeletry is found mostly among mountain- colous. This elytral reduction is increased among
ous or desert frequenting species or genera, but some endogeous Staphylinidae (Leptotyphlinae
also among parasitic species. It seems absent and Osoriinae), where the elytra are reduced to
from arctic species, which would seem to benefit two contiguous scales, covering only the poste-
from protection on the abdomen, though apter- rior thoracic segments and the first abdominal
ism or brachypterism there remains frequent. segment. A similar situation is found among a
Brachelytry is also frequently linked with brachy-or Moroccan Staphylotroglops (Cantharidae). The
apterism, though some brachelytrous beetles reduction of the elytra can also be done laterally,
maintain complete wings and fly very well. revealing the sides of the abdomen (some Cetoni-
Brachelytry is a very old, derived character dae) or be disjunct on the back (Oedemeridae).
(Fig.59). There are a number of beetle families There are also cases where only the females are
 Brachelytry
B 557

Brachelytry, Figure 59 Somes cases of brachelytry (a) Nyctiphantus nocturnus (Semenov). Russia. Tran-
scaspia; (b) Marseulia dilativentris (Reiche). Israel; (c) Theone octocostata (Weise). Tibet; (d) Parageina
andrewesi (Jacoby). India; (e) Galeruca barovskyi Jacobson. Tibet (after Jolivet P (2005) Brachelytry
among Chrysomelidae. Lambilionea 105(3):371384).
558
B Brachelytry

apterous and brachelytrous, as with Metacycla in highlands of South America (Metalepta tubercu-
Central America (Chrysomelidae: Galerucinae). lata). Between 60 and 100 galerucine species in the
Also, the elytra are completely absent in the whole world display brachelytry. Strangely, brache-
females of glow-worms (Lampyridae), Drilidae lytrous forms are extremely rare in South Africa
and some Scarabeidae (Pachypus candidae) and probably absent from Madagascar. Some live
(Fig.60). in India and Malaysia, but generally are linked with
Among the parasites, apterism can be linked mountains. The genus Galeruca, which is essen-
with shortening of the elytra among the females tially palaearctic, has numerous species (nearly 70
(Silphopsyllus), or even among both sexes taxa) from Western Europe to Siberia, China, and
(Platypsyllus) (both Leiodidae). We find also a Japan, and normally is macroelytrous and
total disappearance of elytra among females of macropterous. However, it displays brachelytrism,
Pachypus (Dynastidae), Thylodrias, and Rhipidius joined with brachypterism or apterism, at higher
(Rhipiphoridae). altitudes. It can occur, as Chrysolina, above 5300 m
in China, Himalayas and Tibet and many of those
highland frequenting species are brachelytrous and
all apterous. Very few real brachelytrous Alticinae
Some Examples Among can be quoted: Hespera brachelytra from the Yun-
Chrysomelidae nan mountains, Sjoestedtina fordi, S. montivaga
from mountains in eastern African, though there
Brachypterism or apterism is common among may be more.
Chrysomelidae, whereas brachelytry seems limited Flightlessness and brachelytry generally
to Galerucinae and a very few Alticinae. As far as occur in both sexes. Metacycla is an exception,
we know, macro-brachypterism seems to be with only the female brachelytrous and apterous.
transmitted in Mendelian fashion, when both Flightlessness is favored in females because it
morphologies are present. Brachelytrism is a allows greater allocation of resources to egg pro-
derived character, but mixed forms do not exist. duction (physogastry); however, flight seems
Brachelytrous leaf beetles, which are gener- retained in males because it increases the proba-
ally apterous, are evidently devoid of a subelytral bility of finding a mate. Many brachelytrous
cavity, which exists among many apterous Chry- species walk on the ground and are relatively
somelinae and Tenebrionidae. Probably, this lack polyphagous, like Arima in Europe, Galeruca in
of isolation against cold in mountains or heat and China, Marseulia in Middle East, Metalepta on
UV in deserts is compensated by other means, the Peruvian plateau, or Rupilia in Australia.
such as stronger sclerotizaton of the upper Metacycla occurs in Mexico on Ambrosia ambro-
abdomen (tergites). sioides, a small plant (Asteraceae). In this species,
Brachelytry among Galerucinae is distributed the beetle does not walk on the ground, but the
in the Mediterranean region (Arima marginata, male is flying and active, searching for females.
Galeruca monticola, Marseulia dilativentris); in The female, black in the collections, is red and
mountains or steppe areas of Siberian, Indian and pink in some species when alive and probably it is
Chinese mountains (Theone octocostata, Galeruca an aposematic color.
barovskyi, Paregeina andrewesi, Geinula antennata); A review of the brachelytrous Chrysomelidae
in Australian desert areas, where apterous beetles (Galerucinae and Alticinae) has been made by
are common (Rupilia ruficollis); in the Ethiopian Pierre Jolivet, but due to the numerous galerucine
and East African mountainous areas (Mahutia genera affected, the list is not complete. The
alluaudi); in the Mexican and Central America phenomenon is more frequent among mountain,
dry tropics (Metacycla caeruleipennis); and in the steppe or desert-inhabiting genera and species,
 Brachelytry
B 559

Brachelytry, Figure 60 Some additional cases of brachelytry (a) Galeruca littoralis (Fabricius). South of
France. Pygidium prominent. Winged; (b) Galeruca monticola Kiesenwetter. France: Pyrenean mountains.
Apterous; (c) Arima marginata (Fabricius). South of France. Apterous; (d) Metacycla marginata Chapuis.
Female. Mexico. Apterous; (after Jolivet P (2005) Brachelytry among Chrysomelidae. Lambilionea
105(3):371384).
560
B Brachelytry

mostly in the tropics, but it also exists in temperate ifferent in both families. When the beetles are on
d
areas. Life on the edge has its constraints, but such their back, the staphylinids use their abdomen to
mutants not only survived, but have persisted for a recover and attain their footing, whereas histerids
very long time. Other families like Staphylinidae use their elytral stump. For Degallier (pers.
seem more consistent; only in the Arctic, where comm.), histerid elytra are shortened organs,
many apterous or brachypterous species occur, whereas for staphylinids the elytra could be
brachelytry is absent. Apparently it can be main- vestigial in relation to an elongated abdomen.
tained only under hot or relatively temperate There seems not to be any synapomorphy between
climates. Brachelytry seems ancient and linked to the two groups.
harsh environmental conditions. It is known that Often, brachelytry or apterism are connec
wing atrophy helps the female in producing more ted with a reduced metasternum and various
eggs. That must also be the same for brachelytry. morphological and anatomical correlations
There are many cases where only the female is (timarchisation of Rschkamp, 1927). Among
brachelytrous. We must distinguish between elytra ground Chrysomelidae and others, reflex bleed-
fully developed or truncate (brachelytry), but ing, hoemocoelous toxicity, thanatosis, aposema-
there are degrees between relictual scales (some tism, extra-sclerotization of the abdominal tergites
Staphylinidae) and relative shortening of the elytra. help in protection against predators for those
However, very rarely the elytra disappeared com- wingless and relatively unprotected beetles. Most
pletely. Often scales persist. Among Bruchidae, of those beetles are black, as in Timarcha, but
Alticinae, many Galerucinae, very often the end of some are brilliantly colored. Black for a ground
the abdomen is apparent, but it is not a case of insect can be aposematic on grasses. A set of
brachelytry. mutations should have produced these condi-
Certainly the shortening of elytra helps the tions, and apterism and brachelytry are generally
mobility of the abdomen among the Staphylini- associated with the many usual morphological
dae. Among the Histeridae, the function for trun- conditions.
cated elytra is less clear, but among saprophagous
beetles the wings are always covered. This may be
a necessity in a dirty and humid environment. In
the case of Cerambycidae, mimetism with ants References
could be responsible, but among floricolous groups
the wings can remain free. In many cases, the rea- Beutel RG, Leschen RAB (eds) (2005) Coleoptera, Beetles. I.
morphology and systematics (Archostemata, Adephaga,
son for brachypterism is not clearly understood.
Myxophaga, Polyphaga partim). Walter de Gruyter.
The case of the Metacycla species (Galerucinae) is Berlin, New York, 567 pp
unique, having physogastric, brachelytrous, apter- Beutel RG, Leschen RAB (2005) Phylogenetic analysis of
ous females and, macroelytrous, probably flying Staphyliniformia (Coleoptera) based on characters of
larvae and adults. Syst Entomol 30:510548
males. In some species of this genus, the drawings Crowson RA (1981) The biology of the Coleoptera. Academic
(yellow bands) of the elytra are printed over the Press, London, 802 pp
upper side of the abdomen. In most cases of Jolivet P (2005) Brachelytry among Chrysomelidae. Lambil-
brachyletry, the upper abdomen is strongly sclero- ionea 105(3):371384
Paulian R (1988) Biologie des Coloptres. Lechevalier, Paris,
tized to replace the absence of protection by the 719 pp
lost elytra. Rschkamp F (1927) Der Flugapparat der Kfer. Zoologica.
Brachelytry does not seem to be analogous Stuttgart 28(75):188
Seguy E (1967) Der Flugapparat Kfer. Zoologica. Stuttgart
between the various families of beetles. It has
28(75):188
appeared independently, for instance, among Seguy E (1967) Dictionnaire des Termes Techniques
Staphylinidae and Histeridae. Wing folding also is dEntomologie Elmentaire. Lechevalier, Paris, 465 pp
 Brahmin Moths (Lepidoptera: Brahmaeidae)
B 561

Brachodidae Brackish

A family of moths (order Lepidoptera). They also Saline water with a concentration of salt between
are known as little bear moths. that of fresh and salt water.
Little Bear Moths
Butterflies and Moths
Braconidae

A family of wasps (order Hymenoptera).

Brachycentridae Wasps, Ants, Bees and Sawflies
Natural Enemies Important in Biological
A family of caddisflies (order Trichoptera). Control
Caddisflies

Bradynobaenidae

Brachypsectridae A family of wasps (order Hymenoptera).

Wasps, Ants, Bees and Sawflies
A family of beetles (order Coleoptera). They com-
monly are known as Texas beetles.
Beetles Brahmaeidae

A family of moths (order Lepidoptera) also known

as brahmin moths.
Brachypteridae Brahmin Moths
Butterflies and Moths
A family of beetles (order Coleoptera). They
commonly are known as short-winged flower
beetles.
Beetles Brahmin Moths (Lepidoptera:
Brahmaeidae)

john b. heppner
Brachypterous Florida State Collection of Arthropods,
Gainesville, FL, USA
Having short wings, that do not cover the abdo-
men or nearly so. (contrast with macropterous). Brahmin moths, family Brahmaeidae, are a small
Brachelytry family of 28 species, mostly Palearctic and African.
There are two subfamilies: Dactyloceratinae and
Brahmaeinae. The family is in the superfamily
Brachytosis Bombycoidea (series Saturniiformes), in the section
Cossina, subsection Bombycina, of the division
A bacterial disease of certain Malacosoma Ditrysia. Adults medium size to very large
species (tent caterpillars), caused by Clostridium (50180 mm wingspan), with head vertex rough-
brevifaciens. ened; haustellum average (rarely vestigial); labial
562
B Brain

Brain
The brain of insects consists of three fused gang-
lionic masses: the protocerebrum,the deutocerebrum,
and the tritocerebrum (Fig. 62) (Fig. 63).
Nervous System

Brain Hormone

An earlier name for the hormone that activates

the prothoracic glands to produce molting
Brahmin Moths (Lepidoptera: Brahmaeidae), hormone (ecdysone). It also is known as protho-
Figure 61 Example of brahmin moths (Brahmaeidae), racicotropic hormone (PTTH). The brain is now
Brahmaea wallichii (Gray) from Taiwan. known to produce several hormones with different
functions.
Endocrine Regulation of Insect Reproduction
palpi upcurved or porrect; maxillary palpi vestigial Diapause
or very small (2-segmented); antennae bipectinate;
body robust. Wings broadly triangular but mostly
rounded (rarely with apex somewhat falcate); Brauer, Friedrich Moritz
hindwings rounded (Fig. 61). Maculation mostly
dark browns with numerous scalloped and con- Friedrich Brauer was born in Vienna on May 12,
centric light lines, plus other markings; rarely more 1832. His professional work began as assistant in
colorful. Adults nocturnal. Larvae are leaf feeders. the entomological museum of Universitt Wien,
Host plants recorded in Asclepiadaceae and and he was appointed custodian in 1873. In 1874
Oleaceae. he was appointed professor of zoology in that
university. He became director of the Naturhisto-
risches Hofmuseum and published extensively
References on Neuroptera and Diptera. He died on December
29, 1904.
Chu HF, Wang LY (1977) The Brahmaeidae of China
(Lepidoptera). Acta Entomologicae Sinica 20:8384
Holloway JD (1987). Family Brahmaeidae. In: The moths of Reference
Borneo. Malay Nat J 3:9193, pl 7
Nssig WA, Pauksstadt U (1990) The Brahmaeidae of Sumatra.
In: Heterocera Sumatrana, 6:117136 Poulton EB (1905) Professor Friedrich Moritz Brauer. Ento-
Nssig WA, Treadaway CG (1998) The Brahmaeidae mologists Monthly Magazine 41:7374
(Lepidoptera) of the Philippines. Nachrichten des
Entomologischen Verein Apollo Suppl 17:425440
Rougeot PC (1971) Brahmaeidae. In: Les Bombycoides
(Lepidoptera-Bombycoi dea) de l Europe et du Bassin Braulidae
Mditerranen. In Faune de l Europe et du Bassin Mdi-
terranen, 5: 4659 A family of flies (order Diptera). They commonly
Seitz A (19111928) Familie: Brahmaeidae. In: Die
Gross-Schmetterlinge der Erde, 2:227228, pl. 35
are known as bee lice.
(1911); 10:521522, pl. 56 (1928); 14:349351, pl. Flies
47, 60 (1927) Bee Louse
 Braulidae
B 563

Brain, Figure 62 Lateral view of the insect brain (adapted from Snodgrass, Insect morphology).

Brain, Figure 63 Cross section of an insect brain (adapted from Snodgrass, Insect morphology).
564
B Brentidae

Brentidae biogeography. In: Handbuch der Zoologie. Band IV.

Arthropoda: Insecta. Teilband. W. De Gruyter,
B erlin, 35:217232
A family of beetles (order Coleoptera). They com- Falkovitsh MI (1978) Schreckensteiniidae. In: Identification
monly are known as straight-snouted weevils. keys to the insects of European Russia. 4. Lepidoptera,
2:526529. St. Petersburg: Academie Nauk USSR [in
Beetles
Russian], Russia
Heppner JB (2003) Schreckensteiniidae. In: Lepidopterorum
Catalogus, (n.s.). Fasc. 29. Association for Tropical
Bristle-Legged Moths Lepidoptera Gainesville, FL, 8 pp
(Lepidoptera:
Schreckensteiniidae)
Bristletails (Archeognatha)
john b. heppner
Florida State Collection of Arthropods, This is a primitive order of insects known as
Gainesville, FL, USA Archeognatha or Microcoryphia. The order name is
derived from the Greek words archaios ( primitive)
Bristle-legged moths. family Schreckensteinii- and gnathos (jaw). Because these insects are wingless,
dae, are a small family of only five known spe- and none of their ancestors appear to be winged,
cies (three in North America, one in Central the order is placed (with the order Zygentoma) in
America, and one in Europe). Some place the the subclass Apterygota; in this regard they
family in its own monobasic superfamily, (apterygotes) differ from all other insects.
Schreckensteinoidea. The family is part of the
superfamily Tineoidea, in the section Tineina,
subsection Tineina, of the division Ditrysia. Classification
Adults are small (1012 mm wingspan), with
head smooth-scaled and hind tibiae with long There are about 250 species found throughout the
bristles; haustellum naked; maxillary palpi world
minute, 1-segmented. Maculation is lustrous in Class: Insecta
shades of gray or brown, with reduced vena- Apterygota
tion and long hindwing fringes. Adults are Order: Archeognatha
diurnal. Larvae are leaf skeletonizers on Anac- Family: Machilidae
ardiaceae or Rosaceae. The family and nomi- Family: Meinertellidae
nate genus Schreckensteinia are named after
the German lepidopterist and coleopterist,
Baron Friedrich Roth von Schreckenstein Characteristics
(17531808).
Like other insects (but unlike some similar-ap-
pearing wingless animals such as diplurans, order
References
Entotrophi, and proturans, order Protura), the
mouthparts are external (ectognathous). They also
Buszko J, Skalski AW (1980) Schreckensteiniidae. In: Klucze
do Oznaczania Owadw Polski. 27. Motyle Lepi- lack metamorphosis; they do not change in form
doptera, 23:3236. Polskie Towardzystwo Entomologic- as they molt, only increase in size. The number of
zne [in Polish], Warsaw molts is considerable; 2070 have been reported.
Dugdale JS, Kristensen NP, Robinson GS, Scoble MJ
They can live from 1 to 4 years.
(1999) The smaller Microlepidoptera-grade super-
families. In: Kristensen NP (ed) Lepidoptera, moths Bristletails are small, measuring 1012 mm in
and butterflies. vol 1: Evolution, systematics, and length. The body is cylindrical, but somewhat
 Bromeliad Fauna
B 565

attened. The thorax is strongly arched, resulting in

fl Broadleaf Plant
a hump-backed appearance. Bristletails have large
compound eyes that are almost touching, and also One of the major plant groups, with net-veined,
ocelli. They are covered with scales, and their color is broad leaves. Synonymous with dicotyledonous
gray, whitish, or brownish. The mandibles are long. plants. (contrast with grass).
The body segments are well-defined, including the
three thoracic segments. The tarsi have three seg-
ments, the abdomen 11. The abdomen bears a long Broad Mite, Polyphagotarsonemus
median apical filament (a tail-like structure) and latus (Banks) (Acari:
two shorter lateral cerci. The antennae are fairly long, Tarsonemidae)
and least half the length of the body, and filiform.
This mite affects several important crops.
Citrus Pests and Their Management
Biology Vegetable Pests and Their Management

Bristletails are nocturnal, and hide during the day

is such cryptic habitats as leaf litter and decaying
Broad-Shouldered Water Treaders
logs. Some frequent the shorelines water bodies,
particularly among rocks near the shore. They are Members of the family Veliidae (order Hemiptera).
known for their ability to leap. Bristletails feed on Bugs
algae, lichens, and plant debris. Bristletails do not
copulate. They transfer their sperm indirectly by
suspending droplets of sperm on strands or
Broad-Winged Damselflies
threads, which are taken up by the female.
A family of damselflies in the order Odonata:
References Calopterygidae.
Dragonflies and Damselflies
Arnett RH Jr (2000) American insects, 2nd edn. CRC Press,
Boca Raton, FL, 1003 pp
Remington CL (1954) The suprageneric classification of the Broad-Winged Thrips
order Thysanura (Insecta). Ann Entomol Soc Am
47:277286
Wygodzinsky P (1987) Order Microcoryphia. In: Stehr FW Members of the family Aeolothripidae (order
(ed) Immature insects, vol 1. Kendall/Hunt Publishing, Thysanoptera).
Dubuque, Iowa, pp 6870 Thrips

Broadcast Application
The application of a material such as an insecticide
Bromeliad Fauna
to the entire surface of a field.
j. howard frank
University of Florida, Gainesville, FL, USA
Broad-Headed Bugs
Bromeliads are a family (Bromeliaceae) of mono-
Members of the family Aldyidae (order Hemiptera). cotyledonous plants with about 2,500 described
Bugs species assigned to about 60 genera. Almost all of
566
B Bromeliad Fauna

them are native to the neotropics, but the range of Some authors define tank bromeliads as those
a few extends farther north. Sixteen species are that have a central water-impounding tank, perhaps
native to southern Florida, three of which attain surrounded by additional water-impounding axils.
northern Florida, and one of these reaches Others include any bromeliads that impound water
southeastern Virginia (USA). Many bromeliad in their axils, even if the water is distributed among
species are epiphytic whereas others are terrestrial. many axils. The latter position is adopted here for
Roots of those that are epiphytic do not penetrate convenience, not because the concept has greater
their tree hosts, and serve as holdfasts rather than merit.
nutrient-absorbing structures. Thus, minerals are One bromeliad species, Ananas comosus L.
absorbed through the leaves, not the roots, and the (pineapple), is a very important agricultural crop
plants are not parasitic. In contrast, roots of in tropical countries worldwide. A few other species
ground-dwelling bromeliads may absorb minerals. are grown locally in the neotropics to provide food
Some bromeliads that grow on the ground dwell or drink (e.g., Bromelia pinguin L. and Puya
on rock surfaces (are saxicolous), some in arid raimondii Harms) or fiber (e.g., Aechmea magdale-
habitats and others in marshy soils. Some major nae (Andr) and Neoglaziovia variegata (Arruda
genera are Aechmea, Billbergia, Brocchinia, Brome- da Camara)). Bromelain, extracted from pineapple
lia, Catopsis, Cryptanthus, Dyckia, Guzmania, fruits, has pharmaceutical use as an anti-inflam-
Hechtia, Hohenbergia, Neoregelia, Nidularium, matory, and is also used as a meat-tenderizer. There
Pitcairnia, Tillandsia, and Vriesia. is widespread harvesting of bromeliad inflorescences
A remarkable feature of many bromeliad from the wild as decoration for churches on
species in many genera is the ability to impound religious holidays in neotropical countries. Very
water in the leaf axils. Water thus impounded is many species and cultivars and hybrids are grown
rainwater, or rainwater enriched with nutrients as ornamental plants especially in Europe and
leached from tree canopies (throughfall). Large North America.
specimens of many species may impound sub- Bromeliads are used in four ways by animals.
stantial volumes of water, up to many liters. First, the habitat formed by bromeliad phytotelmata
Depending upon architecture of individual species, is exploited by some aquatic animals as aquaria.
each of many axils may hold a separate small pool Second, some small animals live permanently or
of water, or the axils may combine to form a central almost so in the non-water-holding axils of bro-
tank. These pools of plant-impounded water are meliads, the terraria. Third, bromeliads are used
called phytotelmata. They serve to provide a as an occasional place of concealment or hunting
reservoir of water for absorption by the plant. grounds, or the impounded water is used as a
Bromeliads under tree canopies contain fallen, source of moisture, by some terrestrial animals,
decomposing leaves and seeds and twigs of trees. so these animals are visitors. Fourth, the bromeli-
These decomposing materials provide nutrients ads are eaten by some terrestrial animals. Insects
that can be absorbed by the bromeliad (dendro- exploit the plants in all four ways, and among the
philous nutrition). Decomposition is caused by insects using each way are specialist species
fungal and bacterial action, and by aquatic which have no other means of e xistence or habitat.
invertebrate animals. Bromeliads not under tree Bromeliads are therefore essential to the existence
canopies depend on inputs of wind-blown nutri- of many insect species. Many other invertebrate
ents (anemophilous nutrition). Typically, algae use animals and a few vertebrates also play a role.
these wind-blown nutrients and a food chain Additionally, there are three ways in which
depends upon consumption of algae. Epiphytic bromeliads exploit animals: first, as dispersers of
bromeliads that lack tanks are said to be aerobic, seed; second, as pollinators; and third, as food
and have in the USA been labeled as air plants. (carnivory).
 Bromeliad Fauna
B 567

Aquatic Animals Using Bromeliad genera Metacypris, Candonopsis, and Elpidium.

Phytotelmata as Habitat for their The first to be described was Metacypris
Immature Stages bromeliarum Mller, from Brazil. Others have
been found in Colombia, Costa Rica, Jamaica,
The account below is not intended as a catalog, Mexico, Puerto Rica, and Florida. Some are
and it omits some groups and mentions few of the known from no habitat other than bromeliad
individual species. phytotelmata.
Cyclopoid and harpacticoid copepods have
been found in bromeliad phytotelmata in sev-
Rotifera
eral neotropical countries and at least some of
them are specialists to that habitat. The finding
Rotifers (wheel animalcules) dwell in many fresh-
of one of the harpacticoid species (Phyllogna-
water habitats, and some of these habitats are bro-
thopus viguieri Maupas) in cultured bromeliads
meliad phytotelmata. The earliest mention of a
in Indonesia and the United Kingdom, and
rotifer in bromeliads was in Costa Rica in 1913.
another (Attheyella aliena (Noodt)) in G ermany
The most thorough study to date was made in
suggested that these organisms had been trans-
Jamaica in the early 1990s, when 41 of the 211 spe-
ported in horticulturalspecimens. A cyclopoid
cies reported from Jamaica were documented
species, Bryocyclops anninae Menzel, also was
from bromeliads. They belong to 12 genera includ-
found in a botanical garden in Indonesia,
ing Lecane, Lepadella, and Cephalodella.
although its occurrence in Puerto Rico suggests
the latter locality or a wider area of the West
Annelida Indies is its origin.
Cladocera are rare inhabitants of bromeliad
An aquatic oligochaete worm, Dero superterrenus phytotelmata; they are represented only by
Michaelsen, was first detected and described from Daphnia ambigua Scourfield in Jamaica and Alona
Costa Rican bromeliads and found to be an bromelicola Smirnov in Nicaragua. Sesarma and
obligate bromeliad inhabitant. Later, it was found Metopaulias are genera of crabs. Sesarma angusti-
to be quite widespread in neotropical countries. pes Dana was described from Brazil (later detected
The mystery of how it manages to distribute itself in Trinidad), and Metopaulias depressus Rathbun
among epiphytic bromeliads when it seems from Jamaica, both in the nineteenth century. They
limited to the aquatic environment of bromeliad reproduce only in the habitat provided by bro-
axils was solved when worms were seen to be meliad axils, and M. depressus provides maternal
attracted to bromeliad-dwelling frogs. Quite sim- care to its brood. The crabs are able to climb trees
ply, the worm is phoretic on the moist skin of frogs. to distribute themselves from bromeliad to
This method phoresy, or hitching rides has bromeliad.
been detected in other aquatic invertebrates having
limited mobility. In contrast, the aquatic insects
present in bromeliad phytotelmata have winged Acari
adults, so their ability to disperse is assured.
Arrenurus andrewfieldi Orghidan & Gruia is an
aquatic mite known from axils of Aechmea aquilega
Crustacea in Venezuela. Other aquatic mites of the same
family (Arrenuridae), and some attributed to the
Ostracods (seed shrimps) found in the water in family Anoetidae, have been reported from
bromeliad phytotelmata include species of the bromeliad phytotelmata in other countries.
568
B Bromeliad Fauna

Odonata strictly aquatic larvae (Odonata, Plecoptera, and

Trichoptera) are represented in bromeliads in neo-
Larvae of dragonflies and damselflies are aquatic tropical countries.
and predatory. They have well-developed legs and
thereby are able to climb out of the water from one
leaf axil and into the water in another. At least 12 Diptera
species are now reported to have been detected in
bromeliad phytotelmata in neotropical countries, It is the order Diptera (flies) which has the record
and some of them appear to be specialists to this forthe largest number of families (at least 15) and
habitat, having been found nowhere else. These species (hundreds) with aquatic larvae reported
specialists are all species of damselflies, especially from bromeliad phytotelmata. They include lar-
of the genus Leptagrion. vae of Tipulidae, Anisopodidae, Sciaridae, Ceci-
dodomyiidae, and Psychodidae. They include
Ceratopogonidae whose adults are important in
Hemiptera pollination of cacao, case-making and non-case-
making larvae of Chironomidae. They include
Aquatic Hemiptera are represented by eight Tabanidae, Stratiomyiidae, Phoridae, Syrphidae,
species of seemingly obligate bromeliad-dwellers Borboridae, Aulacigastridae, and Muscidae.
in the family Veliidae (sometimes called broad The family Culicidae (mosquitoes) is espe-
shouldered water striders). Four belong to the cially well represented, with well over 200 species
genus Paravelia and four to Microvelia. That reported in the literature. Furthermore, a few of
these genera belong to separate subfamilies sug- these mosquitoes are among the best studied
gests that adaptation to the bromeliad habitat denizens of bromeliad phytotelmata. This began
occurred independently at least twice. Veliids with the realization that the subgenus Kerteszia of
are predators. the genus Anopheles contains several species which
develop only in bromeliad phytotelmata, and
Kerteszia adults are important vectors of malaria.
Coleoptera Studies in Trinidad in the late 1940s were followed
by studies in the Brazilian state of Santa Catarina,
Larvae of three families of water beetles have been and were aimed at preventing transmission of
found in bromeliad phytotelmata in neotropical malaria to workers on cacao plantations and in
countries. The families are Dytiscidae and Hydro- urban areas surrounded by forest. Unfortunately,
philidae (both with predatory larvae), and Scirtidae the simplest solution appeared to be destruction
(once known as Helodidae or Cyphonidae) with of bromeliads, and in southern Brazil this took the
larvae believed to be filter-feeding detritivores. form of deforestation of a cordon sanitaire
around urban areas. Public health workers seem to
have adopted a concept that bromeliads are a
Trichoptera major source of mosquitoes transmitting diseases.
Thus, when Old World forms of dengue fever were
Larvae of most caddis flies live in freshwater detected in the Neotropics, beginning in the late
streams. One species, Phylloicus bromeliarum Ml- 1970s and with continuing problems, public health
ler, has adapted in Brazil to the habitat provided by workers targeted bromeliads as a source of the
bromeliad phytotelmata. From Costa Rica there is vector mosquitoes (Aedes aegypti (L.) and, begin-
a record of a stonefly (Plecoptera) in bromeliad ning in the late 1980s, Aedes albopictus (Skuse)).
phytotelmata. So all three insect orders with That concept is almost wholly erroneous, because
 Bromeliad Fauna
B 569

these species of Aedes mosquitoes rarely develop Thus, the presence of the mosquito larvae is
in bromeliad phytotelmata. Likewise, public health helpful to the bromeliads, and the bromeliads
workers in Florida have erroneously targeted provide a habitat for the mosquito larvae, so this
bromeliads as a source of the Culex mosquitoes is a symbiosis. These mosquitoes are not known
that transmit West Nile virus in the USA, although to transmit any diseases to humans, although they
such larvae of such mosquitoes rarely develop in take human blood as well as the blood of other
bromeliad phytotelmata. vertebrates such as rabbits. They are viewed by
In Florida, larvae of two mosquito species, humans as pests. The most appropriate long-term
Wyeomyia mitchellii (Theobald) and W. vanduzeei solution to their population control is biological
Dyar & Knab, are highly adapted to existence in control by competition. Such biological control
the water in bromeliad leaf axils. Typically, few of would introduce organisms that would compete
them survive to adulthood because of food for nutrients with the mosquito larvae. Such
shortage. Thus, they compete with each other in competitors would probably be neotropical species
scramble competition, and they are adept at of non-biting midges such as Chironomidae. Use
sequestering the small amounts of food available. of predators against the mosquito larvae would
They are able to survive weeks of starvation which likely provide no solution at all, because survivors
non-specialist mosquito larvae are unable to do. of predation would inherit the food resources and
This also allows them to out compete larvae of thus develop faster and produce larger and thus
other mosquitoes that from time to time occur in more fecund adults (Fig.64).
bromeliad axils. Females of these mosquitoes have
color vision and select light-colored (light green)
oviposition sites, in contrast to the dark-colored Anura (frogs)
sites (preferably black) typically selected by tree
hole-inhabiting mosquitoes. Females hover over Tadpoles belonging to at least five frog genera:
bromeliad axils while ovipositing. When they are Dendrobates (Dendrobatidae), Anotheca, Hyla, and
not ovipositing or blood-feeding, they may be Sphaenorhynchus (Hylidae), Syncope (Microhyli-
found perched on the trunks of trees harboring dae), and Eleutherodactylus (Leptodactylidae)
bromeliads. Males perform up-and-down flights have been reported from bromeliad phytotelmata.
over small areas of tree trunks when searching for Adults of Physalaemus spiniger (Miranda-Ribeiro)
females. Eggs of W. vanduzeei are made excep- (Leptodactylidae) may deposit their eggs in foam
tionally buoyant by having a wax-like coating of nests in bromeliad axils in Brazil, but the tadpoles
minute mushroom-shaped structures that trap a develop elsewhere. In contrast, tadpoles of
plastron of air; they float vertically at the water Dendrobates pumilio Schmidt in Central America
surface and may even be washed out of bromeliad are carried up trees to bromeliads on the backs of
axils during heavy rain. In contrast, the eggs of parents, and the tadpoles develop in bromeliad
W.mitchellii are coated only with a thin layer of a axils feeding on nutritional eggs provided by the
greasy substance, are less buoyant, and they float female. Regrettably, the bright colors of many
horizontally. Larvae depend upon input of dead dendrobatid frogs (poison-arrow or poison-dart
leaves, twigs, and seeds that fall into bromeliad frogs) has made them popular in the pet trade, no
axils from tree canopies above and are decom- matter that they are poisonous. To supply the pop-
posed by fungal and bacterial action. Further ular demand to keep such frogs in aquaria with
breakdown of the organic particles and probably bromeliads, hunters have plundered them from
digestion of bacteria and fungi in the guts of mos- their natural environment. Consequently, and
quito larvae make the nitrogenous content more because of habitat loss, D. pumilio is listed in the
rapidly available for uptake by the bromeliads. IUCN Red Book as a threatened species. Other
570
B Bromeliad Fauna

Bromeliad Fauna, Figure 64 Schematic representation of a mosquito and a bromeliad: (a) Female
Wyeomyia mosquito hovering over a Tillandsia sp. leaf axil while ovipositing. (b) Male Wyeomyia
mosquito performing up-and-down flight over a small area of a tree trunk while searching for females.
(c) Schematic showing how Wyeomyia vanduzeei eggs may be washed out of Tillandsia bromeliads
during heavy rain. (d) Schematic showing how leaves and seeds from tree canopies fall and are trapped
in bromeliad leaf axils, forming the basis of a food chain. Drawings by John Stark.
 Bromeliad Fauna
B 571

strange development is exhibited by tadpoles of Ants may nest in bromeliad terraria. Some
Syncope antenori Walker, which develop in the leaf belong to species that also nest on the ground.
axils of a Guzmania bromeliad in Ecuador. Here, Some belong to species that typically are arboreal,
the tadpoles are born with yolk-filled gastrointes- nesting in hollow twigs and branches. Some
tinal tracts, and are able to complete their develop- b romeliad species in the genus Tillandsia
ment without feeding. (e.g., T. paucifolia Baker) have inflated leaf bases
providing cavities protected from rain, and the
cavities thus formed are often occupied by ants.
Terrestrial Animals Using The ants may cut a small hole in a leaf base for
Bromeliad Terraria as Habitat ease of access to the cavity. Investigation may
for their Immature Stages reveal whether such bromeliads and their ant
tenants participate in a mutualism in which the
Bromeliad terraria are the leaf axils that cannot plants also benefit.
impound water because they leak. Instead, they
accumulate moist organic materials. Typically,
inner axils form phytotelmata whereas outer axils Terrestrial Animals Using
form terraria. We may also consider the upper Bromeliads as Occasional Habitat,
parts of those water-impounding axils that are the Visitors
choked with fallen plant debris as terraria. Brome-
liad terraria provide habitat for some specialist These visitors are here defined as animals that
organisms and many generalists. neither eat nor reproduce in bromeliads. They may
Beetles of the genus Platynus (Coleoptera: be hunting for prey, they may be seeking moisture or
Carabidae) typify this group. Among the several concealment from enemies, or they may be present
hundred species of this genus, some have specialized just because their wanderings have taken them there.
to existence in leaf axils of epiphytic bromeliads, and In Brazil and elsewhere, adult frogs seek refuge
their adults and immature stages occur nowhere during the daytime in bromeliads. Such vertebrates
else. Although their food has not been investigated, differ from bromeliad specialist frogs found in some
they are most likely predatory in concordance parts of the tropics in that their tadpoles develop in
with their closest relatives. So bromeliads serve as other kinds of habitats. But perhaps because of the
hunting grounds for their adults and larvae. These presence of frogs (potential prey), bromeliads are
bromeliad specialists occur in Mexico, Central visited by snakes and other frog-eating vertebrates.
America, and the West Indies. Birds may find drinking water there. In tropical areas
In eastern Brazil, a scorpion Tityus neglectus with pronounced wet and dry seasons, more indi-
Mello-Leito (Buthidae) and a tarantula spider viduals and species of insects may be present in
Pachistopelma rufonigrum Pocock (Therophosidae) bromeliad leaf axils in the dry season, when brome-
have been found so often in terrestrial water- liads provide oases of moisture as well as prey for the
impounding bromeliads that their association seems predators among these insects.
to be obligate. Both are predatory. In Brazil, the spider
Psecas chapoda (Peckham and Peckham) (Salticidae)
reproduces only on the non-water-impounding Bro- Terrestrial Animals Eating
melia balansae Mez. In the southern USA, one spider Bromeliads
Pelegrina tillandsia Kaston (Salticidae) is constantly
associated with the atmospheric epiphytic bromeliad Bromeliads in greenhouse cultivation seem more
Tillandsia usneoides (L.) although the growth form of often to be attacked by scale insects than by insects
the plant does not provide terraria. of any other group, and this may be an artifact due
572
B Bromeliad Fauna

to crowding of plants under unnatural conditions were classified within the family Curculionidae,
that exclude organisms which could control these but recently the part of that family containing
pests. In Florida, these scale insects belong to the Cactophagus and Metamasius has been considered
following six families (numbers of species in a separate family (Dryophthoridae). It is unclear
parentheses): Asterolecaniidae (2), Coccidae (1), whether any of them is a substantial pest in its
Ortheziidae (1), Pseudococcidae (6), and Diaspi- native ecosystem. However, some of them cause
didae (8). They can be controlled by chemical substantial damage to cultivated pineapples in
pesticides or, perhaps, they may be controlled by agro-ecosystems. One of them, Metamasius calli-
opening greenhouse walls to allow ingress of tiny zona Chevrolat, which is native to southern Mex-
parasitoid wasps (if the greenhouse is in a tropical ico and Guatemala, also causes enormous damage
or subtropical area), or by deliberate release of to Floridas native bromeliad populations after
such wasps purchased from biocontrol supply having arrived as a contaminant in one or more
companies (none of the necessary wasp species shipments of ornamental bromeliads. A biologi-
seems now to be available commercially, but this cal control project against M. callizona is in prog-
could change if there were demand). ress in Florida with intent to reduce its populations
Among pests of fruits of cultivated pineapple, (not eradicate them as is sometimes misstated by
the most widespread miner is the larva of a the news media); the objective of biological con-
butterfly, Strymon (=Thecla) basilides (Geyer) trol is not to eradicate.
(Lepidoptera: Lycaenidae). Perhaps it also attacks Insects that have specialized to eat the leaves of
fruits of wild pineapples and perhaps other bromeliads by chewing the surfaces or by mining
members of the genus Ananas. are surprisingly few. They include a few leaf beetles
Insect larvae that mine stems of bromeliads (Coleoptera: Chrysomelidae) such as Acentroptera
include Castniidae and Acrolophidae (Lepi- basilica Thomson and A. pulchella Gurin Mneville
doptera) and Curculionidae and Dryophthoridae in southern South America, the abovementioned
(Coleoptera). The castniid species concerned seem adult weevils (Coleoptera: Dryophthoridae and
not to have been identified to species level, but Curculionidae), a few caterpillars such as Napaea
have been detected by this writer in bromeliads in eucharilla Bates (Lepidoptera: Riodinidae), and
natural areas in Mexico, Honduras, and Panama larvae of a leaf-mining fly, Melanagromyza rosales
and doubtless are yet more widely distributed in Woodley (Diptera: Agromyzidae), in Costa Rica.
the tropics. Fully grown larvae are large (~ 5cm), Generalist insects that chew bromeliad leaves
and their mining activities surely result in plant include cockroaches (Blattaria), whose actions are
death. They have not been seen to be abundant scarcely noticeable outside a greenhouse environ-
and their population sizes may be limited by para- ment, and grasshoppers (Orthoptera: Acrididae). In
sitoids, although such parasitoids have not been spring in southern Florida (USA), population
detected. Larvae of the one acrolophid species explosions of lubber grasshoppers (Romalea
implicated, Acrolophus vigia Beutelspacher, are guttata Houttyn (Acrididae)) attack many mono-
parasitized by larvae of at least one unidentified cotyledonous plants, including bromeliads; although
wasp (Hymenoptera: Braconidae). The subject is the damage they cause initially appears severe, the
of academic interest but currently of no economic plants seem to recover by new growth. In Andean
interest because A. vigia has not been detected in countries, the spectacled bear, Tremarctos ornatus
the USA Larvae of at least 24 weevil species (Cuvier), is reported to include a substantial
specialize in mining stems of bromeliads. They proportion of bromeliads in its diet.
belong to three genera, Cholus, Cactophagus, and Larvae of Epimorius testaceellus Ragonot
Metamasius. The life cycle of the weevil Diastethus (Lepidoptera: Pyralidae) develop within the flower
bromeliarum Champion seems unrecorded. All pods of the bromeliad Tillandsia fasciculata Swartz,
 Bromeliad Fauna
B 573

causing considerable local damage. A tiny wasp the plants trap insects which are decomposed
parasitoid attacks these larvae and may limit by bacterial action in their tanks. Although some
populations of this moth. writers have deemed this to be proto-carnivory
because the three bromeliads in question do not
produce digestive enzymes, the effect is the same.
Animals as Dispersers of Bromeliad The first detected instance was in the bromeliad
Seed Catopsis berteroniana (Schultes) in southern
Florida, although the plant has a wider distribution
Dispersal of seed in the bromeliad subfamily in the neotropics. Although it grows epiphytically, it
Tillandsioidea is by wind. The fleshy seeds of many grows typically above tree canopies, so it accumu-
Bromelioidea, however, seem designed to attract lates little or no organic debris from trees. It seems
feeding by vertebrate animals, and indeed birds to have evolved a method of confusing winged
have been reported to consume the seeds, pass terrestrial insects so that they stumble into it, have
them through alimentary tracts, and disperse them difficulty escaping, and drown and are decomposed
together with feces in new habitats. The subject of in the water-filled leaf axils. The two Brocchinia
seed-dispersal by animals is not well documented. species are terrestrial and grow in nutrient-poor
habitats in inland Venezuela. We may only hope that
the gluttonous commercial trade in carnivorous
Animals as Pollinators plants will not plunder these plants from the wild.
ofBromeliads Hobbyists should at least be warned that the two
Brocchinia species require cool, humid, breezy
Feeding by animals at bromeliad nectar may be climatic conditions that are hard to match in cultiva-
considered as a special case of phytophagy because tion, that populations of C. berteroniana in southern
this does no harm to the plants, unless perhaps the Florida are all in protected lands, that the plants are
animals should consume nectar without effecting specifically protected by law, and that none of the
pollination. There are remarkably few observations plants can withstand freezing temperatures.
of nectar feeding. Those that are mentioned most
are by hummingbirds at large flowers of some large
bromeliads, and these may well be over-empha- Conclusion
sized because hummingbirds are diurnal and easy
to see, and by butterflies and a few beetles. Bats are In pre-Columbian times, bromeliads and their
documented as pollinators of the genus Werauhia. denizens were a huge ecosystem extending in the
Feeding by moths is nocturnal, hard to observe, and Americas from southeastern Virginia (USA) to
may be vastly underrated. There is much scope for Argentina. Bromeliads and their animal denizens
collaboration between entomologists who can iden- are being destroyed overwhelmingly by encroach-
tify the insects effecting pollination and botanists ment by human populations. This has been called
who can identify the bromeliads specifically and development. One of the most species-rich areas
demonstrate pollination, especially at night. was Brazils Atlantic forest, which has been reduced
to less than 7% of its former extent, but a similar
story prevails everywhere. Some, especially in
Animals as Food for Bromeliads Trinidad and Brazil, were destroyed in the twenti-
(Carnivory) eth century because of an oversimplified concept
that bromeliads are a source of malaria-carrying
In just three bromeliad species (one Catopsis and Anopheles mosquitoes, and so the simplest method
two Brocchinia) carnivory has developed, because of controlling malaria is to destroy the forest and
574
B Bronzed Cutworm, Nephelodes minians Guene (Lepidoptera: Noctuidae)

the bromeliads. This concept has spilled over, public educational support to laws of many
irrationally, to other countries, other bromeliads, countries that already prohibit harvesting of
other mosquitoes, and other diseases (or no bromeliads from nature for commercial purposes.
diseases), to which it does not apply.
Lesser constraints on bromeliad populations References
and their denizens have made their mark because
so much has been destroyed by development. Frank JH (1983) Bromeliad phytotelmata and their biota,
Widespread and vast harvesting of bromeliad especially mosquitoes. In: Frank JH, Lounibos LP (eds)
Phytotelmata: terrestrial plants as hosts for aquatic
blooms for church activities is having an affect. insect communities. Plexus Publishing, Marlton, NJ,
The harvesting of bromeliads from nature has USA, pp 101128
unequivocally contributed to the spread of pest Frank JH (1996) Bromeliad Biota. Available at http://Bromeli-
insects internationally. Selective harvesting of the adBiota.ifas.ufl.edu. Accessed Oct 2006
Janetzky W (1997) Crustacea in bromeliad phytotelmata.
rarest bromeliads for the horticulture trade may Available at http://BromeliadBiota.ifas.ufl.edu/crbrom.
be having a negative affect, although a counter- htm. Accessed Oct 2006
argument has been made that they are being Janetzky W, Koste W (1997) Rotifera in bromeliad phytotel-
mata. Available at http://BromeliadBiota.ifas.ufl.edu/
propagated and thus will survive in culture.
robrom.htm. Accessed Oct 2006
Destruction of native bromeliad populations in Picado C (1913) Les bromliaces piphytes consideres
Florida by a pest weevil (which arrived as a comme milieu biologique. Bulletin des Sciences de la
contaminant of ornamental bromeliads from France et de la Belgique 47:215360
Polhemus JT, Polhemus DA (1991) A review of the veliid
Mexico) is having an overwhelming negative affect fauna of bromeliads with a key and description of a new
on the bromeliad populations its affect on the species (Heteroptera Veliidae). J New York Entomol Soc
bromeliad fauna in Florida has not yet been 99:204216
addressed although it surely must likewise be
negative. We have some idea of the reduction of
Bronzed Cutworm, Nephelodes
bromeliad populations throughout their former
minians Guene (Lepidoptera:
range, but we have no idea of the reduction of
Noctuidae)
populations of the animals that depend upon bro-
meliads; we can only guess that it is at very least as
This caterpillar is a pest of turfgrass, and occasion-
bad, most likely worse. Harvesting of selected bro-
ally other crops.
meliad-inhabiting animals from nature, such as
Turfgrass Insects and Their Management
Dendrobates frogs, threatens their very existence
Turfgrass Insects of The United States: Biology
but fortunately most bromeliad-dwelling organ-
and Management
isms lack appeal to hobbyists, and so are threatened
merely by development destroying bromeliads.
Involved biologists have four major options. Brood
The first is to study the heck out of native brome-
liad faunas in numerous neotropical countries In asocial insects, this generally refers to a cohort
while there still is a fauna. The second is political of individuals resulting from deposition of a
lobbying for the preservation of tracts of land that cluster of eggs and developing concurrently.
may preserve part of the fauna (some of it will However, sometimes it is used to refer to all the
inevitably be lost with development). The third is offspring of a parent, which may include several
to persuade churchgoers of Latin American clusters of eggs produced over the lifespan of the
churches not to harvest bromeliads from nature female. In social insects, this refers to all the imma-
to use other sorts of decorations instead of ture offspring of a colony, and may consist of eggs,
destroying the environment. The fourth is to provide larvae, nymphs and pupae.
 Brown Citrus Aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae)
B 575

Brood Cell

Among social insects, a cell, chamber or pocket

constructed to house the immature stages.

Brooding
A form of parental care wherein the young insects
remain near the parent insect (though in some
insects surrogate parents are employed). Some-
times the parents actively engage in defense of the
young, but often they do not.
Broun, Thomas, Figure 65 Thomas Broun.

Brood Sac
In cockroaches, an internal pouch, usually under the Brown Citrus Aphid, Toxoptera
wing covers, where eggs are incubated in females. citricida (Kirkaldy) (Hemiptera:
Aphididae)

Broun, Thomas james h. tsai

University of Florida, Ft. Lauderdale, FL, USA
Thomas Broun was born in Edinburgh on July
15, 1838. His father and an uncle were natural- The brown citrus aphid, Toxoptera citricida, is
ists and probably influenced him. At the age of believed to originate from China. Until 1900, this
16, he joined the British army, took part in the insect was confined to southeast Asia, Australia,
Crimean war, and then served in Burma and New Zealand, the Pacific Islands including Hawaii,
India during the Indian Mutiny. In 1862 he South Africa, and South America. Since then it has
married and emigrated to New Zealand. At become established in several countries of Central
outbreak of the Maori war, he was commis- America and many islands in the Caribbean Basin.
sioned as captain, served throughout the war, Brown citrus aphid was first discovered in 1995 in
and attained his majority. After that war, he south Florida; in the following two years, this
began to work on New Zealand insects. In 1880 insect had expanded into all citrus production
was published his Manual of New Zealand areas in Florida. Because of its ability to transmit
Coleoptera which listed 1,140 species. Supple- citrus tristeza virus (CTV) in an efficient manner,
ments increased this total to 3,979 species. In the combina tion of brown citrus aphid and CTV
1890 he was appointed Government Entomo has become an important problem of citrus world-
logist. His type specimens are mainly in the wide. Disastrous epidemics of citrus tristeza virus
Natural History Museum, L ondon. He died on have occurred in association with brown citrus
August 24, 1919 (Fig. 65). aphid in Argentina, Brazil, Colombia, and Peru.
CTV is known to cause decline and death of citrus
References trees grafted on sour orange (Citrus aurantium L.)
rootstock, but some CTV isolates can cause stem
Herman LH (2001) Broun, Thomas. Bull Am Mus Nat Hist pitting regardless of rootstock, and can result in
265:49 long-term debilitation that reduces yields of sweet
576
B Brown Citrus Aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae)

orange and grapefruit from 5 to 45%. Currently, there Nymphs undergo four instars. The developmental
are about 185 million citrus trees in Florida grafted times for nymphal stages vary with temperatures
on the susceptible sour orange rootstock. Citrus and host plants. Within a temperature range of
tristeza poses a real threat not only to Floridas cit- 830C, the length of nymphal development
rus industry, but also to other citrus producing decreases as temperature increases. The average
states in the U.S. Brown citrus aphid feeding causes developmental times for first, second, third and
leaf distortion and shortening of terminal growth. fourth instars are 112, 113, 216 and 222
Its honeydew provides a good medium for growth days, respectively. At 5C, nymphs fail to develop
of sooty mold. More importantly, brown citrus beyond the second instar. At 32C, the develop-
aphid is the most efficient vector of CTV as mental times for all nymphal stages increase com-
compared with other citrus aphids such as Aphis pared to those at 2830C. The adults can survive
gossypii, A. spiraecola and Toxoptera aurantii. and reproduce within the temperature range of
The overall transmission efficiency of CTV by 1032C (Fig. 66).
T. citricida ranges from 1 to 13% dependent upon The mean longevity of females decline expo-
CTV isolates and biotypes of vector. Brown citrus nentially from 60 days to 7 days as temperatures
aphid reproduces parthenogenetically. Most females increase from 10 to 32C. The maximal longevities
start to produce nymphs within 24 h after emergence. of individual females are 90, 62, 47, 30, 19, 15 and

Brown Citrus Aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae), Figure 66 Winged and
wingless adults of brown citrus aphid, Toxoptera citricida (photo P. Choate, University of Florida).
 Brown Dog Tick or Kennel Tick, Rhipicephalus sanguineus (Latreille) (Acari: Ixodida: Ixodidae)
B 577

9days at 10, 15, 20, 25, 28, 30 and 32C. Fecundity is References
more affected by temperatures; at 10 and 32C, the
fecundity is adversely affected. The average nymph Bar-Joseph M, Roistacher CN, Garnsey SM, Gumpf DJ (1981)
production by adults within 1530C increases to a A review on tristeza: an ongoing threat to citriculture.
Proc ISC 1:419422
maximum of 53 nymphs per female at 20C, then Michaud JP (1998) A review of the literature on the brown
decreases sharply as temperature increases. The citrus aphid, Toxoptera citricida (Kirkaldy). Fla Entomol
daily rate of nymph production varies with adult 81:3761
age. The peaks of reproduction appear at 4 through Michaud JP, Browning HW (1999) Seasonal abundance of the
brown citrus aphid, Toxoptera citricida (Homoptera:
10 days after adult emergence, with an average of Aphididae) and its natural enemies in Puerto Rico. Fla
25 nymphs per day. The duration of reproduction Entomol 82:424447
lasts as long as adult longevity within the tempera- Rocha-Pea MA, Lee RF, Lastra R, Niblett CL, Ochoa-Co-
rona FM, Garnsey SM, Yokomi RK (1995) Citrus
ture range of 1530C.
tristeza virus and its aphid vector, Toxoptera citri-
The biology of brown citrus aphid is also cida. Threats to citrus production in the Caribbean
affected by host plants on which the populations are and Central and North America. Plant Dis
reared. The average nymphal development periods 79:437445
Tsai JH (1998) Development, survivorship, and reproduc-
on rough lemon, sour orange, grapefruit, and key tion of Toxoptera citricida (Kirkaldy) (Homoptera:
lime are from 5.9 to 6.2 days. However, longer devel- Aphididae) on eight host plants. Environ Entomol
opmental periods (6.57.2 days) are required on 27:11901195
box orange, calamondin, lime berry and orange Tsai JH, Wang K (1999) Life table study of brown citrus aphid
(Homoptera: Aphididae) at different temperatures.
jassamine. The average number of nymphs produced Environ Entomol 23:412419
per female reared on sour orange, grapefruit, key
lime, rough lemon, calamondin, box orange, lime
berry and orange jassamine are 59, 43, 34, 43, 33, 18,
21 and 23 nymphs. Female adults live an average of Brown Dog Tick or Kennel Tick,
23 days on these hosts. Because young citrus flush Rhipicephalus sanguineus
occurs only intermittently in commercial groves, it (Latreille) (Acari: Ixodida:
is believed that plants other than commercial citrus Ixodidae)
play an important role in sustaining brown citrus
aphid populations when young citrus shoots are igor uspensky
not available. The Hebrew University of Jerusalem, Jerusalem,
Brown citrus aphid can be controlled by a Israel
number of pesticides. Hymenopteran insects play a
critical role in pollination and fruit set. Pesticide Rhipicephalus sanguineus is the main vector and
application can greatly affect the pollination pro- reservoir of a group of bacteria now called the
cess in the blooming season; thus the material and Rickettsia conorii complex. They are causative
time of application are of great significance in agents of a number of similar human diseases
reducing mortality of pollinators. Other biocontrol known earlier as Mediterranean spotted fever, and
agents such as parasitoids (Lysiphlebia spp., Apheli- distributed all around the Mediterranean and
nus sp. and Lipolexis sp.), syrphid fly (Pseudorus Black Seas as well as in India and some countries
clavatus), ladybeetles (Cycloneda sanguinea, Har- of southeastern Asia. According to the current
monia axyridis and Coelophora inaequalis), lace- data, new varieties of this disease connected with
wing (Chrysopa spp.), and entomopathogenic fungi R. sanguineus have been distinguished that are
(Beauveria bassiana isolates) show various degrees caused by different subspecies of R. conorii, namely
of effectiveness in control of brown citrus aphid. Mediterranean spotted fever (subsp. conorii) in
Citrus Pests and Their Management theMediterranean area, including northern Africa
578
B Brown Dog Tick or Kennel Tick, Rhipicephalus sanguineus (Latreille) (Acari: Ixodida: Ixodidae)

and southern Europe; Israeli tick typhus (subsp. ungulates. Later, dogs became its main and often
israelensis) in Israel; Astrakhan fever (subsp. caspia) only hosts. Spread of the tick worldwide has been
in the lower reaches of the Volga River in Russia; connected with human transport of dogs over the
and Indian tick typhus (subsp. indica) in Asia. In globe. At present, this tick can be found in all
addition, the brown dog tick was known as the continents between the latitudes of 50N and
vector of Rickettsia rickettsii, the causative agent of 35S, but sometimes even further in association
Rocky Mountain spotted fever in Central America, with dogs living indoors (in houses or kennels). It
mainly in Mexico. Recently, a focus of this disease was recorded from all 50 states of the USA, many
with R. sanguineus as the only vector was described sites in Canada, as well as from such European
and investigated in Arizona, USA. The broad countries as Belgium, Denmark, England, Ger-
distribution of this tick raises concern about such many, Norway, Poland and some others. Some
foci in adjacent states. Several new species of Rick- cases of human infection with R. conorii by ticks
ettsia were also isolated from R. sanguineus, and inside human dwellings were documented.
Rickettsia massiliae was documented as a human Being ecologically flexible and tolerant of a
pathogen. The brown dog tick was shown to harbor large range of climatic conditions, R. sanguineus
Coxiella burnetii (the causative agent of Q-fever) populates various areas, mainly inhabited localities
for many years after the death of the tick. Rhipi- including human dwellings, but also uninhabited
cephalus sanguineus transmits several agents environments which may be humid tropical,
pathogenic for dogs. The causative agent of canine subtropical or continental (semi-desert). Unfed
ehrlichiosis, Ehrlichia canis, originally described in ticks are active for the whole year in the tropics,
the Mediterranean area, was later found in numer- indoors as well as in the field. Under tropical
ous areas of the world, and today its distribution conditions, ticks may have three generations
completely coincides with the ticks range. during the year. Year round activity has also been
Rhipicephalus sanguineus also transmits protozoan observed in ticks living together with dogs in
dog pathogens, such as Babesia canis endemic in human dwellings in all regions. Unfed ticks living
the USA and Africa, and B. gibsoni in the Far East in the field to the north or south of the tropical
and North Africa. Several other pathogens were zone are active from spring until autumn. Here
isolated from this tick, but their epidemiological they have two or sometimes only one generation
or epizootiological significance is either small or annually. The more temperate the climatic
unclear. Transstadial and transovarial passage of conditions, the shorter is the period of activity of
R. conorii, R. massiliae and B. canis has been unfed R. sanguineus specimens. In Mediterranean
proven. countries, the season of adult activity lasts for 68
The difficulties of species identification in the months, from March-April until October-November,
genus Rhipicephalus resulted in subdividing the depending on the environmental conditions of a
genus into groups of closely related species. In par- particular area.
ticular, the R. sanguineus group includes about ten Host seeking behavior of unfed ticks depends
species, with R. turanicus being the most difficult to on the conditions of their habitation. When the
distinguish from R. sanguineus. At the same time, dog ticks live in human localities, they are
genetic analysis of ticks from different areas of the constantly rather close to their main hosts, often
world showed that there are distinct patterns for just around the dogs bedding area. When ticks are
R. sanguineus and that the intraspecific variability ready to feed, they migrate a very short distance to
of sequences within the species is very low. This their hosts, catch onto them and move over the
means that R. sanguineus is a valid species. dogs body looking for an attachment site. In the
The brown dog tick is the only cosmopolitan field, the ticks use an ambush strategy positioning
species of ticks. This species originated from on the vegetation, preferably on the tips of low
Africa where its hosts were local carnivores and grass, often in clusters. In the adult ticks, the
 Brown Dog Tick or Kennel Tick, Rhipicephalus sanguineus (Latreille) (Acari: Ixodida: Ixodidae)
B 579

a nterior end of the body usually points towards The brown dog tick (Fig. 67) is a typical exo-
the ground. Questing ticks can catch onto a pass- philic three-host tick. The larva feeds for 36 days,
ing host or, sensing it from a distance, they move the nymph for 410 days and an adult female for
in its direction, rather quickly over the sandy 613 days. Insemination of the adult female takes
ground. Rhipicephalus sanguineus in the open field place on the host after 34 days of feeding. With-
lives under much more inhospitable conditions out insemination, the female stops its engorge-
than ticks living in dense forests due to low humid- ment and lives in an attached position until
ity and great fluctuations of ambient temperature. insemination, or death from drying. The larvae
Under such conditions, the ticks are incapable of increase their weight during feeding 10 to 20-fold,
prolonged questing activity. To replenish their while nymphs increase their weight 60 to 75-fold
water reserves, ticks must regularly migrate down and adult females 70 to 120-fold. The adult males
to the litter and soil where temperature is lower feed for 35 days, increasing their weight 1.5 to
and humidity higher. Dog ticks have eyes and 2-fold. Henceforth, males migrate over the host
apparently use them effectively both for choice of body, attaching in different sites. The mass of an
optimal illumination and for searching for hosts. unfed larva is 0.020.025 mg, whereas the mass of
The capacity of R. sanguineus for active a fully engorged female reaches 200350 mg and it
migrations is rather limited. There are no data can lay up to 5,000 eggs. Two main components
about tick migrations in tropical areas, but in provide the increase of tick reproductive capacity:
semi-desert areas the unfed specimens can move minimizing egg size (and, hence, unfed larval
upwards up to 2040 cm, with the difference mass) and increased capability for interstage
between ticks of different stages being undetect- growth during nymphal feeding.
able. An interesting phenomenon concerning The minimal weight of engorgement after which
engorged nymphs and females in or near human females are capable of laying eggs is about 20 mg.
dwellings has been documented many times: after After the female reaches the weight of 170200 mg,
repletion and detachment, they migrate vertically
over the walls looking for suitable sites (cracks,
crevices) for molting or egg-laying. The height of
such migrations may be up to 2.5 m.
The season of activity for unfed subadults
(larvae and nymphs) depends on the seasonality
of adult ticks. In the tropical zone, subadults can
be active during the entire year, with periodic and
sometimes rather small fluctuations in their abun-
dance. Under more temperate climatic conditions,
the abundance of unfed subadults increases soon
after the decrease in adult abundance, larval activ-
ity preceding that of nymphs. The life span of
individual adults after molting continues from
34 months during summer months, to about 89
months if the hibernation followed with behav-
ioral diapause takes place. In continental climates,
only engorged nymphs and unfed adults can suc-
cessfully survive during the winter. Unfed ticks Brown Dog Tick or Kennel Tick, Rhipicephalus
that do not find a host and cannot feed during the Sanguineus (Latreille)Acari: Ixodida: Ixodidae),
activity season die due to complete expenditure Figure 67The brown dog tick, Rhipicephalus
of their nutritional reserves. sanguineus.
580
B Brown Dog Tick or Kennel Tick, Rhipicephalus sanguineus (Latreille) (Acari: Ixodida: Ixodidae)

the dependence of egg number/mg of engorged importance. Experiments on the treatment of tick
female becomes linear and equals approximately hosts or tick location sites by preparations based on
1517 eggs/mg of the female weight. Weight char- fungi and nematodes have shown that some patho-
acteristics and fecundity of the cosmopolitan gens have an obvious acaricidal effect. However, it is
R. sanguineus are different in populations from too early to estimate their real possibility for practi-
different regions. The populations from tropical cal purposes of human protection.
conditions have smaller engorged female weights Ticks
and, hence, lower fecundity.
The brown dog tick is a host-specific species, References
having the dog as its main host, though it can also
feed on different vertebrates, such as livestock, Beati L, Keirans JE (2001) Analysis of the systematic relation-
some carnivores, lagomorphs, rodents, insecti- ships among ticks of the genera Rhipicephalus and Boo-
vores. All three parasitic stages can use dogs philus (Acari: Ixodidae) based on mitochondrial 12S
ribosomal DNA sequences and morphological charac-
(sometimes the same individual) as hosts. Under ters. Journal of Parasitology 87:3248
conditions of extreme proximity with the host, Goodman JL, Dennis DT, Sonenshine DE (eds) (2005)
there are cases where the tick changed from a Tick-borne diseases of humans. American Society for
three-host type of development to a two-host type. Microbiology, Washington, DC
Ioffe-Uspensky I, Mumcuoglu KY, Uspensky I, Galun R (1997)
Sometimes larvae did not leave the dog after Rhipicephalus sanguineus and R. turanicus (Acari: Ixodi
engorgement, and molted to nymphs on the host. dae): closely related species with different biological
In other observations, these were engorged nymphs characteristics. J Med Entomol 134:7481
Ioffe-UspenskyI, Uspensky I, Mumcuoglu KY, Galun R (2005)
that molted on the host to adults. Adults actively
Rhipicephalus sanguineus and R. turanicus (Acari: Ixo-
attack people in the Palaearctic and are the main didae): numerical indices for distinguishing between
source of human infection by different pathogens. adults of closely related species in Israel. In:5th interna-
Until recently, R. sanguineus rarely attacked people tional conference on ticks and tick-borne pathogens,
programme, proceedings. Universit de Neuchtel
in the Nearctic, particularly in the USA. However, Switzerland, pp 171175
during the last several decades this tendency seems Nicholson WL, Paddock CD, Demma L, Traeger M, Johnson B,
to have changed and a number of cases of human Dickson J, McQuiston J, Swerdlow D (2006) Rocky moun-
bites by the brown dog tick have been recorded. tain spotted fever in Arizona: documentation of heavy
environmental infestations of Rhipicephalus sanguineus
The recent outbreak of Rocky Mountain spotted atan endemic site. Ann N Y Acad Sci 1078:338341
fever in Arizona was connected to heavy infesta- Parola P, Paddock CD, Raoult D (2005) Tick-borne rickettsio-
tion of dogs by R. sanguineus and numerous ticks ses around the world: emerging diseases challenging old
concepts. Clin Microbiol Rev 18:719756
of this species in the yards of patients homesites.
Pegram RG, Keirans JE, Clifford CM, Walker JB (1987) Clari-
Because the dog is a principal factor in human fication of the Rhipicephalus sanguineus group (Acari,
tick-borne infections, the suppression of ticks on Ixodoidea, Ixodidae). II. R. sanguineus (Latreille, 1806)
dogs by using systemic acaricides or plastic collars and related species. Syst Parasitol 10:2744
Uspensky I, Ioffe-Uspensky I (2002) The dog factor in brown
impregnated with acaricides is an effective protec- dog tick Rhipicephalus sanguineus (Acari: Ixodidae)
tion of humans from tick attacks and bites. Dogs infestations in and near human dwellings. Int J Med
heavily infested by ticks are dipped into water mix- Microbiol 291(Suppl 33): 156163
tures prepared with acaricidal emulsifiable concen- Uspensky I, Ioffe-Uspensky I, Mumcuoglu KY, Galun R (1999)
Body weight characteristics of some ixodid ticks: reflect-
trates and wettable or soluble powders. Regular ing adaptations to conditions of their habitats? In Bruin J,
cleaning of kennels, changing beddings, and acari- van der Geest LPS, Sabelis MW (eds) Ecology and
cidal treatment of sites which dogs frequent are evolution of the Acari. Kluwer Academic Publishers,
Dordrecht, The Netherlands, pp 657665
necessary measures for tick suppression. Educa-
Walker JB, Keirans JE, Horak IG (2000) The genus Rhipiceph-
tional programs for dog owners might be useful for alus (Acari, Ixodidae). A guide to the brown ticks of the
increasing their knowledge about tick medical world. Cambridge University Press, C ambridge, UK
 Brues, II, Charles Thomas
B 581

Brown Lacewings father to Argentina. Later that same year he

obtained a job providing photographic and print-
Members of the family Hemerobiidae (order ing services to the newly-built Museo de La Plata.
Neuroptera). The insect collection that he had formed in
Lacewings, Antlions and Mantidflies Germany became the foundation of the entomo-
logical section of the museum, and later he became
head of that section despite lack of formal training
in entomology. In 1906 he was appointed profes-
Brown Planthopper, Nilaparvata sor of zoology of Universidad de La Plata. In 1913
lugens (Hemiptera: Delphacidae) the title of doctor honoris causa was bestowed
upon him, followed by other titles. His research
This is a serious pest of rice in Southeast Asia.
and some 200 publications were on diverse groups
Area-Wide Insect Pest Management
of insects. He died on July 3, 1943. Pages 4855 of
Revista de la Sociedad Entomologica de Argentina
(vol. 43), written by several authors as representa-
Brown Rot of Fruit tives of several Argentine institutions, laud his
accomplishments.
These are fungal diseases of fruit that are transmit-
ted by insects.
Transmission of Plant Diseases by Insects Reference

Herman LH (2001) Bruch, Carlos. Bull Am Mus Nat Hist

265:4950
Brown Wheat Mite, Petrobia latens
(Mller) (Acari: Tetranychidae)
Bruchidae
This mite causes injury to wheat.
Wheat Pests and Their Management A family of beetles (order Coleoptera). They com-
monly are known as seed beetles.
Beetles
Brown-Banded Cockroach,
Supella longipalpa (Fabricius)
(Blattodea, Blattellidae) Brues, II, Charles Thomas

This common cockroach is one of the more Charles Brues was born on June 20, 1879, in West
important pests in cooler climates. Virginia. His high school years were spent in
Cockroaches Chicago, but instead of attending the University
of Chicago, he went to the University of Texas,
persuaded to do so by William Morton Wheeler
who had just been appointed head of the zoology
Bruch, Carlos department there. A schooldays friendship with
A. L. Melander, both of whom had been intro-
Carlos Bruch was born in Munich in 1869. He was duced to entomology by H. E. Walter, was contin-
interested in natural sciences but at age 14 joined ued in Texas and until the death of Brues many
his fathers business, and then in 1887 followed his years later. They coauthored entomological
582
B Brulle, Gaspard Auguste

papers while at Texas. After graduation with A.B. French government-sponsored expedition to
degree in 1901 and M.S. degree in 1902, Brues Moorea, and enthusiastically studied insects. In
went to Columbia University, but then returned 19331839 he was an assistant at the Musum
to Texas to work for the U.S. Department of Agri- National d Histoire Naturelle in Paris, working
culture. In 1905 he moved to the Milwaukee Pub- for the chairman of entomology. In 1832, with
lic Museum to work as Curator of Invertebrate other entomologists, he contributed to founding
Zoology, but in 1909 relocated to Harvard Uni- the Socit Entomologique de France. His (1839)
versity to become instructor in economic ento- professional thesis presented to the Facult des
mology, with William Morton Wheeler as his Sciences of Universit de Paris was on deposits of
supervisor. In 1935 he was promoted to Professor fossil insects. In 1839 he was appointed to a
of Entomology and also was Associate Curator of professorship of zoology and comparative anat-
Insects at the Museum of Comparative Zoology. omy in Dijon. Unfortunately for entomology, his
In 1946 he was made Emeritus Professor of Ento- duties in Dijon precluded his further contribu-
mology at Harvard. He collected insects through- tions to studies of insects. Nevertheless, from
out the United States, and inthe Philippines, East 1831 to 1843, he published on taxonomy of
Indies, West Indies, and South America. He was Coleoptera and Hymenoptera, mostly in Annales
an active member of the Cambridge Entomologi- de la Socit Entomologique de France. The
cal Club and editor of its publication (Psyche) (18341837) book Histoire naturelle des
from 1910 to 1947. Among his publications are A insectes; that he co-authored with Audouin
key to the families of North American insects (Brull wrote for it the sections of Coleoptera,
(first published in 1915 and coauthored with Orthoptera, and Hemiptera) was not completed.
Melander, and later revised), Insects and human He was awarded Frances highest medal, the
welfare (1921, later revised), and Insect dietary Lgion d Honneur. He died on January 21, 1873.
(1946). His research was on taxonomy and behav-
ior of phorid flies in ant nests, parasitic
Hymenoptera, food and feeding habits of insects, Reference
medical entomology, and tissue staining, and
thermophilous insects. He was a stimulating Desmarest E (1873) Note sur la vie et les travaux ento-
advisor of his graduate students. He died in Flor- mologiques d Auguste Brull. Annales de la Socit
ida on July 22, 1955, survived by his wife and a Entomologique de France (5)2:513516

son and daughter.

Brunner Von Wattenwyl, Carl

Reference
Carl Brunner was born in Bern on June 13, 1823, a
Mallis A (1971) Charles Thomas Brues, II. In American ento- member of a notable Swiss family, but moved at an
mologists. Rutgers University Press, New Brunswick, early age to Vienna. His early publications were in
NJ, p 434435
chemistry, physics, geology, glaciology, and meteo-
rology. In 1861 he published his first important con-
tribution on Orthoptera, then in 1865 the first of a
Brulle, Gaspard Auguste series of papers on classification of Blattodea. These
were followed in 1878 by a paper on classification of
Auguste Brull was born in Paris on April 7, 1809. Tettigoniidae, then in 1888 on that of Stenopelmati-
At school he showed a taste for the natural sci- dae and Gryllacrididae. In 1882 was published his
ences. Then, in 1829 he was able to take part in a encyclopedic work of the European Orthoptera
 Brush-Footed Butterflies (Lepidoptera: Nymphalidae)
B 583

Prodromus der Europischen Orthopteren. In all, Subfamily: Apaturinae

he published 27 works on Orthoptera and was one Subfamily: Nymphalinae
of the most notable of orthopterists. He died on Subfamily: Danainae
August 24, 1914, at Kirchdorf, Austria, and his Subfamily: Heliconiinae
Orthoptera collection is in Vienna. Subfamily: Biblidinae

References Distinguishing Characteristics and

Relationships
Burr M (1900) Brunner von Wattenwyl. Ent Rec J Var
12:12+pl. 1 One distinctive and unambiguous character is
Rehn JAG (1915) Carl Brunner von Wattenwyl. Entomol
News 26:285288 unique to the Nymphalidae: the ventromesial
surface of the antenna has three longitudinal ridges
(termed carinae, meaning keel; the antenna is
hence tricarinate), one lying either side and one
Brush-Footed Butterflies separating two shallow longitudinal grooves. Two
(Lepidoptera: Nymphalidae) further characters may be the presence of a distinc-
tive structure, von Siebolds organ, in the female
keith r. willmott genitalia, and a filiform seta in the mature larva that
The Natural History Museum, London, United is absent in other papilionoid families.
Kingdom The sister taxon (most closely related group)
to the Nymphalidae is thought to be the Lycaeni-
The Nymphalidae is one of five families in the dae plus Riodinidae, which share several thoracic
superfamily Papilionoidea (true butterflies) of the and musculature characters with the family. More
order Lepidoptera (moths and butterflies). obvious characters are provided by the foreleg,
Although a number of lineages within the family which is reduced in adults of most male Lycaeni-
are well circumscribed and have been recognized dae plus Riodinidae, and in male and female
since the 1800s, the taxonomic rank which such Nymphalidae (only in male Libytheinae). The male
lineages should be accorded and how they should foreleg in all three families lacks tarsal claws and
be subdivided remains contentious. A number of has the original five tarsal segments (tarsomeres)
currently recognized subfamilies, and even some reduced in number through fusion, with the latter
tribes, have been considered distinct families by feature also occurring in some female Nymphali-
some authors. However, continuing morphological dae. In male Riodinidae, and both sexes of most
and especially molecular research now provides Nymphalidae, only four legs are used for walking,
real hope of a stable higher classification in the and in male Nymphalidae the forelegs are clothed
future. Ten subfamilies are currently recognized, in hair-like scales, inspiring the common familial
including: name brush-footed butterflies.
Order: Lepidoptera All nymphalid subfamilies, except for
Superfamily: Papilionoidea Libytheinae, are further grouped by the loss of use
Family: Nymphalidae of the foreleg in the female. Relationships between
Subfamily: Libytheinae other nymphalid subfamilies remain obscure,
Subfamily: Calinaginae although certain relationships are often found and
Subfamily: Morphinae seem plausible, such as Morphinae plus Satyrinae.
Subfamily: Satyrinae While most subfamilies are probably natural
Subfamily: Charaxinae (monophyletic) groups, the Nymphalinae, Biblidinae,
584
B Brush-Footed Butterflies (Lepidoptera: Nymphalidae)

and Satyrinae have no convincing autapomorphies to giant Caligo (Morphinae), the size of dinner-
(uniquely derived characteristics). They will plates. The wings may be rounded, elongate (e.g.,
almost certainly be subdivided or merged with Heliconiinae, Ithomiini), scalloped (e.g., Cethosia),
other subfamilies as our knowledge of nymphalid or with long hindwing tails (e.g., Marpesia). The
phylogeny increases. simplest nymphalid wing patterns consist of a series
of dark lines and ocelli (eyespots, a common feature)
on a pale background, which are variably modified
through loss, expansion or fusion into a fantastic
Morphology array of patterns. These patterns range from almost
entirely transparent and colorless in ithomiine dan-
Adult aines to the extremely complex patterns of certain
Charaxes species (Charaxinae), to the brilliant iri-
Nymphalid butterflies (Fig.68) range from tiny descent blue that makes Morpho butterflies visible
melitaeines (Nymphalinae), the size of a fingernail, from low-flying aircraft. Many insights into the

Brush-Footed Butterflies (Lepidoptera: Nymphalidae), Figure68 Representative nymphalid butterflies.

A, Coenophlebia archidona (Charaxinae), Ecuador; B, Mycalesis orseis (Satyrinae), Malaysia; C, Cethosia
penthesilea (Heliconiinae), Malaysia; D, Marpesia petreus (Biblidinae), Ecuador; E, Caligo ilioneus
(Brassolinae), Ecuador; F, Phystis simois (Nymphalinae), Ecuador; G, Idea lynceus ( Danainae), Malaysia;
H,Charaxes castor (Charaxinae), Kenya; I, Consul fabius (Charaxinae), Ecuador; J, Heliconius numata
(Heliconiinae), Ecuador; K, Oleria baizana (Danainae), Ecuador.
 Brush-Footed Butterflies (Lepidoptera: Nymphalidae)
B 585

developmental genetics and evolution of lepi- coremata that characterize the Danaini). Espe-
dopteran wing patterns have been gained from cially complex androconial systems, such as
comparative study of nymphalid wing patterns. those in the Danaini, involve abdominal brushes
Wing color pattern signaling functions that are remote from glandular alar areas but
include crypsis (e.g., the extraordinary leaf-like make contact with them immediately before
Kallima and Coenophlebia; transparent-winged scent dispersal. Secondary sexual structures also
forest understorey satyrines and ithomiines), are known for females of some taxa, most nota-
startle or deflective coloration (e.g., the eyespots bly in some members of the Heliconiinae, which
of Caligo and Satyrinae), interspecific recognition possess a dorsal abdominal gland and associated
(e.g., Nessaea, Catonephele), and both Batesian lateral club-like structures termed stink-clubs or
(e.g., certain Nymphalinae and Charaxinae) and clavatia.
Mllerian (e.g., Heliconiinae, Danainae) mimetic
warning coloration. Color pattern variation
includes seasonal polymorphism (e.g., Junonia), Immature Stages
local genetic polymorphisms (e.g., Heliconius,
Hypolimnas), and often remarkable geographic Nymphalid immature stages are morphologically
racial polymorphism (e.g., Danainae, Heliconius). extremely diverse, and although comparative
The external morphology is rather uniform, study is in relative infancy compared to adult
being responsible, at least in part, for the poorly morphology, immature stage characters may still
resolved high-level classification of the family. provide very significant information for the
Variation in wing venation, thoracic exoskeletal, higher level classification of the family.
leg and labial palpal morphology provides the The eggs are typically spherical, ovoid, or
foundation for the current subfamilial classification. flattened domes, and almost smooth (e.g., Satyri-
In certain species the veins and basal wing scler- nae), ribbed (e.g., Danainae), or faceted with
ites on either fore or hindwing may be modified to interstitial spines (Limenitidini). Larvae may be
form a tympanal organ (e.g., Heliconius, Satyrinae), smooth (e.g., some Danainae), covered with
though its function is poorly understood. At the small granulations (e.g., Satyrinae), or decorated
subtribal, generic and species level genitalic with fleshy tubercles (e.g., Danainae), dense
morphology, especially male, has been used exten- spines (e.g., Nymphalinae) that may be modified
sively, although there is often no variation between into highly elongate and branched scoli (some
closely related species. Biblidinae), or hair tufts (e.g., some Brassolinae).
The Nymphalidae exhibit a rich diversity of In later instars of some neotropical Charaxinae
secondary sexual structures. Most commonly the third thoracic and first abdominal segments
these are modified scales with glandular bases, also may be expanded to form dorsal or dorso-
typically confined to the male sex, termed lateral humps. The head capsule may be striped
androconia. Androconial scales usually form or colored, and may be smooth (e.g., Danainae),
patches, fringes, tufts or pockets, and may be or ornamented with chalazae (raised wart-like
flattened or elongate, but often are hair-like and processes, frequently bearing setae), that often
erectile (e.g., Satyrinae, Danainae). Alar andro- form elaborate dorsal and subdorsal head horns.
conia are often associated with wing veins, and The ninth abdominal segment is often bifid,
occur commonly in the Satyrinae and Danainae. forming tails (e.g., Satyrinae, Charaxinae, Mor-
Abdominal androconia may be located on ever- phinae). Larvae may be cryptically colored (most
sible glands (e.g., Vila) or contained within a Satyrinae, Limenitidini) or black with bright
membranous sheath that can be everted through orange, white or yellow markings that suggest
an increase in haemolymph pressure (e.g., the warning coloration.
586
B Brush-Footed Butterflies (Lepidoptera: Nymphalidae)

Except for a few satyrines that pupate from 500 to 1,000 m above sea-level, due to overlap
t errestrially, the pupa is suspended by the cremaster of lowland and sub-montane faunas.
and never has a girdle. Pupae may be smooth, The variation in dispersal ability within the
elongate ovoids (e.g., some Satyrinae and Nymphalidae is perhaps more extreme than in any
Danainae), or highly ornamented with various other butterfly family. Certain nymphalids are
spines, flanges, and elongate projections renowned as great wanderers: the famed Monarch
(e.g., some Biblidinae). The pupal color pattern (Danaus plexippus, Danainae) occurs throughout
ranges from highly cryptic, mottled brown or much of the globe, even on Hawaii, while the
green, to bright colors that may be aposematic, nymphaline Hypolimnas misippus is almost as
and many other species are notable for their widely distributed. However, the vast majority of
brilliant opalescent or metallic coloration species occur only within a single biogeographic
(e.g., Limenitidini, Danainae). region, and a number of species have much more
restricted ranges, sometimes down to the level of a
single mountain range. Distribution patterns in
Diversity, Distribution and neotropical montane satyrines (tribe Pronophilini)
Biogeography and the nymphaline genus Hypanartia have
been used to examine geographic modes of
The family includes approximately 6,000 to 7,000 speciation in montane habitats. Ithomiine dan-
species and 350400 genera. The largest subfamily aines and heliconiines have featured promi-
is the Satyrinae with some 2,500 species, many of nently in studies of the historical biogeography
which remain undescribed. In contrast, the of the Amazon basin.
Calinaginae contains only a single genus of about
eight species and the Libytheinae only two genera
with 12 species. Habitats
The majority of the subfamilies are cosmo-
politan, although the Calinaginae are confined Nymphalid butterflies occur in almost all terrestrial
to the Sino-Himalayan region and the Morphinae ecosystems. They are found in deserts, grasslands
are entirely tropical. However, at the tribal level (especially Satyrinae), temperate and tropical
endemism is much higher, with large tribes lowland and montane forests, ranging from sea-level
confined to or overwhelmingly more diverse in to over 5,000 m in high ice-fields of the Himalayas
single regions. Notable examples include the and the Andes. They are found in all stages of habitat
Brassolini, Morphini and Ithomiini, restricted to succession, from primary forest to arid scrub, with
the Neotropics; the Amathusiini, occurring only varying ecological fidelity.
in the Oriental region; the Acraeini, with its spec-
tacular radiation in the Afrotropical region; and
the Danaini, largely confined to the Old World. Ecology
Species diversity increases steeply from
temperate to tropical regions, reaching a peak in Immature Stages
the Neotropical region which contains perhaps
40% of the family. Community species richness is All nymphalid larvae are phytophagous, with the
also greatest in the Neotropics, in the foothills of vast majority concentrating on about 100 families
the eastern Andes, where lowland tropical rainfor- of flowering plants, in addition to a few groups on
est may contain over 450 species, about a quarter Cycadaceae (cycads), Selaginellaceae (club-mosses)
of the butterfly fauna. Species richness decreases and Neckeraceae (mosses). The Satyrinae and
with elevation, though richness peaks may occur Morphinae feed largely on monocotyledons, as do
 Brush-Footed Butterflies (Lepidoptera: Nymphalidae)
B 587

a few Charaxinae, with the remainder almost Adult nymphalids feed on various food sub-
exclusively on dicotyledons. strates including flower nectar, pollen, rotting fruit,
Eggs may be laid in clusters or singly, varying carrion, and damp sand. Flower nectar and rotting
between species, and on or off the foodplant, or, in fruits provide the carbohydrates that power flight,
some satyrines, be dropped from the air. Larvae of a while pollen is used by Heliconius butterflies to
number of species are gregarious and aposematic, provide nutrients for egg production. Damp sand
suggesting unpalatability (e.g., Heliconiinae), while and carrion are thought to provide sodium ions,
others adopt a variety of defensive strategies. These important for neuromuscular activity, which are
include camouflage through decoration of the early typically in low concentration in larval food plants.
instars with frass pellets (stercophory), maintenance These last two sources may also provide amino
and extension of the leaf mid-rib with frass to form acids that are used in manufacturing body pro-
a perch (common in Biblidinae), and construction teins. To some extent the preferred food source
of a mass of frass and leaf material at the base of the may be dependent on habitat, with open-country
leaf mid-rib to provide additional camouflage, which species seeking flowers and damp sand, and forest
may be elaborated further into an apparent decoy species feeding on rotting fruit and carrion.
larva-shaped mass (Limenitidini). Spinose larvae A variety of strategies protect nymphalid
may react violently to disturbance, swinging the butterflies from predators, particularly birds. Many
body and head (e.g., Biblidini), or curl into a defen- species have cryptic underside markings, especially
sive posture with the spines directed outwards (e.g., in the Satyrinae and Morphinae, while bright
Limenitidini), while smooth-bodied satyrine larvae dorsal coloration in the same species probably con-
may simply drop from the plant into the ground lit- fuses predators. Most Biblidinae and Charaxinae
ter. A number of nymphalid larvae hibernate in shel- probably rely on fast flight to evade predators.
ters made from cut and sewn leaves, and in some Warningly colored ithomiine danaines and
species (e.g., Adelpha), this behavior apparently has heliconiines were instrumental in the formulation
been co-opted for protection. of mimicry theory, providing some of the most
Pupation takes place on or off the foodplant, outstanding examples of this phenomenon in the
and some satyrines form a weak cocoon on the animal kingdom. Unpalatable danaines and
ground in which they pupate heliconiines are the basis for numerous Mllerian
mimicry rings, in which other nymphalids
(e.g., Charaxainae, Nymphalinae), as well as other
Adults butterflies and moths, participate as probable
Batesian (palatable) mimics.
Nymphalids exhibit a broad range of behavior. Unpalatable nymphalids obtain protective
Unpalatable groups, such as Danainae and chemicals by several means. They may sequester
Heliconiinae, have a typically slow and even flight, secondary chemicals from larval feeding, such asthe
while palatable species in the Apaturinae and cardiac glycosides obtained by Danaini from their
Charaxinae are some of the fastest and most agile apocynaceous foodplants. Alternatively, protective
butterflies. They may be found in open areas compounds, such as the cyanogenic glucosides in
(e.g., Satyrinae, Nymphalinae), in shady forest H`eliconius, may be synthesized from amino acids
understorey (e.g., Satyrinae, Morphinae, Danainae), in the larval or adult food. More complex precursors
and at various levels within forest subcanopy and also may be stored from the larval stage, or obtained
canopy (e.g., Heliconiinae, Biblidinae, Charaxinae). through adult pharmacophagy (literally, chemical
Throughout the day a succession of different groups feeding). Adult danaines obtain dehydropyrroliz-
becomes active, with the fastest-flying species being idine alkaloids by feeding on Asteraceae flowers
active only during the hotter hours of the day. (sometimes Boraginaceae), or dried or withered
588
B Brush-Footed Butterflies (Lepidoptera: Nymphalidae)

Boraginaceae plants (sometimes Asteraceae). In species where courtship has been studied in some
ithomiine danaines, it is predominantly males detail (Satyrinae, Danainae, Heliconiinae), the impor-
which exploit these alkaloid sources, transferring tance of androconially disseminated pheromones
the compounds to females in the spermatophore in achieving successful courtship has been demon-
during mating. strated. In the Danainae, sex pheromones like
Nymphalids generally seek females for mating danaidone (Danaini) are manufactured from
by patrolling appropriate areas of habitat (e.g., pyrrolizidine alkaloids that also confer protection
Morpho butterflies may patrol several kilometers from predators.
along rivers or roads), or by perching. Perching
nymphalids wait for passing females in species-
specific locations, such as a forest light-gap or edge, Economic Importance
hilltop, riverside, or prominent patch of vegetation,
usually at a characteristic height above ground and With the exception of Brassolis and Caligo
at a particular time of day. Many satyrines and (Brassolinae) which may be pests on coconut palm
brassoline morphines are crepuscular, actively and banana plantations, respectively, and certain
perching or patrolling only at dusk and dawn. Heliconiinae which attack passion fruit plants,
Ithomiine danaines perch most actively in the mid- few other nymphalid butterflies cause any serious
dle to late afternoon, while fast-flying forest canopy damage to crops. Nymphalid butterflies, however,
species, such as the Charaxinae, are active in the do have a positive economic value. Nymphalid
middle of the day. The same perching location may butterflies are an important component of the dead
be maintained for years. Perching males are territo- butterfly specimen trade (e.g., Agrias, Charaxes),
rial and pugnacious, swiftly engaging in high spi- the trade in specimens for education (e.g., the
raling flights with intruding conspecific males, Monarch), and are widely used in butterfly houses
with the resident male typically winning the in temperate countries (e.g., Heliconius, Caligo).
encounter to return to the perching site. Some Butterfly houses import much livestock from
Charaxes butterflies have serrate forewing costal butterfly farms in tropical countries, providing an
margins, which are reported to be used in male- alternative source of income in rural areas.
male interactions. Certain species in the genus
Hamadryas (Biblidinae) are notable for loud
crackling sounds that are emitted by perching Conservation
males in flight, by percussion of the forewings.
Male ithomiine danaines are remarkable in Because of their aesthetic appeal, butterflies may
forming dense aggregations, or leks, of up to be used as flagship taxa for conservation. Attempts
2030 species, which may last several months. to preserve the spectacular over-wintering colonies
Pheromones released through the hindwing hair- of the Monarch butterfly in Mexico have raised
pencil androconia attract both sexes, including awareness of conservation in that region. Butterfly
those of non-conspecific but co-mimetic species, diversity and abundance are increasingly being
thus providing increased protection from predation used at the habitat scale as indicators of distur-
and providing a mating place that can be more bance and its effects on biodiversity. Nymphalidae
easily located through the concentrated odor. are diverse, one of the easiest groups to identify,
Aggregations of similar origin and function also and many respond to baited traps, and are thus a
are reported in some danaines (Euploea). principal group in such studies. At the biogeo-
Males of certain species of Heliconius patrol graphic scale, the Ithomiini have been proposed as
foodplants and mate with females before eclosion an indicator taxon for neotropical lowland forest
from the pupa, thus avoiding courtship. In those butterfly diversity, because of their ease of sampling
 Bubonic Plague
B 589

and apparent close correlation with overall butterfly Bubo

diversity. Finally, recent shifts in geographic range
limits of butterflies, especially nymphalids, have An enlargement of a lymph gland caused by an
been used as evidence for global climate change. infection.
Bubonic Plague
Plague: Biology and Epidemiology
References

Ackery PR (1988) Hostplants and classification: a review of

nymphalid butterflies. Biol J Linn Soc 33:95203
Ackery PR, de Jong R, Vane-Wright RI (1999) The butterflies:
Bubonic Plague
Hedayloidea, and Papilionoidea. In: Kristensen NP (ed)
Handbook of zoology 4. de Gruyter, Berlin, Germany, pp The dominant form of plague (also known as black
263300 death), caused by the bacterium Yersinia pestis and
Brower AVZ (2000) Phylogenetic relationships among the
Nymphalidae (Lepidoptera) inferred from partial
vectored by several fleas, but especially Xenopsylla
sequences of the wingless gene. Proc R Soc (Biol Sci B) spp. It is primarily a disease of rodents, but fleas
267:12011211 can spread it to other animals and humans. Bubonic
DeVries PJ (1987) The butterflies of Costa Rica and their plague is one form of plague, with the others being
natural history. Papilionidae, Pieridae, Nymphalidae.
Princeton University Press, Princeton, New Jersey. septicemia plague (infection of the blood) and
Harvey DJ (1991) Appendix B. Higher classification of the pneumonic plague (infection of the lungs). Bubonic
Nymphalidae. In: Nijhout HF (ed) The development plague causes headache, elevated temperatures,
and evolution of butterfly wing patterns. Smithsonian
chills, tiredness, abdominal pains, and painful
Institution Press, Washington, DC, pp 255273
Parsons MJ (1998) The butterflies of Papua New Guinea. Their swellings (buboes) of the lymph nodes. Anyone
systematics and biology. Academic Press, London, UK with large, painful, and tender lymph glands and
experiencing extreme tiredness and fever should
be considered a possible plague victim, especially if
Brush Organ they have had potential exposure to animals
capable of harboring plague. People most likely to
Clusters of long setae on the body of certain insects contract bubonic plague are those living in rural
(particularly male Lepidoptera and some Neu- environments, and people active in rural environ-
roptera). They occur on various parts of the body, ment such as biologists, campers and hunters.
but usually on the abdomen. They are associated If untreated, it often is fatal to humans.
with exocrine glands, and usually used during Treatment is accomplished by application of
courtship to disperse sex pheromones. This term is antibiotics, often streptomycin, but early detec-
synonymous with hair pencils. tion is important. Other important measures to
prevent plague are educating the public to avoid
places where plague may occur, informing the
Bryopsocidae
medical community about diagnosis of plague,
A family of psocids (order Psocoptera). and treatment using appropriate medicine. An
Bark-Lice, Book-Lice and Psocids early warning sign of potential human infection
is die-off of rodents. Although rats have histori-
cally been implicated in disease transmission,
B.t. plague is also associated with rock and ground
squirrels, wood rats, chipmunks, prairie dogs,
Abbreviation for the bacterium Bacillus mice and voles. To prevent plague problems, it
thuringiensis. may be useful to use insecticides to kill fleas
590
B Buccal Cavity

uring epidemics (e.g., treatment of prairie dog

d the parental nest of one or more reproductive forms
burrows), to apply flea control treatments to pets accompanied by workers. Thus, the parental nest
regularly, to avoid handling sick animals, and to remains functional and new ones are founded.
use insect repellents.
Plague: Biology and Epidemiology
Fleas (Siphonaptera) Buffalo Gnats
History and Insects
Members of the family Simulidae (order Diptera).
Flies

Buccal Cavity
Buffalograss Chinch Bug, Blissus
The entry way to the insect mouth, surrounded by occiduus Barber (Hemiptera:
the mouthparts. The oral cavity (Fig.69). Blissidae)
Alimentary System
Alimentary Canal This insect has become a pest of buffalograss in
Digestion some areas.
Turfgrass Insects and Their Management
Turfgrass Insects of The United States: Biology
Bucculatricidae and Management

A family of moths (order Lepidoptera). They are

commonly known as ribbed-cocoon maker moths. Buffer Zone
Ribbed-Cocoon Maker Moths
Butterflies This term has different meanings depending on
Moths the context. From the perspective of insect
control, a buffer zone may be established around
a treated field by treating surrounding land and
Budding vegetation. This reduces the possibility that an
insect can arrive successfully in a susceptible field
Among social insects, the same as colony fission: because nearby insects are eliminated not only in
multiplication of colonies by the departure from the field, but from surrounding areas. This ismost

foregut midgut hindgut

gastric
esophagus crop ventriculus pylorus ileum rectum
caecum
pharynx

buccal anus
cavity proventriculus
mouth Malpighian tubule

Buccal Cavity, Figure 69 Generalized insect alimentary system (adapted from Chapman, The insects:
structure and function).
 Bugs (Hemiptera)
B 591

important for dispersive species, and particularly by Louis XV, king of France, bestowing on him the
for disease vectors. From a regulatory perspec- title of Comte de Buffon. He died in 1788, leaving
tive, a buffer zone is an area in which a specific his wife Marie and one son.
pest of concern does not occur, or occurs at a
very low level and is controlled, and also encloses,
or is adjacent to, an infested area. In both cases, References
however, the purpose of the buffer zone is to
reduce or eliminate spread of a pest. Anon. 1999 Georges-Louis Le Clerc, Comte de Buffon.
Risk Analysis (Assessment) Thomson Gale: World of scientific discovery, 2nd ed.
Farmington Hills, MI, USA
Regulatory Entomology Tuxen SL (1973) Entomology systematizes and describes:
Invasive Species 17001815. In Smith RF, Mittler, TE Smith CN (ed)
History of Entomology. Annual Reviews Inc., Palo
Alto, California, pp 95117

Buffon, Georges Louis Leclerc

(Comte De)
Bugs (Hemiptera)
Georges-Louis LeClerc was born in Montbard,
France, on September 7, 1707. He is believed to julieta brambila, greg s. hodges
have been educated in the Jesuit college of Dijon Florida Department of Agriculture and Consumer
and later received a diploma in law from the Services Division of Plant Industry, Gainesville,
Universit de Dijon. His early scientific studies FL, USA
were in mathematics and physics, and he performed
experiments on the tensile strength of wood. He Hemiptera are the largest order of insects with
entered the Academie Royale des Sciences of Paris incomplete metamorphosis. This order includes
in 1734. Six years later he was appointed director pond skaters, squash bugs, big-eyed bugs, stink
of the royal garden, which later was called the bugs, cicadas, leafhoppers, planthoppers, tree-
Jardin des Plantes and was the French center of hoppers, froghoppers, psyllids, aphids, scales,
study not only of botany, but also of zoology, mealybugs, whiteflies, and others (Figs.70
chemistry, and mineralogy. Perhaps he would have and71). Although less well known than beetles
studied insects if his eyesight had been adequate. or butterflies, they are a diverse group of insects,
Although he did not do so, he had profound ubiquitous, interesting, or even spectacular, and
influence onentomology by his founding a huge in some cases agriculturally and medically
work (17491804) Histoire naturelle, gnrale important. Approximately 82,000 species have
et particulire in 44 volumes. There were later been described worldwide, comprising about
supplements [see for example, Audinet-Serville 810 percent of all known insect species, with
above]. The work set out to contradict Linn, an estimated 105,000 species not yet described.
because Georges-Louis did not believe in the They range from minute, wingless scales to fish-
classification into genera, families, orders and eating giant water bugs, which may reach a length
classes that Linn had proposed. The work was of 11 cm. These fascinating insects occur in
very influential especially because so many spe- nearly every type of habitat, including several
cialists (including entomologists) became involved species that live on the surface of the ocean
in its writing, and because of its completeness (for hundreds of miles from land and others that can
its time). Furthermore, it was written in French, be found occasionally drifting in the wind. The
rather than Latin, breaking the precedent of so majority are plant-feeders, but many species are
many earlier books. He was made a peer of France predatory on other insects, while others feed on
592
B Bugs (Hemiptera)

Bugs (Hemiptera), Figure70 (Continued)

 Bugs (Hemiptera)
B 593

the blood of vertebrates and are of great medi- These suborders are Sternorrhyncha, Fulgoromorpha,
cal importance. Cicadomorpha, Coleorhyncha, and Heteroptera.
In general, hemipterans have simple or incom- These names refer to monophyletic groups and will
plete metamorphosis, in which the young, called provide stability to the nomenclature within
nymphs, are similar to adults in shape. The wings Hemiptera. Some classification schemes present Het-
develop externally as budlike outgrowths which eroptera and Coleorhyncha together as Prosorrhyn-
increase in size at each molt and become functional cha, another apparently monophyletic group. The old
after the last molt. term Homoptera does not refer to a monophyletic
The mouthparts of Hemiptera are group and has essentially been abandoned. Another
e longate, forming a slender and usually seg- classification has four suborders, Sternorrhyncha,
mented beak that is used for piercing the host, Auchenorrhyncha, Coleorhyncha, and Heteroptera;
either plant or animal, and sucking liquids again, the term Auchenorrhyncha refers to a non-
after injecting enzymes that enable extraoral monophyletic taxon and apparently is being aban-
digestion. In many Hemiptera, the basal por- doned. The arrangement of the various groups
tion of the front wing is thickened to form a (suborders, superfamilies, and families) in the order
wing cover and the apical portion is thin and Hemiptera has been debated for many years. The
usually transparent while the hind wings are present classification should not be regarded as fixed.
entirely membranous. The front wing, or hem- Order: Hemiptera
elytron (from the Greek words hemi, meaning Suborder: Sternorrhyncha
half, and pteron, meaning wing), gives the Suborder: Fulgoromorpha
order its name. The name Hemiptera was Suborder: Cicadomorpha
coined by L innaeus in 1758. Suborder: Coleorhyncha
Suborder: Heteroptera
Classification
Suborder Sternorrhyncha
The earliest book to deal exclusively with the
Hemiptera was written in 1803 by J. C. Fabricius, a Sternorrhynchans are common insects found in a
student of C. Linnaeus. He renamed the group Rhyn- wide variety of ecosystems throughout the world.
gota, later changed to Rhynchota, a name that is being All members of the Sternorrhyncha feed on phloem
used today. The term Rhynchota (from the Greek, or xylem from host plants and many are considered
rhynchos, for beak) refers to the morphology of the plant pests. The group name Sternorrhyncha
mouth parts, an elongate structure known as probos- (Greek, sternon, chest; rhynchos, nose or snout) is
cis or rostrum. This name should eventually replace derived from the location of the mouthparts occur-
Hemiptera because the rostrum is characteristic to all ring between the bases of the front legs. In previous
groups in this order. Up-to-date classifications recog- classification schemes, both the Auchenorrhyncha
nize five suborders within Hemiptera instead of the and Sternorrhyncha have been recognized as sub-
familiar two suborders, Homoptera and Heteroptera. orders of the Homoptera. However, the legitimacy

Bugs (Hemiptera), Figure70 Representative bugs (Hemiptera): top left, a leaffootted bug,
Acanthocephala femorata (Coreidae); top right, a broad-headed bug, Alydus pilosulus (Alydidae); second
row left, a largid bug, Largus succinctus (Largidae); second row right, a seed bug, Dieuches armatipes
(Lygaeidae); third row left, a plant bug, Creontiades rubrinerus (Miridae); third row right, Jadera bug,
Jadera haematoloma (Rhopalidae); bottom left, avocado lace bug, Pseudacysta persa (Tingidae);
southern green stink bug, Nezara viridula (Pentatomidae) (all photos by Lyle Buss).
594
B Bugs (Hemiptera)

Bugs (Hemiptera), Figure71 (Continued)

 Bugs (Hemiptera)
B 595

of the order Homoptera has been and is the topic of Lecanodiaspididae-false pit scales
many debates. There is taxonomic evidence demon- Margarodidae-margarodid scales
strating that the Homoptera grouping is paraphyl- Micrococcidae
etic (derived from a single ancestor but not Ortheziidae-ensign scales
containing all descendants). Many taxonomists Phenacoleachiidae
agree that this group should be recognized as part Phoenicococcidae-palm scales
of the Hemiptera but debates occur when discuss- Pseudococcidae-mealy bugs
ing placement of the Homopteran groups as subor- Putoidae-giant mealy bugs
ders within the Hemiptera. For the purpose of this Stictococcidae-false soft scales
discussion, we will recognize the Sternorrhyncha Superfamily: Psylloidea
as a suborder of the Hemiptera. The suborder Calophyllidae
Sternorrhyncha contains four major super Carsidaridae
families: Aleyrodoidea (whiteflies); Aphidoidea Homotomidae
(aphids); Coccoidea (scale insects); and Psylloidea Phacopteronidae
(jumping plant lice). The classification system is: Psyllidae
Order: Hemiptera Triozidae
Suborder: Sternorrhyncha One of the most common characters associated
Superfamily: Aleyrodoidea with the Hemiptera are the modifications seen in
Aleyrodidae-whiteflies the mouthparts that appear to many as being a
Superfamily: Aphidoidea beak. The mandibles, maxillae, labium and
Adelgidae-adelgids labrum are present, but are modified into a ros-
Aphidiidae-aphids trum where the mandibles and maxillae are modi-
Phylloxeridae fied into needle-like or thread-like stylets lying
Superfamily: Coccoidea within a grooved labium. Hemiptera use their
Aclerdidae-flat grass scales mouthparts to feed on plant or animal tissues. The
Asterolecaniidae-pit scales sternorrhynchans share the mouthpart modifica-
Beesoniidae tions, but differ by using their stylets to probe plant
Carayonemiidae tissues intercellularly or intracellularly, and form-
Cerococcidae-ornate pit scales ing a protective sheath from secreted saliva around
Coccidae-soft scales the mouthparts.
Conchaspididae Many of the sternorrhyncans are phloem feed-
Dactylopiidae-cochineal scales ers with a diet rich in carbohydrates and deficient
Diaspididae-armored scales in amino acids and other nitrogenous materials. To
Eriocococcidae-felt scales compensate for this deficiency, sternorrhynchans
Halimococcidae have endosymbionts (intracellular bacteria or
Kermesidae-gall-like scales fungi) housed in special tissues and contribute to
Kerriidae-lac scales the nutrition of the insect host. Because many

Bugs (Hemiptera), Figure71 Additional representative bugs (Hemiptera): top left, acacia whitefly,
Tetraleurodes acaciae (Aleyrodidae); top right Asian woolly hackberry aphid, Shivaphis celti (Aphididae);
second row left, oleander aphid, Aphis nereii (Aphididae); second row right, twolined spittlebug,
Prosophia bicincta (Cercopidae); third row left, grenade scale, Cerococcus deklei (Cerococcidae); third
row right, ananas scale, Melanaspis bromeliae (Diaspididae); bottom left, Asian citrus psyllid, Diaphorina
citri (Psyllidae); bottom right, thorn bug, Umbonia crassicornis (Membracidae) (all photos by Lyle Buss).
596
B Bugs (Hemiptera)

s ternorrhynchans feed on phloem, too many car- The life cycles of the aphidoids include both
bohydrates are taken in and must be expelled. They asexual (parthenogenic) and sexual reproductive
expel excess carbohydrates by excreting a sugary strategies. Life cycles where sexual generations
substance called honeydew. Honeydew can con- are present are termed holocyclic and those
taminate foliage and serves as a good growth where sexual generations are absent are termed
medium for sooty molds. Sooty molds can detract anholocyclic. There are six stages to development
from the overall appearance of the host plant and for the aphidoids; egg, four nymphal stages and the
can interfere with photosynthesis. Honeydew can adult stage. Morphological differences occur between
also attract ants that may protect the sternorrhyn- and within families. For example, members of
chans from their natural enemies and help in the Eriosoma (Aphidae) can produce cottony wax
removal of excess honeydew secretions. to cover their bodies, whereas other members of
the Aphidae produce no wax. There are three
families (Aphididae, Adelgidae and Phylloxeridae)
Aphidoidea (Aphidoids) with roughly 4,500 known species comprising
the Aphidoidea. The Aphididae (aphids) comprise
Aphids or aphidoids are probably the most the largest family within the Aphidoidea, containing
universally recognized members of the Sternor- roughly 4,300 species. As in the higher classifica-
rhyncha due primarily to their presence on orna- tion of the Sternorrhyncha, there is much debate
mental plants and crops. Members of the on numbers of subfamilies and/or tribes within
superfamily Aphidoidea are best recognized by the Aphididae. There are two genera and roughly
the presence of siphunculi (cornicles) arising 50 species within the Adelgidae. Most adelgids are
from the abdomen. Other key characteristics in found on coniferous hosts and readily induce gall
recognizing aphidoids include: 2-segmented tarsi formation on their hosts. The Phylloxeridae
with the second segment bearing two claws and contain eight genera and approximately 75 species.
the presence of a cauda (equivalent to the lingula Most species primarily occur on oaks (Fagaceae)
found on whiteflies) on the posterior tip of the and hickories (Juglandaceae).
abdomen. Aphidoids are generally soft-bodied
(ranging between 1 and 8 mm in length) and vari-
ously pigmented from yellow to green to brown
and occasionally red. They tend to be gregarious, Aleyrodoidea (Whiteflies)
and live in colonies or aggregations on their host
plants. Both alates (winged) and apterous (with- Aleyrodids or whiteflies are one of the most recog-
out wings) individuals may be present in colonies. nized plant pests in the world with various diseases
Immature stages look like smaller versions of the being transmitted to crops and with the over-
adults. They typically travel short distances to (or whelming numbers of adults present in infested
on) host plants by walking or by being transported crops. A tell-tale sign indicating whitefly presence
by ants. Dispersal over great distances can be is the white cloud that emerges when plant foliage
accomplished through flight or by wind currents. is disturbed. Adult whiteflies derive their common
Most aphidoids feed either on phloem or in the name (aleuro, flour) from the powdery, white wax
parenchyma tissue with most being monoecious secretions that cover their bodies. The adults are
but a few species being heteroecious. Many aphi- small, with wingspans being 4 mm or less. There
doids are pests of crops and some species are are roughly 1,200 described species within the
capable of transmitting viruses such as barley yel- single family of the Aleyrodoidea. The family
lows, plum pox, and various diseases of cucurbits Aleyrodidae is recognized as having two subfamilies:
and melons. the Aleurodicinae and the Aleyrodinae. The
 Bugs (Hemiptera)
B 597

Aleyrodidae are unusual with the subfamilies being mites and lacewing larvae) and parasitic wasps
defined by both adult and nymphal characters, and that are often specific to the whitefly species that
the species are defined solely on the characteristics they attack.
of the puparium. Members of the Aleurodicinae
can be distinguished from the Aleyrodinae by hav-
ing larger adults with more complex wing venation, Coccoidea (Scale Insects)
and also by the presence of large agglomerate wax
pores on the puparium. The coccoids or scale insects comprise the most
Whiteflies typically reproduce sexually, with diverse group within the Sternorrhyncha. They
unfertilized eggs becoming males. There are six derive their common name from the presence of a
stages of development for whiteflies: egg, three thin layer of secreted wax, resin, or other secreted
nymphal instars, pupal instar and the adult. Once materials held over or affixed to the body of the
mating occurs, whitefly females typically lay their insect. Scale insects occur throughout the world
stalked eggs in arcs or circles on the underside of on a wide range of host plants, and many are
leaves. Once eggs hatch, first instars emerge and considered economically important plant pests in
generally settle close to deposition sites. Subse- agricultural crops, urban landscapes, greenhouses
quent development occurs on the underside of and forests. Many have been the focus of a variety
leaves. Economically important species undergo of biology and ecology studies over the years. The
multiple generations in a season, whereas many first example of a successful biological control
benign species usually have only one to two gen- program was with the vedalia beetle on cottony
erations per season. Adult males are interesting in cushion scale (Icerya purchasi). Scale insects
that they perform courtship behaviors prior to (Dactylopiidae) have even been used as biological
mating (abdominal oscillations that cause acous- control agents on prickly pear cacti (Opuntia sp).
tic substrate vibrations). Others such as the pela wax scale (Ceroplastes
Many species are considered economically pela), cochineal insects (Dactylopius sp.) and lac
important. They feed from the plant vascular tissues insects (Kerriidae) have been used to produce
and all feeding stages produce honeydew. Adult commercial products.
whiteflies cue into plant chemicals and colors Scale insects also have many unique biological
(green and yellow). Most host plants are angio- and morphological characteristics. They are a good
sperms, with relatively few hosts being herbs, example of gender dimorphism with the adult
grasses, ferns or palms. Feeding damage from males resembling small flies, with one pair of true
whiteflies can be seen in a myriad of symptoms, wings and a second, but reduced pair. The classifica-
including leaf chlorosis, wilting, leaf drop and tion has primarily been based on the morphology
presence of honeydew. Some species are associ- of the adult female. The adult females are usually
ated with viral disease transmission and the most sedentary and affixed to the host plant. The imma-
serious pests are associated with orchards, crops ture stages are often smaller than the adult life stages
and greenhouses. Probably the most recognized with the dispersal stage (or crawlers) ranging from
significant pest of this group is Bemisia tabaci 300 to 700 m in length and having a flattened
(sweetpotato whitefly). This pest is highly polypha- ovoid body shape. Perhaps one of the most unique
gous and is thought to vector more than 70 and fascinating morphological oddities within the
different viruses (e.g., Gemini virus, melon leaf scale insects can be seen in the ground pearls (Mar-
curl virus). The most virulent form of this species garodidae). They have a quiescent stage where an
is biotype B or B. argentifolii (silverleaf whitefly). immature developmental stage may form a protec-
Generally control of these whiteflies is realized tive covering (cyst) around the body to help in
with the use of non-specific predators (predaceous adverse environmental conditions. Scale insects
598
B Bugs (Hemiptera)

demonstrate a wide range of reproductive systems Some species such as pink hibiscus mealybug
including: hermaphroditism (cottony cushion scale, (Pseudococcidae: Maconellicoccus hirsutus) and
Icerya purchasi), asexual reproduction (up to seven lobate lac scale (Kerriidae: Paratachardina lobata
different types of parthenogenesis) and sexual lobata) have multivoltine (numerous generations
reproduction. Eggs may be laid outside the body per year) life cycles. Others, such as European fruit
underneath a protective covering such as an ovisac lecanium (Coccidae: Parthenolecanium corni) and
(some Coccidae, Margarodidae, Ortheziidae and Indian wax scale (Coccidae: Ceroplastes ceriferus)
Pseudococcidae) or underneath the testa, or scale generally are univoltine. Proper environmental
covering, as seen in many armored scales (Diaspidi- conditions, such as prolonged warm periods and
dae). In others cases, eggs are withheld in the body high humidity, can allow some univoltine species
and live birth occurs (some armored scales and to have more than one generation per season.
members of the Phoenicococcidae). After eggs are laid, and once the crawlers or first
Taxonomically, scale insects have always instars emerge, they will begin searching for
been divided into two informal groups, the suitable feeding sites. They will settle on the natal
archaecococcids and the neocococcids. The host plant, or will be dispersed to other hosts via
archaecococcids are comprised of the Margar- wind currents. Some crawlers have demonstrated
odidae (roughly 400 species), Ortheziidae (ensign behaviors (such as arching their bodies) that aid in
scales, 135 species), Carayonemidae (four species) their ability to become airborne. Once a suitable
and the Phenacoleachiidae (two species). The host is found, crawlers settle (becoming sedentary
archaeococcid grouping is not monophyletic and in many cases) and begin the feeding process.
members of this group share primitive character- Scale insects feed in the phloem or paren-
istics (e.g., retention of abdominal spiracles). The chyma of the host plants. The coccoids demon-
neocococcoids comprise the rest of the coccoids strate the complete spectrum of feeding preference
(17 families, approximately 7,000 species). This ranging from monophagous to oligophagous to
informal grouping is considered monophyletic polyphagous. Primary damage to the host plant
based on derived features such as apical setae on is through sap removal. This process can cause the
the labium, loss of abdominal spiracles. The three plant to have chlorosis in the foliage, premature
largest families of neococcoids are the Diaspididae leaf drop, twig die back and possibly death of
(armored scales, 2,400 species), the Pseudococci- the host plant. Many coccoids produce copious
dae (mealybugs, 2,000 species) and the Coccidae amounts of honeydew. In turn, the honeydew
(soft scales, 1,000 species). Other neococcid families becomes a good growth media for sooty molds
include: Aclerdidae (flat grass scales, approxi- that can hinder photosynthesis of the host plant
mately 50 species), Asterolecaniidae (pit scales, and detract from the aesthetic value of the host.
200+species), Beesoniidae (nine species), Con- A key factor in controlling scale insect infes-
chaspididae (approximately 30 species), Cerococ- tations is detection. Many scale insects are able to
cidae (ornate pit scales, 70 species), Dactylopiidae slip by inspections by being present in very small
(cochineal insects, nine species), Eriococcidae (felt population numbers. Growers and homeowners
scales, 550 species), Halimococcidae (20 species), should attempt to thoroughly inspect their plants
Kermesidae (gall-like scales, 90 species), Kerriidae to insure that populations of scales do not become
(lac insects, 100 species), Lecanodiaspididae established. Control of scale insect infestations is
(false pit scales, 80 species), Micrococcidae (eight realized through a variety of methods: (i) cultural
species), Phoenicococcidae (one species) and the (ii) natural enemies (iii) oils (iv) pesticides. Cul-
Stictococcidae (16 species). tural control methods, such as pruning and
There are species of scale insects that repre- destruction of infested material, can be effective
sent every major cyclic system seen in insects. when populations are at low levels. In some cases,
 Bugs (Hemiptera)
B 599

natural enemies keep populations of scale insects pyricola (transmits fireblight in pears), Bactericera
at low levels. The best scale insect predators are the cockerelli (vectors psyllid yellows in several garden
ladybird beetles (Coccinellidae: Chilocorus, Cryp- crops), and Diaphorina citri (vectors citrus
tolaemus and Rodolia). When crawlers are present, greening disease in citrus).
lacewing larvae can be good predators, but should There is much discussion concerning the
not be relied upon due to their polyphagous taxonomy and numbers of families within the
nature. Most parasitoids that attack scale insects Psylloidea. Here we recognize six families: Calo-
are from the Aphelinidae (e.g., Aphytis sp.) and phyidae, Carsidaridae, Homotomidae, Phacopter-
the Encyrtidae (e.g., Metaphycus sp.). Use of horti- onidae, Psyllidae, and the Triozidae. The majority
cultural oils can be a good support treatment when of the families have very select host ranges:
natural enemies are present. Horticultural oils are Calophyidae feed primarily on plants from the
not as toxic as other pesticides to the natural Anacardiaceae; Carsidaridae are restricted to
enemies. Proper application of oils in conjunction members of the Bombaceae, Malvaceae, and
with natural enemies can suppress and keep scale Sterculiaceae; Homotomidae are restricted to the
populations at levels below the economic thresh- Moraceae; Phacopteronidae feed on plants in
old. Lastly, chemical control is relied on in many the Meliaceae; Psyllidae feed on a wide range of
situations with severe infestations to help reduce hosts.
the scale insect populations. Unlike many of the other sternorrhynchans,
psylloids reproduce solely through sexual means.
They have seven life stages: egg, five nymphal
instars and the adult. Many species occurring in
Psylloidea (Jumping Plant Lice) tropical to warm temperate regions tend to have
multivoltine life cycles. Those species occurring in
The Psylloidea or jumping plant lice are found in northern climates tend to have univoltine or occa-
most regions of the world, with the majority of sionally bivoltine life cycles. Psylloids tend to
species present in tropical regions. Psylloids are migrate or disperse over short distances by jump-
the most attractive of the sternorrhynchans, with ing or flying and much like whiteflies or aphids,
many possessing brilliant color patterns. Psylloid can travel great distances on air currents.
adults are very small, ranging from less than 18 mm Many species are specialists as nymphs, often
in length, and often resemble miniature cicadas. feeding on a particular plant structure on a specific
The immature stages closely resemble the adult life host. Feeding preference exhibited by the adults
stage but lack wings. Immatures from the Psyllidae differs from that of the immature stages. They are
can occur on the surface of the host plant, within a typically polyphagous but host plants are generally
gall or within lerps. Lerps are protective cover- defined as those that the immature stages can
ings formed from exudates from the immatures develop. Like other sternorrhynchans, psylloids
(liquid feces and wax filaments). produce honeydew that attracts ants that benefit
The common name (jumping plant lice) the psylloids by potentially driving away their
refers to the ability of the adults to jump natural enemies.
backwards when disturbed. All members of this
superfamily feed primarily on the phloem of
woody-dicotylendonous plants. Many members Suborder Fulgoromorpha
of the Psylloidea are plant pests. Damage from
psylloids can be in the form of galls, stunting or Fulgoromorphans, or planthoppers, are common
poor plant growth. In some instances, psylloids in nearly all habitats and some are either bizarre or
can transmit diseases. Examples include Cacopsylla spectacular in form. They occur throughout the
600
B Bugs (Hemiptera)

world, although most are from the tropical and the family Fulgoridae, all from subtropical and
subtropical regions. All species are plant sap tropical regions. Both adults and nymphs feed
feeders. Some feed on trees or shrubs, others prefer above ground on their host plants, which are usu-
lower-growing grasses or sedges. Some feed under- ally are dicots. These insects range from 4 mm to
ground on plant roots; still others feed on ferns or 10 cm in length with wingspans of up to 15 cm. In
on fungi growing under bark or on moist logs. some species the hind wings have large colorful
Some planthopper species are of agricultural eyespots, designed to startle potential predators.
importance because of the plant pathogens they The most distinctive feature in many fulgorids is
transmit when feeding, or because of the sooty the bizarre shape of their head, which can be long
mildew promoted by their sugary exudates and toothed, slender, or bulbous. In Fulgora, the
(honeydew). One species has caused, if indirectly, lantern bug, the head resembles a crocodiles head,
cases of poisoning in humans. Analysis of molecu- complete with false eyes, nostrils and teeth. Despite
lar data and new interpretations of morphological its name, the head of Fulgora does not glow. Most
characters of both adults and nymphs strongly likely, though, they mimic lizards, positioning
support the monophyly of the Fulgoromorpha. themselves vertically with the head uppermost,
About 12,000 planthopper species have been just as lizards do. Another family of planthoppers
described and arranged into 20 families, the larg- in which both adults and nymphs feed above the
est and most economically important being Del- ground is Dictyopharidae, the sister group of the
phacidae. Since only a few families have been Fulgoridae. The 600 described species ranging in
shown to be monophyletic, this classification will length from 3 to 33 mm are found throughout the
surely be modified in the future. world. Most dictyopharids are green or brown and
Order: Hemiptera have a long head projection referred to as a cephalic
Superfamily: Fulgoroidea-planthoppers horn. A few species have modified front legs that are
Fulgoridae broad and flat. Most species are monophagous and
Dictyopharidae feed above ground on their hosts, primarily dicots.
Flatidae Flatids are the next most spectacular hoppers,
Hypochthonellidae especially those in the tropics. They range from 4 to
Issidae 32 mm in length and their front wings, which are
Acanaloniidae broad, blunt-ended and opaque, and have many
Caliscelidae cross veins in the costal area, may be pink, red, yel-
Nogodinidae low, green, white, brown, black, and plain, stripped,
Tropiduchidae or spotted. Sexual dimorphism is not uncommon.
Delphacidae Mostly pantropical but occurring world wide, Flati-
Cixiidae dae is a large family of more than 1,000 species
Derbidae related most closely to the Tropiduchid group of
Achilixiidae families, Issidae, Nogodinidae, and Tropiduchidae.
Achilidae Most species of flatids feed on woody dicots, above
Kinnaridae ground, and many are polyphagous. Nymphs and
Meenoplidae adults of many species feed together in large groups,
Tettigometridae the nymphs protecting themselves by producing
Lophopidae long, curly wax threads on the surfaces of their
Eurybrachidae bodies. Metcalfa pruinosa (Say), a polyphagous
Ricaniidae species from the United States, was introduced into
The most spectacular planthoppers are the fulgo- Italy in the late 1970s and is causing damage espe-
rids. Seven hundred and fifty species are known in cially to grapes in southern Europe. Wax from the
 Bugs (Hemiptera)
B 601

nymphs covers the fruit, and their honeydew pro- date palms in the Middle East because it can result
motes the growth of sooty mold. Hypochthonelli- in the death of the plant.
dae, a family composed of only two species in Delphacidae is the largest family in Fulgoro-
Africa, is presently considered as a subgroup within morpha, with nearly 2,000 species worldwide.
Flatidae. Hypochthonella caeca China & Fennah is Delphacids are small (210 mm in length), usually
the only known true subterranean fulgoroid, and brown or greenish planthoppers. They are charac-
has reduced wings and eyes and lacks ocelli. Both terized by a hind tibia with triangular cross-section
adults and immatures are found in the soil, where coupled with an articulated spur at its distal end.
they feed on roots of plants. Delphacids are important pest species because
The majority of the 1,000 described species in they feed on monocots that include rice, wheat,
the family Issidae feed as adults and nymphs on corn, and sugarcane. Many of them cause more
trees and grasses, above-ground. They are widely damage by vectoring viral diseases than by direct
distributed, although the majority are found in feeding.
tropical regions. More issids are monophagous The most economically important delphacid is
than polyphagous. Most adults, which are between the brown planthopper Nilaparvata lugens (Stl).
2 and 8 mm in length, are dark-colored with Since the early 1970s, this species has been the most
opaque wings. Some appear beetle-like due to their serious pest of rice in South East Asia, the Pacific,
tough, short front wings. Some even resemble New Guinea, India and Sri Lanka. It can travel long
weevils because of a long snout-like structure and distances, assisted by strong wings, reaching Korea
expanded forelegs. Acanaloniidae (about 80 species), and Japan from China. It transmits a virus (grassy
a group presently considered within Isiidae, are stunt disease) to rice, a crop that feeds at least 60%
hoppers that resemble flatids, except that they do of the world.
not have the many cross veins in the costal area of The nymphs of cixiids, derbids, achilixiids,
the front wings characteristic of Flatidae. They feed achilids, kinnarids, and meenoplids are thought to
on grasses and herbaceous plants. have their nymphal stages cryptic or associated
Another group of hoppers that resemble weevils with soil, or in spaces under bark or on logs, rather
is Caliscelidae. They previously were placed within than being in the open on the plants as are the
Issidae, and are a small family found worldwide. adults. With almost 2,000 species, Cixiidae is one
Caliscelids are small (15 mm long) and brachypter- of the largest families in Fulgoromorpha. Cixiids
ous. They are known to feed on grasses, sedges, and are found in all regions of the world. Adults (rang-
palms, and some are associated with ants. ing from 3 to 13 mm in length) look superficially
Nogodinidae is a primarily tropical family of like minute cicadas, being slightly broad and flat
approximately 150 species, 417 mm long, that and with clear, membranous wings held at a low
feed as adults and nymphs above ground on angle over the body when at rest. The nymphs feed
woody dicots; all known species are monopha- on the roots of grasses and herbaceous plants, on
gous. It is unknown at present if this group is fungi on rotten wood, or on ferns, while adults
monophyletic. feed on a variety of tree and shrub species. Some
Tropiduchidae has about 350 species described, nymphs have been found in association with ants.
ranging in length from 5 to 13 mm; this family is Nymphs in the genus Oliarus are subterranean.
primarily pantropical but occurs worldwide. Tropi- In Hawaii, nymphs of Oliarus live in caves and
duchids usually have an oddly shaped head and feed on roots while protecting themselves with a
wings of variable color patterns. Both adults and cocoon of wax filaments. As adults, they move
nymphs feed above-ground, usually on understory through the caves holding to the rock walls with
plants in moist, tropical forests. The Dubas Bug, the help of modified pretarsal claws. Some species
Ommatissus lybicus (Bergevin), is the worst pest of are blind, unpigmented, and flightless.
602
B Bugs (Hemiptera)

Cixiids are economically important because Kinnaridae, have been found in caves. Eighty
they can transmit plant diseases. One species, species have been described, mostly from the
Myndus crudus Van Duzee, acts as disease vector Ethiopian and Oriental tropical regions. Adult
for the phytoplasma that causes Lethal Yellowing, a meenoplids are very small, flattened planthoppers
lethal disease of palms, including the coconut palm. that range from 3 to 7 mm in length. Most adults
It was first reported (1830s) in the West Indies and feed on monocots, the majority of the species
later appeared in the Florida Keys (1950) and in feeding across several families (they are among
other areas of the United States. It has now spread the most polyphagous in Fulgoromorpha).
to others parts of the world. Other cixiids are Tettigometridae is a small family of less than
suspected of also transmitting this disease. 100 species, sized 311 mm, that occurs in the
Derbids (4mm) are planthoppers with long, Ethiopian and Palearctic regions. The nymphs of
narrow, fragile wings, sometimes white or brightly most species live underground in groups feeding
colored. More than 800 species of Derbidae exist on plant roots, while adults live on foliage, mostly
worldwide, primarily in the tropical and subtropi- dicots. In some species ants attend the nymphs.
cal regions. Adults of these bugs have been found Lophopidae includes about 140 described
feeding on fungi associated with plant or wood species, 515 mm long, nearly all from the Old
decay, on flowering plants, on palms and on a few World tropics. Their wings are usually opaque tan
deciduous trees. Nymphs are thought to be or brown. Pyrilla spp., which feed on monocots
obligate fungus feeders. Members in the group that include sugarcane, corn and rice, are serious
called moth derbids congregate on one leaf and sit sugarcane pests in India.
characteristically with their wings held flat against Eurybrachidae (729 mm long) is a tropical
the underside of the leaf. family of about 200 species with opaque tan or
More than 350 species of Achilidae (recog- brown rectangular wings. The group occurs in
nized by the overlapping tips of the front wings) the Australian, Ethiopian and Oriental regions.
have been described throughout the world. Adults, Adults and immatures are monophagous and
which range from 3 to 13 mm in length, feed on feed above ground; one example is Platybrachys
the phloem of trees or shrubs while the nymphs leucostigma Walker from Australia, which feeds
are thought to feed on fungi in holes in logs, or on Eucalyptus maculatus. The front wings of
under loose bark, or in decaying vegetation. some species are shaped and colored at the apex
Achilixiidae is a small tropical family with 24 to look like a head, some complete with false
described species ranging from 4 to 8 mm in antennae.
length. Achilixiid planthoppers are known from Gengid planthoppers are found only in
the Neotropics, Philippines, and Borneo. Some South Africa (two species described), believed
include Achilixiidae within Achilidae, but their by some authors to belong within the family
placement is uncertain at present. Eurybrachidae.
Forty species have been described in the Ricaniids (380 species) range from 4 to 12
family Kinnaridae (24 mm in length) mostly mm long with their wings, when spread, reaching
from the Neotropical and tropical Oriental up to 30 mm in some species. These are moth-
regions. Nymphs feed on roots and some are cave like planthoppers found in the warmer parts of
adapted; most adults feed from the upper portion the eastern hemisphere. They feed above ground
of plants, usually dicots. Some species lay their primarily on dicots, although some feed on
egg masses in the soil or on wood, and cover monocots or ferns, with polyphagy common.
them with water repellent waxes. The nymphs of Some species damage ornamental and agricultural
Meenoplidae, the sister group of the Kinnaridae, crops. A species that occasionally causes poison-
are also associated with soil and some, as in ing in humans is Scolypopa australis Walker, a
 Bugs (Hemiptera)
B 603

ricaniid from Australia, now also found in New Melizoderidae

Zealand. This species occasionally feeds on the Cicadellidae-leafhoppers
poisonous plant Coriaria arborea and produces Myerslopiidae
honeydew that, in time of low nectar, may be
collected by honey bees. This honey is poisonous
to humans. Cicadoidea-Cicadas

Cicadas are large insects, reaching lengths of 10

cm, although some are as small as 1 cm. Approxi-
Suborder Cicadomorpha mately 4,000 species are known, if not all described.
With a stout body, broad head, large compound
The suborder Cicadomorpha has three superfami- eyes, and long, usually transparent wings, they are
lies with about 30,000 species described, all of which easily recognized. They are also known for their
are terrestrial plant-feeders. They are extraordi- loud singing, which usually takes place during the
narily diverse and ubiquitous. The most familiar day or at twilight, males calling to attract the
insects in this group are the cicadas (Cicadoidea), females. Each species has a characteristic song
the largest and loudest insects in Cicadomorpha. produced by an enlarged abdomen that serves as
Cercopoidea includes the two-striped froghopper, the resonating chamber.
Prosapia bicincta (Say), a cercopid native to the Although cicadas occur from the tundra to
southeastern United States that damages forage the tropics, they are most diverse and abundant in
and turf grasses and some ornamentals. Within the tropical regions. Both adults and nymphs
Membracoidea are two important groups, the usually feed on xylem from trees and shrubs, and
Cicadellidae, which is considered the tenth largest are commonly polyphagous. Nymphs are entirely
family of insects, as well as one of the most abun- subterranean, possessing digging front legs,
dant, and the Membracidae, which includes some feeding usually on perennial roots, and emerging
of the most fantastically designed insects. Cicado- after several years in the soil to molt into adults.
morpha is considered a monophyletic group. It was Some cicadas are able to be active at temperatures
previously placed in Auchenorrhyncha together that would induce torpor in other insects because
with Fulgoromorpha. The classification of Cicado- they are facultatively endothermic. They can warm
morpha is: themselves through shivering of flight and/or
Order: Hemiptera tymbal muscles or cool themselves by releasing
Suborder: Cicadomorpha-cicadas, spittlebugs, water (i.e., evaporative cooling). Within the family
leafhoppers and treehoppers Cicadidae, the most famous might be the gregari-
Superfamily: Cicadoidea: cicadas ous periodical cicada (genus Magicicada, seven
Cicadidae-cicadas species) from the eastern United States. Broods
Tettigarctidae: hairy cicadas emerge simultaneously in millions at intervals of
Superfamily: Cercopoidea-froghoppers either 13 or 17 years. These cicadas can cause
Aphrophoridae considerable damage to trees. The damage is done
Cercopidae-spittlebugs by the egg-laying females, which cut slits in twigs
Clastopteridae to insert their eggs. In Australia, sugarcane can be
Machaerotidae tremendously damaged (even shredded) when
Superfamily: Membracoidea-treehoppers and thousands of cicadas oviposit in a single crop.
leafhoppers Two species of importance are the Brown Buzzer
Membracidae-treehoppers (Cicadetta crucifera [Ashton]), also known as the
Aetalionidae Brown Sugarcane Cicada, and the Grass Fairy
604
B Bugs (Hemiptera)

(Parnkalla muelleri [Distant]), also known as the clover, and alfalfa. Some species are capable of
Yellow Sugarcane Cicada, both of which become transmitting pathogens. Most froghoppers live
abundant in sugarcane fields in certain seasons. in grasslands with nymphs feeding on roots.
The former lives in open grasslands, and edges of Froghoppers, as a group, are considered the
woodland and mangroves, while the latter species most important pest insects of sugar cane in
prefers areas of open grassland or woodland/ the Neotropics.
scrub habitats. Aphrophoridae is a large family of spittlebugs
Only two species are included in the family distributed worldwide. Not all species produce
Tettigarctidae, both in the genus Tettigarcta. One froth or foam as immatures. Some species feed on
species is found only in southeastern Australia legumes and several are of economic importance.
and the second only in Tasmania. Many characters In Australia, the most common and widespread
distinguish this family from Cicadidae, including species is Philagra parva (Donovan), which has a
a large pronotum, eyes close together, simple curved horn on the head.
sound-producing organs (timbals) in both sexes Nymphs of Clastopteridae also hide within
rather than only in males; and no true auditory spittle masses. Some clastopterids are of economic
tympana. Rather than communicating with audi- importance. For example, the pecan spittlebug
ble songs, these cicadas communicate using vibra- (Clastoptera achatina Germar, 2 mm long) heavily
tions through substrate. They are called hairy infests and feeds on terminal shoots of pecan trees,
cicadas because the underside of their body is reducing the nut crop.
densely covered with brown or grey hairs. Also Cercopidae are found worldwide and are
unlike Cicadidae, hairy cicadas remain hidden richly represented in the tropics, where they
during daylight hours. are the most brightly colored. Nymphs live
within spittle masses, explaining their common
name spittlebugs. They feed on shrubs, trees,
and herbaceous plants, but some prefer grasses.
Cercopoidea-Froghoppers The largest cercopids (including Megastethodon
urvillei [Le Pelletier and Serville]) are found in
Cercopoidea is the least studied lineage of Australia and New Guinea, and may reach up to
Cicadomorpha, with about 3,000 species known. 20 mm. Spittlebugs are considered the most
They are found almost worldwide, with highest important pest insects of Neotropical sugar
diversity in the tropics. Their anterior wings are cane. A grassland spittlebug, Prosapia simulans
coriaceous and many, especially in the tropics, (Walker), is a threat to sugarcane and forage
are of contrasting colors of red with black or grasses and also feeds on many of the major
yellow. Their hind legs are long and adapted for forage grasses, including corn, and also on some
leaping, hence their common name froghoppers. non-graminoid hosts. It is known from the
The hind tibiae are long and have one or two lowland tropics from Mexico to Panama but has
stout spines and a single or double row of spines now been found in Venezuela and Colombia. It
at the apex. Some species are gregarious. Nymphs threatens sugarcane crops in southern United
are mostly stationary and hidden, protected from States, which already is under attack from the
desiccation and parasites by a fluid secreted from native froghopper, Prosapia bicincta (Say).
epidermal glands in the abdomen, which is C ercopids are also important because they are
converted into foam (spittle) with expelled air. capable of vectoring Xylella fastidiosa, a bacte-
Most species feed on sap from herbaceous plants, rium that affects many economic plants in the
but some feed on trees. Some are of economic world, including citrus, maple, coffee, grape,
importance, causing damage to pecans, cotton, and others.
 Bugs (Hemiptera)
B 605

Machaerotidae is a small family restricted to exposed to extreme heat and when predators tend
the Oriental region, tropical Africa, and Australia. to be inactive. For defense, nymphs feed among
The nymphs do not live within spittle masses, but adults. The nymphs of some species are attended
live instead within calcareous tubes attached to by ants. Parental care is common (egg guarding,
the host plant, immersed in their liquid excretions. principally) in Membracidae.
A new classification has recently been proposed Aetalionidae also feed on trees, are gregari-
for Cercopoidea, with three families, Cercopidae, ous, are commonly tended by ants, or by Meliponi-
Clastopteridae (including machaerotid froghop- nae bees, and display parental care. Some are as
pers), and Epipygidae, a new family from the long as 28 mm; the beak extends to the hind coxae.
Neotropics. In this classification the family Their pronotum and sometimes their head have
Aphrophoridae is not considered monophyletic cuticular expansions, but some resemble cicadel-
and its genera are divided among the other lidae or cercopidae. This family of 44 described
families. species is Neotropical, except for two species found
in the south of the Himalayas. The genus Aetalion,
which resembles a large cercopid, occurs in Flor-
Membracoidea-Treehoppers and ida, Arizona and California.
Leafhoppers Melizoderidae is a very small family of eight
species known only from Chile and Argentina.
Membracoidea is a monophyletic group com- The pronotum has a unique, somewhat conical
prised of approximately 25,000 described species shape. Nothing is known of their biology. This
in five or more families. It is the most diverse of family is considered a distinct lineage between
the Cicadomorpha superfamilies. Membracidae Cicadellidae and Membracidae.
(up to 12 mm long and with 3,200 species) are Cicadellidae, with more than 20,000 described
extremely diverse in tropical America, where they species worldwide, is the largest family in Hemip-
occur in rainforests, savannas, and deserts. Adults tera and the tenth largest family of insects. Since
have cuticular expansions on the pronotum that most species are likely undescribed, an estimate of
often extend over the abdomen. The pronotal the family size is not possible at present. The spe-
modifications range in shape from simple (spines, cies richness is highest in the tropics. Cicadellids
horns) to fantastic, which sometimes differ in are 322 mm long, with narrow and often colorful
males and females of the same species. Membrac- wings, with posterior tibia prismatic in cross-sec-
ids feed primarily on trees and shrubs. Many spe- tion and with spines. For defense they rely mostly
cies are gregarious, with young and adults feeding on agility, for they jump and fly. Some leafhoppers
together. Much has been speculated on the func- are Batesian mimics of bees or wasps; that is, by
tion of the pronotal expansions. Some shapes shape, coloration, and even behavior they mimic
might provide protection in the form of mimicry bees or wasps. For example, leafhoppers in the
of their host, looking like thorns (as in Umbonia), genus Lissocarta and Propetes imitate paper wasps
seeds, or bark; others mimic ants or wasps, as in (Vespidae), and the genus Teletusa imitates bees
Cyphonia. Some have aposematic (warning) col- in the family Megachilidae. A trait unique to
oration. Others might be protected from verte- Cicadellidae among all insects is the production
brate predators by their spiny projections; all those of brochosomes, small protein-lipid particles of
with pronotal expansions might survive mutila- intricate structure produced by cells in the
tion from predators. However, the latest theory is Malpighian tubules. They actively spread this
that it has a thermoregulatory function, providing material over their body, wings, and legs and
large surfaces for water evaporation. Treehoppers also on their eggs. There is some evidence that
tend to be active during the day, when they are this material serves to form a protective layer
606
B Bugs (Hemiptera)

that repels water or honeydew and prevents a simple color pattern. Most species lack hind
fungal infections. wings and feed on the roots or root-necks of
Cicadellid leafhoppers are of major agro- plants, hiding in the soil, although a few feed on
nomic importance because they can injure plants shrubs and trees.
in several ways, including the transmission of
pathogens. Scaphoideus titanus Ball (56 mm
long) is an example of a cicadellid that can cause Suborder Coleorhyncha-Moss Bugs
diseases. It is able to transmit phytoplasmas
(unicellular organisms without a rigid wall) to The suborder Coleorhyncha contains the single
grapevines if they fed previously on infected family Peloridiidae, considered the sister group of
plants whether as young or as adult. This North the Heteroptera. Their distribution is limited to
American species was accidentally introduced to the Southern Hemisphere. Twenty-five species
France in 1960 and has spread throughout have been described from eastern Australia,
southern and eastern Europe, reaching Spain and Tasmania, Lord Howe Island, New Zealand, New
Portugal in 2000. The phytoplasma disease called Caledonia, Chile and Patagonia in Argentina; they
Golden Flavescence is of considerable economic may also occur in New Guinea. Peloridiids
importance, and has been already found in Spain, resemble planthoppers but have hemelytron-like
France and Italy. forewings. Adult peloridiids are small (between 2
Pierces disease is a lethal grapevine disease and 4 mm long), flattened, oval, greenish or
caused by Xylella fastidiosa, one of the most brownish. Among their unique characteristics are
significant disease-causing pathogens in the the broad head and the pronotum with lateral
Americas. This bacterium causes water stress areolate expansions. They are primarily phytopha-
due to vascular occlusions by aggregates of the gous on mosses, thus known as moss bugs, and
bacteria. Different strains of this species attack usually live in moist habitats such as damp leaf
different hosts, which include citrus, coffee, elm, litter on forest floors with mosses, liverworts, and
oak, oleander, maple, sycamore, almond, alfalfa, decaying trunks but a few species have been found
peach, grape, and others. The primary vectors in caves.
for Pierces disease are cicadellines, or sharp-
shooters. Homalodisca coagulata (Say) (the
glassy-winged sharpshooter) is an important Suborder Heteroptera
vector of Xylella fastidiosa in the southeastern
United States. Recently, it has become established Heteroptera are the only insects correctly called true
in California, where it is threatening the large bugs. This is the most abundant and biologically
wine industry because of increased spread of diverse group of insects with incomplete metamor-
Pierces disease. phosis. Species of Heteroptera are characterized pri-
Myerslopiidae are a small family found only marily by having the first pair of their wings divided
in New Zealand and South America. These into two areas (hence the name Heteroptera, differ-
leafhoppers inhabit forests, and both adults and ent wings), one part thickened and opaque and the
nymphs living in leaf litter and soil with high other part membranous and usually transparent.
organic content. This family has less than 20 Most true bugs are diurnal plant-feeders with well
species. developed eyes and wings, although many variations
A group of archaic cicadellids, with 120 spe- and exceptions exist. Some species are of agricultural,
cies, is treated by some as a family named veterinary, or medical importance. Heteroptera are a
Ulopidae. They are 2.512 mm long and have relatively small monophyletic group of approxi-
stiff front wings that are either plain or that have mately 37,000 described species with at least 25,000
 Bugs (Hemiptera)
B 607

yet to be described. Although they are arranged Microphysidae

among 88 families, the classification will undergo Joppeicidae
changes in the future. Presently the suborder Het- Thaumastocoridae-palm bugs
eroptera is divided into seven infraorders, as follows: Miridae-plant bugs or leaf bugsTingidae-lace
Infraorder: Enicocephalomorpha: unique headed- bugs
bugs Medocostidae
Aenictopecheidae Nabidae-damsel bugs
Enicocephalidae-unique headed-bugs Lasiochilidae
Infraorder: Dipsocoromorpha Plokiophilidae-web lovers
Ceratocombidae Lyctocoridae
Dipsocoridae-jumping ground bugs Anthocoridae-minute pirate bugs or flower
Hypsypterygidae bugs
Schizopteridae Cimicidae-bed bugs
Stemmocryptidae Polyctenidae: bat bugs
Infraorder: Gerromorpha: semiaquatic bugs Infraorder: Pentatomorpha
Mesoveliidae-water treaders Superfamily: Aradoidea
Hebridae-velvet water bugs Aradidae-bark bugs
Paraphrynoveliidae Termitaphididae
Macroveliidae Superfamily: Coreoidea
Hydrometridae-marsh treaders Alydidae-broad-headed bugs
Hermatobatidae-coral treaders Coreidae-leaf-footed bugs
Veliidae-small water striders Hyocephalidae
Gerridae-water striders and pond skaters Rhopalidae-scentless plant bugs
Infraorder: Nepomorpha: water bugs Stenocephalidae
Belostomatide-giant water bugs Superfamily: Idiostoloidea
Nepidae-water scorpions Idiostolidae
Gelastocoridae-toad bugs Henicocoridae
Ochteridae-velvety shore bugs Superfamily: Lygaeoidea
Corixidae-water boatmen Artheneidae
Potamocoridae Berytidae-stilt bugs
Naucoridae-creeping water bugs Blissidae-chinch bugs
Aphelocheiridae Colobathristidae
Notonectidae-back swimmers Cryptorhamphidae
Pleidae-pygmy back swimmers Cymidae
Helotrephidae Geocoridae-big-eyed bugs
Infraorder: Leptopodomorpha Heterogastridae
Aepophilidae-marine bugs Lygaeidae
Saldidae-shore bugs Malcidae
Omaniidae-intertidal dwarf bugs Ninidae
Leptopodidae-spiny shore bugs Oxycarenidae
Infraorder: Cimicomorpha Pachygronthidae
Pachynomidae Piesmatidae
Reduviidae-assassin bugs (includes ambush Rhypharochromidae
bugs, kissing bugs, thread-legged bugs) Orsillidae
Velocipedidae-fast-footed bugs Ischnorhynchidae
608
B Bugs (Hemiptera)

Superfamily: Pentatomoidea The scutellum, which means little shield, is a

Acanthosomatidae-shield bugs triangular part of the thorax seen dorsally between
Aphylidae the first pair of wings. The shape and size of the
Canopidae scutellum is highly variable among true bugs and
Cydnidae-burrower bugs is frequently used for purposes of classification. In
Dinidoridae the Scutelleridae (at least 450 species worldwide),
Lestoniidae the scutellum is so large that it covers the entire
Megarididae abdomen and wings. These insects, known also as
Pentatomidae-stink bugs shield bugs, are among the most spectacular of all
Cyrtocoridae Heteroptera, some species being iridescent or
Phloeidae metallically colored. All shield bugs are plant
Plataspidae feeders; some are of agricultural importance.
Scutelleridae-shield bugs Heteropterans are characterized by elongate
Tessaratomidae-giant shield bugs mouthparts in the form of a segmented beak, or ros-
Thaumastellidae trum, used for sucking fluids. The beak has two
Urostylidae channels, one through which saliva (a fluid with
Superfamily: Pyrrhocoroidea enzymes) is pumped to predigest and liquefy their
Largidae food and the other through which fluids are sucked.
Pyrrhocoridae-cotton stainers Because their beak is located far forward on the
Heteropterans differ from other Hemiptera lower surface of the head, in contrast with the other
by their characteristic wings, mouthparts, scutel- hemipterans, the heteropteran beak is versatile,
lum, and scent glands. They have two pairs of allowing them to exploit a great variety of resources,
wings; the first pair is held flat over their body, including plants, other arthropods, carrion, tadpoles
above the second pair of wings, which are or small fish, and even blood from vertebrates.
membranous and transparent. The design of the Nearly all heteropterans have scent glands that
forewings is a compromise between the needs for produce pungent chemicals used primarily for
efficient flight and protection. The cuticle of the defense. In adults, the external openings of these
corium and clavus is thickened for protection but glands are located on each side of the thorax between
these wing parts are also shaped and hinged for the second and third pairs of legs. The openings end
facilitating and controlling flight. The wing mem- in a variety of grooves, lobes and spouts that allow
brane is thin and usually transparent. All parts of the evaporation of the noxious chemicals. These
the wing, including corium, clavus, and membrane, external structures are distinctive in many groups
are supported by veins. Some adults have lost their and are commonly used for classification or identifi-
wings entirely, while others are winged but are cation purposes. Some bugs lack functional scent
unable to fly due to flight muscle reduction. Many glands; for example, members of the family Rhopali-
species of Gerridae (500 species worldwide), an dae (about 210 species described) are commonly
aquatic group known as water striders, are wing- referred to as scentless plant bugs.
less. In other true bugs, the wings are variously
modified or strongly abbreviated. An example of a
group with modified wings is the rarely encoun- Defense
tered family Schizopteridae (120 described species
worldwide). Schizopterids resemble tiny beetles Heteropterans are in general highly mobile, diurnal
due to their near-black coloration, compact and insects with well developed compound eyes. This
rotund shape, and uniformly sclerotized, shell-like mobility allows them to find new hosts and allows
forewings. them to escape potential predators or parasites.
 Bugs (Hemiptera)
B 609

True bugs escape predators by flying (e.g., stink are generally not effective in the transmission of
bugs, plant bugs, leaf-footed bugs), dropping plant diseases. The damage caused to plants is
(e.g., lace bugs, shield bugs); burrowing (e.g., bur- usually direct, by feeding on the reproductive parts
rower bugs or cydnids); running (e.g., shore bugs, of the plants such as flowers, ovaries, developing
seed bugs, water striders), moving into narrow fruits, or ripening or mature seeds. Some species,
places (e.g., flat bugs, chinch bugs, palm bugs, however, cause indirect damage by feeding on
bed bugs), hopping (e.g., toad bugs), jumping stems and roots, forcing the plant to repair dam-
(e.g., schizopterids), or swimming (e.g., water aged tissue. Feeding with a beak allows them to
boatmen, giant water bugs, velvet water bugs). bypass many of the plants defenses (wax, thorns,
Aside from their mobility, the main defense spines, setae, tannins) as well as most pesticides,
employed by true bugs is the secretion of a which are most effective against insects that bite
noxious chemical which serves to repel enemies, and chew. Most of the species in the family Miridae,
especially ants, which are important predators. or plant bugs, (approximately 10,000 described
Other natural enemies include lizards, birds, species, or one-third of all Heteroptera), are
frogs, spiders, and other insects. Other defense phytophagous. Many species in this family are of
mechanisms known among Heteroptera are significant economic importance. Most mirids
biting (e.g., assassin bugs, damsel bugs, creeping feed on growing portions of the plant such as
water bugs, and others), sharp spines on the flowers, buds, pollen, or new foliage. A few, however,
thorax (e.g., some stink bugs, assassin bugs, and feed on both plant and animal material. Most
others), cryptic shapes and colors (e.g., ambush rhyparochromids are mature-seed feeders, inject-
bugs, most seed bugs, leaf-footed bugs, toad ing enzymes into the seed where the nitrogen-rich
bugs, and others), mimicry (e.g., ant mimetic contents are liquefied and predigested. Most rhyp-
seed bugs and others), aggregation (e.g., immature arochromids feed on fallen seeds, although some
leaf-footed bugs, scentless plant bugs, cotton feed on mature seeds while still on the plants;
stainers), and aposematic, or warning, coloration some are of occasional economic importance
(e.g., nymphs of scentless plant bugs, milkweed because they can feed in large numbers. Oncopel-
bugs, assassin bugs). Some bugs simply stay very tus are colorful lygaeids that feed on maturing
still to avoid being noticed, such as the narrow- seeds of the milkweed plant, the same plant known
bodied bugs marsh treaders, stilt bugs, water as primary host of the Monarch butterfly caterpil-
scorpions, and the spider-web inhabiting lars. An example of stem feeding is presented by
reduviids. Members of the Coreidae are Blissus, the famous chinch bugs, known by home-
outstanding in their fantastic shapes and colors. owners as major lawn pests; they often feed in
Some designs function as disruptive coloration great numbers and kill large patches, occasionally
in which the outline of the insect is obscured by wiping out entire lawns. Extensive biological
contrasting color patterns. studies have been done on this pest. Cydnids are
soil-inhabiting bugs that feed on the roots of
plants, hence their name, burrower bugs. Aradids,
Feeding or bark bugs, feed on the mycelia of various fungi
under tree bark. Tingidae, or lace bugs, are entirely
About 60% of all true bug species are plant feeders, phytophagous, usually found in large numbers on
some of which are of great economic importance. mature foliage. Many species attack and damage
The remaining 40% are predatory or ectoparasitic. important ornamental plants. All species of lace
Because of their method of feeding, in which they bugs of economic significance are in the subfamily
insert their beak stylets into tissues between cells Tinginae, comprised of delicate and beautiful
to suck juices rather than directly into cells, they forms with lacelike appearance.
610
B Bugs (Hemiptera)

Of all hemipterans, only heteropterans feed on T. maculata, T. pseudomaculata, T. rubrovaria,

both other arthropods and on vertebrates. Exam- T. sordida, and Rhodnius prolixus, ecuatoriensis,
ples of predaceous bugs are the back swimmers and pallescens. All feed at night on humans or
(Notonectidae, 343 species recognized) that feed on their pets, and hide during the day, often inside
insects trapped in the water surface; damsel bugs human habitations. Cimicids, or bed bugs (about
(Nabidae, 500 species) that feed on insects among 100 species), are hematophagous as well, acting
foliage and on the ground, or on insects caught in as temporary ectoparasites on bats, humans, and
spider webs, and ambush bugs (Phymatinae, 281 birds or rodents living in groups. All are wingless
species in the family Reduviidae) that commonly and the majority feed on bats. They spend most
hide on or below flowers waiting for pollinating of their time in crevices and other hiding places
insects such a flies or bees, although other insects near their hosts, remaining on the host only while
are attacked as well. Other reduviids, within the feeding. They can be found in the bedroom, bed,
subfamily Emesinae, can walk on spider webs and and among the bedclothes. Bed bugs exist wher-
feed on spiders. Geocorids (219 species described), ever humans live. Much research has been con-
known as big-eyed bugs, prey on other insects and ducted on the two cimicid species, both known
have proven useful in biological control programs. as the bed bug, Cimex hemipterus and Cimex
A unique group of predatory insects are water strid- lectularius. Most bed bugs do not serve as vectors
ers in the subfamily Halobatinae, which inhabit an of pathogens of human or animal disease. Their
usual marine habitat, the surface of the ocean, both importance is generally as a nuisance pest,
near the shore or far out at sea. Plokiophilids, or although large populations can result in serious
web lovers, live either on spider webs to steal the loss of blood. The word bug is derived from the
spiders prey, or with web-spinners (insect order Anglo-Saxon bugge, which almost certainly
Embioptera) feeding on the eggs and weak or dead referred to the bed bug.
individuals; their tarsi (feet) are adapted to walking
on webs. Some aquatic bugs (Belostomatidae or
giant water bugs, and Nepidae or water scorpions) Development and Cytogenetics
feed on other insects, on tadpoles and even small
fish. All species of Polyctenidae, known as bat bugs, Immature heteropterans, called nymphs or larvae,
are ectoparasitic, that is, they feed externally on bats. usually pass through five instars or stages before
Cimicids and lygaeoids in the tribe Cleradini feed reaching the adult, or winged, form. They usually
on vertebrate blood. live in the same habitat as the adults and are com-
monly similar to them in coloration, shape, and
feeding habits. Nymphs of some species form large
Medically Important Species defensive aggregations.
True bugs seem to show a great deal of
Triatomine bugs (more than 110 species) are cytogenetic diversity, including polyploidy of the
nocturnal hematophagous reduviids that feed on autosomes, with the sex chromosome number
the blood of mammals, including humans. The highly variable as well. Sex determination in
insects tend to feed near the mouth area of sleeping Heteroptera is not like that of mammals. The
humans and are thus commonly called kissing majority of the species have a simple XX:XY
bugs. Some species transmit Chagas Disease, an system, though many species have XO males, and
important disease in Latin America caused by some have multiple X and Y chromosomes and
Trypanosoma cruzi Chagas. The most important still are males.
triatomine species are Triatoma infestans, T. san- Aphids
guisuga, T. dimidiata, T. barberi, T. brasiliensis, Cicadas
 Bulb Mites, Rhizoglyphus (Acari: Acaridae)
B 611

Lace Bugs Bulb Mites, Rhizoglyphus (Acari:

Leafhoppers Acaridae)
Plant Bugs
Planthoppers chyi-chen ho
Scale Insects and Mealybugs Taiwan Agricultural Research Institute, Taiwan-
Spittlebugs Republic of China
Stink Bugs
Treehoppers Bulb mites are mite species of the family Acaridae
Whiteflies that infests the bulb, rhizome, corm and tuber of
plants of Amaryllidaceae, Liliaceae, Iviraceae, Sola-
neae and Cruciferae. Customarily, it refers only to
References mites of the genus Rhizoglyphus. Seventy-three spe-
cies are recorded in this genus over the world. How-
Ben Dov Y, Hodgson CJ (eds) (1997) Soft scale insects: their
biology, natural enemies and control, vol 7A & B. World
ever, only two of them, R. echinopus and R. robini, are
crop pests. Elsevier Press, Dordrecht, The Netherlands, found worldwide, causing serious problems to the
452 & 443 pp culture of numerous crops. R. echinopus has been
Bourgoin Th, Campbell BC (2002) Inferring a phylogeny reported from Argentina (as R. callae), Canada, USA
for Hemiptera: falling into the autapomorphic trap.
In: Holzinger WE (ed) Zikaden: leafhoppers, planthoppers (Texas), Belgium, Denmark, France, Germany, Hun-
and cicadas (Insecta: Hemiptera: Auchenorrhyncha). gary, Italy, Netherlands, Poland, Romania, Russia,
Denisia 4, Biologiezentrum des Obersterreichischen Scotland, Spain, the United Kingdom, Ukraine,
Landesmuseums, Austria, pp 6782
Egypt, Israel, China, India, Iran, Japan, Korea and
Blackman RL, Eastop VF (2000) Aphids on the worlds crops.
An identification and information guide, 2nd edn.Wiley, New Zealand. R. robini has been reported from Can-
Chichester, 466 pp ada, USA, Mexico, China, Japan, Korea, Taiwan, New
Cassis G, Gross GF (1995) Hemiptera: Heteroptera (Coleor- Zealand, Israel, Egypt, Poland and the United King-
rhyncha to Cimicomomorpha). In: Houston WWK
Maynard GV (eds) Zoological catalogue of Australia,
dom. Rhizoglyphys echinopus and Rhizoglyphus rob-
vol 27.3A. CSIRO, Australia, 506 pp ini were not properly distinguished in earlier years,
Denno RT, Perfect TJ (eds) (1994) Planthoppers. Their not until van Eyndhoven set them apart. Conse-
ecology and management. Chapman & Hall, New York, quently, records on these two species in early reports
New York, 799 pp
Dietrich CH, Deitz LL (1993) Superfamily Membracoidea are subject to uncertainty. A third species, Rhizogly-
(Homoptera: Auchenorrhyncha). II. Cladistic analysis phus setosus, is reported to infest various hosts in
and conclusions. Syst Entomol 18:297311 Taiwan. This species was reported first by Manson in
Gillot C 1995 The Hemipteroid orders. In: Entomology.
1972, from New Guinea. It may also be distributed
Plenum Press, New York, New York, pp. 195232
Holzinger WE (ed) (2002) Zikaden. Leafhoppers, planthoppers in countries nearby. Another species, R. hyacinthi,
and cicadas (Insecta: Hemiptera: Auchenorrhyncha). that appeared in early reports causing
heavy loss to
Denisia 4, Biologiezentrum des Obersterreichischen gladiolus and lily is probably not a valid species, as
Landesmuseums, Austria, VIII+556 pp
McGavin GC (1993) Bugs of the world. Blandford, London,
there is neither a well-defined description on this
UK, 192 pp species nor specimens available.
Schaefer CW, Panizzi AR (2000) Heteroptera of economic Acarid mites, in the genera Caloglyphus and
importance. CRC Press, New York, NY, 828 pp Schwiebea, were also found to infest bulbs in the
Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera:
Heteropera): classification and natural history. Cornell 1990s. These mites reproduce on bulbs, and may be
University Press, Ithaca, NY, 336 pp as hard as the Rhizoglyphus species to control. The
Woodward TE, Evans JW, Eastop VF (1970) Hemiptera term bulb mite shall, therefore, include mites of
(bugs, leafhoppers, etc.). In: The insects of Australia.
these two genera. Mites reported under the generic
A textbook for students and research workers.
Melbourne University Press, Melbourne, Australia, name of Caloglyphus actually belong to three gen-
pp 387457 era: Caloglyphus, Cosmoglyphus and Sancssania.
612
B Bulb Mites, Rhizoglyphus (Acari: Acaridae)

Bulb Mites, Rhizoglyphus (Acari: Acaridae), Table 10 List of Rhizoglyphus mites reported as pests, crops
and ornamentals affected, and geographic location
Species Crop affected Country
algericus Gladiolus sp Algeria
alliensis Allium sativum Mexico
allii Allium sativum China
caladii Caladium sp New Guinea
costarricensis Oryza sativa Costa Rica
echinopus Allium bakeri Japan
Allium cepa Argentina (as R. callae), India,
Russia
Allium sativum India, Korea, New Zealand,
Romania, Spain
Capsicum sp India
Curcuma domestica India
Freesia sp UK
Gladiolus sp Argentina (as R. callae), New
Zealand
Hyacinthus sp Argentina (as R. callae), New
Zealand, Russia
Iris sp New Zealand
Lolium longiflorum USA (as R. hyacinthi)
Narcissus sp Canada, New Zealand, Russia,
Scotland, UK
Solanum sp France, India, USA
(as R. phylloxerae)
Tulipa sp Netherlands, New Zealand,
Russia
engeli Freesia sp Netherlands
Lilium sp Netherlands
Gladiolus sp Netherlands
fumouzi Narcissus sp Canada (from Netherlands)
longispinosus Taro Taiwan
Giant alocasia Taiwan
narcissi Narcissus sp China
nepos Hypomoea sp Italy
robini Allium cepa Israel, Japan, Mexico, New
Zealand, USA
Allium chinense Japan
Allium fistulosum Taiwan
Allium porrum Taiwan
Allium sativum Egypt, Israel, New Zealand
Allium tuberosum Japan
 Mites, Rhizoglyhus (Acari: Acaridae)
B 613

Bulb Mites, Rhizoglyphus (Acari: Acaridae), Table 10 List of Rhizoglyphus mites reported as pests, crops
and ornamentals affected, and geographic location (Continued)
Species Crop affected Country
Daucus carrota New Zealand
Freesia sp Japan, UK
Gladiolus sp China, New Zealand, Taiwan,
USA
Iris sp New Zealand
Lolium longiflorum Japan, New Zealand, USA
Narcissus sp Canada, New Zealand, UK
Solanum tuberosum New Zealand
Secale cereale Poland
robustus Allium sativum Mexico
singularis Dioscorea sp India, New Zealand
(from India)
setosus Allium cepa Taiwan
Allium porrum Taiwan
Allium sativum Taiwan
Caladium sp New Guinea
Lilium sp Taiwan
Gladiolus sp Taiwan
solanumi Solanum sp Pakistan
tacitri Citrus sp Tahiti
tardus Allium cepa USSR
tarsalis Sugar Beets USA
tsutienensis Lily Taiwan
Green onion Taiwan
Leek Taiwan
Tuberose Taiwan

Species of these genera are often found in stored adequate host plant, and can maintain their popu-
products or materials that are rich in organic sub- lation in the soil for a long time.
strates. More research is needed to determine The damage caused by bulb mites to plants
exactly how often these species infest bulbs. includes direct infestation and indirect transmis-
Bulb mites are generally polyphagous, with sion of plant disease. Bulb mites feeding on bulbs
numerous host plants recorded. The recorded host or roots can cause yellowing, wilt and early defo-
plants of R. robini, for example, include at least 28 liation of lower leaves, dwarfing or even death of
crops that belong to 14 families. Bulb mites usually the plant. Plant pathogens transmitted by bulb
inhabit the surface of the bulb where the stems or mites include Fusarium oxysporum, Rhizoctonia
roots grow. When the population is high, mites solani, Pythium ultimum, and Pseudomonas mar-
can also be located between the tissue layers of the ginata, which infest gladiolus and/or lily. Heavy
basal part of the stems. Bulb mites can also feed loss can result from the infestation of bulb mites.
and reproduce on plant debris when there is no Destruction of 1070% of bulbs or plants have
614
B Bulldog Ant or Bull Ant, Myrmecia spp. (Hymenoptera: Formicidae)

been reported for lily, gladiolus, onion and rakkyo. are still required. There seems no way to eradicate
When the bulb mite population is too high, farm- bulb mites from a field once they have invaded the
ers may have to shift to grow non-bulb crops. field. The best way to protect the crop is: (i) Treat
The life cycle of bulb mite normally under- the bulbs before planting to kill mites that may live
goes four stages, namely the larva, protonymph, on them. (ii) Reducing the bulb mite population in
tritonymph and the adult. When the environment soil before planting by solar heat or fumigating
is suboptimal, such as poor quality or quantity of with acaricides. (iii) Apply acaricide sometimes
food, crowding or poor environmental quality, the later in the growing season. However, acaricide
protonymph will molt into a deuteronymph. The applied after planting will have a limited effect.
deuteronymph stage is also called the hypopus,
which does not have a functional mouthpart. The References
hypopus will actively seek a host, usually an arthro-
pod, to attach to and be transferred to a new envi- Bu GS, Li LS (1998) Taxonomic notes on and key to the
ronment with plenty of food. The hypopus or known species of the genus Rhizoglyphus (Acari: Acar-
deuteronymph will, then, molt into tritonymph idae) from China. Syst Appl Acarol 3:179182
Garman P (1937) A study of the bulb mite (Rhizoglyphus hya-
and resume the normal life cycle.
cinthi Banks). Bull Conn A E S 402:889907
Rhizoglyphus mites develop quickly. At 28C, Ho CC (1988) An introduction to the exotic mite-pests in
development from egg to adult only takes Taiwan. Chin J Entomol (Special Publ.) 2:155166
approximately nine days. Adult females live about Nesbitt HHJ (1988) Three new mites of the subfamily Rhizo-
twenty-four days and produce 180280 eggs. glyphine. Can Entomol 76:2127
Caloglyphus mites are similar to Rhizoglyphus mites Woodring JP (1969) Observations on the biology of six species
in development rate, but have an even higher of acarid mites. Ann Entomol Soc Am 62:102108
fecundity. The populations of these mites can build
up to a huge number within a short time period.
A single bulb may harbor a population of hundreds Bulldog Ant or Bull Ant, Myrmecia
or even more than a thousand mites. spp. (Hymenoptera: Formicidae)
Bulb mites are difficult to control. Rhizogly-
phus echinopus, Rhizoglyphus robini, and Rhizogly- Bulldog or bull ants are some of the best-known
phus setosus are all resistant to a large number of ants in Australia due to their large size, very painful
acaricides. It appears that Caloglyphus mites are as sting, and aggressive behavior. Their mandibles are
potent as Rhizoglyphus mites in the development exceptionally large and well equipped with teeth.
of acaricide resistance. Additionally, they inhabit a Their name is derived from their habit of gripping
niche below the soil surface, which is difficult for something with their strong mandibles and hang-
acaricides to reach. A large amount of acaricide ing on to it. These ants are aggressive and have well
must be applied to have it reach bulb mites. developed vision. If disturbed, these large ants will
Irrigation can affect bulb mites though, some adult often come swarming rapidly from their nest in the
females of R. robini could survive immersion for 30 soil straight towards the intruder with mandibles
days. In the field, the mites can hide in air bubbles open and ready to use, but they also are quick to
among soil particles, and, hence, live even longer. sting any intruder after grasping it in its mandibles.
Plowing of fields to expose the interior of soil to Their sting is an important cause of anaphylaxis in
solar heat to build up its temperature has been Australia, even causing death of humans. There are
recommended to kill the bulb mites inside. How- about 90 species of bulldog ants in Australia, and
ever, some bulb mites may escape by moving down they range greatly in size. Many are brightly col-
to a depth of thirty cm or more. Fumigation of the ored red or orange on the head and abdomen.
soil does not make the crop immune from bulb Bulldog ants are some of the most primitive
mites. Applications of acaricide later in the season ant species and only have relatively small colonies.
 Bunchy Top of Papaya
B 615

The workers forage in a solitary manner, and The ants in this subfamily (Paraponerinae)
unlike many other ant species do not form scent are primitive, and their stings are morphologi-
trails when foraging. Instead, bulldog ants forage cally similar to those of some solitary wasps Wasp
independently and upon finding food carry it stings are multi-purpose defensive tools rather
back to the nest, which is located in the soil. than the more specialized weapons of more
Despite their aggressive nature, adult bull ants advanced ants, and tend to be more painful than
feed predominantly on honeydew, nectar and the stings ofants.
other sweet substances, but their larvae are car- Bullet ant is a relatively primitive ponerine, and
nivorous and are fed on insects collected by for- unlike more advanced ants, does not display a great
aging workers. Bulldog ants are most active deal of polymorphism. Queens are only slightly
during the day and forage either on the ground larger than workers. Mature colonies are small and
or on low vegetation. Some of the smaller species at most contain a few thousand ants. However,
are called jumper ants due to their tendency to workers exhibit a size-based division of labor, and
leap; despite their relatively small size they are the smaller ants tend to remain in the nest as nurse-
extremely aggressive. maids while larger workers serve as guards and for-
Ants (Hymenoptera: Formicidae) agers. Colonies consist of several thousand
Venoms and Toxins in Insects individuals, and are usually found at the bases of
Bullet Ant, Paraponera clavata (Fabricius) trees. The workers forage in the trees in the area
directly above the nest, where they search for insect
prey and plant nectaries. Extra-floral nectar is an
Bullet Ant, Paraponera clavata important part of their diet. Water is also collected.
(Fabricius) (Hymenoptera: Both nectar and water are shared with nest ants, or
Formicidae) placed as tiny droplets on feeding larvae. Solid food
consists mostly of arthropods, other invertebrates,
Paraponera clavata is best known for its large size and occasionally pieces of small vertebrates. Ter-
and severe sting. Workers are 1825 mm long and mites are especially attractive prey. Nestmates are
resemble stout, reddish-black, wingless wasps. The recruited using pheromone trails, although experi-
pain caused by the sting of this insect is purported enced foragers also use landmarks. Most foraging
to be greater than that of any other wasp or ant, activity occurs at dusk and during the night.
and is ranked as perhaps the most painful insect Ants (Hymenoptera: Formicidae)
sting. The pain may persist for a full 24 h. The pain Venoms and Toxins in Insects
is caused by a paralyzing neurotoxic peptide in the Bulldog Ant or Bull Ant, Myrmecia spp
venom called poneratoxin.
The genus Paraponera is found in Central
and South America, south from Costa Rica and Bumble Bees
Nicaragua to Brazil and Peru. Bullet ants are used
by some indigenous people in their initiation rites Members of the family Apidae (order Hyme
to manhood. In this process, the ants are first noptera, superfamily Apoidae).
immobilized, and then hundreds of them are Wasps, Ants, Bees and Sawflies
woven into sleeves made out of leaves, with the Bees
stinger facing inward. As part of this rite, boys slip
the sleeve down onto their arm. The goal of this Bunchy Top of Papaya
initiation rite is to keep the sleeve on for a full 10
min. After exposure to the ants, the boys arms are This is an important bacterial disease of papaya
temporarily paralyzed because of the venom, and that is transmitted by insects.
they may shake uncontrollably for days. Transmission of Plant Diseases by Insects
616
B Buprestidae

Buprestidae

A family of beetles (order Coleoptera). They

commonly are known as metallic wood-boring
beetles.
Beetles

Burgess, Albert Franklin

Albert Burgess was on October 2, 1873, in Massa-

chusetts. He received a first degree in 1895 and an
M.S. in 1897 from Massachusetts Agricultural Burgess, Albert Franklin, Figure72 Albert F.
Academy. From 1899 to 1907 he worked as Assis- Burgess.
tant in Entomology at the University of Illinois
and inspector of nurseries and orchards for the
Ohio Department of Agriculture. Then he returned doctorate in medicine and a doctorate in zoology
to Massachusetts to work for the U.S. Department in 1929. He did his military service in 1832. He
of Agriculture in the Gypsy Moth Project, and taught in schools in Berlin until, in 1837, he
continued this work until his retirement in 1943. became professor of zoology in Halle. He married
However, in 1916, work on the browntail moth in 1836, and had two sons. His first insect collec-
was added to his duties. His American Association tion is in Halle. He published a five-volume textbook,
of Economic Entomologists, and for years contrib- Handbuch der Entomologie in 18321847.
uted much time to that society and its Journal of Between 1850 and 1852, with one of his sons, he
Economic Entomology. He died on February 23, travelled in eastern Brazil and then returned to
1953, survived by his second wife and two sons Halle. One account of his Brazilian travels was
from his first marriage (Fig.72). published in 1853 as Reise nach Brasilien, durch
die Provinzen von Rio de Janeiro und Minas
Geraes, another in 18541856 as Systematische
Uebersicht der Tiere Brasiliens, although it was
Reference incomplete and deals only with mammals and
birds. He returned to Halle, but in 1856 he left
Mallis A (1971) Albert Franklin Burgess. In: American ento- again, this time for Argentina, and spent four years
mologists. Rutgers University Press, New Brunswick, NJ, (18571860) travelling within Argentina before
pp 435437
publishing (1862) a 2-volume book Reise durch
die La Plata-Staaten He returned to Halle, but
resigned from his position in 1861, divorced his
Burmeister, Carl Hermann Conrad German wife Marie Elise, and travelled once more
to Argentina. His previous work resulted in his
Hermann Burmeister was born in Stralsund, being offered directorship of the Museo Publico
Germany, on January 15, 1807. His early university de Historia Natural in Buenos Aires in 1862. His
education was at Universitt Greifwald (18251827), interests were in all areas of natural history, but
whence he moved to Universitt Halle. His disser- especially entomology. He wrote on paleontology,
tation at Halle and academic training gave him a insect anatomy, the beetle family Scarabaeidae,
 Burnet Moth Biology (Lepidoptera: Zygaenidae)
B 617

The family Zygaenidae is a member of the order

Lepidoptera, suborder Ditrysia and the super-
family Zygaenoidea. Other than Zygaenidae, the
superfamily Zygaenoidea consist of the following
families: Megalopygidae (Lagoidae), Heterogyni-
dae, Chrysopolomidae, Metarbelidae (Teragrii-
dae), Limacodidae (including Cochlidiidae,
Heterogenidae, Eucleidae), Cyclotornidae, and
Epipyropidae. The Zygaenidae are further subdi-
vided into seven subfamilies: Zygaeninae (burnet
moths), Procridinae (forester moths), Chalcosii-
nae, Charideinae, Phaudinae, Anomoeotinae and
Himantopterinae from which only Zygaeninae
and Procridinae (and to a lesser extent Charidei-
nae) are frequently mentioned even though Chal-
cosiinae are considered to be the largest group
Burmeister, Carl Hermann Conrad, Figure 73 living in tropics. It is worth noting that the genus
C.Hermann Burmeister. Zygaena is the most studied genus of the family.

and many other subjects, and published about 300 External Morphology
titles. He remarried in Argentina and had two
sons. He died on May 2, 1892, following an accident The adults of the family Zygaenidae closely resem-
in which he fell from a ladder into a glass showcase ble the Ctenuchidae from the superfamily Noctu-
at the museum (Fig.73). oidea, but are readily distinguished by the presence
of Cu2 in the hind wings. Many are very brilliantly
colored and there is considerable diversity of
References structure. It is interesting to note that all subfami-
lies, except Phaudinae and Himantopterinae, have
Essig EO (1931) Burmeister, Hermann Carl Conrad. In: A been shown to contain the cyanogenic glucosides
history of entomology. The Macmillan Company, New linamarin and lotaustralin. The larvae are short
York, NY, pp 562563
Papavero N (1973) Burmeister. In: Essays on the history of
and cylindrical and have short hairs protruding
Neotropical dipterology, with special reference to col- from numerous verrucae. The pupae are enclosed
lectors (17501905). Museu de Zoologia, vol 2. So in tough, elongate, membranous cocoons
Paulo, Brazil, pp 292293 aboveground.
Ulrich W (1972) Hermann Burmeister, 1807 to 1892. Ann
Rev Entomol 17:120

Life History and Habits

Burnet Moth Biology The zygaenid moths (Figs.74 and 75) usually are
(Lepidoptera: Zygaenidae) diurnal in habit, though several species are
known as nocturnal or are active during both
cyrus abivardi night and day. Zygaena (Mesembrynus) nocturna
Swiss Federal Institute of Technology, Zurich, Ebert, also known as a subspecies of Z. (M.) seitzi
Switzerland Reiss, is an example of the latter case. While it
618
B Burnet Moth Biology (Lepidoptera: Zygaenidae)

Sc R1 R2
R3
R4
M R5
M1
2A M2
M3
Cu1a
Cu1b
1A Cu2

M Sc+R1
Rs
M1
M2
M3
3A Cu Cu1a
2A Cu2 1b

Burnet Moth Biology (Lepidoptera: Zygaenidae),

Figure75 Resemblance of the family
Burnet Moth Biology (Lepidoptera: Zygaenidae), Ctenuchidae (Noctuoidea) (above left) to the
Figure74 The adults of two Zygaena species: family Zygaenidae, but readily distinguished by
(above) Z. fraxini Mn.; (below) Z. carniolica Scop. their wing venation (above right: Ctenuchidae
(After Abivardi C (2001) Iranian entomologyan (Euchromia polymena); below: Zygaenidae
introduction, 2 vols. Springer Verlag, Heidelberg, (Zygaena filipendulae L.).
Germany, XXXIII, 1033 pp).

stems and twigs or on the surface of the box

was originally described as exclusively nocturnal, provided for pupation. The number of instars
it is also reported from Yasudj (Iran) to fly during varies among species, with Z. (M.) lydia
the day. Staudinger displaying seven instars and Artona
In general, the zygaenid larvae live exposed chorista Jordan with seven.
on herbaceous plants. The larvae of the genus The most interesting life cycle (Fig.76)
Zygaena show a certain oligophagy: while those strategies have been observed in species of the
belonging to the subgenera Agrumenia and Palaearctic genus Zygaena. Development time
Zygaena feed exclusively on Fabaceae, those of varies markedly within a population. This varia-
the subgenus Mesembrynus feed, with few excep- tion is due to repeated larval hibernations between
tions, on Apiaceae. Laboratory studies on the the third to the tenth instar and are due either to
biology of a zygaenid from Iran, Z. (M.) tamara repeated or prolonged diapause periods. This
ssp. Kendevanica Tremewan, revealed nine larval phenomenon has been described as fractionized
instars during which two to three stages of dia- development. Larvae normally pupate after six
pause were observed. In the final instar, the lar- or seven feeding instars.The high flexibility in
vae constructed their cocoons either on the different Zygaena life cycle phenologies is based
 Burnet Moth Biology (Lepidoptera: Zygaenidae)
B 619

Burnet Moth Biology (Lepidoptera: Zygaenidae), Figure76 External morphology of eggs (a), larvae
(b & c; left: dorsal position; right: lateral position) and cocoon (d) of Z. carniolica Scop. with its adults
(e)resting on thistle flowers. (Courtesy of Professor Clas M. Naumann and Pro Natura- The Swiss Alliance
for Nature Conservation, Basel, Switzerland.)

on both exogenous and endogenous factors. plants, the enzyme comes into contact with the
The variability in diapause and the consequent glucoside leading to the release of hydrocyanic
variable generation times may (Fig.77) represent acid. Hydrocyanic acid is a powerful toxin that
a strategy of spreading of the risk, thereby buffer- fends off herbivores and thus protects the plants.
ing the populations against adverse and fluctuat- Within the insects, cyanogenesis occurs in bee-
ing climatic conditions. tles (Coleoptera) and bugs (Hemiptera) and
seems to be quite common in Lepidoptera. In
the order Lepidoptera, cyanogenesis is reported
Cyanogenesis for several families of butterflies (Nymphalidae,
Lycaenidae, Pieridae, Papilionidae and Hesperi-
The phenomenon of cyanogenesis is known to idae) and moths (Megalopygidae, Heterogyni-
occur in more than 2,500 plant species (includ- dae, Limacodidae, Zygaenidae, Thyatiridae,
ing important crop plants such as cassava, sor- Geometridae, Notodontidae, Arctiidae, Noctui-
ghum, flax, clovers and almond) as well as in dae and Lymantriidae). Within the family
some arthropods. Cyanogenesis is the process Zygaenidae, five of the seven subfamilies (except
by which either plants or animals release hydro- the Phaudinae and Himantopterinae) have been
gen cyanide (HCN) from endogenous cyanide- shown to contain the cyanogenic glucosides
containing compounds and is thought to play a linamarin and lotaustralin (Figs.78 and 79).
role in defense against generalist, natural ene- Cyanogenesis is closely related to aposematic
mies. In plants, the cyanogenic glucosides and patterns in both larvae and adults, and mimicry
the corresponding enzymes are usually stored is common. In Zygaena larvae there are three
in different compartments. When herbivores defenses against natural enemies: (i) an apose-
such as cattle and insects feed on cyanogenic matic coloration that discourages an attack by a
620
B Burnet Moth Biology (Lepidoptera: Zygaenidae)

Burnet Moth Biology (Lepidoptera: Zygaenidae), Figure77 Fractionized development in Zygaena

species: Z. transalpina hippocrepidis Hueb. and Z. filipendulae L. as examples. (Courtesy of Prof. Clas M.
Naumann.)

Burnet Moth Biology (Lepidoptera: Zygaenidae), Figure78 The process of cyanogenesis or enzymatic
release of hydrogen cyanide (HCN) from endogenous cyanide-containing compounds.

predator when visual contact is made, (ii) a the viscosity of the fluid, and (iii) when a larva
secretion that is released following a relatively is eaten by a predator, the liberated hydrocyanic
slight touch that fends off enemies by the nox- acid of the hemolymph deters predation of other
ious taste of the cyanogenic glucosides and/or larvae.
 Burnet Moth Biology (Lepidoptera: Zygaenidae)
B 621

Trichogramma evanescens (Hymenoptera: Tricho-

grammatidae). However, the percentage of para-
sitism was not high enough to control the pest.

Economic Importance

Knowledge about the economic importance of

the members of the family Zygaenidae is confined
to the subfamily Procridinae (forester moths)
and, to a much lesser extent, to the subfamily
Zygaeninae (burnet moths). The members of both
subfamilies have been reported to play a role in
pollination of the orchid Anacamptis pyramidalis
(Orchidaceae).
Among the serious pests are western grape-
leaf skeletonizer, European grape leaf skeletonizer,
Burnet Moth Biology (Lepidoptera: Zygaenidae), Artona chorista Jordan, and coconut leaf miner.
Figure79 Structure of two cyanogenic glucosides The western grapeleaf skeletonizer, Harri-
(above: Linamarin; below: Lotaustralin) produced sina brillians, has been the subject of numerous
by the members of the family Zygaenidae. studies in California (USA) and in northwestern
Mexico. While the populations of this moth in
southern California appear to be maintained at
low levels of abundance by the combined activ-
Predators and Parasitoids ity of a granulovirus (HbGV) and the parasitoid
Ametadoria misella (Diptera: Tachinidae), out-
Several natural enemies are known. Ectemnius breaks of this insect have been common in cen-
kriechbaumeri (Hymenoptera: Sphecidae) para- tral California. The host plant is damaged as
sitizes larvae of the six-spot burnet (Zygaena fil- follows: first, the early fourth instar larvae feed
ipendulae L.) in Italy and Spain. In Iran, larvae of on the lower leaf surface, leaving only the veins
Zygaena (Agrumenia) esseni Blom are parasitized and upper cuticle. This gives leaves a whitish,
by the ichneumonid Casinaria orbitalis Graven- paper like appearance. Then, the late fourth and
horst. They also are susceptible to infection by the all fifth instar larvae skeletonize the leaves, leav-
entomopathogenic nematode Steinernema sp. ing only the larger veins. In high populations,
Populations of western grapeleaf skeletonizer, larvae can defoliate vines by July. When the vines
Harrisina brillians, in southern California appear are severely defoliated, larvae will then feed on
to be maintained at low levels of abundance by the grape clusters, which can result in bunch rot.
the combined activity of a granulovirus (HbGV) Defoliation can also result in sunburn of the
and the parasitoid Ametadoria misella (Diptera: fruit and quality loss. Furthermore, defoliation
Tachinidae). after harvest may also weaken vines by affecting
In Italy, the European grapeleaf skeletonizer food reserves.
(Theresimima ampellophaga) is attacked by six The European grapeleaf skeletonizer, Theres-
species of parasitoids namely, two (chalcidids imima ampellophaga, is a bivoltine species in the
Brachymeria intermedia and Hockeria unicolor), southern part of its range (south Italy) and
a braconid (Apanteles ultor), two tachinids (Zenil- univoltine in France, north Italy, Austria, Hungary
lia libatrix and Exorista sp.) and the famous and the former USSR. The larvae feed on
622
B Burnet Moths (Lepidoptera: Zygaenidae) Burrower Bugs

thelower leaf surface and in late July, they aban- granulovirus of Harrisina brillians (Lepidoptera:
Zygaenidae) in California. Environ Entomol
don the leaves and move to the stumps left after
28:868875
pruning in the previous year where they spin Wipking W, Naumann CM (1992) Diapause and related
cocoons in which they overwinter. Damage Phenomena in Zyganidae moths. In: Dutreix C, Nau-
includes injuries to the young leaves by the small mann CM, Tremewan WG (eds) Recent advances in
burnet moth research (Lepidoptera: Zygaenidae).
larvae in summer, injuries to the unopened buds Koeltz Scientific Books, Champaign, IL, pp 107128
immediately after hibernation and destruction
of the young leaves by the older larvae in spring,
which consume the whole leaf except for the
midrib. Burnet Moths (Lepidoptera:
Artona chorista Jordan is recorded as a Zygaenidae) Burrower Bugs
major pest of large cardamon plantations in
India. Eggs are laid on the underside of leaves in Members of the family Cydnidae (order
batches of over 300 and hatch after about two Hemiptera).
weeks. The young larvae skeletonize the leaves, Bugs
while mature larvae leave only the midribs
exposed. There are seven larval instars and the
larval and pupal stages last about two months or
one month, respectively. Adult males and females Burrowing Water Beetles
live for about one week.
Coconut leaf miner, Artona catoxantha Members of the family Noteridae (order Coleoptera).
Hamps, is an important pest of coconut in Beetles
Indonesia. Although Apanteles artonae (Glypta-
panteles artonae) has been found to be the most
important parasitoid of the pest, hyperparasit- Bursa Copulatrix
ism of the parasitoid by other insects reduce
the activity of A. artonae leading to frequent A sac-like modification of the oviduct, or copula-
outbreaks of the coconut leaf miner. tory chamber, that receives the male aedeagus.
Reproduction

References
Bursicon
Abivardi C (2001) Iranian entomologyan introduction, 2 vols.
Springer Verlag, Heidelberg, Germany, XXXIII, 1033 pp A neuropeptide hormone produced by the neu-
Efetov KA, Tarmann GM (1999) Forester moths. Apollo rosecretory cells of the brain that controls scle-
Books, Stenstrup, Denmark, 191 pp rotization (tanning) and cuticle expansion.
Franzl S (1992) Synthesis, transport and storage of cyanogenic
glucosides in larva of Zygaena Trifolii (Esper, 1783) (Lep-
Integument: Structure and Function
idoptera: Zyaenidae). In: Dutreix C, Naumann CM,
Tremewan WG (eds) Recent advances in burnet moth
research (Lepidoptera: Zygaenidae). Koeltz Scientific
Books, Champaign, IL, pp 2131 Bush Crickets
Naumann CM, Tarmann GM, Tremewan WG (1999) The
western Palaearctic Zygaenidae (Lepidoptera). Apollo A subfamily of crickets (Eneopterinae) in the
Books, Stenstrup, Denmark, 304 pp
Stark DM, Purcell AH, Mills NJ (1999) Natural occurrence order Orthoptera: Gryllidae.
of Ametadoria misella (Diptera: Tachinidae) and the Grasshoppers, Katydids and Crickets
 Butterflies (Lepidoptera: Rhopalocera)
B 623

Butterflies (Lepidoptera: specialists combine Riodinidae with Lycaenidae.

Rhopalocera) Contrarily, most of the subfamilies in Nymphali-
dae in the past often have been separated as their
john b. heppner own families, like Satyridae, Charaxidae, Morphi-
Florida State Collection of Arthropods, dae, Amathusidae, Danaidae, Heliconiidae, etc.
Gainesville, FLorida, USA Butterflies now are thought to be a lineage from
ancestors of what remain now as the most primi-
Among the insect order Lepidoptera, butterflies tive of bombycine moths (perhaps resembling
comprise about 9% of the order worldwide, Ratardidae and relatives of Southeast Asia), which
totaling about 20,400 described species (moths then evolved to geometer moth ancestors (families
represent the other 91% of all lepidopterans). Geometridae and Hedylidae) and an alternate lin-
There are perhaps another 3,500 butterfly species eage that evolved to diurnal lifestyles and modern
awaiting discovery and naming, mostly from trop- butterflies.
ical regions of the world, and especially among Butterfly adults typically have large eyes, a large
the smaller species such as skippers (family Hes- haustellum (or tongue), and knobbed, or clubbed,
periidae) and blues (family Lycaenidae). The antennae; but skippers (family Hesperiidae) mostly
Nymphalidae are the largest butterfly family, with have the antennae with elongated hooked clubs.
about 7,080 known species worldwide; second Although most butterfly adults have strong tho-
largest is Lycaenidae with 5,955 known species. racic legs, in the family Nymphalidae the first pair
Although the name Rhopalocera is not used in of thoracic legs are not used for walking and instead
modern classification of Lepidoptera, the name are held folded under the prothorax. The bodies of
can be used to refer to all the butterflies (Hetero- adult butterflies are typically rather slender, but
cera is used as the name for all moths). While many groups have very robust bodies, allowing them
most moths are nocturnal (with many exceptions), to be very strong fliers (e.g., charaxine and danaine
most all butterflies are diurnal, although some are Nymphalidae). Some groups have scent organs
known to be crepuscular (especially a few tropical (coremata) on the abdomen that can be everted
skippers). either for protection or as pheromone releasers
Out of the total of 125 families of Lepidoptera, during mating behavior. Danainae butterflies (fam-
there are seven families of butterflies, although ily Nymphalidae) have wing vein scent organs
many specialists continue to place snout butter- (androconia) in males, and Satyrinae butterflies
flies (family Libytheidae, only 12 known species) (family Nymphalidae) have tymbal organs used for
among the Nymphalidae and thus have only six hearing within some wing veins. Wings include a
families. Likewise, there is controversy about pair of forewings and a pair of typically smaller
whether skippers (family Hesperiidae) should be hindwings (some Pieridae have larger hindwings
in their own superfamily, Hesperioidea, or together than forewings, particularly in the tropical American
with other butterflies in a single superfamily subfamily Dismorphiinae), and generally the fore-
Papilionoidea. One solution to this controversy is wings are rather triangular in shape and the hind-
to use a sub classification below the superfamily wings are more rounded. Great variety of wing
level, thus the series Hesperiiformes and series shape, however, is known and many groups have
Papilioniformes are used. The main true butterfly hindwing tails (e.g., many Lycaenidae and Papil-
families are Papilionidae (swallowtail butterflies), ionidae). A huge variety of color patterns exist
Pieridae (yellow-white butterflies), Lycaenidae among butterflies, from monotone browns or grays,
(gossamer-winged butterflies), Riodinidae (metal- to extremely colorful, to some that even are nearly
mark butterflies), Libytheidae (snout butterflies), colorless or transparent (e.g., some tropical
and Nymphalidae (brush-footed butterflies). Some glasswings of the subfamily Ithomiinae, family
624
B Butterflies (Lepidoptera: Rhopalocera)

Butterflies (Lepidoptera: Rhopalocera) , Figure80 Representative butterflies (Lepidoptera: Rhopalocera):

top left, Isoteinon lamprospilus formosanus Fruhstorfer (Hesperiidae) from Taiwan (photo C.C. Lin);
top right, Zerynthia polyxena cassandra (Geyer) (Papilionidae, Parnassiinae) from France (photo J.H.H.
 Butterflies (Lepidoptera: Rhopalocera)
B 625

Nymphalidae). The morpho butterflies of the sub- hang upside down (Lycaenidae pupae tend to be
family Morphinae (family Nymphalidae), from laid flat on a plant surface).
tropical America, are well known for their brilliant Butterflies, while a small percentage of the
blue coloration that is the result of structural scales order Lepidoptera, have served as the model organ-
that reflect light, rather than the typical lepi- isms for a large number of ecological and biological
dopteran wing scales that have pigmented colors. studies of the Lepidoptera, much more than among
Butterfly caterpillars for the most part are typ- the moths. Part of this study usage pertains to their
ical lepidopteran caterpillars, with the usual num- being diurnally active, and thus easier to study than
ber of prolegs (4 pairs plus a posterior pair), but the nocturnal moths. Butterflies also are mostly
many different setal vestitures and color forms are more colorful and larger than typical moths, and
known. Caterpillars typically have a hard head cap- are thus the most well known lepidopterans among
sule, three pairs of clawed thoracic legs, and 4 pairs the general public. Butterflies have complex flight
of abdominal prolegs having crochets (hook-like behavior and mating rituals that have been the sub-
spines on the base of the prolegs that provide foot- ject of many detailed studies over the years. Flight
ing when climbing on plants), plus a posterior pro- among butterflies also involves directed migration
leg pair. Most of the Nymphalidae larvae have in some cases, the most well known example being
various kinds of bizarre spined and enlarged setae, the yearly mass autumn flights of the American
called scoli, typically even on the head. Swallowtail monarch butterfly (Danaus plexippus, family
larvae, on the other hand, have a unique defensive Nymphalidae) from as far as southern Canada to
odiferous and usually brightly colored forked scent wintering refugia in Mexico, and then back again
organ, called an osmeterium, just behind the head the following spring. There are many other cases of
capsule that is extruded to help defend against a lesser migrations among other species and on all
predator. Larvae among most Lycaenidae are continents. Other studies on butterflies have focused
slug-like and can retract their head into folds of the on their life histories, which involve such intricate
prothorax. The more primitive skipper caterpillars aspects as commensal myrmecophilous adaptations,
(family Hesperiidae) have few body setae and as among most larvae of the blues (family Lycaeni-
mostly feed on grasses and other monocots. Other dae) and metalmarks (family Riodinidae), where
butterfly larvae feed on a great variety of hostplants, ants protect the larvae from predators and the lar-
although most individual species have a narrow vae provide the ants with desirable secretions.
hostplant preference (e.g., monarch butterfly larvae However, most butterflies still remain unknown
feed only on milkweed leaves, Asclepiadaceae). biologically, particularly among tropical species.
Most butterfly larvae pupate as exposed pupae and The largest known butterflies are among the
do not make cocoons. Swallowtail pupae (family birdwings (family Papilionidae) (Fig.80) of the
Papilionidae) typically use a silken girdle to angle Indo-Australian tropics, especially in New Guinea
away from a plant stem, while most other butter- and the Solomon Islands, where the largest females
flies attach their pupae using the cremaster and attain wingspans of up to 280 mm. One African

Thiele); second row left, Eurytides marcellus (Cramer) (Papilionidae, Graphiini) from
Florida, USA (photo H.O. Hilton); second row right, Papilio glaucus Linnaeus (Papilionidae, Papilionini)
from Florida, USA (photo H.O. Hilton); third row left, Pieris canidia (Sparrman) (Pieridae, Pierinae) from
Taiwan (photo C.C. Lin); third row right, Heliophorus ila matsumurae (Fruhstorfer) (Lycaenidae, Lycaeninae)
from Taiwan (photo C.C. Lin); bottom left, Libythea celtis formosana Fruhstorfer) (Libytheidae) from
Taiwan (photo C.C. Lin); bottom right, Agraulis vanillae (Linnaeus) (Nymphalidae, Heliconiini)
from Florida, USA (photo J. B. Heppner).
626
B Butterflies and Moths (Lepidoptera)

swallowtail species (Papilio antimachus) has males The Lepidoptera, one of the main plant-feeding
with a wingspan of up to 250 mm (females in this groups of insects in the world, are well known to
species are smaller than the males). The smallest most all persons familiar with nature or the garden,
known butterflies are some of the high altitude or as the day-flying butterflies and the mostly
desert blues (family Lycaenidae), where wingspans nocturnal moths. Included are all the butterflies
as small as 6 mm are known. The average butterfly, and skippers (superfamily Papilionoidea), plus
however, has a wingspan of about 30 mm, not much such common moth groups as silkworms (or silk-
different from the average moth adult, since there moths) (family Bombycidae), emperor moths (or
are a large number of very small skippers and blues, giant silkmoths) (family Saturniidae), hornworms
and fewer of the larger swallowtails and Nymphali- (or hawk moths) (family Sphingidae), cutworms
dae in the world. (or millers and owlet moths) (family Noctuidae),
Butterflies and Moths inch worms (or geometer moths) (family
Geometridae), clothes moths (family Tineidae),
References and many others. The spectacular variety of wing
coloration and markings of the Lepidoptera has
D Abrera B (198095) Butterflies of the world, 12th vol. Hill evolved over millions of years, from the rather
House, Melbourne, Victoria, Australia drab primitive moths that hardly appear much
Douglas MM (1986) The lives of butterflies. University of different than the related Trichoptera, to the most
Michigan Press, Ann Arbor, Michigan, 241 pp, 16 pl
Feltwell J (1986) The natural history of butterflies. Facts on
brilliantly colored butterflies. The Lepidoptera are
file, New York, New York, 133 pp notably differentiated from Trichoptera by the
Feltwell J (1993) The illustrated encyclopedia of butterflies. scales which cover the wings and all external body
Blandford, London, UK, 288 pp parts.
Kitching RL, Scheermeyer E, Jones RE, Pierce NE (eds)
(1999) Biology of Australian butterflies. CSIRO, Lepidoptera (or scaly wings) are perhaps
Canberra, Australia, 395 pp (Monograph of the Austra- best known for the colorful day-flying butterflies.
lian Lepidopterists Society 6) Such famous species as the American monarch
Manos-Jones M (2000) The spirit of butterflies: myth, magic,
butterfly (Danaus plexippus, family Nymphalidae,
and art. H. N. Abrams, New York, NY, 144 pp
Nijhout HF (1991) The development and evolution of but- subfamily Danainae), the swallowtails and the
terfly wing patterns. Smithsonian Institution Press, tropical birdwings (family Papilionidae), the many
Washington, DC, 297 pp, 8 pl common yellow butterflies (family Pieridae), and
Owen DF (1971) Tropical butterflies: the ecology and behaviour
of butterflies in the tropics with special reference to
blues and hairstreaks (family Lycaenidae), are
African species. Clarendon Press, Oxford, UK, 214 pp, 40 pl known by most persons in the world from their
Vane-Wright RI, Ackery PR (eds) (1984) The biology of butter- earliest school days. The name butterfly is
flies. Royal Entomological Society of London, 429 pp thoughtto come from Old English usage related to
(Reprinted 1989, Princeton University Press, Princeton, NJ)
Watson A, Whalley PES (1975) The dictionary of butterflies and yellow butterflies looking like slices of butter on
moths in color. McGraw Hill, New York, NY, 296 pp, 144 pl the wing, or butter-fly (the Old English or Old
German buterfloege), or even ancient folklore of
fairies stealing butter. Other languages and cultures
all have their own common names for butterfly:
Butterflies and Moths farfalla (Italian), lepke (Hungarian), Schmetterling
(Lepidoptera) or Tagfalter (German), papillon (French), vlinder
(Dutch), sommerfugl (Danish), psyche (Greek),
john b. heppner ch-ch (Japanese), h deh (Chinese), borborleta
Florida State Collection of Arthropods, (Portuguese), mariposa (Spanish), fluture (Roma-
Gainesville, FL, USA nian), farasha (Arabic), kupu-kupu (Indonesian),
 Butterflies and Moths (Lepidoptera)
B 627

rama-rama (Malaysian), titli (Urdu), boboochka modern understanding of the evolution of the
(Russian), kipepeo (Swahili), and so on. Many order, the simplified divisions nonetheless are a
names refer to both butterflies and moths, such as way of referring to each group using Latin
the German word Schmetterling and the French names and are still commonly encountered in
papillon, while moths are sometimes referred to the popular literature. Likewise, for the terms
what in English would be night butterflies, or Microlepidoptera (or the smaller and primitive
special words are available just for moths as, for moths) and Macrolepidoptera (the usually larger
example, Nachtfalter (German), moth (English), and more advanced moths and butterflies):
and polilla (Spanish). these terms are not universally applicable since
Most cultures in the world have mythology some micro -moths include very large species
and words for butterflies and moths. Moths, (some Hepialidae and Cossidae) and some
however, while also having well known common macro -moths also include some very small
names, have mostly been associated since ancient species (e.g., some Geometridae and Noctuidae).
days with those few species that are destructive Some butterflies (e.g., some blues, Lycaenidae)
to man: thus, cutworms (Noctuidae), clothes are smaller even than some of the average
moths (Tineidae), rice moths and grain moths Microlepidoptera.
(Pyralidae), cankerworms (Geometridae), and so There is incredible diversity of form, biol-
forth. Folklore for Lepidoptera also includes such ogy, behavior, and feeding habits among the Lep-
superstitions as the fear of death associated with idoptera, which occur in almost all known
the death-head sphinx of Europe and Asia (Acher- habitats, from the Arctic to the densest jungles.
ontia atropos, Sphingidae): the large-bodied adults The only region lacking Lepidoptera is Antarc-
in this genus have markings on the thorax that tica, although some small brachypterous species
resemble a human skull, and they also squeak like could conceivably be present on the northern-
a mouse when held by their bodies. Likewise, the most tip of the continent nearest to Tierra del
very large black witch moth (Ascalapha odorata, Fuego. There are also completely different life-
Noctuidae) of tropical America is also feared as styles between the adults and the larvae of Lepi-
an omen of death when one flies into a house doptera. For example, while adult butterflies seek
through an open window. Many native cultures, nectar for the most part, and most moths at least
like in the Amazon Basin, believe butterflies seek moisture (there are a few that do not feed as
are the departed souls from recently deceased adults), there are such strange larval adaptations
persons. Contrarily, among all the Lepidoptera, as the myrmecophilous larvae of many Lycaeni-
perhaps the most beneficial to man has been the dae, where the larvae are tended and protected
silkworm moth, Bombyx mori (Bombycidae), a by ants. As a contrary example, in larvae of Dal-
domesticated variety of a native Chinese silk- ceridae, the larvae are protected from ant attacks
worm moth which has been cultured for centuries by an integumental defensive secretion, while
in China to produce fine silk, spun from the the adults of these slug caterpillars lead simple
strands of its white cocoons. lives in search of mates, as do most moths.
The Lepidoptera are estimated to number In the overall world fauna of 255,000 species
approximately 255,000 extant species in the of Lepidoptera, most of the evolutionary devel-
world, with about 156,100 species already named opment and biodiversity is among the moths
and cataloged. The order has often been divided (an estimated 231,500 species), while butterflies
into the generalized groupings of Rhopalocera, and skippers total an estimated 23,500 species
or butterflies, and Heterocera, or moths. worldwide, and represent only about 9% of the
Although this separation has no validity in our total extant species of Lepidoptera.
628
B Butterflies and Moths (Lepidoptera)

Classification Order: LEPIDOPTERA

Suborder: Zeugloptera
The order is now divided into four suborders, Micropterigoidea
based on modern studies using cladistics and Suborder: Aglossata
other techniques for analysis of morphological Agathiphagoidea
characters and other evolutionary information: Suborder: Heterobathmiina
Zeugloptera, Aglossata, Heterobathmiina, and Heterobathmioidea
Glossata. Each of the first three suborders include Suborder: Glossata
only a single nominate family of primitive moths Cohort: Dacnonypha
and all the remainder of the order is under Glossata. Infraorder: Dacnonypha
There are differing modern classifications adhered Eriocranioidea
to, although in general most lepidopterists now Infraorder: Lophocoronina
agree on the overall treatment of families and Lophocoronoidea
higher categories. In the classification adopted Cohort: Myoglossata
herein, the Glossata are further divided into the Subcohort: Myoglossata
cohorts Dacnonypha and Myoglossata. Dacnonypha Infraorder: Neopseustina
are subdivided into two infraorders: Dacnonypha Neopseustoidea
and Lophocoronina. Myoglossata are divided into Subcohort: Neolepidoptera
two subcohorts, Myoglossata and Neolepidoptera, Infraorder: Exoporia
with the first containing only the infraorder Mnesarchaeoidea
Neopseustina, and Neolepidoptera having two Hepialoidea
infraorders: Exoporia, and Heteroneura. Most Infraorder: Heteroneura
Lepidoptera are in Heteroneura, which are divided Division: Monotrysia
into two divisions: Monotrysia and Ditrysia. Section: Nepticulina
Monotrysia have two sections: Nepticulina and Andesianoidea
Incurvariina. Ditrysia, then, contain the majority Nepticuloidea
of the order, with section Tineina having most of Tischerioidea
the micro-moths, and section Cossina mostly the Palaephatoidea
larger moths and the butterflies. The remaining Section: Incurvariina
classification details in Lepidoptera involve further Incurvarioidea
divisions into subsections, superfamilies, and Division: Ditrysia
families. Section: Tineina
The following listing gives an overview of the Subsection: Tineina
main groupings and superfamilies of Lepidoptera. Tineoidea
Butterflies are in Papilionoidea, including skippers Gelechioidea
which sometimes are placed in their own super- Copromorphoidea
family, Hesperioidea. Butterflies are placed near Yponomeutoidea
the middle of the Bombycina, and not at the end Immoidea
of the order as many older works have them, Pyraloidea
since the Noctuidae are now considered the most Pterophoroidea
evolutionarily advanced Lepidoptera. Groups Subsection: Sesiina
preceeding Ditrysia contain the most primitive Sesioidea
Lepidoptera, and among these, the first three Zygaenoidea
suborders contain the most archaic relicts of Section: Cossina
ancient lepidopteran lineages still extant. Subsection: Cossina
 Butterflies and Moths (Lepidoptera)
B 629

Cossoidea a subfamily or as a separate family, etc. Even some

Castnioidea unusual tribes within subfamilies are considered
Tortricoidea separate families by some specialists. Among the
Subsection: Bombycina butterflies, nearly all subfamilies have at one time
Calliduloidea or another been considered separate families, and
Uranioidea some of the currently adopted families were listed
Geometroidea as their own superfamilies (viz., Nymphaloidea
Papilionoidea and Lycaenoidea, etc.) in some past
Drepanoidea classifications.
Bombycoidea As the diversity of the Lepidoptera came to
Sphingoidea light after Linnaeus, as more species were discov-
Noctuoidea ered in tropical regions, more and more categories
The arrangement of the classification of and families were needed to classify the enormous
epidoptera follows a progression somewhat in
L biodiversity discovered in the world. Where
line with our knowledge of how the order Linnaeus had only five families of Lepidoptera in
evolved, from the most primitive moths that 1758, we now have 125 families, 290 subfamilies,
resembled Micropterigidae, to what are now and several hundred tribes. As noted above,
considered the most advanced lepidopterans, remaining controversies often involve whether
the Noctuidae. Yet, advanced features are also some of the subfamilies should be separate fami-
found in other groups, such as the Sesiidae, with lies: for example, in one recent classification, most
their unique wing locking mechanism that nearly of the Gelechioidea families have been reduced to
approaches the similar wing locking found in subfamilies in one enormous family Elachistidae,
wasps (Hymenoptera), and butterflies, where which itself is only a small family among several
some have evolved advanced features like the families of Gelechioidea in the classification used
chordotonal organs found in wing veins of herein. Another case involves the slug caterpillar
Satyrinae (Nymphalidae). families, which evidently have converged on a
Overall, the order has 32 superfamilies and common larval habitus while their fundamental
125 families in the classification adopted herein. evolution, as based on the position of the heart
There is still some controversy in terms of how vessel, demonstrates that the different families
many families and superfamilies there are and belong in two different lineages within the Ditrysia:
how they should be arranged. For example, some the flannel moths (Somabrachyidae and Mega-
other recent classifications for Lepidoptera use 46 lopygidae), as well as the burnet-type moths
superfamilies, splitting many odd families to their (Heterogynidae, Zygaenidae, Himantopteridae,
own monobasic superfamilies. However, the foun- and Lacturidae), all Zygaenoidea, being in Section
dations of the primitive groups (non-Ditrysian Tineina, while the other families with slug cater-
groups) are fairly well established now, although pillars (Dalceridae, Limacodidae, and Chrysopo-
new discoveries can still come to light from remote lomidae), of the Cossoidea, belonging in Section
tropical regions of the world: for example, one Cossina. However, some specialists continue
small family of primitive moths, the Neotheoridae, placing all slug caterpillar families together. These
was only discovered within the past 25 years and differing arrangements often are dependent on the
was based on a single known specimen from experience of various specialists, since many only
Brazil. Since many specialists elevate odd groups study local faunas, for example, and not the
to higher levels, many of the remaining controver- entire global fauna of a family, thus limiting their
sies in Lepidoptera classification pertain to how knowledge and often resulting in the view that
different groups should be treated, i.e., whether as some unusual tropical species should be in a new
630
B Butterflies and Moths (Lepidoptera)

family or subfamily, etc., rather than integrating it Denmark. Some of the most primitive of butterflies
within existing groups. Yet, since most of the bio- still extant, like in the genera Baronia (Papilionidae)
diversity of the order is in the tropics, much study from Mexico and Calinaga (Nymphalidae) from
is still needed for many Lepidoptera groups, and Asia, resemble some of the ancient fossil butter-
especially so on their biologies and immature flies. Evidence of larval feeding is also known in
stages. One can note below in the biodiversity sec- fossils, as for example, from leafminers. Because
tion how many entire families remain completely almost all Lepidoptera are plant feeders, there has
unknown biologically. necessarily also been considerable adaptation to
various plants, what we now consider as insect-
plant coevolution.
Evolution The evolution of Lepidoptera lineages to the
extant families we have today was undoubtedly
Lepidoptera are known as fossils from at least as very reticulate, rather than a simple linear pro-
far back as the Lower Jurassic; thus, the split from gression, and this is evident in our classification
Trichoptera-like relatives undoubtedly occurred as well. For example, among Ditrysian groups
already much earlier. However, fossils of lepi- the families are not related in the sequential
dopterans are not as common as they are for other manner they are listed on paper, but rather they
insect orders, so the evolutionary record is little represent progressions from ancestral divisions
documented. The greatest number of fossil that evolved like branches on a tree. Thus, there
Lepidoptera are known from amber, particularly remain today in each division both primitive
Eocene aged Baltic amber and the younger elements (e.g., those with spined pupae) and
Dominican amber from the Caribbean. There are advanced groups. One can see the relictual
also considerable numbers of Oligocene lepi- groups in the basal families of the main divi-
dopteran fossils known from rocky sediments, like sions, as in the first listed families in Tineoidea,
from Florissant, Colorado, from Tertiary sedi- Sesioidea, Cossoidea and Calliduloidea, while
ments in Italy and other parts of Europe, and from advanced families are present in each division as
late Jurassic layers from Central Asia, among oth- well, each with some advanced features yet in
ers. Most all known fossil Lepidoptera have been different lineages than what led to the most
found in the Northern Hemisphere, and only a few advanced, the Noctuidae.
are known from the Southern Hemisphere, but
this may well be the result of more searching in
Europe and North America than has been done
south of the equator. Characteristics
The older fossil lepidopterans are all of the
kind of species now found in the most primitive All Lepidoptera have a complete, holometabolous
families, such as the mandibulate Micropterigidae life cycle, with separate egg, larva, pupa, and adult
and other homoneurous groups of primitive stages. The morphology of the lepidopteran adult
Lepidoptera. The oldest known lepidopteran fossil and immature stages have been extensively studied,
is from Lower Jurassic layers from England, named with some of the larger species, like some of the
Archeolepis mane. Primitive Hepialidae have been large hawk moths (e.g., Manduca sp., Sphingidae)
found in Palaeocene British limestone and mid- and emperor moths (e.g., the North American
Miocene Chinese deposits. Butterflies are most cecropia moth, Hyalophora cecropia, and the
well known from deposits found at Florissant, polyphemus moth, Antheraea polyphemus, Sat-
Colorado, of Eocene age. An earlier butterfly has urniidae) being used as experimental subjects for
been found in Upper Palaeocene deposits in anatomy and physiology studies, due to their
 Butterflies and Moths (Lepidoptera)
B 631

a vailability and large size. The monarch butterfly the genus Itylos from the high Andes of Bolivia
(Danaus plexippus, Nymphalidae) has also been and Chile is about 610 mm in wingspan, while
used as a model for many morphological studies. the genus Micropsyche, from Afghanistan, is about
7 mm in wingspan, and some American Brephid-
ium specimens are 69 mm in wingspan. Many of
Adults the Microlepidoptera are larger than these small
butterflies. The largest butterflies, such as female
Most Lepidoptera are moderate-sized, winged birdwings of Ornithoptera alexandrae (Papilioni-
insects, averaging about 30 mm in wingspan. The dae) from New Guinea, are over 280 mm in wing-
(Figs.81 and 82) smallest known species, as small span. Another large butterfly is the African
as 2.5 mm in wingspan, are in the pygmy leafminer swallowtail, Papilio antimachus (Papilionidae)
family Nepticulidae, while the largest known lepi- where the elongated wings of some males attain
dopterans are about 300 mm in wingspan, as in 250 mm in wingspan; in this species the females
the emperor moth (or giant silkmoth) family (Sat- are smaller in size.
urniidae). The largest moths among these Saturni- Lepidoptera typically have four wings and
idae include females of the hercules moth scales cover all body parts. Some exceptions occur,
(Coscinocera hercules) from Australia, which have whereby various surfaces may be devoid of scales
large quadrate wings and a large, heavy body, and (e.g., so-called eyespots or clear spots in some
likewise females of the atlas moth, Attacus atlas, and moths and butterflies), but all Lepidoptera have at
related species of the genus Attacus of Southeast least some areas of their external body with the
Asia; males in these species are somewhat smaller. unique lepidopteran scale structures, or squamae
Some of the larger hawk moths (Sphingidae) also (Fig.83). Trichoptera in rare cases also have some
have massive bodies and very thick, strongly veined wing scales, but they typically are hair-like and not
wings, as do some of the carpenterworm moths like scales among lepidopterans and do not cover
(Cossidae), like the Australian Xyleutes affinis, where other body parts. Most lepidopteran scales are flattened
the abdomen in large females attains 70 mm in and ribbed, containing pigments for color. Other
length. There also are exceptionally large winged modified scales include androconia, or scent organs,
species among the primitive ghost moths, family prevalent in such groups as the monarch subfamily
Hepialidae, especially from Australia (e.g., Zelotypia Danainae (family Nymphalidae), where they occur
stacyi) and South Africa (e.g., Leto venus), and such as a patch near the central veins of the hindwings.
other moth families as the giant butterfly moths Wing scales in such species as Morpho butterflies
(Castniidae) and owlet moths (Noctuidae), as well. (subfamily Morphinae, family Nymphalidae) and
An owlet moth (Noctuidae) actually has the record the metallic-like spots of some day-flying moths, as
wingspan, where some females of the white witch in the metalmark moth family (Choreutidae), have
moth (Thysania agrippina) of the Amazon attain the scales modified to refract light, thus producing
wingspans of 305 mm, but the largest emperor the brilliant iridescent blues seen in male Morpho
moths (Saturniidae) have an overall larger wing area butterflies. Many species also have specialized scales
due to their quadrate wing shape. that reflect patterns of ultraviolet light, which wave-
Butterflies also average about 30 mm in wing- lengths are in the main spectrum that Lepidoptera
span, since even though many are large sized, there actually see. Consequently, the UV pattern of many
are a great number of smaller species, particularly lepidopteran wings is very different than what we
among the skippers (Hesperiidae), and also the see as their coloration in white light, and the UV
blues and hairstreaks (Lycaenidae). Butterflies pattern is what is actually being used as visual cues
range in size from less than 7 mm in wingspan to over in mating behavior which may isolate related species.
280 mm. Among the smallest blues (Lycaenidae), Lepidopteran UV patterns have mostly been studied
632
B Butterflies and Moths (Lepidoptera)

Butterflies and Moths (Lepidoptera), Figure81 Lepidopteran head and associated structures: 1. Head
morphology (after Hodges, 1971); 2. Lepidopteran morphology; 3. Head details showing eye cap (after
Hodges, 1971); 4. Haustellum (galea), with inneraspect of right maxilla (left) and outer aspect of left maxilla
(right); 5. Head scaling, rough (Tineidae) (after Falkovitsh and Zagulajev, 1978); 6. Head scaling, smooth
(Gelechiidae) (after Falkovitsh and Zagulajev, 1978); 7. Antennal types: (a) filiform (Eriocraniidae), (b) pecti-
nate (Hepialidae), (c) bipectinate (Saturniidae), (d) club-hooked (Hesperiidae), (e) clubbed (Papilionidae),
(f) thickened (Sphingidae) (after Zerny and Beier, 193638).
 Butterflies and Moths (Lepidoptera)
B 633

Butterflies and Moths (Lepidoptera), Figure82 Lepidopteran wings: 1. Wing regions (after Hodges, 1971);
2. Wing locking mechanisms: Sesiidae double fold (after Heppner and Duckworth, 1981), (a) jugum
(Hepialidae), (b) female frenulum and retinaculum (Sphingidae), (c) male frenulum and retinaculum
(Sphingidae) (ac, after Tillyard, 1926), 3. Wing venation, leafminer (Lyonetiidae) (after Seksjeva, 1981);
4. Wing nomenclature (after Hodges, 1971); 5. Wing venation (Brachodidae) (after Heppner, 1981); 6.
Lepidopteran wing scale (after Spuler, 1910).
634
B Butterflies and Moths (Lepidoptera)

Butterflies and Moths (Lepidoptera), Figure83 Lepidopteran scale morphology (after Ghiradella, 1998): (a)
scale ridges may be modified as lamellae for interference coloration (e.g., Morpho wings); (b) flats between
ridges may be elaborated to produce Tyndall blue coloration (e.g., some Papilio sp.); (c) lamellae of complex
ridges may be shaped to produce reflective coloration (e.g., for metallic-like spots); (d) inter-ridge microribs
may have reduced window-like shapes; (e) flats between ridges may be plate-and-pore configuration (e.g., in
androconial scales of Pieridae); (f) scale interiors may have body-lamellae to produce thin-film interference
colors; and (g) scale interior may be filled with crystallite lattices that produce diffraction colors. ( Ghiradella,
1998; used with permission from author and John Wiley & Sons, Inc.)
 Butterflies and Moths (Lepidoptera)
B 635

in butterflies and not in moths, nor even in day-flying within some species. The more advanced groups
moths, but of course all lepidopteran wing macula- display venation that is more reduced in the number
tion is only seen in UV by the mates, other species, of veins in the hindwings. Some moths, particularly
and other insects. While most lepidopteran scale the tiny leafminer groups (e.g., Nepticulidae, Oposte-
colors will fade after some time exposed to light, gidae, Tischeriidae, Heliozelidae, Gracillariidae,
the structural colors of the modified scales will not Bucculatricidae, among others), often have greatly
fade over time. Most lepidopteran colors are p igment reduced venation in both fore- and hindwings. In
based within the scales, but some is structural. In the homoneurous venation, the fore- and hindwings
yellow and white butterflies, family Pieridae, some of have similar venation, while more importantly, the
the coloration is from excretory deposits. Color hindwing is locked to the forewing in flight by
patterns in Lepidoptera have been the subject of what is called a jugum, rather than the more evolved
extensive studies, especially for butterflies, but also and complicated frenulum and retinaculum
for some of the moths. wing-locking mechanism of the advanced families
Lepidopteran wing shapes can vary consider- of Lepidoptera. The most highly evolved wing-
ably, although the typical form is of four similar locking mechanism is found in most clearwing
wings, with the forewings usually larger than the moths, family Sesiidae, where there is not just a
hindwings. Some unusual species have the hind- frenulum-retinaculum arrangement but the entire
wings greatly reduced in a few cases, or extremely mesal margins of the fore- and hindwings are
narrowed as in the Old World tropical burnet-like recurved to interlock. Butterflies have a humeral
moths of the family Himantopteridae (superfamily lobe wing-coupling mechanism.
Zygaenoidea) and the Amazonian Copiopteryx Body structure in Lepidoptera adults includes
moths (Saturniidae). There are a few rare examples a head, thorax and abdomen, as in other insects,
where the hindwings are almost completely but all covered in lepidopteran scales. The head
atrophied (e.g., some wasp moths, subfamily usually has large compound eyes and prominent
Ctenuchinae, family Arctiidae), and likewise even labial palpi (one tropical Asian family, the Amphi-
for the forewings among a few brachypterous theridae, has the compound eyes of males split in
species. For typical lepidopterans there also are a half). Labial palpi typically are 3-segmented and
variety of wing shapes that are encountered, from the upcurved, but great variation exists in different
more average shape as found in most Noctuidae, for Lepidoptera families. Maxillary palpi, contrast-
example, to the tailed hindwings of swallowtails ingly, are mostly small or even vestigial (sometimes
(Papilionidae), or very pointed wings as in some absent), while the most primitive groups have
tropical burnet moths (Zygaenidae), or the split 5-segmented maxillary palpi. Lepidoptera have
wings found in plume moths (Pterophoridae), and sucking mouthparts as adults, except for the most
the even more split many-plumed moths (Aluciti- primitive families (Micropterigidae, Agathip-
dae), where each wing vein is separated. Many of hagidae, and Heterobathmiidae), which have
the Microlepidoptera have very long hair-like fringe retained mandibular mouthparts (Eriocraniidae
scales along the wing edges, particularly on the have a reduced haustellum and vestigial mandi-
hindwings, as in Gelechioidea families and many bles). The proboscis, or tongue of typical adult
of the leafminers in particular. Lepidoptera, more correctly termed a haustellum,
Wing venation in Lepidoptera has been used is composed of two parts (galeae) that interlock to
for classification since the time of Linnaeus. Most form a sucking tube, usually curled between or
families have wing venation that can help to identify beneath the labial palpi. While some moths have
them, although we now also use many other the haustellum greatly reduced and very short
characters of the body that often are more reliable, (even vestigial or absent in some non-feeding
since wing venation can vary to some extent even Saturniidae, for example), some moths and
636
B Butterflies and Moths (Lepidoptera)

utterflies have a very long haustellum, possibly

b families. The usually 5-segmented tarsi have two
developed to reach nectar sources in long-stemmed hook-like tarsal claws on the last segment. The
flowers. The longest known haustella are in some main thoracic structures of Lepidoptera, however,
hawk moth (Sphingidae) species, where lengths of are the enlarged wings of most species. Brachyp-
up to 30 cm are known. terous species were already mentioned earlier, but
The lepidopteran head has various other most Lepidoptera have well developed wings for
structures (or lack thereof) in different families, all active flight. Some females, however, are flightless
of which are in part used to define the various and without wings, particularly in the family
families, as for example, ocelli and chaetosemata Psychidae, and some species of geometer moths
sensory organs near the antennal bases, and (Geometridae) and tussock moths (Lymantriidae).
maxillary palpi: these vary in different families In the bagworm moths, family Psychidae
and sometimes are atrophied or even completely (Tineoidea), the females are even larviform and
absent. The antennae also vary among different remain within the larval shelter and cocoon as
families, or even among different genera within a adults, waiting for the winged males to find them.
family, with short or very long antennae. Although Like many Lepidoptera, the female bagworm moths
moths typically have antennae of many segments emit a pheromone to attract the males. Among the
that extend to fine points and butterflies have emperor moths (Saturniidae), even faint phero-
antennae with terminal knobs or clubs, there are mone scents have been shown to attract males from
exceptions among some moths (e.g., agaristine up to 20 miles downwind from a female.
Noctuidae and Castniidae have clubbed antennae) The abdomen of adult Lepidoptera is typi-
and even many skippers (Hesperiidae) have curved cally elongated, composed of up to ten segments,
clubs that also resemble some moth antennae usually with the basal segment and the most dis-
(e.g., Sematuridae and Uraniidae). Very long tal segments very reduced. The distal segments
antennae are typical of the small long horned fairy also usually are reduced to integrate with the
moths (family Adelidae), and some others like the genitalic attachments (Fig.84). The main charac-
Asian double eye moths (family Amphitheridae) ters of lepidopteran species identification involve
and most of the tropical longhorned moths (family the usually complex genitalia of male and female
Lecithoceridae). Antennal structure also varies adults. Lepidoptera have some of the most com-
considerably, from simple form to complex bipec- plex genital structures of any insect group, both
tinate antennae (even quadripectinate) as found in the males and the females. Some of the more
in many emperor moths (Saturniidae), or greatly bizarre examples of Lepidoptera genitalia involve
thickened as in most clearwing moths (Sesiidae) such things are complicated spines and setae of
and hawk moths (Sphingidae). The antennae of males, plus variously shaped claspers, and in
male Saturniidae are particularly complex and some females the amazing elongation of the
attuned to dedect faint pheromone plumes from ductus bursae into an extremely long, thin and
females. convoluted tube, as in some Choreutidae (espe-
The thorax of adult lepidopterans has the cially the genus Brenthia). In Gelechiidae, many
usual three pairs of thoracic legs, also covered with of the species have asymmetrical male genitalia,
scales. Butterflies of the family Nymphalidae where one clasper is larger than the other. Among
typically use only the posterior two pairs of butterflies, the parnassians (subfamily Parnassii-
thoracic legs for walking, although they possess all nae, Papilionidae) and also some Acraeinae
three pairs of legs. The tibiae and femora usually (Nymphalidae), have the strange trait of the male
have spurs on the end of the segment and this has adding a post-copulatory plug or covering (called
been used to classify various families, particularly a sphragis) to the female abdomen, preventing
the tibial spurs, which vary in number in different further mating by the female.
 Butterflies and Moths (Lepidoptera)
B 637

Larvae horned devil, which is the larva of the American

regal moth (Citheronia regalis, Saturniidae). Some
While adult Lepidoptera present a large array of hawk moth larvae, or hornworms (Sphingidae)
characters used in classification, the larvae have a can also be very large, as well as some of the larger
completely different set of characters (Fig.85). In carpenter worm larvae (Cossidae). Leafminers,
fact larval classification often conflicts with trends contrarily, are among the tiniest of Lepidoptera
one finds in adult classification. Lepidopteran larvae. The vast majority of Lepidoptera, however,
larvae have mandibles for chewing, and are unique remain unknown biologically and their larvae
in having specialized abdominal legs, called prolegs, have never been seen or studied, nor are their
which usually have ventral hooked setae called hostplants known. Thus, much research remains
crochets. While the similar appearing sawflies to be done on Lepidoptera larvae and their bio
(Symphyta), in the Hymenoptera, are also caterpillar- logies. It can be noted here that even such large
like, they do not have the lepidopteran crochets moths as the white witch moth, Thysania agrippina
and also have too many prolegs, usually 67 pairs (Noctuidae), mentioned earlier as the species with
plus the rear pair, while Lepidoptera typically have the largest known wingspan of any lepidopteran,
only four pairs of prolegs plus a rear pair. The only remains completely unknown biologically, and
known exceptions with supplemental prolegs in that even though the adults are commonly attracted
Lepidoptera occur in one of the families of slug to lights in the Neotropical lowland jungles.
caterpillars, Dalceridae, where late instar larvae Proposed phylogenies based on adults often are
have six pairs of rudimentary prolegs. Contrarily, not substantiated when larvae are compared, and
reduction exceptions are more common, where this often is the cause of taxonomic argument among
larvae have fewer prolegs in unusual cases, as in specialists, particularly for those unfamiliar with lar-
some Noctuidae and most Geometridae where vae or who do not study larvae but instead rely only
there usually are only a single pair of prolegs plus on adult characters. The kind of controversies that
the rear pair. Most leafminers also have evolved arise between larval taxonomy and adult taxonomy,
proleg reduction and even thoracic leg reductions, where the adult taxonomists may not know the lar-
like in Gracillariidae and Nepticulidae, where the vae very well or even ignore their characters, can be
minute larvae have three or fewer pairs of vestigial seen in the Noctuidae, where a recent larval work for
prolegs, or are almost devoid of recognizable European owlet moths has different conclusions for
prolegs (the feeding style inside of leaves has pro- many of the subfamilies from what those studying
duced the evolutionary reduction of the unneeded only adult characters have published.
legs in these cases). Likewise, most of the slug-like Since Lepidoptera larvae spend most of their
caterpillars (e.g., Zygaenoidea, Limacodidae, and time feeding in microhabitats far different than
Megalopygidae) utilize the entire ventral body their adults prefer, larval features are often attuned
surface as a moving platform, much like slugs do, to their needs with very specific body characters.
such that the prolegs are often reduced to mere Thus, larvae that feed inside plants usually have
bumps on the body. reduced setae and smaller legs than do those that
Lepidoptera larvae have their own set of feed externally on plants. Some bizarre shapes and
characters, in particular the array of head and life styles are known among Lepidoptera larvae.
body setae and spines that can be mapped (called For example, the only known aggressively carnivo-
chaetotaxy) and usually are diagnostic for particu- rous lepidopteran larvae occur in Hawaii: species
lar families. Many species can be identified by their of the genus Eupithecia (Geometridae) capture
larvae, but only for those where the larvae are flies as food using massive, modified tarsal claws.
known and have been studied. Some caterpillars A few other moth larvae are also carnivorous
are extremely large and grotesque, like the hickory on aphids and scale insects, like in the genus
638
B Butterflies and Moths (Lepidoptera)

Butterflies and Moths (Lepidoptera), Figure84 Lepidopteran reproductive structures and eggs; 1.
Female genital morphology (after Hodges, 1971); 2. Typical lepidopteran eggs: upper left) Noctuidae
(Amathes), upper right) Notodontidae (Hoplitis), second row left) Notodontidae (Phoesia), second row
right) Noctuidae (Naenia), third row left) Lycaenidae (Thecla), third row right) Nymphalidae (Limentis),
bottom row left) Noctuidae (Spodoptera), bottom row right) Zygaenidae (Zygaena) (after Zagulajev,
1978); 3. Male genital morphology (two types), with detail of typical aedeagus (after Hodges, 1971).
 Butterflies and Moths (Lepidoptera)
B 639

Butterflies and Moths (Lepidoptera), Figure85 Lepidoptera larvae: 1. Larval morphology, with details
of crochets and proleg (after Chapman, 1969; and Mellis and Zocchi, 1958); 2. Larval head morphology
(after Common, 1970); 3. Typical lepidopteran larval types: (a) Hepialidae, (b) Tortricidae, (c) Noctuidae,
(d) Geometridae, (e) Pyralidae, aquatic (Nymphulinae), (f) Gracillariidae (late instar), (g) Gracillariidae
(early instar, Phyllonorycter), (h) Sphingidae) (a-d, after Tillyard, 1926; e, after Bourgogne, 1951; f-g, after
Patocka, 1980; h, after Lutz, 1935).

Pyroderces (Cosmopterigidae), but they do not primitive genera in Lycaenidae, where larvae feed
capture winged insects in rapid attacks like the on ant larvae yet are tolerated by the ants they
larvae in Hawaii. Carnivorous butterfly larvae are live with because of the secretions the larvae give
known in the Asian genus Liphyra, one of the more the ants.
640
B Butterflies and Moths (Lepidoptera)

Eggs Euchloe (Pieridae), Parnassius (Papilionidae), and

Erebia (Nymphalidae)), where living larvae (usually
Lepidoptera eggs usually are rounded and relatively only one) are present in the oviduct of the female
small (about 1 mm), but some groups have flattened and presumably remain there until the female dies,
eggs, as for example among the Tortricidae (Fig. 84). as no actual deposition of living larvae has been
Many butterfly eggs are upright and ribbed. All witnessed in butterflies.
Lepidoptera eggs have a tough shell, called the cho-
rion, plus various degrees of external sculpturing
and usually four sperm entry holes, or micropyles Pupae
(up to 16 in some Notodontidae). The largest lepi-
dopteran eggs are found among some of the The pupal stage varies in form (Fig.86), from those
emperor moth species (Saturniidae) and hawk with loose legs, as in the primitive moths such as Eri-
moths (Sphingidae), up to about 4 mm in diameter ocraniidae, to the most advanced groups where the
(e.g., 4 mm in Argema mittrei and 3.2 mm in Attacus legs of the future adult are fused to the pupal shell.
crameri, Saturniidae). Many of the primitive families, as also Tortricidae
Eggs usually are laid singly or in groups and Sesiidae for example, have noticeable dorsal
directly onto host leaves or stems, but some moth spines on the abdomen of the pupa, used to help
females insert the eggs into plant tissues using a the pupa wiggle out of the cocoon when the adult
very strong ovipositor, particularly among the emerges. Most Lepidoptera pupae have a cremaster
more primitive moths (e.g., Eriocraniidae). The of strong spines or protrusions at the distal end of
average lepidopteran female lays about 100200 the abdomen. Some of the Microlepidoptera pupae
eggs. Species with the greatest numbers of eggs per have only thin hooked setae as a cremaster-like
female are known among the ghost moths (Hepi- structure. While most Lepidoptera larvae spin a
alidae), where some females have been recorded cocoon before transforming into the pupal stage,
with close to 50,000 minute eggs: these moths spray many groups have an exposed pupa, as in most
their eggs randomly about while flying over likely butterflies and some advanced moths like Noctui-
hosts, leaving it to the young caterpillars to find dae. While most pupation and cocoon-making is
their hostplants to feed on upon hatching. on the hostplant, many pupate among debris or in
Although no lepidopteran has been discov- the ground, as for example most of the hawk moth
ered where the adults care for eggs or larvae, as is larvae (Sphingidae) make a pupal cell in soil, from
known in some beetles, many lay their eggs in which the adult must burrow upwards to escape by
secretive sites or devise other protective solutions, means of temporarily retaining the hard pupal
and some species have developed protective com- head covering to push through the soil. The leaf-
mensal relationships with other insects. A notable miners pupate within their leaf mine for the most
case involves the blue butterflies (Lycaenidae), part. Many butterflies simply hang their pupae
where ants typically tend to the larvae and protect upside down from the cremaster plug of silk the
them from predators and parasitoids while getting larva spins just before pupation. Some butterfly
desirable secretions from the larvae. Ovovivipary, larvae (mainly Papilionidae) spin a silken girdle for
however, is known in a few groups of lepidopterans, the pupa (also in Hedylidae and some Geometri-
notably a few Tineidae, Psychidae, Coleophoridae, dae), thus keeping it upright at the pupation site.
and Cosmopterigidae. Psychidae in particular Bagworms (Psychidae) pupate within the larval
have numerous species that are parthenogenetic. shelter (or bag), and likewise for such families
A modified form of this phenomenon is known as the casebearer moths (Coleophoridae) and
among some butterflies (e.g., some Colias and some sackbearer moths (Mimallonidae). Most leaf
 Butterflies and Moths (Lepidoptera)
B 641

Butterflies and Moths (Lepidoptera), Figure86 Lepidoptera pupae: 1. Pupal morphology (after Urguart,
1960), and typical forms: (a) Eriocraniidae, (b) Opostegidae (front and back), (c) Psychidae, (d) Elachistidae,
(e) Pyralidae, (f) Pterophoridae (front and side), (g) Papilionidae, (h) Pieridae, 1951), (i) Lycaenidae, (j)
Nymphalidae, (k) Hedylidae, (l) Sphingidae, (m) Dioptidae (front and back), (n) Noctuidae (a, e, after
Patocka, 1980; b, after Davis, 1989; c, ln, after Mosher, 1916; d, after Falkovitsh, 1981; f, after Zagulajev,
1986; gi, after Bourgogne, 1951; j, after Tillyard, 1926; k, after Scoble and Aiello, 1990).
642
B Butterflies and Moths (Lepidoptera)

webbers, leaf tiers, and leafrollers pupate within the moths (Saturniidae) which have large bright
larval shelter (mostly in the families Oecophoridae, eyespots on the hindwings, use startle techniques
Gelechiidae, Pyralidae, and Tortricidae). to evade predators, since these moths will flash
their hindwings when distrubed from their normal
resting positions where the hindwings are hidden
Ecology beneath the more camouflaged coloration of the
forewings. Butterflies use eye spots for startle effects
Lepidoptera biology includes many strange behav- as well, as for example among the owl butterflies
ioral traits and biologies that have evolved in of the genus Caligo (Brassolinae, Nymphalidae) of
different groups and species.Whereas most the American tropics, and even such species
lepidopterans have rather drab colors that lend as the European peacock butterfly, Inachisio
themselves to good camouflaging when at rest on (Nymphalidae).
leaves or trees, other species have adopted bright Other species, both moths and butterflies,
coloration or startle techniques for protection. use bright coloration not for startle effects but as
Butterflies, of course, as some day-flying moths, warning colors. One of the reasons the warning
use bright coloration or color spots for mating colors are recognized by predators is that the
behavior as well. For example, the bright blues of bodies of these Lepidoptera (or other insects)
the morpho butterflies (Morphinae, Nymphalidae), contain alkaloids their larvae have embibed from
already mentioned for their scale structure, are their hostplants, and thus the adults are poison-
used by males to keep other males away from their ous to most predators like birds and frogs. For
territories, while females may also respond to the example, monarch butterflies (Danaus plexippus,
bright coloration during mating rituals. Likewise, Nymphalidae) and relatives contain poisonous
the bright coloration of morpho butterflies also alkaloids (heart poisons for predators), and most
involves startle defense, since roosting males will birds will not eat the adults once they learn that
congregate on a branch and, when disturbed, flash brightly colored insects are distasteful. Likewise,
their blue colors together (the flash and dazzle for such moths as the very colorful flag moths,
defense), probably scaring away many predators in subfamily Pericopinae (Arctiidae), which are
this way. The morpho flight pattern, a rather believed to all be poisonous as well, due to bodily
bouncing kind of rapid flight in males, also makes alkaloids. Such moths as Zygaenidae, which are
it difficult for predators to find them on the wing, mostly also very colorful, have phytocyanides in
since the blue color flashes only every few seconds their bodies. Some adults of various Lepidoptera
or so as the butterfly flaps its wings when flying groups also imbibe plant chemicals from nectar
through the forest, thus showing only intermit- sources.
tantly where the butterfly is at any instant. However, A varied group of lepidopterans have evolved
some birds have learned how to capture them the use of various plant poisons (mostly alkaloids,
anyway. Some butterflies, especially among the glycosides, phytocyanides, and cardenolides) as
hairstreaks (Lycaenidae), use their hindwing tails defensive agents. Monarch butterflies (Danainae,
as false heads to confuse predators, and many of Nymphalidae), as already noted, sequester alkaloids
the other tailed butterflies may have developed from their hostplants, milkweeds (Asclepiadaceae)
tails for this purpose as well, and likewise for some by the feeding of their larvae. Burnet moths
of the diurnal tailed moths (e.g., Sematuridae and (Zygaenidae) and Heliconius butterflies (Heliconiinae,
Uraniidae). Nymphalidae), among others, do the same for plant
Among the moths, eye spots are well known cyanides, as already noted for larval defense. In the
markings among those species that are not com- case of the burnet moths, the adults are even some-
pletely colored for camouflage. The many emperor what resistant to the fumes of cyanide gas, since
 Butterflies and Moths (Lepidoptera)
B 643

they will survive in a cyanide vial much longer than toxic models known in Lepidoptera, and many
any other Lepidoptera can. Many of these and other appear and behave so much like true wasps that on
traits in Lepidoptera have evolved as defensive the wing one cannot be sure what they are. All
measures against birds and other predators, and these kinds of cases involve what is called Mllerian
parasitoids. There are also many other forms of mimicry, where the mimic has a clear benefit by
defense that lepidopterans use, such as death looking like the model. There is also simple mimicry,
feigning (e.g., many emperor moths will do this if called Batesian mimicry, where the mimics look
disturbed), and excretion of alkaloids from wing like various models and each other, but there is no
bases or abdominal glands (e.g., many Arctiidae do apparent benefit evident like that of having a
this, especially in Pericopinae and the wasp moths, poisonous model. However, there may be some
subfamilies Ctenuchinae and Syntominae). Addi- benefit to mimicking a color pattern that has been
tional adult defenses include such things as loud found to be advantageous for some reason. For
noises, as are found in some brush-footed butterflies example, there is a large mimicry complex of swal-
in the genus Hamadryas (Nymphalidae), where the lowtail butterflies (Papilionidae) and swallowtail
adults make a clicking or crackling sound when moths (Urania, Uraniidae) in the Neotropics, yet
they fly, possibly scaring bird predators in this way. where none of the possible models are poisonous
Mimicry with other insects and among each but do all have variegated patterns of striped green
other is a further use of color and maculation as and black. Likewise, there is a similar mimicry
part of defense strategies in Lepidoptera. Mimicry complex in New Guinea involving blue Uraniidae
among Lepidoptera involves various species (genus Alcides) and several swallowtail butterflies
looking similar to one or more that are poisonous (Papilio laglaizei, P. ulysses, and P. pericles, and even
by their bodily alkaloids, as noted earlier. Thus, a P. woodfordi), where all have bands or patches of
poisonous tiger moth (Arctiidae), or butterfly like blue color surrounded by black bands.
the monarch, is the model that other lepidopterans Although most Lepidoptera larvae use cam-
have taken the appearance to obtain the same ouflage for protection, others use startle effects or
defensive protection yet without themselves being bright coloration as a protective strategy, much as
poisonous. For example, in the case of the monarch do some adult lepidopterans. For example, the
there is the well known North American mimic, bright colors of some hawk moth larvae such as
the Viceroy butterfly, Limenitis archippus (Nymph- the giant gray sphinx of the Neotropics, also called
alidae), which itself is not distasteful or poisonous the frangipani sphinx (Pseudosphinx tetrio, Sphin-
to birds and other predators. Extensive mimicry gidae), where the large larvae are banded in bright
complexes occur, particularly in the tropics, yellow and black, with an orange head, are thought
especially modelled around some of the flag moths to possibly mimic coral snakes, since they also
(subfamily Pericopinae, family Arctiidae). Like- move their bodies rapidly when disturbed and will
wise, there are also mimicry complexes modelled even strike at a predator like a snake. Some make
after other insects that are avoided by birds and noises if disturbed, as for example in the death-
other predators, such as polistine wasps (Vespidae, head sphinx, Acherontia atropos (Sphingidae),
Hymenoptera) and stink bugs (Pentatomidae, mentioned earlier for its adult noises, which also
Hemiptera). Thus, we find many so-called wasp makes noises in the larval stage using its mandibles;
moths, subfamilies Ctenuchinae and Syntominae and likewise for some Saturniidae larvae and
(family Arctiidae), that appear remarkably like real others. Even some larvae among the Microlepi-
species of wasps, plus other moths both among doptera make noises when disturbed, as for example
Arctiidae and Pyralidae that have modelled them- in the larvae of Diurnea fagella (Oecophoridae), of
selves after some bugs or beetles. The wasp moths Europe, where larvae scrap their claws on a leaf
include mimics that are among the most precise to surface. Pupal noises are also known among some
644
B Butterflies and Moths (Lepidoptera)

lepidopterans. Some Lepidoptera pupae also can are also irritating in some cases. Even deaths have
make rasping sounds by moving their abdominal occurred by persons in the tropics from contact
segments together. with some caterpillars of the emperor moths
Larval defense also takes on the form of (Saturniidae), especially the Brazilian Lonomia sp.
ferocious appearance and head movements, as for (even the adults in this group have irritating wing
example in the large hickory horned devil, scales). The larvae of this genus have poison glands
Citheronia regalis (Saturniidae), of North America, that inject a chemical, when touched, that triggers
which not only has large spined horns but will rear human blood coagulation problems and also
its head swiftly back to hit anything that grabs its haemorrhagic reactions in some cases, thus causing
body. A number of tropical hawk moth larvae some of the reported deaths in Brazil. Another
(Sphingidae) rear up when disturbed and retract potent genus among the emperor moths, both for
their head into a large thorax, while thoracic eye larval poisonous spines and irritation from adult
spots make them then appear like snake heads. scales, is Hylesia (Saturniidae). These so-called
One of the most accurate snake mimics, or viper stinging caterpillars are well protected in this way
worms, is the larva of the Neotropical hawk from most predators, but still can be subject to the
moth, Hemeroplanes ornatus (Sphingidae). As with tiny parasitoid wasps that can insert their eggs
adults, some larvae also have poisonous alkaloids between larval spines, or circumvent their defenses
as defensive measures that back up their bright by getting to the egg stage instead.
colors, as in the wasp moths (Ctenuchinae) of the The topic of stinging caterpillars is called lepi-
American tropics and their Old World cousins, dopterism in the medical profession, and deals
wasp moths in the subfamily Syntominae (family with allergic reactions to certain poisons. The genus
Arctiidae), and the American flag moth larvae Lonomia is part of the New World subfamily
(subfamily Pericopinae), for example, where larvae Hemileucinae (Saturniidae) and most all of these
can also be colorful. have poisonous spines, as for example the io moth
Some larvae also make use of defense in num- (Automerisio) of North America and the several
bers, thus feeding in large masses so any predator hundred species in this group from South America.
finding them will undoubtedly still enable some to The slug caterpillars, families Limacodidae and
escape: for example, many of the tent caterpillars Megalopygidae, are likewise well known for their
(Lasiocampidae) feed in large masses and make poisonous spines. Some stinging caterpillars even
tent protective webs as well. The same massing spin the left over spines from their larval skin into
behavior is also known in other lepidopteran their cocoon and protect the cocoon in this way as
larvae, like the processionary caterpillars of the well, as for example in the Lonomia moths from
subfamily Thaumetopoeinae (Notodontidae), Brazil. Lepidopterism is also known in other
famous for traveling in a long single file when families, even in the Australian Anthelidae, where
moving from one host tree to another, both in contact with cocoons of one species can cause
Europe and in tropical species of the group. The allergic reactions due to urticating setae.
unusual tropical Himantopteridae (Zygaenoidea) Commensal relationships among larvae, where
also congregate as masses of larvae. some benefit is obtained from the interaction with
Other larval defenses include poisonous setae, another insect, is a further form of protection for
which can be very potent for persons particularly some lepidopterans. Many blues and relatives
allergic to the stings. There are a number of such (Lycaenidae) have commensal relations as larvae
stinging caterpillars in North America, as also in with ants, so-called myrmecophily. The larvae
other faunal regions, particularly in the moth obtain protection from predators and even parasi-
families Limacodidae, Megalopygidae, and Sat- toids in many cases, and the ants obtain wanted
urniidae. Setae of tussock moth larvae (Lymantriidae) secretions from the larvae, much like we do with
 Butterflies and Moths (Lepidoptera)
B 645

milk cows. Some metalmark butterflies (Riodinidae) Asia, fly in the late afternoon and at dusk, while
also have myrmecophilous larvae. during most of the day they are to be found at rest
Flight is what is most typical of Lepidoptera, in dark thickets in the forest. Likewise, many moths
besides their often colorful wing maculation. will fly only in the evening hours before midnight,
Some groups, like the clearwing moths (Sesiidae) while some fly only before dawn. Some moths are
and hawk moths (Sphingidae), have developed also diurnal and like butterflies, have particular
very strong wings used for often exceedingly fast flight periods, as before noon (e.g., most Sesiidae),
flight. Among the fastest known lepidopterans are or at dusk only (most Hepialidae, and some Sphin-
some in the family Sphingidae, especially in some gidae and Saturniidae). Crepuscular moths also
of the day-flying species, where flight speeds to include some of the giant butterfly moths (family
35 mph are known. While most lepidopteran flight Castniidae) of the Neotropics, Australia, and
is rather slow, with slowly flapping wings and some Southeast Asia, and also a large number of leafro
gliding, the fastest fliers and hoverers have exceed- ller moths (family Tortricidae). The Hedylidae,
ingly rapid wing beats. For example, the hawk which some consider nocturnal butterflies but are
moths (Sphingidae) typically fly like humming- herein retained in Geometroidea, fly at night. All
birds and can hover in place while feeding on the above is likewise true for larval feeding activity
flower nectar. Butterflies can hover at nectar among various groups, with some feeding only at
sources to some extent as well, by flapping their night and others at various times, or only during
wings, but only hawk moths have the excessively daylight.
rapid wing beat that allows hummingbird-like For adults, there is also specialized flight,
steady hovering in place. Even within one family besides searching for food or mates, like directed
flight behavior can vary considerably among migration, as exhibited in such species as the mon-
different genera, as for example, in Saturniidae, arch butterfly (Danaus plexippus, Nymphalidae)
where most have rather slow lumbering flight in their migrations in North America to spend
behavior, yet in the American genus Hemileuca the winter months in Mexico. Western North American
day-flying males can rival hawk moths in speed of monarchs overwinter in coastal California. Related
flight. Likewise, male yucca skippers (Megathymi- danaines on Hispaniola, of the genus Anetia
nae, family Hesperiidae), mostly in the American (Nymphalidae), congregate in the higher elevations
Southwest, also typically fly very fast in search of of the Dominican Republic. There are many other
females. Of course, flight in Lepidoptera has been migratory species recorded, and in all faunal
studied extensively, and particularly how this regions. For example, some owlet moths (Noctuidae)
relates to adult mating behavior and migration in Australia and Europe, snout butterflies (Libyt-
in butterflies. heidae) in North America and Africa, and black
Activity regimes among Lepidoptera vary as danaines (Euploea spp., Nymphalidae) in Taiwan,
much as other features of their life histories. While which overwinter in secluded areas protected from
most butterflies are diurnally active as adults and sever frosts, like the North American monarchs
most moths are nocturnal, there are many excep- do. Hawk moths and owlet moths migrate over
tions. Many butterfly species have particular times mountain passes during certain times of the year
of active flight, such as only briefly in the morning in Venezuela, as do some butterflies. Some diurnal
or at dusk, or only midday. For example, the moths also have migratory flights, like the migra-
Neotropical owl butterflies (Caligo, subfamily tions of Urania moths (Uraniidae) in the Neotropics.
Brassolinae, Nymphalidae), and their relatives, Many other cases of migrating Lepidoptera are
typically fly at dusk. The related jungle queen known. Some of the cases of large flights are more
butterflies, as in the genus Stichophthalma (sub- seasonal and directed mass movement in relation
family Amathusiinae, Nymphalidae) from Southeast to population pressure than they are migration in
646
B Butterflies and Moths (Lepidoptera)

the sense of the complex annual two-way migration moths, mainly Noctuidae and some Geometridae
sequence as evidenced in the American monarch. and Pyralidae, but also a few Notodontidae and
Aggregation is well known with some Thyatiridae, which rest on the edges of the eyes of
overwintering butterflies, but there also are mass large mammals and suck eye juices from the
roostings that some species use during the night, surface of the eyes. In the case of the blood sucking
presumably as protection against predators, species, the haustellum has been modified to pierce
although this has not been proven conclusively. skin and suck blood, much as in mosquitoes, a
For example, Heliconius butterflies (Nymphalidae) modification from fruit-piercing owlet moths
typically roost in large assemblages at night. (Noctuidae), like in the Asian genus Othreis and
Likewise, for morpho butterflies (Morphinae, the New World Gonodonta.
Nymphalidae). Roosting behavior has also been Of all studies on Lepidoptera, besides those on
documented in other tropical butterflies as well. butterfly and moth life histories, those pertaining to
Few moths have roosting activity like those noted population biology and biogeography of butterflies
for some butterflies, and most such cases for moths have probably been the most numerous over the
involve resting sites for large groups of adults in years, and include most all aspects of lepidopteran
one area but not like the dense roosting biology, from larval food preferences, to genetics, to
documented for butterflies. For example, one finds mimetic relationships, to seasonality, to taxonomy
large numbers of grass loopers, genus Mocis of the species involved. Many such studies world-
(Noctuidae), resting together in Florida, which wide, many now classic, can be referenced. Among
can be startled into mass flight over short distances the hundreds of examples are the well known stud-
when disturbed during the day. Likewise, Nyctemera ies on various checkspot butterflies (Euphydryas sp.,
tiger moths (Arctiidae) have similar mass startle Nymphalidae) in California and other areas of
flight responses in the Oriental tropics when North America. Likewise, studies in North America
disturbed during the day. Various other owlet for Colorado butterflies and the many recent studies
moths (Noctuidae), geometer moths (Geometridae), on swallowtails (Papilionidae), as well as innumer-
and snout moths (Pyralidae) also rest in groups able similar studies in Japan, Africa, and other
and fly away in swarms when disturbed during regions. In Europe, one has studies like on blues
daylight. Most cases of diurnal moths coming to (Lycaenidae), various other British butterflies, and
lights at night are due to being disturbed and then many others. Likewise, innumerable studies have
going to the nearest light source. There are also been done on the ecology and population biologies
cases of cold adaptation techniques where moths of tropical butterflies. Such studies for moths, how-
at high altitudes or during the winter will mass in ever, are much fewer, as for example on European
large numbers: for example, there are some owlet pine looper moths (Geometridae) and California
moths, genus Euxoa (Noctuidae), that do this oak moths (Dioptidae), to give just a few examples
during cold nights in the North American Rockies, out of thousands of studies, but mainly on economic
notably recorded as also being a food source species and their control.
for bears.
Among some of the other more bizarre behav-
ior found among the Lepidoptera, one can note Biodiversity
the blood sucking activity of one species of owlet
moth in the genus Calyptra (Noctuidae) from The following notes summarize the main
Southeast Asia, which attacks large mammals such groupings and the 125 extant families of Lepi-
as buffalo, cows and deer. This behavior is appar- doptera in the world. The most primitive moths
ently a development of the eye-frequenting (or are discussed together, while more advanced
lachryphagous) behavior among other Asian families are treated according to their respective
 Butterflies and Moths (Lepidoptera)
B 647

superfamilies. Families are listed in the table. AGATHIPHAGOIDEA

The species totals given for each family have AGATHIPHAGIDAE - Kauri Moths
been updated to include all valid species Suborder: HETEROBATHMIINA
described to the year 2000. HETEROBATHMIOIDEA
The world total number of known species HETEROBATHMIIDAE - Valdivian Archaic Moths
comes to 156,100 species. An estimated additional Suborder: GLOSSATA
100,000 species remain to be discovered and Cohort: DACNONYPHA
named, mainly from tropical regions of the world, Infraorder: DACNONYPHA
including many of the most imperiled habitats. ERIOCRANIOIDEA
During the decade from 1990 to 2000, about 8,500 ERIOCRANIIDAE - Sparkling Archaic Sun Moths
Lepidoptera species were described from all ACANTHOPTEROCTETIDAE - Archaic Sun
regions, particularly from remote areas of tem- Moths
perate Central Asia and from the tropical forests Acanthopteroctetinae
of Southeast Asia and Central Africa. Thus, the Catapteriginae
rate of new discoveries and descriptions of new Infraorder LOPHOCORONINA
species remains fairly steady, averaging about 850 LOPHOCORONOIDEA
species per year among Lepidoptera. However, LOPHOCORONIDAE - Australian Archaic Sun
unless larger and more active surveys are made of Moths
critical and unknown tropical and other remote Cohort: MYOGLOSSATA
regions, and unless the training of more taxono- Subcohort: MYOGLOSSATA
mists to study new material is increased, it will Infraorder: NEOPSEUSTINA
take another 100 years to complete the basic NEOPSEUSTOIDEA
inventory of the remainder of the Lepidoptera NEOPSEUSTIDAE - Archaic Bell Moths
not yet identified from among the total extant Subcohort: NEOLEPIDOPTERA
worldwide fauna of about 255,000 living species. Infraorder: EXOPORIA
Unfortunately, estimates of yearly forest and other MNESARCHAEOIDEA
habitat destruction do not leave us 100 years for MNESARCHAEIDAE - New Zealand Primitive
this inventory to be accomplished in many areas Moths
of the world under the most intense human pop- HEPIALOIDEA
ulation and development pressures. And likewise, NEOTHEORIDAE - Amazonian Primitive Ghost
the basic inventories to describe all extant species Moths
do not involve detailed biological studies to deter- ANOMOSETIDAE - Australian Primitive Ghost
mine the life histories of these newly discovered Moths
species. Even most of the species already described PROTOTHEORIDAE - African Primitive Ghost
remain unknown biologically, so another larger Moths
cadre of researchers is needed to study the biolo- HEPIALIDAE - Ghost Moths
gies involved. PALAEOSETIDAE - Miniature Ghost M oths
ORDER: LEPIDOPTERA Infraorder: HETERONEURA
Suborder: ZEUGLOPTERA Division: MONOTRYSIA
MICROPTERIGOIDEA Section: NEPTICULINA
MICROPTERIGIDAE - Mandibulate Archaic ANDESIANOIDEA
Moths ANDESIANIDAE - Valdivian Forest M
oths
Micropteriginae NEPTICULOIDEA
Sabatincinae NEPTICULIDAE - Pygmy Moths
Suborder: AGLOSSATA Pectinivalvinae
648
B Butterflies and Moths (Lepidoptera)

Nepticulinae Eriocottinae
OPOSTEGIDAE - Eye-Cap Moths Compsocteninae
TISCHERIOIDEA PSYCHIDAE - Bagworm Moths
TISCHERIIDAE - Trumpet Leafminer M
oths Lypusinae
PALAEPHATOIDEA Naryciinae
PALAEPHATIDAE - Gondwanaland Moths Taleporiinae
Section: INCURVARIINA Penestoglossinae
INCURVARIOIDEA Psychinae
INCURVARIIDAE - Leafcutter Moths Oiketicinae
Incurvariinae ARRHENOPHANIDAE - Tropical Lattice Moths
Crinopteryginae Series Gracillariiformes
CECIDOSIDAE - Gall Moths AMPHITHERIDAE - Double-Eye Moths
PRODOXIDAE - Yucca Moths SCHRECKENSTEINIIDAE - Bristle-Legged Moths
Lamproniinae DOUGLASIIDAE - Douglas Moths
Prodoxinae BUCCULATRICIDAE - Ribbed-Cocoon Maker
ADELIDAE - Longhorned Fairy Moths Moths
Nematopogoninae GRACILLARIIDAE - Leafminer Moths
Adelinae Gracillariinae
HELIOZELIDAE - Shield Bearer Moths Lithocolletinae
Division: DITRYSIA Phyllocnistinae
Section: TINEINA GELECHIOIDEA
Subsection: TINEINA OECOPHORIDAE - Concealer Moths
TINEOIDEA Depressariinae
Series Tineiformes Ethmiinae
ACROLOPHIDAE - Tube Moths Peleopodinae
Amydriinae Autostichinae
Acrolophinae Xyloryctinae
TINEIDAE - Fungus Moths Stenomatinae
Euplocaminae Oecophorinae
Myrmecozelinae Hypertrophinae
Harmacloninae Chimabachinae
Meessiinae Deuterogoniinae
Dryadaulinae LECITHOCERIDAE - Tropical Longhorned Moths
Scardiinae Ceuthomadarinae
Nemapogoninae Oditinae
Tineinae Lecithocerinae
Setomorphinae Torodorinae
Perissomasticinae ELACHISTIDAE - Grass Miner Moths
Hapsiferinae Perittiinae
Hieroxestinae Elachistinae
Erechthiinae PTEROLONCHIDAE- Lance-Wing Moths
Siloscinae GELECHIIDAE - Twirler Moths
Stathmopolitinae Physoptilinae
Teichobiinae Gelechiinae
ERIOCOTTIDAE - Old World Spiny-Winged Moths Pexicopiinae
 Butterflies and Moths (Lepidoptera)
B 649

Dichomeridinae IMMOIDEA
BLASTOBASIDAE - Scavenger Moths IMMIDAE - Imma Moths
Holcocerinae PYRALOIDEA
Blastobasinae HYBLAEIDAE - Teak Moths
COLEOPHORIDAE - Casebearer Moths THYRIDIDAE - Picture-Winged Leaf M
oths
Coleophorinae Simaethistinae
Batrachedrinae Whalleyaninae
MOMPHIDAE - Mompha Moths Argyrotypinae
AGONOXENIDAE - Palm Moths Thyridinae
Agonoxeninae Siculodinae
Blastodacninae Striglininae
COSMOPTERIGIDAE - Cosmet Moths PYRALIDAE - Snout Moths
Antequerinae Group Crambinina
Cosmopteriginae Crambinae
Chrysopeleiinae Schoenobiinae
SCYTHRIDIDAE - Flower Moths Cybalomiinae
COPROMORPHOIDEA Linostinae
COPROMORPHIDAE - Tropical Fruitworm Moths Scopariinae
ALUCITIDAE - Many-Plumed Moths Musotiminae
CARPOSINIDAE - Fruitworm Moths Midilinae
EPERMENIIDAE - Fringe-Tufted Moths Nymphulinae
Epermeniinae Odontiinae
Ochromolopinae Noordinae
YPONOMEUTOIDEA Wurthiinae
OCHSENHEIMERIIDAE - Cereal Stem Moths Evergestinae
GLYPHIPTERIGIDAE - Sedge Moths Glaphyriinae
Orthoteliinae Pyraustinae
Glyphipteriginae Group Pyralinina
PLUTELLIDAE - Diamondback Moths Pyralinae
Ypsolophinae Chrysauginae
Plutellinae Galleriinae
Scythropiinae Epipaschiinae
Praydinae Phycitinae
ATTEVIDAE - Tropical Ermine Moths PTEROPHOROIDEA
YPONOMEUTIDAE - Ermine Moths TINEODIDAE - False Plume Moths
Saridoscelinae OXYCHIROTIDAE - Tropical Plume M oths
Yponomeutinae PTEROPHORIDAE - Plume Moths
Cedestinae Macropiratinae
ARGYRESTHIIDAE - Shiny Head-Standing Moths Agdistinae
LYONETIIDAE - Lyonet Moths Ochyroticinae
Cemiostominae Deuterocopinae
Lyonetiinae Pterophorinae
Bedelliinae Subsection: SESIINA
ACROLEPIIDAE - False Diamondback Moths SESIOIDEA
HELIODINIDAE - Sun Moths BRACHODIDAE - Little Bear Moths
650
B Butterflies and Moths (Lepidoptera)

Pseudocossinae METARBELIDAE - Tropical Carpenterworm Mo-

Brachodinae ths
Phycodinae Series Limacodiformes
SESIIDAE - Clearwing Moths CYCLOTORNIDAE - Australian Parasite Moths
Tinthiinae EPIPYROPIDAE - Planthopper Parasite Moths
Paranthreninae Epipyropinae
Sesiinae Heteropsychinae
URODIDAE - False Burnet Moths DALCERIDAE - Tropical Slug Caterpillar Moths
Galacticinae Acraginae
Urodinae Dalcerinae
CHOREUTIDAE - Metalmark Moths LIMACODIDAE - Slug Caterpillar Moths
Millieriinae CHRYSOPOLOMIDAE - African Slug Caterpillar
Brenthiinae Moths
Choreutinae Ectropinae
ZYGAENOIDEA Chrysopolominae
HETEROGYNIDAE - Mediterranean B urnet Moths CASTNIOIDEA
ZYGAENIDAE - Burnet Moths CASTNIIDAE - Giant Butterfly Moths
Zygaeninae Synemoninae
Phaudinae Neocastniinae
Charideinae Castniinae
Chalcosiinae TORTRICOIDEA
Anomoeotinae TORTRICIDAE - Leafroller Moths
Callizygaeninae Tortricinae
Procridinae Chlidanotinae
HIMANTOPTERIDAE - Long-Tailed Burnet Olethreutinae
Moths Subsection: BOMBYCINA
LACTURIDAE - Tropical Burnet Moths CALLIDULOIDEA
SOMABRACHYIDAE - Mediterranean Flannel RATARDIDAE - Oriental Parnassian M
oths
Moths PTEROTHYSANIDAE - Parnassian M oths
MEGALOPYGIDAE - Flannel Moths Pterothysaninae
Aidinae Hibrildinae
Megalopyginae CALLIDULIDAE - Old World Butterfly Moths
Trosiinae Griveaudiinae
Section: COSSINA Callidulinae
Subsection: COSSINA URANIOIDEA
COSSOIDEA EPICOPEIIDAE - Oriental Swallowtail Moths
Series Cossiformes Schistomitrinae
COSSIDAE - Carpenterworm Moths Epicopeiinae
Chilecomadiinae APOPROGONIDAE - African Skipper Moths
Cossulinae SEMATURIDAE - American Swallowtail Moths
Cossinae URANIIDAE - Swallowtail Moths
Hypoptinae Uraniinae
Zeuzerinae Microniinae
DUDGEONEIDAE - Dudgeon Carpenterworm EPIPLEMIDAE - Crenulate Moths
Moths Auzeinae
 Butterflies and Moths (Lepidoptera)
B 651

Epipleminae Riodininae
GEOMETROIDEA LIBYTHEIDAE - Snout Butterflies
GEOMETRIDAE - Geometer Moths NYMPHALIDAE - Brush-Footed Butterflies
Archiearinae Group Nymphalinina
Oenochrominae Tellervinae
Orthostixinae Danainae
Ennominae Ithomiinae
Desmobathrinae Acraeinae
Geometrinae Heliconiinae
Sterrhinae Nymphalinae
HEDYLIDAE - American Butterfly Moths Group Satyrinina
PAPILIONOIDEA Calinaginae
Series Hesperiiformes Apaturinae
HESPERIIDAE - Skipper Butterflies Amathusiinae
Megathyminae Morphinae
Coeliadinae Brassolinae
Pyrrhopyginae Satyrinae
Pyrginae DREPANOIDEA
Trapezitinae AXIIDAE - Gold Moths
Heteropterinae THYATIRIDAE - False Owlet Moths
Hesperiinae Thyatirinae
Series Papilioniformes Polyplocinae
PAPILIONIDAE - Swallowtail Butterflies CYCLIDIIDAE - Giant Hooktip Moths
Baroniinae DREPANIDAE - Hooktip Moths
Parnassiinae Drepaninae
Papilioninae Oretinae
PIERIDAE - Yellow-White Butterflies Nidarinae
Pseudopontiinae BOMBYCOIDEA
Dismorphiinae Series Bombyciformes
Pierinae CARTHAEIDAE - Australian Silkworm Moths
Coliadinae EUPTEROTIDAE - Giant Lappet Moths
LYCAENIDAE - Gossamer-Winged Butterflies Janinae
Lipteninae Eupterotinae
Poritiinae Panacelinae
Liphyrinae APATELODIDAE - American Silkworm Moths
Miletinae Apatelodinae
Curetinae Epiinae
Lycaeninae Phiditiinae
Theclinae BOMBYCIDAE - Silkworm Moths
Polyommatinae Bombycinae
RIODINIDAE - Metalmark Butterflies Prismostictinae
Styginae MIMALLONIDAE - Sackbearer Moths
Hamearinae ANTHELIDAE - Australian Lappet Moths
Euselasiinae Munychryiinae
Corrachiinae Anthelinae
652
B Butterflies and Moths (Lepidoptera)

LASIOCAMPIDAE - Lappet Moths Dudusinae

Chondrosteginae Heterocampinae
Chionopsychinae Nystaleinae
Poecilocampinae Meiceratinae
Macromphaliinae DIOPTIDAE - American False Tiger Moths
Lasiocampinae Dioptinae
Series Saturniiformes Doinae
ENDROMIDAE - Glory Moths THYRETIDAE - African Maiden Moths
Endrominae LYMANTRIIDAE - Tussock Moths
Mirininae Orgyiinae
LEMONIIDAE - Autumn Silkworm Moths Lymantriinae
Lemoniinae ARCTIIDAE - Tiger Moths
Sabaliinae Group Pericopinina
BRAHMAEIDAE - Brahmin Moths Pericopinae
Dactyloceratinae Group Arctiinina
Brahmaeinae Lithosiinae
OXYTENIDAE - American Tropical Silkworm Arctiinae
Moths Group Ctenuchinina
CERCOPHANIDAE - Andean Moon Moths Ctenuchinae
Cercophaninae Syntominae
Janiodinae NOCTUIDAE - Owlet Moths
SATURNIIDAE - Emperor Moths Group Aganainina
Arsenurinae Aganainae
Ceratocampinae Group Herminiinina
Hemileucinae Herminiinae
Agliinae Group Noctuinina
Ludiinae Hypenodinae
Salassinae Rivulinae
Saturniinae Hypeninae
SPHINGOIDEA Catocalinae
SPHINGIDAE - Hawk Moths Euteliinae
Smerinthinae Stictopterinae
Sphinginae Sarrothripinae
Macroglossinae Chloephorinae
NOCTUOIDEA Nolinae
NOTODONTIDAE - Prominent Moths Plusiinae
Group Oenosandrinina Acontiinae
Oenosandrinae Condicinae
Group Thaumetopoeinina Amphipyrinae
Thaumetopoeinae Stiriinae
Group Notodontinina Psaphidinae
Pygaerinae Agaristinae
Platychasmatinae Cocytiinae
Notodontinae Heliothinae
Phalerinae Acronictinae
 Butterflies and Moths (Lepidoptera)
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Pantheinae Micropterigidae (mandibulate archaic moths)

Bryophilinae total 130 species worldwide. There are two sub-
Cuculliinae familes. Adults are minute to small and diurnal.
Hadeninae Larvae feed on mosses, liverworts, or detritus.
Noctuinae

Agathiphagoidea
Primitive Moths
Agathiphagoidea are also a monobasic super-
family, containing the relict family, Agathiphagi-
The families considered the most primitive of all
dae.Adults have chewing mouthparts (haustellum
lepidopterans, in the groups up to Myoglossata,
absent) and are similar to Micropterigidae.
include the first six families. The first three
Agathiphagidae (kauri moths) total only two
superfamilies are all relictual base lineages of the
known species, from Australia and Fiji. Adults are
Lepidoptera and also have only one family in each
small and diurnal. Larvae are seed-borers of kauri
superfamily and each suborder: Micropterigidae
pines (Araucariaceae).
(Micropterigoidea, suborder Zeugloptera), Agath-
iphagidae (Agathiphagoidea, suborder Aglossata),
and Heterobathmiidae (Heterobathmioidea, sub-
Heterobathmioidea
order Heterobathmiina). They are all small moths
(not over 16 mm in wingspan), concentrated most
Heterobathmioidea are one of the most obscure
in what are now considered refugia regions of the
groups, based on only a single family, Heterobath-
world where the oldest faunas remain, so-called
miidae. Adults have small mandibles (haustellum
Gondwanaland distributions, notably in South
absent).
Africa, Australia, New Zealand, and Chile,
Heterobathmiidae (Valdivian archaic moths)
although some are more widespread like the
include about nine species, with named thus far all
Micropterigidae which occur in all regions. All
from southern South America. Adults are small
have homoneurous venation and a jugum for wing
and diurnal. Larvae are leafminers of Nothofagus
coupling of the fore- and hindwings during flight,
trees (Fagaceae).
and the hindwings are mostly about the same size
as the forewings. Adults have small mandibles
instead of the usual lepidopteran haustellum (or
Eriocranioidea
proboscis) of the Aglossata, but the primitive
families of the Glossata also have a reduced
The superfamily Eriocranioidea contains two
haustellum in addition to vestigial mandibles.
families, together comprising the Infraorder
Most of the primitive moths also have large
Dacnonypha. Adults have a reduced haustellum
5-segmented maxillary palpi and the head ver-
but retain vestigial mandibles.
tex vestiture with long scales or hair-like scales.
Eriocraniidae (sparkling archaic sun moths)
are a Holarctic family of 25 species, about half in
Europe and half in North America. Adults are
Micropterigoidea small and diurnal. Larvae are leafminers on a vari-
ety of hardwood trees and other plants.
Micropterigoidea contain the single family, Acanthopteroctetidae (archaic sun moths) are
Micropterigidae (in the past misspelled as very similar to Eriocraniidae, and include only
Micropterygidae). four species, all North American except for one in
654
B Butterflies and Moths (Lepidoptera)

the Palearctic. Adults are small and thought to be Exoporia

diurnal. Larvae are blotch leafminers on Ceanothus
(Rhamnaceae) for the single species known This first infraorder of the Neolepidoptera,
biologically. Exoporia, has two superfamilies, Mnesarchaeoidea
and Hepialoidea, with six primitive moth families
in total. Wing venation is homoneurous and a
Lophocoronoidea jugum is used for wing coupling.

Representing the infraorder Lophocoronina, this

monobasic superfamily contains the small archaic Mnesarchaeoidea
family, Lophocoronidae. Adults have the haustel-
lum reduced (mandibles vestigial). This superfamily is contains a single family of
Lophocoronidae (Australian archaic sun primitive moths, the Mnesarchaeidae. Adults
moths) have six known species in Australia. Adults have the haustellum short (mandibles vestigial).
are small and crepuscular in sclerophyll eucalyptus Mnesarchaeidae (New Zealand primitive
woods. Biologies and larvae remain unknown.. moths) occur only in New Zealand, with eight
known species. Adults are small and diurnally
active in forest clearings and near ferns. Biologies
Myoglossata and larvae remain unknown.

The cohort Myoglossata are divided into two sub-

cohorts: Myoglossata and Neolepidoptera, where Hepialoidea
the subcohort Myoglossata contains only a single
infraorder, Neopseustina, and the Neolepidoptera This superfamily comprises the first group of
have two infraorders (Exoporia and Heteroneura) lepidopterans with several families, although most
which contain all the remaining Lepidoptera. species are in Hepialidae, the ghost moths. The
superfamily comprises 616 known species world-
Neopseustina wide. All are relict groups that retain a jugum for
wing coupling, and are rather small moths, but
This infraorder contains only the single superfamily Hepialidae also have some of the largest species of
Neopseustoidea. Wing venation is homoneurous the micro -moths known (up to 250 mm in wing-
and a jugum is used for wing coupling. Adults have span). Adults with reduced haustellum (sometimes
the haustellum short (mandibles vestigial). absent) and usually with vestigial mandibles (absent
in Hepialidae and Palaeosetidae); antennae are
mostly short; hindwings tend to be nearly as long
Neopseustoidea as the forewings.
Neotheoridae (Amazonian primitive ghost
This first group of the Myoglossata includes only moths) include a single species from the Mato
the single archaic family Neopseustidae. Grosso area of Brazil (two more species have been
Neopseustidae (archaic bell moths) include discovered recently). Adults are medium size.
nine known species (six from Southeast Asia and Biologies and larvae remain unknown.
three from Chile). Adults are small (bell-shaped Anomosetidae (Australian primitive ghost
when at rest) and crepuscular or diurnal. Biologies moths) comprise a single genus with one known
and larvae remain unknown, but species in Chile species from Australia. Adults are small. Biologies
are thought to possibly feed on native bamboos. and larvae remain unknown
 Butterflies and Moths (Lepidoptera)
B 655

Prototheoridae (African primitive ghost was found to be monotrysian. Only one family is
moths) comprise 12 species from southern Africa. known. Adults with head roughened; haustellum
Adults are small. Biologies and larvae remain very short (with vestigial mandibles present);
unknown, but a pupa has been found in moss. antennae bipectinate in males; labial palpi elon-
Hepialidae (ghost moths, or swifts) comprise gated; and maxillary palpi 5-segmented (unfolded).
about 594 species from all faunal regions, but most Wing venation is somewhat primitive.
are from Australia, South Africa and Chile. Adults are Andesianidae (Valdiviar forest moths) total
medium size to very large and typically crepuscular only three known species from southern Andean
or nocturnal, but a few are diurnally active. Larvae forest zones of Argentina and Chile. Adults are
feed as borers on roots, trunks or under bark of trees, robust and of medium size, apparently nocturnal
various bushes, or grasses, or even leaf litter. (possibly crepuscular). Biologies are unknown, but
Palaeosetidae (miniature ghost moths) com- larvae are likely to be stem borers.
prise eight species worldwide (five in Assam,
Thailand and Taiwan, two in Australia, and one in
Nepticuloidea
Colombia). Adults are small and crepuscular or
active during the day in dark forested areas, typically
The superfamily Nepticuloidea includes two
near wet moss-covered rock faces. Biologies remain
families of the tiniest leafminer moths known:
unknown but larvae of a species in Taiwan are
Nepticulidae and Opostegidae. Adults with haust-
thought to feed on mosses.
ellum very short; antennae with distinct eye caps;
labial palpi reduced; maxillary palpi 5-segmented
Monotrysian Moths and folded; and head vestiture very rough-scaled.
Wing venation is greatly reduced.
The division Monotrysia, of the infraorder Nepticulidae (pygmy moths) comprise 868
Heteroneura, comprises sections Nepticulina and species from all faunal regions, although most
Incurvariina, and include the first more evolved (over 510 sp.) are from the Palearctic region; actual
moths leading to the main Ditrysian Lepidoptera. world fauna likely exceeds 1,200 species. Two sub-
All have frenular bristles as the wing coupling families are used. Adults are minute and diurnally
mechanism instead of a jugum. The Monotrysia active. Larvae are leafminers, usually blotch mines,
comprise nine families in recent classifications, all although some also mine other plant parts. A large
with a single genital opening in females (Ditrysia variety of hostplants are used.
have two female genital openings). Mandibles are Opostegidae (eye-cap moths) total 122 known
not present in any of the species in this group species from all faunal regions and especially
(except Andesianidae and Palaephatidae), nor in Australia; actual fauna probably exceeds 175 species.
any higher lepidopterans. Nepticulina have four Adults are minute to small and diurnally active. The
families in four superfamilies (Andesianidae, few larvae known are leafminers, but some are stem
Nepticuloidea, Tischerioidea, and Palaephatoidea) borers. Hostplants are in several plant families.
and Incurvariina have five families in the single
superfamily, Incurvarioidea.
Tischerioidea

Andesianoidea The superfamily Tischerioidea includes the single

family Tischeriidae Adults with head vestiture
The superfamily was formed in 2003 for odd rough; haustellum short and scaled; labial palpi
Valdivian moths formerly considered to be Cossi- short; maxillary palpi minute, 1-segmented, and
dae. Their female genital morphology, however, wing venation is very reduced.
656
B Butterflies and Moths (Lepidoptera)

Tischeriidae (trumpet leafminer moths) total arvae are leafminers at first, then switch to leaf
L
81 known species from all regions except Australia, skeletonizing on a variety of hostplants; some are
with most species in the Nearctic (48 sp.); actual case bearers or shoot borers.
fauna likely exceeds 125 species. Adults are small Cecidosidae (gall moths) total only seven
and diurnally active. Larvae are leafminers, usually species, with five species from southern South
trumpet-shaped mines or blotch mines, on a variety America and two from South Africa. Adults are
of hostplants. small and probably diurnal. In Argentina larvae
are gall makers on Schinus (Anacardiaceae).
Prodoxidae (yucca moths) total 65 species,
Palaephatoidea mostly western Nearctic. There are two subfamilies.
Adults are minute to small and diurnal. Larvae are
The monobasic superfamily Palaephatoidea con- seed, flower stalk, or stem borers; rarely gall makers.
tains one family from southern refugia regions of Hostplants are various yucca plants (Agavaceae) and
the world (except South Africa), the Palaephatidae. other species are on hardwood trees and bushes.
Adults with head roughened; haustellum short, Adelidae (longhorned fairy moths) comprise
naked (vestigial mandibles usually present); labial 295 species worldwide, but most are Palearctic (143
palpi short; maxillary palpi 5-segmented and sp.), with two subfamilies; actual fauna probably
folded, and wing venation is heteroneurous. exceeds 400 species. Adults are minute to small;
Palaephatidae (Gondwanaland moths) total antennae extremely long (often 2X wing lengths)
39 described species (28 from Chile and Argentina, in males, but of average length in females (some-
and 11 from Australia), but at least 25 more unde- times thickened). Adults are usually diurnal but a
scribed species are known from Australia alone; few are crepuscular. Larvae are leafminers, but in
actual fauna probably exceeds 90 species. Adults later instars change to casebearers. Hostplants
are small to medium size. Biologies little known include a number of different plant families.
but adults presumed diurnally active. Larvae tie Heliozelidae (shield bearer moths) total 106
hostplant twigs together (on Verbenaceae and species from all regions, with more than half the
Proteaceae). species split between North America (31 sp.) and
Australia (36 sp.); actual fauna probably exceeds
200 species. Adults are minute to small and diurnal.
Incurvarioidea Larvae make serpentine leaf mines at first, then
make blotch mines in later instars. Hostplants
This superfamily is the sole group comprising include a variety of hardwood trees and bushes.
section Incurvariina of the Monotrysia. Included
are a number of odd groups that have been consid-
ered families in the past, but only five families are Ditrysia
now recognized. The superfamily has 589 known
species. All have a scaled haustellum, although This division of the infraorder Heteroneura
mostly reduced; head vestiture is rough-scaled comprises all the remaining Lepidoptera, divided
except for Heliozelidae; some have 5-segmented into the sections Tineina and Cossina. All the
maxillary palpi (Incurvariidae and Prodoxidae, remaining Lepidoptera have heteroneurous wing
plus rarely in Adelidae), while reduced in others. venation (although often with reduced venation in
Incurvariidae (leafcutter moths) total about the tiny leafminers) and a frenulum-retinaculum
116 species from all regions, but most are Palearctic wing coupling (rarely reduced). Typically, they
(64 sp.), divided into two subfamilies. Adults are have 3-segmented labial palpi, generally upcurved,
small and mostly diurnal in shaded habitats. and a haustellum (rarely reduced or absent).
 Butterflies and Moths (Lepidoptera)
B 657

Tineina are used. Adults are small to medium size, with

rather robust bodies and usually large recurved
This section of the Ditrysia involves those groups labial palpi. Adults are mostly nocturnal, but some
with a ventral heart vessel in the adult (consid- may be crepuscular. Larvae are root feeders, mostly
ered more primitive than the dorsal heart vessel of grasses, and construct long underground silken
of the Cossina), and are further divided into the tubes to feed on hostplant roots.
subsections Tineina and Sesiina. Most of the Tineidae (fungus moths) comprise the first
Microlepidoptera families are in this section of very large family of Lepidoptera, with about
the Ditrysia, other than the primitive moths and a 2,160 described species. The actual world fauna
few groups in Cossina often included among the probably exceeds 4,000 species. The family is
micro-moths. The subsection Sesiina have a spined divided into 16 subfamilies. Adults are minute to
pupa, while most of the subsection Tineina have an medium size and nocturnal or crepuscular;
unspined pupa (Gelechioidea, Copromorphoidea, rarely diurnal. Larval habits vary greatly, but
Yponomeutoidea, Immoidea, Pyraloidea, and most are detritus feeders, some making cases,
Pterophoroidea), other than the basal groups that tunnels, or silken tubes; also, odd groups are
form the Tineoidea, which also have a spined pupa. coprophagous, keratophagous,woolen feeders,
(Pterophoridae pupae have scolus-like projections and even myrmecophilous and termitophilous
but not spined as here defined). larvae are known. Included among Tineidae are
some of the most well known household pest
species, such as clothes moths and grain moths.
Tineoidea Eriocottidae (Old World spiny-winged moths)
are a small family of 212 known species, mostly
The superfamily Tineoidea includes the most African (120 sp.) and Oriental (66 sp.), now
primitive of the Ditrysia and also are basal groups divided into two subfamiles. Adults are small to
with ancestors that evolved to the Sesiina groups, medium size and mostly diurnally active, or may
Sesioidea and Zygaenoidea, while also having be crepuscular. Biologies are little known but
begun the development to the other superfamilies some larvae reported to tunnel in the soil, possibly
of the subsection Tineina. Tineoidea are split into feeding on roots or detritus.
two series, Tineiformes (Acrolophidae, Tineidae, Psychidae (bagworm moths) total 1,001
Eriocottidae, Psychidae, and Arrhenophanidae) known species, mostly Palearctic and African, with
and Gracillariiformes (Amphitheridae, Schreck- only 88 known for the New World; actual fauna
ensteiniidae, Douglasiidae, Bucculatricidae, and likely exceeds 1,200 species. The family is now
Gracillariidae), which some specialists consider divided into six subfamilies. Adults are minute to
separate superfamilies. The superfamily total medium size and mostly diurnal or crepuscular.
comes to about 5,730 known species. Adults with Larvae are mostly leaf feeders or feed on lichens,
head vestiture mostly rough-scaled; haustellum all making distinctive types of larval cases, or bags.
naked (unscaled); labial palpi mostly upcurved, Pupation is within the larval case and females
3-segmented (except most Psychidae); maxillary often remain there in a wingless or larviform
palpi mostly small; antennae mostly filiform shape, using pheromones to attract the winged
(mostly bipectinate in Psychidae); wing venation males. A number of species are economic and
reduced in some species (mainly leafminers). many are general plant feeders.
Larvae with three lateral setae on the prothorax. Arrhenophanidae (tropical lattice moths)
Acrolophidae (tube moths) total 270 species in total about 30 species, mostly Neotropical, but
the New World, mostly in the large genus Acrolophus; recently with some Southeast Asian additions;
actual fauna likely exceeds 350 species. Two subfamilies actual fauna probably exceeds 50 species. Adults
658
B Butterflies and Moths (Lepidoptera)

are small to medium size. Adult activity mostly from sap feeders with reduced legs, to later instars
nocturnal, but some are diurnal. Biologies with a 3-proleg pair larval form, which is unique
unknown except for one Neotropical species with among the Microlepidoptera. Later instars some-
case bearing larvae that feed on fungi. times feed externally as leaf skeletonizers. Host-
Amphitheridae (double-eye moths) are an plants include a great number of plant families.
unusual and small family of mostly tropical moths, A few species are of economic importance, such as
totaling 57 species, mostly Indo-Australian (one the citrus leafminer (Phyllocnistis citrella).
genus occurs in Europe and possibly another in
South America). Adults are small, with eyes usually
divided. Adults active diurnally. Larvae are Gelechioidea
leafminers, becoming leaf skeletonizers in later
instars; host records are mostly in Betulaceae and This superfamily comprises a huge group of micro-
Aceraceae. The family has been erroneously called moths, all having a scaled haustellum and unspined
Roeslerstammiidae in recent European literature. pupa. There has been considerable turmoil in
Schreckensteiniidae (bristle-legged moths) recent classifications proposed for the group, either
are a small family of only eight known species with a large family Oecophoridae or with con-
(three in North America, one in Central America, glomeration of various groups into an enlarged
and one in Europe). Adults are small and diurnal. family Elachistidae. In the classification adopted
Larvae are leaf skeletonizers on Anacardiaceae or herein, there are 11 families recognized, the largest
Rosaceae. being Oecophoridae and Gelechiidae. The entire
Douglasiidae (Douglas moths) comprise only superfamily encompasses about 18,230 described
28 known species, mostly Palearctic (20 sp.). Adults species worldwide, but the actual fauna may well
are minute to small and crepuscular or diurnal. exceed 45,000 species, since there are huge
Larvae are leafminers or borers in petioles or numbers of undescribed tropical species. Adults
stems. Hostplants are known in Boraginaceae, mostly with head vestiture mostly relatively
Labiatae, and Rosaceae. smooth-scaled (rarely roughened); haustellum
Bucculatricidae (ribbed-cocoon maker always scaled; labial palpi mostly recurved,
moths) total 247 species worldwide, with most 3-segmented; maxillary palpi vary but mostly
species being Nearctic (103 sp.) or Palearctic (86 small; antennae mostly filiform. Larvae mostly with
sp.); most species are in the genus Bucculatrix. three lateral setae on the prothorax (except two in
Adults are minute to small and mostly diurnal. Momphidae).
Larvae are leafminers, with some changing to Oecophoridae (concealer moths) is a large
external leaf skeletonizing in later instars, but a family of about 7,550 described species from all
few are gall makers or stem miners. Pupation is in faunal regions, with most species being from
a white spindle-shaped cocoon with a ribbed Australia; the actual fauna may well exceed 12,000
surface, unique to the family. Many different host- species worldwide. There are ten subfamilies
plants are known but many feed on Compositae. recognized. Adults are small to medium size and
Some species are economic. mostly nocturnal but some are diurnal or crepus-
Gracillariidae (leafminer moths) comprise the cular. Larvae include many leaf litter feeders, but
major leafmining family of Lepidoptera, with about also leaf tiers, leaf webbers, bark feeders, and a
1,740 species from all regions. The actual world few leafminers. Hostplants include a large number
total probably exceeds 6,000 species. There are of plant families, plus lichens, fungi, and detritus
three subfamilies. Adults are minute to small and or leaf litter. Few are economic.
active diurnally. Larvae are usually leafminers but Lecithoceridae (tropical longhorned moths)
change form in later instars (hypermetamorphism) total about 1,038 described species, mostly tropical
 Butterflies and Moths (Lepidoptera)
B 659

Oriental, but also with one group in the Palearctic; Coleophoridae (casebearer moths) comprise
actual fauna probably exceeds 1,500 species. There about 1,525 species worldwide, with most being
are four subfamilies. Adults are small and mostly Palearctic and in the genus, Coleophora. The actual
diurnal and many have the habit of holding the world fauna likely exceeds 2,000 species. Most are
long antennae together to the front when at rest. in subfamily Coleophorinae, while non casebear-
Larvae may mostly be leaf litter feeders or leaf tiers, ers are in Batrachedrinae. Adults are small and
but few species are known biologically. A few varied may be mostly crepuscular but many are diurnal.
hostplants are recorded. Larvae make small cases (except for Batrachedri-
Elachistidae (grass miner moths) comprise nae), often distinctly shaped for each species, skel-
about 723 species worldwide, but most are Palearctic etonizing host leaves, but some are seed borers,
(472 sp.). Two subfamilies are used (or only tribes). leafminers, or stalk borers, or skeletonize leaves
Adults are small and often crespuscular or noc- beneath frass webs. A few Batrachedrinae are
turnal, but some are diurnal. Larvae are leafminers predaceous on scale insects (Hemiptera). Various
(sometimes gregarious) or stem miners, especially hostplants are utilized. A few species are eco-
on grasses (Gramineae) and related plant groups nomic. Ovovivipary has been recorded for a few
like Juncaceae and Cyperaceae, but other plant species.
families are also utilized. Momphidae (mompha moths) total 127
Pterolonchidae (lance-wing moths) total only species worldwide, with about half from the
11 species, mostly Mediterranean, plus two are Palearctic. Adults are small and mostly diur-
from South Africa. Adults are small and may be nal or crepuscular. Larvae mostly leafminers,
mostly crepuscular. Larvae are root borers as far but some are borers in flowers and stems,
as is known. Only recorded hostplants are in or gall makers. Hosts are only known in
Compositae. Onagraceae.
Gelechiidae (twirler moths) are a very large Agonoxenidae (palm moths) are a small
family, with over 4,830 species described, how- family of 68 known species from all faunal regions.
ever, possibly with a fauna exceeding 10,000 spe- Adults are small and diurnal. Larvae are leaf
cies worldwide. Subfamily arrangements have skeletonizers, or borers in leaves, stems, and fruits;
varied but now include 4. Adults are small and rarely gall-makers. Hostplants mostly in Rosaceae
mostly nocturnal but some are diurnal or crepus- or Palmae. A few are economic.
cular. Larvae have a range of feeding habits but Cosmopterigidae (cosmet moths) total over
most are leaf skeletonizers, using a leaf fold or 1,540 species worldwide, but the extant fauna may
leaf tie as protection. A large variety of plants are encompass 3,500 species. There are three subfami-
used as hosts. Some species are economically lies. Adults are small and mostly diurnal, but some
important. are crepuscular. Larvae mostly leafminers or
Blastobasidae (scavenger moths) total over needleminers, but some are borers of various plant
296 species worldwide, with many known from parts; a few are predaceous on Hemiptera. Hosts
North America and Europe; actual fauna probably are varied. Ovovivipary recorded in a few species.
exceeds 600 species. There are two subfamilies. Some economic species are known.
Adults are small and nocturnal as far as is known. Scythrididae (flower moths) total about 523
Larvae are scavengers or detritus feeders, some- species worldwide, but mostly known from Europe.
times feeding on plant fruits, flowers, or seeds, Adults are small and diurnal but some may be cre-
among a number of plant families, but few are puscular. Larvae are skeletonizers on leaves, buds,
known biologically. At least one species lives with flowers, hiding under webbings. Many plant fami-
coccids (Hemiptera) but predation on the coccids lies are used as hosts, plus some on lichens and
has not been confirmed. mosses.
660
B Butterflies and Moths (Lepidoptera)

Copromorphoidea Tineoidea, while other previously contained groups

are now in other superfamilies. About 1,853 species
This superfamily comprises four families related are known in the superfamily. Adults with head
especially by larval characters. The world fauna totals vestiture mostly relatively smooth-scaled (rough-
623 species. Adults with head vestiture mostly ened in Ochsenheimeriidae, Argyresthiidae and
smooth-scaled; haustellum naked (unscaled); Lyonetiidae); haustellum developed and naked
labial palpi porrect (except for Epermeniidae), (unscaled); labial palpi mostly upcurved; maxillary
3-segmented; maxillary palpi vary; antennae mostly palpi mostly reduced; antennae mostly filiform.
filiform. Larvae with two lateral setae on the Larvae mostly with three lateral setae on the
prothorax. prothorax (two in Glyphipterigidae, and a few
Copromorphidae (tropical fruitworm moths) Plutellidae and Yponomeutidae).
are a small family of 58 species, mostly tropical; Ochsenheimeriidae (cereal stem moths)
actual fauna probably exceeds 100 species. Adults include only 17 species from the Palearctic (one
are small to medium and nocturnal. Larvae are species is from Kashmir), with one species intro-
leaf feeders using a leaf web, or are borers (one duced into North America. Adults are small and
feeds beneath bark), but few biologies are known. diurnal. Larvae are leafminers, but become stem
Hostplants include Berberidaceae, Ericaceae, borers in later instars, primarily on grasses
Moraceae, Podocarpaceae, and Rubiaceae. (Gramineae), sedges (Cyperaceae) and rushes
Alucitidae (many-plumed moths) total about (Juncaceae). One species is economic.
184 species worldwide. Adults are small; wings with Glyphipterigidae (sedge moths) total 431
all veins as separate wing clefts to near the wing species from all regions, mostly in the genus
bases (rarely split only to center of wings). Adults Glyphipterix, with the largest number from the
active in deep shade, or may be crepuscular. Larvae Australian-New Zealand region; actual world
are borers or gall makers as far as is known. Various fauna probably exceeds 600 species. There are two
hostplant records are known. subfamilies. Adults are small and diurnal, usually
Carposinidae (fruitworm moths) total about in proximity to the hostplants. Larvae are mostly
279 species from all regions, but most are borers in seeds, stems, or leaf axils, and a few are
Australian and South Pacific. Adults are small to leafminers, but most tropical species are unknown
medium and nocturnal or crepuscular. Larvae biologically. Hostplants are mostly sedges (Cyper-
are borers in fruits, seeds, buds, or trunks and aceae), rushes (Juncaceae), and grasses (Gramineae),
limbs, but a few are leafminers. Hosts include a plus a few other plant families.
variety of plants. A few species are economic. Plutellidae (diamondback moths) include 386
Epermeniidae (fringe-tufted moths) total 102 species worldwide; actual fauna probably exceeds
species, with many being Palearctic (36 sp.) and 600 species. There are four subfamilies. Adults are
Australian (23 sp.), in two subfamilies. Adults are small to medium size and mostly nocturnal or
small and diurnal or crepuscular. Larvae are leaf- crepuscular, but some are diurnal. Larvae are leaf
miners, leaf skeletonizers, or borers of seeds, fruits, skeletonizers, but most remain unknown biologi-
or buds; a few are gall makers. Host records include cally. Hosts include different plant groups. A few
several plant families. species are economic.
Attevidae (tropical ermine moths) include 48
species, mostly tropical and in the genus Atteva
Yponomeutoidea (the single partially non-tropical species known
occurs across the southern United States and into
This superfamily of varied moths includes nine the Caribbean and Mexico); actual fauna probably
families, some of which have been transferred from at least 60 species. Adults are small to medium
 Butterflies and Moths (Lepidoptera)
B 661

size and are diurnal or crepuscular. Larvae are leaf ancestors. Adults with head vestiture relatively
webbers and leaf skeletonizers on Araliaceae and smooth-scaled; haustellum naked; labial palpi
Simaroubaceae. Minor economic species occur upcurved and often prominent, with long second
on Ailanthus trees in India and the United States. segment; maxillary palpi minute, 1 to 2-segmented;
Yponomeutidae (ermine moths) total 395 antennae mostly filiform; body robust. Larvae with
species worldwide; actual fauna likely exceeds 500 three lateral setae on the prothorax.
species. Three subfamilies are recognized. Adults Immidae (imma moths) comprise 246 species,
are small to medium size and mostly nocturnal. all tropical, and mostly Indo-Australian and South
Larvae are leaf skeletonizers and leaf webbers, but Pacific; actual fauna likely exceeds 450 species.
some are leafminers or needleminers. Hosts Adults are small to medium size and diurnal,
include many different plant families. A few species but some may be crepuscular. Larvae are leaf
are economic. feeders, but only three species have biological data.
Argyresthiidae (shiny head-standing moths) Hostplants are in Myrtaceae, Podocarpaceae, and
include 160 species, mostly from Holarctic region; Violaceae.
actual fauna probably exceeds 450 species. Adults are
small and mostly crepuscular, but many may be diur-
nal. Larvae are leafminers and needleminers, and Pyraloidea
some mine in various plant parts. Numerous plants
are recorded as hosts. Several species are economic. This superfamily includes three families but mainly
Lyonetiidae (Lyonet moths) total 264 species, the very large family, Pyralidae. The superfamily
mostly Holarctic; the actual fauna probably comprises about 17,312 species worldwide. Recent
exceeds 600 species. There are three subfamilies. specialists have taken to splitting Pyralidae into its
Adults are minute to small and mostly crepuscular two major lineages, as the separate families Cram-
and nocturnal. Larvae are blotch leafminers; rarely bidae and Pyralidae, but this reversion to what was
mining stems. Many plant groups are recorded as done over 100 years ago is unnecessary and amply
hosts. A few species are economic. clarified by using the group category below the
Acrolepiidae (false diamondback moths) family level within a single family Pyralidae. Some
include 96 species, mostly Palearctic. Adults are specialists do even more splitting by placing each
small and crepuscular or diurnal. Larvae mostly pyraloid family in its own monobasic superfamily
leafminers, but some are borers in seeds, stems and (Hyblaeoidea, Thyridoidea, and Pyraloidea).
flower buds. Several hostplant groups are used, but Adults with head vestiture mostly smooth-scaled;
mostly on Compositae. Very few are economic. haustellum mostly scaled (not Hyblaeidae and
Heliodinidae (sun moths) are a small family Thyrididae); labial palpi mostly porrect, 3-seg-
of 56 species, mostly Neotropical (31 sp.); actual mented; maxillary palpi varied; antennae mostly
fauna probably exceeds 100 species. Adults are filiform. Larvae have two lateral setae on the
small and diurnal. Larvae are mostly leaf skeleton- prothorax.
izers, but some are borers in fruit racemes. Several Hyblaeidae (teak moths) are a small tropical
plant families are used as hosts. family of 18 species, mostly Indo-Australian and
in the genus Hyblaea (one pantropical species
is also established in southern Florida). Adults are
Immoidea medium size; body usually robust. Adults are diur-
nal or perhaps crepuscular. Larvae are leaf rollers.
This is a monobasic superfamily for the single Hostplants are in Bignoniaceae and Verbenaceae.
small family Immidae. It is somewhat related to One economic species: the teak leafroller (Hyblaca
Pyraloidea and may represent relatives of common puera).
662
B Butterflies and Moths (Lepidoptera)

Thyrididae (picture-winged leaf moths) total Oxychirotidae (tropical plume moths) include
794 species worldwide, nearly all tropical, with only six species, all Indo-Australian and South
nearly half the species Indo Australian (only a few Pacific. Some specialists include this family as part
species are in the Nearctic and Palearctic regions); of the Tineodidae. Adults are small and may be
actual fauna likely exceeds 1,200 species. There are crepuscular. Larva of one species feeds on seeds of
six subfamilies. Adults are small to large and white mangrove (Avicenniaceae); remainder
diurnal or crepuscular. Larvae are leafrollers (one unknown biologically.
Australian species is gregarious), or borers in Pterophoridae (plume moths) comprise about
stems and flower racemes; a few are gall makers. 1,292 species worldwide, with about a third being
A number of hostplants are used. Only a few Palearctic; actual world fauna probably exceeds
species are economic. 1,800 species. Subfamilies number five. Adults are
Pyralidae (snout moths) comprise the third small, usually with hindwings split into three
largest family of Lepidoptera, with about 16,500 fringed plumes; forewings often entire or split into
described species, but a probable fauna of at least two parts near the termen (a few species have both
25,000 species worldwide; 19 subfamilies are used wings entire). Adults mostly nocturnal but some
in the classification. Adults are small to large and crepuscular or in shaded areas during the day. Lar-
mostly nocturnal, but some are crepuscular and a vae mostly leaf feeders, or miners and borers of
few are diurnal. Larvae are mostly leafrollers or leaf various plant parts; a few are gall makers. Host-
webbers, but many are borers, root feeders, detritus plants include many families. Several species are
feeders (including stored products pests), and a economic.
few are leafminers, plus rare myrmecophilous
species, and even some aquatic groups making
cases (Nymphulinae). A large number of economic Sesiina
species are in this family, including pests on
virtually all crops and forest trees. Hostplants are in The subsection Sesiina of the Tineina include two
a large number of plant families. superfamilies: Sesioidea and Zygaenoidea.

Pterophoroidea
Sesioidea
This superfamily includes only three families,
but most species are in the Pterophoridae. About The Sesioidea include four families, although many
1,309 species are known for the superfamily. specialists maintain separate superfamilies for most
Adults with head vestiture average (rather of them: Brachodidae, Sesiidae, Urodidae, and
smooth scaled); haustellum naked (unscaled); Choreutidae. Brachodidae are thought to be the
labial palpi porrect; maxillary palpi mostly short; basal group, with close ties to Sesiidae. The world
antennae filiform. Larvae have three lateral setae fauna totals 1,963 known species in the superfamily.
on the prothorax in Pterophoridae, but only two Adults mostly with head vestiture mostly smooth-
lateral setae in Tineodidae (not known for scaled (rough in most Brachodidae); haustellum
Oxychirotidae). mostly naked (scaled in Choreutidae); labial palpi
Tineodidae (false plume moths) include only mostly upcurved; maxillary palpi mostly small;
11 species, all from Australia. Adults are small and antennae vary but many with thickened antennae
possibly diurnal or crepuscular. Larvae are leaftiers, (Sesiidae). Larvae mostly with three lateral setae on
but most are not known biologically. Only recorded the prothorax, but most Brachodidae and a few
hostplants are in Euphorbiaceae and Oleaceae. Choreutidae with only two lateral setae.
 Butterflies and Moths (Lepidoptera)
B 663

Brachodidae (little bear moths) comprise but some are budworms; rarely leafminers (Mil-
140 species, most being Old World tropical, lieriinae). Numerous hostplant families are
particularly Indo-Australian (none are North recorded, but many in Compositae and Moraceae.
American). There are three subfamilies. Adults
are small to medium size and diurnal. Larvae are
root feeders of grasses (in the European Brachodes,
Brachodinae), using silken tubes, or borers in Zygaenoidea
palm trunks and leaf stems, or other plants; some
are leaftiers (Phycodinae). Hostplants are in This superfamily contains the burnet moth and
Gramineae, and also Bromeliaceae, Melistomaceae, flannel moth groups, with six families involved (in
Moraceae, and Palmae. A few are economic on Europe also called forester moths, which name is
palms. used for one of the Noctuidae subfamilies in North
Sesiidae (clearwing moths) include about America). Some very colorful species are included,
1,325 species from all regions; the actual number especially some of the larger Zygaenidae which in
probably exceeds 1,800 species. Subfamilies are the Oriental region are as large as some butterflies.
three. Adults are small to medium size; antennae The superfamily has 1,609 known species from
usually thickened and with a slight distal club all regions. Adults with head vestiture usually
(most also with unique small terminal bristles on average but often rough-scaled; haustellum naked
antennae). Wings very elongated and with unique (unscaled), but sometimes absent or vestigial; labial
wing-locking folding where the margins meet. palpi mostly upcurved; maxillary palpi mostly
Adults are diurnal, particularly during morning small or reduced; and antennae mostly bipectinate
hours. Many species mimic various wasps (sometimes clubbed). Larvae all have three lateral
(Hymenoptera). Larvae mostly borers on various setae on the prothorax and most are slug-like.
plant parts, and a few are gall makers; two species Heterogynidae (Mediterranean burnet moths)
are predaceous on scale insects (Hemiptera). Host include only seven species, with three species
specificity is high for most species, but overall many from the Mediterranean region of southern
plant families are used as hosts. A number of species Europe and northern Africa and four species from
are economic, including some major pests of fruit South Africa. Adults are small and diurnal, but
trees, forest trees, and grape vines. females are apterous and larviform. Larvae, upon
Urodidae (false burnet moths) total only about hatching inside the female cocoon, feed first on
80 species, primarily Neotropical, but with a few the dead female and then become external leaf
species in North America and in Eurasia. Adults are feeders. Hostplants are in Leguminosae.
small and may be crepuscular or mostly nocturnal, Zygaenidae (burnet moths) comprise about
but a few possibly diurnal. Larvae are leaf webbers 1,140 species worldwide, particularly well devel-
or skeletonizers, but few are known biologically. oped in tropical Asia (450 sp.) where also the
Pupation is in a specialized filigreed cocoon. largest species occur; actual world fauna likely
Hostplants known in Lauraceae, Leguminosae, exceeds 1,500 species. There are seven subfamilies.
Salicaceae, Sapotaceae, and Theaceae. A few are Adults are small to large, with antennae sometimes
minor pests. clubbed. Adults are diurnal, often flying like
Choreutidae (metalmark moths) comprise418 butterflies, or commonly on flowers. Larvae are
species worldwide; actual world fauna probably leaf skeletonizers, sometimes feeding communally
exceeds 800 species. There are three subfamilies. and usually at night; often slug-like, with concealed
Adults are small, with haustellum scaled. Adults are head. Hostplants include various plant families.
diurnal; usually near their hostplants and tend to hop Economic species are mostly pests on grapevines
about on leaves. Larvae mostly leaf skeletonizers, in North America and Europe.
664
B Butterflies and Moths (Lepidoptera)

Himantopteridae (long-tailed burnet moths) the pupae have dorsal spines (tribe Ceracini of
include 56 species from Africa and tropical Asia. Tortricidae are an exception). All the larger moths
Adults are small to medium size; hindwings with and butterflies are in subsection Bombycina, where
extremely long tails. Adults are diurnal but few are the pupae are unspined. Subsection Cossina has
known biologically. Larvae are leaf skeletonizers, three superfamilies: Cossoidae, Castnioidea, and
often communal; sometimes massing in the 1000s. Tortricoidea. Subsection Bombycina has eight
Known hostplants are in Dipterocarpaceae. superfamilies: Calliduloidea, Uranioidea, Geome-
Lacturidae (tropical burnet moths) total 138 troidea, Papilionoidea (including Hesperioidea),
species, mostly Indo-Australian but with a few in Drepanoidea, Bombycoidea, Sphingoidea, and
the southern United States; actual world fauna Noctuoidea. All have the haustellum naked
probably exceeds 250 species. Adults are small to (unscaled), when present.
medium size and nocturnal, but some may be
crepuscular. Larvae are leaf skeletonizers and are
colorful, but most are not known biologically. Cossoidea
Hostplants are in families Celastraceae, Moraceae,
and Sapotaceae. This superfamily includes large micro -moths,
Somabrachyidae (Mediterranean flannel such as in the carpenterworm moths (Cossidae),
moths) include only five species, with three species plus the slug caterpillar moth groups. There are two
from southern Europe and north Africa, plus two series used to divide the superfamily: Cossiformes,
species from South Africa. Adults are small. Adults for the more primitive carpenterworm families
are diurnal, but females are larviform and wingless (Cossidae, Dudgeoneidae, Metarbelidae, Cyclo-
(females of the South African species are tornidae, and Epipyropidae), and Limacodiformes,
unknown). Larvae are leaf feeders (eggs laid on for the slug caterpillar families (Dalceridae, Limaco-
leaves, not in the female cocoon), somewhat didae, and Chrysopolomidae). About 2,054 species
slug-like, with concealed head. Hosts are grasses are known in the superfamily. Adults with head
(Gramineae) and Compositae. vestiture mostly rough-scaled; haustellum naked (or
Megalopygidae (flannel moths) are a New vestigial); labial palpi upcurved or short; maxillary
World family of 263 species, mostly Neotropical; palpi mostly reduced or absent; antennae mostly
actual fauna likely exceeds 350 species. Adults are bipectinate; body mostly robust. Larvae have three
small to large and nocturnal. Larvae are leaf feeders, lateral setae on the prothorax.
usually communal in early instars; slug-like, with Cossidae (carpenterworm moths) total 682
concealed head; with poison spines usually beneath species worldwide; actual fauna probably exceeds
long hair-like setae. A large number of hostplants 750 species. There are five subfamilies. Adults are
are recorded, and some species are polyphagous. A small to very large and nocturnal. Larvae are
few are economic on forest trees and palms, but borers in trunks and limbs. Hostplants are recorded
most are of medical importance due to urticating in a large number of plant families. A number of
setae in adults and the poison spines in larvae. species are economic pests of forest trees.
Dudgeoneidae (Dudgeon carpenterworm
moths) include only six species in the single genus
Cossina Dudgeonea, with two species from Africa, one
from India, and three from Australia. Adults are
This is the second division of the Ditrysia (with a medium size; abdomen with small tympanal
dorsal heart vessel) and includes all the macro- organs. Adults nocturnal as far as is known. Larvae
moths and butterflies, plus a few more of the mostly unknown, but one Australian species is a
Microlepidoptera in subsection Cossina, where stem borer on Rubiaceae.
 Butterflies and Moths (Lepidoptera)
B 665

Metarbelidae (tropical carpenterworm moths) orsally. Large numbers of hostplants utilized. Few
d
include 103 species, mainly Afrotropical and species are economic other than medically as
Oriental, with one species in the Palearctic region; stinging caterpillars, but palm defoliators can be a
actual world fauna likely exceeds 150 species. problem in the tropics.
Adults are small to medium size and may be Chrysopolomidae (African slug caterpillar
crepuscular. Larvae nocturnal borers on tree bark moths) are a small African family of about 30
or in tree trunks, but most species remain unknown known species. Two subfamilies are known. Adults
biologically. Hostplants include various trees. A few are medium size and nocturnal. Larvae leaf-feeding
have minor economic status. and slug-like, with small spines; often colorful.
Cyclotornidae (Australian parasite moths) Hostplants include Celastraceae. No economic
include only five known species from Australia, species are known.
the most primitive of the Limacodiformes group
of Cossoidea. Adults are small. Adult activity
uncertain but may be crepuscular. Larvae flattened, Castnioidea
with lateral protrusions; highly evolved as parasites
of leafhoppers, scale insects, or psyllids (Hemiptera) This superfamily contains only the single family
in early instars, and then as predators of ant larvae. Castniidae. Often in the past thought of as the
Epipyropidae (planthopper parasite moths) progenitor lineage to butterflies, they are now con-
total 40 described species, with at least another 30 sidered only an offshoot of cossoid like ancestors,
known species awaiting naming; most diversity is while butterflies are evolved from geometroid-like
in Australia. Two subfamilies are known. Adults ancestors that also developed into Hedylidae.
are minute to small and crepuscular or nocturnal; Adults with head vestiture smooth-scaled and eyes
females are sedentary. Larvae slug-like with large; haustellum naked (rarely vestigial); labial
rounded dorsum; parasitic on fulgorids and palpi often with distal segment erect; maxillary
planthoppers (Hemiptera). palpi 2 to 4-segmented; antennae clubbed. Body
Dalceridae (tropical slug caterpillar moths) robust. Larvae with two or three lateral setae on
include 84 Neotropical species (one sp. intrudes the prothorax.
from Mexico into southern Arizona). Two sub- Castniidae (giant butterfly moths) total 170
families are known. Adults are small to medium known species, mostly Neotropical but with
size. Adult activity uncertain; possibly only noc- some species also in the Indo-Australian region;
turnal or crepuscular. Larvae slug-like, often with likely world total may exceed 180 species. Three
translucent gelatinous wart-like surface; feeding subfamlies are known. Adults are medium to
as leaf feeders (early instars as leaf skeletonizers), large size and diurnal or crepuscular. Larvae are
but few are known biologically. Various hostplants borers of monocot plants, including grasses
are used and some larvae are polyphagous. Few (Gramineae), Cyperaceae, Bromeliaceae, Maran-
have any economic status. taceae, Musaceae, and Palmae, among others.
Limacodidae (slug caterpillar moths) total A few are economic on banana plants, various
1,104 known species worldwide, the largest family palms, and sugarcane.
of Cossoidea, mostly tropical and especially bio
diverse in the Oriental tropics; likely world total is
near 1,600 species or more. Adults are small to Tortricoidea
medium size. Adults perhaps only nocturnal; many
with unique resting postures. Larvae slug-like and Another monobasic superfamily exclusively for
mostly polyphagous leaf feeders, usually with an the family Tortricidae. In the past, the tortricid
extensive array of poisonous stinging spines subfamilies were often considered separate
666
B Butterflies and Moths (Lepidoptera)

f amilies, such as Olethreutidae and Chlidanotidae, rounded or quadratic, or more acute; hindwings
and even groups like Ceracidae and Cocylidae more rounded. Immature stages remain little
which now are only tribes (Ceracini are odd for known; larvae with two lateral setae on prothorax
Tortricoidea also due to their unspined pupae). in Callidulidae.
Adults with head vestiture mostly roughened; Ratardidae (Oriental parnassian moths) are
haustellum naked (unscaled); labial palpi mostly butterfly-like moths of the Himalayas and Oriental
porrect; maxillary palpi usually 4-segmented; tropics, with ten described species, plus a few more
antennae filiform; and body usually relatively still undescribed. Adults are medium sized, but
stout. Larvae have three lateral setae on the males often much smaller than females. Adults are
prothorax. diurnal. Larvae are bark feeders, but biologies and
Tortricidae (leafroller moths) are a large larvae are mostly unknown.
family of 8,945 described species from all faunal Pterothysanidae (parnassian moths) include
regions; the actual fauna likely will exceed 12,000 19 species, from southern Africa (seven sp.) and
species. Three subfamilies are known. Adults are Southeast Asia (12 sp.). There are two subfamilies.
small (rarely medium sized) and mostly nocturnal Adults are medium size and diurnal, possibly also
or crepuscular, but some are diurnal. Larvae crepuscular. Biologies and larvae remain unknown.
mostly leafrollers, but some are borers in various Callidulidae (Old World butterfly moths)
plant parts, including stems, branches, flowers, include 102 species, mostly tropical Oriental, in
and seeds; a rare few are leaf litter feeders. Most two subfamilies. Adults are medium size and
species are restricted to certain hostplants among diurnal, flying like some butterflies in quick
innumerable plant families. Many species are bursts to alternate leaf perches; resting position
economic. with wings held together and upright. Larvae
largely unknown, except for two species which
are leafrollers of ferns.
Bombycina

Remaining larger moths and the butterflies are in Uranioidea

this subsection of the Cossina, including eight
superfamilies. This superfamily encompasses both very large
and small moths among five families, mostly
Old World: Epicopeiidae, Apoprogonidae, Sema-
Calliduloidea turidae, Uraniidae, and Epiplemidae. Some of
these families continue to be mixed up with
This superfamily includes three families of ancient Drepanoidea and Geometroidea, or have been
lineage with many primitive features: Ratardidae, combined into Epiplemidae. About 814 species
Pterothysanidae, and Callidulidae. All are Old are known in the superfamily. Adults with head
World and total 131 known species for the vestiture mostly roughened (more average in
superfamily. Ratardidae are sometimes placed in Epiplemidae); haustellum naked; labial palpi
Cossidae by some specialists, but represent a basal mostly upcurved or short; maxillary palpi
relict from cossoid ancestors similar to Metarbelidae, minute and one segmented; antennae filiform,
however on the lineage to Callidulidae. Adults but also bipectinate and clubbed or thickened in
with head vestiture average (rough in Ratardidae); some species; forewings quadratic to triangular
haustellum naked (absent in Ratardidae); labial and somewhat pointed apically; hindwings
palpi usually porrect; maxillary palpi vestigial; usually rounded (some tailed). Larvae with two
antennae filiform or bipectinate; forewings broadly lateral setae on the prothorax, as far as is known.
 Butterflies and Moths (Lepidoptera)
B 667

Epicopeiidae (Oriental swallowtail moths) superfamily total comes to 21,190 known species.
are a small family with 25 species known in two Adults with head vestiture normal; haustellum
subfamilies, mostly Himalayan and East Asian. naked; labial palpi upcurved; maxillary palpi
Adults are medium to large and diurnal. Larvae small; antennae mostly filiform (rarely bipecti-
little known, but leaf feeders with waxy secre- nate); forewings triangular, usually with somewhat
tions over body. Hostplants are in Clethraceae, pointed forewings (sometimes rounded), but
Cornaceae, Ericaceae, Theaceae, and Ulmaceae. sometimes emarginate or with falcate apex; hind-
Apoprogonidae (African skipper moths) wings more rounded in most species (rarely
include only a single species from South Africa. tailed); and body mostly slender and abdomen
Adults are medium size; antennae clubbed (hooked with tympanal organs. Larvae with two lateral
at tip); body robust. Adults presumed diurnal, but setae on the prothorax, and most larvae have a
nothing is known of the biology or larvae. reduced proleg number.
Sematuridae (American swallowtail moths) Geometridae (geometer moths), also called
total 36 Neotropical species, one of which just inch worms, are the second largest family of
reaches into the United States, in southern Arizona. Lepidoptera, with about 21,150 described species
Adults are medium to large; antennae thickened, from all faunal regions; the actual fauna probably
with elongated club (slightly hooked at tip). Adults exceeds 26,500 species. The major biodiversity is
nocturnal but some may be crepuscular. Larvae in the Neotropics, with over 6,500 species
are leaf feeders, but few known biologically. described, and the Indo-Australian region with
Hostplants are unrecorded. about 6,670 species. The family is divided into
Uraniidae (swallowtail moths) comprise eight subfamilies. Adults are small to large; a
about 120 species from all tropical regions, mostly number of genera have brachypterous or apterous
Indo-Australian (85 sp.); one species strays into females. Adults mostly nocturnal, but also some
the United States-Mexican border region (mainly crepuscular and diurnal groups. Larvae mostly
in Texas). Two subfamilies are used. Adults are leaf feeders, typically moving in looping fashion
medium to large and nocturnal or diurnal, with due to reductions in proleg numbers. Hostplants
some of the larger diurnal species known to include most all plant families. Some major
migrate. Larvae are leaf feeders. Hostplants are defoliating pests are known in this family.
known in Asclepiadaceae, Myrtaceae, and Hedylidae (American butterfly moths) total
Euphorbiaceae. only 40 known species, all Neotropical. Adults
Epiplemidae (crenulate moths) total about 632 are medium size and nocturnal. Larvae are leaf
species worldwide, with most being Neotropical feeders. Hostplants are recorded in Euphorbiaceae,
(230 sp.) and Indo-Australian (301 sp.). Two Malvaceae, Streculiaceae, and Tiliaceae.
subfamilies are used. Adults are small to medium
size and nocturnal. Larvae are leaf feeders or
webbers. Hostplants are in several plant families. Papilionoidea

The butterflies, also called Rhopalocera, include

Geometroidea seven families, including the skippers, family
Hesperiidae. Skippers are sometimes placed in
One of the largest superfamilies of Lepidoptera, their own monobasic superfamily, Hesperioidea,
mainly with the large family Geometridae, but but the differences can also be noted by using
also including the odd Hedylidae (some special- series Hesperiiformes and Papilioniformes. True
ists place the latter family near the true butter- butterflies include families Papilionidae, Pieri-
flies, in its own superfamily, Hedyloidea). The dae, Lycaenidae, Riodinidae, Libytheidae, and
668
B Butterflies and Moths (Lepidoptera)

Nymphalidae. In the past, many of the subfami- Pieridae (yellow-white butterflies) total about
lies, especially in Nymphalidae, have been con- 1,275 species worldwide, most being Indo-Australian
sidered separate families, and the entire (ca. 515 sp.). Four subfamilies are recognized.
superfamily has on occasion been split into sev- Adults are small to large and diurnal. Larvae are
eral superfamilies, such as Lycaenoidea and leaf feeding. Various plants are utilized. Some
Nymphaloidea. Some specialists still include economic species are known, particularly on
Riodinidae within Lycaenidae, and Libytheidae cabbages amd other crucifers.
within Nymphalidae, and controversies about Lycaenidae (gossamer-winged butterflies)
this continue. Extant butterflies number about total about 5,955 species worldwide; the actual
20,400 described species, but the actual butterfly fauna probably exceeds 7,000 species. About 1,125
fauna probably is about 23,500 species world- species are Neotropical. The family has eight
wide, due to the numerous still unnamed small subfamilies. Adults are small to medium size and
skippers (Hesperiidae) and blues (Lycaenidae). diurnal, but a few of the relict genera possibly
Butterflies have 3-segmented, mostly upcurved crepuscular or only in dark forests. Larvae mostly
labial palpi (only long and porrect in Libythei- somewhat slug-like, with tubercles and short setae;
dae), small or vestigial maxillary palpi (1-seg- head usually retractable into thorax. Larvae feed
mented), head scaling relatively smooth in most as leaf feeders (some on other plant parts), but
groups, and a naked haustellum; antennae with many are myrmecophilous and some even are
clubs (hooked at tip in Hesperiidae); forewings carnivorous on ant larvae or hemipterans.
mostly triangular, while hindwings are usually Hostplants are in a wide variety of plant families,
more rounded (sometimes with tails). Wing cou- but particularly Fagaceae and Leguminosae. A few
pling via a humeral lobe rather than the frenu- economic species are known.
lum-retinaculum arrangement of most moths. Riodinidae (metalmark butterflies) total
Larvae with two lateral setae on the prothorax. about 1,419 species worldwide but predominate in
Hesperiidae (skipper butterflies) include the Neotropics (1,322 sp.); the actual world fauna
about 4,100 species from all faunal regions; most probably exceeds 2,500 species. Five subfamilies
are Neotropical, with over 2,338 species. The actual are recognized. Adults are small to medium size
world fauna probably exceeds 4,500 species. Seven and diurnal; often with rapid flight. Larvae are leaf
skipper subfamilies are recognized. Adults are feeders, but many are myrmecophilous; one is
small to medium size and diurnal, usually with known to be carnivorous on hemipterans. Larvae
very rapid flight, but a few tropical species are mostly slug-like with short setae. Hostplants are
crepuscular. Larvae are leafrollers or borers. recorded in numerous plant families.
Hostplants are primarily grasses (Gramineae) and Libytheidae (snout butterflies) are a small
other monocots. A few economic species are family of only 12 species, with at least one species
known, particularly on rice. in each faunal region. Adults are medium size and
Papilionidae (swallowtail butterflies) total diurnal. Larvae are leaf feeders. Hostplants are in
about 589 species worldwide, with about 260 Ulmaceae.
species being Indo-Australian, including the Nymphalidae (brush-footed butterflies) are
largest of all butterflies, the birdwings. Three the largest family of butterflies, with about 7,080
subfamilies are recognized. Adults are medium described species worldwide; the actual fauna
size to very large and diurnal. Larvae are leaf probably exceeds 8,000 species. To represent the
feeders; with an osmeterium defensive gland division of relict basal groups within the family,
behind head. Hostplants include many plant the subfamilies are divided into two groups:
groups. Some economic species are known, Nymphalinina, with six subfamilies, and Satyr-
mainly citrus feeders inina, also with six subfamilies. Adults are medium
 Butterflies and Moths (Lepidoptera)
B 669

to large and diurnal, although crepuscular activity medium to large size and nocturnal. Larvae are
is known in a few cases (some Amathusiinae and leaf feeders. Hostplants recorded so far only in
Brassolinae). Larvae are mostly leaf feeders; a few Alangiaceae
feeding gregariously. Hostplant records are among Drepanidae (hooktip moths) comprise 812
almost all higher plants. species worldwide, but predominately Oriental
(647 sp.); none are known for the Neotropics and
only a few are in the Nearctic; the actual fauna
Drepanoidea probably exceeds 950 species. Three subfamilies
are known. Adults are small to medium size and
This superfamily includes four families perhaps nocturnal. Larvae are leaf feeders. Hostplants
most related to Geometroidea. The branching and include a variety of plants. A few are economic.
reticulate nature of evolution places the butterflies
first after Geometroidea and before Drepanoidea
when listed on paper, representing a more evolved Bombycoidea
side branch. Some recent classifications have greatly
disorganized this superfamily, placing Axiidae in its This superfamily includes many of the largest moths
own monobasic superfamily (Axioidea) and merg- and encompasses 13 families and about 4,810 known
ing Cyclidiidae and Thyatiridae into Drepanidae as species. The superfamily is divided into two groups:
subfamilies: the latter three families all have some series Bombyciformes (Carthaeidae, Eupterotidae,
cohesive features (e.g., abdominal tympanal organs) Apatelodidae, Bombycidae, Mimallonidae, Antheli-
but also many unique features that provide evidence dae, and Lasiocampidae) and series Saturniiformes
of family status. The superfamily comprises about (Endromidae, Lemoniidae, Brahmaeidae, Oxytenidae,
1,056 known species. Adults with head scaling Cercophanidae, and Saturniidae). Some specialists
normal; haustellum normal (small or absent in use the series names for two superfamilies, or even
some Drepanidae); labial palpi mostly upcurved; other superfamilies are added (such as Mimal-
maxillary palpi mostly vestigial; antennae varied lonoidea), and there also is some confusion as to
but mostly serrate of filiform; body generally robust; how many families are involved (e.g., Oxytenidae
forewings mostly triangular or somewhat elongated; and Cercophanidae are sometimes included among
and hindwings rounded. Larvae with two lateral Saturniidae by some researchers). Adults with head
setae on the prothorax. scaling often roughened; haustellum mostly absent;
Axiidae (gold moths) are a very small family labial palpi mostly upcurved but sometimes reduced;
of only six Palearctic species in the Mediterranean maxillary palpi mostly vestigial or absent; antennae
region. Adults are medium size and nocturnal. mostly bipectinate (also quadripectinate in Saturnii-
Larvae are leaf feeders. Hostplants are in dae); body generally robust and often with hair-like
Euphorbiaceae. setae; forewings mostly triangular and hindwings
Thyatiridae (false owlet moths) comprise 224 rounded (some with long tails). Larvae with two lat-
species from all regions except Australia, but most eral setae on the prothorax.
are tropical Oriental (199 sp.); the actual fauna Carthaeidae (Australian silkworm moths) are
probably exceeds 275 species. Two subfamilies are a monobasic relict family in Bombycoidea with a
recognized. Adults are medium size and noctur- single species from western Australia. Adults are
nal. Larvae are mostly nocturnal leaf feeders. Host- large and nocturnal (usually flying after midnight).
plants are recorded in a number of plant groups. Larvae are leaf feeders, with numerous clubbed
Cyclidiidae (giant hooktip moths) are a small setae. Hostplants are only in Proteaceae.
family of 14 described species, all Oriental plus Eupterotidae (giant lappet moths) total 325
one species in the southern Palearctic. Adults are species worldwide (except the Nearctic), but most
670
B Butterflies and Moths (Lepidoptera)

are Oriental (238 sp.); only four species are octurnal. Larvae are leaf feeders. Hostplants
n
recorded in the Neotropics. Three subfamilies are recorded in Betulaceae, Caprifoliaceae, Salicaceae,
known. Adults are small to large and nocturnal. Tiliaceae, and Ulmaceae.
Larvae are leaf feeders. Hostplants among numer- Lemoniidae (autumn silkworm moths) total
ous different plants. Few species are economic 21 species, mostly Mediterranean. There are two
(e.g., rice or forest pests). subfamilies. Adults are medium size and noctur-
Apatelodidae (American silkworm moths) nal, but some males are diurnal; flight periods are
are exclusively New World, and total 252 species, often in the autumn in Europe. Larvae are leaf
mostly Neotropical (247 sp.). Three subfamilies feeders. Hostplants are mostly in Compositae and
are used. Adults are small to medium size and noc- Euphorbiaceae.
turnal. Larvae are leaf feeders. Hostplants are in Brahmaeidae (brahmin moths) are a small
various plant families. family of 28 species, mostly Palearctic and African.
Bombycidae (silkworm moths) total 166 There are two subfamilies. Adults are medium size
described species, all Old World and primarily to very large and nocturnal. Larvae are leaf feed-
Oriental (146 sp.), with only five species known for ers. Hostplants recorded in Asclepiadaceae and
Africa. Two subfamilies are involved. Adults are Oleaceae
medium size and nocturnal. Larvae are leaf feeders. Oxytenidae (American tropical silkworm
Hostplants predominate in Moraceae. The silk- moths) include 60 species, all Neotropical. Adults
worm (Bombyx mori) is used for silk production. are medium size to large and nocturnal. Larvae are
Mimallonidae (sackbearer moths) total 254 leaf feeders; some mimic snakes. Hostplants
species, all New World and primarily Neotropical recorded in Rubiaceae.
(250 sp.). Adults are medium size and nocturnal. Cercophanidae (Andean moon moths)
Larvae are leaf feeders, with larval cases. Host- include 30 species of mostly austral South Ameri-
plants are recorded in a number of plant families. can moths. There are two subfamilies Adults are
A few can be economic. medium size to large and nocturnal. Larvae are
Anthelidae (Australian lappet moths) total leaf feeders. Hostplants recorded in Celastraceae,
100 species, all from Australia. There are two sub- Lauraceae, Saxifragaceae, and Tiliaceae.
families. Adults are medium size to large; rarely Saturniidae (emperor moths) include 1,435
with micropterous females. Adults nocturnal, but species worldwide, but are predominately Neotro-
at least one species with diurnal males. Larvae are pical (860 sp.). There are seven subfamilies. Adults
leaf feeders and generally colorful. Host plants are medium size to very large and mostly noctur-
recorded in several plant families. Some species nal or crepuscular, but some are diurnal. Larvae
have urticating larval setae. are leaf feeders and many are polyphagous, some
Lasiocampidae (lappet moths) include 2,130 being communal or gregarious; many are extremely
species worldwide, with many in Africa (790 sp.). large. Hostplants are extremely varied. Some spe-
Subfamilies are five. Adults are small to large; some cies are economic for agriculture, but major
with micropterous females. Adults mostly noctur- urticating larvae are involved in dermatitis and
nal but some males are diurnal. Larvae are leaf more severe allergic reactions, and in a few cases
feeders, sometimes communally in silken tent-like even from adult scales.
webbings. Hostplants are various. Some species
are economic as tree defoliators.
Endromidae (glory moths) are a monobasic Sphingoidea
family of four species, from Europe to Central
Asia. There are two subfamilies. Adults are medium This is a monobasic superfamily for the hawk
size. Adult males are diurnal but females are moth family, Sphingidae. Some specialists include
 Butterflies and Moths (Lepidoptera)
B 671

the family in Bombycoidea. Adults with head scal- family Arctiidae). Larvae with two lateral setae on
ing mostly normal (sometimes roughened); haus- the prothorax.
tellum often very long; labial palpi mostly Notodontidae (prominent moths) total 3,562
upcurved; maxillary palpi mostly small; antennae species from all faunal regions, particularly from the
mostly clavate or lamellate and thickened; body Neotropics (1,766 sp.); actual world fauna likely
robust; forewings mostly elongate-triangular and exceeds 4,000 species. The subfamily classification
hindwings much smaller. Larvae with two lateral varies, but currently involves ten subfamilies, with
setae on the prothorax. segregation into three groups: Oenosandrinina (for
Sphingidae (hawk moths) total 1,230 species Oenosandrinae, with three species in Australia),
worldwide. Tropical regions of the New World, Thaumetopoeinina (for Thaumetopoeinae), and
Africa and Asia have the most biodiversity. There Notodontinina (for the remaining eight subfamilies).
are three subfamilies. Adults are medium size to Adults are small to very large; some with massive
very large and nocturnal or crepuscular, but some bodies. Adults are mostly nocturnal. Larvae are leaf
a diurnal. Larvae are leaf feeders, usually with pos- feeders, sometimes gregarious (especially among
terior horn-like scolus (thus, the common name, Thaumetopoeinae) and feeding nocturnally. Host-
hornworms, for the larvae); many larvae extremely plants include a large variety of plant families,
large. Hostplants recorded in numerous plant especially for broadleaf forest trees. A number of
families. Some are economic. economic species are known.
Dioptidae (American false tiger moths) total
507 species, primarily Neotropical (505 sp.); actual
Noctuoidea fauna likely exceeds 800 species. Two subfamilies
are known. Adults are medium size and mostly
The largest superfamily, containing nearly a third nocturnal, but some are diurnal or crepuscular.
of all lepidopterans, the Noctuoidea comprise Larvae are leaf feeders, particularly toxic plants
about 44,025 described species, mainly in the in families like Aristolochiaceae, Euphorbiaceae,
families Noctuidae and Arctiidae. Six families are Passifloraceae, and Violaceae, but also on various
included in the superfamily: Notodontidae, Diop- others like Fagaceae. Very few are economic.
tidae, Thyretidae, Lymantriidae, Arctiidae, and Thyretidae (African maiden moths) include
Noctuidae. Numerous subfamilies among these 212 species, all African. Adults are medium-size.
families have at various times been considered Adults perhaps mostly diurnal; often wasp mim-
families, and various specialists are still undecided ics. Larvae are thought to be leaf feeders, but most
on the number of families to use. For example, species remain unknown biologically. Hostplant
Thyretidae are sometimes included in Arctiidae records include Thymelaeaceae and Ulmaceae.
and Dioptidae are included among Notodontidae. Lymantriidae (tussock moths) total 2,490 spe-
Contrarily, Oenosandrinae, Thaumetopoeinae, and cies worldwide; actual fauna likely exceeds 3,000
Doinae are often listed as separate families. Adults species. Most of the fauna is Old World tropical (ca.
with head scaling mostly normal (rarely rough- 2,090 sp.). Two subfamilies are used. Adults are
ened); haustellum naked (sometimes reduced); small to very large and mostly nocturnal, but some
labial palpi mostly upcurved but many porrect or are diurnal or crepuscular. Larvae are leaf feeders,
recurved; maxillary palpi mostly vestigial or absent sometimes gregariously. Hostplants include many
(some larger in Notodontidae); antennae varied; different plant families. Many species are serious
body mostly robust; forewings mostly elongate defoliators of forest trees.
triangular and hindwings more rounded; body Arctiidae (tiger moths) include 11,155 species
usually robust and with metathoracic tympanal worldwide, primarily Neotropical (ca. 6,000 sp.);
organs (but absent or vestigial in Syntominae, actual world fauna likely exceeds 14,000 species.
672
B Butterfly Counts

There are five subfamilies among groups: group Holloway JD, Bradley JD, Carter DJ (1987) Lepidoptera. In:
CIE guides to insects of importance to man. 1. CABI
Pericopinina (with Pericopinae), group Arctiinina
and British Museum of Natural History, London, UK,
(for Lithosiinae and Arctiinae), and group Ctenu- 262 pp
chinina (for Ctenuchinae and Syntominae). Adults Kristensen NP (ed) (1999) Lepidoptera, moths and butter-
are small to large; hindwings greatly reduced in flies. Vol. 1: Evolution, systematics, and biogeography.
In: Handbuch der Zoologie. Band IV. Arthropoda:
some groups (wasp moths). Adults mostly nocturnal Insecta. Teilband 35. W. De Gruyter, Berlin, Germany,
but many are crepuscular or diurnal (Pericopinae, 487 pp
Ctenuchinae, and Syntominae). Larvae are leaf Portier P (1949) La biologie le lpidoptres. In: Encyclopdie
feeders. Hostplants are varied among numerous entomologique (A) 23:1643, 1 pl. P. Lechevalier, Paris,
France
plant families, including mosses and lichens. Scoble MJ (1992) The Lepidoptera: form, function and
Noctuidae (owlet moths) are the largest family diversity. Oxford University Press, Oxford, UK, 404 pp
of Lepidoptera, with about 26,310 described species Stehr FW (ed) (1987) In Lepidoptera. In: Stehr FW (ed)
Immature insects [1]. Kendall-Hunt, Dubuque, Iowa,
worldwide; actual fauna likely exceeds 30,000
pp 288596
species. Major regions of biodiversity are in the Vane-Wright RI, Ackery PR (eds) (1984) The biology of
Neotropics (ca. 8,600 sp.) and the Indo Australian butterflies. Royal Entomological Society of London,
region (6,500 sp.). Numerous subfamilies and tribes London, UK, 429 pp. (Reprinted 1989. Princeton
University Press, Princeton, NJ)
have been described and the classification is still in Watson A, Whalley PES (1975) The dictionary of butterflies
flux, but 26 subfamilies are now recognized, mostly and moths in color. McGraw Hill, New York, New York,
in group Noctuinina; also segregated are Aganainae 296 pp, 144 pl
(previously in Arctiidae), in group Aganainina, and Young M (1997)The natural history of moths. T. & A. D.
Poyser, London, UK, 271 pp, 16 pl
Herminiinae, in group Herminiinina. Adults are
small to very large and mostly nocturnal, but some
are crepuscular and several groups are diurnal. Lar-
vae mostly leaf feeders, but many are borers. Host- Butterfly Counts
plants include numerous plant families, but the
majority of owlet moths are not known biologically. linda wiener
Some agricultural pests are included in the family St. Johns College, Santa Fe, NM, USA
(e.g., cutworms, armyworms, and others).
Butterflies The North American Butterfly Association,
Butterfly Counts together with the Xerxes Society, coordinates the
Butterfly Gardening and Individual Families annual North American butterfly counts. Partici-
Conservation of Insects pants in this event pick a date, usually within two
weeks on either side of July 4. On this date, the aim
References is to count, in a 24 h period, the number of species
of butterflies and the number of individuals of
Bourgogne J (1951) Order des lpidoptres. In: Grass PP each species within a circle 15 miles in diameter.
(ed) Trait de Zoologie. Anatomie, Systmatique, Biolo- When the same locations are visited year after
gie. Insectes 10:174448, 3 pl. Masson, Paris, France year, a long term record of butterfly diversity and
Eaton JL (1988) Lepidopteran anatomy. Wiley, New York, NY,
abundance is available from each site.
257 pp
Heppner JB (1991) Faunal regions and the diversity of This has been an annual event since 1975
Lepidoptera. Trop Lepid 2 (suppl 1):185 when there were 29 official counts. In 2000, 422
Heppner JB (1998) Classification of Lepidoptera. In: Holarctic counts were held; 349 in 44 states in the U.S., 66
Lepidoptera, 5 (suppl 1):1148 (1998); 14 (suppl 1):149
320 (2003); 15 (suppl 1): (in prep)
Canadian counts in five provinces, and seven
Hering EM (1925) Biologie der Schmetterlinge. J Springer, Mexican counts in three states. The purpose of the
Berlin, Germany, 480 pp counts is to get long term records, over a wide
 Butterfly Counts
B 673

Butterfly Counts, Table 11 Santa Fe Butterfly Count Results (Glorieta Canyon/Glorieta Peak)a*
1994 1995 1996 1997
SWALLOWTALLS
Black Swallowtail 1 -/5
Anise Swallowtail -/1
Western Tiger 14 4 1/3
Two-tailed Swallowtail 5 2/1
Pale Swallowtail 5 -/-
WHITES AND SULFURS
Pine White 6 -/-
Checkered White 2 44 24/-
Mustard White 37 11 12/-
Orange Sulfur 13 30 1 19/13
Southern Dogface 2 -/-
Mexican Yellow 14 -/-
Dainty Sulfur 1 29 2/-
LITTLE BUTTERFLIES
Colorado Hairstreak 1 -/-
Great Blue Hairstreak 1 -/-
Coral Hairstreak 1 -/-
Behrs Hairstreak 7 1 -/-
Banded Hairstreak 72 38 2 10/-
Western Pine Elfin 1 -/-
Thicket Hairstreak 3 1/-
Juniper Hairstreak 2 -/-
Gray Hairstreak 1 1/-
Leda Ministreak 1 -/-
Marine Blue 4 -/-
Reakirts Blue 62 33 1/-
Western Tailed-Blue 2 1 -/-
Melissa Blue 2 -/-
Acmon Blue 5 4 1/-
BRUSH-FOOTED BUTTERFLIES
Variegated Fritillary 27 3 26/-
Atlantis Fritillary 4 20 7 10/4
Arachne Checkerspot 16 -/1
Silvery Checkerspot 1 36 1
Northern Crescent 2 2/-
Field Crescent 1 3/-
Mylitta Crescent 1 6/-
674
B Butterfly Counts

Butterfly Counts, Table 11 (Continued)

Satyr Anglewing 1
Green Anglewing 1
Zephyr Anglewing 6 2 2/-
Mourning Cloak 7 11 3 7/2
American Lady 5 7 1/-
Painted Lady 20 1 5/7
West Coast Lady 10 -/-
Weidemeyers Admiral 3 3 5 21/1
California Sister 3 -/-
Goatweed Butterfly 1/-
SATYRS AND WOOD NYMPHS
Canyonland Satyr 1 1/-
Common Ringlet 2
Small Wood-Nymph 74 45 86 27/7
MILKWEED BUTTERFLIES
Monarch 1/-
SKIPPERS
Silver-spotted Skipper 1 -/-
Mexican Cloudywing 2 3 -/1
Northern Cloudywing 2 2 -/-
Rocky Mountain Duskywing 2 -/-
Persius Duskywing -/8
Afranius Duskywing 1 3/-
Common Checkered-Skipper 10 34 4 49/-
Sootywing sp 1/-
Russet Skipperling 7 7 1 3/-
Garita Skipperling 1/1
Pahaska Skipper 1/3
Tawny-edged Skipper 10 10 4 3/-
Snows Skipper 6
Golden Skipper 41 17 16 4/-
Dun Skipper 60 9 1 2/-
Common Roadside-Skipper 2
Total species 36 32 20 35/17 (42)
Total butterflies 519 455 146 258/61(319)
 Butterfly Gardening
B 675

g eographical area, of butterfly diversity and about host plants, habitat, habits and behaviors,
abundance. A second, but equally important goal, and of course, butterfly identification. Many
is to increase public awareness of insect conserva- people who show up out of curiosity come back
tion. Consequently, counts are advertised and the year after year and find it a great pleasure to
general public is invited to participate. Each group compare results from year to year.
records every species seen as well as the number of For those who want more precise data
individuals of each species. Other information generated in a more systematic manner, Pollard
recorded is how many people counted, total num- transects are a good way to go. This technique
ber of miles covered, and total amount of time in uses a transect route which is marked out and
the field as well as information about weather and followed, usually once per week. The counter
habitat. Annual results are published by the North walks at a standard pace and all butterflies within
American Butterfly Association. a fixed distance of the path are counted. This
The data obtained in these counts is, due to monitoring scheme is used in Great Britain and
the uncontrolled conditions, not the most system- the Netherlands, and to a limited degree in the
atic. However, it has still proven to be useful for United States.
looking at large trends. For example, the count The accompanying table shows some typical
data from 1989 to 1997 have been used to assess count data from the Santa Fe, New Mexico, but-
patterns of species richness and abundance across terfly count Butterfly Counts From Areas of New
North America. The log of party hours (number of Mexico, USA.
hours spent making observations in the field was
used summed across all groups in a single count References
circle) to standardize species richness and abun-
dance data. The study concluded that (i) species
Kocher SD, Williams EH (2000) The diversity and abundance
richness is highest in low latitudes and Rocky of North American butterflies vary with habitat, distur-
Mountain longitudes, (ii) total abundance is high- bance, and geography. J Biogeogr 27:785794
est in northern U.S. latitudes and Great Plains lon- North American Butterfly Association website. Available at
gitudes, (iii) species richness increases with greater www.naba.org
Pollard E, Yates TJ (1993) Monitoring butterflies for ecology
topographical relief, and (iv) species richness and and conservation. Chapman and Hall, London, UK
diversity indices are lower in more disturbed
habitats. The North American Butterfly Associa-
tion magazine, American Butterflies, publishes a
count column which gives information about the Butterfly Gardening
counts and analyses of results. Butterfly enthusi-
asts interested in starting their own counts should jaret c. daniels
visit the NABA web site www.naba.org. At this site University of Florida, Gainesville, FL, USA
information is available on running and reporting
a count and who to contact in your region about Butterfly gardening has become a very popular
count locations which already exist. pastime in recent years. Planting a butterfly garden
Butterfly counts are a wonderful way to is a simple and rewarding experience for both
introduce children, parents, and other interested children and adults. If you like bird watching or
individuals to butterflies. There does need to be flower gardening, you will love butterfly gardening!
at least one experienced butterfly identifier in the Unlike most wildlife, butterflies are not strictly
group, but everyone can run around and catch limited to remote natural areas. They are commonly
them. There are numerous opportunities to teach found in both country and city and can easily be
676
B Butterfly Gardening

attracted with a little know-how and the proper The Butterfly Life Cycle
planning. A butterfly garden does not require much
land; even a few strategic additions to an existing All butterflies go through a life cycle consisting of
garden can make a big difference. four distinct developmental stages: the egg, the
Whether it fits in a container on the patio larva or caterpillar, the pupa and the adult. Adult
or stretches over several acres, a well-planned females typically deposit small eggs singly or in
butterfly garden can be as simple or as compli- clusters on or near specific plant species. These
cated as you want to make it. The same basic host plants provide growing larvae with the proper
concepts and guidelines apply, regardless of nutrition they need to complete growth and
the size. The most important thing to under- development. Larval host plants may also furnish
stand before you begin is that butterflies have shelter, camouflage, and chemicals used for pro-
many different behaviors, affinities, and needs. tection, courtship, and reproduction. Caterpillars
Also, these requirements often change dra- (larvae) are herbivores (plant feeders) and have
matically throughout their life-cycle. A well- very selective tastes. Each butterfly species only
planned butterfly garden should provide feeds on specific plant species. Consequently, but-
variety to attract different kinds of butterflies terfly larvae rarely become pests of vegetable and
and cater to both adult butterflies and their ornamental plants, though they will greedily eat
larvae. Proper choice of plants and l andscape the host plants you provide for them.
design is essential. Such decisions will help Butterfly larvae can grow at an astonishing
determine which butterfly species will be rate, increasing in size and weight many times over
attracted, remain in the area, and ultimately before reaching maturity. To accommodate this
reproduce. tremendous change in proportion, each larva
Why You Should Plant a Butterfly Garden molts numerous times during its life, revealing
Butterflies are the most popular of all insects. each time a new and often radically different larval
Besides being attractive, they play some important skin. Once fully grown, the larva seeks a safe place
roles in the environment, including: to pupate. Most attach themselves to a branch, twig
1. Butterflies help pollinate a wide range of native and or other support by spinning silk. After a short
cultivated flowering plants. rest, the larva molts for the last time to reveal the
2. Butterflies provide food for many other organisms. pupa, or chrysalis. Inside, larval structures break
Various small mammals, nesting birds, lizards, spi- down and reorganize to form the adult butterfly.
ders, and other insects all feed on adult butterflies or When environmental conditions are right, the
their larvae. pupa splits open and an adult butterfly emerges.
3. Due to their tremendous appeal and popularity,
butterflies often serve as umbrella species. When
butterflies are protected, their habitats and the other The Elements of a Butterfly Garden
creatures that live there are also protected.
4. Butterflies are indicator species. They are among There are several simple guidelines that, if fol-
the first organisms to show a negative reaction to lowed, will result in a successful butterfly garden:
environmental changes and pollutants. Just like a Provide a combination of adult nectar sources
canary in a coalmine, butterflies can help alert us to and larval host plants. A garden with both adult
problems in the local environment that may affect nectar sources and larval host plants can accom-
our own health and well-being. modate the entire life cycle of a butterfly. Having
5. Butterflies are a convenient way for you and your both adult and larval resources available will
children to learn about insects, an abundant, impor- encourage adult butterflies to remain in your yard,
tant, but poorly known group of organisms. reproduce, and build populations year after year.
 Butterfly Gardening
B 677

Plant in both full sun and partial shade if you Weeds can be good for your garden. Many
can. Most butterflies and their adult nectar sources common weeds serve as larval host plants. Care-
are fond of bright sunlight. However, some butter- fully search each plant for larvae before you pull it
flies are at home in woodlands or along forest out. If larvae are present, leave the plant alone until
edges and rarely venture out into open, sunny they have finished feeding.
areas. They often are more attracted to nectar Learn to identify the butterflies in your area.
sources and larval host plants located in the shad- Become familiar with your local butterfly species.
ier sections of the garden. Try to learn which ones are common, which ones
Plan for consistent host plant and nectar are rare, and which ones you most want to attract.
availability throughout the growing season. Then when it is time to choose the larval host plants
Choose plants that bloom, grow or perform better for your garden, select your plants accordingly.
at different times of the year, as well as plants hav-
ing one peak season. The added variety insures
that your garden will provide continuous food for Adult Nectar Sources
butterflies.
Plan for diversity. Choose plants that have a Adult butterflies are highly active, but short-lived.
variety of different heights and growth habits. A During their brief adult period, they must find a
diverse planting scheme helps to increase the mate, reproduce, seek out food and shelter, and
number of microclimates and feeding levels avail- avoid being. To accomplish all this, most adult
able to butterflies. Also, provide a mix of flower butterflies rely on sugar-rich nectar as fuel.
colors, shapes, and sizes. Different butterfly species Nectar-rich, colorful flowering plants, there-
have distinct color preferences, feeding behaviors, fore, are the backbone of any successful butterfly
and proboscis (tongue) lengths. These factors garden. They draw in adult butterflies from the
determine which flowers a butterfly chooses or is surrounding environment like a magnet while
able to visit. A wide mix of adult nectar sources adding beauty and interest to the landscape. They
provides accessible and attractive food to a greater also attract butterflies rapidly. Therefore, adult
number of butterfly species. nectar sources should always be the first additions
Plant in groupings. If space allows, try to com- to a new butterfly garden.
bine several plants of the same species in a large When selecting flower colors, aim for a vari-
grouping. Large drifts of color and clusters of veg- ety. While reds, pinks and purples are generally
etation tend to be more apparent and attractive to the most attractive adult nectar source colors, a
adult butterflies. Groups of larval host plants pro- great many butterfly species are also drawn to yel-
vide larvae with additional resources in the event lows, blues, and whites. Each butterfly species has
one is depleted, and help to mask leaf damage or its own color preferences.
defoliation. Flower shape also influences visitation. In
Include native plants. Native plants are well acquiring nectar, butterflies are limited by the length
adapted to the soil type and climate of the region of their proboscis, or tongue. As a result, the nectar
where they naturally occur and are not as prone to in long, tubular flowers is typically more accessible
disease or pest attack. to butterflies possessing a longer proboscis. A but-
Choose the appropriate plant for each loca- terflys behavior while feeding affects its flower
tion. Determine the basic light, water, and soil choice as well. Many large swallowtail butterflies, for
requirements of each plant before planting. For example, continuously flutter their wings while
example, avoid putting a sun-loving species in nectaring. This enables them to feed much like hum-
deep shade. This will insure ensure that your plants mingbirds, with access to flowers too delicate to land
grow and perform to their maximum potential. on. On the other hand, many smaller butterflies such
678
B Butterfly Gardening

as blues and hairstreaks prefer to feed while at rest. butterflies, mourning cloaks, malachites, buckeyes,
They are strongly attracted to large clusters of small, as well as some satyrs and wood nymphs are also
short-tubed flowers that form a stable platform on drawn to or feed solely on tree sap, rotting fruit,
which to alight. dung or carrion.
The greater the variety of flower colors, shapes, To accommodate their needs, simply place
and sizes available, the greater variety of butterfly one or more shallow dishes on the ground at
species will be attracted. Double- and triple-flow- various locations throughout the garden. Fill
ered plants are the only major exception to this them with a selection of rotting fruit, banana
rule. While such flowers produce spectacular peels, and melon rinds. Mash large pieces or
blooms, they have been bred to impress humans, whole fruit to help increase the available surface
not butterflies. In the process, external features area and expose the juicy interior. Once a week
have been artificially manipulated, often at the or so, rinse out each dish with a garden hose and
expense of nectar content or accessibility. refill. If ants are a problem, fill a slightly larger
dish with water and set the smaller fruit dish in
the center. This creates a small moat and prevents
Larval Host Plants the ants but not the butterflies from gaining
access to the tasty meal.
Larval host plants also are key ingredients to any
successful butterfly garden. They are generally not
as showy, nor are they absolutely necessary to attract Water
adult butterflies. However, a garden composed
solely of nectar plants provides nothing more than Males of many butterfly species commonly gather
a simple, fast-food refueling spot. It completely at water sources such as stream banks, mud pud-
ignores the requirements of the other stages of a dles, moist gravel or damp sand for access to water,
butterfly life cycle. Consequently, adult butterflies dissolved salts, and amino acids. Such groupings
come into the garden to feed but soon leave. can form rather impressive displays. For the more
Larval host plants offer butterflies a reason ambitious butterfly gardener, artificial mud pud-
to stay and not just pass through. Adults drawn dles or water stations can be created with varying
into the garden by colorful nectar plants will now degrees of effort.
find all the necessary resources to reproduce. You The simplest method is to fill a large plastic
will soon notice some of the same individuals container, such as a sweater storage box, with sand.
returning day after day and many of the same Locate an open, sunlit area of your garden, dig a
butterfly species becoming garden regulars. Most shallow hole, and place the container into the
adult butterflies tend not to wander far from their ground so that the rim is even with the top of the
larval hosts. Thus, you may notice a greater number soil. Fill in any gaps around the outside of the con-
of butterflies. Instead of just attracting individuals tainer with loose earth and thoroughly wet the
from the surrounding area, your garden will pro- sand. The plastic container will hold in the water
duce new adults from the maturing larvae present. and keep the sand moist for some time.
The same process can be accomplished on a
larger scale by lining an existing depression or
Other Attractants newly dug hole with plastic. Simply make sure
that the edges of the plastic are covered with soil
Not all butterflies are exclusively attracted to flow- and fill the center with sand or small gravel. A
ers. Many species, such as red-spotted purples, leaf slightly concave design will help moisture collect
wings, question marks, tawny emperors, hackberry from occasional rain and regular garden watering.
 Butterfly Gardening
B 679

The spray from a small garden fountain placed Avoid using pesticides. All butterfly life stages
nearby can also help keep the ground consis- are extremely sensitive to pesticides. Even the
tently moist. slightest drift from nearby spraying can be deadly.
To make the area even more attractive, ini- If you want to have a butterfly garden, you must be
tially mix in a small amount of table salt with the willing to tolerate insects, including some that eat
sand or occasionally add a capful of natural fish the flowers. Try to allow the natural enemies of
emulsion (an organic fertilizer available at most insects to take care of the insect problems. Even
garden centers). Bacillus thuringiensis, or Bt, a natural bacterial
disease of caterpillar pests that is normally consid-
ered harmless because it does not affect most
Shelter insects, people, or pests, can be deadly to butterfly
larvae. If you must use insect control, always
In addition to food and water, butterflies often choose the least toxic chemical first. Insecticidal
need protection from wind, rain, temperature soaps and horticultural oils, for example, can be
extremes, and predators. The easiest way to effective against many small garden pests. They
accomplish this in the garden is to include many are harmless to humans and generally biodegrad-
kinds of plants, including shrubs and small able. If the problem persists, move on to a stronger
trees. Try also to cluster vegetation and add a chemical, but apply it selectively. Apply pesticides
few nondeciduous species. Given time, as your only to the infested branch or plant and never treat
garden grows and matures, the diversity of the entire garden. Choose short-lived (non-resid-
plantings will naturally create several microcli- ual) products. Particularly avoid using systemic
mates, or small localized environments, that pesticides on larval host plants. Unlike contact
offer butterflies shelter. poisons, systemic pesticides are taken up by the
plant. They kill when an insect eats the treated
vegetation.
Keeping the Butterfly Garden Trim off old blossoms. Periodic deadheading,
Productive or removal of old, spent blossoms on your nectar
plants, will encourage the continued production
There are a few basic steps that will help you keep of new flowers. It can also extend the flowering
your garden healthy, productive and looking its period of some species.
best:
Give new plants a good start. New plants can
quickly become stressed. As a result, they are more Choice of Butterfly Plants
vulnerable to disease and pest attack. They may grow
poorly and even die if not properly attended. There- The choice of plants for your butterfly garden is
fore, make sure to mulch and regularly water all new determined by several factors, including the amount
plants. This will help reduce weed competition, keep of sun or shade, the soil and moisture conditions,
them from drying out, and insure that they become and the climate where you live. Therefore, the
firmly established. Healthy plants will reward you preferred plants vary from place to place, and for
with vigorous growth and healthy blossoms. specific recommendations it is advisable to check
Fertilize regularly. Routine fertilizer applica- with local butterfly gardening publications and edu-
tions will help produce maximum plant growth and cational sources such as the cooperative extension
flower production. Consult a local nursery specialist service in your area. As examples, following are lists
or Extension agent if you have questions about of plants recommended for a northern climate,
specific fertilizers or particular plant requirements. Nebraska, and a southern climate, Florida. Note that
680
B Butterfly Gardening

although some plants are recommended in both Parsley - Petroselinum crispum {L,N}
locations, few are recommended for both locations. Queen Annes Lace - Daucus carota {L,N}
Sweet Fennel - Foeniculum vulgare {L,N}
Thistle - Cirsium spp. {L,N}
List of Plants to Attract Butterflies
in Nebraska
Shrubs
Source: Nebraska Cooperative Extension Service,
Nebguide G931183-A Butterfly Bush - Buddleia davidii {N}
{L}=Larval Food Plants Cinquefoil - Potentilla spp. {N}
{N}=Nectar Plants Chokecherry - Prunus virginiana {L,N}
Cotoneaster - Cotoneaster spp. {N}
Lilac - Syringa spp. {N}
Annual Flowers Mock Orange - Philadelphus spp. {N}
Privet - Ligustrum spp. {N}
Ageratum - Ageratum houstonianum {N} Spirea - Spiraea spp. {N}
Common Sunflower - Helianthus annuus {L,N} Viburnum - Viburnum spp. {N}
Cosmos - Cosmos spp. {N} Wild Plum - Prunus americana {L,N}
Fetid Marigold - Dyssodia papposa {L}
Globe Candytuft - Iberis umbellata {N}
Gomphrena - Gomphrena globosa {N} Perennial Herbaceous Plants
Heliotrope - Heliotropium arborescens {N}
Lantana - Lantana camara {N} Aster - Aster spp. {L,N}
Marigold - Tagetes spp. {N} BeeBalm - Monarda spp. {N}
Nasturtium Tropaeolum spp. {N} Blanketflower - Gaillardia spp. {N}
Nicotiana - Nicotiana alata {N} Butterfly Weed - Asclepias tuberosa {L,N}
Petunia - Petunia x hybrida {N} Chrysanthemum - Chrysanthemum spp. (open-
Salvia - Salvia spp. {N} centered types) {N}
Scabiosa - Scabiosa atropurpurea {N} Clover - Melilotus spp., Trifolium spp. {L,N}
Snapdragon - Antirrhinum majus {L,N} Coreopsis - Coreopsis spp. {N}
Statice - Limonium sinuatum {N} Daylily - Hemerocalli s spp. {N}
Sunflower - Helianthus spp. {N} Dogbane - Apocynum spp. {N}
Sweet Alyssum - Lobularia maritima {N} Gayfeather - Liatris spp. {N}
Verbena - Verbena spp. {N} Goldenrod - Solidago rigida {N}
Zinnia - Zinnia spp. {N} Hollyhock - Alcea rosea {L}
Ironweed - Vernonia spp. {N}
Joe-Pye Weed - Eupatorium spp. {N}
Biennials Mallow - Malva spp. {L}
Milk-vetch - Astragalus spp. {L,N}
Catnip - Nepeta cataria {N} Milkweed - Asclepias spp. {L,N}
Chives - Allium schoenoprasum {N} Ornamental Onion - Allium spp. {N}
Dames Rocket - Hesperis matronalis {N} Partridge Pea - Cassia fasciculata {L,N}
Dill - Anethum graveolens {L,N} Phlox - Phlox spp. {N}
Lavender - Lavender angustifolia {N} Pinks - Dianthus spp. {N}
Mint - Mentha spp. {N} Prairie Clover - Dalea spp. {L,N}
 Butterfly Gardening
B 681

Purple Coneflower - Echinacea spp. {N} Sweet Pepperbush - Clethra alnifolia

Pussy-toes - Antennaria spp. {N} Virginia Willow - Itea virginica
Rudbeckia - Rudbeckia spp. {N}
Sedum - Sedum spp. {N}
Vines
Shasta Daisy - Chrysanthemum maximum {N}
Yarrow - Achillea spp. {N}
Bougainvillea - Bougainvillea sp.
Coral Vine - Antigon leptopus
Honeysuckle - Lonicera spp.
Plants For Butterfly Gardening in Mexican Flame Vine - Senecio
Florida Morning Glory - Ipomoea spp.
Star Jasmine - Trachelospermum jasminoides
Source: Your Florida guide to butterfly gardening.
A guide for the Deep South
Herbaceous Perennials

Trees Aster - Aster spp

Bachelors Button - Centaurea sp.
American Plum - Prunus americana Black-eyed Susan - Rudbeckia hirta
Black Cherry - Prunus serotina Blazing Star - Liatris spp.
Chaste Tree - Vitex agnus-castu Blue Sage - Salvia azurea
Chickasaw Plum - Prunus angustifolia Bluebeard - Caryopteris chandonensis
Coastal Plains Willow - Salix caroliniana Blue-eyed Grass - Sisyrinchium sp.
Flowering Dogwood - Cornus florida Butterfly Weed - Asclepias tuberosa
Hop Tree - Ptelea trifoliata Cardinal Flower - Lobelia cardinalis
Mimosa - Albiza julibrissum Catchfly - Silene spp.
Redbud - Cercis canadensis Cigar Plant - Cuphea micropetala
Coral Vine - Antigon leptopus
Coralbean - Erythrina heracea
Shrubs Daylily - Hemerocallis sp.
Deer Tongue - Carphephorus sp.
Azalea - Rhododendron sp. Fire Spike - Odontonema strictum
Blackberry - Rubus sp Firecracker Plant - Russelia equisetiformis
Butterfly Bush - Buddleia davidii Frogfruit - Phyla nodiflora
Button Bush - Cephalanthus occidentalis Garden Phlox - Phlox paniculata
Chinese Privet - Ligustrum sinense Glorybower - Clerodendrum bungei
Fire Bush - Hamelia patens Goldenaster - Chrysopsis sp.
Glossy Abelia - Abelia x grandiflora Goldenrod - Solidago spp.
Golden Dewdrop - Duranta repens Groundsel - Senecio spp.
Hibiscus - Hibiscus sp. Heliotrope - Heliotropium arborescens
Ixora - Ixora sp. Indian Blanket - Gaillardia pulchella
Jatropha - Jatropha integerrima Indigo Bush - Amorpha fruticosa
New Jersey Tea -Ceonothus americanus Ironweed - Vernonia spp.
Plumbago - Plumbago capensis Joe-pye Weed - Eupatorium fistulosum
Pride of Barbados - Caeselpina pulcherima Jupiters Beard - Centrantus ruber
Red Buckeye - Aesculus pavia Lantana - Lantana sp.
682
B Butterfly Gardening

Mexican Heather - Cuphea hysoppifolia Corky-stemmed Passion Vine (P. suberosa), Gulf Fritil-
Mexican Milkweed - Asclepias curassavica lary (Agraulis vanillae), Zebra Longwing (Helico-
Mist Flower - Eupatorium coelestinum nius charitonius), Julia (Dryas iulia)
Moss Verbena - Verbena tenuisecta Cudweed (Gnaphalium sp.), American Painted Lady
Mountain Mint - Pycnanthemum sp. (Vanessa virginiensis)
Obedient Plant - Physostegia virginiana Dill (Anethum graveolens), Black Swallowtail (Papilio
Pentas - Pentas lanceolata polyxenes)
Porter Weed - Stachytarphaeta jamaicensis Dutchmans Pipe (Aristolochia sp.), Polydamus
Purple Coneflower - Echinacea purpurea Swallowtail (Battus polydamus), Pipevine Swallo-
Rattlesnake Master - Eryngium yuccifolium wtail (Battus philenor)
Sandhill Milkweed - Asclepias humistrata False Indigo (Amorpha fruticosa), Dogface Butterfly
Sedum - Sedum spp (Zerene cesonia)
Shepherds Needle - Bidens alba False Nettle (Boehmeria sp.), Red Admiral (Vanessa
Shrimp-plant - Beloperone guttata atalanta)
Society Garlic - Tulbaghia violacea Fennel (Feoniculum vulgare), Black Swallowtail (Papilio
Spotted Beebalm - Monarda punctata polyxenes)
Stokes Aster - Aster laevis Frogfruit (Phyla nodiflora), White Peacock (Anartia ja-
Sunflower - Helianthus sp trophae), Phaon Crescent (Pyciodes phaon)
Swamp Milkweed - Asclepias incarnata Gerardia (Agalinus sp.), Buckeye (Junonia coenia)
Tall Wild Verbena - Verbena brasiliensis Green Ash (Fraxinus pennsylvanica), Tiger Swallowtail
Tropical Sage - Salvia coccinea (Papilio glaucus)
Tuber Vervain - Verbena rigida Green Shrimp-plant (Blechum brownei), Malachite (Si-
Verbena - Verbena sp proeta stelenes), White Peacock (Anartia jatrophe)
Wild Petunia - Ruellia brittoniana Hercules-club (Zanthoxylum clava-hercules), Giant
Yarrow - Achillea millefolium Swallowtail (Papilio cresphontes)
Hop Tree (Ptelea trifoliata), Giant Swallowtail (Papilio
cresphontes)
Some Larval Host Plants and Species Indigo Bush (Indigofera sp.), Ceraunus Blue (Hemiar-
Supported: gus ceraunus)
Joint Vetch (Aeschynemone sp.), Barred Sulphur (Eure-
Beggars-tick (Desmodium sp.), Long-tailed Skipper ma daira)
(Urbanus proteus) Live Oak (Quercus virginiana), White M Hairstreak
Black Cherry (Prunus serotina), Tiger Swallowtail (Parrhasius m-album)
(Papilio glaucus), Red-spotted Purple (Limenitis Maypop (Passiflora incarnata), Zebra Longwing (Heli-
arthemis astyanax) conius charitonius), Gulf Fritillary (Agraulis va-
Blue Passionflower (Passiflora caerulea), Gulf Fritil lary nillae), Julia (Dryas iulia), Variegated Fritillary
(Agraulis vanillae) (Euptoieta claudia)
Camphor Tree (Cinnamonum camphora), Spicebush Mexican Milkweed (Asclepias curassavica), Monarch
Swallowtail (Papilio troilus) (Danaus plexippus), Queen (Danaus gilippus)
Cassia (Cassia sp.), Cloudless Sulphur (Phoebis sennae), Partridge Pea (Cassia fasciculata), Cloudless Sulphur
Orange-barred Sulphur (Phoebis philea), Sleepy (Phoebis sennae), Little Sulphur (Eurema lisa)
Orange (Eurema nicippe) Parsley (Petroselinium crispum), Black Swallowtail (Pa-
Coastal Plain Willow (Salix caroliniana), Viceroy (Li- pilio polyxenes)
menitis archippus floridensis) Pawpaw (Asimina sp.), Zebra Swallowtail (Eurytides
Coontie (Zamia pumila), Atala (Eumaeus atala florida) marcellus)
 Buxton, Patrick Alfred
B 683

Pencil Flower (Stylosanthes biflora), Barred Sulphur Swallowtail (Battus philenor), Polydamus Swallo-
(Eurema daira) wtail (Battus polydamus)
Plantain (Plantago sp.), Buckeye (Junonia coenia) Wax Myrtle (Myrica cerifera), Red-banded Hairstreak
Red Bay (Persea borbonia), Palamedes Swallowtail (Pa- (Calycopis cecrops)
pilio palamedes), Spicebush Swallowtail (Papilio White Ash (Fraxinus americana), Tiger Swallowtail
troilus) (Papilio glaucus)
Rue (Ruta graveolens), Black Swallowtail (Papilio poly- White Oak (Quercus alba), Banded Hairstreak (Satyri-
xenes), Giant Swallowtail (Papilio cresphontes) um calanus)
Ruellia (Ruellia sp.), Buckeye (Junonia coenia), Mala- White Sweet Clover (Melilotus alba), Gray Hairstreak
chite (Siproeta stelenes), White Peacock (Anartia (Strymon melinus), Alfalfa Butterfly (Colias eury-
jatrophe) theme)
Saltwort (Batis sp.), Great Southern White (Ascia mo- Wild Lime (Zanthoxylum fagara), Giant Swallowtail
nuste) (Papilio cresphontes)
Sassafras (Sassafras albidum), Spicebush Swallowtail Winged Elm (Ulmus alata), Question Mark (Polygonia
(Papilio troilus) interrogationis)
Shepherds Needle (Bidens alba), Dainty Sulphur (Na- Winged Sumac (Rhus copallina), Red-banded Hairstreak
thalis iole) (Calycopis cecrops)
Slippery Elm (Ulmus rubra), Question Mark (Polygonia The butterfly web site: http://www.thebutterflysite.com/
interrogationis) gardening.shtml
Smooth Water Hyssop (Bacopa monnieri), White Pea-
cock (Anartia jatrophe)
Southern Red Cedar (Juniperus virginiana), Swead ners
Hairstreak (Mitoura gryneus sweadneri) References
Spicebush (Lindera benzoin), Spicebush Swallowtail
(Papilio troilus) Daniels JC (2000) Your Florida guide to butterfly gardening: a
guide for the Deep South. University Press of Florida,
Sugarberry (Celtis laevigata), Hackberry Butterfly (As- Gainesville, FL
terocampa celtis), Tawny Emperor (Asterocampa Minno M, Minno M (1999) Florida butterfly gardening. Uni-
clyton), Question Mark (Polygonia interrogatio- versity Press of Florida, Gainesville, FL
North American Butterfly Association web site. Available at
nis), Snout Butterfly (Libytheana bachmanii)
http://www.naba.org/pubs/bgh.html
Swamp Bay (Persea palustris), Palamedes Swallowtail Tekulsky M (1985) The butterfly garden. The Harvard Com-
(Papilio palamedes), Spicebush Swallowtail (Pa- mon Press, Boston, MA
pilio troilus)
Sweet Bay (Magnolia virginiana), Tiger Swallowtail
(Papilio glaucus), Palamedes Swallowtail (Papi-
lio palamedes), Spicebush Swallowtail (Papilio Buxton, Patrick Alfred
troilus)
Toadflax (Linaria sp.), Buckeye (Junonia coenia) Patrick Buxton was born in 1892. He attended
Tree Pawpaw (Asimina triloba), Zebra Swallowtail (Eu- Cambridge University in 19161921, and in those
rytides marcellus) years completed his medical training and quali-
Turkey Oak (Quercus laevis), Banded Hairstreak (Saty- fied with the degrees of M.R.C.S. and L.R.C.P.
rium calanus) However, his attendance was disrupted by service
Virginia Peppergrass (Lipidium virginicum), Checkered in World War I, during which he was stationed in
White (Pontia protodice), Great Southern White Iraq (Mesopotamia) and Iran (northwestern
(Ascia monuste), Cabbageworm (Pieris rapae) Persia). He concluded those studies in 1921, with
Virginia Snakeroot (Aristolochia serpentaria), Pipevine a diploma in tropical medicine and hygiene. Then,
684
B Byrrhidae

he accepted an appointment to the government of Reference

Palestine (which later became Israel) as entomol-
ogist, and worked there for two years. Next, he Hall WJ (1956) The presidents remarks. Proceedings of the
joined a medical and scientific expedition to Royal Entomological Society of London (C) 20:7377
Samoa. From the expedition resulted his publica-
tions Researches in Polynesia and Melanesia;
and Insects of Samoa. In 1925, he was appointed
Byrrhidae
director of the Department of Entomology of the
A family of beetles (order Coleoptera). They com-
London School of Hygiene and Tropical Medi-
monly are known as pill beetles.
cine, and from 1931 he also held the chair of medical
Beetles
entomology in the University of London. He took
numerous trips to Africa to work on Glossina and
sleeping sickness, and from these visits resulted Byturidae
his (1948) Memoirs on trypanosomiasis in east-
ern Africa; and (1955) History of tsetse flies. He A family of beetles (order Coleoptera). They com-
was elected a fellow of The Royal Society in 1947. monly are known as fruitworm beetles.
He died in 1956. Beetles
C

Cabbage Aphid, Brevicoryne Depending on the temperature and humidity

brassicae (L.) (Hemiptera: conditions, one cabbage aphid generation develops
Aphididae) in 710 days.
Cabbage aphid is monoecious, its host range
Beata Gabrys consisting primarily of plants in the family Bras-
University of Zielona Gora, Poland, Zielona Gora sicaceae (=Cruciferae) in summer as well as in
winter, including such important crops as oilseed
Apterous females (called apterae) are green-yellow rape and cabbage vegetables (head cabbage, Brus-
or greyish-green, with a dark head and two rows sels sprouts, cauliflower, kale, collards). The host
of dark spots dorsally on the thorax and abdomen. plants may be divided into three groups depend-
The body is covered with a thick greyish-white or ing on their ability to support aphid populations:
bluish mealy wax (Fig.1). The siphunculi (corni- permanent, temporal, and accidental host plants.
cles) are small and dark. The body is 1.62.6 mm Permanent host plants support the cabbage aphid
long. Winged females (called alatae) are green, population throughout the whole vegetation
with the head and ventral side black, and black period. A female may give birth to about 20
transverse bars on dorsal abdomen. The wax layer nymphs (larvae) in 10 days on these plants (e.g.,
is thinner in the alatae than in the apterae. The Brassica napus L., B. oleracea L., Sinapis alba L.).
body is 1.62.8 mm long. Males are winged. The Temporal host-plants support 23 aphid genera-
number of chromosomes is 2n=16. tions. A female feeding on temporal host plants
Cabbage aphid occurs throughout all the produces about ten larvae in 10 days (such plants
temperate and warm temperate parts of the world. as Lepidium sativum L., Isatis tinctoria L.). On
B. brassicae lives in colonies that can contain accidental host-plants, aphids may develop less
hundreds to several thousand densely packed than one generation (e.g., Thlaspi arvense L. (10
individuals. larvae/10 days/female), Capsella bursa-pastoris
The type of cabbage aphid life cycle depends (L.) Med. (5 larvae/10 days/female), Lunaria annua
on the climatic conditions during winter. In colder L. (4 larvae/10 days/female), Erysimum cheiran-
regions it is holocyclic (sexual forms winged thoides L. (0 larvae/10 days/female).
males and apterous oviparous females (oviparae) Older nymphs and adult apterae leave plants
appear in autumn; females release a sex phero- in response to overcrowding and decline in plant
mone, nepetalactone, and after mating they lay quality; they move within a plant or between plants
overwintering eggs). Where the winter is mild, via touching stems or the soil. Winged morphs
they are anholocyclic (aphids reproduce parthe- appear following overcrowding and decline in
nogenetically the year round). Parthenogenetic plant quality, or in reaction to environmental
females are viviparous (they give birth to nymphs). factors such as temperature (below 1015C for at
686
C Cabbage Aphid, Brevicoryne brassicae (L.) (Hemiptera: Aphididae)

Cabbage Aphid, Brevicoryne brassicae (L.) (Hemiptera: Aphididae), Figure 1 Cabbage aphids on cabbage
leaf. Note white waxy exudates on aphid bodies.

least 24 h), and seasonal changes in day length While on the plant surface, B. brassicae is rela-
(photoperiod). Overcrowding alone is not respon- tively unaffected by mechanical barriers. However,
sible for appearance of winged forms in cabbage exceptionally dense hairs can protect plant parts
aphid colonies. against aphid infestation. Epicuticular wax struc-
During flight, cabbage aphid responds to ture also is important; cabbage aphids drop off
physical and chemical stimuli. Shape, size, and smooth surfaces. Glucosinolates typical of a given
density of plants, as well as light of high intensity plant species, and n-alkane mixture in epicuticular
(especially wavelengths of 550590 nm) are sig- waxes present on the plant surface, can be recog-
nificant cues. Particularly important is the contrast nized by cabbage aphids. It is not clear whether
between light reflected from bare soil and plants. these chemicals bear any importance in host selec-
Summer migrants do not respond to host plant tion. The existence of external contact chemore-
volatiles from large distances; however, they do ceptors at the tips of aphid antennae is not well
react positively to host plant volatiles in close documented. It is assumed that aphids tend to ini-
proximity, especially the volatile products of tiate stylet probes into plant tissues regardless of
glucosinolate breakdown. the nature of surface chemicals. Landing on an
 Cabbage Looper, Trichoplusia ni (Hbner) (Lepidoptera: Noctuidae)
C 687

unsuitable plant motivates cabbage aphids for new mechanism for this toxicity may be binding of lectin
flights. Flight muscle autolysis occurs several days to chitinous structures in the stylets and foregut.
after settling and the start of reproduction. Cabbage aphid may reduce plant growth by
When probing (i.e., inserting and moving the 35%, the number of side branches by 43%, and the
stylets within plant tissues), cabbage aphid selects oil content by over 10%. Aphids may cause 85%
for high turgor and high amino acid, sucrose, and yield loss and may induce the increase in glu-
glucosinolate content in young and growing plant cosinolate content in rapeseed. Content of certain
parts of its host plants. When aphid stylets are in amino acids (e.g., methionine) increases in phloem
peripheral tissues (epidermis and mesophyll), the sap due to cabbage aphid feeding. B. brassicae
continuation of probing depends on detection of transmits about 20 plant viruses.
chemical stimulants glucosinolates in mesophyll The natural enemies of the cabbage aphid are
cells. Aphids are able to sample mesophyll cell con- primarily generalist insect predators such as Coc-
tent during brief cell punctures along the stylet path- cinellidae and Carabidae (Coleoptera), Syrphidae
way. Feeding deterrents may impede stylet (Diptera), Chrysopidae (Neuroptera), and parasi-
penetration at epidermis and parenchymatous tis- toids. There is only one primary parasitoid species
sues as well as at vascular tissue level. When aphid of B. brassicae Diaeretiella rapae (Mc Intosh)
stylets are in vascular tissues (phloem and xylem), (Hymenoptera, Aphidiidae). It may reduce aphid
cabbage aphid responds positively to a high content populations by 3040% at the peak infestation.
of amino-acid nitrogen, and at the same time it is Crucifer Pests and their Management
relatively resistant to its loss. High nitrogen fertiliza-
tion of soil promotes cabbage aphid population
development under field conditions. The develop- References
ment of B. brassicae is positively correlated with
treonine, tyrosine, alanine, leucine, and glutamic Gabrys B (1999) Semiochemicals in the biology and ecology
acid content, and negatively correlated with pheny- of the cabbage aphid Brevicoryne brassicae (L.). Zeszyty
Naukowe Akademii Rolniczej we Wroclawiu. Rozprawy.
lalanine content. A minimum of 15% sucrose con- CLXIV. 356. 84 pp
tent stimulates feeding by the cabbage aphid. Such Hafez M (1961) Seasonal fluctuations of population density of
concentrations occur in phloem sap of growing the cabbage aphid, Brevicoryne brassicae (L.) in the Neth-
leaves. Among plant allelochemicals, the glucosino- erlands and the role of its parasite, Aphidius (Diaeretiella)
rapae (Curtis).Tijdscrift vor Plantenziekten 67:445548
lates are very strong phagostimulants for the cab- Klingauf FA (1987) Host plant finding and acceptance. In:
bage aphid. In phloem sap of young leaves, the Minks AK, Harrewijn P (eds) Aphids, their biology, nat-
glucosinolate concentration reaches 10 mM. How- ural enemies and control, vol 2B. Elsevier, Amsterdam,
pp 209223
ever, most glucosinolates do not have direct effect on
Markkula M (1953) Biologisch-kologische Untersuchungen
aphid performance. Cabbage aphid fecundity is pos- uber die Khlblattlaus, Brevicoryne brassicae. (L.) (Hem.,
itively correlated with some alkenyl glucosinolates Aphididae) Ann Soc Zool Bot Fenn Van 15:1133
(e.g., progoitrin, sinigrin) content, and a negative Nault LR, Styer WE (1972) Effect of sinigrin on host selection
by aphids. Entomol Exp Appl 15:423437
correlation is found for indole ones (e.g., glucobras-
sicanapin, neoglucobrassicin). Glucosinolate metab-
olism in the aphid is not known. Some amount of
the ingested glucosinolates is sequestered in cabbage Cabbage Looper, Trichoplusia ni
aphid hemolymph. The glucosinolates may also be (Hbner) (Lepidoptera:
hydrolyzed by endogenous aphid myrosinases Noctuidae)
(aphid myrosinases are not identical with plant
myrosinases). High lectin content in the phloem sap The cabbage looper is found in many crucifer-
causes high mortality of B. brassicae. The possible growing areas of the world, including parts of
688
C Cabbage Looper, Trichoplusia ni (Hbner) (Lepidoptera: Noctuidae)

Africa, Asia, Europe and North America. However, back to form a loop and then projecting the front
overwintering occurs only in warm-winter regions. section (Fig.3) of the body forward. The mature
The cabbage looper is highly dispersive, and adults larva is predominantly green, but is usually marked
have sometimes found at high altitudes and far with a distinct white stripe on each side. The tho-
from shore. Flight ranges of approximately 200 km racic legs and head capsule are usually pale green
have been estimated. or brown. Dorsally, the larva bears several narrow,
faint white stripes clustered into two broad white
bands. In some cases the mature larva is entirely
Description and Life Cycle green. The body is narrower at the anterior end,
and broadens toward the posterior. It measures
The number of generations completed per year var- 34 cm in length at maturity. Head capsule width
ies from two to three in cool-summer climates to is 0.29, 0.47, 0.74, 1.15, and 1.79 mm, respectively,
several overlapping generations in warmer climates. for instars one through five. Larval development
Development time (egg to adult) requires 1825 generally requires 1920 days.
days when insects are held at 3221C, respectively,
so at least one generation per month could be com-
pleted successfully under favorable weather condi- Pupa
tions. There is no diapause present in this insect,
and although it is capable of spending considerable At pupation, a white, thin, fragile cocoon in
time as a pupa, it does not tolerate prolonged cold formed on the underside of foliage, in plant debris,
weather. It reinvades most temperate regions annu- or among clods of soil. The pupa measures about
ally after overwintering in warmer latitudes. In the 2 cm in length. Duration of the pupal stage
eastern United States, overwintering regularly is about 4, 6, and 13 days at 32, 27, and 20C,
occurs only in the southern half of Florida. respectively.

Egg Adult

Cabbage looper eggs are hemispherical in shape, The forewings of the cabbage looper moth are
with the flat side affixed to foliage. They are depos- mottled gray-brown in color; the hind wings are
ited singly on either the upper or lower surface of light brown at the base, with the distal portions
the leaf, although clusters of six to seven eggs are dark brown (Fig. 2). The forewing bears silvery
not uncommon. The eggs are yellowish white or white spots centrally: a U-shaped mark and a
greenish in color, bear longitudinal ridges, and circle or dot that are often connected. The fore-
measure about 0.6 mm in diameter and 0.4 mm in wing spots, although slightly variable, serve to
height. Eggs hatch in about 25 days. distinguish cabbage looper from most other
crop-feeding noctuid moths. The moths have a
wingspan of 3338 mm. During the adult stage,
Larva which averages 1012 days, 300600 eggs are
produced by females. Moths are considered to be
Young larvae initially are dusky white, but become seminocturnal because feeding and oviposition
pale green as they feed on foliage. They are some- sometimes occurs about dusk. They may become
what hairy initially, but the number of hairs active on cloudy days or during cool weather, but
decreases rapidly as larvae mature. Larvae have are even more active during the nighttime
three pairs of prolegs, and crawl by arching their hours.
 Cabbage Looper, Tricoplusia ni (Hbner) (Lepidoptera: Noctuidae)
C 689

dogbane, Apocynum spp.; sunflower, Helianthus

spp.; and others.

Damage

Cabbage loopers are leaf feeders, and in the first

three instars they confine their feeding to the lower
leaf surface, leaving the upper surface intact. The
fourth and fifth instars chew large holes, and usu-
ally do not feed at the leaf margin. In the case of
Cabbage Looper, Trichoplusia ni (Hbner) cabbage, however, they feed not only on the wrap-
(Lepidoptera: Noctuidae), Figure 2 Adult of per leaves, but also may bore into the developing
cabbage looper, Trichoplusia ni. head.

Natural Enemies

The cabbage looper is attacked by numerous natu-

ral enemies, and the effectiveness of each seems
tovary greatly. Most studies note the effectiveness
of wasp and tachinid parasitoids, and a nuclear
Cabbage Looper, Trichoplusia ni (Hbner)
polyhedrosis virus (NPV). During the latter instars,
(Lepidoptera: Noctuidae), Figure 3 Cabbage
Voria ruralis (Fallen) (Diptera: Tachinidae), a soli-
looper larva.
tary or gregarious endoparasite attacking the
medium or large size larvae, often is the dominant
Host Plants cause of death, accounting for an average of about
53% mortality. Trichoplusia ni NPV causes about
The cabbage looper feeds on a wide variety of 12% mortality, and undetermined fungi about 10%.
cultivated plants and weeds. As the common Copidosoma truncatellum (Dalman) (Hymenoptera:
name implies, it feeds readily on crucifers, and Encyrtidae) is the other significant mortality factor,
has been reported damaging broccoli, cabbage, but accounted for only six to seven percent mortal-
cauliflower, Chinese cabbage, collards, kale, mus- ity. Other studies reported that egg parasitism of
tard, radish, rutabaga, turnip, and watercress. cabbage looper by Trichogramma (Hymenoptera:
Other vegetable crops injured include beet, can- Trichogrammatidae), while variable, could reach
taloupe, celery, cucumber, lima bean, lettuce, about 35%. Despite the abundance of parasitoids,
parsnip, pea, pepper, potato, snap bean, spinach, however, T. ni NPV is usually considered the key
squash, sweetpotato, tomato, and watermelon. factor affecting populations. Early signs of larval
Additional hosts are flower crops such as chry- infection by NPV are a faint mottling of the abdo-
santhemum, hollyhock, snapdragon, and sweet- men in the area of the third to the sixth abdominal
pea, and field crops such as cotton and tobacco. segments. This is followed by a more generalized
Surprisingly few common agricultural weeds blotchy appearance, and the caterpillar eventually
arefrequent hosts. Adults feed on nectar from a becomes creamy white in color, swollen, and limp.
wide range of flowering plants, including clover, Caterpillars die within 57 days of contracting
Trifolium spp.; goldenrod, Solidago canadensis; thedisease.
690
C Cabbage Maggot or Cabbage Root Fly, Delia radicum (Linnaeus) (Diptera: Anthomyiidae)

Management thrives under cool conditions, and rarely is reported

to be a pest south of about latitude 45 degrees
Blacklight traps and pheromone traps have been north, and when it is, it usually occurs at a high
used in an attempt to predict looper population elevation. Quite cold tolerant, it is found in some of
densities. Pheromone releasers and blacklight the northernmost agricultural regions.
traps can be combined to increase moth catches.
Insecticide resistance has become a problem in
cabbage looper control, but susceptibility varies Life History
widely among populations. Bacillus thuringiensis
has long been used for effective suppression of The number of generations occurring annually
cabbage looper, and has the advantage of not dis- varies from one in the far north to three in optimal
rupting populations of beneficial insects. climates, although there are occasional reports of
Crucifer Pests and their Management four generations. The generations may overlap
Vegetable Pests and their Management considerably. A developmental threshold of about
6C has been determined for most life stages. The
time required for a complete generation is esti-
References mated at 4060 days.
Eggs normally are laid in the soil around the
Capinera JL (2001) Handbook of vegetable pests. Academic stem of cruciferous plants, but sometimes eggs are
Press, San Diego, 729 pp deposited directly on the stem of plants. The elon-
Elsey KD, Rabb RL (1970) Analysis of the seasonal mortality
of the cabbage looper in North Carolina. Ann Entomol
gate eggs are white in color, and taper markedly at
Soc Am 63:15971604 both ends, but one end is more blunt than the
McEwen FL, Hervey GER (1960) Mass-rearing the cabbage other. One side of the egg is flattened or slightly
looper, Trichoplusia ni, with notes on its biology in the concave, with the opposite side convex. Eggs mea-
laboratory. Ann Entomol Soc Am 53:229234
Oatman ER, Platner GR (1969) An ecological study of insect sure about 1.1 mm long and 0.34 mm wide. The
populations on cabbage in southern California. Hilgardia eggs are often laid in clumps of a few eggs, but
40:140 sometimes hundreds of eggs are found at the same
Shorey HH (1963) The biology of Trichoplusia ni (Lepi-
location, evidence that more than one female may
doptera: Noctuidae). II. Factors affecting adult fecundity
and longevity. Ann Entomol Soc Am 56:476480 oviposit at the same spot. Females commonly pro-
Shorey HH, Andres LA, Hale RL (1962) The biology of duce 300400 eggs during their life span of 3060
Trichoplusia ni (Lepidoptera: Noctuidae). I. Life history days. Eggs hatch in 35 days, averaging about 3.5
and behavior. Ann Entomol Soc Am 55:591597
days at 20C.
There are three instars. The length of the
mouthparts (cephalopharyngeal skeleton) can be
Cabbage Maggot or Cabbage used to differentiate instars, with mean lengths of
Root Fly, Delia radicum (Linnaeus) 0.44, 0.80, and 1.24 mm, respectively. The larvae
(Diptera: Anthomyiidae) are white in color and attain lengths of about 1.5,
3.7, and up to 8 mm, respectively. The mouth hooks
John L. Capinera are black. Located immediately behind the head is
University of Florida, Gainesville, FL, USA a pair of brownish fan-like spiracles, each of which
is divided into about 12 lobes. Larvae feed exter-
Cabbage maggot (cabbage root fly) is known as a nally and internally on roots, and internally on
pest throughout the northern hemisphere. It appar- stem tissue. The larval period requires about 1822
ently was introduced accidentally from Europe to days under field conditions, but development time
North America in the early 1800s. Cabbage maggot may be altered by weather. Exposure of first and
 Cabbage Maggot or Cabbage Root Fly, Delia radicum (Linnaeus) (Diptera: Anthomyiidae)
C 691

second instar larvae to cool temperatures or short on the thorax, but these markings are less distinct
photoperiods seems to induce diapause in the on the female. The flies are quite bristly, and mea-
pupal stage. sure 57 mm long. Adults feed on nectar from
The puparium is oval, bluntly rounded at both flowering plants. If they obtain adequate food they
ends, and brown in color. The average length is 5.5 may persist for 24 weeks, whereas they perish in
mm, with a range of 3.56.5 mm. The duration of 23 days if denied food. Adults are highly attracted
the prepupal stage is about 35 days, and the pupa to crucifers for oviposition. The preoviposition
requires 1225 days during the summer. However, period of adults is about 6 days.
this is the overwintering stage, so it is prolonged Cabbage maggot commonly attacks crucifer-
for 58 months in the overwintering generation(s). ous vegetable crops, including broccoli, Brussels
Overwintering pupae require at least 22 weeks of sprouts, cabbage, cauliflower, collard, kale, kohlrabi,
temperatures < 6C to complete diapause develop- mustard, radish, rutabaga, turnip, and watercress.
ment. The puparia from the summer generations It has been reported from noncrucifer crops on
are usually found in the soil immediately adjacent occasion, but these are misidentifications that stem
to the root on which the larvae last fed. Sometimes from the difficulty in accurately identifying this fly.
they occur within the plant tissue, including the Cruciferous weeds apparently do not play a signifi-
aboveground stem tissue. Aestivation occurs in cant role in the biology of this insect; although
response to warm temperatures, above 20C, and some appear to be suitable hosts, they rarely are
especially in response to hot temperatures, mentioned in the economic entomology literature.
2730C. In preparation for overwintering, the Important natural enemies include staphylin-
larvae seem to disperse further from the plant, and ids of several genera, particularly Aleochara sp.
deeper into the soil. Overwintering puparia may (Coleoptera: Staphylinidae); a wasp, Trybliographa
be found 1215 cm from the plant, and commonly rapae (Westwood) (Hymenoptera: Eucoilidae);
are found in the soil at a depth of 10 cm. and a mite, Trombidium sp. (Acari: Trombidiidae).
The adults are dark with gray markings (Fig. 4). Aleochara sp. attack the pupal stage of cabbage
The male bears three blackish longitudinal bands maggot, Trybliographa attacks the larvae, and the
mite destroys the eggs.
Natural control has been studied extensively
in both Europe and North America. Egg predation
by staphylinids and carabids may reach 9095%
annually. Aleochara are very effective predators,
but become active too late in the spring to have
much effect on first generation cabbage maggot.
Trybliographa is fairly effective at high host densi-
ties, often parasitizing in excess of 50% of available
hosts. Other natural enemies of the immature
cabbage maggot include numerous hymenopter-
ous parasitoids of questionable economic impor-
tance, carabids (Coleoptera: Carabidae) and ants
(Hymenoptera: Formicidae). General predators
undoubtedly attack the adults, but they are not
Cabbage Maggot or Cabbage Root Fly, Delia considered to be important.
radicum (Linnaeus) (Diptera: Anthomyiidae), Fungi are commonly observed infecting flies.
Figure 4 Adult cabbage maggot (cabbage root Entomophthora muscae and Strongwellsea castrans
fly), Delia radicum (Linnaeus). cause epizootics among adults during wet weather,
692
C Cabbage Maggot or Cabbage Root Fly, Delia radicum (Linnaeus) (Diptera: Anthomyiidae)

and though impressive, act too late to prevent early damage results in severe crop loss, and in this case
season crop damage. the autumn generation may be quite important.
The spring generation tends to appear consis- The summer generation causes little damage.
tently, but latter generations are greatly influenced Damage tends to be greater on loamy sand soil
by weather. Rain and cool weather may decrease than on sand or clay soil, but as a general rule light
egg production and egg predation, and cause star- soils are more problem prone.
vation of flies, but optimal egg production is asso- Although most eggs are laid on the soil, a
ciated with temperatures of 1821C, which small number are sometimes deposited on plant
corresponds well with the weather occurring dur- tissue, resulting in injury by larvae to leaflets, espe-
ing most spring generations. Pupal development is cially to Brussels sprout buttons. Occasionally the
particularly susceptible to delay caused by hot growing points of plants are attacked, resulting in
temperatures, which normally is associated with multiple heads.
summer generations. Dry soil is lethal to eggs.

Management
Damage
Adult flight periods can be monitored by using
Larvae (Fig.5) damage crucifers by feeding on the cone screen traps baited with crucifers. Baits are
roots and, to a much lesser degree, the stems or more effective than yellow sticky traps, although
petioles of plants. Damage to leaf crops such as sticky trap captures are correlated with egg
cabbage is most evident in the late spring; signs of deposition rates. Horizontal surfaces are more
feeding damage are initially seen as drooping or suitable than vertical surfaces for landing by flies.
wilting of a few leaves, and then perhaps the entire Dispensers that release isothiocyanates, naturally
plant. Delayed maturity and stunting are common occurring odors released by crucifers, can be used
responses to root maggot injury. Plant death often as lures. Color, but not leaf pattern, also can influ-
coincides with drought or water stress, when the ence host selection. Water traps baited with iso-
injury to roots is fully expressed. When plants are thiocyanate can be used to monitor population,
small, five to ten maggots are necessary to kill the but trap catches do not predict egg numbers
seedling. However, later in the season densities of accurately.
100 maggots or more may be supported satisfacto- Flight activity can be predicted from thermal
rily if the plant has adequate water. unit accumulations. The overwintering (partly
Cabbage maggot larvae feed on the rootlets or developed) generation require about 300 day-
feeder roots, but invariably move to the main or degrees (above a base temperature of 43F). Subse-
tap root as they mature. They scar the surface and quent generations require about 1200 degree-days.
burrow into the root. In the case of crops that are With the introduction of chlorinated hydro-
harvested for their root, such as radish and turnip, carbon insecticides, damage by cabbage maggot
was greatly reduced. Long-lasting insecticides,
applied to the soil at planting, protect the roots
from larvae. This remains the principal method of
plant protection in commercial crucifer produc-
tion, but the insecticides have been changed over
Cabbage Maggot or Cabbage Root Fly, Delia time as resistance to insecticides developed. Loss
radicum (Linnaeus) (Diptera: Anthomyiidae), of insecticide efficacy is due not only to selection
Figure 5 Mature cabbage maggot (larva of for insecticide resistant insects, but enhanced
cabbage root fly), Delia radicum (Linnaeus). degradation of insecticide by soil microbes.
 Cabbageworm, Pieris rapae (Linnaeus) (Lepidoptera: Pieridae)
C 693

Insecticides are typically applied as a granular Heterorhabditidae) have been evaluated for sup-
formulation over the seed bed or incorporated pression of larvae. Although heterorhabditid nema-
into the soil, or as a liquid drench. Foliar applica- todes are attracted to cabbage maggot larvae and
tions are sometimes made to suppress adults. pupae, under field conditions they have not been
Foliar application of insecticides, timed according shown to be effective. Steinernematid nematodes
to temperature accumulations, can be superior to provide some suppression of cabbage maggot larvae
soil applications or calendar-based sprays. Seed in pot and field trials, but very high densities of
treatment can be an effective method of providing nematodes are needed, at least 100,000 nematodes
protection to seedlings, but it does not work well per plant. This is not entirely surprising because fly
for all insecticides. Naphthalene has been investi- larvae are less susceptible to nematodes than are
gated in Europe for repellency to ovipositing flies; many other insects. In Europe, the potential of using
although good protection occurs for about 6 the predatory beetle Aleochara bilineata (Gyllenhal)
weeks, the cost of application is high. (Coleoptera: Staphylinidae) to achieve biological
Modification of planting and tillage practices suppression of cabbage maggot is being studied;
is often recommended for reduction in cabbage while technically feasible, the costs thus far are high.
maggot damage. Delayed planting is reported to Despite the common name, cabbage is less
allow the young plants to escape oviposition by the attractive to cabbage maggots than some other
spring adults. Sanitation also is quite important, as crucifer crops. Chinese cabbage, mustard, ruta-
the roots and stems of crucifers left in the field can baga, and turnip tend to be more severely injured
be very suitable for autumn and early spring gen- than cabbage. There also is some variation within
erations of cabbage maggot. Crop residues should vegetable crops in resistance to attack; fast grow-
be deeply buried, or pulled and allowed to dry ing varieties seem most injured. Overall, not much
completely. High plant densities are more attractive progress has been made on finding cultivars resis-
than low densities to flies, but because there are tant to cabbage maggot.
more plants on which to distribute the eggs, yield Crucifer Pests and their Management
may be equivalent at both plant densities. Intro- Vegetable Pests and their Management
ducing diversity into the landscape, as by under-
sowing portions of a crucifer crop with clover, will
disturb the normal host orientation pattern and References
reduce oviposition. Similarly, single row intercrop-
ping of crucifers with unrelated plants will greatly Capinera JL (2001) Handbook of vegetable pests. Academic
Press, San Diego, 729 pp
reduce the oviposition rate on crucifers.
Finch S (1989) Ecological considerations in the management
Physical manipulations of the crop environ- ofDelia pest species in vegetable crops. Ann Rev Entomol
ment also assist pest suppression. Crops covered 34:117137
tightly with row covers escape injury by cabbage Finch S (1993) Integrated management of the cabbage root fly
and the carrot fly. Crop Protection 12:423430
maggot. Tar paper or cardboard discs, or collars Fulton BB (1943) The cabbage maggot in North Carolina.
made of other weather-resistant material, placed North Carolina. Agr Exp Stn Bull 335, 24 pp
around the stem of seedlings have long been
recommended as a physical barrier to reduce the
ability of females to deposit eggs at the soil-stem Cabbageworm, Pieris rapae
interface. A precise fit is required, however, or the (Linnaeus) (Lepidoptera: Pieridae)
flies will circumvent the barrier.
Reliable biological control techniques have The cabbageworm occurs in temperate regions
not yet been developed. Entomopathogenic around the world, and is easily confused with
nematodes (Nematoda: Steinernematidae and other common cabbage white butterflies. In most
694
C Cabbageworm, Pieris rapae (Linnaeus) (Lepidoptera: Pieridae)

temperate areas, it is a serious pest if insecticides about 15 days to complete its development during
are not used to protect cabbage. In North America, August. Average development times for each instar
it is known as the imported cabbageworm because at 19C was observed to be 4.5, 3.0, 3.3, 4.1, and 7.8
it is an invader; in Europe it is known as the small days, respectively. All larval stages except the first
white cabbage butterfly. instar bear a narrow yellow line running along the
center of the back; this stripe is sometimes incom-
plete on the early instars. A broken yellow line, or
Life Cycle and Description series of yellow spots, also occurs on each side.

The complete life cycle of this insect requires 36

Pupa
weeks, depending on weather. The number of gen-
erations reported annually is two to three in cool
Pupation normally occurs on the food plant. The
climates such as Canada, increasing to six to eight
chrysalis is about 1820 mm in length, and varies
in southern areas.
in color, usually yellow, gray, green and speckled
brown. A sharply angled, keel-like projection is
evident dorsally on the thorax, and dorsolaterally
Egg
on each side of the abdomen. At pupation, the
chrysalis is anchored by the tip of the abdomen to
Eggs are laid singly, usually on the lower surface of
the silk pad, and a strand of silk is loosely spun
outer leaves of plants. The egg measures 0.5 mm in
around the thorax. Pupation during the summer
width and 1.0 mm in length, and initially is pale
generations lasts about 11 days. The chrysalis is
white in color but eventually turns yellowish. The
the overwintering stage, however, so its duration
egg is laid on end, with the point of attachment
may be prolonged for months. The proportion of
flattened and the distal end tapering to a blunt
pupae that diapause increases as autumn pro-
point. The shape is sometimes described as resem-
gresses, so that at the time of the final generation
bling a bullet.
all pupae are in diapause.

Larva Adult

The larva is green, velvety in appearance (Fig.6), Upon emergence from the chrysalis the butterfly
and bears five pairs of prolegs. There are five has a wingspan of about 4.56.5 cm. It is white above
instars. Head capsule widths are about 0.4, 0.6, with black at the tips of the forewings. The front
0.97, 1.5, and 2.2 mm, respectively. Body lengths at wings are also marked with black dots: two in the
maturity of each instar averages 3.2, 8.8, 14.0, 20.2, central area of each forewing in the female, and one
and 30.1 mm, respectively. The larva requires in case of males (Fig.7). When viewed from below,
the wings generally are yellowish, and the black spots
usually show faintly through the wings. The hind
wing of each sex also bears a black spot on the ante-
rior edge. The body of the butterfly is covered with
dense hair, which is colored white in females, but
darker in males. The adult typically lives about
Cabbageworm, Pieris rapae (Linnaeus) 3 weeks. The female produces 300400 eggs. The
(Lepidoptera: Pieridae), Figure 6 Larva of adult is very active during the daylight hours, often
cabbageworm, Pieris rapae. moving from the crop to flowering weeds to feed.
 Cabbageworm, Pieris rapae (Linnaeus) (Lepidoptera: Pieridae)
C 695

glomeratus (L.) (Hymenoptera: Braconidae) attacks

the early instars, and emerges from the mature
larva as it prepares to pupate. A. glomeratus is read-
ily observed in the field, searching diligently on
foliage for larvae. Dead cabbageworm larvae are
often found with clusters of 2030 A. glomeratus
cocoons attached. In some areas tachinids (Dip-
tera: Tachinidae) are more important than wasps.
Virus and fungal diseases of imported cab-
bageworm have been reported, but the predomi-
Cabbageworm, Pieris rapae (Linnaeus)
nant natural disease in a granulosis virus (GV).
(Lepidoptera: Pieridae), Figure 7 Adult of
P. rapae GV occurs most commonly under high
cabbageworm.
density conditions, and often among late instar
larvae after they have consumed the exterior foliage
Damage of plants and are forced into close contact. Over
90% mortality of larvae due to natural occurrence
Cabbageworms feed on foliage, and if left of this disease has been reported. In the early
unchecked often will reduce mature plants to stages of infection, larvae are inactive and paler in
stems and large veins. Although they prefer leafy color. As the disease progresses, the caterpillar
foliage, larvae may burrow into the heads of broc- body turns yellow, and tends to appear bloated.
coli and cabbage, especially as they mature. Larvae After death, the body blackens, the integument
are often immobile, and difficult to dislodge, and ruptures, and the liquefied body contents ooze on
may be overlooked when cleaning produce. Lar- the plant foliage. Rainfall has a major roll in assist-
vae produce copious quantities of fecal material ing the spread of the virus on the plant, and from
which also contaminate and stain produce. the soil to the plant.

Host Plants Management

Larvae of this insect feed widely on plants in the Imported cabbageworm are readily killed by foliar
family Cruciferae, but occasionally on a few other application of insecticides, including the bacterial
plant families that contain mustard oils. Com- insecticide Bacillus thuringiensis. Crucifer crops
monly attacked are vegetable crops such as broc- differ is their susceptibility to attack by imported
coli, Brussels sprouts, cabbage, cauliflower, collard, cabbageworm. Chinese cabbage, turnip, mustard,
horseradish, kale, and kohlrabi. Also sometimes rutabaga, and kale are less preferred than cabbage,
attacked are flowers such as nasturtium and sweet collards, Brussels sprouts, broccoli, and cauliflower.
alyssum, and weeds in the family Cruciferae. Some cultivars of certain crops also have moder-
Adults sip nectar from flowers, and are commonly ate levels of resistance to infestation by imported
seen feeding at a number of plants. cabbageworm. Cabbage butterflies avoid oviposit-
ing on red cabbage varieties. However, larval sur-
vival is favored by red cabbage, so red varieties
Natural Enemies are not a satisfactory solution to the caterpillar
problem.
The imported cabbageworm is subject to numer- Crucifer Pests and their Management
ous predators, parasitoids, and diseases. Apanteles Vegetable Pests and their Management
696
C Cactus Flies

References followed by southern California. Despite attempts

to prevent migration to the valuable cactus grow-
Capinera JL (2001) Handbook of vegetable pests. Academic ing regions in Mexico, Cactoblastis was found in
Press, San Diego, 729 pp Isla Mujeres, Mexico, in August 2006. Over
Chittenden FH (1916) The common cabbage worm. USDA
Farmers Bull 766, 16 pp
250,000 ha are cultivated in Mexico producing
Harcourt DG (1963) Biology of cabbage caterpillars in east- annual economic revenue of about $50 million
ern Ontario. Proc Entomol Soc Ontario 93:6175 (19901998).
Richards OW (1940) The biology of the small white butterfly Although the importations into Australia and
(Pieris rapae. ), with special reference to the factors con-
trolling its abundance. J Anim Ecol 9:243288 the invasion into the USA and Mexico occurred
many years apart, the Cactoblastis moth has now
become a cautionary example in the practice of
biological control. Research on the moth has
Cactus Flies shifted from mass release to control. Here, we
attempt to summarize the current state of knowl-
Members of the family Neriidae (order Diptera). edge on the biology, distribution and control
Flies methods against Cactoblastis.

Cactus Moth, Cactoblastis Biology

cactorum (Berg) (Lepidoptera:
Pyralidae) Like other cactus-feeding moths, the Cactoblastis
female lays its eggs (Fig.8) on top of each other to
jesusa c. legaspi, benjamin c. legaspi jr. form an eggstick, often averaging 60100 eggs
USDA-ARS, FAMU-Center for Biological per eggstick. Young larvae burrow into the cactus
Control, Tallahassee, FL, USA cladode through a single entry hole, negating the
USDA-ARS, FAMU-Center for Biological effect of the cactus secretions. Larvae feed collec-
Control, Tallahassee, FL, USA tively within the cladode for about 2 months in the
summer and four in the winter. Afterwards, the
The cactus moth became a textbook example of larvae exit the plant to pupate in the leaf litter or
successful classical biological control after it was soil. Adult lifespan is short, about 9 days, or rang-
imported from Argentina into Australia in 1926 to ing from about 5 days at 34C to about 12 days at
control invasive Opuntia cacti. To date, the moth 18C in females. Sex ratios are typically 1:1.
continues to play an active role in controlling Depending on climate and season, Cactoblastis
Opuntia in Australia. In 1989, Cactoblastis was undergoes 23 generations per year. In South
found in Florida (USA), subsequently spreading Africa, summer and winter generation times are
northward to South Carolina and westward to 113132 days and 234256 days, respectively. In
Alabama by 2004. The arrival of the moth in the Australia, summer and winter generation times
United States was cause for concern in the cactus are 100120 and 235265 days, respectively. Under
industry. In the United States, cacti are grown laboratory conditions, generation time ranges
primarily as ornamentals in Arizona, California, from 67 days at 30C to 185 days at 18C. Duration
Nevada, New Mexico, and Texas. Highest nursery of lifestages is generally: egg (50 days); larval
production is in Arizona (wholesale and retail (130180 days); pupal (4070 days). Duration of
values of $4.5 million and $9.5 million, respectively), immature life stages is affected by temperature
 Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae)
C 697

Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), Figure 8 Life cycle of Cactoblastis
cactorum: (a) eggs deposited on a cactus spine, forming an eggstick; (b) larvae hatching from eggs; (c)
mature larvae are strikingly colored orange and black; (d) pupae and a pupal case, with arrows pointing
to the genital slit, a character that can be used to sex the pupae; (e) male (left) and female (right) moths;
(f) a cactus pad hollowed out by feeding of the larvae. Note that the larvae are visible within the pad
(photographs by Ignacio Baez).
698
C Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae)

(Table 1, Fig.9). At 30C, development from eggs the equation: eggs = (11.241 + 0.854T) d exp
to pupae averages 64.8 days, increasing to 179.9 (0.020Td); where T is temperature (C) and d is
days at 18C. Duration of immature life stages was time (days) (Fig.10). The estimated parameters
used to generate adevelopment rate curve (Fig.9) p and q describe how quickly maximal oviposi-
and to calculate a theoretical development thresh- tion is reached as a function of temperature; and
old temperature of13.3C. w how quickly it returns to zero. Net reproduc-
Lifetime fecundity is about 172 eggs on Opun- tive rate (R0), gross reproductive rate (GRR),
tia ficus-indica, compared to 138 on O. aurantiaca generation time (T), intrinsic rate of increase (r),
for the summer generation. Respective values for finite rate of increase (), and doubling time
the winter generation were 177 and 159. Total (DT) were 43.68 females/female, 44.02 females/
fecundity of winter generations ranges from 8897 female, 67.14 days, 0.0562 females/female/day,
in South Africa, and 99125 in Australia, although 1.058 females/female/day, and 12.33 days, res
some estimates for total fecundity are as high as pectively, at 30C. The life history parameters of
200300 eggs per female. Total lifetime fecundity Cactoblastis (Table 2) indicate an insect with
changes with temperature, and ranges from about relatively low reproductive potential and suscep-
12 at 34C to about 100 at 26C. The combined tibility to control measures at the egg stage that
effects of insect age and temperature are shown is exposed for periods of 2048 days, depending
using an Enkegaard oviposition rate surface using on temperature.

Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), Table 1 Immature development of
Cactoblastis cactorum (mean SE; days)
Life stage Temperature (C)
18 22 26 30 34
Eggs 47.900.28 29.600.22 22.500.22 20.900.23 22.900.35
Larvae 78.392.58 61.362.77 33.520.61 29.890.80 30.081.05
Pupae 53.461.52 24.910.14 16.280.51 13.880.66 13.790.67
Complete 179.862.92 115.962.84 72.220.79 64.750.88 67.041.65

Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), Figure 9 Development rate for
Cactoblastis cactorum immatures (eggs to pupae). Development rate was fitted to the logistic e quation
rate=0.0165/(1+(T/20.7093)5.8823
). The linear portion of the curve was used to estimate a lower
development threshold temperature of 13.3C.
 Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae)
C 699

Distribution infested areas, exceeding all expectations of the

Australian government and resulting in collapse
After importation into Australia from Argentina of cactus stands at the original release sites by
in 1926, Cactoblastis moths dispersed throughout 1932. In 1956, Cactoblastis was shipped from South
Africa to the Caribbean island of Nevis where it
established and provided successful biological
control against a complex of native prickly pear
cacti. Successful introductions followed in
Montserrat and Antigua in 1960. Through natural
migration, intentional or unintentional human
action, Cactoblastis has been reported throughout
the Caribbean (or West Indies; including St. Kitts,
the US Virgin Islands, Hispaniola [Haiti], Cuba, the
Dominica Republic, the Bahamas, the Cayman
Islands, Puerto Rico, Barbados), New Caledonia,
Hawaii, Mauritius, St. Helena, and Ascension
Cactus Moth, Cactoblastis cactorum (Berg) Island with varying degrees of establishment and
(Lepidoptera: Pyralidae), Figure 10Enkegaard success against Opuntia. The moth was imported
surface showing simultaneous effects of time into Pakistan and Kenya but apparently failed to
and temperature on mean oviposition rate establish.
(female eggs). The estimated equation is: In 1989, the arrival of Cactoblastis in mainland
eggs=(11.241+0.854T) d exp (0.020Td) North America was documented by reports in
(F=16.96; df=3, 54: P<0.001; R2=0.35). south Florida. Cactoblastis likely entered Florida

Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), Table 2 Life history parameters for
Cactoblastis cactorum at different temperatures
Parameter Temperature (C)
18 22 26 30 34
Net Reproductive 8.550 46.24 49.20 43.68 5.95
Rate (R0)a
Gross Reproductive 9.021 48.22 49.38 44.02 6.16
Rate (GRR)b
Generation Time (T)c 185.54 129.58 75.07 67.14 68.95
Intrinsic Rate of 0.0116 0.0296 0.0519 0.0562 0.0258
Increase (r)d
Finite Rate of 1.0116 1.03 1.053 1.058 1.026
Increase ()e
Doubling Time (DT)f 59.90 23.41 13.32 12.33 26.86

a
R0= lxmx expressed in units of female/female; egg numbers divided by 2 because of 1:1 sex ratio
b
GRR= mx in female/female
c
T=( xlxmx)/R0 in days
d
r=ln R0/T in female/female/day
e
=exp(r) in female/female/day
f
DT=ln (2)/r in days
700
C Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae)

through commercial importations of Opuntia from Cactus Moth, Cactoblastis cactorum (Berg)
the Dominican Republic into Miami. By 1999, Cac- (Lepidoptera: Pyralidae), Table 3 CLIMEX
toblastis had spread northwards and was found parameter file for Cactoblastis
throughout the eastern Florida coastline and as far Param- Description Value
north as Tampa on the western coast. By 2002, the eter
moth had expanded westward to Pensacola, Flor- Temperature Index
ida and northward along the eastern coast to DV0 Lower temperature 9
Charleston, South Carolina. In July, 2004, westward threshold=
migration had reached Dauphin Island, Alabama DV1 Lower optimum temperature 25
and Bull Island, South Carolina (about 80 km north DV2 Upper optimum temperature 30
of Charleston). The westward migration of Cacto-
DV3 Upper temperature threshold 36
blastis in the southeastern United States is esti-
Moisture Index
mated at 160 km/year with arrival at the Texas
border predicted to occur in 2007. The much- SM0 Lower soil moisture 0.1
threshold
dreaded arrival of Cactoblastis in Mexico occurred
in August 2006 on Isla Mujeres, a small island off SM1 Lower optimal soil moisture 0.2
the northeast coast of the Yucatan peninsula in SM2 Upper optimal soil moisture 0.8
Mexico. The method by which Cactoblastis SM3 Upper soil moisture 1.0
migrated into Mexico is unknown, although spec- threshold
ulation centers on winds and hurricanes, or acci- Cold Stress
dental transport via tourists or commercial trade. TTCS Cold stress temperature 9.0
The analysis of insect distributions may be threshold
assisted through the use of bioclimatic models such THCS Cold stress temperature rate 0
as CLIMEX. Bioclimatic models incorporate DTCS Cold stress degree-day 0
known ecological and climatic tolerances of organ- threshold
isms in their native habitats to predict potential DHCS Cold stress degree-day rate 0.0001
distribution or densities in other geographical TTCSA Cold stress temperature 9.0
regions. The twofold process typically consists of threshold (average)
replicating the known distribution of the target THCSA Cold stress temperature rate 1.0
species in its native habitat by estimating biological (average)
and stress parameters using experimental data or Heat Stress
estimates from the literature. Afterwards, the geo- SMDS Dry stress threshold 0.01
graphical area of interest is extended or a new area HDS Dry stress rate 0.1
is chosen where the target species may be intro- Wet stress
duced intentionally, as in a biological control agent,
SMWS Wet stress threshold 1.2
or unintentionally, as in an invasive pest species.
HWS Wet stress rate 0.0015
Temperature index parameters were estimated
using the laboratory data on development time at dif- PDD Degree days per generation 1500
ferent constant temperatures (Table3). The moisture
index parameters were based on those of the Mediter- Predicted and known worldwide distribu-
ranean fruitfly, Ceratitis capitata (Diptera: Tephriti- tions of Cactoblastis are shown together in the
dae), with a native South American distribution similar map. In its native distribution range of Uruguay,
to that of Cactoblastis. The target area of distribution Paraguay, south Brazil and north Argentina, Cac-
was the documented native habitat of Paraguay, Uru- toblastis appears to be limited by cold stress to the
guay, southern Brazil and northern Argentina. south and along the Andes mountain range, and
 Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae)
C 701

by wet stress to the north in parts of Brazil. Areas were predicted to be along the northern border
in eastern Brazil may be conducive to moth sur- through Texas, or less likely, through southeastern
vival despite the absence of records in that area. Mexico.
The fact that no records of Cactoblastis exist in this The validity and utility of bioclimatic models
area may be due to the absence of host Opuntia is controversial. Clearly, distribution of organisms
species, or the lack of efforts to find the moth. The is determined by factors other than climate. The
model suggests potential distribution may occur problems encountered in collecting data to both
in North America (from the Caribbean Islands to calibrate and validate the CLIMEX model are
Florida, Texas and Mexico), Africa (South Africa, likely to be typical for most scientists attempting
and parts of the eastern coast), southern India, similar studies. Detailed distribution records are
parts of Southeast Asia and in the northeastern difficult to obtain, despite the fact that Cactoblastis
coast of Australia. As partial validation of these is a well-documented insect. There is a need to
predictions, the moth was recorded in the Carib- determine definitively whether the absence of
bean, including Cuba, Bahamas and Puerto Rico. records from large regions such as eastern Brazil is
Furthermore, the moth has been recorded in because sampling was performed, but no moths
southern Africa and Australia. Cactoblastis was were collected, or simply because no sampling
released, but apparently did not establish, in Kenya efforts were undertaken. Absence data is almost as
and Pakistan. Based on the model output, estab- important as presence data. In addition to prob-
lishment might have been expected in Kenya, but lems with distribution record data, weather data
not in Pakistan. New Caledonia, Hawaii and the may not be available for specific times and loca-
islands of St. Helena and Ascension did not appear tions of interest. In an insect as cosmopolitan as
on the maps generated. Based on the current Cactoblastis, a potentially significant complication
parameter values, the moth is close to its predicted is that strains of different geographical origins
northern range along the Atlantic coast. However, have differing bionomics, perhaps as adaptations
new data and revised parameter values could allow to local climate. Despite numerous valid criticisms
further expansion northwards. Therefore, the cur- against the climate matching approach, in the
rent projections are likely to be conservative esti- absence of appropriate data, climate matching
mates of Cactoblastis range in North America. may be the only viable option to predict species
Because the potential range is likely to be distributions.
conservative, more problematic is that the pre-
dicted range already encompasses Florida, Texas,
eastern Mexico, as well as a bridge of favorable cli- Control
mate linking Florida to Texas along the Gulf Coast.
Therefore, even without human intervention such Currently there are no consistently effective chem-
as contaminated shipments of cacti, climatic con- ical or biological methods to control Cactoblastis.
ditions may support natural migration of the moth To limit Cactoblastis infestations, adequate sur-
from Florida into Texas, provided adequate Opun- veillance and early detection are critical. Effective
tia populations exist along the Gulf Coast. Other surveillance may require the use of specialized
bioclimatic models yield results similar to those traps such as those baited with virgin female
from CLIMEX. GARP (Genetic Algorithm for moths. In areas where Cactoblastis has established
Rule set Prediction) was used to estimate distribu- as a pest, the selection of a control agent is deter-
tion of host cacti. Flora Map predicted potential mined by considering the value of the crop, the
distribution of Cactoblastis. When the distribution size of the affected area, and if the moth is itself
maps of both host plant and cactus moth were used as a control agent against invasive cactus spe-
overlaid, possible invasion routes into Mexico cies. Control methods may include management
702
C Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae)

practices such as the collection and destruction of parasitized up to 25% of the larvae in South Africa;
infested cacti. Systemic insecticides have not this wasp can be mass reared on alternate hosts.
proven effective against Cactobastis, but selected Larval predators of Cactoblastis include ants
contact insecticides may be used against early (Pheidole sp. and Anoplolepis steingroeveri (Forel))
instars, before they penetrate the cactus. and a tachinid (Pseudoperichaeta sp.). Pupal pre-
There are many potential biological control dation by the ant species Dorylus helvolus (L.) has
agents against Cactoblastis, but none appear to be been measured at about 1334%. Pupal parasitism
specific. As discussed in the Biology section, the by chalcid parasites Invreia sp. and Euchalcidia sp.
moth is characterized by a relatively low reproduc- was estimated at about 5%. In Florida, the chalcid
tive potential, which suggests that potential bio- parasite Brachymeria ovata Say, attacked 55% of
logical control agents need not possess extremely Cactoblastis pupae at one site. Limited work has
high reproductive rates. Candidate agents for eval- been done on evaluating insect pathogens as a
uation might include egg parasitoids or predators control agent against Cactoblastis. Beauveria sp.
that attack the vulnerable and exposed egg stage. caused high larval death rates in Australia and the
Egg parasitoids belonging to the genus Tricho- species B. bassiana may have potential in inunda-
gramma have been suggested as agents, possibly in tive control programs. The protozoan Nosema cac-
augmentative biological control programs. In Aus- toblastis has been reported from South Africa, but
tralia, Trichogramma minutum Riley caused up to recorded infection levels are only 06%. The
32% egg parasitism. This egg parasitoid is commer- pathogen Bacillus thuringiensis Berliner has dem-
cially available. In South Africa and Australia, egg onstrated efficacy against Lepidopteran pests but
predation by ants is a significant regulatory factor is not likely to be effective against Cactoblastis
in the Cactoblastis populations. Important ant inside the cactus plant.
predators include Crematogaster liengmei Forel, The Sterile Insect Technique (SIT) method is
Pheidole sp., Tetramorium erectum Emery, T. bac- being developed to study Cactoblastis populations,
chus Forel, Tetramorium sp., Monomorium albopi- and possibly for eradication in colonization sites
losum Emery, M. minutum Mayr, and Camponotus or for controlling dispersal and movement into
niveosetosus Mayr. Egg mortality due primarily to new areas. SIT may have the most potential in the
ant predation has been found to range from 55 to northern Gulf coast region where cacti are rare
78% depending on season and cactus species. and Cactoblastis populations are low, although
Other ant species suspected of being egg predators control will be expensive.
on Cactoblastis are Technomyrmex albipes Smith, Control measures against Cactoblastis infes-
Monomorium delagoense Forel, Camponotus euge- tations in the United States will probably be lim-
niae Forel, and C. rufoglaucus (Jerdon). ited in most regions because Opuntia species are
Alternatively, potential agents might be those usually a low value crop. Life history data indicate
specialized for searching and attacking the moth that the moth does not display particularly high
larvae within the cactus plant. Possible classical reproduction, so its pest status is due largely to
biological control agents from South America theprotection afforded by the cactus plant once the
include one braconid larval parasitoid, five to six larvae have gained entry into the cactus tissue. The
ichneumonid wasps, and a tachnid fly. Apanteles most vulnerable life stage appears to be the egg
alexanderi Brethes (Hymenoptera: Braconidae) stage, both because it is exposed, and also because
can cause parasitism levels over 30%. The ichneu- of its relatively long duration. Natural predation
monid Temelucha sp. caused 530% larval parasit- by ants may be encouraged. However, even after
ism. The tachinid fly Epicoronimyia mundelli moth larvae have entered the plant, specialized
(Blanchard) also attacks other species of cactus natural enemies may be effective in seeking and
moths. The braconid wasp, Bracon hebetor Say, attacking larvae inside the cactus plant. Effective
 Caddisflies (Trichoptera)
C 703

integrated pest management of Cactoblastis will mainly on liquid diets as adults and are detritivorous
require an understanding of all the management or predaceous as larvae. Adults are nocturnal and
options available to develop comprehensive, yet typically found alongside lakes and streams, but may
cost-effective strategies under different geographi- also be encountered away from bodies ofwater. Lar-
cal and socio-economic situations, while limiting vae are found in a variety of aquatic habitats, mainly
detrimental effects against non-target organisms. cool swift-flowing streams. Caddisflies are an impor-
Sterile Insect Technique tant component in aquatic food chains and also are
Area-Wide Insect Pest Management used as bioindicators of pollution.
Biological Control of Weeds Caddisfly larvae can be distinguished from
Foreign Exploration for Insects that Feed on other aquatic insects by the presence of modified
Weeds anal prolegs and a portable case or silken retreat
that protects their delicate body. Larval cases are
constructed from a variety of materials, ranging
References from stick and leaf fragments to small stones and
grains of sand, and are held together by silk pro-
Legaspi JC, Legaspi BC Jr (2007) Life table analysis for Cacto- duced by labial silk glands. Larval caddisflies
blastis cactorum immatures and female adults under (Fig.11) have a closed respiratory system marked
five constant temperatures: implications for pest man-
agement. Ann Entomol Soc Am 100:497505
by the absence of spiracles and the presence of
Mahr DL (2001) Cactoblastis cactorum (Lepidoptera: Pyrali- abdominal gills in some members. Respiration of
dae) in North America: a workshop of assessment and larvae occurs through the cuticle and gills (if pres-
planning. Fla Entomol 84:465473 (and papers con- ent). Abdominal undulation and morphological
tained in this volume)
Sutherst RW, Maywald GF, Bottomley W, Bourne A (2004) adaptations, mainly humps on the anterior seg-
CLIMEX v2: users guide. CSIRO, Queensland Australia ments of the abdomen and lateral fringes of hair,
Zimmermann HG, Moran VC, Hoffmann JH (2000) The allow for circulation of water through the case.
renowned cactus moth, Cactoblastis cactorum: its natu-
Larvae go through five to seven instars before
ral history and threat to native Opuntia floras in Mexico
and the United States of America. Divers Distrib pupation. They cease feeding and become inactive
6:259269 for up to several weeks inside the silken pupal
Zimmermann HG, Bloem S, Klein H (2004) Biology, history, cases. Pharate adults use their sharp mandibles to
threat, surveillance and control of the cactus moth,
Cactoblastis cactorum. International Atomic Energy
cut away the case, and then float to the surface and
Agency, Vienna, Austria, 46 pp emerge from the pupal integument.
Adults live for approximately a month (up to
three in some families). After mating, females enter
Caddisflies (Trichoptera) the water to deposit eggs on the underside of rocks.
Hairs on the body act as a water-proof layer, essen-
lewis s. long tially allowing the adult to breathe underwater by
University of Florida, Gainesville, FL, USA preventing the spiracles from coming into contact
with the surrounding water. The eggs of some
The Trichoptera, or caddisflies, is an advanced order species are surrounded by a gelatinous mass that
of aquatic insects that, as adults, are easily distin- swells to form a protective covering.
guished by the presence of two pairs of wings cov- Caddisflies are a product of their environ-
ered with hair and held in a roof like manner over ment. One reason they are so diverse is their abil-
the abdomen. They typically exhibit a rather dull ity to occupy so many diverse habitats, from cool
appearance (some being distinctly patterned) with flowing streams to warm still waters. Morphology
long, slender antennae. They possess chewing type and behavior of the larvae allow a variety of means
mouthparts with reduced mandibles, but feed to collect food, in addition to several families
704
C Caddisflies (Trichoptera)

Caddisflies (Trichoptera), Figure 11 Diagram of adult male and larval caddisflies.

occupying different feeding guilds. For example, hypothesize that an ancestral tube-dwelling cadd-
aperture size of the net-spinning caddisfly retreat isfly gave rise to other forms. Keys to caddisfly lar-
is directly correlated to the size of their food item: vae, pupae and adults of North American species
a larger aperture for larger prey, and a smaller can be found in the publications cited in the Ref-
aperture for particulate material. Morphological erences section. A worldwide database and cur-
modifications found in some families allow for a rent higher classification is available at the website,
diet of diatoms by scraping the surface of rocks, http://entweb.clemson.edu/database/trichopt/
while others are more suited for a filtering collect- hierarch.htm. An overview of classification is:
ing lifestyle using forelegs or delicate nets and Order Trichopteralt
retreats. Nets, cases and tubes constructed by the Suborder Annulipalpia
larvae also allow for protection and concealment Superfamily: Hydropsychoidea
while feeding or during pupation. Cases match Family: Dipseudopsidae
the habitat in which the larvae are found, from Family: Arctopsychidae
sand and pebble cases in sandy streams, to plant Family: Ecnomidae
material found in many springs, lakes and ponds. Family: Hydropsychidae
Caddisflies are considered the sister group to Family: Polycentropodidae
butterflies and moths(Order Lepidoptera) and are Family: Psychomyiidae
unique in the fact that they are the only holome- Family: Xiphocentronidae
tabolous group of insects that are considered Superfamily: Hydroptiloidea
aquatic. Some Trichoptera also share similar pher- Family: Glossosomatidae
omone detection systems like these found in some Family: Hydroptilidae
primitive Lepidoptera. Superfamily: Philopotamoidea
Currently, there are an estimated 1,400 species Family: Philopotamidae
of caddisflies recognized from North America Superfamily: Rhyacophiloidea
within 27 families, and approximately 7,000 species Family: Hydrobiosidae
in 60 extant families worldwide. Weaver and Family: Rhyacophilidae
Morse(1986) reviewed different phylogenies and Suborder: Integripalpialt
examined feeding and case-making behavior to Superfamily: Limnephiloidea
 Caddisflies (Trichoptera)
C 705

Family: Apataniidae Family: Helicopsychidae

Family: Brachycentridae (Snail-case Cadisflies)
Family: Goeridae
Family: Lepidostomatidae This family is unique within the order with larvae
Family: Limnephilidae constructing coiled cases similar in appearance to
Family: Rossianidae snail shells. They are found primarily in swift flow-
Family: Uenoidae ing waters with sandy substrates and the wave
Superfamily: Phayganeoidea swept shores of lakes and also in springs. Helicops-
Family: Phryganeidae yche is the only genus within the family.
Superfamily: Leptoceroidea
Family: Calamoceratidae
Family: Leptoceridae
Family: Molannidae
Family: Hydropsychidae
Family: Odontoceridae
(Net-spinning Caddisflies)
Superfamily: Sericostomatoidea
These caddisflies are known for their cup-shaped
Family: Beraeidae
nets that allow for both a secure place to reside
Family: Helicopsychidae
and a means of collecting food. The net acts as a
Family: Sericostomatidae
strainer and is permanently held in place with
A brief synopsis of the more common fami-
pupation occurring inside of the structure. Hydrop-
lies follows.
syche, Cheumatopsyche and Ceratopsyche are the
more diverse and widely distributed genera within
this family.
Family: Brachycentridae (Humpless
Caddisflies)

The larval cases of this family range from pieces of Family: Hydroptilidae
plant material to small pebbles and grains of sand. (Microcaddisflies)
Some members of this family are filter feeders,
collecting food particles from the current with the Microcaddisflies are unique in that the first four
use of their hairy forelegs, switching to a preda- instars are free-living with later instars increasing
ceous diet in later instars. The genera Brachycen- in size and making a purse or flask-shaped case
trus and Micrasema are the two more common open at each end. Larval case material is varied,
genera that are found throughout North America. ranging from pure silk to plant material and grains
of sand. Hydroptila, Ochrotrichia and Oxythira are
the most diverse and widespread genera within
Family: Glossosomatidae (Saddle- the family.
case Caddisflies)

Larvae of this family form saddle-like cases that Family: Lepidostomatidae

are similar to turtle shells. The upper portion of (Lepidostomatid Caddisflies)
the case is comprised of large stones while the
lower portion is generally made up of sand. They Generally found in cool headwater streams, these
are usually found on the upper surface of stones in caddisflies are also known from springs. Larvae
swift, cool streams. Two common genera are Glos- construct four sided cases or slender tubes of con-
soma and Agapetus. centric rings, each made up of sticks, twigs and
706
C Caddisflies (Trichoptera)

sand. Lepidostoma is a common genus, accounting much smaller lower opening, which results in the
for most of the diversity within the family. collection of food particles within the net. Pupa-
tion occurs in a silk lined pebble case. Three wide-
spread genera, Chimarra, Doliphiloides and
Family: Leptoceridae (Long-horned Wormalida, are found within this family.
Caddisflies)

Named for their long antennae in both the larval Family: Phyrganeidae (Large
and adult stages, long-horned caddisflies are pri- Caddisflies)
marily detritivorous or predaceous with some mem-
bers known to feed on freshwater sponges. Larval As the name implies, these are larger than most
cases vary, with some resembling short, stout log caddisflies, found primarily in cold, lentic habitats
cabins of twigs to slender tubes made ofsilk and and sometimes along the slow margins of streams.
plant material. Oecetis, Ceraclea and Triaenodes are Larval cases consist of portions of grass stems
three widespread genera found within this family. arranged spirally. Representative genera within
the family are Agrypina and Ptilostomis.

Family: Limnephilidae (Northern

Caddisflies) Family: Polycentropodidae
(Trumpet-net Caddisflies)
This is the largest family of caddisflies in North
America with more that 300 species, with the These caddisflies are found in a variety of lentic
widespread genus Limnephilus accounting for and lotic habitats and within a variety of retreats
almost a third of the diversity. Larvae are found in and cases. Some members construct delicate trum-
both lentic and lotic habitats and cases differ pet-shaped retreats while others haverigid tubes
between young and older larvae. strengthened with sand. Primarily collectors,
members of this family are also known to be pre-
daceous. Common genera include Neureclipsis and
Family: Molanidae (Hood-case Polycentropus.
Caddisflies)

This widespread family is only represented by a Family: Rhyacophilidae (Primitive

few species known mainly in eastern North Amer- Caddisflies)
ica in lentic habitats. The case is distinctive in that
it consists of a tapered tube of sand with a flat- This family is caseless, or free-living, until pupation
tened hood, allowing the larvae to feed in the open and is typically predaceous. The genus Rhyacoph-
under concealment. Molanna is the more com- ilia is a diverse group containing over 100 species
mon genus of this family. and is typically found in swift mountain streams.

Family: Philopotamidae References

(Finger-net Caddisflies)
McCafferty WP (1981) Aquatic entomology. Science book
international, Boston, MA, 448 pp
The larvae of this family are found primarily on
Merritt RW, Cummins KW (eds) (1996) An introduction to
rocks in swiftly flowing, cold streams. The finger the aquatic insects of North America, 3rd edn. Kendall/
shaped tubes have a large upper opening and a Hunt, Dubuque, IA
 Callow
C 707

Weaver JS III, Morse JC (1986) Evolution of feeding and case- application technology, calibration refers to adjust-
making behavior in Trichoptera. J North Am Benthol ment of nozzles on a spray apparatus, or determi-
Soc 5:150158
Wiggins GB (1996) Larvae of North American caddisfly gen- nation of the amount of pesticide that is produced
eral Trichoptera, 2nd edn. University of Toronto Press, by a sprayer when it is operated.
Toronto, Ontario, Canada

Cadelle, Tenebroides mauritanicus California Red Scale, Aonidiella

(Linnaeus) (Coleoptera: auranti (Maskell) (Hemiptera:
Tenebrionidae) Diaspidae)

This is a grain and flower-infesting species. This is a major pest of citrus in California, USA.
Stored Grain and Flour Insects Citrus Pests and their Management

Caeciliidae Calipharixenidae

A family of psocids (order Psocoptera). A family of insects in the order Strepsiptera.

Bark-Lice, Book-Lice or Psocids Stylopids

Caecum (pl., caeca) Callidulidae

A sac-like or tube-like structure, opened at one A family of moths (order Lepidoptera) also known
end only. as Old World butterfly moths.
Gastric Caecum Old World Butterfly Moths
Butterflies and Moths
Caenidae
Calliphoridae
A family of mayflies (order Ephemeroptera).
Mayflies A family of flies (order Diptera). They commonly
are known as blow flies, bluebottle flies, and green-
bottle flies.
Calamoceratidae
Flies
A family of caddisflies (order Trichoptera).
Caddisflies Callirhipidae

Calcaria A family of beetles (order Coleoptera). They com-

monly are known as cedar beetles.
Moveable spurs at the tip of the tibia. Beetles

Calibrate Callow
A process designed to standardize or correct the Newly molted individuals whose exoskeleton is
measuring devices on instruments. In pesticide still relatively soft and lightly pigmented.
708
C Calophllidae

Calophllidae Rican natural history followed his sabbatical leave

in Costa Rica in 19091910. He was president of
A family of bugs (order Hemiptera, superfamily the American Entomological Society from 1901 to
Psylloidea). 1915, editor of Entomological News from 1911 to
Bugs 1944, and one of the founders of the Entomological
Society of America. He died on August 23, 1961.

Calopsocidae
A family of psocids (order Psocoptera). References
Bark-Lice, Book-Lice or Psocids
*Mallis A (1971)Philip Powell Calvert. In: American entomol-
ogists. Rutgers University Press, New Brunswick, NJ, pp
Calopterygidae 178180
Rehn JAG (1962) Philip Powell Calvert (18711961). Entomol
News 63:113121
A family of damselflies (order Odonata). Schmieder RG (1962) Additions to the bibliography of
Theycommonly are known as broad-winged Philip P Calvert, subsequent to 1950. Entomol News
damselflies. 63:121
Schmieder RG, Phillips ME (1951) Bibliography of Philip P
Dragonflies and Damselflies Calvert. Entomol News 62:340

Calvert, Philip Powell

Calypter (pl., calypteres)
Philip Calvert was born in Philadelphia on January
A small fold or lobe in the hind margin of fly
29, 1871, and grew up there, leaving school in 1888
wings (Diptera) covering the haltere.
and graduating from the University of Pennsylva-
nia in 1892 with a certificate in biology, and in 1895
with a Ph.D. He then spent a year in Germany, at
the universities of Berlin and Jena. In 1907 he began
Calyptodomous
to teach zoology at the University of Pennsylvania,
Pertaining to nests, particularly wasp nests, in
retiring in 1959 with the rank of Emeritus Profes-
which the combs are surrounded by an
sor. Teaching played a major role in his life. His
envelope.
research contribution was on Odonata, on which
group he published over 300 papers, beginning in
1899. He wrote especially on taxonomy, but also on
anatomy, distribution, paleontology, and ecology.
Camel Crickets
Some of his major publications were (1893) Cata-
A family of crickets (Rhaphidophoridae) in the
logue of the Odonata (dragonflies) of the vicinity
order Orthoptera.
of Philadelphia with an introduction to the study
Grasshoppers, Katydids and Crickets
of this group of insects, (19011906) Insecta Neu-
roptera Odonata in Biologia Centrali-Americana,
(1909) Contribution to a knowledge of the Odo-
nata of the Neotropical Region, exclusive of Mexico Cameron, Malcolm
and Central America, and (1944) The rates of
growth, larval development, and seasonal distribu- Malcolm Cameron was born in London in 1873,
tion of the genus Anax. A book, A year of Costa and died there on October 24, 1954. He obtained
 Candeze, Ernest Charles Auguste
C 709

an M.D. degree at The London Hospital and Camillidae

entered the British navy as naval surgeon. He
served in the British navy during the Boer War A family of flies (order Diptera). They commonly
and in the first World War (campaigns in the Falk- are known as camillid flies.
lands and East Africa). He retired in 1920 and Flies
devoted the rest of his life to entomology, although
he had about 40 publications before retirement.
He went to India, where he collected Staphylini- Campestral
dae extensively, but returned in 1925 to London
due to a lung illness. His five-volume contribution Inhabiting open fields.
on Staphylinidae of British India was his major
work, but 206 other papers on Staphylinidae
worldwide together enabled him to describe 4,136 Campodeidae
species and 195 genera in Staphylinidae, making
him the most profuse describer of species of this A family of diplurans (order Diplura).
family after Max Bernhauer. Like Bernhauer, he Diplurans
did not provide illustrations or keys for most of
his works (the Fauna of British India was an
exception), so identification of specimens of the
Campodeiform Larva
species he described is not easy.His collection of
A term used to describe larvae that are elongate
some 55,000 specimens was bequeathed to the
and flattened, with well-developed thoracic legs
British Museum (Natural History), later called
and antennae, and a prognathous head. Such larvae
The Natural History Museum.
are usually active and predacious. It is named for
Campodea, a dipluran. This body form is found in
the orders Ephmeroptera, Odonata, Plecoptera,
References and Neuroptera.

Herman LH (2001) Cameron, Malcolm. Bull Am Mus Nat

Hist 265:5152 Canacidae
Puthz V (1986) Bibliographie de Publikationen Malcolm
Cameron s (18731954). Philippia 5:301310
A family of flies (order Diptera). They commonly
are known as beach flies.
Flies
Cambrian Period
A geological period of the Paleozoic era, extend- Candeze, Ernest Charles
ing from about 580 to 500 million years ago. Che- Auguste
licerate arthropods date from this time.
Geological Time Ernest Candze was born in Lige, Belgium,
on February 27, 1827. He studied medicine in
Paris and Lige, and became a physician and
Camillid Flies director in a hospital for the insane. In Lige he
was a pupil of Lacordaire. His taxonomic inter-
Members of the family Camillidae (order Diptera). est was the study of Elateridae (Coleoptera), in
Flies which family he became a world authority, and
710
C Canine Babesiosis

his mostnotable achievement (18571860) was redatory species, though it also occurs among
p
a four-volume monograph on Elateridae supple- detritivores and herbivores. Cannibalism is often
mented by papers in Annales de la Socit viewed as a population self-regulatory measure, act-
Entomologique de Belgique. Additionally, he ing to limit population size and suppress population
published on insect pests of horticulture, was a outbreaks. Shortage of food, high density, or both of
member of the Academie de Belgique and of the these factors contribute to cannibalism. Elimination
Socit Royale des Sciences de Lige, president of of competition is considered bysome to be the basis
the Socit Entomologique de Belgique in 1873 and for such cannibalism. However, possibly of equal
1874, one of the five commissioners of the Musum benefit is the fitness advantage resulting from
d Histoire Naturelle of Brussels, and a member of improved nutrition by cannibalistic individuals.
several foreign entomological societies. One of his Cannibals can benefit from larger food supplies fol-
collections of Elateridae is in the Natural History lowing the elimination of competition, but also from
Museum (London) and another in Brussels. His the higher nutritional quality of feeding on arthro-
wife died in 1872; they had five children, of whom pod body tissues rather than plant tissues. Probably
Lon Candze became an entomologist. He died less important are the benefits derived from reduced
near Lige on June 30, 1898. predation and parasitism following cannibalism;
lower host densities often result in less frequent
attack by predators and parasitoids. Cannibalism
References may select for shorter egg development times, as
eggs are a particularly vulnerable stage. Cannibalism
*EssigEO (1931) Candze, Ernst Charles Auguste. In: A his-
likely has contributed to development of parental
tory of entomology. MacMillan, New York, pp 563564
Lameere A (1898) Notice sur le Dr. Ernest Candze. Ann Soc care. In eusocial insects, cannibalism can be used to
Entomol Belg 42:504519 adjust caste ratios or sex allocation ratios.
Cannibalism is a normal phenomenon for
many arthropods, not an anomaly. Cannibalism has
Canine Babesiosis been documented in many insect orders, including
Odonata, Orthoptera, Thysanoptera, Hemiptera,
This is a tick-transmitted protozoan disease. It is
Trichoptera, Lepidoptera, Diptera, Neuroptera,
also known as canine piroplasmosis.
Coleoptera, and Hymenoptera. It occurs among
Piroplasmosis
predatory species and herbivores, and involves pre-
dation by the mobile adults and larvae or nymphs
Canine Piroplasmosis on each other, and on immobile eggs and pupae.
Arthropods occurring at high densities, faced with
This is a tick-transmitted protozoan disease. It is inadequate food availability, or spatially constrained
also known as canine babesiosis. (e.g., limited to feeding within a fruit or stem) more
Piroplasmosis commonly display cannibalism. Also, generalist
species are more prone to display cannibalism than
are specialist species, and females are more canni-
Cannibalism balistic than males. The greater occurrence of can-
nibalism among females may simply be a
john l. capinera manifestation of the greater size of females, allow-
University of Florida, Gainesville, FL, USA ing them to overpower prey more easily. Cannibal-
ism is common among freshwater insects. Perhaps
Cannibalism is intraspecific predation. It occurs surprisingly, cannibalism is quite common among
widely among arthropods. It is best known in some groups of herbivorous insects.
 Cannibalism
C 711

Some adaptations to deter cannibalism are actively seek out cannibalism data to document
evident. Deposition of eggs on long thin stalks by the relative importance of cannibalism. For exam-
lacewings (Neuroptera: Chrysopidae) is often ple, studies of Gerris water striders (Hemiptera:
given as an example of evolution of a cannibalism- Gerridae) have shown that the presence or absence
deterring behavior. Synchronous hatching of eggs of older water striders significantly influences
is much more widespread, and similarly deters the survival of young Gerris. If broods overlap, the
early-hatching individuals from taking advantage older bugs feed heavily on the younger, but if
of their late-hatching siblings. Dispersion of indi- theolder insects are artificially removed, survival
viduals, particularly of eggs, is another good way of the young bugs is quite high. This effect of
to reduce cannibalism. cannibalism is not easy to discern without the
artificial manipulation of the older age class.
After hatching, the predatory and cannibalis-
Population Regulation tic Mormon cricket (Fig. 12), Anabrus simplex
Haldeman (Orthoptera: Tettigoniidae), forms
Cannibalism can reduce population size before groups (called bands) that move each day, stop-
resource (food) shortages occur, thereby averting ping only briefly to feed and to rest at night. The
physiological stress. This is not unlike other popula- benefit of almost continuous movement is thought
tion regulation behaviors such as spacing, disper- to be a mechanism to protect the defenseless molt-
sion, and the benefits resulting from marking ing individuals from being consumed by their sib-
pheromones (which serve to deter insects from lings, as the molting crickets are left behind while
ovipositing repeatedly into a limited food resource). the non-molting and aggressively cannibalistic
For many species, cannibalism is correlated with individuals continue to seek food. If these high-
frequency of encounter, and higher levels of canni- density aggregations were not moving the molting
balism occur if there is an abundance of susceptible individuals would be easy prey and most would be
prey. For example, ladybird beetle (Coleoptera: killed. This may represent an unusual example of
Coccinellidae) larvae often feed on nearby the significance of cannibalism, and the evolution
unhatched eggs, but if hatching is simultaneous of a novel defense against it.
there is no cannibalism. Cannibalism occurs among Cannibalism can also be important in main-
herbivorous insects even when normal food is taining populations during periods of food scarcity.
plentiful, as in the ladybird beetle example men- From the perspective of population persistence, it is
tioned above. Hatching Danaus spp. (Lepidoptera: better to have a few well-fed cannibalistic individu-
Nymphalidae) caterpillars feed readily on their als surviving than to have all individuals die from
siblings (eggs), even while feeding on foliage. temporary lack of food. Physiological quality can be
The importance of cannibalism in population as important as abundance. Population stability and
regulation is generally poorly documented. Often persistence is enhanced during periods of food
such losses are simply attributed to disappearance, deprivation if the few survivors are well fed and
and it is unknown whether losses are due to capable of reproduction; the alternative may be
intraspecific or interspecific predation, or disper- more but malnourished individuals incapable of
sion. Cannibalism also is hard to measure because reproducing.
it may be restricted to a short period in time, and
often is detectable only via direct observation. As
noted above, ladybird beetle larvae often feed on Nutrition
eggs, but once hatch occurs, predation diminishes
or disappears because eggs, not other larvae, are Conflicting data exist on the nutritional benefits
the preferred alternate food. It may be necessary to of being a cannibal. For example, a study of
712
C Cannibalism

Cannibalism, Figure 12 Cannibalism by Mormon cricket, Anabrus simplex Haldeman (Orthoptera:

Tettigoniidae). (i) Cannibalism of a cricket; this species attacks congeners whenever the opportunity
arises. Perhaps because of this, it forms groups (called bands) that move each day, stopping only briefly
to feed and to rest at night. The benefit of almost continuous movement is thought to be a mechanism
to protect the defenseless molting individuals from being consumed by their siblings, as the i nactive
molting crickets are left behind while the non-molting and aggressively cannibalistic i ndividuals
continue to seek food. (ii) When cricket bands cross highways some are killed by the tires of passing
vehicles. The other crickets are quick to take advantage of this food source and stop to feast on their
killed or injured comrades. They, in turn will be killed by additional vehicular traffic. After several vehicles
have passed by, the roadways are marked by slippery, greasy bands marking the paths of vehicle tires.

redatory ladybird beetles showed that although

p higher body weight are considered favorable to
individuals cannibalizing eggs did not benefit in population growth. Another study involving Har-
terms of survival rates, they displayed more rapid monia axyridis ladybird beetles found that can-
development and (in the case of females) a higher nibalism allowed beetle larvae to supplement an
final body weight. Both rapid development and otherwise inadequate diet of aphids and to survive
 Cannibalism
C 713

to maturity. Cannibalistic willow leaf beetles, Pla- Cannibalism, Table 4 Levels of cannibalism
giodera versicolora (Coleoptera: Chrysomelidae), and subsequent egg production by beet
gain a size advantage and are more successful at armyworm larvae fed on sugarbeet foliage
initiating feeding sites on tough vegetation as grown in nutrient solution with nitrogen
compared to non-cannibalistic individuals. Simi- deficiency (0N), normal nitrogen (1N), or twice
larly, many aquatic detritivores supplement their the normal level of nitrogen (2N) (adapted from
diet with animal material obtained through can- Al-Zubaidi and Capinera (1983) Environ Entomol
nibalism, and a study of caddisflies (Trichoptera) 12:16871689)
found that individuals with animal material in Nutrient level (N)
their diet had higher larval survival, shorter lar- 0N 1N 2N
val and pupal development times, earlier emer-
Cannibalism (%) 60 38 24
gence dates, larger adult body mass (3040%),
Mean no. eggs after fed:
and higher fecundity (30% more eggs). In con-
trast, a study of the herbivorous caterpillar Acsia Foliage+pupae 467 512 615
monuste (Lepidoptera: Pieridae) found no benefit Foliage only 382 481 512
from cannibalism of eggs or larvae, and study of
the caterpillar Spodoptera frugiperda (Lepi-
doptera: Noctuidae) found lower body rates and were able to compensate for poor quality diet by
development times among cannibals. However, increasing cannibalism, with a subsequent boost
many studies do not separate the effects of den- (Table 4) in egg production.
sity per se (higher density increases the rate of
cannibalism but decreases fitness) from the
effects of cannibalism (which sometimes benefits Trophic Eggs
the cannibal).
Herbivorous insects have greater difficulty in Trophic eggs ar e homologous to fertile eggs but
obtaining protein than many other insects, par- they cannot develop into viable offspring and are
ticularly predators and parasitoids, due to the rela- normally eaten by siblings. Thus, in a sense, con-
tively low levels of protein in their diet. Not sumption of these eggs is an expression of can-
surprisingly, many have evolved supplemental nibalism. They are most commonly found in
feeding behaviors that provide additional protein, eusocial (social) insects such as Isoptera (ter-
including feeding on pollen, exuviae, and mem- mites) and Hymenoptera (wasps, bees, ants) but
bers of the same species (conspecifics). Early stages sometimes in other, non-eusocial groups such as
of development especially benefit from extra pro- owlflies (Neuroptera), crickets (Orthoptera),
tein, and later in life it is not unusual for holome- ladybird beetles (Coleoptera), psocids (Psocop-
tabolous insects to shift toward more carbohydrates tera), and spiders (Aranea). Trophic eggs likely
in their diet. The level of cannibalism displayed by evolved due to the survival benefits of having
an herbivorous species can change according to viable or nonviable (sterile) eggs available for
dietary levels of protein. Addition of casein to a offspring to feed upon. Trophic eggs provide a
laboratory diet of pure cellulose greatly dimin- uniform food for offspring, and in the case of
ished cannibalistic behavior of the Pacific damp- colonial species, can be stored for use during
wood termite, Zootermopsis angusticollis (Isoptera: unfavorable periods. Trophic eggs are most com-
Hodotermitidae). The level of cannibalism by the mon among eusocial species due to the interde-
beet armyworm, Spodoptera exigua (Lepidoptera: pendency on the different castes and (usually)
Noctuidae), was inversely related with the nitro- the ability of the queen to manipulate the mem-
gen level of the host plant. Thus, armyworm larvae bers of the colony.
714
C Canopidae

Sexual Cannibalism pathogens if they are ingested. Thirdly, cannibal-

ism often is particularly widespread among sib-
This is a special type of cannibalism wherein an lings because adults deposit clusters of eggs. This
insect (usually a female) consumes a conspecific, can result in reduction of inclusive fitness, because
normally a male, in association with mating. Such there is little opportunity to distinguish relatives
cannibalism usually occurs after copulation, and is from nonrelatives. Aggressive cannibals may also
widespread among mantids (Mantodea) but eliminate prospective mates if they consume all
uncommon in other taxa. In mantids, this has been conspecifics. The genetic costs of destroying rela-
documented to be a significant source of nutrition tives and eliminating prospective mates are likely
for the female. It is easy to understand the benefits very important evolutionary factors in the selec-
of cannibalism to the female, and some have pos- tion against cannibalistic behavior. Finally, many
tulated that cannibalism pre-coitus is more likely insects benefit from living in groups. Although
with unsuitable males and post-coitus more likely most apparent for social insects, even nonsocial
with more suitable mates. What is less apparent, insects enjoy benefits from group living such as
however, is why the male is successfully duped easier exploitation of food resources or more
into becoming a food resource for his mate. With effective deterrence of predation. Cannibalism
mantids, the larger size of females perhaps accounts works against the accrual of such group-derived
for the females success; it is easy for her to over- benefits.
power him. On the other hand, it can be argued Facultative Predators
that natural selection favors post-coitus sexual Nutrient Content of Insects
cannibalism because the male is making the Praying Mantids (Mantodea)
supreme parental investment in his offspring. Mormon Cricket, Anabrus simplex Haldeman
Perhaps this is consistent with other nuptial gifts Katydids
such as the large proteinaceous sperm capsule Gregarious Behavior in insects
(spermatophylax) provided to females by males of
some katydids (Orthoptera: Tettigoniidae) such as
References
the Mormon cricket, Anabrus simplex. If such sac-
rifice on the part of male mantids occurs willingly,
Bernays EA (1998) Evolution of feeding behavior in insect
it certainly represents an extreme form of paternal herbivores. Bioscience 48:3544
investment. Though not well understood, it appears Elgar MA, Crespi BJ (1992) Cannibalism. Ecology and evolu-
that males are rather cautious with females, and tion among diverse taxa. Oxford University Press,
Oxford, UK, 361 pp
strive to escape after mating. Fox LR (1975) Cannibalism in natural populations. Ann Rev
Ecol Syst 6:87106
Joyner K, Gould F (1987) Conspecific tissues and secretions as
Costs of Cannibalism sources of nutrition. In: Slansky F Jr, andRodriguez JG
(eds) Nutritional ecology of insects, mites, spiders, and
related invertebrates. Wiley, New York, NY, pp 697719
Cannibalism clearly is not always beneficial. Simpson SJ, Sword GA, Lorch PD, Couzin ID (2006) Cannibal
Cannibals risk injury or death from the defensive crickets on a forced march for protein and salt. Proc
Natl Acad Sci 103:41524156
responses of their prey. Typically, cannibals prey
on smaller or younger conspecifics, minimizing
their risk of injury. Cannibalism can also result in Canopidae
the transmission of microbial pathogens to the
predatory individual. Infected individuals early in A family of bugs (order Hemiptera, suborder
the disease cycle are sluggish, and are relatively Pentamorpha).
easy prey, but they may harbor a lethal dose of Bugs
 Cape Honey Bees, Apis mellifera capensis Escholtz
C 715

Canopy Cape Honey Bees, Apis mellifera

capensis Escholtz
The leafy part of plants or trees.
Jamie Ellis
University of Florida, Gainesville, FL, USA
Canthariasis
The Cape honey bee, Apis mellifera capensis
Infestation of the organs of the body, including the Escholtz is a subspecies (or race) of western
alimentary canal, with beetle larvae. This is an honey bee, A. mellifera Linnaeus, that occurs
unusual condition, and most often occurs by con- naturally in the Cape region of South Africa.
suming flour or other grain products that are Upon casual observation, Cape bees look very
infested with grain beetles. similar to another race of honey bee present
in South Africa, Apis mellifera scutellata (the
African honey bee of the Americas). Yet repro-
Cantharidae ductively, Cape bees differ significantly from
Apis mellifera scutellata and other honey bee
A family of beetles (order Coleoptera). They com-
races, making it perhaps the most distinctive
monly are known as soldier beetles.
race of A. mellifera worldwide.
Beetles

Cantharidin Identification

A defensive chemical produced by blister beetles Cape bees have been distinguished from scutellata
and found in their blood. It can cause blisters onthe and other African races of honey bees using mor-
skin of humans if they crush the beetles. Blisters phometric techniques. Genetic analyses are used
can also form in the mouth and digestive tract of increasingly as complications with morphometric
animals that consume the beetles along with forage techniques arise. Most beekeepers in South Africa
plants. Horses are more susceptible to injury and use other characteristics to identify Cape bees,
death than other livestock. In North America, namely (i) the ability of worker bees to produce
alfalfa hay is the principal source of blister beetles, female offspring, (ii) the highly developed ovaries
and it is contaminated when hay is crimped in Cape laying-workers, and (iii) small, queenless
(crushed) to hasten drying, as beetles are also killed swarms. Once these phenotypes can be detected,
at this time and incorporated into the hay. Prob- Cape bees usually are established already.
lems occur mostly during or following grasshop-
per outbreaks because Epicauta spp. blister beetle
larvae develop on the eggs of grasshoppers, and the Distribution
adults move to alfalfa blossoms to feed.
Blister Beetles The natural distribution of Cape bees mirrors that
Multifunctional Semiochemicals of the fynbos region in the southwestern section
of South Africa. Part of the Cape Floral Kingdom
(one of six floral kingdoms worldwide), the fynbos
Canthus is a narrow strip of land stretching from the south-
western-most corner of South Africa, eastward to
A chitinous process that, in some insects, divides Port Elizabeth. Even though it is small, the fynbos
the eyes into an upper and lower half. region contains over 80% of the flower diversity
716
C Cape Honey Bees, Apis mellifera capensis Escholtz

found in the Cape Floral Kingdom, and it has more one will find the pure race of Apis mellifera
plants species than any area in the world, includ- scutellata.
ing tropical rain forests.
Because it is rich in plant biodiversity, the fyn-
bos region is able to support a remarkable diver-
sity of life, from insects to higher animals. Cape Reproduction in Cape Bees
honey bees specialize in foraging on plant species
found in the fynbos, and beekeepers in this area Understanding reproduction in Cape bees is fun-
use Cape bees as their bee of choice. Like other damental to understanding their biology and
western honey bee races, Cape bees can be man- behavior. For the most part, reproduction in Cape
aged readily for purposes of pollination and honey bees follows that of other races of honey bees.
production. Queens are the reproductive individuals in honey
Because the fynbos region is limited climati- bee colonies. When queens emerge from the waxy
cally to the small belt stretching from southwest- cells in which they pupate, they spend the first
ern South Africa eastward to Port Elizabeth, Cape 1014 days of their lives maturing and mating.
bee distribution is limited to this area as well During this time, a queen bee will leave the colony
(Fig.13). Here, one can find the pure race of Cape in search of drones or male honey bees. Queens
bee. However, Cape bees can hybridize with Apis and drones mate in the air, following which the
mellifera scutellata, and they begin to do so just drones die. The queen will repeat this process over
north of the fynbos belt. This zone of hybridiza- the course of a few days, mating with anywhere
tion also encompasses a narrow stretch of land, from 1020 drones. Queens store all of the semen
running the entire length of area just north of the collected from the various drones in an organ
fynbos region. North of the zone of hybridization, called a spermatheca.

Cape Honey Bees, Apis mellifera capensis Escholtz, Figure 13 The distribution of Cape honey bees in
South Africa (shaded gray). The area shaded black represents where A.m. capensis and A.m. s cutellata
hybridize. The checkered area indicates the natural distribution of A.m. scutellata (modified from
Hepburn and Radloff, 1998).
 Cape Honey Bees, Apis mellifera capensis Escholtz
C 717

When a queen bee lays an egg, she can control Drones produced from laying workers are sexually
whether or not the egg is fertilized. If she chooses viable, thus they are able to mate with virgin
not to fertilize the egg, the resulting offspring will queens from other colonies in the area.
be a male bee or drone. If she chooses to fertilize This is the point in the reproductive cycle where
the egg, the resulting offspring will be a female bee, Cape bees differ from all other races of honey bees.
either a queen or a worker. This type of reproduc- When a Cape bee colony goes queenless, it attempts
tion is referred to as haplodiploid reproduction to rear a new queen. And if for whatever reason the
because male honey bees (from unfertilized eggs) colony becomes hopelessly queenless, some workers
are haploid while female honey bees (from fertil- ovaries will develop and the workers will begin to
ized eggs) are diploid. oviposit. However, unlike eggs produced by laying
Queen and worker bees both originate from workers in other honey bee races, eggs produced by
the same type of egg. The quantity and quality of Cape laying workers are usually diploid, even though
food they are fed while young determines whether Cape workers cannot mate. This means that Cape
the female larvae will become a queen or a worker. workers are fully capable of producing female off-
So it is correct to suggest that workers are under- spring, both workers and queens.
developed queens (though, some rightly argue that The process by which Cape workers produce
the reciprocal is most true, at least behaviorally diploid eggs is called thelytokous parthenogenesis
and physiologically) because they were fed less they can produce males and females parthenoge-
food while developing as larvae. netically. In this system, the egg pronucleus fuses
Worker bees, despite being sexually imma- with one of the polar bodies that results from meio-
ture, have ovaries but they are unable to mate. They sis, thus forming a diploid nucleus that continues to
can, however, lay eggs. Because the eggs cannot be develop normally into a female bee (either a queen
fertilized, workers are able to produce only drone or worker). Queenless colonies of Cape bees can
offspring. This leads to an interesting dynamic in survive for some period of time and even rear a new
honey bee colonies. The presence of a queen in a queen from one of the laying workers eggs. If, how-
colony suppresses a workers desire to reproduce. ever, the colony fails to requeen itself, the population
As long as the colony has a functioning queen, will dwindle and the colony will die. Even multiple
worker bees typically do not oviposit. laying workers present in a colony cannot maintain
However, honey bee colonies may lose their the reproductive output of a single queen.
queens for a number of reasons. This event usually Thelytoky in Cape bees leads to a number of
results in the rearing of a new queen, a feat accom- different important considerations. For example,
plished by worker bees that begin to nurture a young worker offspring produced by Cape laying workers
female larva originally produced by the now-de- are a type of clone, being genetically identical to
ceased queen. Despite this safety mechanism, many their mother (who provided both sets of chromo-
colonies fail to requeen themselves before the female somes). Furthermore, the ability of workers to lay
larvae in the colony become too old to become diploid eggs breeds a type of reproductive conflict
queens. Because of this, many colonies become not seen in colonies of other races of honey bees.
hopelessly queenless and are destined to perish. For example, queenless Cape colonies have a num-
Despite the fact that the colony will die with- ber of options: (i) produce a new queen from a
out a queen, it does have one last chance to pass its queen mother egg, (ii) produce a new queen from
genetics on to other honey bees in the area. When a worker-laid egg, (iii) proceed as a laying worker
a colony has become hopelessly queenless for a colony, or (iv) proceed as a laying worker colony
period of time (usually>2 weeks), some workers and later produce a queen from a worker-laid egg.
ovaries develop, and the workers begin to oviposit. It is important to note that thelytoky is not
The resulting, haploid offspring all become drones. unique to Cape bees. It is believed that workers
718
C Cape Honey Bees, Apis mellifera capensis Escholtz

from most (if not all) races of honey bees are capa- reproductive individual in the colony. This process
ble of laying diploid eggs. However,<1% of work- can be exacerbated when two or more Cape worker
er-laid eggs are diploid in other honey bee races. bees drift into the same colony.
So while it is the exception, rather than the rule, in Laying workers not only possess the ability to
other honey bee races, thelytoky is common and produce female offspring, but their pheromonal
the predominant scenario in Cape bee colonies. bouquet changes from that of a worker to that of a
A number of hypotheses have been proposed queen. This is especially true with respect to the
for the prevalence of thelytoky in Cape bees. Per- pheromones of the mandibular glands, which
haps the leading hypothesis is that because the change to a very queen-like scent. This change in
Cape region of South Africa is very windy, Cape scent makes the Cape laying worker become
colonies experience a significant queen loss when adopted by the parasitized colony as its new queen.
queens leave the colonies to mate. Colonies with That is why it is difficult to requeen a laying worker
thelytokous capabilities would not suffer the loss colony. The bees in the colony think they have a
of a queen the same way as colonies without thely- queen. Any introduction of a new queen into a
tokous capabilities, thus favoring the propagation Cape laying worker colony almost always results
of colonies with thelytokous workers. in the new queens death.
The ability of Cape workers to produce female
offspring elicits another interesting behavior in Cape
Biology and Behavior colonies worker policing. In worker policing, work-
ers produced from one Cape laying worker candetect
Behaviorally, Cape bees are not unlike other eggs oviposited by other laying workers and destroy
African races of honey bees. They are flighty on or eat those eggs. This establishes a dominance hier-
the comb (run on the comb when the colony is archy within Cape laying worker colonies whereby
disturbed), abscond (completely abandon the females from the same mother police the colony and
nest) readily in response to nest disturbances or destroy their aunts offspring in favor of their own
diseases/pests, have smaller colonies than Euro- mothers offspring (their sisters). Research has shown
pean races (an artifact of being in a warmer cli- that this behavior has led to territory grabbing within
mate), use copious amounts of propolis (resins Cape laying worker colonies.
collected from trees and plants, used as a weather- Because a Cape laying worker colony is com-
proofing agent and antibiotic in the colony), and posed of many laying workers, all whose offspring
are well-suited to warm climates. Unlike other are working to ensure their mother is the domi-
African bee races (especially Apis mellifera scutel- nant laying force in the colony, bees produced by
lata), Cape bees are docile, at least usually. Yet, the same laying worker may congregate in the
there is a key behavioral difference that separates same area of the colony. So within a colony, one
them from all other races of honey bees. Cape bees might find smaller sub-colonies, each headed by
are considered social parasites. a laying worker. This system is truly amazing and
Social parasitism in Cape bees is not under- has advanced the study of the development of
stood fully. In instances of larger numbers of colonies sociality and reproductive castes.
per unit area (e.g., managed-colony situations),
worker bees and drones will drift between colonies.
When the drifting bees are Cape worker bees, the Problems for Beekeepers
worker bees can takeover or parasitize the host
colony. In this regard, the mother queen of the Although the biology and behavior of Cape bees are
hostcolony is lost (a process not understood fully fascinating, they present a problem for beekeepers in
at this point) and the Cape worker becomes the South Africa. Cape workers can parasitize colonies
 Carabid Beetles (Coleoptera: Carabidae) as Parasitoids
C 719

of any race of A. mellifera. Migratory beekeepers Capsid

managing scutellata in the northern part of South
Africa have moved bees into the fynbos region of The protein coat or shell of a virus particle; the
South Africa where the Cape bee is present (the capsid is a surface crystal, built of structure units.
reciprocal also happens). This has allowed Cape
workers to drift into and parasitize Apis mellifera Capsids
scutellata colonies. This action has been a significant
problem for beekeepers because Cape-parasitized Some members of the family Miridae (order
colonies often dwindle and die. Furthermore, Cape Hemiptera).
bees are specialist foragers in the fynbos region and Plant Bugs
they often perform poorly when taken outside of this Bugs
region. So Apis mellifera scutellata colonies parasit-
ized by Cape bees in the northern part of South Capsomere
Africa can become useless to beekeepers.
Beekeepers in South Africa often consider A cluster of structure units arranged on the sur-
Cape bees more of a serious threat to their colo- face of the nucleocapsid, in viruses possessing
nies than varroa mites (Varroa destructor, the most cubic symmetry.
prolific pest of honey bees). Because of this,
researchers globally have taken notice of Cape
bees. Many fear that if Cape bees ever spread out-
Carabidae
side of South Africa, they may be a significant
A family of beetles (order Coleoptera). They com-
problem for beekeepers worldwide.
monly are known as ground beetles.
Beetles
References

Hepburn HR (2001) The enigmatic Cape honey bee, Apis mel- Carabid Beetles (Coleoptera:
lifera capensis. Bee World 82:181191 Carabidae) as Parasitoids
Hepburn HR, Radloff SE (1998) Honeybees of Africa. Spring-
er-Verlag, Berlin, Germany, 370 pp
Johannsmeier MF (ed) (2001) Beekeeping in South Africa. donald c. weber, pavel saska, caroline
Plant protection handbook No. 14, Agricultural Research s.chaboo
Council, Pretoria, South Africa, 288 pp USDA Agricultural Research Service, Beltsville,
MD, USA
Crop Research Institute, Praha, Czech Republic
Capitate
University of Kansas, Lawrence, KS, USA
Having an expanded tip or club-shaped, and usu-
ally used in reference to antennae. Several genera of carabid beetles are ectoparasitoids
Antennae of Hexapods as larvae. The parasitoid habit is uncommon in
beetles; only eleven beetle families include parasitoid
species, compared to a much wider diversity of para-
Capniidae sitoids in the Diptera and Hymenoptera. The evolution
and ecology of these parasitoid beetles is fascinating,
A family of stoneflies (order Plecoptera). They but their host associations are poorly known.
sometimes are called small winter stoneflies. Carabid beetles have been stereotyped as
Stoneflies ground-dwelling generalist predators, yet in recent
720
C Carabid Beetles (Coleoptera: Carabidae) as Parasitoids

years many counter-examples have shown the Car- On the basis of fragmentary observation, it
abidae to be more diverse in form, habit, and trophic appears that Pelecium sulcatum (Pelecinii) develop
association. Many carabids, especially tropical spe- as parasitoids on chrysomelid pupae and imma-
cies, are arboreal. Granivory, herbivory, and special- ture millipedes, and have only one larval instar.
ized predatory habits are widespread. Three of the Lebia species number over 450 and the genus is
76 recognized tribes are known to have parasitoid cosmopolitan, with 47 in North America. Adults
species: Brachinini, Peleciini, and Lebiini. All of typically seek prey in plant canopies, and all known
these are ectoparasitoids on pupae of other beetles larvae are ectoparasitoids of chrysomelid beetle
or, in one Peleciine genus, on immature millipedes. pupae, yet only four species hosts have been docu-
In all known parasitoid carabids, the larva mented. Many additional Lebia species are reported
passes through three distinct development phases. to be associated (often with adult mimicry) with
First, the free-living first larval instar emerges from specific chrysomelids, particularly flea beetles (Altic-
an egg laid in the hosts habitat, and locates a host. inae) and casebearers (Cryptocephalinae), implying
Then, the larva feeds on a single pupal or pre-pupal a host-parasitoid relationship. Two species parasitize
host, while it molts zero to four times. Third, after economically important hosts: L. scapularis on elm
the host is consumed, the larva undergoes a non- leaf beetle, Xanthogaleruca luteola in Europe, and
feeding larval stage (pre-pupa) with zero to two L. grandis on (Fig.14) Colorado potato beetle, Lepti-
molts; it then pupates next to the remains of the host. notarsa decemlineata in North America. Although
The total number of larval instars often deviates elm leaf beetle is a significant invasive pest of
from the three molts typical for Carabidae, ranging ornamental elms in North America and elsewhere,
from one (Pelecium) to five instars (some Brachinus). L. scapularis apparently has not been considered for
The adults live in the host habitat and may have a classical biological control. In contrast, L. grandis
narrow or broad range of prey, including the imma- was introduced to France in the 1930s, and its para-
ture stages of the host. sitoid life history discovered, as part of a USA-France
The best-known genera of parasitoid carabids
are Brachinus, Lebia, and Lebistina. Brachinus, the
celebrated bombardier beetle, emits a directed,
explosive spray of boiling-hot quinone solution,
which is considered the most highly evolved defen-
sive secretion of the many types documented in the
Carabidae. Studies by Eisner and colleagues have
shown the elaborate mechanisms which allow the
orchestration of this exothermic reaction while
protecting the emitter and instantly repelling poten-
tial predators. They have also shown the chain of
evolutionary developments leading to this impres-
sive set of defensive organs. North American Brachi-
nus are found in littoral habitats near fresh water,
where the known beetle hosts in families Hydro-
philidae, Dytiscidae, and Gyrinidae emerge to
pupate from their larval aquatic habitats. Recently, Carabid Beetles (Coleoptera: Carabidae) as
dryland European Brachinus have been associated Parasitoids, Figure 14 Lebia grandis fed first instar
with carabid hosts of the genus Amara, broadening larva (top) with its prepupal host, Colorado potato
the known hosts to 11 species, for only nine of the beetle, Leptinotarsa decemlineata (photo by
approximately 300 Brachinus species described. Caroline Chaboo).
 Carayonemidae
C 721

classical biocontrol program. Since the carabid was Erwin TL (1979) A review of the natural history and evolution
of ectoparasitoid relationships in carabid beetles. In:
originally described from North Carolina in 1830,
Erwin TL, Ball GE, Whitehead DR, Halpern AL (eds)
over 60 years before Colorado beetle arrived there, Carabid Beetles: their evolution, natural history, and
its putative original host was the false potato beetle, classification. Dr W Junk, The Hague, The Netherlands,
L. juncta, the only Leptinotarsa present. Although the pp 479484
Robertson H (2004) How San hunters use beetles to poison
introduction to Europe failed, there is interest in their arrows. Iziko museum of Cape Town. Available at
future classical biocontrol because of the apparent www.biodiversityexplorer.org/beetles/chrysomelidae/
host specificity and the fact that the adults are the alticinae/arrows.htm (accessed 26 March 2008)
most voracious predators known on eggs and larvae Saska P, Honek A (2004) Development of the beetle parasi-
toids, Brachinus explodens and B. crepitans (Coleoptera:
of Colorado potato beetle. Lebia adults are typically Carabidae). J Zool (Lond) 262:2936
found in close association with their host species, Weber DC, Rowley DR, Greenstone MH, Athanas MM (2006)
and females oviposit in close proximity to the host Prey preference and host suitability of the predatory
and parasitoid carabid beetle, Lebia grandis, for several
pupal habitat; in the case of L. grandis, this takes
species of Leptinotarsa beetles. J Insect Sci 6:9. Available
place in the soil below infested host plants. online at http://insectscience.org/6.09/
Lebistina, an African genus closely related to
Lebia, shows adult mimicry of its chrysomelid hosts,
a pattern shared with some Lebia species. Lebistina Carabiform Larva
is one part of a complex anthro-ecological story
involving the San indigenous tribe of Southern This is another term for campodeiform larva.
Africa. San tribe members dig underground for Campodeiform Larva
the pupae of chrysomelids and their carabid par-
asitoids, both associated with the aromatic shrub
Commiphora in the incense tree family, Burseraceae.
Pupae of both the chrysomelid Diamphidia, and Caraboid Larva
especially its parasitoid Lebistina, are collected for
their potent neurotoxic arrow-poisons, which allow A larval form that is similar to campodeiform,
San hunters to fell large prey such as giraffes with but usually more chitinized and with stronger
small bows and arrows, but usually only after several mandibles and short antennae. It is found in the
days of tracking the injured animal. families Staphylinidae, Carabidae, Dytisidae, and
Parasitoid carabids present some fascinating Hydophylidae (all in the order Coleoptera).
evolutionary questions, not the least of which is why Campodeiform Larva
both the impressive arrow-poisons and the explo-
sive exocrine toxins are associated with these genera.
Yet, at most, 1% of their hosts are known. In addi- Carapace
tion, the possible management of predator/parasi-
toid beetles may offer an interesting opportunity for This is not a term used with insects (hexapods). It
double control of chrysomelid pest species. is used to describe the fused dorsal covering of
crustaceans.

References
Carayonemidae
Eggleton P, Belshaw R (1993) Comparisons of dipteran,
hymenopteran and coleopteran parasitoids: provisional
A family of insects in the superfamily Coccoidae
phylogenetic explanations. Biol J Linn Soc 48:213226
Eisner T (2003) For love of insects. Belknap Press, Harvard (order Hemiptera).
University, Cambridge, MA, 464 pp Bugs
722
C Carbamate Insecticide

Carbamate Insecticide
cardo

One of a class of cholinesterase inhibiting insecti-

cides derived from carbamic acid. stipes
Insecticides palpifer

lacinia
Carbohydrate subgalea

A large class of carbon-hydrogen-oxygen com- galea

pounds, including simple sugars (monosaccha-
rides) such as glucose. Glucose is the major fuel
for most organisms and is the basic building
block of polysaccharides such as starch and
palpus
cellulose.

Carboniferous Period Cardo, Figure 15 External lateral aspect of the left

maxilla in an adult grasshopper, showing some
A geological period of the Paleozoic era, extend- major elements.
ing from about 360 to 300 million years ago. The
oldest insect fossils date from this period.
Geological Periods Careers in Entomology

linda wiener
St. Johns College, Santa Fe, NM, USA
Carcinogen
A substance or agent capable of causing cancer. Entomologists are lucky to have a wide range of
career choices. These include research in a wide
variety of contexts, from universities, to many
Carcinophoridae government agencies, to private corporations. The
following is a summary of the institutions which
A family of earwigs (order Dermaptera). They hire entomologists, the types of work available
sometimes are called seaside and ring-legged and the qualifications usually required.
earwigs. Faculty research, teaching, and extension
Earwigs positions almost always require a Ph.D. in ento-
mology or a related field. Leadership positions in
government agencies and heads of research groups
Cardo in industry and government require a Ph.D. plus
related administrative experience.
A term that is used differently among orders Research assistant positions are available for
(Fig.15) and structures, but most commonly refers most graduate students. These are funded posi-
to the base or proximal section of a maxillary tions to perform research which also include
appendage. tuition and a stipend. Teaching assistant positions
Mouthparts of Hexapods are also available to graduate students. These
 Careers in Entomology
C 723

include helping professors teach lecture and labo- Regulatory

ratory classes and grade papers and projects. Post
doctoral fellowships are available to people with a Regulatory work involves inspection of plants
Ph.D. to perform research on funded projects. and animals entering an area with the goal of detect-
There are a wide variety of research technician ing, excluding, containing, or eradicatingpatho-
jobs that require an M.S. or relevant work experi- gens, weeds, and other undesirable organisms.
ence or a combination of education and work
experience. Positions in county extension and
many regulatory positions require a B.S. and/or
relevant work experience. There are many part time Industry
and intern positions which are available to high
school or college students without a degree. Jobs in Industry work may involve research, but also invent-
the urban pest control industry rarely require any ing, patenting, and marketing new products. This
special education. also involves service oriented skills such as advis-
ing clients and providing pest control services.

Qualifications and Skills

Opportunities
Each job listing will have a list of desired qualifica-
tions and skills. Educational Institutions

Land Grant Universities and Cooperative

Research Extension

Research requires skills in areas such as devis- These institutions usually have a focus on agricultural
ing, setting up, and running experiments, taking research and teaching with a network of extension
data, analyzing and recording data using com- stations throughout the state. Faculty positions
puter programs, writing up results for publica- generally involve a combination of research and
tion and presenting results in lectures and teaching, often, but not always, focusing on applied
conferences. rather than pure research. The research portion of
the work involves the design and implementation of
research projects, identifying sources and applying
Teaching for research funding, training of graduate students
and other students who participate in the research,
Teaching skills include knowledge of the field writing up papers for publications, delivering lec-
and the ability to help students learn through lec- tures at conferences, and (if extension) interacting
ture and discussion as well as designing courses with and advising farmers. These positions usually
and putting together course materials for a class. include teaching in an area of expertise as well as
teaching entry level courses in entomology.
Land grant universities have insect collections
Extension for reference and research. Positions are available in
the museums for taxonomists and collections managers
Extension usually requires a combination of who help identify, sort, label, and collect specimens.
research skills and facility interacting with the Extension work involves research on agricul-
public and other government organizations. tural and urban plant and animal husbandry.
724
C Careers in Entomology

Extension positions are available and based in and Plant Health Inspection Service (APHIS) and
each county to advise people about raising and the Forest Service. They hire for research, extension,
caring for plants and animals. Extension work and regulatory positions.
involves research and survey work as well as con-
siderable interaction with the public and other
government agencies. Extension positions often Armed Forces
focus on agriculture and animal husbandry, but
increasingly focus on urban landscapes and other The Navy, Army, and Air Force hire entomologists
urban pests. Positions also are available in the to do research on insects which transmit vector
extension research stations connected with the borne diseases such as malaria, dengue fever, and
university, but located in agricultural areas. encephalitis as well as pest control specialists who
work on ships and bases.

Other Public and Private Research

Universities Other Agencies

There are many other research universities that Other agencies hire specialists in mosquito con-
hire entomologists as part of biology departments trol and to track and advise on other public health
or departments of entomology, ecology, behavior, concerns such as bubonic plague. The National
or evolution. Medical and veterinary schools also Park Service and other government agencies hire
hire entomologists to do research on insect trans- entomologists for implementing IPM programs
mitted diseases and other insect related illnesses. and handling pest control problems.
Duties and qualifications are similar to the above.

Industry
Undergraduate Colleges and Universities
with a Focus on Teaching Urban Pest Control and Landscape
Maintenance
There are many smaller universities and colleges
where a professors primary duties are in teaching. This is a large and diverse industry that services
In these institutions, teaching duties can be quite business and residential customers. They need
various and a person with training in entomology entomologists to do identifications, advise custo
might find herself teaching human anatomy or mers, and apply pesticides and other pest
animal physiology, as well as courses in her spe- controls.
cialty. Many professors also have research projects,
though these are not as central to advancement as
in the aforementioned research universities. Pesticide and Pest Control Device
Manufacturers

United States Government These businesses need entomologists to design

and run evaluation tests on the pesticides and
U.S. Department of Agriculture devices that a company markets. They also need
experts to identify areas of need in the pest control
The principal agencies hiring entomologists include industry and to consult with distributors and
the Agricultural Research Service (ARS), Animal customers.
 Careers in Entomology
C 725

Food, Tobacco, and Drug Companies family situations. Many independent entomolo-
gists got their start working at a university or in
These industries hire entomologists to research industry and later struck out on their own. The
methods of keeping insects out of their packaged following are typical examples of the work of inde-
products and out of their manufacturing and pro- pendent entomologists. Keep in mind that these
cessing areas. They also hire entomologists to do categories are rather general and not mutually
pest control in processing and packaging areas. exclusive. Many independent entomologists work
in several of these areas.
This brief survey should show that there are
International Aid Organizations numerous opportunities available to those who
prefer to work independently. Undoubtedly, there
A variety of agencies such as the World Health are some possibilities left out or still to be invented.
Organization (WHO), the United States Agency The benefits mentioned most frequently of
for International Development (USAID), and the doing independent work are the ability to do what
International Center for Tropical Agriculture you love all the time, making (more or less) your own
(CIAT) hire entomologists to work on a variety of hours, the diversity of contacts that are developed,
public health and agriculture projects overseas. and the ability to conceive of a dream and bring it to
There are many non-governmental organizations fruition, while offering a valuable service not other-
(NGOs) which hire entomologists for similar wise available. Some, with a lifelong passion for ento-
projects. These are research and extension positions, mology but little or no formal education, have found
generally temporary, and may require foreign their way to satisfying careers via the independent
language skills. route. A few of these people have eventually obtained
traditional jobs in universities or industry.
Naturally, there is a downside to such work.
Difficulties include the lack of support staff and the
Independent Entomologists necessity of doing everything yourself, including
all the bookkeeping, hiring, firing, advertising,
This section will focus on entomologists who phone answering, etc. Also, there is a frequent
choose not to work for an institution, but who go necessity of looking for new work which may
into business for themselves. It is anticipated that involve lots of phone calls, drawing up of propos-
this section will give ideas, inspiration, and some als, and periods without much income. On the
caution to those who are thinking of working other hand, many people mentioned that getting
independently as an entomologist. started was difficult, but after a few years, the work
The individuals consulted for this section just keeps coming in with very little necessity to go
chose the independent route for a great variety of out and look for it. Many independent entomo
reasons. Some did not have the formal education logists have second jobs on the side ranging from
to get a job in a university or government follow- teaching to police officer.
ing established routes. Others did not like being a
part of a large institution, or preferred working by
themselves. Others could not realize their ambi- Research and Development of Products
tions or dreams at a university and so formed their
own foundations and businesses. Circumstances Entomologists working in this area often contract
of all sorts cause some aspiring entomologists to to test and develop products for pest control as
put together a career in a location that lacks uni- well as helping the developers through the com-
versities or industries that fit their skills or their plex procedures for registering a new product.
726
C Caribbean Fruit Fly, Anastrepha suspensa (Loew) (Diptera: Tephritidae)

People doing this work generally started out with traditional chemical control programs), advising
standard jobs in universities or industry where about rearing and displaying live insects, and advis-
they received training and made the contacts ing industry about development or marketing of
necessary to run a business on their own. products. Many entomologists contract with other
organizations to do specific tasks such as curating a
particular group of insects for a museum, surveying
Lectures, Workshops and Other Courses private or public land for butterflies and other
insects, and scouting fields for pests and beneficial
Entomologists working in this area design and teach insects and making control recommendations.
courses on a wide range of topics from parasitic
insects to tropical biology to urban pest control to
the design, building, and maintenance of insect zoos. Non Profit Organizations
Such courses may be for professionals, graduate or
undergraduate students, or the general public. They These organizations usually are focused on con-
may also develop and sell educational materials. servation of particular insect groups or insect
Lectures and classes on insects are also popu- habitats. These organizations also may include
lar with garden clubs, elementary schools, nature insects and pest control in a larger context such as
centers, museums, state and national parks, elder preserving traditional agricultural techniques.
hostels, agricultural associations, and many others.

Retail or Wholesale Business

Writing and Photography
At least one intrepid entomologist has a store spe-
Many independent entomologists write field guides, cializing in insect toys, jewelry, food, books, and
childrens books, and other books about animals and other products. Other businesses sell insect con-
insects. A passion for photography or art involving trol devices and chemicals.
insects frequently is the driving force for those who
pursue a career in publishing books on insects.
Caribbean Fruit Fly, Anastrepha
suspensa (Loew) (Diptera:
Tephritidae)
Urban Pest Control
This fly affects various fruits in the Caribbean
Perform routine and specialized pest control for
region.
home owners and businesses. This involves diagnos-
Citrus Pests and their Management
ing problems, applying pesticides or otherwise con-
Tropical Fruit Pests and their Management
trolling pest populations. It may also involve doing
home repairs and other preventive measures.
Carina (pl., Carinae)
Consultant and Contract Work A ridge or keel. This character is evident on many
orthopterans, and both lateral and medial carinae
Consultants are probably the largest category of occur on the pronotum of some grasshoppers. It
independent entomologists. Consulting work can has considerable diagnostic value at the species
range from pest control in urban or agricultural set- level in grasshoppers.
tings (often involving IPM and other alternatives to Thorax of Hexapods
 Carnivorous Plants
C 727

Carnid Flies extremes of temperature and rainfall. All carnivo-

rous plants are insectivorous except for the few
Members of the family Carnidae (order Diptera). species with aquatic traps.
Flies Among the insectivorous plants, there are
three kinds of structures that are responsible for
trapping insects: mucilage (sticky) traps (found
Carnidae among the Lentibulariaceae, Roridulaceae, Bybli-
daceae, Droseraceae and Dioncophyllaceae); pitfall
A family of flies (order Diptera). They commonly (pitcher) traps (Sarraceniaceae, Nepenthaceae,
are known as carnid flies. Cephalotaceae and Bromeliaceae); and snap traps
Flies (Droseraceae). Stalked glands bearing a droplet of
adhesive liquid are the basis of mucilage traps. The
glands are borne on leaf surfaces, and insects
Carnivore become entangled in the mucilage when they alight
on or walk onto the glandular surface. Enzymatic
A flesh-eating organism (contrast with herbivore). juices are released by the plant and digestion of the
prey ensues. Pitcher traps are modified leaves that
are formed into vase-like structures that are held
Carnivore Fleas erect with the aperture uppermost. The lip of the
pitcher may bear nectaries and pigment patterns
Members of the family Vermipsyllidae (order that serve to attract insect visitors. Below the necta-
Siphonaptera). ries, the interior surface of the pitcher is smooth
Fleas and slippery, and may be covered with minute,
downward-pointing projections that prevent insect
feet from obtaining a firm grip on the surface. The
Carnivorous hapless insect visitor falls into the fluid in the base
of the pitcher and drowns. Pitcher plants have
Feeding on animals. digestive glands, but the dissolution of the prey is
further assisted by various pitcher inhabitants,
including microbes and insect larvae. Plants with
Carnivorous Plants snap traps have a pair of lobed structures that are
capable of movement at the end of certain leaves.
James Cresswell The trap responds to stimulation of trigger hairs on
University of Exeter, Exeter, United Kingdom the trap surface by rapidly closing the lobes, which
have marginal spines that interdigitate and thereby
Carnivorous plants use entrapped animal tissues, enclose the insect visitor. The trap reopens after the
mainly insects, as a source of nutrition. There are prey is digested by secreted enzymes.
approximately 600 species of carnivorous plants in The prey of insectivorous plants typically
six angiosperm subclasses, which include both aresmall, mobile individuals from a diverse arrayof
monocotyledons and eudicotyledons. The multi- taxa: Collembola,Diptera,Hymenoptera,Coleoptera,
ple, polyphyletic origins of the carnivorous plants Hemiptera, Thysanoptera; with less frequent repre-
suggest that the syndrome is an adaptation to the sentation from Lepidoptera, Odonata, Orthoptera
low nutrient, bright, waterlogged habitats that and other orders. Spiders, mites and isopods are also
the plants typically inhabit. Carnivorous plants are caught. To attract insects, the traps of some carnivo-
found worldwide in varied climates that span rous plants provide nectar rewards and some are
728
C Carnivory and Symbiosis in the Purple Pitcher Plant

pigmented, scented or glisten in ways that may emu- Carnivory and Symbiosis in the
late the attributes of flowers or carrion. Other traps Purple Pitcher Plant
rely simply on the tendency of insects to alight on, or
walk across, convenient surfaces. Insect tissues are Donna Giberson
particularly rich in nitrogenous compounds, and University of Prince Edward Island,
plants reportedly obtain 1075% of their nitrogen Charlottetown, PE, Canada
from prey, depending on species and location. Prey
capture promotes flower production and the repro- Pitcher plants are a widely recognized group of
ductive success of the plant. carnivorous plants, well known for capturing and
All carnivorous plants are pollinated by digesting small animals to supplement more
insects and there is a potential conflict between usual nutrient sources. Carnivorous plants have
prey capture and pollination. Many plants have a fascinated biologists for centuries, despite mak-
spatial or temporal separation between their flow- ing up only a tiny percentage of the species of
ers and their traps that promotes segregation of flowering plants. Only about 600 species occur in
these processes, so evidence for the existence of six angiosperm subclasses. They generally inhabit
this conflict is rare. nutrient-poor habitats, and the captured and
Pitcher traps often support a phytotelm, digested insects provide a source of nitrogen,
which is a plant-borne pool that comprises an phosphorus, and micronutrients. Pitcher plants
aquatic ecosystem. The volume of phytotelms make up a substantial proportion of the carnivo-
ranges from a few milliliters in Sarracenia pitchers rous flora, with known representatives in three
to approximately 2 L in Nepenthes rajah. The insect unrelated families: the new world Sarraceniaceae
members of the phytotelm community are Dip- (27 + species), the tropical Nepenthaceae
teran larvae, and different species adopt various (103+species) and the Australian Cephalotaceae
lifestyles, such as filter feeding (e.g., mosquito lar- (one species).
vae), saprophagy and predation. These inhabitants The pitcher plants have modified tubular
are sometimes referred to as pitcher inquilines leaves or pitchers that act as simple pitfall traps
or the infauna. Phytotelms are much studied by for insects and other small terrestrial animals.
community ecologists looking at patterns of coex- Insects are attracted to the plant by color patterns
istence and community structure. There are also or production of extrafloral nectar, then may lose
non-aquatic associates of pitcher traps. Ants (e.g., their footing and fall into the pitcher to drown in
genus Camponotus) inhabit pitchers in certain fluid retained in the pitchers. In many cases, slip-
pitcher plants (Nepenthes bicalcarata) and scav- pery surfaces and/or downward pointing hairs
enge from the pitcher fluid. Additionally, spiders prevent the insects from climbing out and escaping.
occasionally spin webs across pitcher apertures, Some pitchers exclude rainfall by hoods that cover
thus acting as resource parasites. the pitcher opening (e.g., Nepenthes, some Sar-
Insectivorous Plants racenia) and secrete fluids that include digestive
enzymes (including proteases, esterases, acid phos-
References phatases, and amylases) that collect at the bottom
of the pitcher. Other species (e.g., Heliamphora
Cresswell JE (2000) Resource input and the community spp. and Sarracenia purpurea) collect rainwater
structure of larval infaunas of an eastern tropical pitcher and may or may not secrete digestive enzymes into
plant. Ecol Entomol 25:1925 the water.
Ellison AM, Gotelli NJ (2001) Evolutionary ecology of the
One reason for the fascination with these
carnivorous plants. Trends Ecol Evol 16:623629
Juniper BE, Robins RJ, Joel DM (1989) The carnivorous plants. plants is that they represent a type of plant/insect
Academic Press, London, UK interaction that falls outside of the more expected
 Carnivory and Symbiosis in the Purple Pitcher Plant
C 729

interactions such as herbivory or pollination. purpurea, which is the most widely distributed
Therefore, many studies have concentrated on pitcher plant in North America, and which has
aspects of carnivory, such as cost-benefit analyses relatively long-lived pitcher habitats.
(i.e., cost of attracting insect prey versus nutri-
tional benefit from prey), prey species composi-
tion, digestive enzymes, etc. Other researchers Sarracenia Species in North
have focused on pitcher plants as habitat for a wide America
variety of organisms. Pitcher plant inhabitants
include aquatic taxa that live in the fluid in the The Sarraceniaceae includes three genera in the
pitcher (insects, mites, rotifers, protozoa, and bac- New World: Sarracenia (811 species, depending
teria), but may also include wasps that build nests on taxonomic opinion), Darlontonia (a single spe-
in the pitchers, ants that live in specialized parts of cies in California and Oregon) and Heliamphora
the plants, and spiders that spin webs across the (at least 15 species in South America). Sarracenia
mouth of pitchers. Because the pitchers function is North American, and is mainly a genus of the
as discrete habitats with clear boundaries between American southeast (Table5). As many as five spe-
the internal and external environment, they have cies may occur naturally at a single site along the
been the subject of many process-related studies, Gulf coast, but pitcher plant habitat is declining
examining food-web, energy flow, and community dramatically in these areas, and many species and
questions within entire ecosystems. This is partic- subspecies in the genus are threatened by habitat
ularly true for the purple pitcher plant, Sarracenia loss. One species, S. purpurea (the purple pitcher

Carnivory and Symbiosis in the Purple Pitcher Plant, Table 5 Sarracenia species in North America
Species Common name Distribution
S. alata pale pitcher plant, or US Gulf coastal plain; SW Alabama to Texas
winged pitcher plant
S. flava yellow pitcher plant US southeastern coastal plain; SW Alabama to SE Virginia
S. leucophylla white-topped pitcher plant US Gulf coastal plain; Florida to E Mississippi
S. minor hooded pitcher plant Northern Florida to North Carolina
S. oreophila green pitcher plant rare in North Carolina, Georgia, and Alabama; protected
status
S. psittacina parrot pitcher plant US southern Gulf coast; Georgia to Mississippi
S. purpurea purple pitcher plant fragmented locations through the eastern US from Florida
north to Maine and westward to Minnesota; widespread
across Canada from the Atlantic coast to the northern prai-
rie provinces and into northern British Columbia and south-
ern Northwest Territories
S. purpurea var. Burkes variety US Gulf coastal plain; some elevate this to species status as
burkii S. rosea
(or S. rosea)
S. rubra sweet pitcher plant SE USA; North Carolina to Florida and Mississippi
S. rubra alaba- canebrake pitcher plant rare in Alabama; protected; some elevate this to species
mensis (or S. status as S. alabamensis
alabamensis)
S. rubra jonesii mountain pitcher plant rare in North and South Carolina; protected; some elevate
(or S. jonesii) this subspecies to species status as S. jonesii
730
C Carnivory and Symbiosis in the Purple Pitcher Plant

plant), ranges throughout much of North America, and symbiosis have concentrated on S. purpurea
from Florida and Labrador in the east, and north- because its wide distribution and ability to hold
westward through Minnesota and the Canadian water for relatively long periods of time allow the
prairie provinces, into northern British Columbia development of a surprisingly complex commu-
and the southern Northwest Territories. Popula- nity of inhabitants.
tions are generally stable in the northern parts of
the range, especially in the less human-populated
areas of the Canadian boreal zone. Species are
perennial, and have tube-shaped leaves that form The Purple Pitcher Plant,
pitfall traps for small, mobile invertebrates. All Sarracenia purpurea
species also produce photosynthetic non-tubular
leaves in response to light intensity and nutrients. Sarracenia purpurea is a long-lived herbaceous
Sarracenia species interact with insects in perennial that is widespread over much of North
four major ways, (i) carnivory, (ii) pollination, America. Pitcher-shaped leaves are produced in a
(iii) herbivory, and (iv) symbiosis. All pitcher rosette, with new pitchers produced every 15 or 20
plants are carnivorous and attract insects as prey. days. Soon after a new pitcher opens, it fills up with
The plants can self-pollinate, but several insects, rainwater and begins attracting insect prey, and
especially bumblebees, are important in providing several new leaves may be produced over the sum-
cross-pollination for the plants. Several insects mer. The purple pitcher plant is exposed to a wide
feed on different parts of pitcher plants, and some variety of conditions throughout a range which
of them are obligate pitcher herbivores, especially encompasses 30 longitude and 70 latitude. In the
noctuid moths in the genus Exyra. Finally, some south, the species grows year round in a variety of
insects live inside the pitchers, especially in S. pur- nutrient poor habitats, whereas in the north, it has
purea, which provides a relatively long-lasting a relatively short growing season and is strongly
aquatic habitat. Some wasps and spiders may also associated with peatlands. Unlike other pitcher
build nests in pitchers, and block the capture of plants, pitchers of S. purpurea provide a stable
prey by the plant. Information on herbivory and habitat for several months, including over the
pollination ecology of pitcher plants can be found winter, before degrading and losing water in their
in the excellent review of pitcher plant-arthropod second year. In the northern part of the range, the
interactions by Debbie Folkerts. pitcher fluid may freeze during the winter, but the
Most Sarracenia species secrete a small pitcher retains its integrity for at least a few weeks
amount of fluid that collects in the bottom of the into the new season and continues to hold water.
pitcher, and prey collects in this moist zone rich in Like most carnivorous plants, purple pitcher plants
digestive enzymes. The types of prey that are are associated with habitats where nutrients are
attracted and retained by the plant vary with not generally available. Interestingly, the plants
pitcher morphology, mainly relating to the height have been shown to be nutrient limited in locali-
of the pitchers and the size of the pitcher opening, ties even where nitrogen amounts do not appear
but ants are a frequent prey item in most pitcher limiting. In these cases, soil microbes and plants
species. Most species have a hood that covers the such as Sphagnum intercept the nutrients before
pitcher opening, preventing rain from diluting angiosperms like the pitcher plants can assimilate
the digestive enzymes. In contrast, pitchers in them. The ability to capture and digest animal prey
S. purpurea lack this covering hood, so the pitcher provides nitrogen, phosphorus, and some micro-
fills up with rain, providing a larger and more nutrients, and though the plant can grow without
complex aquatic habitat than other Sarracenia prey, the added nutrients are thought to be impor-
species. Most North American studies of carnivory tant for plant processes like flowering.
 Carnivory and Symbiosis in the Purple Pitcher Plant
C 731

Carnivory in Purple Pitcher Plants actual pitcher plant-insect interactions show that
many insects are able to escape from the pitchers
Insects are attracted to the pitchers by both visual and capture efficiency is really quite low. In one
and chemical cues. The plant produces extrafloral study, several thousand insects were recorded in
nectar containing both carbohydrates and amino and around the pitcher mouth, but only about 2%
acids, allowing it to attract a wide variety of insects were captured, and some groups (e.g., ants) were
and other small invertebrates. Nectar, which is quite successful in escaping the pitcher trap. Most
most abundant in newer pitchers, is produced in pitchers that have been evaluated in this authors
nectaries around the pitcher rim, where it accu- lab, though, have had significant deposits of
mulates and entices insects to move downward on decomposing insect detritus in the bottom, and no
the plant. UV light guides and purple streaks are pitchers were devoid of prey, so even if capture
found at the top of the pitchers and these also efficiency is low, it is likely still high enough to add
direct insects into the plant and downward into nutrients to the plant. Young pitchers attract the
the pitcher fluid. Downward pointing hairs pre- most prey, possibly due to the relatively large
vent the insects from escaping, and they eventu- amounts of nectar produced in new pitchers com-
ally drown and are digested by the plant. In most pared to old ones. Pitchers continue to accumulate
Sarracenia species, digestion occurs through prey throughout the summer, however, and the
the action of digestive enzymes (e.g., proteases, highest overall amounts of detritus are found in
hydrolases) produced in glands in the epidermis. the older, overwintered pitchers.
Digestive glands and plant-produced enzymes had
not been shown conclusively in S. purpurea and
digestion was believed to result from proteolytic
activity from bacteria and autolytic enzymes from Limnological Characteristics in
the drowned victims. However, recent study has Pitchers of the Purple Pitcher Plant
shown that not only does S. purpurea produce
digestive enzymes (hydrolases), but that enzyme Individual pitchers on purple pitcher plants
induction relates to pitcher developmental stage form temporary aquatic habitats that can hold
and to the presence of prey. Newly opened pitch- up to about 60 ml of water (for large pitchers),
ers produce hydrolases even before the pitcher fills but more typically hold between 20 and 40 ml.
with water and before any bacteria or prey are The plant maintains a clean water environment
present, but hydrolase levels decline if no prey in pitchers through uptake of CO2 and ammonia,
are captured. The production of hydrolases can be and infusion of oxygen during photosynthesis.
re-induced, though, if prey is attracted to the Oxygen levels are usually maintained at or
pitcher at a later time. This may be a strategy to near saturation for given temperatures (usually
minimize the cost of carnivory to the plant, since 510 mg/L), and pitchers rarely go anoxic in the
digestive enzymes are produced only during the field, and only if prey volumes are unusually high.
time when the pitcher is most attractive to prey or However, other conditions within pitchers are
when prey are actually present. usually highly variable, on both short and long-
Carnivory is usually examined by identifying term scales, with large fluctuations in pH, tem-
the captured and decomposing prey found in perature, and nutrients. Reported pH levels range
pitchers. Ants generally make up the majority of from highly acidic (pH of about 3.0) to near
the prey items, but flies, bees, wasps, moths, beetles, neutral, depending on the pH of rainwater that
leafhoppers, grasshoppers, and spiders are also fills the pitchers, the pH of plant secretions, and
found. Despite all the adaptations that the pitcher the pattern of prey decomposition. Several
shows to attract and retain prey, videotape of researchers have reported that pitcher pH declines
732
C Carnivory and Symbiosis in the Purple Pitcher Plant

over time as prey is captured, and have related for several months, they form surprisingly complex
the declines to the decomposition processes in aquatic communities comprising several trophic
the leaves. We have also found dramatic diurnal levels. The inhabitants have sometimes been referred
variations in pH within individual pitchers, due to as resource parasites, intercepting prey that has
to low alkalinity conditions and the uptake and been captured by the plant and using it for their
release of CO2 during photosynthesis and respi- own growth and development. However, it is now
ration by the plant. clear that these species also free up nutrients
Temperature patterns within the pitcher can and prevent them from becoming sequestered in
also be highly variable, both geographically (over bacteria or protozoa, and can actually enhance
the extremely large geographical range of the release of nutrients to the plant. In return, the
plant) and seasonally or diurnally within a site. pitcher provides habitat and maintains a clean
Pitcher plants usually grow in open bogs in full water habitat by actively taking up the toxic ammonia
sunlight, so can be exposed to a wide range of and CO2 produced by the living organisms in the
ambient temperatures. Conditions within the pitcher.
pitcher usually do not vary as much as in the sur- Several species of aquatic insect have been
rounding bog. recorded alive in S. purpurea pitchers, but many of
Nutrient levels in the fluid depend on the age these (including stoneflies, caddisflies, midges,
of the leaf, mainly because of temporal differ- etc.) are thought to wash into pitchers during bog
ences in the amount of prey captured. Hydrolases flooding events, and survive to emerge but not to
are secreted as the leaf opens and begins attract- actively colonize new pitchers. Three Diptera spe-
ing insect prey, and then these enzymes combine cies (the pitcher plant mosquito, Wyeomyia smithii;
with bacterial action and prey-derived autolytic pitcher plant midge, Metriocnemus knabi; and
enzymes to release ammonia and other dissolved pitcher plant fleshfly, Fletcherimyia fletcheri) are
nutrients. A steady supply of soluble nitrogen is obligate inhabitants of S. purpurea, and have been
therefore supplied for the plant through the widely studied across their range, which approxi-
breakdown of prey. Nitrogen fixing bacteria are mates the range of the plant. At least eight other
also found in pitcher fluid, and these provide a sarcophagids are associated with Sarracenia spp.
further source of nitrogen to the plant. Animals pitchers, including Sarcophaga sarraceniae, and
living within the pitchers (arthropods and the other species of Fletcherimyia, but these are
rotifers) feed on bacteria, protozoa, and the not as well studied as Fletcherimyia fletcheri. Other
decaying prey and they excrete ammonia, which organisms that have been reported from purple
prevents nutrients from becoming sequestered pitcher plants include mites (especially Sarrace-
in the bacteria and protozoa. The ammonia does niopus gibsoni), a rotifer (Habrotrocha rosa), and a
not accumulate to toxic levels since the plant suite of protozoa and bacteria species.
actively takes it up, especially when temperatures
and light are at high levels.

Wyeomyia smithii (Coquillett)

Aquatic Pitcher Inhabitants (Diptera: Culicidae): The Pitcher
Plant Mosquito
All Sarracenia species are associated with a suite
of organisms (arthropods, rotifers, protozoa, bac- The pitcher plant mosquito is, without doubt, the
teria) that reside within the pitcher and form best studied of the pitcher plant inhabitants. Its
communities of varying levels of complexity. Since range is slightly smaller than that of the pitcher
S. purpurea pitchers hold water and provide habitat plant itself, but it still extends over a wide area of
 Carnivory and Symbiosis in the Purple Pitcher Plant
C 733

North America. The life history patterns vary The mosquitoes feed by filtering bacteria, pro-
depending on latitude. The species is univoltine in tozoa, and fine detritus from the water column,
the north and bivoltine or even multivoltine in the and they obtain their oxygen directly from the air
south. It is autogenous for its first ovarian cycle through a breathing siphon, and through their
throughout its range, but will take a blood meal to cuticle. They are tolerant to wide diurnal varia-
mature additional egg batches. It is an obligate tions in temperature, oxygen, and pH.
pitcher plant inhabitant and is restricted to the
purple pitcher plant in the north, though it will
oviposit in other Sarracenia species in the south. Metriocnemus knabi Coquillet
Adult females are attracted to the pitchers through (Diptera: Chironomidae): The
chemical cues and oviposit preferentially into new Pitcher Plant Midge
pitchers, increasing the chance that the pitcher will
retain water throughout the insects life cycle. In The pitcher plant midge has been less studied than
the more northerly parts of the range, adult emer- the mosquito, but is found in pitchers throughout
gence and oviposition correspond to the period most of the range of the plant, and is often present
when pitchers are just opening in spring. Adults in very high numbers in pitchers. Larvae (Fig.17)
desiccate easily, and do not travel far from their can overwinter in more than one instar, depend-
natal pitchers. In one study in Prince Edward ing upon the stage of development when daylength
Island, Canada, it took 6 years for mosquitoes to begins to shorten; for example, different cohorts
recolonize pitcher plants (Fig. 16) that had been may overwinter as 2nd or 3rd or 4th instar larvae.
transplanted from another bog, despite a rich sup- Life cycles may be univoltine or bivoltine, depend-
ply of pitchers with mosquito inhabitants within a ing on the summer temperatures during develop-
few meters of the transplanted plants. ment, and oviposition occurs in both young and
Wyeomyia smithii larvae (Fig.17) overwinter older leaves. The midges are more tolerant to cold
as larvae throughout their range, but again, there than the mosquito, and they are found in many
are differences that relate to latitude. They over- northern bogs where the mosquitoes are absent.
winter as 4th instar larvae in the south, and as 3rd Similar to the mosquito, the midge requires enough
instar larvae in the north (often frozen in the water to maintain an aquatic environment, but if
pitcher fluid), and diapause is both initiated and the pitcher loses water (common in older pitchers
terminated via photoperiod. Recent work has that can lose their integrity), the midge larva can
shown that the photoperiodic responses are chang- crawl from one pitcher to another on the same
ing in response to global warming, and that mea- plant. They pupate in a gelatinous mass on the
surable changes in the required daylength to sides of the pitchers, and adults emerge and mate,
induce diapause have occurred over the last 30 then search for oviposition sites.
years. Despite their ability to overwinter in the fro- The midge lives in the wad of detritus that
zen pitcher fluid in northern locations, they are collects at the bottom of the pitcher, and feeds by
not very tolerant of low temperatures, and will die chewing into the bodies of the drowned insects or
if winter temperatures are too cold, or if sufficient scavenges on the decomposing particulate mate-
snow cover is not available for insulation. There- rial. They respire cutaneously and are relatively
fore, at northern edges of the range, there are many intolerant of low oxygen, so will only be found in
plants, and even entire bogs, where the mosquito pitchers with sufficient oxygen for respiration.
is absent. They also die if there isnt enough aquatic Few natural pitchers experience anoxia, however,
habitat for survival, for example, if the fluid dries so it is rare to find pitchers in northern peat bogs
under drought conditions or if the pitcher devel- without a strong complement of pitcher plant
ops a hole through which the water escapes. midges.
734
C Carnivory and Symbiosis in the Purple Pitcher Plant

Carnivory and Symbiosis in the Purple Pitcher Plant, Figure 16 Glenfinnan bog and pitcher plants, Prince
Edward Island, Canada: (a) bog habitat; (b) purple pitcher plant, Sarracenia purpurea.
 Carnivory and Symbiosis in the Purple Pitcher Plant
C 735

Carnivory and Symbiosis in the Purple Pitcher Plant, Figure 17 (a) Larvae of pitcher plant midge,
Metriocnemus knabi; (b) larva of pitcher plant flesh fly Fletcherimyia fletcheri; (c) larvae of pitcher plant
mosquito, Wyeomyia smithii; (d) modified tubular leaves or pitchers that act as simple pitfall traps for
insects and other small terrestrial animals, and serve as a home to the aforementioned flies.

Fletcherimyia fletcheri (Aldrich) Larvae (Fig.17) are deposited directly into pitcher
(Diptera: Sarcophagidae): The plants, with larvipositing females preferring new
Pitcher Plant Flesh Fly pitchers at the height of their prey attractance.
Usually only one larva is found per pitcher, since
Sarcophagid flies are usually not associated with larvae are aggressive and territorial and will kill or
aquatic habitats, but several species, particularly chase away any additional larvae. Not all larvae die
within the genus Fletcherimyia, are found in after territorial encounters, though, since they are
pitcher plants. Fletcherimyia fletcheri is the most capable of limited movements to other pitchers.
aquatic of the suite of pitcher plant species, and is They are usually considered to be univoltine in the
an obligate inhabitant of the purple pitcher plant. northern part of the range, and multivoltine in
736
C Carnivory and Symbiosis in the Purple Pitcher Plant

the south. Larvae develop in the pitchers, then and dispersal patterns, as well as food webs and
crawl out to pupate in the surrounding moss. energetics, can be studied relatively easily, and
Larvae feed at the surface of the water on with a degree of replication that is not possible in
newly drowned prey items. They attach to the sur- most habitats. They are also easily manipulated,
face tension and breathe surface oxygen through since it is relatively simple to add or remove food
posterior spiracles, so are tolerant to wide varia- materials or top predators, to monitor population
tions in oxygen in the water. effects. Since purple pitcher plants occur over a
vast geographical area, it is also possible to study
ecological processes in entire ecosystems over a
Other Pitcher Plant Inhabitants wide latitudinal range.
The pitcher ecosystem is mainly detritus based,
Mites are often found in pitcher plants, and feed with energy coming from the insects that are cap-
either on the captured prey or on other mite spe- tured by the plant, then drown and decay in the
cies. It isnt clear how the mites disperse from pitcher fluid. The lowest level of the food web is
pitcher to pitcher, but they may travel on the bod- therefore made up of detritivores, including bacte-
ies of the adult insect inhabitants or be associated ria, some mites, the pitcher plant midge, and when
with some of the obligate herbivores of pitcher present, the flesh fly. The pitchers may also contain
plants. A species of bdelloid rotifer, Habrotrocha phytoplankton. Protozoans and rotifers feed on the
rosa, is also common in purple pitcher plants, bacteria and algae, then are themselves fed on by
though it is rarely seen unless pitcher fluid is the top predator in the system, the pitcher plant
examined without preservation, since the rotifers mosquito. There are usually no predators for the
dont preserve well and are usually washed through midges and flesh flies, despite their low position in
sieves before examination. The rotifers are very the food web. Manipulations of various food web
active, however, and can be fascinating to watch, if components have shown that pitcher plant com-
a researcher is patient enough to look for them. munities respond to a combination of top-down
The rotifers feed on bacteria and particulate and bottom-up regulation. Generally, the lower
organic matter in the water column, and may be trophic levels are resource limited with respect to
critical in providing soluble nitrogen and other both population size and taxonomic richness, so as
nutrients to the plant. Protozoan and bacterial resources (prey) are added to pitchers, abundance
species diversity have rarely been enumerated, but and richness increases. In contrast, predator limita-
at least 40 Protozoa species and several bacterial tion targets specific groups only, so that addition of
types have been recorded from pitchers. mosquito larvae results in a decrease in rotifers, but
increases in bacterial abundance and richness.
Many other studies have concentrated on
Pitcher Plants as Model other aspects of community structure, especially
Ecosystems the interactions among the pitcher macrofauna
(midges, mosquitoes, flesh flies). Some studies
Purple pitcher plant leaves provide ideal systems have found that the feeding of the midges releases
for investigating a variety of ecological questions. nutrients that support mosquito populations, in a
The pitchers form small, discrete, aquatic systems processing chain commensalism. Others have
that support complex aquatic communities con- not found relationships among the major insect
sisting of at least three trophic levels. Although groups, suggesting that these patterns may relate
they are aquatic ecosystems, they are located to food availability. A recent study which evalu-
within terrestrial ecosystems, and therefore pro- ated latitudinal trends in species richness across
vide small islands of habitat where colonization most of the range of the purple pitcher plant found
 Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus
C 737

that species richness (mainly of the bacteria and Folkerts D (1999) Pitcher plant wetlands of the Southeastern
United States: arthropod associates. In: Batzer DP, Rader
protozoa) increases with increasing latitude, con-
RB, Wissinger SA (eds) Invertebrates in freshwater wet-
trary to most predictions of latitudinal patterns. lands of North America: ecology and management.
This may also be driven by food web patterns, Wiley, New York, pp 247275
since the top predator in the system, the mosquito, Gallie DR, Chang S-C (1997) Signal transduction in the car-
nivorous plant Sarracenia purpurea: regulation of secre-
declines in abundance with increasing latitude. tory hydrolase expression during development and
response to resources. Plant Physiol 115:14611471
Giberson DJ, Hardwick ML (1999) Pitcher plants (Sarracenia
Summary purpurea) in eastern Canadian peatlands: ecology and
conservation of the invertebrate inquilines. In Batzer DP,
Rader RB, Wissinger SA (eds) Invertebrates in freshwa-
The purple pitcher plant is a widespread carnivo- ter wetlands of North America: ecology and manage-
rous plant which interacts with insects through ment. Wiley, New York, pp 401419
Heard SB (1994) Pitcher-plant midges and mosquitoes: a pro-
carnivory and by providing habitat, as well as
cessing chain commensalism. Ecology 75:16471660
through herbivory and pollination. The pitchers Juniper BE, Robins RJ, Joel DM (1989). The carnivorous
form discrete aquatic habitats within a terrestrial plants. Academic Press, London, UK
landscape, and provide a home to a surprisingly Kitching RL (2001) Food webs in phytotelmata: bottom-up
and top-down explanations for community structure.
complex community of aquatic organisms. Because Ann Rev Entomol 46:729760
of the ease of studying and manipulating these Rice BA (2007) Carnivorous plant FAQ v11.0. Available
habitats, considerable information is available on at (http://www.sarracenia.com/faq.html.) Accessed 2
both the individual taxa and their interactions, May, 2007
Rymal DE, Folkerts GW (1982) Insects associated with pitcher
over a wide geographical range. plants (Sarracenia: Sarraceniaceae) and their relation-
Carnivorous Plants ship to pitcher plant conservation: a review. J Alabama
Insectivorous Plants Acad Sci 53:131151
Van Breeman, N (1995) How Sphagnum bogs down other
Bromeliad Fauna
plants. Trends Ecol Evol 10:270275
Phytotelmata

References Carob Midge Complex,

Asphondylia spp. (Diptera:
Bradshaw WE, Creelman RA (1984) Mutualism between the Cecidomyiidae) in Cyprus
carnivorous purple pitcher plant and its inhabitants. Am
Midl Nat 112:294304
George M. Orphanides
Bradshaw WE, Holzapfel CM (2001) Genetic shift in photo-
periodic response correlated with global warming. Proc A Research Institute, Nicosia, Cyprus
Natl Acad Sci 98:1450914511
Buckley HL, Miller TE, Ellison AM, Gotelli NJ (2003) Reverse In Cyprus, a cecidomyiid complex, Asphondylia
latitudinal trends in species richness of pitcher-plant
food webs. Ecol Lett 6:825829
spp. attacks the pods of carob, Ceratonia siliqua,
Dahlem GA, Naczi RFC (2006) Flesh flies (Diptera: Sar- causing a fruit stunting deformation known as
cophagidae) associated with North American pitcher brachycarpia. This malformation is reported to
plants (Sarraceniaceae), with descriptions of three new have been noticed on the island for the first time
species. Ann Entomol Soc Am 99:218240
Dress WJ, Newell SJ, Nastase AJ, Ford JC (1997) Analysis of around 1870. The adult female (Fig.18) inserts the
amino acids in nectar from pitchers of Sarracenia pur- eggs with its ovipositor in the carob pods when
purea. (Sarraceniaceae) Am J Bot 84:17011706 these are about 0.5 cm long. Infestation becomes
Fish D, Hall DW (1978) Succession and stratification of
evident 710 days later with the pod swelling
aquatic insects inhabiting the leaves of the insectivorous
pitcher plant, Sarracenia purpurea. Am Midl Nat gradually as the midge larva grows. The pupa is
99:172183 formed in the infested pod in a rather hardened
738
C Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus

Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus, Figure 18 Adult of the
carob midge, Asphondylia sp.

whitish niche. Upon completing its development caper the females insert the eggs within the flower
the adult emerges leaving the pupal skins half- bud among the petals, the stamens and on the
protruding from the infested pod. Initially it was ovary. On pepper, squill, potato and St. Johnswort
believed that the cecidomyiid responsible for they insert their eggs in the ovary during the flower-
brachycarpia was Asphondylia gennadii (Marchal) bud stage (Fig.21). As a result, infested flower buds
and that it attacked only carobs. Later biological harden and never bloom. Five or six generations
studies in Cyprus, however, revealed that the develop on the secondary plants, which are avail-
midges from carob pods (Figs.1920) required an able for infestation until SeptemberOctober. At
alternate host for the summer. The adults of the that time, the midges return to carobs to lay their
overwintering generation emerging from carob eggs in the newly formed pods of the normal flow-
pods in April would not deposit their eggs in the ering season for the overwintering generation.
few out-of-season young carob pods that could The above findings stimulated a re-examination
sometimes be available. No alternative points of of the generic placement and the overall taxonomic
attack on the carob tree could be found. Instead, status of the carob gall midge. Adults, larvae and
they would search for secondary host-plants pupae from all the mentioned host plants are
like caper (Capparis spinosa), pepper (Capsicum anatomically identical, suggesting that all these
annuum), potato (Solanum tuberosum), garden midges may belong to one species. However, there
rocket (Eruca sativa), mustard (Sinapis spp.), sea is a differential host preference among adults from
squill (Urginea maritima), asphodel (Asphodelus the various secondary hosts. For example, adult
fistulosus), and St. Johnswort (Hypericum crispum). females from pepper readily attacked only pepper
The successful development of the carob midge on and garden rocket, rarely attacked caper and
all these host plants was proved experimentally in did not attack squill and St. Johnswort. Those from
cages and supported by meticulous observations caper readily attacked caper, mustard, garden
in isolated areas under natural conditions. On rocket, asphodel and St. Johnswort, rarely attacked
 Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus
C 739

Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus, Figure 19 Normal (n) and
midge-infested (i) carob pods.

Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus, Figure 20 Ovipositor of the
carob midge, Asphondylia sp.
740
C Carob Midge Complex, Asphondylia spp. (Diptera: Cecidomyiidae) in Cyprus

CYPRUS
Squill

Mustard

Garden Rocket

Asphodel

St. Johnswort

Pepper Caper

Carob Midge Complex, Asphondylia spp. (Diptera:

Carob Midge Complex, Asphondylia spp. (Diptera:
Cecidomyiidae) in Cyprus, Figure 22 Distribution
Cecidomyiidae) in Cyprus, Figure 21 Differential
of carob midge infestation on pepper in Cyprus.
host preference among carob midge adults from
squill, pepper and caper.

pepper and did not attack squill. Finally, midges of carob pods on each inflorescence is generally
from squill readily attacked squill, garden rocket very large and certainly not all of them reach
and mustard but did not attack pepper and St. maturity. All the unfertilized pods drop at an
Johnswort. early stage of their development unless the carob
In an older survey (19701972) midge infes- midge attacks them. Infested pods do not drop.
tation on carobs and caper, in contrast with that The majority of the fertilized pods will also
on the other host plants, was widely distributed drop at their early growing stages because trees
all over the island. A striking difference, however, cannot bear to maturity all the pods produced.
was observed with the infestation on pepper that Consequently, it is misleading to calculate the
occurred only on the northern coast and the damage by comparing the infested and normal
whole Karpasia peninsula (Fig. 22). The southern pods because among the infested pods, a signifi-
part of the island is still free from midge infesta- cant number would have dropped even in the
tion on pepper. The northern part is now inac- absence of the carob midge. The relationship
cessible to repeat the survey. This characteristic between the estimated loss of yield and the
distribution of midge infestation on the different observed infestation was found to be described
host plants and the midge behavior on host pref- by a second-degree polynomial curve with the
erence indicates that the carob midge complex equation =- 0.12+0.177x+0.00247x2.
consists of the overwintering generation of a
morphologically homogenous but biologically
heterogeneous population of Asphondylia. It is Mortality Factors
possible that there are three races or sibling
species of this gall midge. The natural mortality factors recorded were:
(i) the parasites Eurytoma sp. A., Eurytoma sp.
B., Pseudocatolaccus nitescens (Walker), Tetrastichus
Damage brevicornis (Panzer), Eupelmus urozonus Dalm.,
Adontomerus sp. and Paraholaspis sp.; (ii) predators
On carobs, the estimated loss of yield is signifi- ants, earwigs, spiders; (iii) unidentified molds; and
cantly lower than the apparent one. The number (iv) weather conditions.
 Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae)
C 741

Molds appear in the interior part of the occur in some non-photosynthetic microbial
infested carob pods, causing the death of the midge organisms. Animals are incapable of carotenoid
larva. Subsequently, the pods drop. Ants have been synthesis, but they obtain them from their diet
observed cutting holes through the infested carob where they serve as antioxidants, serve as a pre-
pods and earwigs would enlarge these holes. The cursor to vitamin A, and impart bright coloration.
midge larvae or pupae would then be destroyed Carotenoids are responsible for much of the red,
either by these predators or by the development of orange, yellow, and brown color found in plants, as
molds or they would dry up. Spiders attack adult well as some of the coloration of animals, includ-
midges while the latter rest during the day. The ing insects.
midge mortality occurring from November to At least 600 different carotenoids are known.
April is mainly due to abiotic factors (weather). They are derived from a 40-carbon polyene chain,
The effectiveness of the biotic factors (parasites, and display alternating single and double bonds.
predators and molds) becomes evident from April The specific end groups on these molecules affect
onwards. polarity and help determine how they interact
with membranes. The hydrocarbon carotenoids
are known as carotenes. The oxygenated carote-
References noids are called xanthophylls. Beta-carotene is
perhaps the best known carotenoid.
Anon (1914) Entomological notes. Cyprus Agr J 35:805807 In insects, carotenoids are responsible for
Gagn RJ, Orphanides GM (1992) The pupa and larva of the yellow color of such insects as pierid butter-
Asphondylia gennadii (Diptera: Cecidomyiidae) and
taxonomic implications. Bull Entomol Res 82:313316
flies and the orange of ladybird beetles. Com-
Gennadius P (1902) The carob tree. Government Printing bined with blue pigment, carotenoids can produce
Office, Nicosia, Cyprus, 30 pp green color. One of their most important func-
Harris KM (1975) The taxonomic status of the carob gall midge, tions is the production of the visual pigment
Asphondylia gennadii (Marchal), comb. N. (Diptera, Ceci-
domyiidae), and of other Asphondylia species recorded retinene.
from Cyprus. Bull Entomol Res 65:377380
Morris HM (1930) Report of the entomologist for 1929.
Report of the Director of Agriculture, Cyprus, pp
4755
Orphanides GM (1975) Biology of the carob midge complex, Carpenter Ants, Camponotus spp.
Asphondylia spp. (Diptera, Cecidmyiidae), in Cyprus. (Hymenoptera: Formicidae)
Bull Entomol Res 65:381390
Orphanides GM (1976) Damage assessment and natural
control of the carob midge complex, Asphondylia spp.
John H. Klotz, Laurel D. Hansen
(Diptera, Cecidomyiidae) in Cyprus. Bollettino del University of California, Riverside, Riverside,
Laboratorio di Entomologia Agraria F. Silvestri CA, USA
33:8098 Spokane Falls Community College, Spokane,
WA, USA

Carpenter ants play critical roles in forest eco-

Carotenoids systems as predators of defoliating insects,
decomposers of cellulose, and as vital links in
Carotenoids are among the most common and food webs. They may become serious household
important natural pigments. They are fat-soluble, and pests, however, when they infest structures and
found principally in plants and photosynthetic damage wood.
bacteria, where they are abundant in chloroplasts Carpenter ants belong to the highly diverse
and play a critical role in photosynthesis. They also and cosmopolitan genus, Camponotus, in the
742
C Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae)

subfamily Formicinae (Table 6). The formicines her first brood in isolation, is typical for carpen-
are characterized by their production of formic ter ants. After the spring mating flights, insemi-
acid in the venom gland, a potent alarm phero- nated queens search for suitable nest sites in
mone and defensive compound that is sprayed wood where they construct a cavity and lay a
on its victims. There are 19 other subfamilies in clutch of eggs. The queen does not leave the
the family Formicidae. Of the 288 genera of ants, chamber to forage, instead metabolizing her fat
with approximately 11,800 species described so bodies and wing muscles to provide nourishment
far, Camponotus is one of the most impressive for herself and the growing brood. Depending on
with an estimated 1,000 species worldwide. temperature and species, complete metamorpho-
In the United States and Canada there are sis (development of egg-larva-pupa and adult
approximately 50 species of Camponotus, of which stages) takes from 6 to 10 weeks before the first
24 are considered to be structural or nuisance workers emerge. These first workers are small due
pests. Those causing the most damage belong to to the limited food supply and are therefore called
the subgenus Camponotus. Since the majority of minims. With their arrival, foraging commences
species in this group nest in wood, they are com- and the colony begins to grow. The queen lays a
monly called carpenter ants. Two of the most com- second clutch of eggs in late summer but these
mon species that infest structures are black do not complete development until after winter
carpenter ants, C. modoc in western states, and dormancy. After the first year, the queens of
C.pennsylvanicus in central and eastern states. C. modoc and C. pennsylvanicus have two annual
periods of oviposition, the first in late winter or
early spring and the second in summer. Major
Colony Development (larger) and media (smaller than major, but larger
than minim) workers are not produced until
The claustral mode of colony founding, wherein the third season, and reproductives only after
the queen seals herself off in a chamber and rears several years.

Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae), Table 6 Some common species of
carpenter ants and their geographic distribution
Camponotus species Geographical distribution
C. americanus Mayr Eastern and central USA, SE Canada
C. chromaiodes Bolton Eastern and central USA, SE Canada
C. herculeanus (Linnaeus) Northern USA, Canada, Alaska, Europe
C. ligniperdus (Latreille) Europe
C. modoc Wheeler Western USA, southwestern Canada
C. novaeboracensis (Fitch) Northern USA, southern Canada
C. pennsylvanicus (DeGeer) Eastern and central USA, SE and S central Canada
C. essigi Smith NW Mexico to S Canada
C. nearcticus Emery Northern USA, eastern USA, S Canada
C. sayi Emery Southwestern USA and Mexico
C. floridanus (Buckley) Southeastern USA
C. castaneus (Latreille) Eastern central USA
C. variegatus (Smith) Hawaiian islands
C. vicinus Mayr Western USA, Mexico to S Canada
 Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae)
C 743

Mature colonies are partitioned into a main case of C. pennsylvanicus, for example, odor trails
or parent nest where the queen resides, and into are the primary orientation cue, but workers are
satellite nests that contain workers, mature larvae, also capable of landmark and celestial orientation.
pupae, and winged reproductives. Generating sat- As with other ants, tactile cues are also used for
ellite nests expands the territory of a colony, while orientation, and edge-following is commonly
a network of interconnecting trails maintains observed in carpenter ants, particularly along
communication and flow of resources between structural guidelines in man-made environments.
the nests. The number of satellite nests per colony
and their size varies. For example, ten nests
were counted in a colony of Florida carpenter Foraging
ants, C. floridanus, and 12,000 workers were found
in a satellite nest (Fig.23) of C. modoc. Thus, the Carpenter ants use group foraging to exploit ephem-
total number of ants in a colony may attain over eral resources. The discovery of a food item too
50,000 in the case of C. modoc and more than large to handle individually prompts a scout to
100,000 in C. vicinus. The difference in size may deposit a chemical trail pheromone on the ground
be attributed to the presence of multiple queens as she returns to the nest. The trail pheromone is
(polygyny) in C. vicinus colonies versus a single produced in the hindgut and, in combination with
queen (monogyny) that is typically found in col- formic acid, stimulates trail-following by other ants
onies of C. modoc and C. pennsylvanicus. that the scout actively solicits when she arrives back
Wood with high moisture content is selected at the nest. Established trails are used for more per-
for colony initiation by inseminated queens. Mois- manent resource sites such as aphid colonies that
ture is a requirement for the development of eggs may remain in use from one season to the next. It is
and young larvae, and parent nests will often be thought that the foraging population makes up no
located in areas outside structures where there is more than 10% of the colony population. Some of
sufficient humidity. Satellite nests are typically the larger species make prime targets for visual
found in drier areas because eggs and young larvae predators such as birds, so it is not surprising that
are not present. These nests are often found in their foraging is conducted primarily at night. The
structures under insulation, in attics, wall voids, onset of foraging in C. pennsylvanicus and C. modoc
and subfloors where higher temperatures and is a dramatic event to observe, with large numbers
humidity occur. of ants pouring out of the nest at dusk.

Home Range Trophallaxis

The territory of a colony is determined by its daily Honeydew is a favorite food of carpenter ants.
activity range, which includes the network of trails Excreted by homopterans such as aphids, it con-
connecting its various nests with resource sites. tains sugars, amino acids, minerals, and vitamins.
The area covered by a large mature colony may be Carpenter ants have specialized digestive tracts
considerable. For example, in the case of the Flor- for handling this liquid diet, and removing solids
ida carpenter ant nest complex mentioned above, with a filtration mechanism in their mouthparts.
it spread over an area measuring 43 m across; and The crop, also known as the social stomach, is a
trails 200 m long have been reported for C. modoc. distensible sac located in the gaster of the ant
Many species of carpenter ants are nocturnal, and which expands to hold liquids that are stored,
they have evolved special adaptations for finding transported, and finally regurgitated and shared
their way in the environment at night. In the via trophallaxis with other ants. This food-sharing
744
C Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae)

Carpenter Ants, Camponotus spp. (Hymenoptera: Formicidae), Figure 23 Carpenter ants and damage:
workers of Camponotus vicinus in a nest (above); satellite nest of Camponotus modoc under subfloor
insulation (center); damage caused by Camponotus modoc to building timber (below) (photos by Laurel
Hansen).
 Carpenter Bees (Hymenoptera: Apidae: Xylocopinae)
C 745

behavior among workers, and from workers to of a structure, along door and window frames, and
larvae and the queen, is a fundamental bond in the under the lower edge of siding. Depending on the
social behavior of ants. insecticide used, some act as barriers to the ants
while others are non-repellent. In the latter case,
the insecticide is picked up by the ant and car-
Pest Management ried back to the nest where it can be spread to
other ants. Toxic baits may be effective if they are
The structural pest management industry ranks car- sufficiently attractive to the ants. Their recruit-
penter ants as one of the most important economic ment and food-sharing behavior facilitates the
pests. In certain regions of the United States, such as distribution of a toxicant throughout the colony.
the Northeast and Pacific Northwest, carpenter
ants outrank termites as wood-destroying organ-
isms. They are also notoriously difficult to control. References
In order to be effective, a management pro-
gram for a household infestation of carpenter ants Cannon CA, Fell RD (1992) Cold hardiness of the over-
must be based on a thorough inspection. Ideally, wintering black carpenter ant. Physiol Entomol
17:121126
all of the nests on the property should be located, Hansen LD, Akre RD (1985) Biology of carpenter ants in
both inside and outside. Structural infestations are Washington State (Hymenoptera: Formicidae: Cam-
more commonly caused by satellite nests; however, ponotus). Melanderia 43:163
the original source of the problem often results Hansen LD, Klotz JH (2005) Carpenter ants of the United
States and Canada. Cornell University Press. Ithaca,
from a parent nest located outside. New York, 224 pp
Locating nests is often difficult due to the Klotz JH, Greenberg L, Reid BL, Davis L Jr (1998) Spatial
cryptic behavior of carpenter ants. In this regard, distribution of colonies of three carpenter ants, Cam-
ponotus pennsylvanicus, Camponotus floridanus, Campono-
a feed and follow technique can be helpful.
tus laevigatus (Hymenoptera: Formicidae). Sociobiology
Chopped insects such as crickets or mealworms 32:5162
are provided to the ants, which are then followed Hedges, SA (1998) Field guide for the management of struc-
back to their nest. This technique is most effective ture-infesting ants. Franzak & Foster Co, Cleveland,
OH, 155 pp
when conducted at night when the majority of
foragers are active. Outdoor nests may be located
in live or dead trees, stumps or logs, landscape
timbers, firewood piles, and buried wood. Indoors, Carpenter Bees (Hymenoptera:
common nest locations include crawl spaces and Apidae: Xylocopinae)
attics, often in or under insulation. In addition,
satellite colonies will nest in exterior and interior John L. Capinera
wall voids, and hollow doors. Ant activity is often University of Florida, Gainesville, FL, USA
associated with moist conditions in and around
sinks, dishwashers, bathtubs, showers, and toilets. The common name of these insects is derived
Once the nests have been located, they can be from their nesting habits. Although small carpen-
treated with a contact insecticide appropriate for ter bees, Ceratina spp., excavate tunnels in pithy
the situation (e.g., a dust formulation in a wall stems of various bushes, the large carpenter bees,
void, or spray for infested landscape timbers). If Xylocopa spp., chew nesting galleries in solid wood
nests are not located, there are other treatment or in stumps, logs, or dead branches of trees. Obvi-
options offered by pest control companies. In what ously, the wood-attacking species are the basis for
is known as a perimeter treatment, a band of in- the carpenter bee name designation. The latter
secticide is sprayed around the outside foundation bees may become economic pests if nesting takes
746
C Carpenter Bees (Hymenoptera: Apidae: Xylocopinae)

place in structural timbers, fence posts, and other refurbished, but new nests are also constructed at
wood structures. It is Xylocopa that most people old locations. In new nests, female bees chew their
know about or are concerned about, at least in way into the wood, excavating a burrow about 15 mm
North America. The easiest method of separating in diameter. Boring proceeds more slowly against
Ceratina from Xylocopa is by size: Ceratina are < 8 mm the grain (about 15 mm a day) than with the grain.
in length, whereas Xylocopa are 20 mm or larger. The direction of galleries in the wood appeared to
At various times, carpenter bees have been depend on the direction of the grain. If the grain is
placed in the families Anthophoridae, Xylocopidae, oriented vertically, the nests are vertical; if horizon-
or Apidae, though the most recent placement is tally, then the nests tend to be horizontal with
within the Apidae. This family is characterized, in respect to the ground. Galleries extend about 3045 cm
part, by the jugal lobe of the hind wing being in newly completed nests. New tunnels are smooth
absent or shorter than the submedian cell and by and uniform throughout, but older galleries show
the forewing having three submarginal cells. evidence of less uniformity with random depres-
Within the family, carpenter bees are distinguished sions and irregularities. Apparently these older
most easily by the triangular second submarginal galleries are used by several generations of bees.
cell, and by the lower margin of the eye almost in Also, several bees may use a common entry hole
contact with the base of the mandible (i.e., the connecting to different tunnels. After excavating
malar space is absent). the gallery, female bees gather pollen, which is
Xylocopa spp. generally resemble bumble bees mixed with regurgitated nectar. The pollen mass is
in size and color. They are black, metallic bluish or placed at the end of a gallery, an egg is laid, and the
greenish black, or purplish blue. Some males have female places a partition or cap over the cell com-
yellowish areas on the face. Both sexes may have posed of chewed wood pulp. This process is repeated
pale or yellowish pubescence on the thorax, legs, or until a linear complement of six to eight end-to-end
abdomen, but there tends to be less yellow color cells is completed. Females apparently construct
than in bumble bees. Sometimes they are unicolor- only one nest per year in northern locations, with
ous, ranging from entirely yellow to entirely black. bees emerging in the late summer and overwinter-
Large carpenter bees are readily distinguished from ing as adults, and with mating taking place in the
bumble bees primarily by the absence of pubes- spring. In warm-weather areas such as Florida,
cence on the dorsum of the abdomen, which is however, at least two generations are produced per
somewhat shiny. They also lack a malar space year, with broods occurring in February-March and
(present in bumble bees), and the triangular second during the summer. In Florida, adult bees are
submarginal cell. active from November to January and from April to
Xylocopa virginica is the species of most con- summer.
cern in the USA, though locally other species can be Several types of damage are directly associ-
abundant. Xylocopa virginica normally uses dry, ated with carpenter bees: weakening of structural
coniferous woods as nesting sites, including Pinus, timbers in barns, sheds and other open structures
Juniperus, and Taxodium spp., but some deciduous where bees have ready entry; defacing of wood
woods used in fence railings are also used. Hard- trim on structures, usually the eves of houses; gal-
wood timber is usually avoided. Xylocopa virginica lery excavation in wood water tanks (much less a
selects nesting sites in well-lighted areas where the problem now that metal has replaced wood in
wood is not painted (though they may not be most instances); and human annoyance. The last
deterred by stains) or covered with bark. In general, point is included because carpenter bee females
these bees are gregarious, often building several may sting (rarely, and males do not sting), and
tunnels in the same location, and also tending to male bees may hover or dart at humans who venture
nest in the same areas for generations. Old nests are into the nesting area. In general, carpenter bees are
 Carpenter, Frank Morton
C 747

not much of a threat to people, but this does not stacked within the hollowed stem. The last cell area
prevent people from becoming alarmed because is left incomplete, and she uses this area to rest and
these are large insects. Also, there sometimes is an to defend her nest from intruders. She remains close
indirect effect of carpenter bee colonization on to the nest until her offspring emerge. Interestingly,
structures. Occasionally woodpeckers are attracted because the first laid eggs hatch first, and they are
to tunnels to feed on the brood. If the tunnels are deepest within the hollow stem, the new adults
in a structure, the damage resulting from the (which do not chew their way laterally through the
woodpecker can be significant. wall of the stem) must navigate around the younger,
A buzzing or drilling sound is heard when a less developed siblings stacked above in order to
carpenter bee is boring into the wood. If the hole is escape. The new adults chew through the cell caps,
not visible, as often is the case when the bee is bor- moving the debris down but being careful not to
ing under the eves of houses, their activities can be damage any wasps still in the pupal stage, and
detected by the presence of sawdust on the ground moving the pupae up to rest on the new, elevated
under the hole. As noted previously, carpenter bees floor of the cell. It may take several days for the first-
rarely attack painted or varnished wood. In areas hatching wasp to dig its way out, and by this time
frequented by these insects, damage to structures other wasps likely have hatched, resulting in a trail
can often be prevented by painting. If this is not of adults, all working in tandem to pass cell cap
effective or desirable, a small amount of insecticide material down.
that is labeled for bees and wasps can be applied to Bees (Apidae)
the affected area, including the entryways of the
tunnels. Also, the holes could be plugged with
caulking, putty, or similar substance, or screened. A References
common approach is to spray or dust the tunnels
with insecticide, allow the bees a day or two to con- Balduf WV (1962) Life of the carpenter bee, Xylocopa virginica
tact the insecticide and move it around the tunnel, (Linn.). Ann Entomol Soc Am 55:263271
Daly HV (1973) Bees of the genus Ceratina in America north
and then plug the hole. Alternatively, because the of Mexico. UC Publ Entomol 74:1113
number of bees is usually not great, and because Howard LO (1892) Note on the hibernation of carpenter bees.
the bees are fairly docile, it is usually possible to Proc Entomol Soc Washington 2:331332
capture them all with an insect net and freeze or Hurd PD Jr (1955) The carpenter bees of California. Bulletin
of the California Insect Survey 4:3572
crush them, thereby avoiding the cost and hazard Hurd PD Jr (1958) Observations on the nesting habits of
of insecticides. some new world carpenter bees with remarks on their
Carpenter bees generally are not pests. Even importance in the problem of species formation. Ann
Entomol Soc Am 51:365375
those species considered to be occasional pests,
Hurd PD Jr (1961) A synopsis of the carpenter bees belonging
such as X. virginica, offset their damage by pollina- to the subgenus Xylocopoides Michener. Trans Am
tion services, including pollination of economically Entomol Soc 87:247257
important plants. Hurd PD Jr, Moure JS (1963) A classification of the large car-
penter bees (Xylocopini). UC Publ Entomol 29:1365
Small carpenter bees are never pests because Rau P (1928) The nesting habits of the little carpenter-
they excavate nests and provision only the hollowed- bee, Ceratina calcarata. Ann Entomol Soc Am
out stems of twigs. Like the larger xylocopines, 21:380397
they excavate nests with their mandibles, and use
these cavities for both nesting and overwintering
sites. The female provisions the nest with pollen and Carpenter, Frank Morton
nectar, deposits an egg, then caps the cell with
masticated plant material. Typically she repeats Frank Carpenter was born in Boston, USA, on
the process again and again until several cells are September 6, 1902. His father, although an
748
C Carpenterworm Moths (Lepidoptera: Cossidae)

employee of a business company, had a strong Carpenterworm Moths

interest in natural history, and encouraged (Lepidoptera: Cossidae)
Frank s interest in insects. He entered Harvard
University in 1922, and graduated with an A.B. John B. Heppner
degree in 1926, a master s degree in 1927, and a Florida State Collection of Arthropods,
D.Sc. in 1929. His doctoral thesis on fossil ants Gainesville, FL, USA
was published in 1930, but was preceded by
seven of his earlier papers on fossil insects. In Carpenterworm moths, family Cossidae, total 682
1928 he was appointed at Harvard University as species worldwide; actual fauna probably exceeds
research fellow in applied biology, in 1931 as 750 species. The group is a relict family which has
associate in entomology, in 1932 as assistant retained many primitive features and often is clas-
curator of invertebrate paleontology, in 1935 as sified closer to Tineidae and Psychidae. There are
instructor in zoology, in 1936 as curator of fossil five subfamilies, two of which are exclusively
insects, in 1939 as assistant professor of ento- Neotropical (Chilecomadiinae and Hypoptinae):
mology, in 1945 as Alexander Agassiz professor Chilecomadiinae, Cossulinae, Cossinae, Hypoptinae,
of zoology, in 1969 as Fisher professor of natural and Zeuzerinae. The family is in the superfamily
history, and in 1973 became emeritus professor. Cossoidea (series Cossiformes) in the section
This is the man who built the fossil insect collec- Cossina, subsection Cossina, of the division Ditrysia.
tions of Harvard University s Museum of Com- Adults small to very large (9240 mm wingspan),
parative Zoology. For nearly 40 years, he taught with head small and average or slightly rough
entomology and paleontology. He was chairman scaling; labial palpi upcurved; maxillary palpi
of the Department of Biology in 19521959 and small, 12-segmented; antennae filiform or bipec-
had a heavy role in extension. His research in tinate (antennal tips usually thinner). Wings are
fossil insects spanned 70 years, and he special- elongated (Fig. 24) and hindwings often rather
ized in the Paleozoic fauna. The fossil dragonfly small and rounded; body very robust (the largest
that he described as Meganeuropsis americana, female cossids rival hawk moths in size and mass).
with a wingspan of 29 inches is the largest insect
known. In addition to work on fossil insects, he
worked on systematics of present-day Neuro
ptera, Raphidioidea and Mecoptera. After retire-
ment in 1973, he continued voluntarily to curate
the collection of fossil insects and to edit Psyche,
the journal of the Cambridge [Massachusetts]
Entomological Club (a job he held from 1947 to
1990). His wife Ruth, to whom he was married
for 64 years, was a constant companion and
helper. He died in Massachusetts on January 18,
1994.

Reference
Carpenterworm Moths (Lepidoptera: Cossidae),
Figure 24 Example of carpenterworm moths
Furth DG (1994) Frank Morton Carpenter (19021994): aca-
demic biography and list of publications. Psyche (Cossidae), Stygia leucomelas Ochsenheimer from
101:126144 France.
 Carrion Beetles (Coleoptera: Silphidae)
C 749

Maculation usually various dark shades of brown of these organisms includes a rich and complex
or gray, with various spots or markings; some array of fascinating evolutionary and ecological
lighter or colorful. Adults are nocturnal. Larvae phenomena.
are borers in trunks and limbs. Host plants are Silphids (Fig.26) have the largest bodies and
recorded in a large number of plant families, espe- are the most conspicuous of the staphylinoid bee-
cially all those with larger tree species. A number tles. However, the family is not very species rich by
of species are economic pests of forest trees. beetle standards, containing only 183 extant species.
Commonly, they are known as carrion beetles
due to their frequent association with vertebrate
References carcasses. They are sometimes referred to as large
carrion beetles to distinguish them from other
Arora GS (1976) A taxonomic revision of the Indian species beetles associated with carrion, such as those in the
of the family Cossidae (Lepidoptera). Rec Zool Surv family Leiodidae (which are sometimes called
India 69:1160
Barnes W, McDunnough JH (1911) Revision of the Cossidae
small carrion beetles). Most species eat carrion
of North America. Contr Nat Hist Lepidoptera North although many will also prey on carrion associated
Am 1:(1)135, pl 17 insects, such as maggots, or other carrion beetles.
Buser R, Huber W, Joos R (2000) Cossidae Holzbohrer. In: Some species are phytophagous, or exclusively pre-
Schmetterlinge und ihre Lebensrume: Arten-Gefhrdung
Pro-Schutz. Schweiz und angrenzenden Gebiete, 3:97116, daceous, while at least one species has been found
pl 2. Pro Natura-Schweizerische Bund fuer Naturschutz, only in dung. The primary food source for the
Basel larvae of most species, however, is vertebrate car-
Schoorl JW Jr (1990) A phylogenetic study on Cossidae (Lep-
rion. A radical departure from this ancestral life
idoptera: Ditrysia) based on external adult morphology.
Zoologische Verhandlingen 263:1295, 1 pl history pattern is seen in the species Nicrophorus
Seitz A (ed) (19121937) Familie: Cossidae. In: Die Gross- pustulatus which, although capable of breeding on
Schmetterlinge der Erde, 2:417431, pl 5255 (1912); carrion, has recently been discovered to be a para-
2(suppl):241245 (1933); 287, pl 16 (1934); 6:12641287,
pl 167, 169, 181184 (1937); 10:807824, pl 93, 9699
sitoid of snake eggs perhaps the only known
(1933); 14:540551, pl 7980 (1929). A. Kernen, Stuttgart example of a parasite of a vertebrate that kills and
consumes its host (in this case, snake embryos).
The family contains two subfamilies, each of
Carposinidae which specializes on a different size of carrion.
Carrion feeding members of the subfamily Silphi-
A family of moths (order Lepidoptera). They com- nae, which lack parental care, prefer large verte-
monly are known as fruitworm moths. brate carcasses (>300 g), and are often found on
Fruitworm Moths megafaunal carcasses, such as elk, moose, or bison.
Butterflies and Moths They must share these carcasses with vertebrate
scavengers and a large suite of necrophilous insects
such as the larvae of blow- and fleshflies, some of
Carrion Beetles (Coleoptera: which become prey for the beetles. Adults of the
Silphidae) subfamily Nicrophorinae, which display parental
care and complex subsocial nesting behaviors,
Derek S. Sikes generally only breed by monopolization of a small
University of Alaska Museum, Fairbanks, AK, carcasses (<300 g, usually <100 g) such as those
USA of birds or rodents. These beetles remove small
carcasses from the competitive arena of flies,
Despite the association of silphids with carrion, ants, and other scavengers by burial into a sub-
which is often repugnant to humans, the biology terranean nest hence their common name of
750
C Carrion Beetles (Coleoptera: Silphidae)

burying beetles or sexton beetles. This remark- Morphology

able behavior attracted the attention of early
naturalists and remains the focus of research today. Adult

Length 745 mm (usually 1220 mm); ovate to

Distinguishing Characteristics and moderately elongate, and slightly to strongly dors-
Relationships oventrally flattened (Silphinae). Frontoclypeal
(epistomal) suture absent (Silphinae), or present
The family as a whole has only one, somewhat as fine line (Nicrophorinae). Antennae are 11-seg-
ambiguous, synapomorphy (diagnostic character) mented but appear as 10-segmented in Nicro-
a bulge on the posterior quarter of each elytron. phorinae due to reduced second segment fused
However, silphids can be easily recognized by a to third segment; ending in 3-segmented club,
combination of characters including their necro- usually preceded by two or three enlarged but
philous habits (most species), their size (usually sparsely setose segments (Silphinae and basal
12 cm), their weakly to strongly clubbed anten- Nicrophorinae) or antennomeres 911 forming a
nae, their very large scutellum, which is sometimes large club (Nicrophorus). Pronotum with lateral
as wide as their head, and their tricostate elytra. edges complete, sometimes explanate. Scutellum
There is strong evidence indicating silphids are large often as wide as head. Elytra truncate,
closely related to members of the family Staphylin- exposing 15 abdominal tergites in Diamesus,
idae. Some evidence suggests silphids may actually Necrodes, and Nicrophorinae; not truncate in
belong inside the family Staphylinidae (which remaining Silphinae, covering abdomen; never
would require changing the family Silphidae into a striate; in Silphinae bearing 03 raised costae or
subfamily of the Staphylinidae). carinae per elytron (present but indistinct in
Members of the subfamily Nicrophorinae do Nicrophorinae); with raised callus near posterior
possess an unambiguous synapomorphy a pair end of outermost costa; epipleura usually well-
of stridulatory files on the dorsal surface of developed and with ridge complete almost to apex.
abdominal segment 5 which are used for auditory The elytra of most Nicrophorus, Ptomascopus and
communication between adults before mating Diamesus species usually have broad colored
(courtship songs) and between adults and larvae bands or spots (fascia and maculae) extending
during development, and for defense when dis- laterally to meet epipleura. Abdomen with sternite
turbed. The files are scraped by the underside of 2 not visible between hind coxae but visible later-
the elytral apices when the beetles pump their ally of metacoxae; sternites 38 visible in females,
abdomens forward and backward. Paired stridula- 39 visible in males. Legs with five tarsal segments
tory files are absent from the Silphinae but adults per tarsus. Males usually with broadly expanded
of the basal genera Ptomaphila (Australia) and protarsal segments and longer protarsal setae
Oxelytrum (Neotropics) possess stridulatory (midtarsal also expanded in male Diamesus), pro-
morphology at least one species of Oxelytrum and midtarsi of female similar.
has been observed stridulating. These beetles have
spines on the underside of the elytra that can be
scraped by the abdominal intersegmental mem- Larvae
brane when the beetles move their abdomens from
side to side a phenomenon that has yet to be Length 1240 mm, campodeiform (most Silphi-
studied in the silphines. Because silphines do not nae) or eruciform (Nicrophorinae); elongate, more
nest, presumably the only function of their stridu- or less parallel-sided to ovate, slightly to strongly
lation would be defense. flattened, relatively straight or slightly curved
 Carrion Beetles (Coleoptera: Silphidae)
C 751

ventrally. Body surfaces heavily pigmented and in various endemic island species restricted to
heavily sclerotized (Silphinae), or lightly pig- montane habitats, and into South America along
mented and lightly sclerotized (Nicrophorinae). the Andes. None are found in Africa south of the
Stemmata 6 (Silphinae) or 1 (Nicrophorinae) on Sahara, in Australia (Fig.25), or Antarctica. These
each side. Mandibles lacking mola. Thoracic terga beetles were once thought to be absent from the
and abdominal terga and sterna consisting of one Indian subcontinent south of the Himalayas, but
or more sclerotized plates, without patches or rows there may be a population of the recently described
of asperities, each tergum with 1 (Silphinae) or 2 species Nicrophorus sausai in Meghalaya India, a
(Ptomascopus) lateral tergal processes extending mountainous region isolated from the Himalayas.
beyond edges of sterna or without such processes This unusual, and perhaps relict, population begs
(Nicrophorus) but with four spinose projections additional study and confirmation.
along posterior margin of abdominal terga. One The silphines are more widespread than the
or two segmented, well developed urogomphi. nicrophorines, with greater representation on
Gondwanan areas. This is thought to be related to
their greater generic diversity (12 genera) and
Classification, Diversity, and possible greater age. There are four species in
Distribution Australia and New Guinea (Ptomaphila, 3 endemic
species; Diamesus 1 species) and a larger radia-
In recent years there have been some changes to tion in South America than is seen in the nicro-
the classification and newly described species phorines (Oxelytrum, 8 species). It has been
added, so a current classification, with updated suggested that this radiation of the Silphinae into
species counts, and distributional information is South America and consequently Australia (via
provided below (Table 7). The family currently Antarctica) took place 5060 million years ago
stands at 183 species. producing these, the only two silphid genera
The distribution of an organism is the result endemic to the southern Hemisphere. There are
of both ecology and evolutionary history. Silphids, also three silphine species in South Africa
especially the nicrophorines, are rare in warmer (Thanatophilus, 2 species; Silpha, 1 species) and
climates, such as lowland tropical forests, and vir- an entire silphine genus (Heterotemna, 3 species)
tually absent from dry climates like deserts these endemic to the Canary Islands off the northwest
ecological constraints certainly have limited their coast of Africa. However, as with the nicro-
distribution in places like Africa, Australia, and phorines, most species of the Silphinae are found
Tibet. A few silphids in northern Africa survive in in the northern hemisphere, although they seem
cooler, wetter mountainous regions but the Sahara to be somewhat more tolerant of warm habitats
presumably prevents southward dispersal. The than are the nicrophorines. This tolerance is per-
family Silphidae is thought to have originated in haps due to their preference for larger carcasses
the northern hemisphere on the paleocontinent of which they do not (and could not) defend from
Laurasia. The subfamily Nicrophorinae best repre- competitors. Nicrophorus species, probably due to
sents this with only three species in territory once their requirement for small carcasses that can be
part of the southern landmass of Gondwana. These buried and defended, do not appear to compete
three species are thought to have radiated down well with the ants, flies and carrion-associated
the Andes of South America, having survived in scarab beetles that are more abundant in warmer
the cooler, montane climate. habitats.
The nicrophorines are distributed in the Together, the Silphidae show an amphitropical
northern hemisphere, with species radiations hav- or amphipolar distribution, i.e. they are restricted
ing occurred in the Malay Archipelago, resulting to northern and southern temperate zones but
752
C Carrion Beetles (Coleoptera: Silphidae)

Carrion Beetles (Coleoptera: Silphidae), Table 7 Carrion beetle classification, species counts, and
distribution
Order Coleoptera
Superfamily Staphylinoidea
Family Silphidae Latreille, 1807 15 genera, 183 species
Subfamily Silphinae Latreille, 1807 12 genera, 111 species
Aclypea Reitter, 1884 13 species, Holarctic
Dendroxena Motschulsky, 1858 2 species, Eurasia
Diamesus Hope, 1840 2 species, Asia, Australia
Heterosilpha Portevin, 1926 2 species, West Nearctic
Heterotemna Wollaston, 1864 3 species, Africa: Canaries
Necrodes Leach, 1815 3 species, Holarctic
Necrophila Kirby and Spence, 1828 17 species, Holarctic
subgenus Necrophila Kirby &
Spence, 1828
subgenus Eusilpha Semenov-
Tian-Shanskij, 1890
subgenus Calosilpha Portevin, 1920
subgenus Deutosilpha Portevin, 1920
subgenus Chrysosilpha Portevin, 1921
Oiceoptoma Leach, 1815 9 species, Holarctic
Oxelytrum Gistel, 1848 8 species, SW Nearctic/Neotropical
Ptomaphila Kirby & Spence, 1828 3 species, Australia, New Guinea
Silpha Linnaeus, 1758 25 species, Eurasia, Africaa
subgenus Silpha Linnaeus, 1758
subgenus Phosphuga Leach, 1817
subgenus Ablattaria Reitter, 1884
Thanatophilus Leach, 1815 24 species, Holarctic & Africa, Madagascar
Subfamily Nicrophorinae Kirby, 1837 3 genera, 72 species
Eonecrophorus Kurosawa, 1985 1 species, Nepal
Ptomascopus Kraatz, 1876 3 species, Asia
Nicrophorus Fabricius, 1775 68 species, Holarctic, N Africa, S America, SE Asia

One species of Europe, Silpha trisits Illiger, has been introduced and established in North America (southern Quebec)
a
 Carrion Beetles (Coleoptera: Silphidae)
C 753

Carrion Beetles (Coleoptera: Silphidae), Figure 25 Map of the subfamily Nicrophorinae (Silphidae). 6,736
localities from 17,250 specimens examined showing the known distribution (99% of records are
Nicrophorus). The lack of records throughout much of Russia is almost certainly a collection artifact
whereas the absence of records in Australia, sub-Saharan Africa, most of India and South America is not.
A corresponding map for the subfamily Silphinae has not yet been prepared see text for description of
the distribution of the Silphinae.

generally absent from the intervening tropics the preference of these organisms for cooler cli-
(with the exception of tropical montane habitats). mates, it seems reasonable to infer these beetles
The lesser generic diversity of the nicrophorines may have radiated during this cooling event of the
(3 genera) compared to the silphines, combined Oligocene. Roughly concurrent with this cooling
with their almost pure Laurasian distribution, sup- event, many modern rodent families appeared and
ports preliminary estimates for a younger age of radiated and these would have been ideal prey
the main radiation in the Nicrophorinae (the items for Nicrophorus beetles. In addition to a
genus Nicrophorus) based on fossil and molecular small-mammal radiation during this time, most
divergence dating methods. All known fossils of modern bird orders and families appeared between
the genus Nicrophorus are Eocene or younger, less the early Eocene and the late Oligocene-early
than 50 million years old, with the majority being Miocene, during a period of intense diversifica-
known from the Pleistocene. Molecular dating tion. Small birds are also ideal prey items for
methods provide a preliminary, and wide, range Nicrophorus.
for the radiation of the genus having happened The family is thought to have originated in
5024 million years ago. The transition to the the Old World, and the subfamily Nicrophorinae
Oligocene from the Eocene is thought to represent certainly shows this pattern in which all but one of
the most dramatic climatic change of the Ceno- the five genera/subgenera are endemic to Asia. The
zoic era, in which the Mesozoic hot house world New World has the minority of world species for
was transformed into the Neogene ice house all groups that are also found in the Old World,
world that persists today. Given the absence of and has only two endemic genera: Oxelytrum
Nicrophorus from lowland tropical habitats and and Heterosilpha. One new species of Nicrophorus,
754
C Carrion Beetles (Coleoptera: Silphidae)

carcass itself. Some species are phytophagous

(11 species of Aclypea) while others are predacious
(Dendroxena, some Silpha and possibly Ptomascopus
zhangla, a poorly known and recently discovered
species from China). The silphine Necrodes surina-
mensis as an adult feeds primarily on fly larvae
but can survive on carrion alone. The majority of
silphids that have been studied are nocturnal or
crepuscular (active at sundown and sunrise),
which might help avoid predation by birds.
Some species of the genus Nicrophorus have
become model organisms for research in ecology,
physiology, and behavior particularly dealing
with questions about parental care, the evolution
of sociality, competition, and other behaviors of
nesting organisms (e.g., brood parasitism). There
have been over 150 behavioral ecology studies on
these species in the past 25 years. Subjects of these
studies include, for example, the ability of adults to
regulate their brood size to match the size of the
carrion resource via control of the number of eggs
produced and subsequent parental culling of
Carrion Beetles (Coleoptera: Silphidae),
extra larvae by cannibalism. Other subjects
Figure26 Nicrophorus olidus Matthews, a silphid
investigated include adult competition and fights
found in Honduras and Mexico; female, dorsal and
to win a carcass, pheromone emission, adult strid-
lateral view.
ulatory communication (between parents and
larvae, precopulatory, and defensive), duration
and explanation for paternal care, and antimicro-
N. hispaniola, was recently discovered and described bial properties of anal and oral secretions, among
in the Dominican Republic. This was the first many others. Biparental care, as seen in Nicrophorus,
Nicrophorus described in the New World since is rare in insects in general, and has been the focus
1925, bringing the total to 21 New World species of much investigation.
ofNicrophorus. There are 25 species of Silphinae The typical progression from discovery to
in the New World, combined with the 21 species new offspring for Nicrophorus species proceeds as
of nicrophorines yielding 46 species of silphids follows: A small vertebrate carcass, like that of a
inthe New World. mouse, is found soon after nightfall and often on
the day of its death. If numerous Nicrophorus
beetles find the carcass the beetles begin to fight to
Ecology dominate the resource. Larger bodied beetles tend
to win these competitions with losers retreating,
Silphids are most frequently encountered at verte- sometimes with minor injuries (missing leg parts
brate carrion but are sometimes found associated or cuts in their wing covers). The loser females
with dung or fungi, or at electric lights. Most sometimes lay eggs near the carcass and some of
species will prey on fly larvae or other insects pres- her offspring might enter and develop in the nest
ent on carcasses or dung, in addition to eating the of the winning beetles. The beetles fights usually
 Carrion Beetles (Coleoptera: Silphidae)
C 755

result in a single species remaining, with smaller of the resulting offspring. These beetles, therefore,
bodied species having been excluded. Within the regulate the size of their brood carefully both by
larger species the males fight the males and the laying a clutch size appropriate to the mass of
females fight the females until the largest male and the carrion resource, and by later fine-tuning the
largest female remain in control of the carcass. clutch size if too many eggs hatch by eating the
Courtship stridulation occurs and can lead to late arriving larvae.
rejection of the male by the female if he cannot Parent beetles stay with the larvae during
stridulate as expected. This may help beetles iden- their approximate 2-week development period
tify conspecifics but no one has carefully investi- defending them against possible usurpers (this
gated how this is accomplished. The mechanisms being the major advantage of paternal care). The
by which closely related species avoid hybridiza- parents also tend the larvae, maintain the brood
tion are equally unstudied. The male and female ball and regurgitate food for the larvae. The burying
pair work together to bury the carcass by digging beetles are unusual among insects in having peak
beneath it. If the substrate is too tough the pair levels of juvenile hormone (normally considered a
might move the carcass to more suitable ground gonadotropic hormone in adult insects) during
by laying beneath it and moving it with their legs. the early parental period when the ovaries are
If a male finds a carcass and no females are present small. Parental regurgitations to young larvae
he will emit a pheromone to attract a female. increase larval growth rates, and in some species,
Sometimes males without carcasses will emit are essential for molting from the first to second
pheromone to attract females with whom they try instar. The larvae molt between each of three
to mate. Females, like all insects, can store sperm instars and either pupate to adult and overwinter
for later use and sometimes can find and bury car- as adults or overwinter as a final larval instar
casses alone, using sperm from prior mating to pre-pupa.
fertilize her eggs. This life history of Nicrophorus species is
It can take 524 h for a carcass to be secured based on finding, concealing and monopolizing
below-ground (with smaller-bodied species tend- small carcasses before their competitors. However,
ing to bury less deeply than larger bodied species). they cannot exclude all interested parties in
The carcass is rolled into a ball that minimizes its addition to a vigilance that prevents usurpation
surface area. Fur or feathers are removed and a by other Nicrophorus adults, the parents must con-
brood chamber is built that will house the carcass tend with both bacterial and fungal decay of the
and the developing larvae. The carcass is treated carcass. Recent studies in both North America and
with oral and anal secretions that help preserve Japan have shown that the treatment of the carcass
the resource from microbial decay. The female will with oral and anal secretions by Nicrophorus adults
then lay eggs based on the mass of carcass (between greatly reduces the microbial decay, and a number
10 and 50 eggs is typical) although more eggs are of antimicrobial agents have been identified.
typically laid than larvae that will be reared. Other animals that often accompany the
Because body size is critical to winning contests beetles into their nest include both nematodes and
for carcasses, larger bodied offspring will be more mites (Acari). The nematode-beetle relationship
likely to successfully reproduce than smaller bod- is poorly known with considerable potential for
ied offspring. A carcass resource can yield either future work. At least two nematode species, Rhab-
many small burying beetle offspring, or fewer large ditis stammeri, and R. vespillonis, have been docu-
burying beetle offspring. This selection pressure mented as associates of Nicrophorus vespilloides
has resulted in a behavior known as filial cannibal- and N. vespillo, respectively, although it is certain
ism the parents kill and consume extra larvae that many more, probably undescribed, nematode
that would otherwise lower the average body size species associate with silphids. The nematodes
756
C Carrion Beetles (Coleoptera: Silphidae)

breed on the carrion and their offspring disperse examples of mutualism, commensalism, and para-
to new carrion resources with the new generation sitism, varying with species and conditions. What
of beetles traveling in the gut of the beetle larvae was once thought to be a single species of mite,
and using the adult hindgut and/or genitalia for Poecilochirus carabi, has since been discovered to
transport to a new carcass. Nematodes have been be a species complex of several morphologically
observed in laboratory settings to reach enormous similar, but reproductively isolated species that are
population sizes causing the beetles to abandon specific to their host beetle species. Only a few of
the carcass but it is unknown if this happens in these cryptic mite species have been described or
the wild. The new generation of nematodes will examined in detail. It is likely that most of the 69
form large aggregations on the surface of the known Nicrophorus species have their own (prob-
carcass, each will arch upwards and start to wave. ably undescribed) Poecilochirus species.
They will also form small, living, waving towers by An even more poorly-known symbiotic rela-
climbing on one another. This behavior brings the tionship involving the Silphidae awaits study:
nematodes in contact with the beetles, onto which nematodes of the family Allantonematidae have
they climb. It is not known how or if the beetles been reported as parasites of the burying beetles
have adapted to competitive pressure from these Poecilochirus mites!
nematodes, nor is it known to what degree the
nematodes reduce the beetles fitness.
The mite-beetle relationship is better under- Conservation
stood than that of the nematodes, but remains one
of the more complex and rich areas for future In the USA, much attention has been focused
research. It is not known how many species of sil- recently on the American burying beetle, Nicro-
phids carry mites (phoretic associates) but most of phorus americanus Olivier, a federally listed endan-
the Nicrophorus species that have been studied gered species and one of five giant species in the
ecologically carry them. Like the nematodes, the genus. As recently as the 1930s, this species was
mites life cycle is tied to that of the beetles with considered to be common over most of the eastern
the deuteronymphs (the last pre-adult stage) dis- half of the North American continent. However, it
persing phoretically on the adult beetles. Mites now occurs in <10% of its former range (popula-
present on silphine species probably are using tions are now restricted to a few islands offshore of
them as alternate hosts opportunistically until Rhode Island and Massachusetts and the western
they can transfer to a burying beetle. Many of the periphery of the historic range). This species was
mites appear to be host-specific, and considerable first listed in 1989 and represents an unusual case
taxonomic work remains to done with them. Over of species endangerment in that there are no appar-
14 species of mites from four families (Parasitidae, ent causal factors for its decline that simultaneously
Macrochelidae, Uropodidae, and Histiomatidae) explain why the eight other co-occurring Nicro-
were found on Nicrophorus species in Michigan, phorus species have not declined. Many weakly
USA. The most frequently encountered and well- supported hypotheses have been suggested, includ-
studied mites in this system are those in the genus ing DDT contamination, extinction of the passenger
Poecilochirus (Mesostigmata: Parasitidae). Initial pigeon, deforestation, artificial lighting, loss of
work in the 1960s indicated an apparent mutualis- carrion availability, and an unknown, intrinsic,
tic mite-beetle relationship resulting from the genetic effect. One important difference between
mites predation on fly eggs that would otherwise N. americanus and its congeners is that this species
hatch and compete with beetle offspring. However, requires larger carcasses (>80 g) than its congeners
more thorough examination of this relationship to maximize its reproductive success. Subsequent
has found much greater complexity including work and review of the literature points to a best,
 Carrion Beetles (Coleoptera: Silphidae)
C 757

albeit provisional, explanation of this species mammals and possibly caused by the key inno-
decline based on (i) known population declines vation of small carcass monopolization.
of optimally sized carrion prey species such as From other recent research we have learned
ground nesting birds and the passenger pigeon, that females with a carcass will not attack males
and (ii) increased vertebrate scavenger and conge- who have recently been in contact with a carcass
ner competition for the reduced carrion available. and typically cared for a brood. These males are
The greater pressure from vertebrate scavengers considered to have a breeders badge, a profile of
may have resulted from competitive release after cuticular hydrocarbons that identifies them as
the loss of larger predators (such as the gray wolf parental and those males lacking this scent are
[Canis lupus] and the mountain lion [Felis con- attacked. This addresses questions of how these
color]) and an increase in habitat fragmentation social beetles recognize each other.
and edge habitats. Nicrophorus americanus may It had already been determined that adults
have declined because it is experiencing greater cannot recognize their own larvae from those of other
vertebrate and congener competition for a reduced couples, nor even, of other species of nicrophorines
resource base. The species is being bred in captivity (in Japan, Ptomascopus larvae are sometimes
and work is underway to establish new popula- brood parasites, mixed into broods of Nicrophorus
tions. The attention it has received due to its federal concolor larvae and raised by Nicrophorus parents).
protection has helped its prospects considerably. The mechanism by which parents can minimize
Given the well-documented and recent rise in such brood parasitism is temporal they kill larvae
mean global temperature, some conservationists are that arrive too early or too late around the window
worried about montane island endemics that cannot of time that their own larvae appear.
survive in the warmer lowlands. As our climate Our understanding of the biology and evolu-
changes, the size of these cooler, montane habitats tion of the Silphidae progresses, with continuing
will contract as they gradually move higher in eleva- work on the phylogenetics, reproductive behaviors
tion. There are at least ten Nicrophorus species of basal lineages, brood parasitism, communal
endemic to the higher elevations of various islands breeding, endocrinology, use of stable isotopes to
in the Malay Archipelago. These species, among determine larval diet, and host shifts, although
many other similarly adapted organisms, could many questions remain uninvestigated.
become threatened with extinction if their cooler, Decomposer Insects
montane habitats start to disappear. Some are already Beetles (Coleoptera)
living at the highest elevations available to them.

References
Recent Research
Ratcliffe BC (1996) The carrion beetles (Coleoptera: Silphidae)
of Nebraska. Bull Univ Nebraska State Mus 13:1100
Recent work on these beetles has resulted in Peck SB (2001) Silphidae Latreille, 1807. In: Arnett RH,
some interesting discoveries. In addition to 11 Thomas MC (eds) American beetles: archostemata,
newly described species since 1999, primarily myxophaga, adephaga, polyphaga: staphyliniformia,
from Asia, there has been phylogenetic work vol1. CRC Press, Boca Raton, FL, pp 268271
Scott MP (1998) The ecology and behavior of burying beetles.
underway which has suggested that the relatively Ann Rev Entomol 43:595618
high species richness of the genus Nicrophorus Sikes DS (2005) Silphidae. In: Kristensen NP, Beutel RG (eds)
may have resulted from a rapid radiation a burst Handbook of zoology, vol IV Arthropoda: Insecta part 38,
Coleoptera, Beetles, vol I: Morphology and systematics
of evolution. This radiation was possibly coinci-
(Archostemmata, Adephaga, Myxophaga, Polyphaga
dent with the global cooling during the Oligocene partim) (RG Beutel RAB Leschen, eds) Walter de Gruyter,
and the subsequent radiation of small birds and Berlin, NY, pp 288296
758
C Carsidaridae

Sikes DS, Newton AF, Madge RB (2002) A catalog of the References

Nicrophorinae (Coleoptera: Silphidae) of the world.
Zootaxa 65:1304
Carter HJ (1933) Gulliver in the bush wanderings of an
Australian entomologist. Angus & Robertson, Sydney,
Australia, 234 pp
Zimmerman EC (1993) Australian weevils, vol 3. CSIRO, East
Carsidaridae Melbourne, pp 493494

A family of bugs (order Hemiptera, superfamily

Psylloidea). Carthaeidae
Bugs
A family of moths (order Lepidoptera) also known
as Australian silkworm moths.
Carter, Herbert James Australian Silkworm Moths
Butterflies and Moths
George Hangay
Narrabeen, NSW, Australia
Carton
Herbert James Carter was born on the 23rd of
April 1858 in Marlborough, Wiltshire, England. The paper manufactured by Hymenoptera for nest
He was educated in England, receiving his Bach- construction.
elor of Art Degree in Cambridge. At the age of 24
he migrated to Australia and took up the position
of Mathematical Master at Sydney Grammar Carrier
School. Later on, in 1902, he was appointed as
Principal of Ascham Girls School in Sydney An inert material serving to dilute a pesticide, and
where he worked until his retirement in 1914. to carry it to its target.
Although he was a devoted educator, his interest
in entomology and his contribution to knowl-
edge of the Australian insect fauna were very Carrying Capacity
significant. He became interested in entomology
soon after his arrival in Australia and produced The theoretical maximum population size that an
his first paper on Australian Coleoptera in 1905. area can support indefinitely within defined set of
He traveled and collected extensively in New conditions.
South Wales, Victoria, Tasmania, South Australia
and Western Australia. He collaborated with A.M.
Lea and a number of other entomologists of his Casebearer Moths (Lepidoptera:
era, including with K.G. Blair, the Coleopterist Coleophoridae)
of the British Museum. During his long life he
published 65 papers, including major works on John B. Heppner
Tenebrionidae, Buprestidae and Colydiidae. He Florida State Collection of Arthropods,
described 55 genera and 1,234 species new to Gainesville, FL, USA
science. After retirement he continued his ento-
mological work until his sudden death on the Casebearer moths, family Coleophoridae, com-
16th of April 1940, in the Sydney suburb of prise over 1,525 species worldwide, with most
Wahroonga. being Palearctic (1,082 sp.) and in the genus,
 Casey, Thomas Lincoln
C 759

Hodges RW (1966) Review of the New World species of

Batrachedra with descriptions of three new genera
(Lepidoptera: Gelechioidea). Trans Am Entomol Soc
92:585651
Landry J-F, Wright B (1993) Systematics of the nearctic
species of metallic-green Coleophora (Lepidoptera:
Coleophoridae). Can Entomol 125:549618
Toll S (1962) Materialien zur kenntnis der palarktischen
arten der familie Coleophoridae (Lepidoptera). Acta
Zool Cracoviensia 7:577720, 133 pl
Vives-Moreno A (1988) Catalogo mundial sistematico y de
distribucion de la familia Coleophoridae Hbner, [1825]
(Insecta: Lepidoptera). Boletin de Sanidad Vegetal
12:1196
Casebearer Moths (Lepidoptera: Coleophoridae),
Figure 27 Example of casebearer moths
(Coleophoridae), Coleophora sp. from Florida, USA.
Casey, Thomas Lincoln
Coleophora. Most are in subfamily Coleo- Thomas Casey was born at West Point, New
phorinae, while non-casebearers are in Batra- York state, on February 19, 1857. His father was
chedrinae. The family is part of the superfamily a general of the U.S. army, and he graduated
Gelechioidea in the section Tineina, subsection from the U.S. Military Academy in 1879. As a
Tineina, of the division Ditrysia. Adults small soldier, he traveled widely in the USA, and used
(524 mm wingspan), with head smooth-scaled; every opportunity to collect beetles as well as
haustellum scaled; labial palpi recurved; maxil- building his collection by purchase from others.
lary palpi minute, 2-segmented. Wings usually He also was interested in applied astronomy. He
very elongated and hindwings spindle-shaped was a prolific describer of insect species, pub-
with long fringes. Maculation shades of brown lishing 77 papers between 1884 and 1924, and in
or gray, sometimes mostly white, and unicolor- them describing more than 9,000 species. How-
ous or with various markings or stripes, but ever, he has been widely criticized not only
rarely more colorful and with iridescence. Adults because his descriptions were brief and lacked
may be mostly crepuscular but many are diurnal. illustrations, but because he often selected
Larvae make small cases (except for Batrache- superficial differences between specimens as
drinae), often distinctly shaped for each species the basis of species separation. In other words,
(Fig. 27), skeletonizing host leaves, but some he failed to recognize that morphological char-
are seed borers, leafminers, or stalk borers, or acters may vary considerably within species.
skeletonize leaves beneath frass webs. A few Consequently, many of the species names that
Batrachedrinae are predaceous on scale insects he proposed have subsequently been sunk as
(Hemiptera). Various host plants are utilized. A synonyms. His collection of almost 117,000
few species are economic. Ovovivipary has been specimens including 9,200 holotypes was
recorded for a few species. bequeathed to the U.S. National Museum of
Natural History. He died on February 3, 1925.

References
Reference
Baldizzone G (1996) A taxonomic review of the Coleophori-
dae (Lepidoptera) of Australia. Tijdschrift voor Ento- Herman LH (2001) Casey, Thomas Lincoln. Bull Am Mus Nat
mologie 139:97144 Hist 265:5354
760
C Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae)

Cassava Mealybug, Phenacoccus parthenogenetic, which means that it reproduces

manihoti Matile-Ferrero without males.
(Hemiptera: Pseudococcidae) The life cycle is completed within 1 month
and the mealybug reproduces throughout the
Peter Neuenschwander year, without any resting stages. It attacks cassava,
International Institute of Tropical Agriculture, Manihot esculenta Crantz (Euphorbiaceae), the
Cotonou, Bnin, West Africa related Ceara rubber Manihot glaziovii Mull. Arg.,
as well as the interspecific hybrid of these two
This is one of many insects that came to the atten- plants, which are of South American origin. At
tion of science only after it had been inadvertently extreme outbreak levels the infestation spills over
transported and established on a new continent. to many other plants of different species which
In the early 1970s, mealybug infestations suddenly happen to grow in the vicinity of infested cassava,
devastated cassava (in French: manioc) in the but when infestations are low no other plant
Congo and what is today the Democratic Republic species are attacked.
of Congo, around the two capitals Brazzaville and
Kinshasa, respectively. From there, this new plague
spread rapidly, at a speed of over 100 km per year. Damage
It got new footholds in Nigeria, near the border to
Benin, then on the border between Gambia and Mealybugs suck preferentially in the growing tip
Senegal, and within a few years had covered the and on the underside of leaves. During heavy
entire cassava growing area of Africa from Senegal attacks the undersides of leaves are covered with a
to Ethiopia and to South Africa. By the mid-1990s, white mass. Mealybugs eject surplus sugar water,
only the Indian Ocean Islands including Mada- which accumulates on the leaves below as a sticky
gascar were still free of this pest, and they have cover of honeydew, which is subsequently attacked
remained so up to today (2001). by fungi. The resulting black sooty-mold cover
Wherever this mealybug, which was newly reduces photosynthesis, and sucking of the insect
described as Phenacoccus manihoti Matile-Ferrero, in the growing tips leads to stunting. In areas
and belonging to the family Pseudoccocidae, where cassava leaves are eaten as a vegetable,
turned up it became the most important cassava such use is made impossible by heavy mealybug
pest, threatening the supply of the main staple infestation. Accumulation of carbohydrates in the
food for about 200 million Africans. storage tubers, which in cassava is a continuous
process, is reduced, and quality is impaired. Tuber
yield losses of up to 80% have been recorded. In
Morphology and Biology addition, because of the stunting, planting sticks
are of poor quality, which compromises the fol-
This is a typical mealybug; pinkish, covered with lowing years crop. Thus, cassava cultivation has
white waxy dust, oval in shape (34 mm length) disappeared from vast areas during the height of
with no wings, weak legs, and long sucking mouth the cassava mealybug epidemic.
parts on the ventral side (Fig. 28). Yellowish
eggs are laid in daily batches protected by wax fila-
ments, mostly underneath the tip of the abdomen Control Options
of the female. The tiny first instar larvae disperse
all over the plants and can be transported by wind. Wherever this mealybug appeared for the first
The three nymphal instars resemble each other and time, extension services tried to combat it with
the adult, except for the size increase. This species is pesticides. As the mealybug is often hidden in the
 Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae)
C 761

Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae), Figure 28

The cassava mealybug, Phenacoccus manihoti, on a cassava leaf (upper left); the exotic parasitoids
Apoanagyrus lopezi (upper right) and A. diversicornis (middle left); one of the widespread and
common indigenous coccinellids, Hyperaspis pumila (middle right); and cassava field devastated by
cassava mealybug (lower) (from Neuenschwander (2005) In: Evaluating indirect ecological effects of
biological control. CABI, Wallingford, UK).

buds, insecticides are generally inefficient, all the Similarly, cassava varieties were tested in a
more because they also preferentially kill the natural quest to find and/or develop resistant varieties.
enemies. In fact, it was demonstrated that repeated As stand-alone component, resistant/tolerant
insecticide applications led to an explosion of the varieties did, however, not give satisfactory
mealybug population. results.
762
C Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae)

The Solution: Biological Control Second instar hosts yield only male parasitoids,
which though small are fully functional; fourth
Cassava was brought to Africa from South America instars yield mostly females, which because of
by Portuguese traders in the sixteenth century, their large size can produce more eggs than small
though it acquired todays importance only in the females.
early twentieth century. It was therefore surmised Several other natural enemies, among them the
that this new mealybug came from South America wasp A. diversicornis Howard and several predatory
and that classical biological control, i.e., the trans- lady beetles, mainly Hyperaspis notata Mulsant
fer of natural enemies that keep this insect under and Diomus hennesseyi Frsch (Coleoptera: Coc-
control in its original home, could bring the cinellidae), were collected mostly in Paraguay and
solution. Foreign exploration, i.e., the search for Brazil in the course of several years and shipped to
natural enemies, in Latin America was undertaken CABI in the United Kingdom for quarantine.
by several international research organizations, There, the insects were reared and checked to
including CAB International and the International be: (i) free of diseases, (ii) not harmful to plants,
Institute of Tropical Agriculture (IITA), but the (iii) not hyperparasitic, i.e., harmful to indigenous
cassava mealybug remained elusive. In the course parasitoids, and (iv) not harmful to useful insects
of this exploration, another mealybug was discov- like bees and silkworms. They were then sent to
ered, Phenacoccus herreni Cox and Williams, but IITA in Nigeria, with the necessary Nigerian
when its parasitoids were tested they did not attack import permits and under the umbrella approval
the P. manihoti known from Africa. of the Inter-African Phytosanitary Council of the
In 1981, a researcher from the Centro Inter- Organization for African Unity. Further studies,
nacional de Agricultura Tropical (CIAT) finally mass rearing with specially developed equipment,
found P. manihoti in Paraguay. Under the leader- and releases followed. In the early 1980s, on the
ship of IITA, foreign exploration was then con- strength of encouraging results in Nigeria, these
centrated and P. manihoti was found on cassava in exotic insects were sent to all African countries
a few sites in the Rio de la Plata valley in Paraguay, requesting them. Releases were executed mostly
Brazil and Bolivia. from the ground and, in a few instances, by aircraft
The first natural enemy of P. manihoti to be using a specially developed apparatus. Thus, a
discovered, the parasitic wasp Apoanagyrus total of about 150 releases was made by IITA,
(Epidinocarsis) lopezi de Santis (Hymenoptera, always in close collaboration with the quarantine
Encyrtidae), eventually also proved to be the best authorities and scientists of the various African
biological control agent. Mated females lay their countries.
eggs into mealybugs (second to fourth instars), By the mid-1990s, A. lopezi was established
where a larva develops freely floating in the everywhere in Africa where P. manihoti occurred.
coelom of the mealybug. Sometimes the host tries It sometimes had dispersed long distances from
to mount a defense action by encapsulating the the release sites (170 km within ten generations of
parasitic larva, but this is successful only in about A. lopezi was documented). The other parasitoid
10% of cases (which might include larvae that failed to establish (i.e., it could not be recovered
died for other reasons). The larva pupates in the after 1 year) and the two coccinellids (Fig. 28)
sausage-shaped dry remains of the mealybug, established only locally in the Democratic Republic
called a mummy, from where the adults emerge, of Congo, Malawi, and perhaps some East African
after a total life cycle of about 2 weeks. Because countries, where they had to compete with numer-
the female determines the sex of its offspring by ous common indigenous lady beetle species.
adding or withholding sperm during oviposition A. lopezi became the target of extensive impact
into the host, she can exploit the host to its best. studies, using paired sleeve cages, chemical
 Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae)
C 763

exclusion experiments, simulation modelling on disturbed by the invasion of P. manihoti, which

the basis of laboratory studies, and direct monitoring offered numerous indigenous predators a new and
through field surveys in many countries. As a result, ample food. With the collapse of this food source,
this is one of the best-researched examples of clas- the abundance of these general predators, as well
sical biological control of an exotic arthropod pest. as of hyperparasitoids, declined drastically, pre-
Wherever A. lopezi had been present for about 2 sumably back to pre-invasion levels.
years (34 years in the East African highlands), The population equilibrium of P. manihoti has
mealybug populations dropped tenfold to non- remained low for the last 20 years, with an occasional
economic levels, thus validating the model predic- short-term low peak in abundance. Ten to 15 years
tions. In local spots with exceedingly poor soils, after the establishment of A. lopezi, extension services
such as pure sand without any mulch, mealybug and governmental research organizations in most
populations, though lower than before, remained previously affected countries reclassified P. manihoti
high enough to cause damage despite the presence as an insect of minor importance. The stability of
of A. lopezi. For such conditions, any further release the system is only disturbed where insecticide inter-
of A. lopezi is useless, but strengthening the plants ventions on neighboring crops like cotton, or against
by applying mulch successfully tipped the balance grasshoppers, disturb the balance by killing the
and reduced mealybug infestation considerably. wasps. This leads to an upsurge in P. manihoti popu-
The key features that made A. lopezi such a lations, a situation well known to practitioners of
successful biological control agent (particularly in integrated pest management.
comparison to A. diversicornis) were: (i) an excep- In field experiments, yields under conditions
tional host finding capacity, higher than any of its of biological control of P. manihoti were compared
exotic or local competitors; (ii) acceptance of a with those where mealybug infestations had been
wide range of host stages; (iii) extensive host feeding, artificially boosted. In surveys, various factors
whereby the female wounds its host and sucks its affecting yield were quantified and their contribu-
hemolymph, thereby killing small hosts outright; tion to yield attributed. On the basis of these results,
(iv) fast development (almost two generations for the savings due to biological control of P. mani-
one by its host; he same as for A. diversicornis). hoti were extrapolated to all affected countries and
These advantages clearly outweighed the per- compared with the investment into this project.
ceived low reproductive rate, low (but density According to different scenarios of how farmers
dependent) parasitism rate, and the fact that can cope with loss of cassava, returns for each
A.lopezi was attacked by local hyperparasitoids. In dollar invested were between $200 and $740. For
fact, 16 species of wasps were found to have switched this evidently successful project, its former leader
over to A. lopezi. They came from parasitoids, mostly was honored with the World Food Prize.
Anagyrus spp. (Hymenoptera, Encyrtidae), that Area-Wide Pest Management
attack Phenacoccus madeirensis Green, a common
mealybug on cassava. Except for an odd case, these
Anagyrus spp. could not reproduce on P. manihoti. References
Though at the time of the release in the early
1980s no indigenous mealybug species had been Gutierrez AP, Neuenschwander P, Schulthess F, Herren HR,
Baumgaertner JU, Wermelinger B, Loehr B, Ellis CK
tested and the whole concept of non-target effects (1988) Analysis of biological control of cassava pests in
was not yet prominent, food-web studies after Africa. II. Cassava mealybug Phenacoccus manihoti.
the establishment showed that A. lopezi developed JAppl Ecol 25:921940
Hammond WNO, Neuenschwander P (1990) Sustained bio-
on P. manihoti only. Environmental effects of this
logical control of the cassava mealybug Phenacoccus
biocontrol project were thus limited to the manihoti (Hom.: Pseudococcidae) by Epidinocarsis
impact on a ecosystem that had been temporarily lopezi (Hym.: Encyrtidae). Entomophaga 35:515526
764
C Cassava Pests and their Management

Herren HR, Neuenschwander P (1991) Biological control of few purchased inputs such as fertilizers and pesti-
cassava pests in Africa. Ann Rev Entomol 36:257283
cides. As yields are low in these systems, pest
Neuenschwander P (1996) Evaluating the efficacy of bio-
logical control of three exotic homopteran pests in control is of low priority due to the high costs and
tropical Africa. Entomophaga 41:405424 the long crop cycle, which may require various
Neuenschwander P (2001) Biological control of cassava applications.
mealybug in Africa: a review. Biol Control 21:214229
Neuenschwander P, Markham R (2001) Biological control
The dynamics of cassava production are
in Africa and its possible effects on biodiversity. In: changing, however, as trends in the food, feed and
Wajnberg E, Scott JK, Quimby PC (eds) Evaluating industrial sectors are leading to an increased
indirect ecological effects of biological control, CABI demand for high-quality cassava starches. In Latin
Publishing, Wallingford, UK, pp 127146
Zeddies J, Schaab RP, Neuenschwander P, Herren HR (2001) America, there are indications of a shift toward
Economics of biological control of cassava mealybug in larger scale production units where cassava is
Africa. Agric Econ 24:209219 grown as a plantation crop, and it is advantageous
for farmers to employ a multiple planting and
harvesting production system in order to meet the
Cassava Pests and their constant market demands of the processing indus-
Management tries. In this type of production system, the cassava
crop will be found at several different growth
Anthony C. Bellotti stages in the same or surrounding fields. Evidence
CIAT (International Center for Tropical now indicates that pest problems will be com-
Agriculture), Cali, Colombia pounded in these overlapping production systems.
Populations of certain pests such as whiteflies,
The origin of cassava (Euphorbiaceae: Manihot hornworms and mealybugs tend to increase when
esculenta Crantz) is the Neotropical Americas, a constant food supply (e.g., young cassava foliage)
where it is estimated that domestication occurred is available. Given this trend, with the concomitant
some 7,0009,000 years ago. At present this peren- increase in pest populations and damage, there
nial shrub is grown throughout the tropical regions will be a greater tendency to apply pesticides to
of the world. The highest production is in Africa control pest outbreaks.
(ca. 55%); while Asia and Latin America account The Consultative Group for International
for 27 and 18%, respectively. In the case of yields Agricultural Research (CGIAR) has two research
on an average per-hectare basis, they are highest in centers the International Center for Tropical
Asia (14.1 t/ha) and the Americas (12.7 t/ha) and Agriculture (CIAT, Cali, Colombia) and the Inter-
lowest in Africa (8.5 t/ha). Cassava is cultivated national Institute of Tropical Agriculture (IITA,
mainly for its starchy roots and is ranked as the Ibadan, Nigeria) with global and regional (Africa)
sixth most important caloric source in the human mandates, respectively, for cassava, oriented toward
diet and the fourth most important staple in the resource-poor farmers. Today, there is a need to
tropics. Cassava leaves may also be consumed and invest in cassava research in order to understand
may be an important source of protein in some fully the role of pests and diseases in these multiple
African countries and Northeast Brazil. production systems, where different stages of
Cassava is vegetatively propagated, has a long the crop overlap, providing a constant source of
growth cycle (824 months), is drought tolerant, nourishment.
and is often intercropped with staggered planting Following is an overview of the cassava
dates so it is almost always present in farmers arthropod complex, and the corresponding damage
fields. Most cassava is grown by small-scale farmers to the crop, aspects of biology, behavior, and man-
in traditional farming systems, often on marginal agement of the most important pests are explored
or fragile soils under rain-fed conditions, using for the following categories: foliage feeders,
 Cassava Pests and their Management
C 765

stemborers/stem feeders, soil-borne pests and where mealybug populations are controlled by
secondary pests. This is followed by a look at future natural enemies not found in Brazil. Phenacoccus
trends. manihoti, which has caused severe crop damage in
Africa, had, until recently, been reported only
from Paraguay, the Mato Grosso area of Brazil,
The Cassava Arthropod Pest and the Santa Cruz area of Bolivia. In 2005, this
Complex and Crop Damage species was collected from the states of Bahia and
Pernambuco in northeastern Brazil. The spread of
Not surprisingly since cassava originated in the P. manihoti into the drier, hotter regions of Brazil
Neotropics, the greatest diversity of arthropods is probably associated with the movement of
reported attacking the crop is from these regions cassava planting material (i.e., stem cuttings) from
(Table 8). More than 200 species have been southern Brazil into the northeast.
reported, many of which are specific to cassava The cassava pest complex can be divided into
and have adapted in varying degrees to the array two groups: those that have probably co-evolved
of natural biochemical defenses in the host, which with cassava, which is their primary or only host;
include laticifers and cyanogenic compounds. and generalist feeders that may attack the cassava
The pest complex varies greatly among the crop sporadically or opportunistically and are often
major cassava-growing areas in the Americas, Africa limited in geographic distribution. The first group
and Asia. The crop, whose origin is in South Amer- includes the Mononychellus mite complex, mealy-
ica, was introduced into Africa in the 1500s and bugs, the hornworm Erinnyis ello, lacebugs, white-
into Asia in the seventeenth century. In Asia, none flies, stemborers, fruit flies, shoot flies, scales, thrips
of the major Neotropical pests has become estab- and gall midges. The generalist feeders consist
lished, and native arthropods that have adapted to mainly of a complex of white grub species, termites,
cassava have not been reported as causing serious cutworms, grasshoppers, leaf-cutting ants, bur-
economic damage. In Africa, the whitefly Bemisia rower bugs, crickets, Tetranychus mite species and
tabaci is presently considered to be the major pest other stemborers.
of cassava because it is the vector of cassava mosaic The most serious pests of cassava those
disease (CMD). Moreover, recent reports indicate causing economic damage or yield losses are
that B. tabaci is also causing root yield reductions generally those that have co-evolved with the crop,
due to direct feeding on the crop. There is also the including mites, hornworms, whiteflies, mealy-
possibility of the accidental introduction of pests bugs, lacebugs and stemborers. Generalist feeders
via planting material, which can wreak havoc. The reported causing yield losses, often on a localized
cassava green mite (Mononychellus tanajoa) and basis, include burrower bugs, white grubs, leaf-
the cassava mealybug (Phenacoccus manihoti), cutting ants and grasshoppers.
which were introduced from South America, have Most cassava arthropod pests cause indirect
caused considerable crop losses and have been the plant damage because they are foliage or stem
target of massive biological control efforts. feeders, reducing leaf area, leaf life or photosyn-
Studies indicate that several arthropod spe- thetic rate. Those pests that can attack the crop
cies can cause considerable yield loss and that the over a prolonged period, especially during season-
pest complex is not geographically uniform. Two ally dry periods (36 months) can cause severe
cassava mealybug species offer an example of the yield losses as a result of decreased photosynthesis,
geographic influence on crop damage. Phenacoccus premature leaf drop and death of the apical
herreni, which has caused considerable damage in meristem. Potential yield reduction by these pests
northeast Brazil, was probably introduced from can be greater than that by cyclical pests such as
northern South America (Venezuela or Colombia), hornworms, leaf-cutter ants and grasshoppers,
766
C Cassava Pests and their Management

Cassava Pests and their Management, Table 8 Global distribution of important arthropod pests
ofcassava
Arthropod pest Major species Americas Africa Asia
Mites Mononychellus caribbeanae x
Mononychellus tanajoa x x
Tetranychus urticae x x
Oligonychus peruvianus x
Stemborers Chilomima clarkei x
Coelosternus spp. x
Lagochirus araneiformis x
Lagochirus spp. x x x
Lacebugs Vatiga illudens x
Vatiga manihotae x
Vatiga lunulata x
Amblystira machalana x
Burrower bugs Cyrtomenus bergi x
Pangaeus piceatus x
Tominotus communis x
Termites Heterotermes tenuis x
Coptotermes sp. x x x
White grubs Phyllophaga menetriesi x
Phyllophaga obsoleta x
Phyllophaga sneblei x
Leucopholis rorada x
Hornworm Erinnyis ello x
Erinnyis alope x
Tiger moth Phoenicoprocta sanguinea x
Leaf-cutter ants Atta sexdens x
Atta cephalotes x
Acromyrmex landolti x
Scale insects Aonidomytilus albus x
Parasaissetia nigra x
Ceroplastes sp. x
Saissetia miranda x
Pests of dried cassava Araecerus fasciculatus x x x
(stored)
Lasioderma serricorne x x x
Rhyzopertha dominica x x x
Tribolium castaneum x x x
Sitophilus oryza x
 Cassava Pests and their Management
C 767

Cassava Pests and their Management, Table 8 Global distribution of important arthropod pests of
cassava (Continued)
Arthropod pest Major species Americas Africa Asia
Sitophilus zeamais x x
Prostephanus truncatus x x
Gall midge Jatrophobia brasiliensis x
Whiteflies Aleurotrachelus socialis x
Aleurothrixus aepim x
Aleurodicus dispersus x x x
Bemisia afer x x
Bemisia tuberculata x
Bemisia tabaci x x x
Trialeurodes variabilis x
Shootflies Neosilba perezi x
Silba pendula x
Fruit flies Anastrepha pickeli x
Anastrepha manihoti x
Mealybugs Phenacoccus manihoti x x
Phenacoccus herreni x
Phenacoccus gossypii x
Phenacoccus madeirensis x
Ferrisia virgarta x
Root mealybugs Pseudococcus mandio x
Stictococcus vayssierei x
Leafhoppers Empoasca bispinata x
Sacphytopius fuliginosus x
Scaphytopius marginelineatus x
Grasshoppers Zonocerus elegans x
Zonocerus variegatus x
Thrips Frankliniella williamsi x x x
Corynothrips stenopterus x
Scirtothrips manihoti x
Scolothrips sp. x

which cause sporadic defoliation; however, these causes root punctures during feeding that can intro-
highly visible pests often induce cassava producers duce fungal pathogens that reduce root yield and
to apply pesticides. quality. White grubs have been found feeding
Few cassava pests damage cassava roots directly. directly on cassava roots causing yield loss and
Three exceptions are burrower bugs (Cyrtomenus severe root rot. Yield losses of 17% have been
bergi), white grubs (Scarabaeidae) and root mealy- reported for P. mandio feeding on cassava roots in
bugs (e.g., Pseudococcus mandio). Cyrtomenus bergi southern Brazil.
768
C Cassava Pests and their Management

In general, arthropod pests are most damag- extent, in Asia. Currently, they may be causing
ing during the dry season, being less severe in more crop damage and yield loss on cassava than
areas of considerable and consistent rainfall; how- any other pest attacking the crop.
ever, there are exceptions to this rule. Hornworm There is a large species complex associated
attacks will frequently occur at the onset of the with the crop, the importance of which can vary
rainy season when there is considerable new between regions or continents. The largest com-
growth and young leaves. Severe whitefly attacks plex on cassava is in the Neotropics, where 11 species
often coincide with the rainy season when young, are reported, including Aleurotrachelus socialis,
succulent leaves are preferred for oviposition. Trialeurodes variabilis, Aleurothrixus aepim, Bemisia
Studies have also shown that burrower bugs and tuberculata and Bemisia tabaci (=B. argentifolii).
white grubs prefer soils with higher soil moisture Aleurotrachelus socialis and T. variabilis cause
content. considerable direct damage and yield losses in
The cassava plant is well adapted to long peri- northern South America (Colombia, Venezuela
ods of limited water and responds to water short- and Ecuador) and in certain regions of Central
age by reducing its evaporative (leaf) surface America. Trialeurodes variabilis is observed
rapidly and efficiently and by partially closing the primarily in the higher altitudes (over 1,000 m),
stomata, thereby increasing water-use efficiency. while A. socialis is confined to lower altitudes (up
The crop has the potential to recover and compen- to 1,200 m). Aleurothrixus aepim is found in
sate for yield losses from seasonally dry periods high populations causing yield loss in Northeast
and pest attack due to the higher photosynthetic Brazil.
rate in newly formed leaves. Younger leaves play a Bemisia tabaci, the vector of CMD, caused by
key role in plant carbon nutrition. Most pests pre- several geminiviruses, has a pantropical distribu-
fer the younger canopy leaves; thus, dry-season tion, feeding on cassava throughout most of Africa,
feeding tends to cause the greatest yield losses in several countries in Asia and more recently in the
cassava. Neotropics. It has been speculated that the absence
Climate change predictions indicate that cer- of CMD in the Americas may be related to the
tain agricultural lands will receive less rainfall in inability of its vector to colonize cassava effectively.
the future. The cassava crop may have a compara- Prior to the early 1990s, the B. tabaci biotypes
tive advantage in these extended seasonally drier found in the Americas did not feed on cassava.
regions; however, increased cassava production in The B biotype of B. tabaci, regarded by some as a
the Neotropics and Africa could result in more separate species (B. argentifolii), has been collected
severe pest outbreaks, reducing yields and/or from cassava in several regions of the Neotropics.
increasing pesticide use. Although seldom observed in high populations, it
is now considered that CMD poses a more serious
threat to cassava production given that most tradi-
Management of Cassava tional cultivars grown in the Neotropics are highly
Arthropod Pests susceptible to the disease.

Foliage Feeders Damage

Whiteflies can cause direct damage to cassava by
Whiteflies feeding on the phloem of leaves, inducing leaf
Considered one of the worlds most damaging curling, chlorosis and defoliation. High popula-
agricultural pest groups, both as direct feeders and tions, combined with prolonged feeding, result in
virus vectors, whiteflies attack cassava-based agro- considerable reduction in root yield. Yield losses
ecosystems in the Americas, Africa and, to a lesser resulting from A. socialis and A. aepim activity are
 Cassava Pests and their Management
C 769

common in Colombia and Brazil, respectively. Arecent survey in an important cassava-growing

With A. socialis feeding, there is a correlation region of Colombia showed that 34% of the
between duration of attack and yield loss. Infesta- farmers surveyed applied chemical pesticides
tions of 1, 6 and 11 months resulted in a 5, 42 and for whitefly control versus only 4.6% applying
79% yield reduction, respectively. More recently, biological products. Farmer field trials in the
yield losses of 58% due to T. variabilis feeding have region revealed a 58% reduction in yield due to
been recorded in the Andean region of northern whitefly attack; however, 52% of the farmers
South America. In several East African countries, surveyed employed no control measures. Pesti-
yield losses due to direct feeding by B. tabaci cide applications have not provided adequate
have been recorded in recent years as a result of control, probably for lack of knowledge of
the higher populations observed. In Uganda, whitefly biology, especially the immature stages
over 50% reductions in root yield have been (the presence of eggs and early-instar nymphs).
recorded. Moreover, around 88% of the farmers had little
or no knowledge of whitefly biology, behavior
Biology and Behavior and management. This has resulted in inappro-
Research with A. socialis and A. aepim indicates priate timing of applications and the misuse of
that populations of both species can occur chemical pesticides.
throughout the growing cycle (1 year or more) but Recent research and field observations on
are usually highest during the rainy season when cassava whiteflies in the Neotropics indicate that
there is considerable new growth. Aleurotrachelus control measures, especially pesticide applica-
socialis females prefer ovipositing on the under- tions, are compromised because of the whiteflys
sides of the young apical leaves, reaching a high of capacity for rapid population increases and its
244 eggs (avg. 181, min. 155) per female. The indi- ability to develop high levels of pesticide resis-
vidually oviposited banana-shaped eggs hatch in tance. When A. socialis feeds on a susceptible cas-
about 10 days and pass through three feeding sava variety, it doubles its population every 4.2
nymphal instars and a pupal stage (4th instar) days. When there are overlapping crop cycles (e.g.,
before reaching the winged adult stage. During the multiple plantings) and favorable rainfall pat-
third instar the body color changes from beige to terns, the conditions are ideal for a rapid buildup
black, surrounded by a waxy white cerosine, making in whitefly populations as a constant food supply
this species easy to distinguish from other whitefly of young cassava leaves are available for adult
species feeding on cassava. Aleurotrachelus socialis feeding, high oviposition and nymphal develop-
egg-to-adult development was 32 days under ment. Field observations indicate that once white-
growth chamber conditions (281C, 70% RH). fly populations begin this rapid increase, they are
Aleurotrachelus socialis may be specific to cassava very difficult to control, requiring repeated pesti-
as populations have not been observed on other cide applications that disrupt natural biological
plant species. control and that are also uneconomical for small
farmers. This capacity for rapid population
Control buildup makes it urgent to introduce efficient
Integrated management of cassava whiteflies management practices early in the plant growth
depends on having effective, low-cost, environ- cycle, possibly during the first month of plant
mentally sound technologies available for farmers. growth and before the economic threshold is
A successful whitefly control program requires reached.
continual research input to acquire the basic Four methods of whitefly control in cassava
knowledge needed to develop the technologies are discussed: host plant resistance (HPR), bio-
and strategies for appropriate implementation. logical, cultural and chemical.
770
C Cassava Pests and their Management

Host Plant Resistance Given that B. tabaci is a pantropical species

This form of resistance to whiteflies is rare in cul- that is the vector of CMD, which causes severe
tivated crops. HPR studies initiated at CIAT more cassava crop damage in Africa and India, several
than 20 years ago have systematically evaluated cassava genotypes were sent by CIAT to NRI (Nat-
the accessions in the CIAT cassava germplasm ural Resources Institute-UK) to be evaluated for
bank for resistance to whiteflies, especially A.socia- resistance to B. tabaci. Genotype MEcu 72 had
lis. Of approximately 5,500 genotypes evaluated in the lowest rate of B. tabaci oviposition so it was
the field in Colombia, about 75% are susceptible, introduced into Uganda during 2005 and will be
with damage ratings above 3.5 (1 = no damage, included in a breeding program to develop white-
6=severe damage). Emphasis is placed on those fly-resistant varieties.
genotypes with damage ratings under 2.0 (about
8%). As there may be susceptible escapes due to Biological Control
insufficient selection pressure, they are reevalu- Numerous natural enemies are found associated
ated in subsequent trials. Several sources of resis- with whiteflies on cassava in the Neotropics
tance to A. socialis have now been identified: (Table 9). In recent field explorations in Colombia,
Genotype MEcu 72 has consistently expressed a Ecuador, Venezuela and Brazil, a complex of parasi-
high level of resistance, while MEcu 64, MPer 334, toids, predators and entomopathogens were col-
MPer 415 and MPer 273 express moderate to high lected from several whitefly species. The most
levels. When feeding on resistant genotypes, representative group is that of the microhy-
A. socialis has less oviposition, a longer develop- menopteran parasitoids. The richness of species in
ment period, smaller size and higher mortality Colombia, Venezuela and Ecuador is primarily
than those feeding on susceptible genotypes. Aleu- represented by the genera Encarsia, Eretmocerus
rotrachelus socialis nymphal instars feeding on and Amitus, frequently associated with A. socialis.
MEcu 72 and MPer 334 suffered 72.5 and 77.5% Gaps in knowledge about this natural enemy com-
mortality, respectively, mostly in the early instars. plex have limited the determination of their effec-
A cross between MEcu 72 (female parent, tiveness in biological control programs. There is
whitefly resistant) and MBra 12 (male parent, little knowledge regarding levels and rates of para-
high yielding, good plant type) resulted in 128 sitism by species or specification of the host and
progeny, four of which were selected for whitefly its effect on the regulation of whitefly populations.
resistance, yield and cooking quality. These four Eleven species of parasitoids (5 genera) were
hybrids, along with susceptible genotypes and collected from the cassava-growing regions of
local farmer varieties, were evaluated at three sites Colombia; an additional five species were collected
in Tolima Province in Colombia by CORPOICA- from Ecuador and seven from Venezuela. On the
MADR (Colombian Corp. for Agricultural Caribbean Coast of Colombia, A. socialis was para-
Research/Ministry of Agricultural and Rural sitized by eight species, with the genus Eretmocerus
Development) over a 4-year period. CG 48931 comprising 70% of the parasitoids. In Magdalena
was selected for high whitefly resistance, high Province, 73% of A. socialis parasitism was by Ami-
yield and good cooking qualities. In 2003, it was tus macgowni, followed by Encarsia sp. (26%). In
officially released by MADR under the name of the Andean region Eretmocerus spp. parasitized all
Nataima-31. It has attained yields of 33 t/ha, whitefly species, but Encarsia pergandiella was the
outyielding the regional farmers variety in Tolima predominant parasitoid of T. variabilis.
by 34% with no pesticide applications. Nataima-31 More than 20 species of entomopathogens
is now being grown commercially in several areas have been reported infecting whiteflies on cassava,
of Colombia and has been introduced into Ecua- including Aschersonia sp., Lecanicillium (Verticil-
dor and Brazil. lium) lecani, Beauveria bassiana and Paecilomyces
 Cassava Pests and their Management
C 771

Cassava Pests and their Management, Table 9 Natural enemies of important cassava arthropod pests
Principal species Parasitoids Predators Entomopathogens
Aleurotrachelus Amitus macgowni Delphastus sp. Beauveria bassiana
socialis
Encarsia sp. D. quinculus Lecanicillium lecani
Encarsia hispida D. pusillus Aschersonia aleyrodes
E. bellotti Chrysopa sp. nr. cincta
E. sofia Condylostylus sp.
E. luteola
E. americana
E. cubensis
Metaphycus sp.
Euderomphale sp.
Signiphora aleyrodis
Eretmocerus spp.
Aleurothrixus aepim Encarsia porteri Cladosporium sp.
E. aleurothrixi
Aleurodicus dispersus Encarsia sp.
E. haitiensis
Aleurotonus vittatus
Eretmocerus sp.
Bemisia tuberculata E. hispida Condylostylus sp.
E. pergandiella
Euderomphale sp.
Encarsia sp. prob.
variegata
Metaphycus sp.
Eretmocerus sp.
Bemisia tabaci Encarsia sophia Delphastus pusillus
E. lutea Condylostylus sp.
E. formosa
E. mineoi
Eretmocerus mundus
Trialeurodes variabilis Encarsia sp. Chrysopa sp. nr. cincta Aschersonia aleyrodes
E. pergandiella Condylostylus sp. B. bassiana
E. Sophia L. lecani
E. luteola
E. strenua
772
C Cassava Pests and their Management

Cassava Pests and their Management, Table 9 Natural enemies of important cassava arthropod pests
(Continued)
Principal species Parasitoids Predators Entomopathogens
E. hispida
E. bellotti
E. nigricephala
Eretmocerus spp.
Aleuroglandulus Encarsia guadeloupae, Nephaspis namolica
malangae Encarsia desantisi
Mononychellus Insects: Hirsutella thompsoni
tanajoa
Stethorus tridens Neozygites floridana
S. darwin N. tanajoae
S. madecasus
Oligota minuta
O. gilvifrons
O. centralis
O. pigmaea
Delphastus argentinicus
Chrysopa sp.
Mites/Phytoseiidae:
Typhlodromalus manihoti
T. aripo
Neoseiulus idaeus
Galendromus annectes
Euseius concordis
Euseius ho
Phenacoccus Apoanagyrus lopezi Cleothera onerata
manihoti
Acerophagus sp. Hyperaspis sp.
Nephus sp.
Chrysopa sp.
Sympherobius sp.
Typhlodromalus aripo
Phenacoccus herreni Acerophagus coccois Ocyptamus sp. Cladosporium sp.
Apoanagyrus diversicornis Sympherobius sp. Neozygites fumosa
Aenasius vexans Hyperaspis sp.
Anagyrus insolitus Nephus sp.
A. thyridopterygis Cleothera onerata
A. pseudococci C. notata
 Cassava Pests and their Management
C 773

Cassava Pests and their Management, Table 9 Natural enemies of important cassava arthropod pests
(Continued)
Principal species Parasitoids Predators Entomopathogens
Anagyrus sp. nr. Greeni Diomus sp.
Aenasius sp. nr. Coccidophylus sp.
putonophylus
Prochiloneurus dactylopii Scymnus sp.
Chartocerus sp. Olla sp.
Hexacnemus sp. Curinus colombianus
Eusemion sp. Cycloneda sanguinea
Hippodamia convergens
Azya sp.
Chrysopa sp.
K. coccidarum
Zelus sp.
Phenacoccus gossypii Anagyrus sp. Curinus colombianus Cladosporium sp.
Apoanagyrus sp. Cleothera onerata
Aenasius masii Coccidophylus sp.
Acerophagus coccois Scymnus sp.
Hexacnemus sp. Olla sp.
Eusemion sp. Hippodamia convergens
Haltichella sp. Azya sp.
Prospaltella sp. Chrysopa sp.
Signiphora sp. K. coccidarum
Pentillia sp.
Sympherobius sp.
Ocyptamus sp.
Kalodiplosis coccidarum
Zelus sp.
Emesaya sp.
Frankliniella williamsi Orius sp.
Scirtothrips manihoti T. aripo
Vatiga illudens Zelus sp.
Vatiga manihotae Zelus nugax
Erinnyis ello Trichogramma spp. Chrysopa spp. Bacillus thuringiensis
Telenomus sphingis Podisus nigrispinus baculovirus of E. ello
Cotesia americana P. obscurus Metarhizium
anisopliae
Cotesia sp. Polistes carnifex Beauveria bassiana
Euplectrus sp. P. erythrocephalus Paecylomices sp.
774
C Cassava Pests and their Management

Cassava Pests and their Management, Table 9 Natural enemies of important cassava arthropod pests
(Continued)
Principal species Parasitoids Predators Entomopathogens
Drino macarensis P. versicolor Nomuraea rileyi
Drino sp. P. canadensis Cordyceps sp.
Euphorocera sp. Polybia emaciata
Sarcodexia innota P. sericea
Thysanomia sp. Zelus nugax
Belvosia sp. Zelus sp.
Forciphomyia eriophora Calosoma sp.
Cryptophion sp. Dolichoderus sp.
Ooencyrtus sp. Alcaeorrhynchus grandis
Chetogena scutellaris
Spiders:
Tomicidae
Salticidae
Erinnyis alope Trichogramma spp. Spiders:
Telenomus sp. Tomicidae
Salticidae
Chrysopa sp.
Chilomima clarkei Brachymeria sp. Metarhizium
anisopliae
Tetrastichus howardi Beauveria bassiana
Trichogramma sp. undetermined virus
Aonidomytilus albus Prodilis sp.
Saissetia miranda Anagyrus sp.
Metaphycus sp.
Scutellista cyanea
Anastrepha pickeli Opius sp.
Anastrepha manihoti Opius sp.
Cyrtomenus bergi Nerthra sp. Heterorhabditis sp.
Metarhizium
anisopliae
Steinernema sp.
Phyllophaga Campsomeris dorsata Metarhizium
menetriesi anisopliae
Beauveria bassiana
Stictococcus Anoplolepis tenella
vayssierei
Zonocerus elegans Metarhizium
anisopliae
 Cassava Pests and their Management
C 775

Cassava Pests and their Management, Table 9 Natural enemies of important cassava arthropod pests
(Continued)
Principal species Parasitoids Predators Entomopathogens
Beauveria bassiana
Zonocerus variegatus Metarhizium
anisopliae
Beauveria bassiana
Iatrophobia Torymoides sulcius
brasiliensis

fumosoroseus; however, there has to be a careful those in monoculture. Yield losses in cassava/
selection of the species, as well as the identifica- maize, cassava monoculture and mixed cultivar
tion of native isolates of entomopathogenic fungi. systems were ca. 60% versus only 12% in cassava/
Greenhouse experiments at CIAT with an isolate cowpea intercrops.
of L. lecani resulted in 5872% A. socialis nymphal When cassava is grown in overlapping cycles
mortality and 82% egg mortality. The L. lecani iso- or multiple plantings, it is difficult to break the
late has been formulated into a commercial biope- whitefly development cycle so rapid population
sticide BioCanii. The commercial biopesticide buildups occur. Upon emerging from the pupal
Mycotrol, (isolate of B. bassiana, a product of stage, adults migrate to feed and oviposit on
Laverlam S.A.), gave very effective control (over recently germinated young plants in adjacent
90% mortality of the egg and first two nymphal fields. A successful tactic for countering this situa-
instar stages) of A. socialis in greenhouse experi- tion is to implement a closed season, defined as
ments at CIAT. Mycotrol, which is also effective an interdiction or prohibition when cassava can-
against B. tabaci and T. variabilis, is presently being not be present in the field. Field observations at
evaluated in field trials. CIAT have shown that a 1- to 2-month period with
The most frequently observed predators feed- no cassava in the field decreases whitefly popula-
ing on cassava whiteflies are chrysopids (Neu- tions dramatically over a 4-year period. The suc-
roptera: Chrysopidae). These generalists feed on the cess of this ban is enhanced by the fact that A.
eggs and immature stages of numerous arthropods. socialis does not appear to have efficient alternate
Chrysoperla carnea is frequently collected feeding hosts so their populations crash when adults can-
on A. socialis in cassava fields. In lab studies at CIAT, not find an alternate host species to sustain or
A. socialis egg and nymphal consumption by increase populations. Nevertheless, the economic
C.carnea were measured by recording the time practicality of this strategy for the producers is
required for 50% consumption of the prey state debatable. In many regions a constant supply of
being offered. Chrysoperla carnea adults required cassava roots is economically desirable for meet-
80 h to consume 50% of the nymphal instars and ing the demands of local fresh and processing
pupae and 77 h to consume 50% of the eggs. markets. This same tactic would not be as effective
for a species such as B. tabaci, which has numerous
Cultural Control alternate hosts where its populations can be sus-
In traditional cropping systems cassava is often tained and multiply.
intercropped, a practice that has been shown to
reduce populations of certain pests. Intercropping Chemical Control
cassava with cowpeas reduced egg populations of Several products with new or novel active
A. socialis and T. variabilis by 70% compared to ingredients have been evaluated for controlling
776
C Cassava Pests and their Management

A.socialis and T. variabilis. Foliar applications of losses of 21, 25 and 53%, respectively. Under high
theamethoxam and imidacloprid were most mite populations on the Colombian Atlantic
efficient in reducing whitefly populations. Best Coast, yields were reduced by 15% in resistant
control was obtained when applied as a drench at cultivars compared with an average 67% loss in
a high doses (0.8 and 0.6 l/ha) on young plants. susceptible cultivars. In Africa, M. tanajoa was
The treatment of cassava planting material (stem first reported from Uganda in 1971; within 15
cuttings) with a 7-min emersion in a solution of years it had spread across most of the cassava-
theamethoxam (Actara) (1 g/l H2O) is also giv- growing belt, occurring in 27 countries and causing
ing promising results. More than two pesticide estimated root losses of 1380%. CGM has been
applications during the crop cycle should be the objective of a major biological control effort
avoided. Field experiments have shown that pesti- since the early 1980s.
cides need not be applied after 6 months of crop
growth as yield loss due to whitefly attack will not Biology and Behavior
occur. A cost-benefit analysis indicates that chem- Mites, especially the cassava green mite, are dry-
ical pesticide applications for whitefly control in season pests that can cause yield losses where
cassava are generally uneconomical for small there is a seasonally dry period of at least 3
farmers and only slightly beneficial for large farm- months. At the onset of the rainy season, mite
ers who can generally receive a higher price for populations decrease and cassava plants produce
the product. Research is under way to evaluate the new foliage. If the rains do not persist, cassava
feasibility of substituting entomopathogens as green mite populations will again increase, caus-
biopesticides to replace chemical pesticide ing defoliation and more severe yield losses. This
applications. pattern has been observed in the semiarid cassa-
va-growing regions of Northeast Brazil. Cassava
Cassava Mites green mite populations prefer to feed on the
More than 40 species of mites have been reported undersides of young emerging leaves, which
feeding on cassava in the Americas, Africa and develop a mottled whitish to yellow appearance
Asia. The most important are Mononychellus tana- and may become deformed or reduced in size.
joa (syn. = M. progresivus), Mononychellus carib- Heavy infestations will cause defoliations, begin-
beanae, Tetranychus cinnabarinus and Tetranychus ning at the top of the plant, often killing apical
urticae (also reported as T. bimaculatus and T. and lateral buds and shoots.
telarius). Cassava is the major host for the Monon- The adult is green in color with an average
ychellus spp., while the Tetranychus spp. have a body length of about 350 m. Females oviposit on
wide host range. Mononychellus tanajoa, the cas- the leaf undersurface; eggs hatch in 34 days (30C
sava green mite (CGM), is the most important and 705% RH). At 15, 20, 25 and 30C, the egg-
species, causing crop losses in the Americas and to-adult stage is 41.4, 19.5, 10.3 and 7.8 days,
Africa. It is native to the Neotropics, first being respectively. These data indicate that cassava
reported from northeast Brazil in 1938. It is pres- green mite populations can increase rapidly in
ently found in most cassava-growing regions in warm regions of the lowland tropics. At 30C, each
the Americas, especially in seasonally dry regions female oviposits 90120 eggs; during the initial
of the lowland tropics in Brazil, Colombia and population buildup, mostly females are produced,
Venezuela. adding to the rapid population increase.

Damage Management
In experimental fields in Colombia, M. tanajoa Pesticide applications for controlling mites on a
attacks of 3, 4 and 6 months resulted in yield long-cycle crop such as cassava are not a feasible or
 Cassava Pests and their Management
C 777

economic option for low-income farmers. Moreover, conducted by CNPMF/EMBRAPA, primarily in

even low doses of pesticides have adverse effects on the semiarid regions of the northeast. Of the 300
natural enemies. Cultural control methods have not cultivars identified by CIAT as promising for CGM
been explored, and there is little mention of their resistance (over several years and 27 field cycles),
use in the literature. Research into the control of 72 have consistently had damage ratings below
M. tanajoa has followed two main thrusts: HPR and 3.0. Low-to-moderate levels of resistance are indi-
biological control. It is expected that these two com- cated by 03.5 (06 damage scale).
plementary strategies can reduce cassava green mite Mite resistance-mechanism studies indicate
populations below economic injury levels. strong antixenosis (preference vs nonpreference)
for oviposition, as well as moderate antibiosis.
Host Plant Resistance In lab studies, M. tanajoa displayed a strong
It is hypothesized that in the presence of efficacious ovipositional preference for susceptible varieties.
natural enemies, only low-to-moderate levels of When paired with the moderately resistant culti-
HPR are needed to reduce CGM populations below vars MEcu 72, MPer 611 and MEcu 64 in free-
economic injury levels. A level of resistance that choice tests, 95, 91 and 88%, respectively, of the
would hinder, delay or suppress the initial buildup eggs were oviposited on the susceptible cultivar
of cassava green mite populations could provide CMC 40. Antibiosis is expressed by mites having
sufficient opportunity for establishing effective lower fecundity, a longer development time, a
natural enemy populations that would prevent an shorter adult life span, and higher larval and
eruption of the cassava green mite population. nymphal mortality when feeding on resistant
Therefore an important objective of an HPR strat- versus susceptible cultivars.
egy is to develop cultivars that are not highly sus-
ceptible to the cassava green mite and that hopefully Biological Control
contain low-to-moderate levels of resistance. Beginning in the early 1980s, extensive evalua-
Immunity or even high levels of resistance do not tions of the natural enemy complex associated
appear to be available in M. esculenta germplasm. with cassava mites were conducted at more than
A considerable effort has been made to identify 2,400 sites in 14 countries of the Neotropics. The
cassava green mite resistance in cultivated cassava. primary target in most of these field and lab stud-
CIAT, IITA and several national research programs ies was the cassava green mite. These ongoing
in the Americas and Africa have screened cassava extensive surveys indicate that the cassava green
germplasm for cassava green mite resistance. Of mite is present throughout much of the lowland
the more than 5,000 landrace cultivars in the CIAT Neotropics. High populations, which can cause
cassava germplasm bank, only 6% (300 cultivars) significant yield loss, occur most frequently in
were identified as having low-to-moderate levels of Northeast Brazil and can be localized.
resistance. A select number of cultivars with moder- Geographic regions of the Americas were
ate levels of resistance have been released to farmers identified and prioritized using GIS support to
after a considerable effort by plant breeders and assist in targeting specific areas for exploration.
entomologists. Two hybrids (ICA Costea and Homologous maps based on agrometeorological
Nataima 31), both with low levels of mite resistance, data and microregional classification comparing
are being grown by cassava farmers in Colombia. Africa and the Neotropics were prepared as one of
Most mite-resistance field evaluations by the major targets for biological control in those
CIAT have been carried out in the lowland tropics areas of Africa where the cassava green mite was
with a prolonged dry season (46 months) and causing economic damage.
high mite populations (Colombian Atlantic Coast). A total of 87 phytoseiid species were collected
In Brazil, cassava green mite evaluations were and stored: 25 are new or unrecorded species; 66
778
C Cassava Pests and their Management

were collected from cassava. The current predator Typhlodromalus manihoti (found in over 50% of
mite reference collection held at CIAT conserves the fields surveyed), Neoseiulus idaeus, Typhlo-
primarily those related to phytophagous mites dromalus aripo, Galendromus annectens, Euseius
found on cassava. A taxonomic key on the species concordis and Euseius ho.
associated with cassava is being prepared with More than ten species of phytoseiids were
Brazilian colleagues. The CIAT-Brazil collection is shipped from Colombia and Brazil to Africa, via
a true reference collection with accompanying quarantine in England (IIBC-International Institute
database and can be readily used for species of Biological Control). None of the Colombian
description. Explorations also identified several species became established, but three of the Brazilian
insect predators of cassava green mite, especially species did (T. manihoti, T. aripo and N. idaeus).
the staphylinid Oligota minuta and the coccinellid Typhlodromalus aripo, the most successful of the
Stethorus sp. After extensive lab and field studies three species, has now spread and is found in more
of this cassava green mite predator complex, it than 14 countries. Typhlodromalus aripo inhabits
was generally agreed that the phytoseiid predators the apex of cassava plants during the day and
offer the best potential for controlling mites, espe- forages on leaves at night; it can persist during
cially when occurring in low densities. The phyto- periods of low cassava green mite densities by
seiid development cycle is shorter than that of consuming alternative food sources (e.g., maize
the cassava green mite. In studies at CIAT with the pollen). On-farm trials in Africa indicate that
species Neoseiulus anonymus, the egg-to-adult T. aripo reduces CGM populations by 3560% and
development period at 25 and 30C was 4.7 and increases fresh root yield by 3037%.
4.0 days, respectively. This is approximately half Neozygites sp. is a fungal pathogen (Zygomy-
the development period for the cassava green mite cetes: Entomophthorales) found on mites through-
at those temperatures. Survey data also revealed out cassava-growing regions of the Neotropics.
that cassava green mite densities were much higher Isolates of Neozygites floridana from Brazil and
in northeast Brazil than in Colombia, but the rich- Colombia, and from M. tanajoa from Brazil and
ness of phytoseiid species was greater in Colombia. Benin were evaluated on the cassava green mite in
Field data from experiments in Colombia Africa. Laboratory and field studies indicate that
demonstrated that a rich phytoseiid species com- the Brazilian strain of N. floridana was the most
plex could reduce cassava green mite populations virulent. Although this fungus shows considerable
and prevent cassava yield loss. When natural enemies promise for biological control of the cassava green
were eliminated by applying low doses of an aca- mite, further research and field evaluations are
ricide that did not affect the cassava green mite needed.
population, cassava root yields were reduced by Exotic phytoseiid mite predators can play an
33%. Application of an acaricide did not increase important role in reducing CGM populations in
yields, indicating the effectiveness of biological Africa; however, field observations in the Neotropics
control. indicate that they are very sensitive to disturbances
A major objective of the surveys for cassava in the agroecosystems, especially the use of pesti-
green mite natural enemies and the substantial cides. For example, when insecticides were applied
research that followed was to identify the key at CIAT for controlling thrips, cassava green mite
phytoseiid species controlling cassava green mite populations erupted, and few phytoseiid predators
populations and introduce them into Africa. This were detected in the fields. Studies in Colombia
was a collaborative effort between CIAT and showed that low acaricide doses that did not cause
EMBRAPA in the Americas and IITA in Africa. Of mortality to cassava green mite were lethal to phyto-
the phytoseiid species identified as feeding on seiids, causing a considerable increase in mite popu-
CGM, those most frequently collected were lations and cassava yield losses. In the Neotropics,
 Cassava Pests and their Management
C 779

especially on larger plantations, cassava farmers may ranged from 6888%, depending on cultivar sus-
use pesticides to control hornworm, whitefly or ceptibility. Farmers in northeast Brazil estimated
thrips outbreaks. This could result in mite outbreaks their losses to be over 80%, and cassava produc-
and yield losses if biological control is the only con- tion decreased in the region during the 1980s. In
trol measure, and highly susceptible cultivars are Africa, yield losses due to P. manihoti feeding and
being grown. damage were around 80%.

Cassava Mealybugs Biology and Behavior

Although more than 15 species are reported attack- Both species are morphologically similar and orig-
ing the crop, only two are important economically, inally thought to be only one species. Phenacoccus
Phenacoccus herreni and P. manihoti, both of manihoti is parthenogenic, whereas males are
Neotropical origin. Phenacoccus manihoti was required for reproduction of P. herreni. The females
introduced inadvertently into Africa in the early deposit ovisacs containing hundreds of eggs on the
1970s, where it spread rapidly across the cassava- undersides of leaves and around apical and lateral
growing regions of that continent, causing consid- buds. Eggs hatch in 68 days, and there are four
erable yield loss. This species has been the object of nymphal instars; the first instars are highly mobile
a successful biological control program. In the and will spread over the plant or between plants.
Americas P. manihoti was first found in Paraguay The fourth instar is the adult stage for females,
in 1980 and later collected from certain areas of while males have four nymphal instars plus the
Bolivia and Mato Grosso do Sul state in Brazil, adult stage. The third and fourth instars occur in a
causing no economic damage. More recently cocoon, from which the winged male adults emerge,
(2005), P. manihoti was collected from two north- living only 24 days. The life cycle of the female
eastern states, Bahia and Pernambuco. is 49.5 days; that of the male, 29.5. The optimal
The origin of P. herreni is probably northern temperature for female development is 2530C.
South America, where it was found in cassava- Populations of both species peak during the dry
growing regions of Colombia and Venezuela. It season. The onset of rains reduces pest populations
was first reported in northeast Brazil during the and plant damage, permitting some crop recovery.
mid-1970s, where high populations caused con- Mealybug dissemination between regions,
siderable yield losses. Surveys in the region found countries or continents is probably through infested
few parasitoid natural enemies, suggesting that stem cuttings. The introduction of P. manihoti into
P.herreni is an exotic pest, probably coming from northeast Brazil from southern Brazil can probably
northern South America where parasitoids are be traced to the movement of cassava varieties
frequently observed. between these two regions.

Damage Management
Both species cause similar damage: adult and Cassava mealybug management is a well-
nymph feeding causes leaf yellowing, curling and documented example of classical biological control,
cabbage-like malformation of the apical growing both in Africa and the Americas. In Africa, P. mani-
points. High populations lead to leaf necrosis, hoti is being controlled successfully after introduc-
defoliation, stem distortion and shoot death. ing the parasitoid Anagyrus lopezi from the
Reductions in photosynthetic rate, transpiration Neotropics. After several years of exploration in the
and mesophyll efficiency together with moder- Neotropics by scientists from IIBC, IITA and CIAT,
ate increases in water-pressure deficit, internal the target species P. manihoti was finally located by a
CO2 and leaf temperature were found in infested CIAT scientist (A.C. Bellotti) in Paraguay in 1980.
plants. Yield losses in experimental fields at CIAT IIBC collected natural enemies of P. manihoti that
780
C Cassava Pests and their Management

were sent via quarantine in London to IITA in Benin release site. Aenasius vexans was consistently
for multiplication and release in Africa. The encyrtid recaptured at its release site in Pernambuco, hav-
parasitoid A. lopezi and the coccinellid predators ing dispersed only 40 km in 5 months.
Hyperaspis notata, Hyperaspis raynevali, and Diomus Personal observations in recent years indicate
sp. became established in Africa. The parasitoid is that P. herreni populations have decreased consid-
credited with being the principal agent reducing erably as cassava farmers in the region have not
the mealybug populations. Anagyrus lopezi became reported severe outbreaks and cassava cultivation
established in all ecological zones occupied by has returned to areas where it had been previously
P.manihoti and is now found in 27 countries, cover- abandoned due to P. herreni damage. However,
ing an area of 2.7 million km2. Cassava losses have the recent introduction of P. manihoti into the
been reduced by 9095% with an estimated savings region has resulted in reports of severe mealybug
of US$7.97120.226 billion. damage in Bahia, causing alarm among cassava
Surveys in Colombia and Venezuela identi- producers. An effort by local institutions and
fied numerous parasitoids, predators and entomo- researchers is needed to determine if key P. manihoti
pathogens associated with P. herreni. Several parasitoids are present or need to be introduced
parasitoids show a specificity or preference for into the region.
P. herreni: Acerophagus coccois, Anagyrus diversi-
cornis, Anagyrus putonophilus, Anagyrus isolitus, Thrips
Anagyrus elegeri and Aenasius vexans. Based on Several species of thrips are reported feeding on
numerous field and lab studies, three encyrtid par- cassava, primarily in the Americas. The most
asitoids (A. diversicornis, A. coccois and A. vexans) important include Frankliniella williamsi, Coryno-
were identified as effective in P. herreni infestations. thrips stenopterus, Scirtothrips manihoti, Caliothrips
Comparative life-cycle studies show that they masculinus and Scolothrips sp. More recently a
completed two cycles for each cycle of P. herreni. new species of thrips (Thrichinothrips strasser)
This is a favorable ratio for biological control. associated with cassava was reported from Costa
Anagyrus diversicornis prefers third instar nymphs, Rica. Frankliniella williamsi is reported feeding on
where as the smaller A. coccois parasitizes male cassava in Africa, and high populations of S. mani-
cocoons, adult females and second instar nymphs. hoti have recently been reported from central Brazil.
Aenasius vexans prefers second and third instar Frankliniella williamsi appears to be the most
nymphs. Field studies with natural populations of important species and the only one reported caus-
A. diversicornis and A. coccois estimated P. herreni ing yield losses.
mortality at 55% for their combined action.
Through the combined efforts of CIAT and Damage
CNPMF/EMBRAPA, these three parasitoids were Frankliniella williamsi larvae and adults feed on the
exported from CIAT to EMBRAPA, Brazil, where growing points and young leaves of cassava, which
they were mass reared and released into P. herreni- do not develop normally; leaflets are deformed and
infested cassava fields, primarily in the northeastern show irregular chlorotic spots. The rasping-sucking
states of Bahia and Pernambuco from 1994 to stylet-like mouthparts damage leaf cells during
1996. More than 35,000 parasitoids were released, expansion, causing deformation and distortion; and
and all three species became established. Studies parts of the leaf lobes are missing. Brown wound
prior to release had determined that none of these tissue appears on the stems and petioles, and inter-
species existed in this region. In Bahia, A. diversi- nodes are shortened. Growing points may die, caus-
cornis dispersed 120 km in 6 months after release ing growth of lateral buds, which may also be attacked,
and 304 km in 21 months. A. coccois was recovered giving the plant a witches-broom appearance that
in high numbers 9 months later, 180 km from its can be confused with viral disease symptoms.
 Cassava Pests and their Management
C 781

Yield reductions induced by F. williamsi range damage upper leaves. Feeding by Vatiga spp. causes
from 528%, depending on varietal susceptibility. leaves to form yellow spots that eventually turn
The average reduction for eight varieties in Colombia reddish brown, resembling Tetranychus mite dam-
was 17.2%. Thrips damage and yield reduction are age. Amblystira machalana feeding is characterized
especially pronounced in the seasonally dry trop- by white feeding spots that increase in area until
ics where the dry season is at least 3 months. Plants leaf centers turn white and eventually darken. High
recover with the onset of the rainy season. lacebug populations will cause leaves to curl and
die, often resulting in defoliation of lower leaves.
Management Higher populations are observed on younger plants
Frankliniella williamsi is not considered a major pest (45 months) but decline as plants age.
of cassava as it is not often reported causing yield The relationship between damage and popu-
losses in farmers fields. It can be controlled easily by lation density and duration is not entirely under-
using resistant pubescent cultivars. Approximately stood. In recent field trials with natural populations
50% of the CIAT cassava germplasm bank are pubes- of A. machalana at CIAT, yield losses ranged from
cent, and resistant to F. williamsi. Resistance is based 8.142.7%, depending on cultivar susceptibility
on leaf bud pilosity, and increasing pubescence of and duration of lacebug attack.
unexpanded leaves increases thrips resistance. Populations of V. illudens in Brazil are endemic
Observations indicate that most landrace varieties and appear to be causing yield losses, especially in
grown by farmers in the seasonally dry lowland the central Campo Cerrado regions, although high
tropics are pubescent. It is hypothesized that cassava populations are also reported from the south and
growers may have selected pubescent varieties over northeast.
time for the absence of thrips damage.
Biology and Behavior
Cassava Lacebugs Prolonged dry periods favor high populations of
Reported as pests of cassava only in the Neotrop- V. illudens and V. manihotae. In contrast, A. macha-
ics, five species of the genus Vatiga show a decided lana attack can occur during both wet and dry
preference for feeding on cassava: Vatiga illudens, seasons, but is more likely during rainy periods.
V. manihotae, V. pauxilla, V. varianta and V. cas- Observations in Colombia indicate shifts in lacebug
siae. The first two are the most widely distributed populations. Vatiga manihotae was the pre-
and the most damaging to cassava. Vatiga illudens dominant species in the Cauca Valley until the
predominates in Brazil but also occurs throughout mid-1980s. By 1990, A. machalana populations
the Caribbean region and may be present in other dominated. More recently, V. manihotae increased
areas. Vatiga manihotae, the most widespread lace- and is once again the predominant species, while
bug, is consistently found on cassava in Colombia A. machalana is difficult to find. The cause for this
and Venezuela, but is also reported from Cuba, shift in populations is unknown. In Ecuador, pop-
Trinidad, Peru, Ecuador, Paraguay, Argentina and ulations of A. machalana remain high.
Brazil. Vatiga spp. have also been reported feeding The egg stage of V. manihotae is 815 days,
on wild species of Manihot. In 1985 the black lace- followed by five nymphal instars averaging 1617
bug, Amblystira machalana, was first observed days; adult longevity was 40 days under field condi-
causing damage to cassava in different regions of tions. Laboratory studies with V. illudens in Brazil
Colombia, Venezuela and Ecuador. reported a nymphal duration of 13.5 days and an
average adult longevity of 27 days. In lab studies with
Damage A. machalana, the egg stage averaged 8.2 days;
Lacebug adults and nymphs feed on the undersur- the five nymphal instars, 14 days; average adult
face of lower and intermediate leaves, but can also longevity was 22 days.
782
C Cassava Pests and their Management

Management amage studies resulted in 064% root loss,

d
Lacebugs are the least studied of the important depending on number of attacks, plant age and
cassava pests, so considerable research is required edaphic conditions. Repeated attacks are more
before sound and efficient management practices common when poorly timed pesticide applica-
can be recommended. These studies should be tions fail to destroy fifth instar larvae or prepupae.
conducted in Brazil where V. illudens is endemic. Frequent attacks often occur on larger plantations
Lacebug control appears difficult as few natural (over 100 ha), where subsequent populations can
enemies have been identified, and chemical oviposit and feed on areas not previously defoli-
control should be avoided. In Colombia and ated. Severe attacks and complete defoliation do
Ecuador, observations indicate that V. manihotae not kill cassava because carbohydrates stored in
or A. machalana populations are not high enough the roots enable recovery, especially during the
to warrant pesticide applications. Preliminary rainy season.
screening of cassava germplasm in Brazil and
Colombia indicates that HPR may be available, but Biology and Behavior
no germplasm development program is attempting Although hornworm outbreaks are sporadic, they
to develop resistant cultivars. In insectary studies mostly occur during the rainy season when foli-
in Brazil using caged V. illudens-infested plants, age is abundant. The grey, nocturnal, migratory
isolates of the fungal entomopathogens Metarhizium adult moths have strong flight abilities. Erinnyis
anisopliae and Beauveria bassiana caused 100 and ello females oviposit small, round, light green to
74% mortality of the lacebugs, respectively, indicating yellow eggs individually on the upper surface of
the potential of these fungi for lacebug control. cassava leaves. In field cage studies, females ovi-
posited an average of 450 eggs, although as many
Cassava Hornworms as 1,850 eggs/female were observed. This high
Several lepidopterans feed on cassava, the most level oviposition, combined with the mass migra-
important being the cassava hornworm, Erinnyis tory behavior of adults, helps explain the rapid
ello, which causes serious damage to cassava in the buildup of hornworm populations and their spo-
Neotropics and has a broad geographic range, radic occurrence. During the larval period, each
extending from southern Brazil, Argentina and hornworm consumes about 1,100 cm2 of foliage,
Paraguay to the Caribbean Basin and southern about 75% of this during the fifth instar. At 15, 20,
USA. The migratory flight capacity of E. ello, its 25 and 30C, the mean duration of the larval stage
broad climatic adaptation, and wide host range is 105, 52, 29 and 23 days, respectively, indicating
probably account for its wide distribution. Several that their peak activity may occur at lower alti-
other species of Erinnyis (E. alope, and subspecies tudes or during the summer in the subtropics.
E. ello ello, E. ello encantado) are reported feeding When considerable leaf area is present, up to 600
on cassava in the Neotropics, but they appear to be eggs may be found on a single plant, and larval
of minor importance and do not cause economic populations may exceed 100 per plant. It is esti-
damage to the crop. mated that 13 fifth instar larvae can defoliate a
3-month-old plant in 34 days, especially on low
Damage fertility soils. Given the foregoing, hornworm out-
Hornworm larvae feed on cassava leaves of all breaks must be controlled when populations are
ages, and high populations will also consume in the early larval stage.
young, tender stems and leaf buds. Severe attacks
cause complete plant defoliation, bulk root loss Management
and poor root quality. In farmers fields, natural The migratory behavior of hornworm adults
attacks resulted in 18% yield loss; simulated makes effective control difficult to achieve and
 Cassava Pests and their Management
C 783

reduces the impact of natural biological control. studies show that certain isolates of Beauveria sp.
Insect migration has been described as an evolved and Metarhizium sp. cause high larval mortality.
adaptation for survival and reproduction, and Hornworm outbreaks can be controlled with
some researchers speculate that the hornworms timely (early instars) applications of commercial
migration evolved as a mechanism to survive low biopesticides of Bacillus thuringiensis.
food availability, unfavorable environmental con- The effectiveness of biological control agents
ditions and attack by natural enemies. It is impor- in a hornworm management strategy depends on
tant to detect hornworm outbreaks while in the the ability to synchronize the release of large num-
early development stages. Successful control bers of predators or parasitoids to augment natural
requires monitoring field populations to detect biological control. Predator and parasitic effectiveness
migrating adults, oviposition or larvae in the early in hornworm control is limited by poor functional
instars. This can be done with black light traps for response during outbreaks, which are of short
adults or by scouting fields for the presence of eggs duration (15 days). In the absence of a reliable
and larvae. commercial source of Trichogramma or other par-
Pesticides give adequate control if applied when asitoid or predator species, the cost of maintaining
hornworm populations in the early larval instar these natural enemies in continuous culture to
stages are detected and treated. Larval populations guarantee availability when an E. ello outbreak
in the fourth and fifth instars are difficult to control. occurs is economically prohibitive and impracti-
Farmers often react only when considerable defolia- cal for most cassava farmers.
tion has occurred, with excessive, ill-timed costly The complexities of inundatory releases of
applications that can lead to repeated or more severe parasitoid and predator species suggest the need
attacks. Pesticide use may also disrupt natural enemy for a cheap, storable biological pesticide. A granu-
populations, leading to more frequent attacks, a losis virus of the family Baculoviridae was found
common occurrence on larger plantations. attacking E. ello in cassava fields at CIAT in the
More than 30 species of parasites, predators early 1970s. Pathogenicity studies using virus
and pathogens of the egg, larval and pupal stages material extracted from infected larvae collected
have been identified and reviewed extensively; in the field were carried out on cassava plants in
however, their effectiveness is limited, most likely the lab and field. Larval mortality reached 100% at
due to the migratory behavior of hornworm adults. 72 h after application. Studies on the effect of virus
Eight microhymenopteran species of the families concentration on mortality of larval instars showed
Trichogrammatidae, Scelionidae and Encryrtidae a sigmoidal relationship for the first, second and
are egg parasites, of which Trichogramma and forth instars. LD50 studies show that progressively
Telenomus are the most important. In recent field higher concentrations are needed for adequate
surveys during a hornworm outbreak at CIAT, egg control of each succeeding larval instar. Most fifth
parasitism reached 68%, 57% due to Trichogramma instar larvae reached the prepupal stage, but few
sp. and 11% to Telenomus sp. Tachinid flies are female adults emerged and those that did had wing
important dipteran larval parasitoids and the Bra- deformities and died without producing progeny.
conidae, especially Cotesia spp., are the most Although the baculovirus can be managed by
important hymenopteran. Chrysopa spp. are com- small farmers, this technology has been most suc-
mon egg predators while important larval preda- cessful with larger producers or where research
tors include Polistes spp. (Hymenoptera: Vespidae) and extension services have provided access to it.
and several spider species. Important entomo- Growers can collect and macerate diseased larvae
pathogens include Cordyceps sp. (Aconycites: and apply the virus suspension to cassava fields.
Clavicipitaceae), a soil-borne fungus that invades The virus can be stored for several years under
hornworm pupae causing mortality. Recent lab refrigeration, and for a few months at room
784
C Cassava Pests and their Management

t emperature. Hornworm management with the also damage the stem (e.g., mites, thrips, mealy-
baculovirus was implemented in southern Brazil bugs, hornworms and grasshoppers); however,
during the late 1980s and early 1990s. Researchers they are primarily leaf feeders and are discussed
and extension workers trained farmers in the han- elsewhere. Dipteran fruit flies (Anastrepha spp.)
dling and use of the virus and distributed free sam- and shoot flies (Neosilba sp.) can also bore into the
ples. By 1991 the virus was being applied on about stem and are discussed here.
34,000 ha in Paran state at a cost of only about Stemborers can damage cassava in two ways;
US$1/ha. In Santa Catarina state, virus applications they can (i) weaken the plant by tunneling in the
to early instars resulted in almost complete control, stems, causing breakage that will reduce yields,
and pesticide applications were reduced by 60%. and (ii) destroy or reduce the quality of stem
In Venezuela, where the hornworm is endemic, cuttings, thereby affecting germination and vigor
the virus preparation was applied (70 ml/ha) to of the planting material.
large cassava plantations (7,000 ha) via overhead
sprinkler irrigation systems when larvae were in Stemborers
the first and second instars. This not only resulted A complex of arthropod stemborers that includes
in 100% control but also eliminated pesticides; the both lepidopteran and coleopteran species feed on
cost of gathering, processing, storing and applying and damage cassava. In the Neotropics stemborers
the virus preparation was only US$4/ha. are most important in Colombia, Venezuela and
In Colombia, a baculovirus biopesticide was Brazil. Seven species of Coelosternus (Coleoptera:
developed by a private company (Biotropical) in Curculionidae) can reduce cassava yields and
collaboration with CIAT. The product has been quality of planting material in Brazil; however, the
approved for commercial release by MADR and is damage is generally sporadic and localized, and
available as a wettable powder. Field trials to eval- significant yield losses are not reported. Although
uate the efficacy of this product (Bio Virus Yuca) stemborer species have been identified in Africa,
were carried out in two locations in Colombia: the there are no reports of severe damage or yield
provinces of Tolima and Risaralda. During natural losses.
hornworm attacks, the baculovirus applications Populations of the stemborer Chilomima
(300 g/ha) resulted in 93% hornworm mortality in clarkei (Lepidoptera: Pyralidae) have increased
Tolima and 85% in Risaralda. dramatically in Colombia and Venezuela in recent
The key to effective hornworm control is years, to the point where it is now considered an
training farmers to detect outbreaks through light important pest of cassava, causing yield losses and
trapping of adults or field monitoring combined damage to stem cuttings. On the Atlantic coast of
with the timely application of a biopesticide (or Colombia (provinces of Magdalena and Cesar),
chemical insecticide) when larvae are in their early C. clarkei damage was detected in 85% of the
instars (13). cassava plantations surveyed.

Damage
Stemborers and Stem Feeders Chilomima clarkei populations can occur through-
out the year but are higher during the rainy sea-
Numerous insect species can feed on and damage son. From 46 overlapping cycles can occur during
cassava stems and branches. Although some spe- the 1-year crop cycle, increasing potential damage
cies are nearly worldwide in distribution, the most and making control more difficult. Stem breakage
important are in the Neotropics. Four pests will be can occur when there is extensive tunneling by
discussed in this section: stemborers, scale insects, larvae. When over 35% of the plants suffer stem
fruit flies and shoot flies. Several other pests can breakage, yield losses range from 4562%. Larval
 Cassava Pests and their Management
C 785

tunneling can also lead to stem rot and a reduction Trichogramma sp.) have been identified, but their
in the quantity and quality of planting material. role in regulating stemborer populations has not
Attacks are easily detected by the presence of been investigated. The fungal entomopathogens
excreta, sawdust and exudates ejected from bur- Metarhizium anisopliae and Beauveria bassiana
rows made in infested stems. have been identified as possible biological control
agents.
Biology and Behavior CIAT has worked on identifying cassava ger-
Adult females are nocturnal and oviposit in cassava mplasm resistant to C. clarkei. More than 1,000
stems, usually around the bud or node. The tan- genotypes have been evaluated on the Colombian
colored females can oviposit more than 200 eggs Caribbean coast, where C. clarkei populations are
in a 56 day period. The egg stage averages 6 days consistently high. Evaluations are based on the
(28C). The highly mobile first instar larvae feed on number of holes and tunnels and percent stem
the outer bark or stem epidermis. Upon finding an breakage. Genotypes with 01 holes/stem indicate
appropriate feeding site, usually around lateral buds, varietal influence and the need for further evalua-
the larvae form a protective web, under which the tion. As natural field populations of C. clarkei are
first four instars feed, enlarging the web with each used in these evaluations, results may be mislead-
instar. Stem penetration occurs during the fifth ing because genotypes exhibiting low infestation
instar larval stage. Extensive tunneling can occur may be escapes (i.e., have avoided damage by
as the larval cycle is completed (612 instars). Pupa- chance). CIAT has initiated research to introduce
tion occurs in the stem and winged adults emerge. insect-resistant Bt genes through Agrobacterium-
The larval stage is 3264 days, followed by the pupal mediated transformation into cassava embryonic
stage (1217 days). Female adults live 56 days; tissue to develop resistant cultivars.
males, 45 days.
Scale Insects
Management Several species of scales are reported attacking
Stemborer control is difficult once the larvae cassava stems and leaves in the Americas, Africa
enter the stem and tunneling begins. In addi- and Asia. Although reductions in yield due to scale
tion, the web formed by the early larval stages attack have been reported, they are not considered
acts as a protective devise against natural ene- to be serious pests of cassava. The most important
mies and pesticide applications. The mobile species are Aonidonytilus albus and Saissetia
first instar larvae are vulnerable and more miranda. Aonidonytilus albus has been reported
exposed to both natural enemies and pesti- on cassava throughout most of the cassava-grow-
cides. Biopesticides such as Bacillus thuringiensis ing regions in the world and is considered the
(Bt) are recommended; however, with overlap- most widely distributed cassava pest. It is easily
ping generations, several applications may be disseminated from one region to another through
required, which would be too costly for small stem cuttings, which probably accounts for its
producers. Intercropping with maize will reduce wide distribution.
C. clarkei populations, but only until the inter-
crop is harvested. Damage
Cultural practices such as selection of clean Outbreaks are more severe during the dry season.
cuttings and burning plant residues, especially Their incidence increases when scale-infested
stems and branches, are recommended for reducing stem cuttings are used for planting material. High
stemborer populations. Natural enemies such as A. albus populations may cover the stem and
hymenopteran parasitoids (Bracon sp., Apanteles lateral buds. Leaves on heavily infested stems
sp., Brachymeria sp., Tetrastichus howardi and yellow, and defoliation can occur. With severe
786
C Cassava Pests and their Management

attacks the plants are stunted and stems can desic- With respect to damage, the tan to yellow
cate, leading to plant mortality. Some scale species colored females will oviposit in the tender upper
can attack the leaves, but the greatest damage portion of the cassava stem in certain areas
appears to be the loss of planting material. The during the rainy season. The developing larvae
germination of heavily infested cuttings is greatly become stemborers, tunneling into the apical
reduced; when they do germinate, the roots are stem, which provides an entrance for soft rot bac-
poorly developed, reducing plant vigor. Yield teria such as Erwinia caratovora, resulting in
losses of 19% were recorded at CIAT on plants severe rotting of stem tissue and apical dieback.
heavily infested with A. albus and there was a Several larvae may be found in one stem; their
5060% loss in germination. presence can be noted by the white liquid exudate
that flows from their tunnel. Damage is more
Management severe on younger (25 months) plants. Never-
The most effective means of control is through the theless, the plants can recover from fruit fly
use of clean, uninfested planting material and damage. Yield losses have not been reported, but
destroying infested plants to prevent the spread of there is a reduction in the quality of stem cuttings
infestation. Stem cuttings for vegetative propaga- for planting material. When there is severe dam-
tion should be carefully selected from uninfested age to the pith region of the stem, there is a reduc-
plants. The mussel-shaped A. albus grey to white tion in germination. Yield losses can occur if
female is difficult to detect, especially when popu- severely damaged cuttings are used as planting
lations are low and attached to stems around the material. It is therefore important that only stem
lateral buds. cuttings without damage to the pith regions be
Treating stem cuttings that have originated sown for vegetative propagation.
from fields with scale attack is highly recom-
mended. Dipping the cuttings in a pesticide emul-
Shoot Flies
sion for 5 min is effective against light A. albus
Damage has been observed in most of the cassava-
infestations. Heavily infested cuttings should not
growing regions of the Americas but has not been
be sown as they will germinate poorly even if
reported from Africa or Asia. The most important
treated with a pesticide. Storing healthy cuttings
species are Silba pendula and Neosilba perezi
with infested ones will increase dissemination and
(Diptera: Lonchaeidae). Severe attacks have been
infestation as the first nymphal instars (crawlers)
reported from Cuba, southern Brazil and parts of
are highly mobile.
Central America, especially Costa Rica.
Fruit Flies
Two species of fruit flies, Anastrepha pickeli and Damage
Anastrepha manihoti (Diptera: Tephritidae:), Larval feeding damage is manifested by a white to
whose origin is the Neotropics, are reported to brown exudate flowing from cassava growing
attack cassava fruits from several regions of points, which eventually die. This breaks apical
Central and South America. Anastrepha montei dominance, retards plant growth, and causes ger-
is reported infesting seed capsules in Costa Rica. mination of side buds which leads to excessive
Infestation of cassava fruits causes no economic branching. The dark metallic blue S. pendula adults
damage and is of no concern to cassava pro- deposit eggs in the growing points between the
ducers. When oviposition occurs in the fruit, unexpanded leaves, and the young larvae tunnel in
the larvae bore throughout the fruit, destroying the soft tissue, eventually killing the apical bud.
the developing seed, which is a problem for plant Attacks may occur throughout the year but are
breeders. more prevalent at the onset of the rainy seasons
 Cassava Pests and their Management
C 787

and on recently germinated or young plants, result- increase were highest on peanuts and forage pea-
ing in a reduction in growth of the stems used for nuts, followed by maize. Sweet cassava, sorghum
planting material. Yield is seldom affected. and onions are not favorable hosts, and C. bergi
could not complete its life cycle on bitter cassava.

Management Damage
If plants are being grown for quality cuttings, the Cyrtomenus bergi nymphs and adults feed on cas-
crop needs to be protected only during the first 3 sava roots by penetrating the peel and parenchyma
months of growth. Usually one timely pesticide with their strong thin stylet, leaving fine lesions
application suffices to protect the crop. in the plant tissue. This feeding action permits
the entrance of several soil-borne pathogens (e.g.,
Aspergillus, Diplodia, Fusarium, Genicularia,
Soil-Borne Pests Phytophthora and Pythium spp.), causing local rot
spots on the parenchyma. The brown to black
The majority of the arthropod pests of cassava are lesions begin to develop within 24 h after feeding
source pests, feeding on leaves and stems, which is initiated.
causes indirect damage by reducing root yield. Few In cassava, a quantitative scale to assess root
are sink pests, which cause direct, irrevocable dam- damage was established, using a 15 rating based
age to the edible roots. The most important and on the percentage of the parenchyma surface cov-
damaging root feeders appear to be generalists, ered by rot lesions (1 = no damage, 2 = 125%,
and there is a hypothesis that cyanogenic potential 3=2650%, 4=5175% and 5=75100%). Studies
in cassava is a defense mechanism against them. All show that even low C. bergi populations (close to
cassava varieties have a high cyanogenic potential zero) can cause more than 20% of the root to be
in leaves, stems and root peel. It can also be theo- covered with rot lesions. The darkened lesions on
rized that the root peel acts as a protective device, the white root parenchyma are not acceptable for
especially in those varieties with low cyanogen the fresh consumption market; middlemen reject
levels in the root parenchyma. Three soil-borne shipments of root with 2030% damage, which
pests are discussed here: the burrower bug, white translates into 100% loss for the farmers. Field
grubs (several species) and root mealybugs. trials in Colombia showed that damage can reach
7080% of total roots, with more than a 50%
Cassava Burrower Bug reduction in starch content, thereby reducing the
First recorded as a pest of cassava in Colombia in commercial value for the processing industry. As
1980, Cyrtomenus bergi (Hemiptera-Heteroptera: damage is not detected until roots are harvested
Cydnidae) appears to be native to the Neotropics, and peeled, producers can lose the value of the
is a polyphagous feeder that attacks a wide range crop as well as labor, time and land use.
of crops, and is one of the few arthropod pests that
feeds on the tuberous root of cassava. Additional Biology and Behavior
hosts include onions, peanuts, maize, potatoes, Cyrtomenus bergi has five nymphal instars. It had a
Arachis pintoi (forage peanuts), sorghum, sugar- lifespan of 286523 days when fed on slices of
cane, coffee, asparagus, beans, peas, pastures and low-HCN cassava roots in the lab (23C, 655%
numerous weeds. It has also been reported feeding RH). Egg eclosion averaged 13.5 days; mean devel-
on cassava in Venezuela, Costa Rica, Panama and opment time of the five nymphal stages was 111
Brazil (states of So Paulo and Par). days; mean longevity for adults was 293 days.
Cassava is not the optimal host for C. bergi. Cyrtomenus bergi is strongly attracted to
Fecundity, survival and intrinsic rate of population moist soils, and populations can occur in the
788
C Cassava Pests and their Management

soil throughout the crop cycle. It will migrate Management

when soil moisture content is below 22% and is Cyrtomenus bergi can be the target of extensive
most persistent when it exceeds 31%. Thus, the chemical control, given the nature of the damage it
rainy season greatly favors adult and nymphal causes to cassava as well as other crops. For exam-
survival, behavior and dispersal, whereas there ple, in Colombia, control of C. bergi on crops such
is increased nymphal mortality during the dry as onions, peanuts and coriander requires consid-
season. erable pesticide use, with only marginal results. In
Feeding preferences may be related to levels of cassava, pesticide use can reduce populations and
cyanogenic glucosides in the cassava roots. Adults damage; however, frequent applications may be
and nymphs that fed on high-HCN (>100 mg/kg) required and they are costly and often fail to reduce
cultivars had longer nymphal development, reduced damage below economic injury levels.
egg production and increased mortality. Oviposition Cyrtomenus bergi control is difficult due to
on CMC 40 (43 mg HCN/kg) was 51 eggs/female the polyphagous nature of the pest and its adapta-
versus only 1.3 on MCol 1684 (627 mg HCN/kg). tion to the soil environment. As the initial damage
Adult longevity on CMC 40 (235 days) was more can occur early in the crop cycle, control methods
than twice that on MCol 1684 (112 days). Addi- should be implemented either prior to or at plant-
tional studies indicate that the earliest instars are ing, or during the first 2 months of crop growth.
most susceptible to root cyanogenic potential Intercropping cassava with Crotalaria sp. (sunn
(CNP). Due to the short length of the stylet, feed- hemp) reduced root damage to 4% versus 61%
ing during the first two instars is confined mainly damage in cassava monoculture. This practice also
to the root peel, whereas third to fifth instars can reduces cassava yields by 22%; because Crotalaria
feed on the root parenchyma. CMC 40 has a low has little commercial value, this technology has
cyanogen level in the root parenchyma, but a high not been readily adopted by producers.
level in the root peel (707 mg HCN/kg). Feeding Recent research indicates that there is consid-
experiments in the lab resulted in 56% mortality of erable potential for biological control of C. bergi.
first and second instar nymphs feeding on CMC Isolates of native Colombian strains of the ento-
40 and 82% for those feeding on MCol 1684. The mopathogenic fungi Metarhizium anisopliae and
high cyanogen level in the peel of CMC 40 is prob- Paecilomyces sp. have been evaluated in the labora-
ably responsible for the high mortality. tory. An isolate of M. anisopliae infecting C. bergi
Feeding preference studies carried out in the in the field resulted in 61% mortality of fifth instar
field in Colombia show that low HCN cultivars nymphs and an overall mortality of 33%. More
suffer more damage than high-HCN ones. Three recent studies with M. anisopliae strains CIAT 224
cassava varieties MCol 1684 (high CPN), MMex and CIAT 245 caused mortalities of 34.7% and
59 (intermediate CPN) and CMC 40 (low CPN) 49.3%, respectively.
were evaluated in field studies to determine the Applications of M. anisopliae (Isolate CIAT
effect of CPN on C. bergi root damage. Ten months 224), combined with a sublethal dose of the insec-
after planting, root damage on the low, intermediate ticide imidacloprid, were evaluated in the labora-
and high CPN varieties was 85, 20 and 4%, respec- tory and greenhouse. Cyrtomenus bergi nymphal
tively. These data indicate that CPN may act as a mortality was always significantly higher when
feeding deterrent and that C. bergi should not be a M. anisopliae was applied in combination with
problem where cassava with high CNP is cultivated imidacloprid, compared to applications of the
(i.e., northeast Brazil and many parts of Africa). fungus alone (80.3% vs. 34.2%). Thus, entomo-
However, in many cassava-producing regions, low pathogens combined with sublethal doses of insec-
CNP or sweet varieties are preferred, especially for ticides such as imidacloprid can be an effective
fresh consumption or starch markets. tool in an IPM strategy for controlling C. bergi
 Cassava Pests and their Management
C 789

or other soil-borne pests; however, field studies Grubs feed on the bark, pith and buds of stem cut-
are required before acceptable technologies can be tings, hindering germination. They also can cause
recommended. plant death by feeding on the basal part of young
Several species of nematodes have been identi- stems.
fied parasitizing C. bergi. Steinernema carpocapsae Recent studies in Colombia on Phyllophaga
successfully infected C. bergi in the laboratory, menetriesi with potted cassava plants under con-
resulting in 59% parasitism after 10 days. Strains trolled conditions showed that one larva caused a
of S. feltiae and a native species of Colombia, Heter- 30% reduction in plant survival and three larvae
orhabditis bacteriophora, were compared in green- per plant destroyed 50% of the plants in 56 days.
house studies with C. bergi adults. The penetration White grub feeding damage has also been observed
rate for S. feltiae was 93.9%, compared to 72.1% for on the roots including the swollen tuberous root.
H. bacteriophora. However, H. bacteriophora caused
higher mortality (42.2%) than S. feltiae (8.6%) after Biology and Behavior
15 days. Field studies are needed to evaluate the Laboratory studies with P. menetriesi resulted in
potential of H. bacteriophora and other nematode an average of 13 days for the egg stage and 19, 27
species in an IPM strategy. and 175 days for the first, second and third instars,
respectively. After the third instar, the larvae
White Grubs entered a diapause stage averaging about 30 days,
A complex of rhizophagous white grubs followed by a pupal stage averaging 34 days. Adults
(Coleoptera: Scarabaeidae) is associated with the remained in the pupal chamber for about 73 days,
cassava crop in many regions of the Americas, followed by a 15-day flight period. The complete
Africa and Asia. White grubs are classified as egg-to-adult cycle of P. menetriesi averaged 386
hemi-edaphic (along with ants and termites) as days.
they spend only a portion of their life cycle in the Phyllophaga menetriesi is mostly observed at
soil. It is during their larval stages in the soil that altitudes between 1,0001,600 m, and damage to
they can damage the cassava crop; the adult scarab cassava is primarily during the rainy months when
beetles are not reported feeding on the aboveg- the crop is planted and early growth occurs.
round organs of the plant. Recent surveys in cassava-
growing regions of Colombia showed that white Management
grubs were well represented in the edaphic com- White grubs populations can often be detected
munities associated with the crop. In Risaralda during land preparation prior to planting. Farmer
province, 1,858 white grubs (eight species) were surveys in a major cassava-growing region in
collected from cassava plots. It is often difficult to Colombia (Risaralda and Quindio provinces) dis-
distinguish the species actually causing damage closed that 71% of the farmers applied pesticides
to the crop. The genus commonly associated with to control soil pests, while only 14% used biological
damage to cassava in the Neotropics and Africa is control. Biological control through the use of ento-
Phyllophaga spp. Leucopholis rorida is reported mopathogenic nematodes and fungi offers promise
causing damage to cassava in Indonesia and other for white grub control. A native Colombian strain
countries in Asia. of Heterorhabditis sp., when applied in high doses
(10,000 infective juveniles/ml) to first and second
Damage instar larvae of P. menetriesi in lab studies, resulted
Severe attacks of white grubs can destroy the stem in 88.3 and 83.4% mortality, respectively. In lab
cuttings used to establish new plantations. In one studies at CIAT, several isolates of M. anisopliae
field study in Colombia there was a 95% loss in caused high levels of mortality of P. menetriesi.
stem cutting germination due to white grub attack. Two isolates (CIAT 515 and CIAT 418) caused
790
C Cassava Pests and their Management

more than 60% white grub mortality. Isolate CIAT Adequate control measures have not been
515, in combination with a low rate of imidaclo- determined for either species. Recommendations
prid, resulted in 90% mortality of second instar for management of S. vayssierei in the Cameroon
larvae. The effectiveness of these biological control include planting on ridges and monocropping
agents needs to be tested in farmers fields before cassava.
they can be recommended as part of a white grub
management strategy.
Secondary Pests
Cassava Root Mealybugs
Two mealybug species have been reported feed- Numerous species of arthropods feed on cassava
ing on and causing damage to cassava roots. In without causing major economic damage to the
South America, Pseudococcus mandio (Hemiptera: crop. These occasional or incidental pests may
Pseudococcidae) has been recorded from south- occur sporadically or at such low population levels
ern Brazil, Paraguay and Bolivia; it is reported as that yield is not affected. If their populations
causing root damage only in Brazil. Stictococcus increase or outbreaks occur in localized areas,
vayssierei (Hemiptera: Stictococcidae) is reported some of these pests could cause yield losses. These
from the Cameroon and neighboring Central secondary pests discussed briefly here include gall
African countries. Stictococcus vayssierei is referred midge, termites, leaf hoppers, leaf-cutting ants and
to in the literature as the root mealybug, the root grasshoppers.
scale or the brown root scale insect of cassava.
Pseudococcus mandio can result in reduced Grasshoppers
quality of tuberous roots and cause some plant Zonocerus elegans and Zonocerus variegatus are
defoliation. Females have three nymphal instars, potentially the most destructive of this group.
and adults oviposit an average of 300 eggs, indicat- They attack cassava primarily in Africa and are
ing a capacity for rapid population increases. The rarely reported feeding on cassava in the Neotropics
life cycle from oviposition to adult was 25 days for (occasionally from Brazil). Several African coun-
females and 30 for males. Yields losses of 17% have tries including Nigeria, Congo, Benin, Uganda,
been reported in southern Brazil. Ivory Coast, Ghana and Central Africa report
Stictococcus vayssierei larvae and adults attack thousands of hectares of cassava defoliated in
young feeder roots on germinating stem cuttings, some years, probably causing yield reductions.
resulting in defoliation, wilting, tip dieback and
plant death. Mature tuberous roots are often Damage
small, covered with mealybugs, and unattractive Grasshoppers feed on the leaves, causing defolia-
for the commercial market. Females (males are tion, but during outbreaks the young tender bark
rare) are dark red in color, circular and flattened. can be stripped. Young plants are preferred and
Eggs are protected by wax threads secreted beneath attacks are more severe during the dry season.
the female body. Larvae are creamy white and Yield losses as high as 60% have been estimated.
mobile. Stictococcus vayssierei infestation is severest
during the dry season and on unfertile, lateritic and Biology and Behavior
clay soils. Infestations were more severe when cas- In Nigeria, grasshopper oviposition usually occurs
sava was planted on flat lands than when planted at the onset of the rainy season; eggs hatch at the
on ridges. Plant vigor and root yield improved by start of the dry season (67 months later). This
approximately 22% when planted on ridges. Inter- population attacks cassava as the dry season pro-
cropping favored higher mealybug infestations than gresses when other preferred herbaceous food
cassava grown in monoculture. plants become scarce. Experiments show that large
 Cassava Pests and their Management
C 791

amounts of HCN in the leaves can act as a deter- and Acromyrmex landolti. Ants cut semicircular
rent to grasshopper feeding. The early instars (14) pieces of leaves, which they carry to their under-
will not consume growing cassava, while instars ground nests. Cassava plants can be completely
5 and 6 will eat it only if deprived of other food defoliated when a large number of worker ants
sources. Wilted cassava leaves are readily con- attack a crop. Outbreaks occur most frequently
sumed by all stages and result in a high grasshopper during the early months of crop establishment, but
growth rate. plants usually recover from ant damage. Recent
field trials in Venezuela resulted in a 55% reduction
Control in root yield due to leaf-cutter ant defoliation. Ant
Chemical control of grasshoppers is feasible but nests are usually visible because of the mound of
may not be financially or ecologically sustainable, soil deposited around the hole. Control of leaf-cutter
especially for small, resource-limited farmers. It is ants is difficult; toxic baits are recommended.
not considered an effective mid- or long-term
solution as pesticide applications may lead to a Termites
resurgence of other pests such as the cassava Termites are reported as pests in several cassava-
mealybug or the cassava green mite when their growing regions of the world, but primarily in
natural enemies are killed indiscriminately. Africa. They attack cassava mainly in the tropical
Biological control with fungal entomopatho- lowlands, feeding on stem cuttings, feeder roots,
gens offers a more effective long-term solution for swollen roots or growing plants. In Colombia, ter-
grasshopper control. Metarhizium anisopliae var. mites have been observed causing losses in germi-
acridum (also known as M. flavoviride), Beauveria nation as well as death of young plants, especially
bassiana and Entomophaga grylli have been identi- in regions with sandy soils. Feeding on swollen
fied infecting Z. variegatus. Efforts are currently roots can lead to root rot (due to soil pathogens)
underway to develop effective biopesticides for damage. Losses in germination of 30% and 50%
grasshopper control. Results with M. anisopliae loss in stored planting material have been recorded.
have been encouraging. Control in the field is difficult, but stored planting
material can be protected with an application of
Gall Midges an insecticide dust.
Iatrophobia brasiliensis (Diptera: Cecidomyiidae)
has been recorded on cassava only in the Ameri- Leafhoppers
cas. They are considered of little economic impor- Several species have been collected feeding on
tance and do not require control. However, the cassava. Several collections have been made by
yellowish green or red galls on the upper leaf sur- CIAT in Colombia, and numerous specimens from
face are highly visible to farmers, who may apply three families (Cicadellidae, Cixiidae and Delpha-
pesticides. A severe attack, especially on young cidae) are being identified. None is considered to
plants, may cause leaf yellowing, and retarding of be a pest causing yield losses, and all are usually
plant growth has been reported. Destruction of observed in low populations. However, several of
infested leaves is recommended to reduce midge these species are being studied as possible vectors
populations. of cassava frog skin disease (CFSD), which proba-
bly originated in the Amazon regions of South
Leaf-cutter Ants America and has now spread to several countries
Several species of leaf-cutter ants (genera Atta and in the region causing considerable crop loss. The
Acromyrmex) are reported feeding on cassava in disease has been described as a virus of the family
the Neotropics, especially in Brazil. Commonly Reoviridae and/or phytoplasm. Damage is charac-
reported species are Atta sexdens, Atta cephalotes terized by the suberization and thickening of the
792
C Cassava Pests and their Management

swollen root epidermis, resulting in low produc- against two introduced pests from the Americas,
tion of little commercial value. Several species have the cassava mealybug (P. manihoti) and the green
now been mass reared, and vector-transmission mite (M. tanajoa). Although natural biological
studies are being carried out. control is probably effective in controlling some
pests in the Neotropics, pest outbreaks and subse-
quent yield losses continue to occur. For example,
Future Trends and Considerations the hornworm Erinnyis ello has a large complex of
natural enemies including predators, parasites and
The success of an ecologically oriented IPM pro- pathogens; however, they are not effective in main-
gram for cassava requires the implementation of a taining the hornworm below the economic injury
strategy that minimizes or prevents chemical pes- level. The adults migratory abilities and sporadic
ticide use. Given the increased emphasis on com- attacks serve as a defense against the more than 30
mercial-scale plantations, where the crop has a natural enemies. The stemborer Chilomima clarkei
high commercial value, there is a tendency to apply causes considerable damage in certain regions of
pesticides when noticeable crop damage occurs. Colombia, but effective natural enemies have not
Pests that trigger pesticide application include the been identified. In recent years whitefly popula-
cassava hornworm, whiteflies, mites, white grubs, tions and damage have increased in several regions
burrower bugs, mealybugs and thrips. of the Neotropics as well as in Africa, causing con-
Crop-protection technologies based on host siderable yield reduction. Several natural enemies
plant resistance, microbial and arthropod biological have been identified, but their role in a biological
control agents, together with appropriate agronomic control program has not been determined.
practices, should be developed and implemented. It should be kept in mind that in cropping sys-
This holistic approach has formed the basic philos- tems where cassava is grown as a functional peren-
ophy for IPM research at international agricultural nial, certain pests and their associated natural
research centers such as CIAT and IITA, as well as enemies may be in equilibrium. When cassava is
in several national research programs such as grown year round in the tropics, often with over-
EMBRAPA (Brazilian Agricultural Research Corp., lapping cycles, pest species may be present through-
Brasilia, Brazil), NARO (National Agricultural out and thereby able to increase rapidly when
Research Organization, Uganda). environmental conditions become favorable to
CIAT, IITA and the Brazilian national pro- their dynamics. Natural enemy populations may not
gram EMBRAPA maintain large germplasm banks respond rapidly enough to suppress the increasing
that offer entomologists and breeders a potential pest populations so outbreaks occur. Populations
pool for pest-resistance genes. Traditional farmers of mites, mealybugs, lacebugs and whiteflies,
will adopt new varieties cautiously if they are although present in the subtropics of the Americas,
adapted to local agroecological and socioeco- do not increase as rapidly or reach the levels of
nomic conditions. New or introduced varieties their counterparts in the tropical regions. During
should not be highly susceptible to major pests in the winter months in subtropical regions, cassava
a given region. In the Neotropics this is especially will lose most or all its foliage. This can cause con-
true for mites, whiteflies, thrips and mealybugs. siderable reduction in pest populations so any
Biological control agents have been identified increases may be retarded when warmer, more
for many of the cassava arthropod pests; however, favorable, growing conditions return in the spring.
the efficacy of naturally occurring biocontrol Biotechnology tools offer the potential for
agents to maintain pests below economic damage developing improved pest-resistant cultivars
levels has not been well documented. Classical and enhancing the effectiveness of natural con-
biological control has been successful in Africa trol organisms including parasitoids and
 Cassava Pests and their Management
C 793

e ntomopathogens. Wild Manihot species are a continue to play an important role in sustaining
rich source of useful genes for the cultivated spe- high cassava-production levels. This will require
cies M. esculenta and for resistance to pests and continued research input to develop new inte-
diseases. Their use in regular breeding programs grated pest management (IPM) technologies.
is restricted by the long reproductive breeding In order to meet the demand for increased
cycle of cassava and linkage drag associated with cassava production, farmers will seek new higher
the use of wild relatives in crop improvement. yielding varieties. This will increase the movement
This source of resistance genes has been exploited of germplasm usually vegetative stem cuttings
for controlling CMD in Africa. CMD resistance between regions, countries and even continents.
was obtained by intercrossing cassava varieties Quarantine measures to prevent the movement of
with Manihot glaziovii, which resulted in inter- pests, especially into Asia, are an important issue.
specific hybrids that were backcrossed to cassava Cassava pests have shown the ability to disseminate
until CMD-resistant varieties were produced. great distances as shown by the introduction of the
Several wild Manihot species have been eval- mite and mealybug into Africa from the Americas.
uated in the greenhouse and field for resistance to There are several additional pests that could cause
mites (M. tanajoa), mealybugs (P. herreni) and severe crop losses if introduced into Africa or Asia,
whiteflies (Aleurotrachelus socialis). Genotypes including several mite species, lacebugs, whiteflies,
(accessions) of the wild species Manihot flabellifolia stemborers, mealybugs and thrips. Moreover, what
and Manihot peruviana displayed intermediate may be considered a secondary pest in the Neotro-
levels of resistance to M. tanajoa and P. herreni pics could become a major pest outside its center of
and high levels of resistance to A. socialis. In addi- origin, as evidenced by the mealybug, P. manihoti.
tion, M. tanajoa oviposition was greatly reduced
when feeding on accessions of Manihot alutacea References
and Manihot tristis. Interspecific crosses between
these wild Manihot species and M. esculenta lan- Bellotti AC (2002) Arthropod pests. In: Hillocks RJ, Thresh
drace varieties have resulted in numerous inter- JM, Bellotti AC (eds) Cassava: biology, production and
specific progeny, which are being evaluated for utilization. CABI Publishing, Wallingford, Oxon, UK,
pest resistance. Initial results indicate that the pp 209223
Bellotti AC, Arias B (2001) Host plant resistance to whiteflies
resistance is heritable as numerous progeny have with emphasis on cassava as a case study. Crop Protect
been identified with resistance to M. tanajoa and 20:813823
A. socialis. Three polymorphic molecular markers Bellotti AC, Riss L (1994) Cassava cyanogenic potential and
resistance to pests and diseases. Acta Hortic 375:141151
for M. tanajoa that showed clear differences
Bellotti AC, Arias B, Guzmn OL (1992) Biological control
between resistant and susceptible individuals were of the cassava hornworm Erinnyis ello (Lepidoptera:
identified in M. flabellifolia. A project is under way Sphingidae). Fla Entomol 75:506515
to develop low-cost tools for accelerated marker- Bellotti AC, Pea J, Arias B, Guerrero JM, Trujillo H, Holgun
C, Ortega A (2005) Biological control of whiteflies by
aided introgression of useful pest-resistance genes indigenous natural enemies for major food crops in the
into cassava gene pools. Neotropics. In: AndersonPK, Morales F (eds) Whitefly
It is predicted that cassava production in and whitefly-borne viruses in the tropics: building a
Africa, Asia and the Americas will increase con- knowledge base for global action. CIAT Publication No
341, Cali, Colombia, pp 313323
siderably during the next decade. This growth will Bellotti AC, Smith L, Lapointe SL (1999) Recent advances
be market driven and influenced by the processing in cassava pest management. Ann Rev Entomol 44:
and private sectors. Cassava can provide the raw 343370
Braun AR, Bellotti AC, Guerrero JM, Wilson LT (1989) Effect
material for the animal feed, starch and bio-fuel
of predator exclusion on cassava infested with tetrany-
industries, as well as remaining an important food chid mites (Acari: Tetranychidae). Environ Entomol
for human consumption. Pest management will 18:711714
794
C Caste

Braun AR, Bellotti AC, Lozano JC (1993) Implementation of species, and therefore overlaps with this definition
IPM for small-scale cassava farmers. In: Altieri MA (ed)
of castes, within the social insects the term castes
Crop protection strategies for subsistence farmers.
Westview, Boulder, Colorado, pp 103115 is always used to describe this condition. In social
El-Sharkawy MA (1993) Drought-tolerant cassava for Africa, insects, there may or may not be marked differences
Asia, and Latin America. BioScience 43:441451 in appearance of the subsets, but they definitely
Herren HR, Neuenschwander P (1991) Biological control of
cassava pests in Africa. Ann Rev Entomol 36:257283
display differences in behavior and biology. An
Holguin CM, Bellotti AC (2004) Efecto de la aplicacin de alternate term for describing the discretely different
insecticidas qumicos en el control de la mosca blanca (lacking intermediate forms) intraspecific variation
Aleurotrachelus socialis Bondar en el cultivo de yuca occurring within insects is polyphenism. (In con-
Manihot esculenta Crantz. Rev Colomb Entomol
30:3742 trast, phenotypes that show gradual change in
Melo EL, Ortega-Ojeda CA, Gaigl A, Ehlers RV, Bellotti AC response to environmental variation, without
(2006) Evaluacin de dos cepas comerciales de ento- producing discretely different subsets, are called
monematodes como agentes de control de Cyrtomenus
reaction norms.) Regulation of caste is deter-
bergi Froeschner (Hemiptera: Cydnidae). Rev Colomb
Entomol 32:3138 mined by hormones, which trigger different pat-
Neuenschwander, P (2004) Cassava mealybug, Phenacoccus terns of gene expression, leading to alternative
manihoti Matile-Ferrero (Hemiptera: Pseudococcidae). phenotypes. Ultimately, however, it is the environ-
In: Capinera JL (ed) Encyclopedia of entomology.
Kluwer, Dordrecht, The Netherlands, pp 464467
ment, acting through hormone intermediaries, that
Ngeve JM (2003) The cassava root mealybug (Stictococcus promotes development of polyphenisms such as
vayssierei Richard) [Hom: Stictococcidae]: present sta- castes. In social insects, the castes cooperate with
tus and future priorities in Cameroon. Afr J Root Tuber each other in a nest to accomplish tasks benefiting
Crops 5:4751
Onzo A, Hanna R, Sabelis MW (2005) Biological control of the entire colony. Some of the castes are sterile,
the cassava green mite in Africa: Impact of the preda- serving as workers or soldiers to facilitate reproduc-
tory mite Typhlodromalus aripo. Entomol Beric 65:27 tion by a small number of reproductives. The sterile
Yaninek JS, Onzo A, Ojo JB (1993) Continent-wide releases of
castes presumably have evolved through the process
Neotropical phytoseiids against the exotic cassava green
mite in Africa. Exp Appl Acarol 17:145160 of kin selection.
Phenotypic plasticity occurs in all organisms,
and the phenotype that is expressed depends on
environmental conditions. Interestingly, the envi-
Caste ronment to which the alternative phenotype is an
adaptation is often not the same as the environ-
A form or type of individuals in social insects. ment that induces the development of that pheno-
Castes may be distinguished by different morphol- type. As noted above, some phenotypes display
ogy and behavior. incremental changes in response to environmental
variables. Others display discrete changes, resulting
in two or more discrete alternative phenotypes. In
Castes either event, it can be advantageous to an organism
to have the ability to develop multiple phenotypes
John L. Capinera without requiring genetic polymorphism.
University of Florida, Gainesville, FL, USA The developmental switch that leads to pro-
duction of alternative phenotypes is regulated by
Castes can be defined as subsets of individuals hormones. For morphological expression of poly-
within a species that are morphologically or bio- phenism, a molt is normally required. Thus, the
logically distinct. Although polymorphism usually developmental trigger typically is in the instar
is understood to mean the occurrence of discretely preceding the expression. Within that sensitive
different morphotypes and biologies within a period when change can be triggered, often there
 Castes
C 795

is only a brief period when hormones can alter anatomically distinctive due to an enlarged abdo-
developmental pathways. The relevant hormones men. The worker ordinarily is a sterile female. Such
generally are juvenile hormone and ecdysone, but females have reduced ovarioles and lack sper-
sometimes other hormones are involved. mathecae for sperm storage. So if they eventually
become reproductives, they can only reproduce
parthenogenetically. The worker caste is often
Ants subdivided into subcastes such as minor, media,
and major, and is based on size. When workers
Among the ants, female castes are usually expressed are specialized for defense, they are called soldiers.
as worker, soldier and queen castes. Males do not The ergatogyne is a reproductive caste intermedi-
display different castes. Soldiers are often referred ate between worker and queen. It can be subdi-
to as major workers, with the coexisting smaller vided into intercaste which is anatomically
members called minor workers. Not all castes occur intermediate between workers and queens, but
in all species. Castes are determined by a number of lacks a spermatheca so cannot mate, and ergatoid
factors, including larval nutrition, winter chilling, queen which also is intermediate but possesses a
post-hibernation temperature, egg size, queen age, spermatheca and can replace the queen. The
and queen influence. The function of castes or gamergate is not common, but occurs in a few
caste polyethism is well described by the afore- groups of ants, and is strictly a physiological caste.
mentioned designations. Queens are mostly con- In this case, the reproductive is morphologically
cerned with production of eggs, though early in the indistinguishable from the worker, but can be
life of the colony the queen may perform various inseminated and produce eggs. The most distin-
tasks, and some grooming of workers may occur guishing feature of the dichthadiiform ergatogyne
indefinitely. Soldiers are specialized for colony is that it possesses an extremely enlarged gaster,
defense, and often bear a large head and oversized but this reproductive also has some additional
mandibles to aid in this task. Workers repair the minor morphological modifications. The final
nest, gather food, and tend larvae and pupae, and caste would be considered to be the temporal caste.
the other colony members. Workers may also be In the temporal caste, differentiation is based solely
involved in colony defense, especially the larger on behavior and age.
workers. Males exist only to fertilize queens. Tem-
poral changes also occur over the course of the
ants lifespan; this is called age polyethism. For Social Bees and Wasps
example, young workers tend to work inside the
nest, whereas older workers tend to forage outside. Among social bees and wasps, the more primi-
Over the years, some authors have recognized tively eusocial groups lack mophological differ-
variants, phases, or anomalies within castes in an ences but display different behaviors. More
attempt to recognize small differences in behavior interesting is the general lack of the worker sub-
and morphology, and this has led to confusion. castes such as those that are found in ants and ter-
Castes can be defined by both morphological mites. This is despite the fact that bees and wasps,
and behavioral characteristics, of course, and E.O. at least the species with very large colonies, display
Wilson has proposed a system of caste naming a sophisticated division of labor (polyethism). In
that integrates both types of characters: The males bees and wasps, however, the division of labor is
play no direct role in colony maintenance, being based less on production of castes, and more on
only sperm donors. The queen or gyne is the temporal polyethism. In temporal polyethism the
principal reproductive, although gyne sometimes same individual passes through different stages of
is used to include all reproductive females. She is specialization as it grows older. Some differences
796
C Castes

exist based on size, however, with larger individu- be either sex, whereas in the holometabolous
als tending to forage more and smaller individuals social insects (ants, bees, wasps) the workers are
tending to conduct nest work and brood care. always female. Also, termite immatures are work-
In social bees and wasps, there is a correlation ers, whereas immatures of the other social insects
between caste evolution and colony size. E.O. Wilson require continual care by adult workers.
divides this into four steps: Termite castes have some unique features. In
1. Colony size of 250 adults the females are semi- the lower termites, the reproductives secrete sex-
social or begin life as workers and later become specific pheromones that inhibit metamorphosis of
egg layers. the immatures into additional reproductives. Ter-
2. Colony size of 10400 adults externally, the mites also are capable of producing supplementary
queen is still identical to the worker caste, but there reproductives. If the primary reproductives are
is functional differentiation of the worker caste removed, fertile but wingless individuals of both
from the queen. The egg-laying females maintain sexes develop in the colony. Thus, termite colonies
the workers in a subordinate position by aggressive display immortality; they may never completely
dominance behavior. This can be expressed by the perish because reproductives can be generated as
stealing and eating of eggs laid by rivals. Temporal necessary. Termite soldiers seem to be capable of
poyethism is weakly developed among workers. suppressing the development of workers into soldiers,
3. Colony size of 1005,000 adults some external maintaining a larger number of termites arrested in
differentiation of queens and workers is evident, the worker stage, probably to the benefit of the colony.
and this is under the control of nurse workers The classification of termite castes is as follows:
that feed larvae differently. Queens do not display The larva (a wingless nymph, as these are hemime-
dominance behavior. Temporal polyethism is tabolous insects) lacks evidence of wings and of the
weak among workers. features that characterize soldiers. The nymph (brac-
4. Colony size of 30080,000 adults queen and hypterous nymphs) develops from the larval stage
worker dimorphism is strong. Queen dominance but possesses wing buds initially, and wing pads
is absent and queens maintain control with pher- aftersome molts. Eye differentiation also occurs at
omones. Temporal polyethism is strongly devel- this stage. A worker stage occurs in the higher ter-
oped among workers. mites, but not the lower. Workers lack wings, and
eyes are reduced or lacking. The head and mandibles
are well developed. Lacking the worker stage, the
Termites lower termites have instead a stage called pseuder-
gate. Pseudergates develop from nymphal stages or
Superficially, termites and ants have similar caste larvae. Soldiers have morphological features that are
systems. However, these taxa are phylogeneti- specialized for defense. This includes large mandi-
cally remote from each other, and careful exami- bles, large heads, and glands capable of discharging
nation shows some important differences, so it is defensive secretion. Primary reproductives are
clear that sociality and caste systems evolved derived from colony-founding queens and males.
separately in Hymenoptera and in Isoptera. Both If the primary reproductives are removed from
ants and termites have evolved a soldier caste the colony, often supplementary reproductives
with specialized head structure and behavior, canappear. The supplementary reproductives take
and both are populated primarily by similar- three forms: (i) the adultoid reproductive, found in
looking but behaviorally versatile workers. Their the higher termites only, which appears identical to
systems of temporal polyethism also are similar. the primary reproductive and may already exist but
Termites differ, however, in that males do not changes behavior in the absence of the primary
exist solely for fertilization. Termite workers can reproductive; (ii) the nymphoid reproductive is a
 Cat Flea, Ctenocephalides felis felis Bouch (Siphonaptera: Pulicidae)
C 797

supplementary male or female derived from a Nijhout HF (1999) Control mechanisms of polyphenic devel-
opment insects. Bioscience 49:181192
nymph and retaining wing buds; (iii) the ergatoid
Wilson EO (1971) The insect societies. Belknap Press,
reproductive is also a supplementary male or female, Cambridge, MA, 548 pp
but is larval in form and lacks wing buds. Zhou X, Oi FM, Scharf ME (2006) Social exploitation of
The primary reproductives construct an initial hexamermin: RNAi reveals a major cast-regulatory
factor in termites. Proc Natl Acad Sci 103:44994504
cell and rear the first brood, providing them not
only with food but the protozoans necessary for
independent feeding on cellulose. The first brood
workers (or worker-like pseudergates or nymphs) Castniidae
soon take over responsibilities for foraging, nest
construction and nursing. The queen and male A family of moths (order Lepidoptera) also known
become specialized reproductive organisms. Inter- as giant butterfly moths.
estingly, the worker caste is morphologically uni- Giant Butterfly Moths
form but behaviorally diverse when species are Butterflies and Moths
compared. The soldier caste is morphologically
diverse but behaviorally uniform. Soldiers can use
their mandibles effectively in defense against insects Caterpillar
their own size, or in the case of those practicing
chemical defense, their glands can secrete or spray a The larva of a butterfly, moth (Fig.29), sawfly, and
number of bioactive substances to deter intruders. some scorpionflies.
Polyphenism
Termites
Bees Cat Flea, Ctenocephalides felis felis
Ants Bouch (Siphonaptera: Pulicidae)

Nancy C. Hinkle1, Philip G. koehler2

References 1
University of Georgia, Athens, GA, USA
2
University of Florida, Gainesville, FL, USA
Ananthakrishnan TN, Whitman D (eds) (2005) Insect
phenotypic plasticity. Diversity of responses. Science Cat fleas are the most common ectoparasite on
Publishers, Enfield, New Hampshire, 213 pp
Hlldobler B, Wilson EO (1990) The ants. Belknap Press, both dogs and cats in North America. These small
Cambridge, MA, 732 pp (2 mm), reddish brown, wingless insects have bod-
Miura T (2004) Proximate mechanisms and evolution of caste ies that are laterally compressed (i.e., flattened
polyphenism in social insects: from sociality to genes.
side-to-side) and covered with many backward-
Ecol Res 19:141148
Miura T (2005) Developmental regulation of caste-specific char- projecting spines, making them, like a cocklebur,
acters in social insect polyphenism. Evol Dev 7:122129 difficult to remove from the animals coat. Their

anal spine

head

thoracic legs prolegs

Caterpillar, Figure 29 Lateral view of a moth caterpillar (Lepidoptera: Sphingidae).

798
C Cat Flea, Ctenocephalides felis felis Bouch (Siphonaptera: Pulicidae)

hind legs are long and well adapted for jumping. The cat flea is a cosmopolitan, eclectic species,
Adult fleas feed exclusively on blood and their having been recorded from over three dozen species,
mouthparts are equipped for sucking blood from including opossums, raccoons, skunks, coyotes,
the host. Cat fleas attack a variety of warm-blooded and even birds. Infested wildlife can move flea infes-
hosts, including humans and pets, making them tations from infested premises to previously non-
both a veterinary problem and household pest. infested areas. The combination of wide host range
Although cat fleas have been collected from more and movement of fleas by urban wildlife explain the
than 30 species of urban and suburban wildlife, fleas ability to repopulate domestic animals follow-
most of these animals are not satisfactory hosts. ing suppression efforts. Because it lacks host speci-
Cat fleas do not commonly serve as disease ficity and tends to feed on humans, the cat flea is a
agent vectors. However, they are capable of trans- pest of both companion animals and their homes.
mitting the causative agents of flea-borne typhus Once adult cat fleas locate a host, they tend to
(Rickettsia typhi) and cat scratch disease (Barto- remain on that animal unless dislodged. They feed
nella henselae). The cat flea is the intermediate host readily, taking several blood meals every day. They
for the dog tapeworm, Dipylidium caninum, which not only feed, but mate and lay eggs while on the
can affect small children as well as dogs and cats. It host, unlike rat fleas that hide in rodent burrows
is supposedly capable of transmitting plague (Yers- between blood meals. Flea eggs (Fig. 30) are not
inia pestis), but has been important in epidemic sticky so they readily fall off into the hosts envi-
situations only outside the U.S. ronment, with large numbers accumulating in
Probably the most common flea symptom is areas frequented by the animal. Scratching caused
that pets bite and scratch themselves repeatedly. by saliva in flea bites speeds the drop of eggs from
Severely flea-infested puppies and kittens risk life- the host. Once the adult flea finds a host, it begins
threatening anemia. Sensitized people suffer pru- to feed. The female mates and begins oviposition
ritus stimulated by antigens in flea saliva, and within a couple of days. On the host, a female flea
resultant scratching opens the skin to infection. averages about one egg per hour and, as a female
Flea saliva has been described as one of the most flea can live on the host for several weeks, poten-
irritating substances known to man, and very tial production can amount to hundreds of eggs in
small amounts cause great irritation and itching. her lifetime. Only the adult stage is parasitic; all
Flea allergy dermatitis (FAD) is a severe condi- other life stages develop off the host.
tion found primarily in dogs, but also occasionally Cat flea eggs are approximately one mm in
seen in cats. In a flea-allergic animal, flea salivary length, with little surface structure. Typically eggs
antigens stimulate intense itching that results in hatch within 2448 h following oviposition, with
self-inflicted trauma such as scratching and biting. more rapid hatching at warm temperatures.
Affected animals display obsessive grooming behav- Small, white, eyeless, legless larvae emerge from
ior, hair loss, and weeping sores with secondary the eggs with chewing mouthparts. They graze
infection. Until successful FAD immunotherapy is through their habitat, feeding on organic debris and
developed, treatment involves flea elimination from adult flea feces (partially digested blood). As they
the animals environment and flea bite prevention. seldom travel far from where they hatch, cat flea
But only one bite can stimulate a full cascade of larvae are usually found in furniture, carpeting, or
symptoms in sensitive animals. outside in areas frequented by host animals. In
Fleas and their associated diseases can consti- efforts to avoid light, flea larvae typically burrow
tute over half a veterinary practices caseload in deep into carpet or, outdoors, into duff.
some regions. More energy and money are spent Flea larvae are highly subject to desiccation
battling these insects than any other problem in and dry out rapidly. Humidity over 50% in the
veterinary medicine. larval environment is essential for development,
 Cat Flea, Ctenocephalides felis felis Bouch (Siphonaptera: Pulicidae)
C 799

Cat Flea, Ctenocephalides felis felis Bouch (Siphonaptera: Pulicidae), Figure 30 The cat flea life cycle:
(left) a flea egg is not sticky so readily falls from the host and hatches a few days later; (second from left)
flea larvae coil when disturbed; (third from left) within the cocoon the larva completes development
through the pupal stage to an adult flea; (right) adult fleas feed exclusively on blood.

and this susceptibility to heat and desiccation from days to several months (or perhaps over a
makes it unlikely that flea larvae survive outdoors year). The pre-emerged adult flea within the cocoon
in sun-exposed areas. Because hosts prefer shaded is more resistant to desiccation than either eggs or
areas, flea eggs are more likely to be deposited in larvae. Stimuli such as pressure, carbon dioxide, and
shade, and flea larvae develop where the ground is warmth (triggers associated with mammalian hosts)
shaded and moist. Likewise, indoors flea larvae cause adult fleas to emerge from their cocoons. This
are protected under the carpet canopy where air emergence from the cocoon causes many problems
movement is minimized and humidity is highest. in homes and apartments where infested pets previ-
Most flea larvae, therefore, tend to be located in ously lived. When the hosts are removed from a resi-
areas where pets spend most of their time. dence, the eggs and larvae all develop to the
Under favorable conditions, flea larvae can pre-emerged adult stage, waiting for a host. As soon
complete development in as little as 10 days. Cool as a new resident occupies the house, thousands of
temperatures, food shortages, or other unsuitable fleas emerge at once, stimulated by the movement,
environmental conditions may extend larval devel- warmth, and carbon dioxide. Emergence of these
opmental time to several weeks or a month. In adults from their protective cocoons may persist for
areas like south to central Florida, flea larvae can 36 weeks despite all efforts to control them.
develop outdoors from egg to pupal stage, even Most fleas emerge within a couple of weeks
during the winter months of November to March, following cocoon formation. Upon emergence, the
due to the mild temperatures and high humidity. flea can survive for approximately 710 days (or
When mature, the larva locates an appropriate site longer under high humidity and low temperature
for pupation and spins a silk cocoon to which conditions) if it does not locate a host.
adheres environmental debris, making the cocoon Because fleas must have blood from a mam-
appear as a small dirt clod or lint ball. mal host to survive, treating host animals to use
Within its cocoon, the larva molts to the pupa them as bait is the most efficient and successful
and continues metamorphosis, becoming an adult suppression tactic. There are several on-animal
flea within about 4 days under favorable conditions. products that are effective for flea control. Many
The pre-emerged adult stadium has the most vari- contain pyrethrins, which are safe, effective
able length of any stage in the flea life cycle, ranging products but kill only fleas on the animal at time
800
C Cat Flea, Ctenocephalides felis felis Bouch (Siphonaptera: Pulicidae)

Cat Flea, Ctenocephalides felis felis Bouch (Siphonaptera: Pulicidae), Figure 31 Fleas are ornamented
with spines and combs that help anchor them in the hosts coat.

of treatment and do not provide residual control. addition to spot-on formulations, some products
Other over-the-counter compounds include are available as sprays. These adulticides kill fleas
spot-on permethrin products, which are limited to on the animal within a few hours, then provide
canine use as they can be lethal to cats. residual flea suppression for several weeks.
Veterinarians can prescribe products that After pets are treated, fleas will continue to
provide several weeks of control with a single emerge and hop onto the animal; the host will
application. These are applied in a small volume harvest fleas from the surrounding environment
(afew milliliters) on the back of the animals neck until they have been killed and no more are emerg-
and distribute over the body surface in skin oils. In ing. Because it will take a while for fleas in the
 Caudate
C 801

environment to die off, some fleas may be seen on Cattle Grub, Hypoderma spp.
the animals for up to a month following treatment, (Diptera: Oestridae)
but that does not indicate product ineffectiveness.
When used prior to flea population build up, insect Livestock-infesting flies that migrate through the
growth regulators can break the flea life cycle. hosts body.
While these compounds do not kill adult fleas, they Myiasis
do prevent eggs and larvae from completing devel- Veterinary Pests and their Management
opment, ensuring that any fleas brought into the
area will not establish a sustaining population.
Due to their wide host range, fleas can con- Cattle Ticks
tinually move into homes and reinfest. Homes
without pets can develop severe cat flea problems Several ticks can be important parasites of cattle.
if wild or feral animals (raccoons, opossums, Ticks
skunks, etc.) nest in the crawl space or attic and Area-Wide Pest Management
share their fleas. Typically migrants den under the
structure in the spring; as their young abandon the Cauda
nest, fleas left behind climb up through subfloor-
ing, seeking a blood meal from any warm-blooded The pointed tip of the abdomen, the modified
host. Excluding potential carriers from the prop- ninth abdominal tergum, in aphids. It is some-
erty will reduce opportunities for reinfestation. times called the tail.
Sanitation is an important flea suppression tac- Abdomen of Hexapods
tic; by eliminating larval development sites and
destroying immature stages before they develop to
the pestiferous adult stage (Fig. 31), pets and people Caudal
can be protected from fleas. Areas frequented by pets
accumulate flea eggs and larval food, so these micro- Pertaining to the anal end of the body.
habitats should be vacuumed and treated with insect
growth regulators or borate products to prevent
flea infestations. Such areas include under furniture, Caudal Filaments
animal bedding and sleeping quarters, and utility
rooms or other locations where the pet spends time. Thread-like processes at the tip of the abdomen
Fleas (Fig. 32), often referred to as tails by non-
entomologists.
Abdomen of Hexapods
References
Caudal Lamellae
Durden LA, Traub R (2002) Fleas (Siphonaptera). In: Mullen
GR, Durden LA (eds) Medical and veterinary entomol-
ogy. Academic Press, San Diego, CA The caudal gills of damselflies.
Dryden MW, Broce AB, Cawthra J, Gnad D (1995) Urban
wildlife as reservoirs of cat fleas, Ctenocephalides felis.
In: American Association of Veterinary Parasitologists,
40th Annual Meeting. Pittsburgh, PA, p 65 Caudate
Holland GP (1964) Evolution, classification, and host rela-
tionships of Siphonaptera. Ann Rev Entomol 9:123146
Rust MK, Dryden MW (1997) The biology, ecology, and man- Having a tail-like process at the anal end of the
agement of the cat flea. Ann Rev Entomol 42:451473 body.
802
C Caudell, Andrew Nelson

Maxillary palpus

Antenna
Compound eye
Median ocellus
Labrum
Maxilla
Labial palpus
Labium
Pronotum

Mesonotum

Metanotum
Style
Coxa
Trochanter
Femur
Tibia
Tarsus
Pretarsus
Abdominal appendage II

Eversible sac

Lateral caudal filament (cercus)

Median caudal filament

Caudal Filaments, Figure 32 Dorsal (left) and ventral (right) view of a silverfish (Collembola).

Caudell, Andrew Nelson he published numerous papers on it. His other accom-
plishments included being president of the Entomo-
Andrew Caudell was born in Indianapolis on August logical Society of Washington in 1915, and publishing
18, 1872, and moved with his parents to a farm in with Nathan Banks The Entomological Code. A code
Oklahoma where he grew up. He became interested of nomenclature for use in entomology. Married,
in insects and later studied at Oklahoma Agricultural and with one daughter, he died on March 1, 1936.
College. After a brief employment in Massachusetts
with the Gypsy Moth Project, in 1898 he joined the
Reference
U.S. Department of Agriculture, studied Orthoptera,
and became custodian of Orthoptera at the U.S.
Mallis A (1971)Andrew Nelson Caudell. In: American ento-
National Museum. Study of this group of insects, mologists. Rutgers University Press, New Brunswick, NJ,
but including Zoraptera, became his lifes work, and pp 198200
 Cave Adapted Insects
C 803

Cave Adapted Insects

Steven J. Taylor
Illinois Natural History Survey, Champaign, IL,
USA

Insects inhabit nearly every conceivable habitat on

earth and often exhibit unique adaptations corre-
sponding to these environments. Caves are cer- Cave Adapted Insects, Figure 33 Haedonoecus
tainly among the more unusual and fascinating of subterraneus (Orthoptera: Rhaphidophoridae),
these habitats. Insects and other organisms living adult female. Note extremely long legs, palps,
in caves have evolved to deal with a set of unique and antennae adaptations that are
environmental conditions, and the species of cave advantageous in a cave. (Source: Packard AS
inhabiting insects vary in the degree to which they (1888) Cave fauna of North America. Memoirs Natl
are limited to life in caves. Species that must spend Acad Sci 4:1156+27 plates.)
their entire lives within caves are called troglobites.
Environmental conditions typical of habitat deep
within caves include: than their nearest surface relatives, further enhanc-
ing the often pale appearance we associate with
Complete absence of light cave-adapted animals.
Stable and usually very high (>95%) humidity Perhaps the most important aspect of cave
Relatively low levels of available nutrients life relating to the absence of light is its effect on
Nearly constant temperature the availability of energy. In the dark zone of caves
there are no primary producers no photosyn-
Troglobites are among the most interesting of thesizing plants. Interesting exceptions to this do
the cave-adapted species. Because they live in the occur, but by and large, cave communities depend
absence of light, many troglobitic insects have on organic debris that falls or washes into caves,
non-functional eyes. Most commonly, this is evi- the bodies of organisms that accidentally fall or
denced by the reduction or even complete loss of wander into caves, and fecal material and some-
the compound eyes. Instead, troglobitic insects times the bodies, eggs, or young of trogloxenes
may have greatly elongated antennae and legs (species that live in caves but must leave the cave
(Fig.33) relative to their nearest epigean (above- for part of their life cycle) that bring in energy
ground) relatives. Equipped with elongate setae, from outside the caves, such as bats and cave
these appendages allow the insects to detect nearby crickets. The cave community, then, is basically a
potential prey or predators in the absence of light. decomposer community. In many caves, insects
Troglobitic insects also may be particularly attuned play important roles in this community.
to detecting vibrations and chemosensory cues. The relatively low levels of energy available
There is little selective pressure for elaborate in many caves means that life is sparse, and, con-
coloration (camouflage, warning coloration) in the sequently, predators are rare. In comparison to
absence of light, and, as a result, many troglobitic their surface kin, troglobitic insects often move
insects are whitish or pale brown in coloration. The more slowly, live longer, and produce fewer and
high humidity of the caves, often in excess of 98%, larger eggs, all adaptations to deal with the lower
means that moisture retention is less of a problem energy levels of the cave environment. For exam-
than in many epigean habitats. Consequently, ple, the European catopid cave beetle, Speonomus
many cave insects have a thinner, less waxy cuticle longicornis, may live more than 3 years.
804
C Cave Adapted Insects

The near constant conditions in the cave Europe (e.g., Troglophilus), in Australia and New
usually mean that troglobites do not have very Zealand (where cave-dwelling species of Gym-
pronounced circadian rhythms of activity. This noplectron and other genera are known as cave
does not, however, mean that there are no envi- wetas) and elsewhere.
ronmental cues to indicate the passing of days or The feces of the roosting crickets provide food
seasons. Many caves breathe, taking in air or for other cave organisms, and the adult female
releasing it as the barometric pressure changes crickets typically deposit their eggs in the protec-
oras the temperature above ground rises and falls. tion of the cave, inserting their ovipositor into the
The movements of trogloxenes, such as cave crickets soft sandy cave soils. These eggs, of course, are a
and bats, also may be informative to the cave- dense source of nutrients, and in some areas there
limited species. Seasonal flooding of cave streams are troblobitic beetles of the family Carabidae. In
also can provide information about seasons (as the United States, common beetle genera that are
well as provide an influx of new nutrients). cave cricket (Ceuthophilus, and the more cave-
What specific organisms, then, live under the adapted but less widespread Haedonoecus) egg
above environmental conditions and exhibit these predators include ground beetles of the genera
sorts of adaptations? Rhadine and Neaphaenops (Fig. 34). Troglobitic
The hexapod order Collembola (Springtails) carabid beetles are often a pale rusty red in color,
contains many troglobites; a few of the genera with and the more cave-adapted species have no eyes,
cave-inhabiting species include Pseudosinella, or compound eyes reduced to only a few facets.
Onychiurus, and Folsomia. These tiny organisms Some cave-adapted carabid predators of cricket
feed on minute organic debris and the ubiquitous eggs have a narrowed and elongated head and
fungi that break down leaf litter, twigs, and fecal
material. Springtails sometimes are found on
the surface film of drip pools on cave floors (e.g.,
some Arrhopalites species). Troglobitic springtails
are sometimes present in large numbers, visible
to us as tiny white flecks moving about on the
substrate.
Trogloxenic cave or camel crickets of the
genus Ceuthophilus are one of the more prominent
insect inhabitants of many Nearctic caves. These
orthopterans roost in caves, usually high on walls
or on ceilings where they are less susceptible to
predation by cave visitors such as mice and rac-
coons. At night, some portion of the caves popula-
tion of Ceuthophilus sp. will emerge from the cave
(often about dusk) to forage for food above ground.
Most cave-inhabiting Ceuthophilus species exhibit
adaptations that suit them both for their night-
time excursions (mottled brown and black color-
ation, large powerful legs for jumping out of harms Cave Adapted Insects, Figure 34 Neaphaenops
way) and for life in the cave (most notably, their tellkampfi, a cave cricket egg predator found in
long, attenuated appendages, especially the anten- some Kentucky, USA, caves. (Source: Packard AS
nae). Other genera of Rhaphidophoridae occur in (1888) Cave fauna of North America. Memoirs Natl
caves in the United States (e.g., Haedonoecus), in Acad Sci 4:1156+27 plates.)
 Cave Adapted Insects
C 805

thorax, which presumably facilitate reaching deep found in caves, especially in the Mediterranean
into holes where cricket eggs may be found. region. In the United States, the staphylinid
The Coleoptera are one of the most successful Quedius spelaeus frequently is encountered, espe-
insect orders in caves, especially the families Cara- cially in association with cave stream riparian
bide, Leiodidae, and Staphylinidae. The first cave zones and leaf litter. One rather distinctive looking
invertebrate to be described (in 1832) was a carabid group of rove beetles, the Pselaphinae (mold beetles),
beetle, Leptodirus hohenwarti (Fig.35), in Europe. contains a number of very small, narrowly endemic
Many of the troglobitic carabids (ground beetles) troglobitic species of Batrisodes, found in caves of
are predators. The North American carabid genera south-central Texas. Round fungus beetles (Leio-
Rhadine and Neaphaenops contain troglobitic didae) of the genus Ptomophagus include several
species that may spend many hours searching for troglobitic species in North America.
the eggs, which they extract from the ground and A surprising number of flies are found in
consume. Psudanophthalmus is another carabid caves. Most famously, the larvae of the New Zealand
beetle genus frequently found in caves of the eastern cave glow-worm (Arachnocampa luminosa, Myce-
United States, where they feed on a variety of differ- tophilidae) are found on the ceilings of sometimes
ent things. Southern European caves harbor an spacious caverns. They are bioluminescent, and
unusually diverse cave carabid fauna. dangle sticky threads down from the ceiling which
Another group of beetles with some success capture prey items attracted to the light. In the
in the cave environment is the rove beetles United States, the predatory larva of the myceto-
(Staphylinidae). While significantly fewer species philid Macrocera nobilis, commonly known as the
of staphylinids are troglobites, they commonly are monorail worm, also makes sticky, web-like
structures on walls and floors of caves and moves
effectively both forward and backward along these
narrow strands. In temperate North American
caves, adults of several species of troglophilic
heleomyzid flies commonly are found on cave
walls and ceilings. Another common cave fly in
the eastern United States is Megaselia cavernicola
(Phoridae). In the winter, it is not unusual to
encounter large numbers of mosquitoes (Culici-
dae) overwintering in the relatively stable and
moderate conditions of a cave.
This brief look at cave insects certainly does
not represent the true diversity of taxa and inter-
esting adaptations that exist. While some of the
more common inhabitants of temperate North
American caves are emphasized here, the fauna of
tropical caves has been short-changed, as have the
incredible faunas of the lava tubes of the Canary
and Hawaiian islands, where pale, stilt-legged
Cave Adapted Insects, Figure 35 Leptodirus emisine reduviids stalk their prey and cixid
hohenwarti Schmidt, 1832. (Source: Jeannel (1949) hemipterans feed on tree roots and produce vibra-
Reprinted in Vandel, A (1965) Biospeloeology: the tory signals intended for potential mates. Nor
biology of caverniculous animals. Pergamon Press, have the other arthropods found in caves been
New York, NY, 524 pp) discussed. These include an amazing array of
806
C Cave Habitat Colonization

arachnids (spiders, mites, opilionids, ricinuliids, researchers have debated over the last 150 years is
etc.) and, especially in aquatic habitats, crusta- how animals came to live in caves, and how they
ceans (copepods, crabs, crayfish, isopods, amphi- have subsequently evolved. These two processes,
pods, etc.). The citations below serve as an cave colonization and speciation, are frequently
introduction to the large body of literature on confused in the literature. Here we describe mod-
cave invertebrates. els of cave colonization, and refer the reader to
Cave Habitat Colonization Taylor (this volume) and references below for fur-
ther details on speciation.
One of the first modern hypotheses for the
References origin of cave organisms was that of Vandel (1965),
who put forward the Pleistocene-effect model
Camacho AI (ed) (1992) The natural history of biospeleology. for the evolution of terrestrial troglobites (obligate
Monografias Museo Nacional de Ciencias Naturales, cave dwellers) in temperate regions. This model
Madrid, Spain, 680 pp
Chapman P (1993) Caves and cave life. HarperCollins,
has also been termed the relictual, isolation,
London, UK, 224 pp refugium or climate-relict model. Vandel pro-
Culver DC (1982) Cave life evolution and ecology. Harvard posed that troglobites evolved allopatrically from
University Press, Cambridge, MA, 189 pp epigean (surface dwelling) species, which had
Mohr CE, Poulson TL (1966) The life of the cave. McGraw-
Hill, New York, NY, 232 pp adapted to the cool climatic conditions of the
Vandel A (1965) Biospeloeology: the biology of caverniculous Pleistocene ice ages (1.5 million10,000 years ago).
animals. Pergamon Press, New York, NY, 524 pp When the glaciers retreated, these organisms were
subsequently restricted to more favorable climatic
habitats, such as deep wooded ravines, cool and
Cave Habitat Colonization moist forest floors and caves. Over time, with con-
tinued climatic variability and subsequent surface
David Slaney, Philip Weinstein habitat changes, the epigean populations became
Wellington School of Medicine and Health extinct. Under this model the resulting geographic
Sciences, Wellington, New Zealand isolation of cave populations leads to the allopat-
ric speciation of cave dwelling organisms. Vandels
Over the centuries people have keenly studied the model has been the traditional view for the origin
animals found in the sea, in rivers, and on the of cave populations, especially in temperate regions
land, but little attention has focused on animals such as Europe and North America where major
that inhabit caves. The ancient Greeks believed climatic changes during the Pleistocene have
that caves were the abode of the dead, and this occurred.
may have led to the belief that caves could not But what about tropical caves? Biological
possibly harbor life. However, large numbers of investigation of the worlds tropical caves did not
cave dwelling animals representing a wide diver- receive much attention until the 1970s. Before this,
sity of groups, such as insects, millipedes, amphi- scientists working in the Pleistocene-effect para-
pods, isopods, fish, and spiders, have been digm believed that troglobites were virtually non-
described over the last 200 years. The first pub- existent in tropical caves. The paucity of troglobites
lished work on biospeleology appeared in 1845, in these regions was explained by the lack of past
by the Danish zoologist, J.C. Schidte, describing climatic extremes required to restrict epigean pop-
animals he collected from caves in Italy. Thereaf- ulations to cave habitats. However, since the 70s
ter, biospeleological research began in earnest, both the discovery of large numbers of terrestrial
focusing on European and North American tem- troglobites in tropical regions such as Australia,
perate caves. One of the key questions that the Canary and Galpagos Islands, Hawaii, and
 Cave Habitat Colonization
C 807

Jamaica, combined with the mounting evidence variant of Howarths adaptive-shift theory, but
that significant past climatic fluctuations occurred includes the possibility of subsequent events,
in much of the world during the Pleistocene, has including climatic changes, leading to speciation.
made biologists reconsider the evolutionary ori- The biological interactions that lead to coloniza-
gins of troglobites in the tropics. For example, it is tion may include invasion as an immediate
postulated that cavernicolous species of cock- refuge from surface abiotic stresses, opportun-
roaches in North Queensland have arisen as a ism (caves as new niches to be colonized) or a
result of isolation in moist refugia during periods result of competition or predation pressure in
of increasing aridity in Australia in the late surface habitats.
Cenozoic. Hypotheses for the evolution of subterra-
In 1973 Howarth proposed the adaptive-shift nean organisms are still debated today, with a
model to account for the origin of tropical troglo- regular re-elaboration of the fundamental sce-
bites in lava tubes of the Hawaiian Islands where narios described above. To date research evidence
epigean congeners of the cave dwelling species has failed to falsify any alternative models, and
have been found. This model has also been termed no generalized single theory has been put for-
the local habitat shift or invasion model. How- ward. The origin of a particular cave dwelling
arth proposed that pre-adapted species move organism should perhaps best be interpreted
into newly developed cave habitats to exploit the based on the evidence that explains the origin
resources not otherwise available on the surface, of that organism, and may invoke a combination
with troglobites evolving parapatrically or sympat- of biological and or abiotic factors leading to col-
rically through an adaptive-shift rather than by onization (and speciation) in those individual
isolation induced by climatic change. Under this circumstances.
model caves do not act as refugia from episodic Cave Adapted Insects
climatic changes, instead their colonization is a
continuing process. Speciation follows as a result
of isolation of organisms brought about by an
References
adaptive-shift, and does not relate directly to climate
change. As with Vandels model, Howarths model
Barr TC Jr (1968) Cave ecology and the evolution of troglo-
incorporates both processes of colonization and bites. Evol Biol 2:35102
of speciation. Culver DC (1982) Cave life: evolution and ecology. Harvard
A related model to the adaptive-shift model University Press, Cambridge, MA
Howarth FG (1973) The cavernicolous fauna of Hawaiian
is the active colonization model put forward by
lava tubes. Pacific J Insects 15:139151
members of the Laboratoire Souterrain du CNRS Howarth FG (1987) The evolution of non-relictual tropical
in France, which applies to temperate as well as troglobites. Int J Speleology 16:116
tropical caves. In addition to cave habitats, the Rouch R, Danielopol DL (1987) L origine de la faune aqua-
tique souterraine, entre le paradigme du refuge et le
researchers have studied the colonization of modle de la colonisation active. Stygologia 3:345372
interstitial voids found in soil and screes (termed Slaney DP (2001) New species of Australian cockroaches in
the milieu souterrain superficiel or superficial the genus Paratemnopteryx Saussure (Blattaria, Blattel-
hypogean compartment). They suggest that cli- lidae, Blattellinae), and a discussion of some behavioural
observations with respect to the evolution and ecology
matic events may not be the primary factors of of cave life. J Nat Hist 35:10011012
cave colonization, but that colonization is an Vandel A (1965) Biospeleology: the biology of cavernicolous
active phenomenon in new biotypes. Climatic animals (translated by Freeman BE). Pergamon Press,
Oxford, UK, 524 pp
changes are considered as a localized model, with
Weinstein P (1994) Behavioural ecology of tropical cave
organisms colonizing caves as a result of a num- cockroaches: preliminary field studies with evolution-
ber of biological interactions. This model is a ary implications. J Aust Entomol Soc 33:367370
808
C Cayenne Tick, Amblyomma cajennense Fabricius (Ixodida: Ixodidae)

Cayenne Tick, Amblyomma Cell

cajennense Fabricius (Ixodida:
Ixodidae) The fundamental unit of life. Each multicelled
organism is composed of cells. Cells may be orga-
This disease vector is found throughout the nized into organs that are relatively autonomous
Americas. but cooperate in the functioning of the organism.
Ticks This term also is used to describe any area of a
wing that is between or bounded by veins. Wing
cells are named after the vein forming the upper
cDNA
margin, and are numbered from the base
The double-stranded DNA copy of a eukaryotic outward.
messenger RNA molecule, produced in vitro by
enzymatic synthesis and used for production of
cDNA libraries or probes for isolating genes in Cell Culture
genomic libraries.
The growing of cells in vitro, or in an artificial con-
tainer rather than in an organism.
cDNA Library
A collection of clones containing dsDNA that is Cell Culture of Insects
complementary to the mRNA. Such clones lack
introns and regulatory regions of eukaryotic genes. Jun Mitsuhashi
Once cDNA molecules are transcribed, they are Tokyo University of Agriculture, Tokyo, Japan
inserted into a vector and amplified in E. coli.
Insect tissue culture was initiated by R. Gold-
Cecidomyiidae schmidt in 1915. He cultured spermatocytes of
Hyalophora cecropia (Lepidoptera: Saturniidae)
A family of flies (order Diptera). They commonly in hemolymph of the same species. He could
are known as gall midges. maintain the spermatocytes for more than 3
Flies weeks, and observed spermatogenesis in vitro. His
Gall Midges (Diptera: Cecidomyiidae) culture may be taken as organ culture, because he
did not aim to proliferate cultured cells. Later,
W. Trager (1935) established standard methods for
Cecidosidae insect cell culture. He devised media proper
for insect cell culture, and with it he successively
A family of moths (order Lepidoptera). They also
cultured Bombyx mori (Lepidoptera: Bombyci-
are known as gall moths.
dae) ovarian cells for several weeks. In 1956, Wyatt
Gall Moths
formulated a synthetic medium based on the
Butterflies and Moths
chemical composition of insect hemolymph. The
composition of her medium is still used at present
Cedar Beetles as the base of formulation of new media. In 1962,
the first insect continuous cell line (a cell popula-
Members of the family Callirhipidae (order tion which continues to proliferate unlimitedly)
Coleoptera). was established by Grace. He obtained perma-
Beetles nently growing cells from the culture of the
 Cell Culture of Insects
C 809

ovarian cells of Antheraea eucalypti (Lepidoptera: Physical Conditions

Saturniidae). Since then, more than 400 insect cell
lines have been established. They include 172 dip- Culture conditions may be divided into physical
teran cell lines (115 from Drosophila melanogaster conditions and chemical conditions. As the former,
and 47 from 22 mosquito species), 147 lepi- temperature, pH, osmotic pressure and illumination
dopteran cell lines, 16 coleopteran cell lines, 15 will be considered. The insect cells are usually cul-
hemipteran cell lines, 13 hymenopteran cell lines, tured. Between 20 and 30C, the growth rate increases
11 blattarian cell lines, and 1 orthopteran cell line. with the rise of temperature. Most of insect cells,
The history of insect tissue culture development however, deteriorate above 30C. Usually insect
before 1962 was reviewed by Day and Grace cells are not affected by the change in the pH of the
(1959). culture media between 6.0 and 7.5, and are rather
Standard methods to initiate primary cul- resistant to the change of osmotic pressure. Most
ture of insect tissues are as follows: The insects insect cell culture media have osmotic pressure
used should be aseptic or surface-sterilized. Tis- between 300 and 400 mOsmol/kg. However, cells
sues or organs to be cultured are excised under may survive even in the medium diluted to half
sterile conditions. The excised tissues or organs strength. Illumination does not affect on cell survival
are washed in saline, and cut into small pieces. or growth, although UV or sunlight is harmful to the
The resulting tissue fragments are washed again, cells. Photoperiodism has no effect on insect cells
and transferred into culture flasks with culture either, i.e., long night photoperiod does not induce
medium (explant culture). In some cases, espe- arrest of cell growth.
cially D. melanogaster cell culture, excised tissues
are often dissociated further into single cells by
means of partial digestion with an enzyme, and Chemical Conditions
are seeded as separated single cells. Generally,
explant culture is common in insect cell culture, For chemical conditions, composition of culture
and gives better results. At present, techniques media and gaseous phase will be considered. Cells
for insect cell culture are far from one which require inorganic salts for maintaining ion bal-
enables scientists to make cell culture from any ance, sugars as energy source, amino acids for
tissue of any species, and improvement of the protein synthesis, vitamins and some growth
techniques continues. factors for survival and proliferation. Usually
In explant culture, cell migration from approximately six inorganic salts are used. Na+, K+,
explants begins soon after the culture is estab- Ca++, Mg++, PO4, and Cl will be required. As energy
lished. These migrated cells generally consist of sources, glucose satisfies the requirement. Usually
epithelial-like, fibroblast-like and hemocyte-like 20 amino acids, which are constituents of proteins,
cells. The epithelial-like cells and fibroblast-like are incorporated into a medium, although the
cells often form cell sheets and cellular networks, essential amino acids are arginine, cystine, glu-
respectively, while the hemocyte-like cells do not tamine, glycine, histidine, isoleucine, leucine,
form any structure. The migrated cells may prolif- lysine, methionine, phenylalanine, proline, serine,
erate by mitoses, and subculture may become threonine, tryptophan, tyrosine, and valine. As
possible, if the culture conditions are appropriate. vitamins, water-soluble B group vitamins are com-
However, usually it takes several months or even monly used. They are, in most media, thiamine,
years for the cells to proliferate enough to be sub- riboflavin, calcium pantothenate, niacin, pyri-
cultured. By repeating subcultures, a cell line may doxine, biotin, folic acid, p-aminobenzoic acid,
become a permanently growing cell population, isoinositol and choline chloride. However, some of
which is called a continuous cell line. them are not essential. For example, the flesh fly
810
C Cell Culture of Insects

(Diptera: Sarcophagidae) embryonic cell line, oxygen supply is necessary, and it is performed by
NIH-SaPe-4, requires only thiamine, riboflavin, oxygen sparger directly into the media. The control
calcium pantothenate and either of niacin or of CO2 concentration in gaseous phase is not nec-
niacinamide. The vitamin requirement by insect essary for insect cells, because insect cells are insen-
cells in culture may depend on cell line species. sitive to the change in the pH of the culture media.
Most insect cells do not require added lipid-soluble
vitamins, such as vitamin A, D, E, and K.
Instead of using individual chemicals, natural Characteristics of Cells
substances, which contain necessary substances
for cell growth, may be used. Seawater may be used The structure of the cultured cells varies even in a
instead of mixtures of inorganic salts. Some pro- cell line. The shape and the size of the cells are not
tein hydrolysates, such as lactalbumin hydrolysate, uniform. Also, karyotype of the cells varies. Tetra-
casein hydrolysate, egg albumin digest and so on, ploid cell lines are common among lepidopteran
are used in lieu of mixture of 20 or 21 individual cell lines. The karyotype may change by repeating
amino acids. Water-soluble yeast extract products subculture. Some insect cell lines are substrate-
contain usually sorts and amounts of vitamins for dependent, and form cell sheets. Others are sub-
insect cell growth, and are used instead of the mix- strate-independent and can grow in suspension.
ture of individual vitamins. The media containing Growth rate is different in different cell lines. The
natural substances are called natural media population doubling time distributes from 20 h to
whereas those contain only known chemicals are several days. Insect cell lines cannot be distin-
called as synthetic media. guished morphologically from each other. However,
However, both types of media need to be forti- they can be distinguished each other by analyses of
fied by addition of sera or some other growth-pro- karyotype, isozyme pattern, PCR, DNA finger print-
moting substances. As sera, heat-treated insect ing, and the combination of these techniques.
hemolymph or fetal bovine serum (FBS) is used. Insect cell culture is a good tool for basic stud-
Among commercially available vertebrate sera, only ies in various fields. Established cell lines are more
FBS is markedly growth-promotive. Other sera, or less different from cells in intact insects. The cell
such as calf serum bovine serum, horse serum, lines, however, retain many characteristics that
turkey serum and sheep serum are either ineffective they had when they were in insect bodies. There-
or even detrimental. Other than sera, growth fac- fore, cell lines can be used as excellent experimental
tors or some other growth-promoting substances materials, if one keeps the difference of cells in
are used as an additive. As growth factors, only one vivo and in vitro in mind. Insect cell lines have
insect growth factor has been isolated from the flesh been used in various fields, such as cell physiology,
fly cell line, so far, NIH-SaPe-4. This growth factor is cytogenetics, biochemistry, endocrinology, toxi-
a polypeptide and acts in autocrine manner, and cology, gene technology and pathology. Among
seems to be species specific, or to have narrow spec- them insect cell cultures have been used frequently
trum. Vertebrate growth factors are ineffective on in the studies of insect pathology, especially virus
insect cells, except insulin, which is reported to be diseases, for a long time.
growth stimulative for D. melanogaster cells.
For the gas composition in gaseous phase as
well as in media, oxygen is required in large-scale Practical Applications
culture of cells. In small-scale culture, insect cells
do not consume much oxygen, and the cells can be For practical use, insect cell culture is being used in
cultured in tightly capped flasks. For large-scale combination with insect viruses for production of
culture (several liters to several 100 L), however, foreign protein, and viral insecticides. In the former
 Centipedes (Class Chilopoda)
C 811

case, baculovirus vector systems are now widely Celyphidae

used to produce proteins not originating from
insects. For example, gene encoding human A family of flies (order Diptera).
interferon- is inserted into the polyhedrin gene Flies
sequence of NPV, which is previously inserted into
an Escherichia coli plasmid. The resulting plasmid is
transfected with wild virus genome to the NPV-sen- Cement
sitive insect cell line. In this way, recombinant NPV,
which contains the human interferon- gene in the This is a very thin lipid or shellac-like layer of
sequence of polyhedrin gene, is obtained. The human integument outside the wax layer. It serves to pro-
interferon- can be produced by inoculating the tect the wax layer from disruption.
recombinant virus to the NPV-sensitive cell culture. Integument: Structure and Function
For the production of viral insecticides, the
process of cell culture, preparation of inoculum,
inoculation, maintenance of infected cells, and Cenchrus (pl., Cenchri)
harvest of replicated viruses have been almost
established. However, when one tries to increase A roughened section of the metanotum in saw-
the scale of culture, various problems arise, and flies; it serves to hold the wings in place when they
the production of viruses by means of large scale are folded over the body.
culture of insect cells and viruses has not yet
been industrialized. The problems to be solved
include oxygen supply, avoidance of shear force, Census
and cost of culture media. The insect cell lines
may be used for toxicity tests. In the screening Complete enumeration of every individual within
tests for insecticides, cultured cells are good a defined sample universe. (contrast with sample).
materials for screening chemicals, which act on Sampling Arthropods
metabolic pathways. Drugs for human such as
anti-cancer drugs may be tested at the screening
level by the use of insect cells. Insect cells can be Centipedes (Class Chilopoda)
cultured without a CO2 incubator, and are toler-
ant to the change in pH, osmotic pressure and The centipedes are not numerous, numbering
temperature. These are advantages of using insect about 3,000 species around the world. However,
cell culture over mammalian cell culture. they are widely distributed in both temperate and
tropical regions, where they are found in soil,
under litter, and beneath stones and bark.
References

Day MF, Grace TDC (1959) Culture of insect tissues. Ann Rev Characteristics
Entomol 4:1738
Goldschmidt R (1915) Some experiments on spermatogene-
sis in vitro. Proc Natl Acad Sci USA 1:220222 Centipedes usually are 110 cm in length, but
Grace TDC (1962) Establishment of four strains of cells from may be larger in the tropics, where they can attain
insect tissues grown in vitro. Nature 195:788789 a length of up to 26 cm. They possess but one pair
Trager W (1935) Cultivation of the virus of grasserie in silk-
of legs per segment, a feature that allows them to
worm tissue cultures. J Exp Med 61:501513
Wyatt SS (1956) Culture in vitro of tissue from the silkworm, be easily distinguished from the superficially sim-
Bombyx mori. LJ Gen Physiol 39:841852 ilar millipedes (Diplopoda). Like many other
812
C Centipedes (Class Chilopoda)

arthropods (millipedes, pauropods, symphylans), Classification

but unlike insects, the centipedes bear a head and
a long trunk with many leg-bearing segments. The As is the case with many taxa of arthropods, the
head bears a pair of antennae, and sometimes classification of centipedes is subject to debate.
ocelli, but not compound eyes. The mouthparts are Following is a recent classification system:
ventral, and positioned to move forward. Gas Phylum: Arthropoda
exchange is through a tracheal system in which Subphylum: Atelocerata
the spiracles cannot be closed. Excretion takes Class: Chilopoda
place through malpighian tubules, and unlike Subclass: Epimorpha
insects and arachnids, centipedes excrete ammo- Order: Geophilomorpha
nia.. The heart is a dorsal tube with paired ostia at Family: Himantariidae
each segment. The ventral nerve cord has a gan- Family: Schendylidae
glion for each body segment. Sperm transfer is Family: Oryidae
indirect, using a spermatophore. Structures called Family: Mecistocephalidae
Tmsvry organs are found at the base of the Family: Geophilidae
antennae in some centipedes. Apparently it is used Family: Chilenophilidae
to detect vibrations. The orders Geophilomorpha Family: Eriphantidae
and Scolopendromorpha exhibit epimorphic Family: Dignathodontidae
development; the young have the full complement Family: Aphilodontidae
of segments when they hatch. Development of the Family: Gonibregmatidae
other orders is anamorphic; the young have only a Family: Neogeophilidae
portion of their eventual complement of segments Order: Scolopendromorpha
upon hatching, and add them as they grow. Family: Scolopendridae
Covering the mouthparts of centipedes is a Family: Cryptopidae
pair of structures called maxillipeds or poison Subclass: Anamorpha
claws. They are derived from the first pair of Order: Lithobiomorpha
trunk appendages, but are involved in feeding. Family: Lithobiidae
Each claw consists of four segments and is curved Family: Ethopolidae
inward toward the midventral line. A poison Family: Watobiidae
gland is found within the base of the claw. Centi- Family: Gosibiidae
pedes are well known for their poison claws, but Family: Pseudolithobiidae
they have other defenses as well. In some, the Family: Pterygotergidae
posterior-most legs may be used for pinching, Family: Henicopidae
and repugnatorial glands on the last four legs are Order: Craterostigmomorha
common. As with millipedes, defensive secre- Order: Scutigeromorpha
tions may include hydrocyanic acid. Except for Family: Scutigeridae
the geophilomorphs, centipedes are adapted for The Epimorpha are longer centipedes, usually
running. Interestingly, the legs of some long- consisting of at least 21 leg-bearing segments.
legged centipedes are progressively longer toward Young epimorphs, upon hatching, bear a full
the posterior of the body, which helps to prevent complement of long or short legs. Tmsvry
interference with leg movement. The soil dwell- organs are absent. In contrast, the Anamorpha are
ing geophilomorphs do not use their legs for shorter, usually with 15 leg-bearing segments.
running, and these animals move through the Young anamorphs, when the hatch, bear 47 pairs
soil using extension and contraction of the body of long or very long legs. Tmsvry organs are
trunk, much the same as earthworms. present. The order Geophilomorpha consists of
 Central Nervous System (CNS)
C 813

about 1,000 species, order Scolopendromorpha of Reference

a bout 550 species, Lithobiomorpha of about 1,100
species, order Craterostigmomorpha only two Lewis JGE (1981) The biology of centipedes. Cambridge
species, and Scutigeromorpha about 130 species. University Press, Cambridge, UK, 476 pp
The geophilomorphs are long worm-like animals,
highly specialized, dwelling in soil, and not primi-
tive, whereas the scutigeromorphs are long-legged Central Body
forms, commonly found around human habita-
tions, and clearly are primitive. The Scolopen- A region in the center of the protocerebrum that
dromorpha and Lithobiomorpha both consist of serves as an integration point for different types
heavy-bodied animals that live beneath stone, of information, and for activation of body move-
bark and logs. ments associated with the thoracic region. The
central body is located between the bases of
the stalks of the mushroom bodies. It receives
Ecology input from both sides of the brain, and from the
optic lobes.
Life histories of centipedes are poorly known, but Central Body
56 instars occur in many species. Longevity is
often 36 years, and it commonly takes more than
a year to attain maturity. It is difficult to separate
instars, but head capsule width is most reliable. Central Dogma
The centipedes are predaceous. Most feed on
The Central Dogma was proposed by F. Crick in
arthropods, snails, earthworms and nematodes, but
1958. It states that the genetic information is con-
even toads and snakes are consumed by some. The
tained in DNA, which is transcribed into RNA,
antennae and legs are used to detect prey. The poi-
which is translated into polypeptides. The transfer
son claws are used to stun or kill the prey. Though
of information was proposed to be unidirectional
painful, the bite of centipedes is normally not lethal
from DNA to polypeptides: polypeptides are
to humans, resembling the pain associated with a
unable to direct synthesis of RNA, and RNA is
wasp sting.
unable to direct synthesis of DNA. The Central
Centipedes require a humid environment.
Dogma was modified in 1970 when RNA viruses
Their integument is not waxy, and their spiracles
were found to transfer information from RNA
do not close. Hence, they are found belowground,
to DNA.
in sheltered environments, or active above-ground
principally at night. Some centipedes have adapted
to a marine existence, living among algae stones
and shells in the intertidal zone. Apparently Central Nervous System (CNS)
they can retain sufficient air during high tides,
or capture a sufficiently bubble of air to allow In insects, the central nervous system consists of
submersion. the brain, ventral ganglia, and the ventral nerve
Some centipedes (scolopendromorphs and cord. The ventral ganglia and connecting nerve
geophilomorphs) produce a cavity in soil or cord usually lie close to the cuticle on the ventral
decayed wood in which to brood their egg clutch, side of the body. The brain occurs on top of the
which often numbers 1535 eggs. The female esophagus, and is sometimes called the suprae-
guards the eggs until the young hatch. Inte remain- sophageal ganglion.
ing taxa, the eggs are deposited singly in the soil. Nervous System
814
C Centromere

Centromere Ceraphronidae

A region of a chromosome to which spindle A family of wasps (order Hymenoptera).

fibers attach during mitosis and meiosis. The Wasps, Ants, Bees and Sawflies
position of the centromere determines whether
the chromosome will appear as a rod, a J, or a V
during migration of the chromosome to the poles
Ceratocanthid Scarab Beetles
in anaphase. In some insects, the spindle fibers
Members of the family Ceratocanthidae (order
attach throughout the length of the chromosome
Coleoptera).
and such chromosomes are called holocentric.
Beetles
Centromeres are usually bordered by heterochro-
matin containing repetitive DNA.
Ceratocanthidae

Cephalothorax A family of beetles (order Coleoptera). They com-

monly are known as ceratocanthid scarab beetles.
The fused head and thorax of Arachnida and Crus- Beetles
tacea, and of coccids.
Ceratocombidae
Cephidae A family of bugs (order Hemiptera).
Bugs
A family of sawflies (order Hymenoptera, subor-
der Symphyta). They commonly are known as
stem sawflies. Ceratophyllidae
Wasps, Ants, Bees and Sawflies
A family of fleas (order Siphonaptera). They some-
times are called bird and rodent fleas.
Cerambycidae Fleas

A family of beetles (order Coleoptera). They com-

Ceratopogonidae
monly are known as longhorned beetles.
Beetles
A family of flies (order Diptera). They commonly
Longicorn, Longhorned, or Round-headed
are known as biting midges, punkies or no-see-ums
Beetles (Coleoptera: Cerambycidae)
midges.
Flies
Biting Midges, Culicoides sp. (Diptera:
Cerambycoid Larva Ceratopogonidae)
A larval body form that is straight, somewhat
flattened or cylindrical, smooth or naked, and Cercoccidae
distinctly segmented. They tend to be found in
wood or soil, and occur in the families Ceramby- A family of insects in the superfamily Coccoidae
cidae, Buprestidae, and Elateridae (all in order (order Hemiptera).
Coleoptera). Bugs
 Cereal Stem Moths (Lepidoptera: Ochsenheimeriidae)
C 815

Cercophanidae Cercus

A family of moths (order Lepidoptera) also known

as Andean moon moths.
Andean Moon Moths
Butterflies and Moths
Cercus

Cercopidae

A family of insects in the order Hemiptera. They

sometimes are called froghoppers or spittlebugs.
Cercus
Bugs

Cercus (pl., cerci)

A sensory appendage (Fig.36) located near the tip Cercus

of the abdomen, usually on abdominal segment
ten. In many insects the c erci are antenna-like in
shape, paired and jointed.
Abdomen of Hexapods

Cercus, (pl., cerci) Figure 36 Diagrams of the tip

Cereal Leaf Beetle, Oulema of the abdomen in various hexapods, showing
melanopus (Linnaeus) various forms of the cercus. Top left, earwig; top
(Coleoptera: Chrysomelidae) right grasshopper, lower left, scorpionfly; lower
right silverfish.
This leaf-feeding beetle is a pest of small grain
crops. superfamily Yponomeutoidea in the section
Wheat Pests and their Management Tineina, subsection Tineina, of the division Ditry-
sia. Adults small (917 mm wingspan), with head
very roughened; eyes large; haustellum short and
naked; labial palpi tufted; maxillary palpi 2-seg-
Cereal Stem Moths (Lepidoptera: mented; antennae often basally swollen in males.
Ochsenheimeriidae) Wings rather elongated but fringes average. Macu-
lation somber hues of brown or gray, with indis-
John B. Heppner tinct markings. Adults are diurnal. Larvae are
Florida State Collection of Arthropods, leafminers, but become stem borers in later instars,
Gainesville, FL, USA primarily on grasses (Gramineae), sedges (Cyper-
aceae) and rushes (Juncaceae). The common name
Cereal stem moths, family Ochsenheimeriidae, for the family is derived from the single economic
include only 17 species from the Palearctic (one species, the cereal stem moth. Some place the fam-
sp. is from Kashmir), with one sp. introduced ily as a subfamily of what is grouped as the fam-
into North America. The family is part of the ily Ypsolophidae (the latter actually a subfamily
816
C Cerebellum

of Plutellidae). The family and nominate genus Cerumen

Ochsenheimeria are named after the German lepi-
dopterist Ferdinand Ochsenheimer (17671822). A brown mixture of wax and propolis used by
social bees for nest construction.

References
Cervical Shield
Davis DR (1975) Review of Ochsenheimeriidae and the intro-
duction of the cereal stem moth Ochsenheimeria vac- A plate on the dorsal surface of caterpillars just
culella into the United States (Lepidoptera: Tineoidea). behind the head. It is also known as the protho-
Smithsonian Contrib Zool 192:120
Davis DR (1998) Ochsenheimeriidae. In Lepidopterorum racic plate or shield.
Catalogus, (n.s.). Fasc 48. Association for Tropical Lep-
idoptera, Gainesville, FL, 12 pp
Karsholt O, Nielsen ES (1984) A taxonomic review of the stem
moths, Ochsenheimeria Hbner, of northern Europe (Lepi-
Cervix
doptera: Ochsenheimeriidae). Entomol Scand 15:233247
Ral P (1966) Famille des Ochsenheimeriidae. In: Balachowsky The membranous region between the head and
AS (ed) Entomologie Applique l Agriculture. Tome 2: thorax (Fig. 37). The cervix is analogous to the
Lpidoptres, 254255. Paris, 1057 pp
Zagulajev AK (1988) Family Ochsenheimeriidae. In: Fauna
neck in vertebrates.
SSSR. 4. Lepidoptera, 7: 70177. Acad. Nauk. [in Russian],
St. Petersburg
Cervical Sclerites
Cerebellum Small chitinous plates on the membrane between
the head and the thorax.
The subesophageal ganglion, a portion of the vis-
ceral nervous system that innervates many of the
appendages associated with feeding. Cerylonidae
Nervous System
A family of beetles (order Coleoptera). They com-
monly are known as minute bark beetles.
Cerebrum Beetles

The portion of the brain above the esophagus; the

region before the subesophageal ganglion. There Cestodes or Tapeworms
are three recognized portions, the proto-, deutero-
and tritocerebrum. Hilary Hurd
Nervous System Keele University, Keele, Staffordshire, United
Kingdom

Cerococcidae The majority of tapeworms (phylum Platyhelmint-

hes, order Cestoda) that have terrestrial life cycles
A family of insects in the superfamily Coccoidae utilize two hosts. The adult worms are found in the
(order Hemiptera). They sometimes are called gut lumen of the final, or definitive host, where
ornate pit scales. they undergo sexual reproduction and produce
Bugs eggs that contain a developing embryo protected
 Cestodes or Tapeworms
C 817

lateral ocellus
compound eye
postocular area
cervix
gena
cervical sclerites
antenna tentorial suture
basimandibular sclerite
maxilla
clypeus labium

labrum labial palpus

mandible

maxillary palpus

Cervix, Figure 37 Side view of the head of an adult grasshopper, showing some major elements.

by several membranes. These eggs are shed into the fleas also ingest tapeworm eggs when feeding on
environment with the host feces, either still con- host feces. The immature worms develop with the
tained within the tapeworm segment, or proglottis, larval flea and are ingested by the definitive host
in which they developed, or free from it. The life when the adult flea is accidentally eaten during
cycle continues when eggs are ingested by an inter- grooming. Dogs become infected with the dog
mediate host, often a coprophagous insect or other tapeworm, Dipylidium caninum, in this way and,
arthropod. They hatch within the insect gut and for the latter species, so do cats and occasionally
burrow through the gut wall with the help of 3 pairs humans.
of curved hooks and the lytic contents of a pair Prevalence of cestode infection in the defini-
of glands. In the hemocoel, they transform into a tive host may be linked with seasonal changes in
metacestode and, once mature, will be transmitted feeding patterns. Thus, a study of the shrew Sorex
and the life cycle completed if their intermediate araneus araneus in Poland demonstrated that a
host falls prey to another definitive host. spring and summer diet including the copropha-
Fecal material from infected definitive hosts gous beetle, Geotrupes stercorosus, gave rise to
may be more attractive to insects than that infections with Ditestolepis diaphana and Staphy-
from uninfected hosts, as is the case for feces from locystis furcata in the summer and autumn.
rats infected with a rate tapeworm, Hymenolepis Whereas in the winter and spring, the predomi-
diminuta. This enhances the chances of the cestodes nance of Pseudodiorchis prolifer infections in the
life cycle being completed. Another rat tapeworm, shrew reflected a change of diet in the autumn and
Raillietina celebensis (also an occasional parasite winter to the myriopod intermediate host of this
of humans), provides an example of the means latter cestode, as beetles were difficult to find.
whereby a non-coprophagous insect becomes an Due to the trophic nature of tapeworm trans-
intermediate host. Gravid proglottides, detached mission, definitive hosts of cestodes associated
from the main tape and remaining intact, are with insects are partially or entirely insectivorous.
picked up from the fecal material by ants, carried Thus, with the possible exception of cestode infec-
to the nest and fed to the ant larvae. Some larval tions in the poultry industry, tapeworms that
818
C Cestodes or Tapeworms

utilize insect intermediate hosts are of no medical the binding site of juvenile hormone to the follicu-
or veterinary importance and have, therefore, lar epithelium results in a retardation in the devel-
attracted little research attention. The exception is opment of patency in the follicular epithelium,
the rat tapeworm, H. diminuta, which has been the thereby affecting yolk uptake. Synthesis of yolk pro-
doyen of cestode laboratory research models tein in the fat body also is inhibited but, in this case,
due to the ease with which its life cycle can be by a factor of parasite origin that is peptidergic in
maintained. nature. The effect of infection on male reproductive
Several insects act as intermediate hosts for the physiology is not as well studied. An increase in the
rat tapeworm including fleas and cockroaches size, protein and trehalose content of the bean-
(Fig.38), but laboratory studies have focused upon shaped accessory glands has been reported and this
the effect of infection on the flour beetles, Tribolium may account for an increase in protein and treha-
spp. and Tenebrio molitor. Long-term studies have lose content of spermatophores produced by
revealed that infection results in a 50% depression infected males. In contrast, male response to female
in the equilibrium population of T. confusum as a sex pheromone is decreased by infection. The effect
result of fecundity reduction in the females. The of these changes on the number of offspring pro-
mechanism underlying fecundity reduction has duced by females mated with infected males is yet
been extensively studied in T. molitor, and appears to be established unequivocally.
to result both from the host response to the pres- Although cestodes cause a reduction in the
ence of the parasite and to the direct action of a reproductive fitness of beetles, it has been demon-
factor(s) produced by the early developmental strated that the life span of infected female T. molitor
stages of the parasite. Several aspects of the process is increased by 40% and males by 25%. This may be
of vitellogenesis or the production and uptake of due to changes in resource management such that
yolk protein are affected. In the ovary, yolk uptake longevity is increased when fewer resources are
by developing follicles is retarded and they contain devoted to reproduction.
less protein than their equivalents from uninfected The production of aggregation pheromones is
beetles. The presence of a competitive inhibitor of down-regulated by infection, and several aspects
of behavioral response to environmental cues are
altered, although this does not appear to increase
Adult worm infects the rat gut the chance of host predation by rats. However,
defensive glands are everted less frequently, and
toluquinone and m-cresol production are reduced,
possibly accounting for the greater likelihood that
infected beetles will be eaten by rats. This may thus
Metacestode in the
insect hemocoel represent an example of host manipulation that
will enhance transmission prospects.
Eggs shed
with feces

References
Intermediate host,
Tenebrio molitor
Blankespoor CL, Pappas PW, Eisner T (1997) Impairment of
the chemical defence of the beetle, Tenebrio molitor, by
metacestodes (cysticercoids) of the tapeworm, Hyme-
nolepis diminuta. Parasitology 115:105110
Cestodes or Tapeworms, Figure 38 The life cycle
Carver FJ, Gilman JL, Hurd H (1999) Spermatophore produc-
of Hymenolepis diminuta, an example of an tion and spermatheca content in Tenebrio molitor infected
insect-associated cestode. with Hymenolepis diminuta. Insect Physiol 45:565569
 Chagas, Carlos Justiniano Ribeiro
C 819

Hurd H (2001)Parasite regulation of insect reproduction: American trypanosomiasis. Chagas disease is an

similar strategies, different mechanisms? In: EdwardsJP,
endemic insect-borne disease found in Central
Weaver RJ (eds) Endocrine interactions of parasites and
pathogens. Bios Scientific Publishers, Oxford, UK and South America from Mexico to Argentina. It
Kisielewska K (1961) Circulation of tapeworms of Sorex ara- is caused by the protozoan Trypanosoma cruzi.
neus araneus L. in biocenosis of Bialowieza National In discovering this malady, he became the only
Park. Acta Parasitol Pol 9:31369
Webb TJ, Hurd H (1999) Direct manipulation of insect repro-
individual investigator so far who described com-
duction by agents of parasite origin. Proc R Soc Lond B pletely all elements of the disease: the pathogen,
Biol Sci 266:15371541 vector, host, clinical manifestations, and epide-
miology. He also developed a new and effective
Chaeta (pl., chaetae) approach to malaria control, a technique that
remains the principal method for malaria sup-
An outgrowth of the cuticle originating in a pit. It pression around the world.
is an articulated spine-like process. Chagas was born on July 9, 1879 in Oliveira,
in the state of Minas Gerais, Brazil. He was the son
of upper-class parents who owned a small coffee
Chaeteessidae plantation. His ancestors had come to Brazil in the
seventeenth century. His father died when Carlos
A family of praying mantids (Mantodea). was only 4 years old, and at the age of seven he
Praying Mantids wassent to a Jesuit boarding school. There he was
befriended by a priest who instilled in him a love
Chaetotaxy of natural history. Following his mothers wishes
that he should become an engineer, at the age of 14
The arrangement and nomenclature of chaetae he enrolled in the School of Mining Engineering
(setae). This is used to create a setal map. in Oro Pieto, Minas Gerais. However, at the age of
16 he was afflicted with beri-beri and spent some
time with his uncle Carlos Ribeiro de Castro,
Chaff Scale, Oulema melanopus an M.D. who had just established a new hospital.
(Linnaeus) (Coleoptera: Brazil at this time was struggling to develop
Chrysomelidae because it had so many endemic diseases. For
example, many European ships refused to dock in
This is an occasional pest of citrus trees. Brazil for fear of their crews contracting yellow
Citrus Pests and their Management fever, bubonic plague, smallpox and other diseases.
Chagas uncle convinced him that through the
Chafers practice of medicine he could perform important
national service. Influenced by his uncle, in 1897
Members of the subfamily Melolonthinae, family Chagas abandoned the plan to become an engi-
Scarabaeidae (order Coleoptera). neer and entered the Faculty of Medicine of Rio de
Beetles Janeiro where he received his M.D. in 1903.
Chagas had opportunity early in his career to
conduct research, but was attracted by clinical
practice in a hospital in Jurujuba. Following finan-
Chagas, Carlos Justiniano Ribeiro cial problems, in 1905 Chagas accepted a position
with a company in the interior of the state of So
Carlos Chagas was a Brazilian physician who Paulo, where malaria was a serious problem for
discovered Chagas disease (Chagas disease), or workers. Studying the transmission cycle closely,
820
C Chagas, Carlos Justiniano Ribeiro

he realized that workers were being bitten while and signs that are not unique to Chagas disease.
sleeping. Up to this time, the only known effective The symptoms noted by the infected individual
preventative approach for malaria control was may include fever, fatigue, aches of the head or
destruction of larvae in breeding areas (swamps). body, rash, loss of appetite, diarrhea, and vomiting.
As this was not effective, he began to use the insec- The signs of infection include mild enlargement of
ticide pyrethrum to disinfect houses. This approach the liver or spleen, swollen glands, and local swell-
proved to be very successful. ing (a chagoma). The most easily recognized indi-
Chagas moved to the Oswaldo Cruz Institute cation of acute Chagas disease is called Romaas
in 1906, which became his base of operations for sign, which includes swelling of the eyelids on the
the remainder of his career. In 1909, Cruz asked side of the face near the bite wound or where the
Chagas to undertake an antimalaria campaign in bug feces were deposited or accidentally rubbed
Lassance, Brazil, where railroad construction was into the eye. Symptoms, if present, usually fade
stalled because so many workers had succumbed away after a few weeks or months. However, if
to malaria. There he remained for 2 years, living untreated, the disease persists. Occasionally young
and working in a railroad car. He soon noticed children die from severe inflammation of the heart
disease symptoms that were not consistent with muscle or brain. The acute phase is more severe in
malaria, and later some locals pointed out to him a immuno-compromised people. The chronic phase
blood-sucking bug called vinchuca that com- of infection may result in no signs of infection for
monly were found in the huts of workers. This decades or even for life. However, some people
blood-sucking insect, an assassin bug or kissing develop heart problems including an enlarged
bug (Hemiptera: Reduviidae), was later deter- heart, heart failure, altered heart rate or rhythm,
mined to be in the genus Triatoma, several species and cardiac arrest. Also, intestinal problems can
of which transmit a disease later named Chagas occur, including an enlarged esophagus or colon,
disease. Chagas dissected the Triatoma bugs and which can lead to difficulties with eating or
found within them a trypanosome (Protozoa). defecation.
Allowing the bugs to feed on marmoset monkeys, Chagas was widely recognized for his note-
he found that the trypanosome could be transmit- worthy achievements. He was elected to the
ted. He identified the trypanosome and named it National Academy of Medicine in 1910, and in
Schizotrypaum cruzi after his mentor and friend 1912 he received the Schaudinn Prize for out-
Oswaldo Cruz. Later it became known as Trypano- standing work in protozoology and tropical
soma cruzi. Suspecting that these bugs could be medicine. He was twice nominated for the Nobel
transmitting the trypanosome to people due to Prize, but never received the award. In 1922,
their great abundance in rural homes, and their Chagas was recognized with the Great Prize of
blood-feeding habits, Chagas soon found tryano- the Pasteur Centenary Commemorative Expo-
somes in the blood of a young girl. He also con- sition in Strasbourg. He was awarded honorary
ducted autopsies of workers dying with acute and doctorate degrees from Harvard University and
chronic forms of the disease, and found brain and the University of Paris.
myocardium abnormalities accounting for the Chagas took over direction of the Institute in
involvement of these organs in the new disease. 1917 following the death of Oswaldo Cruz, and
He conducted surveys of animals in the area, remained in this position until 1934. During this
and determined that armadillos were the likely period the Brazilian government asked him to
reservoir of the trypanosomes. organize a campaign against Spanish influenza,
The acute phase of Chagas disease occurs in which was devastating Rio de Janeiro, and also to
the first few weeks or months of infection. Often it reorganize the Department of Health in Brazil (he
is symptom-free or exhibits only mild symptoms also served as director from 19201924). There he
 Chagas Disease: Biochemistry of the Vector
C 821

introduced many innovations and created centers

of preventative medicine. He died in Rio de Janeiro
from a heart attack on November 8, 1934.
Chagas Disease or American Trypanosomiasis
Trypanosomes

References

Lewinsohn R (1979) Carlos Chagas (18791934): the discov-

ery of Trypanosoma cruzi and of American trypanoso-
miasis (foot-notes to the history of Chagass disease).
Trans R Soc Trop Med Hyg 73:513523
Lewinsohn R (2003) Prophet in his own country: Carlos Cha-
gas and the Nobel Prize. Perspect Biol Med 46:532549

Chagas Disease: Biochemistry of

the Vector

M. Patricia Jurez
National University of La Plata, La Plata,
Argentina
Chagas Disease: Biochemistry of the Vector,
Chagas disease is caused by the parasitic proto-
Figure 39 Triatoma infestans, a major vector of
zoan Trypanosoma cruzi, which is transmitted by
Chagas disease in South America.
blood-feeding insects in the subfamily Triatomi-
nae (Hemiptera: Reduviidae), with 130 species
forming five tribes, among them only the tribes Feeding
Triatomini and Rhodniini possess relevant vector
capacity. Triatoma infestans (Klug) (Fig. 39) and Insect blood feeding impacts directly on human
Rhodnius prolixus (Stl) are representative examples and animal health. When a blood meal is taken,
of each tribe, and the most thoroughly studied, the pathogen T. cruzi might be transmitted via
as they are the major ones responsible for Chagas excreta deposited on the host skin. Rhodnius pro-
disease transmission. Triatomins are called kissing lixus is capable of ingesting 300 mg of blood in 15
bugs or assassin bugs; local names are vinchuca, min. Such highly efficient blood intake is made
chinche or picudo. Trypanosoma cruzi infects some possible by a special mouthpart developed to avoid
1618 million people, with another 90 million at blood coagulation and platelet aggregation. Purifi-
risk in regions of South and Central America. cation, cloning, expression, and mechanism of
There is neither a vaccine against it, nor a safe action of a novel platelet aggregation inhibitor
and effective drug to cure it. Fundamental research from the salivary gland of R. prolixus was recently
in insect physiology was pioneered by V.B. Wig- reported. Serotonin and other major biogenic
glesworth using R. prolixus. Most biochemical amines in insects, dopamine and octopamine, have
studies in Triatominae are focused on blood intake, been reported to modulate a variety of physiologi-
digestion, fat body and integumental lipid metab- cal and behavioral functions, including the control
olism and transport, and molting. of feeding behavior in insects. Feeding was found
822
C Chagas Disease: Biochemistry of the Vector

to be a natural stimulus for the release of serotonin Blood meals trigger the onset of diuresis after
into the hemolymph of R. prolixus, and serotonin the diuretic hormone is released by the neurose-
depletion led to a reduced blood meal size in this cretory cells of the mesothoracic ganglionic mass.
insect. Triatomins produce bioactive molecules in Insects then undergo a rapid elimination of urine
their salivary glands that are inoculated into host during which time the insect may lose 40% of the
skin via saliva during feeding. Four closely related weight of the meal. Multiple diuretic peptide fac-
proteins found in Rhodnius saliva behave as immu- tors have been suggested, and the serotonin role is
nomodulators, countering their hosts haemostatic, well described. Uric acid is the most important
inflammatory and immune responses to facilitate nitrogenous waste material excreted by triatomins.
blood feeding, exhibiting vasodilator, anticoagu- It is formed through the uricotelic pathway by
lant and antiplatelet aggregation activity. Because de novo synthesis from protein.
they bind nitric oxide, and act as a storage and
delivery system for it, they are named nitrophorins.
As a consequence of hematophagia, triatomins Reproduction
feed on a protein- and lipid- rich diet, with fatty
acids as the major source for energy production. Egg production is under hormonal and nutritional
This results in a much larger yield in the amounts control; a blood meal is required to start vitellogen-
of ATP produced, as compared to that of insects esis, and juvenile hormone (JH) secretion by the
consuming carbohydrate. The fat body is the major corpora allata (CA) regulates oocyte development.
metabolic factory, as well as the main storage depot The amount of blood required for oviposition varies
of fat, glycogen and protein. Its metabolites are from 5 to 8 mg/egg for R. prolixus to 1625 mg/egg
transported to target organs via hemolymph. for T. infestans. Vitellogenins (VG) are high molecu-
lar weight lipoproteins synthesized in the fat body of
adult females. They enter the oocytes by pinocytosis
Protein Metabolism to be converted into vitellins (VN). A molecular
weight around 4 105 was estimated for different
Many of the proteins that are crucial in the life of species, after characterization by immunodiffusion
insects are biosynthesized in the fat body. Protein (ID), immunoelectrophoresis (IEP), and electropho-
synthesis is often under control of juvenile hor- resis in polyacrylamide gel (PAGE). Vitellogenin
mone (JH). synthesis also has been detected in R. prolixus
Complete hydrolysis of blood-meal proteins ovaries.
is mediated by exo- and endo-peptidases. Endo-
proteinases cleave proteins to smaller segments
that are finally completely degraded to amino Lipid Composition, Metabolism,
acids by exopeptidases. Triatominae midgut also and Transport
contains endopeptidases B and D, involved in
hemoglobin hydrolysis. Salivary glands have acid A high lipid content (78%) is characteristic of
phosphatase activity with anticoagulant proper- eggs, and remains high through the first instar in
ties to destroy hemoglobin; large amounts of T. infestans. It is close to 1.5% throughout the
sialidase activity are also detected after a blood whole nymphal cycle to adult stage. Major insect
meal, rich in sialic acids. Hemoglobin digestion and egg lipids are triacylglycerols (85%) with
and detoxification of the free haem by its energy storage function; phospholipids (48%),
sequestration into an insoluble pigment known as mainly phosphatidylethanolamine and phospha-
haemozoin (Hz) were recently detected in the ditylcholine, are involved in cell membrane for-
midgut of R. prolixus. mation and metabolic events; and the major sterol
 Chagas Disease: Biochemistry of the Vector
C 823

component is cholesterol, sequestrated from after subcellular fractionation. De novo fatty acid
host blood and stored as cholesterol esters or assays employed radioactive precursors such as
free (58%), which contributes to lipid bilayer [14C]acetate or [14C]propionate by injection into
fluidity regulation. Small amounts of saturated the hemolymph for in vivo or tissue slice assays;
hydrocarbons (straight and multiple methyl- [14C]acetyl-CoA or [14C]malonyl-CoA were used
branched chains of 27 to >41 carbons), primary in cell-free assays. Whole insect, fat body or integ-
fatty alcohols (straight chains of 2434 carbons) and umental tissue mostly metabolize [14C]acetate into
wax esters (4448 carbons) confer water-proofing triacylglycerols (ca. 80%) and phospholipids
properties to the cuticular surface, also preventing (>10%). The major fatty acids formed are 16:0,
chemicals and microorganism penetration. 18:1, 18:0 and 16:1, produced by a cytosolic fatty
The major whole-body insect fatty acid com- acid synthetase (FAS) and a 9 desaturase.
ponents are oleic (18:1) and palmitic (16:0), with Metabolites are incorporated into hemolymph
minor amounts of linoleic (18:2), stearic (18:0), lipoproteins (Lp) that serve multiple functions in
palmitoleic (16:1) and arachidonic (20:4) acids. insect development and reproduction. They trans-
Minor components play specific functions; for port nutrients from the site of absorption or the site
example, volatile fatty acids of short chains (VFA) of synthesis to the site of utilization and storage in
formed in the Brindley glands, are released upon target tissues. Other than vitellogenin, three lipo-
disturbance and serve as defensive secretion, proteins have been identified in triatomins, a high
with isobutyric acid accounting for most of their density lipoprotein (HDL) also named lipophorin,
characteristic stink odor. and two very high density lipoproteins, VHDL-1
Very long chain fatty acids (VLCFA), up to 34 and VHDL-2. Their apo-proteins are polypeptides
total carbons, are also present in the triatomin from 17 to 210 kdaltons (kDa), with a 86 kDa com-
integument, and are detectable precursors to mon component. Lipid transport is mediated by
hydrocarbon and fatty alcohol formation. Specific lipophorin, an ubiquitous lipoprotein, that is widely
fatty acids precursors to cuticular waxes formation distributed among insects. It functions as a reusable
are detected in minute amounts in the integument: shuttle for neutral and polar lipid transport in Tri-
methyl-branched fatty acids of 16 and 18 carbons atominae. HDL from the hemolymph of T. infestans
in the straight carbon chain are intermediates in has an apparent molecular weight of 670 kDa, with
methyl-branched hydrocarbon synthesis. an isoelectric point of 7.0 and a density () of 1.10
Dietary lipids are the only source of 18:2 and g/ml. It contains 53% protein and 47% lipid. The
20:4 acids in Triatominae, which lack both 5 protein moiety consists of two apoproteins: apoLp-I
and 6 desaturating enzymes. These polyunsaturated (255 kDa) and apoLp-II (7080 kDa), rich in the
components contribute to membrane fluidity and amino acids aspartic acid, glutamic acid, and
they are precursors to the eicosanoids prostaglan- leucine. Diacylglycerols constitute 41% of the total
dins, molecules of significance in reproduction. lipids, and satisfy the major energy requirement in
Large amounts of 20:4 acids are stored in male tes- insects. HDL is also the vehicle for transport of
tes. They are metabolized into prostaglandins (PG) phospholipids, hydrocarbons, and cholesterol. It
and transferred to females via spermatophores also behaves as a free fatty acid donor to VHDL, a
during copulation. Eicosanids also participate in hexameric storage protein ( = 1.27 g/ml) with a
the immune response, i.e., to help clear bacteria putative role related to amino acid and free fatty
from contaminated hemolymph, and to regulate acid supply involved in molting, metamorphosis
fluid balance. and reproduction events. Lipophorin binding sites
Fatty acid biosynthesis was extensively studied located on the surface of the oocyte, mainly at the
in the whole insect, the fat body, the integument microvilli, mediate phospholipid transfer from the
and reproductive organs, both in tissue slices and hemolymph to the oocytes.
824
C Chagas Disease or American Trypanosomiasis

The Integument References

The bulk of triatomins cuticular proteins are soluble Brenner RR (1987) Chagas disease vectors. Lipid composition
in urea 7 M, with eight major bands separated by and metabolism. In: Brenner RR, Stoka AM (eds)
Chagas disease vectors. Biochemical aspects and con-
electrophoresis. They contain large amounts of trol, vol 3. CRC Press, Boca Raton, FL, USA, pp 935
hydrophobic and polar uncharged amino acids. The Jurez MP (1994) Hydrocarbon biosynthesis in Triatoma
abdominal cuticle is extensible through the fifth infestans eggs. Arch Insect Biochem Physiol 25:193206
instar, and chitin accounts for <20% (w/w). When Champagne DE, Nussenzveig RH, Ribeiro JM (1995) Purifi-
cation, partial characterization, and cloning of nitric
Rhodnius takes a blood meal, a plasticizing factor is oxide-carrying heme proteins (nitrophorins) from sali-
secreted which lowers the pH of the cuticle, and this vary glands of the blood-sucking insect Rhodnius pro-
changes the degree of bonding between cuticular lixus. J Biol Chem 270:86918695
Rimoldi OJ, Crsico B, Gonzalez MS, Brenner RR (1996)
proteins. Therefore, the cuticle becomes more flexi-
Detection and quantification of a very high density
ble and the abdomen is dramatically expanded up lipoprotein in different tissues of Triatoma infestans
to nearly four times, with the cuticle becoming very during the last nymphal and adult stages. Insect Bio-
thin. Chitin synthesis is started by depletion of gly- chem Mol Biol 26:705713
Wigglesworth VB (1933) The physiology of the cuticle
cogen and trehalose from storage sites for conver- and of ecdysis in Rhodnius prolixus. Q J Microsc Sci
sion to UDP-N-acetylglucosamine units, which are 76:269318
further polymerized to chitin, an aminopolysaccha-
ride. Chitin synthesis occurs mostly in the fat body;
its formation is under ecdysteroid regulation. Chi-
tin is not responsible for the hardness of the integu- Chagas Disease or American
ment; instead this attribute is associated with tanned Trypanosomiasis
proteins, their degree of sclerotization and their
distribution among the polysaccharide matrix. John L. Capinera
Molting evokes major biochemical changes in University of Florida, Gainesville, FL, USA
the cuticle of Triatominae. In preparation for molt-
ing, chitinase and proteinase are secreted to digest Chagas (or Chagas) disease is named after its
the less sclerotized cuticle, but have no effect either discoverer, the Brazilian physician Carlos Chagas.
on exocuticle or on the surface lipids. The oeno- It is caused by the trypanosome (protozoan)
cytes, modified epidermal cells, are the site of parasite Trypanosoma cruzi. This pathogen is
integumental lipid synthesis. They transfer newly transmitted to animals and people by kissing bugs
formed hydrocarbons to hemolymph, which func- (Hemiptera: Reduviidae: Triatominae) (Table 10).
tions as a selective shuttle, storing methylbranched The disease occurs in the western hemisphere
chains while releasing to the site of deposition, the from Mexico to Argentina (Fig.40), primarily in
epicuticular surface, straight and methylbranched rural areas where poverty is widespread. It is
chains in a 1:1 ratio. Inhibition of cuticular lipid estimated that as many as 18 million people in
synthesis in T. infestans was shown to raise detri- Mexico, Central America, and South America
mental effects on hatch and insect development, have Chagas disease. Interestingly, most of these
water barrier properties, and to enhance chemical victims do not know they are infected because
and microbial insecticide penetration; complete the acute symptoms fade away. If the disease
degradation of T. infestans hydrocarbons by fungal remains unrecognized and untreated, however,
pathogens was recently shown. there can be serious consequences later in life
Assassin Bugs and the disease ultimately can be life threatening.
Area-Wide Pest Management About 50,000 people die each year from compli-
Chagas Disease or American Trypanosomiasis cations caused by Chagas disease.
 Chagas Disease or American Trypanosomiasis
C 825

Chagas Disease or American Trypanosomiasis, Table 10 The major vectors of Chagas disease and their
distribution
Species Geographic distribution
Panstrongylus herreri northern Peru
Panstrongylus megistus Brazil, Paraguay, Argentina, Uruguay
Rhodnius prolixus southern Mexico south to Colombia and Venezuela
Rhodnius pallescens Panama, Colombia
Triatoma infestans Peru, Bolivia, Brazil, Paraguay, Argentina, Uruguay, Chile
Triatoma dimidiata Mexico south to Ecuador and Peru
Triatoma pallidipennis Mexico
Triatoma phyllosoma Mexico
Triatoma maculata Colombia, Venezuela, Guyana, Suriname
Triatoma brasiliensis Brazil
Triatoma guasayana Bolivia, Paraguay, Argentina
Triatoma sordida Bolivia, Brazil, Paraguay, Uruguay, Argentina

The acute phase of Chagas disease occurs in

the first few weeks or months of infection. Often it
is symptom-free, or exhibits only mild symptoms
and signs that are not unique to Chagas disease.
The symptoms noted by the infected individual
may include fever, fatigue, aches of the head or
body, rash, loss of appetite, diarrhea, and vomiting.
The signs of infection include mild enlargement of
the liver or spleen, swollen glands, and local swell-
ing. The most easily recognized indication of acute
Chagas disease is called Romaas sign, which
includes swelling of the eyelids on the side of the
face near the bite wound or where the bug feces
were deposited or accidentally rubbed into the
eye. Symptoms, if present, usually fade away after a
few weeks or months. However, if untreated, the
disease persists. Occasionally young children die
from severe inflammation of the heart muscle or
brain. The acute phase is more severe in immuno-
compromised people. The chronic phase of infection
Chagas Disease or American Trypanosomiasis, may result in no signs of infection for decades or
Figure 40 The distribution of Chagas disease in even for life. However, some people develop heart
Latin America; shaded areas indicate problems including an enlarged heart, heart failure,
regions where Chagas disease is most likely altered heart rate or rhythm, and cardiac arrest.
to occur. Also, intestinal problems can occur, including an
826
C Chagas Disease or American Trypanosomiasis

enlarged esophagus or colon, which can lead to ominous reports of Trypanosoma cruzi occurring
difficulties with eating or defecation. A toxin is in wild animal (raccoon, opossum) populations as
responsible for the destruction of tissues. far north as North Carolina. The triatomine bugs
Although Chagas disease occurs primarily in indigenous to North America are capable of trans-
the rural areas in Latin America, the movement of mitting Chagas disease (Fig. 41). The failure of
large numbers of people from rural to urban areas Chagas to be a problem in the USA is attributed to
of Latin America, and to other regions of the the low incidence of infected bugs (6%) and verte-
world, has increased its geographic distribution. It brate hosts (15%), but also to the habit of the
is a growing threat in the United States and the northern species not to defecate immediately after
Caribbean region, where Chagas disease is not feeding, so even if humans are bitten the bugs are
endemic; it is estimated that about 500,000 less likely to defecate on humans in North America
unknowingly infected immigrants now live in than in Central and South America.
these more northern countries. In these areas, In Chagas-endemic areas, the principal route
where kissing bugs are not common or not likely of infection is by being bitten by triatomine bugs,
to bite humans, Chagas management should focus primarily Triatoma spp., and especially T. infestans.
on preventing transmission from blood transfu- The bugs contract the typanosomes by feeding on
sion, organ transplantation, and mother-to-baby infected animals or people. The bite of kissing
(congenital) transmission. Nevertheless, there are bugs typically produces little or no pain, so the

Triatomine bug stages Vertebrate host stages

Triatomine bug takes a blood meal
(passes metacyclic trypastigotes in feces, Metacyclic trypomastigotes
tryposmastigotes enter bite wound penetrate various cells at bite
or mucosal membranes, such as the conjunctiva) wound site. Inside cells they
transform into amastigotes.

Metacyclic trypomastigotes
in hindgut

Multiply in midgut
Amastigotes multiply
Trypomastigotes by binary fission in cells
can infect other cells of infected tissues.
and transform into
intracellular amastigotes
Triatomine bug takes in new infection sites.
Epimastigotes
a blood meal
in midgut
(trypomastigotes ingested)

Intracelluar amastigotes
transform into trypomastigotes,
then burst out of cells
and enter the bloodstream.

Chagas Disease or American Trypanosomiasis, Figure 41 The Chagas disease cycle in triatomine bugs
and animal hosts (adapted from CDC).
 Chagas Disease or American Trypanosomiasis
C 827

sleeping host is usually unaware of the blood- hollow trees, fallen logs, palm fronds and epi-
feeding episode. Once infected, the bugs pass phytes. Though kissing bugs feed on birds, and the
T. cruzi parasites in their feces. The bugs frequently bugs can be quite numerous in chicken houses on
aggregate in barns, sheds or houses if they are not farms, birds seem to be immune against infection
insect-proof. In rural areas, many houses are made and therefore are not considered to be a T. cruzi
from materials such as mud, adobe, straw, and reservoir. The different vectors of Chagas disease
palm thatch, and lack window screening and in have differing host preferences, so the disease
some cases, doors. Thus, there is nothing to pre- transmission cycle varies accordingly.
vent entry of the bugs. During the day, the bugs The generalized infection cycle is as follows:
hide in crevices in the walls and roofs. If the roof is The infected triatomine bug ingests blood and
straw or another material with cracks and crevices, defecates feces containing trypomastigotes near
the bugs can hide easily and are not readily the feeding site. The victim, irritated by the bite,
detected. Then, during the night, when the inhab- scratches the area, thereby rubbing the trypomas-
itants are sleeping, the bugs emerge to feed. (Bugs tigote-containing feces into the wound or into
may feed during the day if their hosts are noctur- intact but susceptible mucosal membranes, such as
nal, such as bats.) Because they tend to feed on the conjunctiva. Once inside the host, the trypo-
peoples faces, triatomine bugs have also come to mastigotes invade cells, where they differentiate
be known as kissing bugs. After they bite and into intracellular amastigotes. The amastigotes
ingest blood, they commonly defecate on the per- multiply by binary fission and differentiate into
son. The person becomes infected if T. cruzi para- trypomastigotes, which are released into the blood-
sites in the bug feces enter the victims body stream. Cells from a number of different tissues
through mucous membranes or breaks in the skin. are susceptible to infection by the trypomastigotes,
The unsuspecting, sleeping person may acciden- and once inside, they transform into intracellular
tally scratch or rub the feces into the bite wound, amastigotes at new infection sites. Intracellular
eyes, or mouth, facilitating entry of the trypano- amastigotes destroy tissues such as the intramural
somes. This is the principal form of T. cruzi entry neurons of the autonomic nervous system in the
into humans, but disease transmission also occurs intestine and heart, leading to digestive and heart
through consumption of uncooked food contami- problems, respectively. Replication resumes only
nated with feces from infected bugs, congenital when the parasites enter another cell or are ingested
transmission (from a pregnant woman to her by another vector. The final step in the cycle is
baby), blood transfusion, organ transplantation, infection of the vector, which occurs when the
and (rarely) accidental laboratory exposure. Ani- bug feeds on an infected host containing trypo-
mals can contract the disease by consuming mastigotes. Once ingested by the bug, the ingested
infected prey, as in consumption of mice by house- trypomastigotes multiply and differentiate (amas-
hold cats. tigote and epimastigote forms) in the midgut and
The natural reservoirs of Trypanosoma cruzi transform into infective metacyclic trypomastig-
are wild animals such as monkeys, opossums, otes in the hindgut. The feces may contain thou-
amphibians, lizards, armadillos, sloths, bats, por- sands of metacyclic tryptomastigotes.
cupines and ground squirrels. These natural hosts Management of bugs to disrupt disease
do not develop pathologies. However, T. cruzi is transmission is possible. In many areas of Latin
also harbored in infected humans, and domestic America, the interiors of houses are treated with
animals like cats, dogs, rabbits, and guinea pigs. pyrethroid insecticides to eliminate kissing
Canine trypanosomiasis is of veterinary impor- (Triatoma) bugs. At least two South American
tance in Latin America. In nature, kissing bugs are countries have rid themselves of the problem in
found in hiding places such as caves, tree holes, this manner. However, complete control is difficult
828
C Chalaza (pl., chalazae)

to accomplish, and houses are often reinfested Treatment in either the acute or chronic phase
because some bugs escape the insecticide within does not guarantee a cure. A vaccine was devel-
the homes by hiding, or because the homes are oped in the 1970s and it proved fairly successful,
reinvaded from nearby, untreated areas. Animal but implementation is constrained by the high
shelters are often good harborages for Triatoma, cost of production.
and if they are not adequately treated and are near The effect of Chagas disease is measured less
homes, the bugs quickly disperse to the treated by mortality and more by morbidity. Chronically
home. A distance of at least 1,500 m is considered infected people often suffer decades of weakness
necessary as a buffer zone between untreated and and fatigue that effectively removes them from the
treated harborages. An economic and effective workplace and prevents them from enjoying a
alternative to chemical control is bed nets, though normal life. This results in considerable social
the edges of the net must be tucked beneath the disruption and economic loss. A survey of the
mattress to assure that bugs cannot enter. Also, the incidence of Chagas disease found that about 12%
net and mattress must be large enough that the of the residents of Chile and Paraguay were infected,
human sleeping beneath the net does not come and in Argentina and Bolivia the rate was 8%.
into contact with the bed netting, because there is Assassin Bugs, Kissing Bugs and Others
risk that bugs will feed through the netting if the (Hemiptera: Reduviidae)
human is immediately adjacent. The logistics and Chagas
cost of meeting these requirements often prove Chagas Disease: Biochemistry of the Vector
daunting to poor people, so insecticide treatment Trypanosomes
is more practical. Likewise, improved housing and Area-Wide Pest Management
sanitation would virtually eliminate this problem,
but achieving this is presently not possible due to
the cost. References
Detection of infection is often done by exam-
ining the patients blood to look for trypanosomes Beard CB, Gordon-Rosales C, Durvasula RV (2002) Bacterial
or T. cruzi-specific antibodies. However, a proce- symbionts of the Triatominae and their potential use in
control of Chagas disease transmission. Ann Rev Ento-
dure called xenodiagnosis is sometimes used, mol 47:123141
wherein laboratory-reared bugs free of trypano- Brenner RR, Stoka AM (eds) Chagas disease vectors, vols 13.
somes are fed on patients, incubated, and then CRC Press, Boca Raton, FL
examined for presence of trypanosomes in the Dias JCP, Schofield CJ (1999) The evolution of Chagas disease
(American Trypanosomiasis) control after 90 years
alimentary tract. Xenodiagnosis is very sensitive since Carl Chagas discovery. Memorias do Instituto
because the trypanosomes, even if few in number Oswaldo Cruz 94:103121
in the human host, build up to large numbers in Kirchhoff LV (1993) American trypanosomiasis (Chagas
disease) a tropical disease now in the United States.
the bug and are easily detected.
NEngl J Med 329:639644
Treatment of infected people is difficult Zeledn R, Rabinovich JE (1981) Chagas disease: an ecologi-
because medication is usually effective only if cal appraisal with special emphasis on its insect vectors.
administered during the acute phase, and many Ann Rev Entomol 26:101133
victims are unaware of their condition. This issue
is compounded by the resistance of the trypano-
some to medication is some regions, and by the Chalaza (pl., chalazae)
toxicity and side effects of the drugs. During the
chronic phase of infection, treatment consists A pimple-like protuberance of the body wall bear-
mostly of treating the symptoms, and both heart ing a seta. Chalazae are commonly found on
replacement and intestinal surgery are practiced. larvae.
 Chaudoir, Maximilien Stanislavovitch De
C 829

Chalcididae Chamaemyiidae

A family of wasps (order Hymenoptera). A family of flies (order Diptera). They commonly
Wasps, Ants, Bees and Sawflies are known as aphid flies.
Flies
Chalkbrood
A fungus disease of honey bee larvae caused by Chaoboridae
Ascosphaera apis. The disease causes the larvae to
become mummified, and usually to take on chalky A family of flies (order Diptera). They commonly
white appearance, but sometimes gray or black. are known as phantom midges.
Early in the infection process the larvae are cov- Flies
ered with a fluffy white growth of mycelia, but later Aphids
they shrink and acquire the chalky appearance.
Though not usually considered serious, occasion-
ally it can be damaging. It occurs widely, though Charipidae
often going unnoticed. Young bees are susceptible
to infection, and normally are infected after being A family of wasps (order Hymenoptera).
fed spores and then exposed to cool weather. Wasps, Ants, Bees and Sawflies
Because the chilling is necessary, it is usually the
cells at the periphery of the hive that are infected.
Bees usually acquire the disease by ingestion Chaudoir, Maximilien
of honey or pollen, and the spores successfully Stanislavovitch De
overwinter and remain infective for many years.
Poor ventilation and excessive precipitation and Maximilien de Chaudoir was born on September
humidity are associated with greater expression of 12, 1816, at Ivnitza, a village in the Ukraine. He
this disease. Poor nutrition is also a factor, as is inherited the title of Baron which had been con-
colony weakening due to other diseases, mites, and ferred on his grandfather by King Maximilien
poor beekeeping practices. The pathogen can also Joseph of Bavaria, and had later been made hered-
be acquired from native bees. itary by Czar Nicholas I of Russia. His private
Management is usually accomplished by tutor was Jean Wavre, who interested him in natu-
reversing the conditions that bring about expres- ral history. In 1831 he was sent to study law to
sion of the disease: improved ventilation, better Dorpat (Tartu), but there spent most of his time
nutrition, keeping the hives closed during winter, working on the insect collections assembled by
and better sanitation. Destruction of infected hives J.F. Eschholtz. In 1834 he was made a member of
is helpful. Antibiotics are not usually suggested. the Socit Entomologique de France, and the fol-
Ascosphaera API lowing year (at the age of 18) presented his first
Honey Bees entomological paper at one of its meetings. After
Apiculture his return to the Ukraine, his entomological col-
lection, especially of Carabidae, grew by purchase
from collectors and dealers and from his own col-
Reference
lecting expeditions in the Ukraine and other Rus-
sian territories in the Caucasus. He published
Morse RA, Nowogrodzki R (1990) Honey bee pests, predators
and diseases, 2nd edn. Cornell University Press, Ithaca, frequently in the Bulletin de la Socit Imperiale
NY, 474 pp des Naturalistes de Moscou. In 1863 he moved to
830
C Champion, George Charles

France, later transporting his worldwide collec- zoology in 1951 at Queen Mary College of
tion of Carabidae there and working on it until London University, United Kingdom. Then,
his death on May 6, 1881. His publications include with a scholarship from the Anti-Locust Research
108 works on Carabidae including major taxo- Centre he studied factors governing roosting
nomic revisions, and are written mainly in French, behavior in locusts, first in the laboratory in
although he knew Russian, German, English, and London and later in Africa. Chapman lived and
Italian. His collection was acquired in 1952 by the worked in a locust outbreak area in one of the
Musum National d Histoire Naturelle of Paris. smaller valleys of the East African rift system
from 1953 to 1957. There was no town, electric-
ity, phone or radio. He was one of the first to
References
make quantitative observations on insect behav-
ior in the field, and one of few combining field
Ball GE, Erwin TL (1982) The Baron Maximilien de Chau-
doir: inheritance, associates, travels, work, and legacy. and lab work (he built his own house and lab).
Coleopt Bull 36:475501 He soon learned that the locusts did not sun-
Basilewsky P (1982) Baron Maximilien de Chaudoir (18161881) down, and if he really wanted to understand
[including a bibliography]. Coleopt Bull 36:462474
what was governing their behavior he needed to
work as they demanded a lesson he passed on
Champion, George Charles to many. In this remote place Reg Chapman
made his first contributions to behavior of
George Champion was born in London on April locusts and grasshoppers (and lizards), includ-
29, 1859. He became interested in beetles early in ing relationships between hemolymph potas-
his life, and was employed in his late twenties by sium levels and feeding activity. He was strongly
Frederick Godman and Osbert Salvin to collect influenced by three extremely rigorous scien-
beetles for the Biologia Centrali-Americana proj- tists who guided his PhD Boris Uvarov, Donald
ect in Central America. Later, he wrote for the Gunn, and John Kennedy.
project and assisted in editing its publications. His At the University of Ghana he studied host-
taxonomic work on beetles then continued, and he finding by tsetse flies for 2 years. In 1959, Reg
wrote many publications on specimens collected was appointed to a faculty position at Birkbeck
by his son H.G.C. Champion in India, eventually College (another college of the University of
publishing more than 420 papers. He died in Wok- London). His main responsibility was to teach
ing, England, on August 8, 1927. invertebrate zoology and advanced entomology.
Subsequently, he developed a masters course
which he taught single-handed, and this led to
Reference
what he is best known for The Insects Struc-
ture and Function. First published in 1969, this
Herman LH (2001) Champion, George Charles. Bull Am Mus
Nat Hist 265:5455 book with its various revisions and finally a total
rewrite (1998) has been a major resource for stu-
dents, teachers, and researchers round the
Chapman, Reginald Frederick world.
At Birkbeck, Chapman extended his inter-
Elizabeth A. Bernays ests in insect feeding to include the sensory sys-
University of Arizona, Tucson, AZ, USA tem, with locusts and grasshoppers as models
with a small, but quite productive, research group
Reg Chapman was born at London, England on including Liz Bernays who was to become his
July 2, 1930. He obtained a bachelors degree in wife. One finding, that insects can differentiate
 Chelating Agent
C 831

between plants on the basis of the surface wax on area of feeding behavior and physiology, are a
the leaves, was quite novel at the time, and his major contribution, but much of the work he did
interest in the plant surface continued. He initi- is under the authorship of others he always
ated work on chemoreceptor physiology with wanted his students and coworkers to get the
another student, Wally Blaney, and on the signifi- credit. Similarly, he was a major influence on
cance of receptor numbers among other things. hundreds of graduate students; he loved to help
He was successively, lecturer, University Reader them, and constructively criticize all who came
and University Professor in the University of to him, not just the 37 he formally guided. His
London. breadth of knowledge and his ability to quickly
In 1970, Chapman became Director of the see to the heart of a problem was legendary. He
Research Division at the Anti-Locust Research cared deeply about getting it right and doing it
Centre and as well as continuing research, directed properly. He will be remembered as one of the
studies on other topics such as insect flight, plant most modest, yet broadly knowledgeable and
chemistry and insects and crop plant resistance. critical entomologists, and a great classroom
As the Centre increased its coverage of insect teacher. Reg Chapman died at Tucson, Arizona
pests in developing countries, he developed and on May 2, 2003.
was responsible for, a wide range of research pro-
grams in many parts of the world groups in the
Philippines working on brown planthopper of
rice, in India on varietal resistance of sorghum to
Checkered Beetles
pests, in Botswana on sorghum pests, in Nigeria
Members of the family Cleridae (order
on a pest grasshopper, the impact of soil termites
Coleoptera).
on grasslands, and the impact of pesticide use on
Beetles
non-target organisms, and in Mali a radar group
studying grasshopper migration. He spent a week
at a time with each, examining data and discuss-
ing the next steps. As well as revising The Insects Cheek
at that time, he wrote a small book on locust
biology. The lateral part of the head between the compound
When Liz Bernays was offered a position in eye and the mouth.
Berkeley in 1983, Reg Chapman, in his usual way
of putting others first, went with her to an unsala-
ried situation. However, in 1987, the University of
Arizona made irresistible offers to both, and Chap-
Chela
man was a professor of insect neurobiology until
The terminal portion of a limb that bears a claw-
his retirement in 2001. In Arizona, his work on
like structure. This term is sometimes used to
taste physiology was productive, with the help of
describe the forelegs of mantids, which effectively
several postdocs and students.
grasp prey.
Besides The Insects, and A Biology of Locusts,
Reg wrote Host-plant Selection by Phytophagous
Insects with Liz, edited four books, and wrote 20
critical reviews, ten book chapters, 110 research Chelating Agent
papers, and twenty entries for encyclopedias
and other popular books. Regs research A molecule capable of binding metal atoms; one
accomplishments and reviews, especially in the example is EDTA, which binds Mg++.
832
C Chelicera (pl. chelicerae)

Chelicera (pl. chelicerae) Chemical ecology as a recognized scientific

discipline came into being in the early 1970s. At
The pincer-like first pair of mouthpart appendages this time there was increasing interest in non-
in arachnids. pesticidal methods of insect control because of the
growing awareness of environmental problems
caused by persistent, toxic pesticides. Simultane-
Chelisochidae ous rapid advances in the instrumentation required
to analyze minute amounts of chemicals found in
A family of earwigs (order Dermaptera). They nature (i.e., gas chromatographs, mass spectrometers
sometimes are called black earwigs. and nuclear magnetic resonance spectroscopes)
Earwigs spurred the development of chemical ecology.
Over the last 30 years, the breadth of insect
chemical ecology has increased from the study
Chelonariidae of insects interacting within one trophic level to
two-trophic level interactions involving insects
A family of beetles (order Coleoptera). They and their food organisms to multitrophic-level
commonly are known as turtle beetles. interactions. Chemical ecologists work on prob-
Beetles lems ranging from applied to basic in nature. For
many chemical ecologists, the primary goal of
their research is to find ways to reduce insect
Cheloniform Larva populations to acceptable levels without using
broad-spectrum insecticides by changing the
A larva that is oval or circular, strongly flattened, insects behavior so that they inflict less harm on
and with a concealed head; resembling a turtle. our food, our livestock and us. Other chemical
ecologists study the chemical ecology of insects to
understand better the more basic aspects of their
Chemical Ecology of Insects species of interest; who is related to whom, why
they eat a particular food plant and not others,
Heather J. McAuslane how they defend themselves, etc
University of Florida, Gainesville, FL, USA The chemicals that mediate interactions bet-
ween organisms in nature are termed semiochem-
Ecology is the study of the effects on organisms of icals. This comes from the Greek word semeon
their biotic (i.e., living) and abiotic (i.e., nonliving) which means a mark or a signal. The semiochemi-
environments. Chemical ecology is simply the cals that mediate interactions between organisms
study of the effects on organisms of chemicals of the same species (intraspecific interactions)
produced by living organisms in their environment are pheromones whereas semiochemicals that
(i.e., their biotic environment). Thus, chemical mediate interactions occurring between different
ecology is a sub-discipline of ecology, emphasizing species (interspecific interactions) are allelochemicals.
interactions within and among species that are Pheromones were the first semiochemicals
mediated by chemicals. The behavior and/or that received intense scientific study and to date,
physiology of all major groups of organisms exam- well over 500 have been identified, most of these
ined to date, from bacteria to plants to insects to being sex attractant pheromones of Lepidoptera.
humans, are to some extent influenced by chemi- Insects use pheromones to communicate with
cals produced and released into the environment members of their species to facilitate reproduction
by other organisms. (sex pheromones), locate food sources (trail
 Chemical Ecology of Insects
C 833

pheromones), warn of danger (alarm pheromones) Allomones in the cabbage plant family (the
and maintain the function and cohesion of large Brassicaceae) are the reason that relatively few
colonies (many pheromones of social insects). We insects feed on these plants. Most members of this
can use pheromones to disrupt communication plant family produce sulfur-containing com-
among members of a pest species so that they do pounds called glucosinolates that deter feeding of
less damage to our crops and animals. We can also herbivores. These chemicals give mustard, collard
use pheromones to detect the presence of insect and turnip greens their distinct taste (which many
pests, monitor their changes in population size, humans consider an acquired taste). Volatile
and time applications of insecticides or other con- breakdown products of the glucosinolates, the
trol measures. isothiocyanates and other compounds, which
Interspecific interactions, involving insects repel most insects, give the condiment mustard its
and other insects, plants or other organisms, are pungent aroma. Plants in the squash, pumpkin
mediated by allelochemicals. These chemicals are and melon family (the Cucurbitaceae) are well
significant to organisms of a species different from defended with exceedingly bitter large steroid-
their source, for reasons other than food. Three type molecules called cucurbitacins. Most insects
types of allelochemicals are recognized: allomones, will not feed on wild species of the Cucurbitaceae
kairomones, and synomones. The designation of a because of the bitter cucurbitacins. However, when
particular chemical depends on which species in humans began domesticating these crops for
the interaction benefits and which, if any, is harmed human consumption, they selectively bred out the
after perceiving the chemical. For example, an all- bitter taste and reduced the levels of the allomones
omone is a chemical that is produced or acquired that the plants use to defend themselves. Thus,
by one organism that causes a behavioral or physi- cucurbit species grown for human consumption
ological response in the receiver of another spe- are non-bitter and are readily attacked by many
cies that is beneficial to the emitter but not to the pest insects.
receiver. The organism, either plant or insect, Chemical ecologists can apply their knowl-
releasing the allomone is benefited by preventing a edge of plant-produced allomones for pest man-
potential predator from eating it. The receiver of agement by developing them as biopesticides or
the allomone is harmed because it is denied what by increasing their levels in non-edible portions of
would otherwise be a suitable meal. a crop with the help of plant breeders. Azadirachtin
Many plants produce allomones that repel from the Indian neem tree Azadirachta indica, oils
herbivorous insects and protect their tissues from of various herbs such as mint, rosemary, and
herbivore damage. Ecologists, such as Gottfried thyme, pyrethrum from chrysanthemums, and
Fraenkel, Paul Erhlich and Peter Raven, in the 1950s rotenone from the roots of the legume Derris,
and 1960s suggested that the huge diversity of insect- among others, have all been developed as botanical
repellent and deterrent chemicals found within insecticides or plant protectants because of their
angiosperm plants might actually have evolved in toxic or repellent effects on insects.
response to the selection pressure of feeding by Many insect species produce allomones, often
herbivorous insects. Today, most ecologists believe surprisingly similar in structure to those of plants,
that these secondary plant compounds, so named which repel or deter predators that may try to eat
because they did not appear to have a function in them. For example, Heliconius butterflies and
the primary metabolism of plants as nutrients or Zygaena moths release the cyanogenic glycosides,
structural compounds, probably arose as defenses linamarin and lotaustralin, which break down to
against plant pathogens and to help in plant-plant release hydrogen cyanide, when predators threaten
competition rather than as defenses against insects; them. Coincidently, clover and birdsfoot trefoil
however, their effects on insects are undisputed. also rely on the same cyanogenic glycosides to
834
C Chemical Ecology of Insects

deter herbivores and grazers. The venoms of wasps, that then parasitize the insect herbivore, thus
bees and ants are allomones that are highly deter- reducing the damage to the plant. The receiving
rent to predators, including the human variety. organism, the parasitoid, benefits by being pro-
The list of allomones synthesized or acquired by vided an additional source of cues with which
insects to defend themselves is lengthy and is to help it locate a potential host. For example,
reviewed elsewhere. the braconid parasitoid, Cardiochiles nigriceps, is
A second group of allelochemicals is the kai- attracted to tobacco, cotton and corn plants that
romones. A kairomone is a semiochemical that is have been damaged by larvae of its host, the tobacco
produced or acquired by an organism that causes a budworm Heliothis virescens (Noctuidae), by vola-
behavioral or physiological response in the receiver tile chemicals that are released by the damaged
of a different species that is beneficial to the receiver plants. Interestingly, the synomonal blend released
but not to the emitter. We know that many species by the plant is specific to the herbivorous insect
of predators and parasitoids are attracted to their that is feeding on it; the parasitoid ignores plants
hosts or prey by volatile chemicals (kairomones) that have been damaged by larvae of a closely
released by the prey or from by-products of the related noctuid, the corn earworm Helicoverpa zea,
prey (e.g., pheromones and excretory products which is not a viable host for this parasitoid.
such as frass and honeydew). For example, some The odor of flowers that attracts pollinating
species of ant-decapitating flies in the genus Pseu- insects can also be considered synomonal because
dacteon (family Phoridae) are attracted to their it is beneficial to both the flower whose pollination
hosts, worker fire ants in the genus Solenopsis (fam- is ensured and, usually, to the receiving insect,
ily Formicidae), by the odor of the ants alarm which is guided to a necessary resource nectar,
pheromone. Specialist herbivorous insects (those pollen, or some other reward. However, some plants
that oviposit on and whose larvae feed on only a have turned their synomones into allomones, by
narrow range of plant species) use distinct chemi- attracting insects and then providing them with
cals produced by their host plants as signposts or nothing in return. For example, many species of
guides to their plants. For example, moths that orchids in the Mediterranean and other places in
specialize on plants in the cabbage family, such as the world attract male bees and wasps of certain
the cabbage white butterfly Pieris rapae, are species with floral odors that mimic the sex phero-
attracted to the volatile isothiocyanates, which are mone of their own species. The males are attracted
allomones for most other insects that do not feed to the flower and attempt to mate with it. During
on cabbage. Thus a kairomone can be a chemical this pseudocopulation, the flower is pollinated
cue that the emitter legitimately uses as a phero- but the male insect gains nothing, and is perhaps
mone or an allomone but that an illegitimate even harmed by wasting its time and energy on an
receiver turns to its advantage. A single chemical activity that will not increase its genetic fitness.
compound could be called a pheromone, a kai- Alarm Pheromones
romone or an allomone, depending on who bene- Allelochemicals
fits, the emitter or the receiver. Attraction of Insects to Organic Sulfur
The last class of semiochemicals that is recog- Compounds in Plants
nized today is the synomones. This term was pro- Host Location in Parasitic Wasps
posed for chemicals that mediate mutualistic Host Marking Pheromones
interactions in which both the emitter and the Host Plant Selection by Insects
receiver benefit. For example, the blend of chemi- Natural Enemy Attraction to Plant Volatiles
cals released by plants when under attack by Pheromones
herbivorous insects may properly be called a Plant Secondary Compounds and
synomone when it attracts parasitoids or predators Phytophagous Insects
 Chestnut Gall Wasp Classical Biological Control in Japan
C 835

Pyrrolizidine Alkaloids and Tiger Moths Chestnut Gall Wasp Classical

Sex Attractant Pheromones Biological Control in Japan
Social Insect Pheromones
Tritrophic Interactions Seiichi Moriya
National Agricultural Research Center, Tsukuba,
References Japan

Bell WJ, Card RT (eds) (1995) Chemical ecology of insects 2. The chestnut gall wasp, Dryocosmus kuriphilus
Chapman & Hall, New York. Yasumatsu (Hymenoptera: Cynipidae), is one of
De Moraes CM, Lewis WJ, Par PW, Alborn HT, Tumlinson the most serious chestnut-tree pests. It is thely-
JH (1998) Herbivore-infested plants selectively attract
tokous and univoltine. This wasp is now thought
parasitoids. Nature 393:570573
Dicke M, Grostal P (2001) Chemical detection of natural to have originated in China and to have been acci-
enemies by arthropods: an ecological perspective. Ann dentally introduced from there into Japan around
Rev Ecol Syst 32:123 1940. Chestnut gall wasp was also introduced into
Harborne JB (2001) Twenty-five years of chemical ecology.
Nat Prod Rep 18:361379
South Korea and Georgia, in the southeastern
Haynes KF, Yeargan KV (1999) Exploitation of intraspecific United States, in 1958 and 1974, respectively,
communication systems: illicit signallers and receivers. probably via Japan.
Ann Entomol Soc Am 92:960970 The adult emerges from the gall during a rel-
Morehead SA, Feener DH Jr (2000) Visual and chemical cues
used in host location and acceptance by a dipteran para- atively brief part of the early summer, and imme-
sitoid. J Insect Behav 13:613625 diately lays eggs inside chestnut buds (Fig. 42)
Schiestl FP, Ayasse M, Paulus HF, Lfstedt C, Hansson BS, When the buds start to develop the following
Ibarra F, Francke W (1999) Orchid pollination by sexual
spring, immature larvae that hatched in the previ-
swindle. Nature 399:421422
ous year resume their growth, and the galls begin
to swell rapidly. Consequently, in heavily infested
Chemigation trees, the yields of chestnuts are diminished, and
the trees themselves may die.
Application of agricultural chemicals, including
insecticides, through the irrigation system.

Chemokinesis
A kinesis response with respect to a chemical
gradient.

Chemoreceptor
A sense organ that perceives chemical stimuli.

Chemotaxis Chestnut Gall Wasp Classical Biological Control in

Japan, Figure 42 Dryocosmus kuriphilus
A taxis with reference to a chemical gradient (taste, ovipositing on the bud of a chestnut tree (photo
odor). by S. Moriya).
836
C Chestnut Gall Wasp Classical Biological Control in Japan

After entering Japan, the pest spread so fast

that it was distributed throughout most of Japan
by the end of the 1950s, seriously damaging chest-
nut production. Because the larva of chestnut gall
wasp is protected by the thick wall of the gall, no
method of chemical control was feasible. But
chestnut gall wasp could be controlled very effec-
tively at first by using resistant chestnut varieties.
Therefore, all of the susceptible varieties of chest-
nut trees were rapidly replaced by resistant ones.
However, a stronger strain of chestnut gall wasp
emerged, and the galls began to appear again
around 1960, even on the highly resistant varieties.
The breakdown of resistance alarmed chestnut
growers, because the use of resistant varieties was
the only available method of controlling the pest.
After diplomatic relations between Japan and
China were re-established in 1972, a Japanese
entomologist found that chestnut gall wasp had Chestnut Gall Wasp Classical Biological Control in
been recorded on a Chinese chestnut, Castanea Japan, Figure 43 Torymus sinensis attacking a gall
mollissima Blume, much earlier in China than in of Dryocosmus kuriphilus (photo by S. Moriya).
Japan. Furthermore, it was found that chestnut gall
wasp had not been a serious pest in China even
though Chinese chestnut varieties were highly sus- Thus, the single release of T. sinensis at NIFTS ulti-
ceptible to chestnut gall wasp. Thus, a Chinese para mately reduced chestnut gall wasp infestation to a
sitoid, Torymus sinensis Kamijo (Hymenoptera: level far below that which chestnut trees can toler-
Torymidae), was selected for introduction to ate (the tolerable injury limit is about 30% infesta-
Japan. In the spring of 1982, a mere 260 mated tion of current shoots). The rate at which T. sinensis
females were released onto Japanese chestnut trees, expanded its distribution range was also deter-
C. crenata Sieb. et Zucc., growing on the grounds mined. The parasitoid spread gradually during the
of the National Institute of Fruit Tree Science first few years, at a rate of <1 km/year, followed by
(NIFTS), Tsukuba, about 50 km northeast of more rapid and accelerated spreading in the next
Tokyo. Like chestnut gall wasp, the parasitoid is few years. In the spring of 1989, T. sinensis was
univoltine, and yet the population of T. sinensis in detected in an area more than 12 km from NIFTS.
Japan increased steadily year after year. The den- Since then, a steady expansion, at a constant rate
sity of T. sinensis females in 1989 was more than 25 of about 60 km per year (=per generation), has
times higher than that in 1983. T. sinensis is now been observed. Consequently, the parasitoids seem
completely dominant among the native parasi- to have dispersed by themselves several hundred
toids of chestnut gall wasp at NIFTS. The effect of kilometers from the point of release by the mid-
the 1982 release of T. sinensis on the chestnut gall 1990s.
wasp population was evaluated by observing gall In Kumamoto Prefecture, in southwestern
formation ratios (Fig.43) on chestnut trees. Infes- Japan, T. sinensis was also released in 1982 and was
tation of chestnut gall wasp steadily decreased later confirmed to have become established there.
after the release until it reached a level of about 3% However, unlike the case in Tsukuba, the popula-
in 1988, then decreased to < 1% in the early 1990s. tion density did not increase significantly. This
 Chewing and Sucking Lice (Phthiraptera)
C 837

delay in population increase might be attributable sinensis, and native parasitoids. In: Yano E, Matsuo K,
Shiyomi M, Andow DA (eds) Biological invasions of
to the high mortality of T. sinensis associated with
ecosystem by pests and beneficial organisms. National
the activity of native facultative hyperparasitoids. Institute of Agro-Environmental Sciences, Tsukuba,
A native Japanese parasitoid, T. beneficus Japan, pp 175188
Yasumatsu et Kamijo, which is closely related to
T.sinensis, consists of at least two strains that differ
from each other only in the time of the adult emer-
gence period. The female of either strain of T.bene- Chevrolat, Louis Alexandre
ficus has a shorter ovipositor sheath than does the Auguste
female of T. sinensis, whereas the male T. beneficus
cannot be distinguished morphologically from the Auguste Chevrolat was born in Paris on March 29,
male T. sinensis. The emergence period of T. sinen- 1799. He had numerous sisters, and was brought
sis is in between those of the two strains of T. bene- up not by his parents but by his grandmother and
ficus and more or less overlaps them. Thus, it a maternal aunt in the town of Melun. He showed
should be noted that crossing between T. sinensis an early interest in natural history, collecting birds
and T. beneficus occurs under natural conditions. and all sorts of insects, but decided to specialize in
When these two torymids were artificially beetles. He made friends with notable entomolo-
crossed, morphologically intermediate females gists (Latreille, Dumril, Dejean, and Gurin) and
were observed among the offspring, and they were began to publish descriptions of new species of
fertile. Although there was no evidence of direct insects, the first being Doryphora 21-punctata
competition between T. sinensis and T. beneficus, published in Magasin de Zoologie. He was charged
the number of T. beneficus apparently decreased by Duponchel to edit the section on chrysomelids
after T. sinensis was introduced into the chestnut for the dictionary directed by d Orbigny. In 1832
groves at NIFTS. he was a founding member of the Socit Ento-
mologique de France, and in 1875 was elected an
honorary member of it. He published more than
References 180 papers during his lifetime, his two most fre-
quent outlets were Annales de la Socit Ento-
Moriya S, Inoue K, Mabuchi M (1989) The use of Torymus mologique de France, and Magasin Zoologique,
sinensis to control chestnut gall wasp, Dryocosmus and he published more on Curculionidae (in the
kuriphilus, in Japan. Food Fertilizer Technology Center broad sense) than on any other insect family. He
Technical Bull 118:112
died on December 16, 1884.
Moriya S, Inoue K, Shiga M, Mabuchi M (1992) Interspecific
relationship between an introduced parasitoid, Torymus
sinensis Kamijo, as a biological control agent of the
chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu, Reference
and an endemic parasitoid, T. beneficus Yasumatsu et
Kamijo. Acta Phytopathol Entomol Hung 27:479483
Murakami Y (1997) Natural enemies of the chestnut gall Reiche L (1884) Notice necrologique sur Auguste Chevrolat.
wasp: approaches to biological control. Kyushu Univer- Ann Soc Entomol Fr (6) 4:357360
sity Press, Fukuoka, Japan, 308 pp (in Japanese)
Murakami Y, Gyoutoku Y (1995) A delayed increase in the
population of an imported parasitoid, Torymus (Syn-
tomaspis) sinensis (Hymenoptera: Torymidae) in Kuma- Chewing and Sucking Lice
moto, southwestern Japan. Appl Entomol Zool (Phthiraptera)
30:215224
Shiga M (1997) Classical biological control of the chestnut
gall wasp, Dryocosmus kuriphilus: present status and This order of wingless ectoparasitic insects is
interactions between an introduced parasitoid, Torymus thought to have evolved from barklice (Psocoptera).
838
C Chewing and Sucking Lice (Phthiraptera)

Certainly it is not difficult to imagine insects Family Boopidae marsupial chewing lice
dwelling in animal nests (many Psocoptera) evolv- Family Gryropidae guinea pig lice
ing into insects that dwell on birds and mammals Family Trimenoponidae marsupial lice
(Phthiraptera), and morphologically they are sim- Family Abrocomophagidae
ilar. Traditionally, the order Phthiraptera has been Suborder Ischnocera
treated as two separate orders (or two suborders), Family Trichodectidae mammal chewing lice
the chewing lice (Mallophaga) and the sucking Family Philopteridae bird lice
lice (Anoplura). However, modern treatment of Family Heptapsogasteridae
this group has Mallophaga divided into three sub- Suborder Rhyncophthirina
orders (Amblycera, Rhyncophthirina, Ischnocera), Family Haematomyzidae
with Anoplura the fourth suborder. Both chewing Suborder Anoplura
and sucking lice are obligate parasites, and cannot Family Polyplacidae spiny rat lice
survive long off their hosts. They are the only truly Family Linognathidae pale lice
parasitic group among the exopterygote insects. Family Enderleinellidae squirrel lice
They display remarkable host specificity, and most Family Hoplopleuridae
individuals spend their entire life cycle on a single Family Neolinognathidae
host. They relocate opportunistically only when Family Hamophthiriidae
individuals are in close proximity, and so they have Family Ratemiidae
developed diverse morphology due to their high Family Microthoraciidae
degree of isolation. Their basic specializations are Family Echinophthiriidae seal lice
based on feeding on skin debris, fur, feathers, and Family Pthiridae pubic lice
blood. The order name (Phthiraptera) is derived Family Pedicinidae
from the Greek words phtheir (louse), plus a Family Pecaroecidae peccary lice
(without), and pteron (wing). Family Hybothiridae
Family Haematopinidae ungulate lice
Family Pediculidae body lice
Classification The hosts of the chewing lice, other than those
suggested by the aforementioned common names,
About 3,000 species of chewing lice from around are hummingbirds for trochiliphagids; ducks,
the world are distributed in three suborders, and geese and swans for trinotonids; a rodent for the
often associated with specific bird hosts, but some- only known abrocomophagid; many birds for hep-
times mammals. There are about 15 families of tapsogasterids; and elephants and warthogs for
sucking lice, containing only about 500 species, haematomyzids. The sucking lice feed on mam-
though many species probably remain to be mals. Interestingly, although humans have domes-
described. Most species of lice are quite host spe- ticated animals for thousands of years, they have
cific. Some families have common names that rarely acquired lice from them. Instead, the lice
reflect their hosts. associated with humans are in the genera Pthirus
Class Insecta and Pediculus, which they share with the higher
Order Phthiraptera primates, particularly the apes.
Suborder Amblycera
Family Menoponidae poultry lice
Family Trinotonidae Characteristics
Family Laemobothriidae hawk lice
Family Ricinidae hummingbird lice Chewing lice are small ectoparasites, generally
Family Trochiliphagidae measuring 0.56 mm long, and wingless. The head
 Chewing and Sucking Lice (Phthiraptera)
C 839

is wide, or at least wider than the thorax (Fig.44), Sucking lice also are small ectoparasites, mea-
and bears small eyes and short antennae(35 seg- suring only 0.55 mm in length, and oval in shape.
ments). The form of the antenna varies; in the sub- Their head is narrow, a distinguishing character
order Amblycera they normally are capitate, relative to the chewing lice (Fig.45). Their eyes are
whereas in the suborder Ischnocera they are fili- reduced or absent; ocelli are absent. The antennae
form. Ocelli are absent. The mouthparts, as sug- are short, and 35 segmented. The mouthparts,
gested by the common name, are the chewing which are about as long as the head, are highly
type. The body is flattened and has six or fewer modified and are adapted for piercing and sucking.
spiracles. The legs have one or two claws. Cerci The mouthparts are retracted into the head when
are lacking. The metamorphosis is incomplete not in use. The body is dorsoventrally flattened.
(hemimetabolous development). These hemime- The segments of the thorax are fused, and the
tabolous insects have three nymphal instars. thoracic spiracles located dorsally. The abdominal

Labrum
Clypeus Mandible
Preocular slit Labium
Antenna Maxillary palp
Eye Ventral ledge of
antennal groove
Antenna
Transverse suture
Antenna groove
Pleural ridge Temple
Longitudinal suture Gula
Pronotum Episternum
Spiracle Pleural ridge
Mesonotum Sternal apophysis
Pleural ridge Sternum
Metanotum 1 Coxa
Pleural ridge 2 Sternum
Pleural ridge
Antecoxal sclerite
Spiracle of 3rd 3
Abdominal segment Coxa
4 Trochanter
Femur
5
Tibia
Tarsus
6 Pretarsus

10th abdominal
Segment
Anus
Gonopore

Chewing and Sucking Lice (Phthiraptera), Figure 44 A diagram of a chewing louse showing a dorsal view
(left) and a ventral view (right).
840
C Chewing and Sucking Lice (Phthiraptera)

Labrum
Clypeus Antenna
Clypeofrontal suture Tibia
Frons Eye
Postfrontal suture Femur
Ocular lobe Trochanter
Prothoracic pleural ridge Coxa
Mesothoracic pleural ridge Thoracic sternum
Tergal pit
Metathoracic pleural ridge
Median tergites
Spiracle

Paratergites

Chewing and Sucking Lice (Phthiraptera), Figure 45 A diagram of a sucking louse showing a dorsal view
(left) and a ventral view (right).

segments are distinct. The tarsi consist of only one Sucking lice feed only on blood of mammals.
segment, and there is only one large claw on each Two (or three, depending on how Pediculus humanus
tarsus. Cerci are absent. Metamorphosis is incom- is treated) species affect humans, and about 12 spe-
plete, as with the chewing lice. cies affect domestic animals. The families tend to
contain lice with very similar feeding habits. For
example, the echinophthiriids feed on seals, sea lions,
Biology walruses and river otter; the enderleinellids on squir-
rels; the haematopinids on ungulates such as pigs,
Probably all species of birds are affected by chew- cattle, horses and deer; the hoplopleurids on rodents
ing lice, but only about 20% of mammals host and insectivores; the linognathids on even-toed
these lice. The eggs are attached to the feathers or ungulates such as cattle, sheep, goats, reindeer and
hairs of the host with glue. The nymphs and adults deer, and on canids such as dogs, foxes and wolves;
feed on feathers, hair, skin, blood, and the oils pro- the pecaroecids on peccaries; the pediculids on the
duced by the skin. Blood feeding seems to be of head and body of humans; the polyplacids on
minor importance, and substantial infestations rodents and insectivores; and pthirids on gorillas
can occur with little ill effect, though the common and humans. The eggs generally are cemented to the
behavior among birds of taking a dust bath is hairs of the host. There are three nymphal instars in
probably an attempt to rid themselves of lice. nearly all species.
However, when populations are very high, they Because lice are co-evolved (co-speciated) with
can be of veterinary importance, especially to their specific hosts, the extinction of hosts results in
young fowl. They are not important in disease extinction of lice species as well. Due to pervasive
transmission. They spread from animal to animal host extinction (for example, about 67% of the gen-
by body contact, and often leave their host soon era of mammals are thought to be extinct), many
after it perishes. species of lice likely have disappeared. However, lice
 Chikungunya
C 841

do not preserve well, and are virtually absent from he relocated to the Temporary University in Ghang-
the fossil record, so their history is not well known. sha, Hunan, and then to Southwestern Associated
Human Lice University in Kunming, Yunan. The latter involved
an incredible 68-day overland trek by Chiang and
his fellow students. After graduating, he joined
References the Agricultural Research Institute in Kunming.
Kunming was the terminus of the Allied Forces air
Arnett RH Jr, (2000) American insects, 2nd edn. CRC Press, supply route from India, and Chiang interacted
Boca Raton, FL, 1003 pp with a military anti-malaria unit, which allowed
Ash JS (1960) A study of the Mallophaga of birds with par-
ticular reference to their ecology. Ibis 102:93110
him to make important contacts and to improve
Durden LA, Musser GG (1994) The sucking lice (Insecta, his English. Chiang contacted the University of
Anoplura) of the world; a taxonomic checklist with Minnesota and enrolled in 1945. He completed his
records of mammalian hosts and geographical distribu- graduate studies in 1948, and accepted a temporary
tions. Bull Br Mus Nat Hist 218:190
Grimaldi D, Engel MS (2005) Evolution of the insects. Cam- position studying European corn borer. This, and a
bridge University Press, Cambridge, UK, 755 pp temporary stint as an instructor of entomology at
Hopkins GHE (1949) The host-associations of the lice of Minnesota, led to a permanent faculty position
mammals. Proc Zool Soc Lond 119:387605
where he worked until retiring in 1984.
Kim KC, Ludwig HW (1978) The family classification of Ano-
plura. Syst Entomol 3:249284 Huai Chiang is best known for his work on
Kim KC (1987) Order Anoplura. In: Stehr FW (ed) Immature corn pests, and he authored about 250 publica-
insects, vol 1 Kendall/Hunt Publishing, Dubuque, IA, pp tions, including two articles in the Annual Review
224245
Kim KC, Pratt HD, Stpjanovich CJ (1986) The sucking lice of
of Entomology. He was considered an expert in
North America. An illustrated manual for identification. biological control and insect ecology. He was active
Pennsylvania State University Press, University Park, in international and government agencies and
Pennsylvania. programs, and was honored by several universities
Price MA, Graham OH (1997) Chewing and sucking lice as
parasites of mammals and birds. U.S. Department of and countries for his research and service. He died
Agriculture Technical Bulletin 1849, 309 pp on March 30, 2005, in Ithaca, New York.
Price RD (1987) Mallophaga. In: Stehr FW (ed) Immature
insects, vol 1. Kendall/Hunt Publishing, Dubuque, IA,
pp 215223 Reference

Radcliffe T (2005) Huai C. Chiang. Am Entomol 51:126127

Chewing Mouthparts
Chigger
Mouthparts that consist of opposable, non-suck-
ing structures; biting mouthparts. A mite of the family Trombiculidae.
Mouthparts of Hexapods Mites

Chiang, Huai C. Chikungunya

Huai Chiang was born February 15, 1915, in Sunji- Kelly Roe, Kenneth W. McCravy
ang County, Jiansu Province, China. He attended Western Illinois University, Macomb, IL, USA
Tsinghua University in Beijing, where he was first
exposed to entomology. During the Sino-Japanese Chikungunya is an Alphavirus in the family Toga-
war of 19371945, his studies were disrupted and viridae. It is an arthropod-borne virus (arbovirus)
842
C Chikungunya

transmitted to humans primarily by Aedes aegypti, virus has shown signs of greater virulence in the
the yellow fever mosquito. Togaviruses replicate in recent Indian Ocean epidemic. Occasionally joint
the cytoplasm and mature by budding out from pain can reoccur intermittently for months or
the cell membrane. They are not very stable in the even years. Unapparent Chikungunya infections
environment and are easily destroyed or inacti- do occur, but how commonly this occurs is
vated by disinfectants. The genus Alphavirus has unknown. It is thought that life-long immunity
27 member viruses, all of which are mosquito- isconferred through clinical or unapparent infec-
borne. Eleven of these viruses cause disease in tion with the Chikungunya virus.
humans, and eight of them produce significant Chikungunya is diagnosed based on symp-
epidemics: Chikungunya, Ross River virus, east- toms and serological testing. At this time there is
ern, western, and Venezuelan equine encephalitis, no cure for the disease. Vaccine trials were carried
Onyong-nyong, Mayaro, and Sindbis. Chikungu- out in 2000, but funding for the project was elimi-
nya virus is widespread throughout Africa, India, nated and the project was discontinued. There is
and Southeast Asia, including the Philippines. no vaccine or antiviral treatment available for
Devastating epidemics, sometimes lasting for Chikungunya fever. The illness is generally self-
months or years, have occurred and reoccurred in limiting and the symptoms usually resolve over
Africa and Asia. A majority of an urban popula- time. Symptomatic treatments are recommended
tion can be infected within a few months. Under after excluding other more dangerous diseases,
these circumstances A. aegypti can maintain the such as dengue and yellow fever. These treatments
virus in a human-mosquito-human cycle. include rest, plenty of fluids, and acetaminophen,
naproxen, ibuprofen, or paracetamol to relieve
fever and aching. Aspirin should not be taken to
Symptoms, Treatment, and treat Chikungunya fever. An infected person
Prevention should stay indoors to protect against further
mosquito exposure and transmission of the dis-
Chikungunya received its name from a Swahili or ease to other people during the first few days of
Makonde term meaning that which bends up, illness. Other measures to reduce the spread of
referring to the stooped posture of patients afflicted Chikungunya fever include use of insecticides to
with severe joint pain associated with this disease. kill adult and larval mosquitoes. Measures that can
Chikungunya is a debilitating but generally self- be taken by individuals include elimination of
limiting febrile viral disease. It is characterized standing water where mosquitoes can breed, use
by arthralgia or arthritis, typically in the small of insect repellents containing permethrin or
joints of the extremities, such as ankles, knees, DEET, wearing long pants and long-sleeved shirts,
toes, wrists, and fingers. Other symptoms include and use of screens on windows and doors to pre-
high fever, headache, nausea, vomiting, photopho- vent entry by mosquitoes.
bia, maculopapular rash, buccal and palatal The present strain of the Chikungunya virus in
enanthema, myalgia, chills, flushed face, lymph- the Indian Ocean region appears to be more viru-
adenopathy, stooped posture, and, in some cases, lent than those causing previous epidemics. A num-
bleeding from the nose and mild hemorrhaging. ber of patients have developed complications and
The incubation period can range from 212 days, died. The death of a 10 year old boy had no other
but is usually 37 days. The onset of this disease is plausible explanation; Chikungunya virus was the
sudden, and is marked by a rapid increase in body only pathogen present in his blood. The death toll
temperature followed by severe pain in the limbs from the Chikungunya virus continues to increase.
and spine. These symptoms usually last 35 days In the Indian Ocean region, 77 death certificates
followed by recovery in 57 days. However, the issued in January through March 2006 state
 Chikungunya
C 843

hikungunya as the cause of death, although for

C has more recently caused massive epidemics in
most cases co-morbidity played a significant role. many countries. The Chikungunya virus is geo-
graphically distributed in Africa, India, and
Southeast Asia. The virus is maintained in Africa
Epidemiology through a sylvatic transmission cycle between
Aedes luteocephalus, Aedes furcifer, or Aedes tay-
Aedes aegypti is the most important vector of the lori mosquitoes and wild primates. The Chikun-
viruses of Chikungunya, dengue, and yellow fever. gunya virus is transmitted among baboons and
This mosquito is widely distributed between 40N humans by A.furcifer. In Africa, baboons are the
and 40S latitude. Aedes aegypti does not thrive in primary vertebrate host from which the virus
hot dry climates and is vulnerable to extreme tem- extends into the human population. In Asia, the
peratures. The primary food source for female A. Chikungunya virus is transmitted from human
aegypti is blood from a vertebrate host; male mos- to human by A. aegypti through an urban trans-
quitoes do not suck blood. The blood meal for A. mission cycle. Because neither a vertebrate res-
aegypti is commonly human blood, but they will ervoir nor a sylvan transmission cycle has been
also feed on other mammals and birds. Aedes identified outside of Africa, it is thought that the
aegypti has been recognized as the chief vector of Chikungunya virus originated in Africa and was
Chikungunya for approximately 50 years, although later introduced into Asia and other parts of the
other species of Aedes (see below) and Culex have world. The Chikungunya virus has caused out-
also been implicated. breaks and epidemics in East Africa (Tanzania
In the 1950s an aggressive mosquito control and Uganda), Austral Africa (Zimbabwe and
campaign greatly reduced A. aegypti on the island South Africa), West Africa (Senegal and Nige-
of Runion, east of Madagascar in the Indian ria), and Central Africa (Central African Repub-
Ocean. Reducing the primary vector of Chikun- lic and Democratic Republic of the Congo) since
gunya should have reduced or eliminated the its discovery in 1953.
spread of this disease. This proved not to be the Chikungunya virus in the Indian Ocean
case. Aedes albopictus, the Asian tiger mosquito, region has recently caused one of the largest epi-
was not viewed as a significant threat, and remained demics reported in the last 40 years, involving
abundant due to lack of control measures. This hundreds of thousands of people. The severity and
mosquito is of Asian origin, and is usually found magnitude of the epidemic has surprised public
far away from human habitation. Aedes albopictus health specialists and the governments. Chikun-
feeds readily on many species of mammals and gunya virus infection has steadily increased within
birds. It was assumed to be an inefficient vector of the human population. In 2005 there were an esti-
Chikungunya in nature because of its habit of mated 12,400 cases reported, whereas in 2006
feeding on non-susceptible hosts that do not con- there were over 200,000 cases reported through
tribute to the transmission cycle. However, the April alone. These numbers do not include cases
recent outbreak and epidemic of Chikungunya on that are misdiagnosed or unreported.
Runion, with roughly 265,000 people infected It has been suggested that many cases of Chi-
(34% of the total population of the island), indi- kungunya fever are misdiagnosed as dengue fever.
cates that A. albopictus can be an effective vector The clinical symptoms of Chikungunya infection
of Chikungunya. often mimic those of dengue fever, and Chikungu-
The Chikungunya virus was first isolated nya virus is present in regions where dengue virus
from the blood serum of a febrile human by R.W. is endemic. There have been documented cases
Ross in 1953 in the Newala district of Tanzania. of simultaneous co-infection with dengue and
It was later recovered in Bangkok in 1958, and Chikungunya viruses. A human-mosquito-human
844
C Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae)

cycle has sustained urban epidemics involving Tesh RB, Gubler DJ, Rosen L (1976) Variation among geo-
graphic strains of Aedes albopictus in susceptibility to
A.aegypti as the vector, and Chikungunya-dengue
infection with Chikungunya virus. Am J Trop Med Hyg
and Chikungunya-yellow fever outbreaks have 25:326335
been described. The association of Chikungunya, World Health Organization. Chikungunya and dengue in the
dengue, and yellow fever is likely due to transmis- south west Indian Ocean. Available at http://www.
WHO.int/csr/don/2006_03_17/en. Accessed 25 May
sion by the same vector species, A. aegypti. Aedes 2007
aegypti is not limited to Africa and Asia, so there is
the possibility that the Chikungunya virus could
spread elsewhere.
In 2006, six complete genome sequences of Chilli Thrips, Scirtothrips dorsalis
selected Chikungunya viral isolates were studied. Hood (Thysanoptera: Thripidae)
Results of this study suggest that the Chikungunya
virus can adapt to new environmental conditions, Dakshina R. Seal, Waldemar Klassen
and can evolve the ability to survive in vectors that University of Florida, Homestead, FL, USA
it was incapable of surviving in previously. These
results underscore the possibility that the Chikun- The common names of Scirtothrips dorsalis are
gunya virus can spread to other parts of the world. chilli thrips, chili thrips, castor thrips, Assam
The Chikungunya virus continues to be a growing thrips, strawberry thrips and yellow tea thrips.
problem since its discovery in 1953. Taxonomists now regard Neophysopus fragariae
Girault, Heliothrips minutissimus Bagnall, Anapho-
thrips andreae Karny and S. dorsalis var. padmae
References Ramakrishna as synonyms of S. dorsalis Hood.

Enserink M (2006) Massive outbreak draws fresh attention to

little-known virus. Science 311:1085
Effler PV, Pang L, Kitsutani P, Vorndam V, Nakata M, Ayers
T, Elm J, Tom T, Reiter P, Rigau-Perez JG, Hayes JM, Economic Importance
Mills K, Napier M, Clark GG, Gubler DJ (2005) Dengue
fever, Hawaii, 20012002. Emerg Infect Dis 11:742749 Scirtothrips dorsalis has long been a pernicious pest
Higgs S (2006) The 20052006 Chikungunya epidemic in the
Indian Ocean. Vector Borne Zoonotic Dis 6:115116 of various vegetable crops, cotton, citrus and other
Jupp PG, McIntosh BM (1988) Chikungunya disease. In: fruit and ornamental crops in its principal range in
Monath TP (ed) The arboviruses: epidemiology and southern Asia, where it may kill newly emerged
ecology. CRC Press, Boca Raton, FL, pp 137157
seedlings, severely distort leaves and scar the surface
Kettle D (1995) Medical and veterinary entomology, 2nd edn.
CABI Publishing, New York. of fruits of its favored hosts. In India, S. dorsalis is a
McIntosh BM, Jupp PG, Dos Santos I (1977) Rural epidemic serious pest of castor bean (Ricinus communis L.),
of Chikungunya in South Africa with involvement of chilli pepper (Capsicum annum L. var. annum), pea-
Aedes furcifer and baboons. S Afr J Sci 73:267269
Myers RM, Carey DE (1967) Concurrent isolation from
nut (Arachis hypogaea L.), cotton (Gossypium spp.),
patient of two arboviruses, Chikungunya and dengue onion (Allium cepa L.), rose (Rosa spp.) and other
type 2. Science 157:13071308 flowers. In Taiwan, S. dorsalis is a significant pest of
Reiter P, Fontenille D, Paupy C (2006) Aedes albopictus as an citrus, especially satsuma mandarin (Citrus unshui
epidemic vector of Chikungunya virus: another emerg-
ing problem? Lancet Infect Dis 6:463464 Marc), tea (Camellia sinensis [L.] O. Kuntze), and
Ross RW (1956) The Newala epidemic. III. The virus: isola- the rubber tree (Hevea brasiliensis Mll. Arg.). In
tion, pathogenic properties and relationship to the epi- Japan, S. dorsalis is notorious for its damage to cit-
demic. J Hyg 54:177191
rus, tea, and grapevine (Vitis vinifera L.). In Cte
Salvan M, Mouchet J (1994) Aedes albopictus and Aedes
aegypti at Ile de la Runion. Ann Soc Belg Med Trop dIvoire, it is a serious pest of cotton. In Indonesia,
74:323326 S. dorsalis is a serious pest of soybean (Glycine max
 Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae)
C 845

[L.] Merr.). In Queensland, Australia. S. dorsalis is a Scirtothrips dorsalis is a vector of various viral
significant pest of strawberry (Fragaria ananassa and bacterial diseases, including peanut bud
Duchesne X F. virginiana Duchesne). necrosis virus (PBNV), peanut chlorotic fan virus
Scirtothrips dorsalis has spread to South (PCFV), tobacco streak virus (TSV) and tomato
Africa, Cte dIvoire, Kenya, Oceania, Australia spotted wilt virus (TSWV).
(Queensland), Papua New Guinea, Indonesia,
and the Solomon Islands; in 2003 it was found to
be established on St. Vincent, an island in the
Caribbean Sea. Since 2003, S. dorsalis has Recognizing S. dorsalis Infestations
emerged as a major pest in certain Caribbean
islands, Suriname, Venezuela, Florida and south- Scirtothrips dorsalis feeds on the meristems of host
ern Texas. The pest is still absent from the Euro- plants terminals and on other tender above-ground
pean and the Mediterranean Region. In the New parts, and creates damaging feeding scars, distor-
World, S. dorsalis is now damaging crops as fol- tions of leaves and discolorations of buds, flowers
lows St. Vincent and St. Lucia: commercial and young fruits (Fig.46). It does not feed on mature
fields of chili pepper; Barbados: sea island cotton tissue. Scirtothrips dorsalis causes damage by suck-
(Gossypium barbadense L.), and carrot (Daucus ing the contents out of individual epidermal cells,
carota L.); Florida: Celosia argentea L., coleus which leads to necrosis of the tissue. Initially such
(Plectranthus scutellaroides [L.] R. Br.), Coreopsis tissue has a silvery sheen, but soon the damaged
spp., geranium (Pelargonium x hortorum Bailey), areas turn brown or black. In heavily infested pep-
Gerber daisy (Gerbera jamesonii H. Bolus ex per fields the appearance of the plants is known as
hook f.), Knockout rose, pepper transplants chilli leaf curl. Heavy feeding causes the tender
(Rosa spp.), impatiens (Impatiens spp.), Japanese leaves and buds to become brittle, so that total defo-
privet (Lagustrum japonicum), lisianthus (Eus- liation and severe crop loss may occur.
toma russellianum), pentas (Pentas lanceolata Usually, S. dorsalis adults are no longer than 1.2
[Frrsk.] Deflers), petunia (Petunia x hybrida), mm and have pale bodies and dark wings. Dark
pittosporum (Pittosporum spp.), plumbago spots are found dorsally on the abdomen, forming
(Plumbago auriculata), snapdragon (Antirrhi- an incomplete stripe. Typically, the first instar lar-
num majus), verbena (Grandualaria x hybrida vae, second instar larvae and pupae are 0.370.39,
[Gnland & Rmpler] Neson & Pruski), Victoria 0.680.71 and 0.780.80 mm long, respectively, and
blue (Salivia farinacea), pansy Viola x wittrocki- all have pale bodies. The presence of distorted
ana Gams, zinnia (Zinnia elegans) and many ordiscolored plant parts is suggestive of presence of
other ornamental plants. Lawn care operators S. dorsalis. Larvae feed on the undersides of young
and other landscape management firms in Flor- tender pepper leaves, and cause the leaf edges to
ida regard S. dorsalis to be nearly as threatening curl upwards and brownish areas to develop
as insecticide-resistant western flower thrips, between the veins. Corky tissue develops on infested
Frankliniella occidentalis (Pergande). Thus, where fruits. Scirtothrips dorsalis larvae and adults tend
the two species both occur, it is important that toaggregate along the midvein or at the borders of
measures taken against one species do not exac- damaged leaf tissues. In some instances, S. dorsalis
erbate the difficulty of suppressing the other. infested plants superficially resemble broad mite
Also in Florida, S. dorsalis has been found fre- infested plants, but broad mites cause pepper leaves
quently on pepper seedlings in retail outlets, to curl downwards and become narrow. On the
but it has not yet become problematic in the other hand, when S. dorsalis populations become
commercial production of pepper or any other dense, the pest then feeds on the upper sides of the
vegetable crop. leaves of a number of host plants.
846
C Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae)

Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae), Figure 46 Chilli thrips and damage:
(a) adult of chilli thrips (photo by L. Mound), (b) larva of chilli thrips (photo by C. Sabines), (c) chilli
thrips-infested rose plants (photo by C. Sabines), (d) chilli thrips damage on a pepper plant (photo by I.
Maguire) (e) chilli thrips damage on a cotton plant (photo by I. Maguire).
 Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae)
C 847

Scirtothrips dorsalis individuals can be dis- dry periods than during rainy periods, and its abun-
lodged onto a white or black paper or plastic sheet dance is negatively affected by torrential rainfall
on which they are readily visible. Samples can be events. The flight activity of S. dorsalis is greatest
taken by rinsing these thrips from plant material between noon and 2 p.m. Not all eggs are fertilized
using 70% ethanol. The ethanol solution is then as a result of mating. Fertilized eggs develop into
poured onto a fine sieve, and the specimens can be females, and unfertilized eggs develop into males.
removed from the latter with a camel hair brush The sex ratio is often shifted in favor of female
and mounted on slides for examination under a progeny.
microscope. Adults are attracted to yellow sticky
cards and perhaps to a lesser extent to yellowish-
Host Plants
green, green or white surfaces. In Japan sticky suc-
tion traps above the canopies of tea plants are used
Before S. dorsalis became established in the Western
to monitor the flight of S. dorsalis and other thrips.
Hemisphere, it was already known to attack a wide
range of hosts belonging to 112 plant taxa in about
40 families; as the pest invades new territory it
Life History
attacks many additional taxa of plants. Economi-
cally important hosts of S. dorsalis, include the
The life cycle stages of S. dorsalis are egg, first instar
following: banana (Musa spp.), bean (Phaseolus vul-
larva, second instar larva, prepupa, pupa and adult.
garis L.), cashew (Anacardium occidentale L.), castor
The microscopic eggs are creamy white, kidney
(Ricinus communis L), Chinese bitter cucumber
shaped and about 0.075 mm long and 0.070 mm
(Momordica charantia L.), citrus (Citrus spp.), corn
wide. They are deposited inside plant tissue above
(Zea mays L.), cocoa (Theobroma cacoa L.), cotton
the ground, and they hatch in 25 days. Larvae and
(Gossypium spp.), eggplant (Solanum melongena L.),
adults tend to aggregate along the midvein or at the
golden dew drop (Duranta erecta Lindl.), grape
borders of damaged leaf tissues. Usually the pupae
(Vitis spp.), kiwi (Actinidia chinensis Planch), litchi
are found in the axils of the leaves, in curled leaves,
(Litchi chinensis Sonn.), longan (Dimocarpus longan
under calyces of flowers and fruits, although they
Lour.), mango (Mangifera indica L), melon (Cucumis
may also be found in the leaf litter or soil. Larval
melo L.), onion (Allium cepa L.), passionfruit (Passi-
development requires 810 days and prepupal and
flora edulis Sims), peach (Prunus persica L. Batsch),
pupal development together require 2.63.3 days. At
peanut, (Arachis hypogaea L.), pepper (Capsicum
about 28C, the period spanning the first instar to
spp.), poplar (Populus spp.), sacara (Sacara spp.),
the adult ranged from 11.0 days on pepper to 13.3
sacred lotus, (Nelumbo nuciferae Gaertn.), soybean
days on squash. S. dorsalis adults lived 13.6 days on
(Glycine max L.), strawberry (Fragaria ananassa
tomato and 15.8 days on eggplant. The base and
Duchesne X F. virginiana Duchesne), sweet potato
upper development temperatures of S. dorsalis are
(Ipomoea batatas L.), tea (Camellia sinesis L.),
9.7C and 33.0C, respectively. The species has a
tobacco (Nicotianum spp.), tomato (Lycopersicon
thermal requirement of 265 degree days from egg to
esculentum L.), viburnum (Viburnum suspensum
adult and 281 degree days from egg to egg. Thus, the
Lindl.), wild yam (Discorea spp.), and yedda haw-
species is believed to undergo up to 18 generations
thorn (Rhaphiolepis umbellata (Thunb.).
per year in warm subtropical and tropical areas and
about eight generations per year in warm temperate
areas. It is believed that S. dorsalis cannot overwinter Monitoring and Management
outdoors in areas where the minimum temperature
reaches 4C for 5 or more days. Scirtothrips dorsalis Host crops such as bean, corn and cotton, are
tends to become more abundant during prolonged produced from seed and should be monitored as
848
C Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae)

soon as the seedlings emerge, because the seed- spp., several mired bugs, ladybird beetles, and
lings are especially attractive and very suscepti- anumber of predatory thrips including Franklino-
ble to severe damage by S. dorsalis. Hosts that thrips vespiformis, the black hunter thrips, the six
appear to serve as preferred, such as pepper, spotted thrips (Leptothrips mali), Scolothrips sex-
Knockout rose, lisianthus, etc., should be mon- maculatus, the banded wing thrips (Aeolothrips
itored for symptoms of S. dorsalis infestation at spp.), and the predatory phytoseiid mites, Ambly-
least twice per week. Samples of symptomatic seius spp., Euseius hibisci and Euseius tularensis.
plant tissues should be sent to a professional for In India the known predators of both larvae
confirmation. and adults of S. dorsalis are Carayonocoris indicus,
The development of systems for managing Erythrothrips asiaticus, Franklinothrips megalops,
S.dorsalis is still in its infancy. The World Vegetable Geocoris ochropterus, Mymarothrips garuda,
Center (AVRDC) recommends the removal of any Orius maxidentex, and Scolothrips indicus. Most
weeds that may serve as hosts, rotation of crops, of the known parasitoids of thrips are in the
fostering the activities of predators and parasites, genera Ceranisus, Goetheana, Thripobius, and
and rotating insecticides. In Japan the use of reflec- Entedonastichus.
tive synthetic films to cover the ground between Under experimental conditions, S. dorsalis
rows of citrus trees is fairly effective. can be suppressed with several entomopatho
Thrips are attacked by an array of preda- gens including Beauveria bassiana, Metarhizium
tors, parasitoids and pathogens. Practical use in anisopliae and Fusar ium semitectum. The first two
managing thrips populations in the field has of these pathogens have been used for insect con-
been made of minute pirate bugs, Orius spp. trol for several decades, whereas the latter was
(Hemiptera: Anthocoridae) and of the ento- recently found to be effective in the laboratory
mopathogenic nematodes, Thripinema spp. studies in India.
(Tylenchida: Allantonematidae). Orius adults The advent of S. dorsalis into the Caribbean
and nymphs eat all stages of thrips, and suppress and Florida stimulated research on its biology and
rapidly growing thrips populations. Since Orius management. Notably the pyrethroid insecticides
also feed on aphids, spider mites, moth eggs, and proved to be only weakly effective. The most effec-
pollen, Orius populations tend to persist long tive materials evaluated to date (Table 11) are
after thrips populations have been decimated. shown in the table. In order to forestall the devel-
Thripinema are tiny parasitic worms, which render opment of resistance to any insecticide, materials
parasitized female thrips incapable of laying eggs. belonging to different classes should be used in a
Male and female thrips parasitized with Thripinema rotation. Formulations of imidacloprid applied to
tend to feed sparingly, cause little feeding damage the soil as a drench are effective, and they do not
and spread pathogens weakly. kill predators and parasites. In instances where
Whether releases of Orius or Thripinema another pest, such as the western flower thrips in
should be made will depend on the value of the Florida, has already developed incipient resistance
plant material to be protected. Also since releases to a given insecticide, great care must be exercised
may be less effective outdoors than in greenhouses in choosing an insecticide to suppress S. dorsalis.
and shadehouses, the cost of releases outdoors Possibly this problem may be avoided by the appli-
may be prohibitive. Nevertheless every effort cation of entomopathogenic fungi, such as Beau-
should be made to conserve valuable natural ene- veria bassiana, and Metarhizium anisopliae, but
mies in field situations. the efficacy of these preparations still requires field
Other predators of thrips, which have not been evaluation.
adequately studied to determine their practical The insecticide data in the table does not con-
suppression value, include lacewings, Chrysoperla stitute control recommendations. All materials
 Chimaeropsyllidae
C 849

Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae), Table 11 Recently developed
insecticides with high effectiveness against Scirtothrips dorsalis
Class of material Trade name Common name Approximate Method of
% control application
Neonicotinoid Actara thiamethoxama 70 Foliar
Provado; Marathon; imidacloprid a
7080 Foliar
Admire imidacloprid a
>90 Soil

Organophosphate Orthene acephate a
>80 Foliar

Pyrrole Pylon Chlorofenapyr a
>90
Fermentation product: Spintor; Conserve Spinosyn A+Ba >90 Foliar
nicotinic acetylcholine
receptor activator
Radiant Spinetoram >90 Foliar

Fermentation product: Agrimek; Avid Abamectin a
7080 Foliar
GABA inhibitor

Entomopathogenic BotaniGard Beauveria bassiana >80 Foliar
Fungi
Tick EX Metarhizium anisoplae 7080 Foliar

This indicates that efficacy was measured in field trials; absence of a indicates that efficacy was m
a
easured in laboratory
or greenhouse trials

must be used in strict accordance with the regis- Chang NT (1995) Major pest thrips in Taiwan. In: Parker BL,
tration label. Use of biologically based prepara- Skinner M, Lewis T (eds) Thrips biology and manage-
ment. Plenum Press, New York, NY, pp 105108
tions such as spinosyn A + B, spinetoram and Moritz G, Morris D, Mound L (2001) Thrips ID. Pest thrips of
abamectin will allow continuation of the activity the world. An interactive identification and information
of naturally occurring predators and parasites. system. CSIRO Publishing, Australia
Mound LA, Palmer JM (1981) Identification, distribution and
Thrips (Thysanoptera)
host plants of the pest species of Scirtothrips (Thys-
anoptera: Thripidae). Bull Entomol Res 71:467479
Seal DR, Ciomperlik M, Richards ML, Klassen W (2006)
Distribution of the chilli thrips, Scirtothrips dorsalis
References Hood (Thysanoptera: Thripidae), within pepper plants
and within pepper fields on St. Vincent. Fla Entomol
Ananthakrishnan TN (1984) Bioecology of thrips. Indira Pub 89:311320
House, West Bloomfield, MI, 233 pp
Ananthakrishnan TN (1993) Bionomics of thrips. Ann Rev
Entomol 38:7192
CABI/EPPO (1997) Quarantine pests for Europe, 2nd edn. Chimaeropsyllidae
CAB International, Wallingford, UK, 1440 pp
CABI (2003). Crop protection compendium: global module.
Commonwealth Agricultural Bureau International, A family of fleas (order Siphonaptera).
Wallingford, UK Fleas
850
C Chinaberry, Melia azedarach L., A Biopesticidal Tree

Chinaberry, Melia azedarach L., A mahogany family (Meliaceae) and other related
Biopesticidal Tree trees, specifically Melia azedarach L., fulfill most of
the strict requirements for modern pesticides.
Efat Abou Fakhr Hammad These ingredients are non-toxic to mammals and
American University of Beirut, Beirut, Lebanon are readily degraded on plants and in the soil. The
high efficacy of these substances and their rapid
Biopesticides are chemicals derived from a bio- biodegradability completely fulfill the require-
logical source. They are described as agents that ments of toxicological and environmental safety.
include natural plant metabolites, microbial pest
control agents such as entomopathogens, insect
growth regulators and behavior-modifying chem- Classification
icals. Biopesticides are generally nontoxic to verte-
brates and plants and are called biorational The name Melia is the Greek name for the ash-tree
insecticides in Integrated Pest Management pro- Fraxinus ornus L. It belongs to the family Meliaceae,
grams. Biorationals are based on natural products subfamily Meloideae, and tribe Melieae. Melia aze-
and synthetic analogues of naturally occurring darach also is called Persian lilac, lilac, chinaberry,
biochemicals and are more acceptable than con- paradise tree, white cedar, umbrella tree, bead tree,
ventional insecticides because they are environ- syringa, hoop tree, China tree, pride of India, etc. In
mentally less hazardous to humans and other India, the most common name is Dharek. The
non-target organisms. names azadirachtin and azedarach are said to be
Botanical insecticides are plant-derived derived from Persian azadirakht, which means the
chemicals used in insect control. Plants synthesize tree azadirachtin (azadirachtin = ash), similar to
secondary compounds that act as a defense against the derivatization of Melia from the Greek name for
pests and diseases. The plant family Meliaceae was ash ( ). Its common names in the Mediterra-
identified as one of the most promising sources of nean region are Zinzalakht and Azadarakht (Day).
compounds with insect-control properties. In par- Species/forms/variations/cultivars of the
ticular, some members of the generas Melia and Melia complex in Asia and the Pacific region were
Azadirachta were outstandingly effective against all considered to be M. azedarach. Consequently,
insects, and their components also were useful in Melia dubia CAV, M. australasica A. Juss, M. toosen-
many other respects. These components are con- dan Sieb. and Zucc., M. volkensii Grke, M. con-
sidered important from economical, environmen- chinchinensis M.J. Roem., M. superba Roxb., M.
tal and ecotoxicological standpoints because, in floribunda Morr., M. azedarach var. sempervirens
general, only 2050 g of the active principle is suf- Sw., M. azedarach var. japonica Don., and numer-
ficient to treat one hectare of area to achieve a sat- ous others are synonyms of M. azedarach. The
isfactory reduction in pest populations, and also Texas umbrella tree, M. azedarach var. umbraculi-
because the products are readily biodegradable. formis, Berkmans which grows in the southern
The non-conventional effects of these prepara- USA, is considered a mutation of M. azedarach. In
tions can include: partial reduction or complete contrast to all other M. azedarach variations/forms,
inhibition of fecundity and sometimes egg hatch- it has a flattened crown of branches.
ability, reduction of adult life span, oviposition
deterrence, direct ovicidal effects, antifeedant and
repellent effects against larvae, nymphs and adults, Geographic Distribution
and action as an insect growth regulator.
Insecticidal active ingredients from the neem The origin of Melia azedarach L., the chinaberry
tree, Azadirachta indica A. Juss, a member of the tree, is from northwestern India, where it is found
 Chinaberry, Melia azedarach L., A Biopesticidal Tree
C 851

up to approximately 1,800 m above sea level. It is takes place in the Mediterranean region during
indigenous to Baluchistan and the Jhelum valley October and November. Some ecotypes in the wet
in Kashmir. However, it is cultivated and natural- tropics (Malaysia) do not regularly shed their
ized throughout India, Burma, and the Malay Pen- leaves. The girth can reach more than 3.2 m. The
insula. It occurs also in Persia and China. bark is relatively smooth and the heartwood is red-
It is a deciduous tree often grown for shade or dish. Fruits are nearly globular, yellow and smooth.
ornament on roadsides, parks and other open The ripe yellow fruits, or drupes, are about the size
places. It is found in nearly all warm climatic areas. of a cherry, globular to oval, 1/2 3/4 in. in diame-
Due to its relatively low temperature requirements, ter, and are enclosed in a very hard endocarp, which
it grows in southern Europe and in the Mediterra- contains 35 elongate-oval seed kernels. The ripe
nean region as well as southern France, northern fruits can remain for several months on the trees.
Italy, and Croatia. It can be found as an avenue tree The kernels have an oil content of approximately
in Algeria, Cyprus, Greece, India, Lebanon, Pales- 40%. The number of chromosomes is the same as
tine, Syria, Tunisia, etc. In northern Argentina, it is in the neem tree, n=14.
planted for firewood and timber production. In
Uganda, Kenya, and South and West Africa, it is
planted as a drought resistant ornamental and Phytochemical Properties
shade tree. Although the chinaberry tree is a native
to tropical Asia, it is now widely distributed in dry More than 280 limonoids have been isolated and
regions of the southern and western United States. identified from Meliacae plants. The most active
In some parts of the southern USA, M. azedarach is constituents of M. azedarach are classified as
regarded as an invasive plant because its seeds are azadirachtin-type C-seco limonoids and apo-eup-
rapidly spread by birds. hol limonoids as trichilins with a 14,15-epoxide
and a C-19/C-29 lactol bridge.
The limonoid azadirachtin is absent from M.
Botanical Characteristics azedarach; it exists only in Azadirachta sp. The
toxic tetranortriterpenoids (meliatoxins A1, A2, B1,
Melia azedarach L. is a tree reaching up to 30 m B2) were isolated from the fruit of M. azedarach.
(about 90 ft), with a thick trunk, spreading branches Meliatoxin A2 was found to be identical to A1
and furrowed bark. Chinese and Indian cultivars except that ester moiety at C-28 is 2-methylpropi-
usually attain a height of 815 m whereas in cer- onyl in place of the 2-methylbutanoyl group in A1.
tain areas in the Southern Hemisphere, such as Meliatoxins B1 and B2 are isomeric with A1 and A2,
Sri Lanka, Malaysia and Indonesia, the tree may respectively except the epoxide ring in B1 and B2
reach 2530 m. The blossoming time is March- is replaced by a 5-member ring ketone at C-15.
May in the Northern Hemisphere, but some forms The chemical structure of the meliatoxins differs
blossom throughout the summer or even the whole from trichilin, only in the lack of the hydroxyl
year round. The flowers are fragrant, are purplish substituent at C-12.
or lilac, in long peduncles and axillary panicles Using bioassay guided fractionation and isola-
which are shorter than the leaves and areglabrous tion technique, the principal insecticidal constitu-
or sparsely puberulent. The bi- to tri-pinnate alter- ents of M. azedarach were isolated from methanolic
nate leaves are usually up to 45 cm (13 ft) long, extracts of green chinaberry fruits and were found
while in young trees often longer (<1m). The leaf- to be two very potent insecticidal tetranortriterpe-
lets are ovate and elliptic to lanceolate, acute, noids. These terpenoids include novel meliacin,
sharply serrate or lobed or have a crenate to serrate called 1-cinnamoyl melianone, and a new de
margin and are 1.25 cm (12 in) long. Leaf shedding rivative of meliacarpine called 1-cinnamoyl-3,
852
C Chinaberry, Melia azedarach L., A Biopesticidal Tree

1 1-dihydroxymeliacarpin. Azadirachtin analogs Production of Meliaceous Trees

were found in M. azedarach fruit extracts. These
isolated compounds were 1-cinnamoyl-3-feruloyl- The trees are easily propagated both sexually and
11-hydroxymeliacarpin, 1-cinnamoyl-3-feruloyl-11- vegetatively. They can be reproduced using seeds,
hydroxy 22, 23-dihydro-23--methoxymeliacarpin, seedlings, saplings, root suckers or cuttings.
and 1-tigloyl-11-methoxy-20-acetylmeliacarpine. Clean seeds, without the pulp, are planted in
Other limonoids that have been found in M. aze- nurseries in prepared plastic sacks. Germination
darach are: azedarchol, nimbin, santonum, sandola- takes place after 815 days, depending on temper-
ctone, ochinal and ochinine actetate, sandanol, ature and water supply. Shade usually is not
melianone, mellanin, melianol and many others required, but a partially shaded nursery may be
such as flavonoids, melianoninol, meliandiol, vanil- advantageous. Ordinary seeds are ready for trans-
lic acid, vanillin and toosendanin. It was found that planting in 12 weeks, when they reach a height of
saponification of the oil from green berries of M. 7.510 cm and their taproot is approximately 15
azedararch yielded 65% linoleic acid and approxi- cm long. Transplanting is done during the rainy
mately 20% oleic acid. Apart from palmitic and season with a high survival rate. It has been
stearic acid, only very low quantities of other fatty reported that trees produced through seed germi-
acids, saturated or unsaturated, were also detected. nation exhibit considerable variation. Hence, tis-
The limonoids salanin and volkensin were isolated sue culture technology was adopted to raise
from the fruits of M. volkensii. uniform plantation permitting multiplication of
Salanin, meldenin and a limonoid glycoside, superior genotypes.
established as 6-acetoxy-11-hydroxy-7-oxo-14-
epoxymeliacin-1,5-diene-3-O-L-rhamnopyraside,
were isolated from 5 kg of powdered M. azedarach Medicinal and Other Uses
seeds extracted in 30 l of ethanol. M. azedarach
leaves were also found to contain santonum, Melia azedarch is a medicinal plant used in East-
melianone, sandolactone, ochinal and ochinine ern medicine. It has been used in many places for
acetate and 1-cinnamoyl melianone. Rutin and the treatment of a variety of human disorders. On
3-O-L rhamnoside were isolated from M. aze- the Island of Maritius and in China, an extract of
darach in India. The two flavonol diglycosides, the bark is used as an antihelminthic. In Algeria,
rutin and kaempferol-3-O- rutinoside, were also the plant is used as a tonic and antipyretic, and in
isolated in high yields from the leaves of M. aze- South Africa, it is used for the treatment of leprosy,
darach in Spain. eczema and the relief of asthmatic attacks. In Asia,
Three trichilin type limonoids with the three leaves are used as an antipyretic while the leaves,
known limonoids, trichilins B and D and melia- fruits and bark are used as an antihelminthic, how-
toxin A2, were isolated from ether-extracted root ever, certain forms are known to be poisonous to
bark of the Chinese M. azedarach L., namely humans and livestock. The oil of M. azedarach is
trichilin H, 12-acetyltrichlin B, and 7,12 diacetyl- also used as an antihelminthic and antiseptic.
trichilin B. A biogenetically interesting ring-C seco Ripe fruits are known to be more toxic to
limonoid, salannal, and a potent insect antifeed- mammals than green ones. Leaves seem to be less
ant, meliacarpine E, were also isolated from the toxic, as they are used as fodder for goats in India.
root bark of the Chinese M. azedarach, along with It was reported that children have died after eating
four other seco-limonoids, salanin, deacetyl sala- six to eight ripe fruits. Records also show that
nin, nimbolinin B, and nimbolidin B. Sandanol, M.azedarach is toxic to livestock, commonly affect-
melianol, mellanine A, and meldenin were isolated ing pigs, but the poisoning of cattle, sheep, goats
from the seeds. and poultry has been reported with symptoms of
 Chinaberry, Melia azedarach L., A Biopesticidal Tree
C 853

nausea, vomiting, constipation or scouring, often M. azedarach leaves were found to retard the
with blood. It was found that the approximate oral growth of first instar larvae of the corn earworm
LD50 values of purified ethanolic solutions of the Heliothis zea and the fall armyworm Spodoptera
meliatoxins attributed to be the cause of high tox- frugiperda. At a concentration of 30 mg-eq/g diet
icity to pigs, was 6.4 mg/kg. Meliatoxins A1, A2, B1 fed to test larvae, 100% mortality occurred and
and B2 have been shown to be responsible for the larvae died before pupation, retarding develop-
acute nervous system dysfunction and death in ment in both insect species. Significant weight
pigs. Toxicity may vary with location and stage of reduction in larvae was observed due to feeding
growth and may be entirely absent in some trees. deterrence of the extract.
Melia azedarach provides a multipurpose, Aqueous extracts of M. azedarach applied
termite-resistant heartwood which is used for tea- on bean plant leaves interfere with the longevity
boxes, furniture, ceilings and other building pur- and development of adults and immature stages of
poses. The white cedar leaves in Australia are B. tabaci. The interference of the extract, in a field
used by aborigines as a fish poison. test, reduced transmission of viruses by 4560%
compared to control plants. This was attributed to
the phago-deterrent effect of the plant extract
Bioactivity of the Melia azedarach against adults. Toxicity of aqueous emulsions of
Tree Against Insects M.azedarach fruits prepared from 5% solutions in
acetone containing also Triton X-100 (0.5%) against
Persian lilac trees remained unharmed during adults of Sitotroga cerealella was approximately
severe invasion by the desert locust Schistocera 0.2% that of malathion, and activity of 4-day-old
gregaria both in Palestine in 1915 and during the residues was 2040%. The extract lost its toxicity
locust plague in India in 192627. It was proposed nearly totally by the 8th day after the spray.
that M. azedarach does not kill acridids but repels Fruit and leaf extracts of M. azedarach showed
them for several days and is unpalatable to Schisto- a comparable and potential repellent effect against
cerca gregaria. B. tabaci adults. Fruit and leaf aqueous extracts
In Punjab, leaves of M. azedarach used as soil caused a significantly lower number of live adult
treatment at a rate of 7 tons/acre reduced the ter- whiteflies to be encountered on treated bean leaves
mite attack on wheat to 0.7% as compared with 8% than the control after 24 h, regardless of whether
in untreated plots. these plant parts were crushed or boiled in water.
M. azedarach is not a good host for the sweet- M. azedarach aqueous extracts at the rate of 1:5
potato whitefly, Bemisia tabaci (Gennadius). Host (w/v) caused a possible antifeedant action against
preference bioassays indicated a significantly lower adult B. tabaci as indicated by fewer eggs laid by
number of live whiteflies on the leaves of the chin- treated adults and fewer pupae produced.
aberry tree versus the leaves of beans, cucumbers, The growth of 2nd and 4th larval instars of
and tomatoes after 24 h. the oak processionary caterpillar Thaumetopoea
processionea, was retarded after being sprayed by
an enriched M. azedarach fruit extract; and after 4
Bioactivity of Extracts of Melia days of spraying, the larvae became quite lethargic.
azedarach Even with lower concentrations of 0.01%, mortal-
ity of 100% was attained within a period of 12
Leaf extracts of M. azedarach protected plants weeks. Death was mainly caused by moult disrup-
against locust feeding and the activity was found tion because the larvae were not able to shed the
to be higher in these extracts than in pulp and the old exuviae. Younger larvae were more sensitive to
very small seed kernels. Chloroform extracts of the plant extracts than older ones.
854
C Chinaberry, Melia azedarach L., A Biopesticidal Tree

The Melia fruit aqueous extract significantly alates in choice experiments from ovipositing on
lowered the number of larvae of the pea leafminer, treated Vicia faba plants.
Liriomyza huidobrensis (Blanchard), per Swiss Adults of B. tabaci were significantly more
chard plant as compared to the control, at 15 days repelled from tomato plants treated by the undi-
after first spray when two consecutive sprays were luted methanol, acetone or water extracts when
performed under field conditions. The Melia fruit compared to the control after 72 h. There were sig-
extract significantly decreased the number of live nificant differences in percent mortality (23.0
larvae per cucumber leaf compared to the control, 48.9%) of nymphal instars when exposed to the
10 days after each spray under greenhouse condi- undiluted extracts compared to the other diluted
tions. Melia fruit extracts and cyromazine caused extracts and the control. M. azedarach leaf and
the formation of deformed larvae which were fruit extracts were found to be repellent to the
partially brown rotted and oozing. This indicates whitefly adults, while the fruit extracts specifically
that the fruit extract may have a growth-regulating have shown a significant detrimental effect against
activity similar to that of cyromazine, a triazine early nymphal instars. The undiluted methanol
insect growth regulator selective to the genus extracts caused a very low number of live adult
Liriomyza. The aqueous leaf extract was found to whiteflies on treated plants in comparison to the
keep the number of live larvae per leaf at a signifi- undiluted water and acetone extracts. This indi-
cantly lower density than the control only at 20 cates that methanol seems to extract more of the
days after the second treatment application. This bioactive components from Melia compared to
indicates that the leaf extract might need a longer that of acetone or water. Similarly, aqueous and
period of time to reveal its effect. Increasing the methanol extracts of leaves, fruits and callus of
number of consecutive sprays enhances the activ- M. azedarach have shown significant repellent
ity of these extracts under field conditions due to activity of 58.967.7% and have decreased signifi-
the known ultraviolet degradation of botanical cantly the oviposition rate of the insect without
extracts. affecting the adult whitefly emergence compared
The activity of mixed function oxidases in the to the control. Extracts of frozen samples were
midgut of 5th-instar larvae of Pieris rapae was found to be as effective against the pest as fresh
reduced to half its value after feeding on toosenda- samples, thus allowing storage of Melia parts to be
nin, an extract from the bark of M. azedarach used incase of shortage. The antifeedant action of
or M. toosendan. Esterase activity in the midgut theM. azedarach extract was observed and it was
was also markedly reduced, but not in the found that the rate of adult mortality of B. tabaci
hemolymph. on plants sprayed with M. azedarach leaf or fruit
Simple preparations from M. azedarach extracts (1:5, w/v) were not significantly different
include: drying of the fruit, milling of the seeds, from the mortality rate when B. tabaci were kept
preparation of aqueous extracts, and of a seed dust unfed.
diluted with 25% zeolite. The main pests controlled The two highest concentrations: 10,000 and
by these preparations were: S. frugiperda, 2,000 ppm of the ethanol extract of fruits of M.
Spodoptera sp., B. tabaci, Plutella xylostella, Mocis azedarach were incorporated into artificial diet of
latipes, Diaphania sp., Herse cingulata, H. virescens, the fall armyworm, S. frugiperda. This caused 100%
Sitophibus oryzae, Cyclas formicarius elegantulus, mortality of the insect before pupation, but the
Aphis gossypii and Myzus persicae. hexane extracts tended to be less effective. Treated
Methanolic extracts of M. azedarach of high larvae showed significant weight loss and delay in
concentrations (25% and 12.5%) caused about the time needed for pupation. Ethanol extracts of
100% mortality of A. fabae nymphs within 4 days. the fruits of M. azedarach containing 32mg/100ml
Extracts of 25%, 12.5%, and 1.25% also deterred caused 97%98% mortality of the cabbage aphid,
 Chinaberry, Melia azedarach L., A Biopesticidal Tree
C 855

Bervicoryne brassicae in 48 h. Ethanol seed kernel citrus red mite, Panonychus ulmi on citrus. The
extract of M. azedarach inhibited feeding of the chinaberry seed oil is also highly toxic to the For-
rice noctuid Spodoptera abyssina by 99.8%. mosan subterranean termite.
Petroleum ether extracts of M. azedarach fruits
are strong antifeedants against nymphs of the brown
planthopper, Nilaparvata lugens. Rice plants treated Bioactivity of Melia azedarach
with a hexane extract of M. azedarach were not only components against insects
repellent to adults of the green rice leafhopper,
Nephetettix nigropictus, and the macropterous Meliatoxins and trichilin type limonoids were
brown planthopper in choice test against control found to be antifeedants against certain insect
plants, but they also reduced the feeding time of the pests. Meliatriol isolated from fruits of M. aze-
insects. Petroleum-ether extract (2%) of both Melia darach showed strong antifeedant properties
toosendan and M. azedarach caused respectively against 5th instar of the desert locust Schistocerca
100% and 89.5% feeding deterrence of third-instar gregaria Forsk. Meliatine, an exceedingly bitter
larvae of Spodoptera litura. substance isolated from the leaves of M. azedarach,
The petroleum-ether, ethanol and methanol was found to effectively protect crop leaves against
extracts of M. azedarach and M. toosendan seed the locust attack.
kernels have bioactivity against several insect pests The steroid, estrer azaderachol, isolated from
such as the rice yellow stem borer Schirpophaga the ether extract of the root bark of M. azedarach
incertulas, the fifth instar of the cabbage butterfly var. japonica, showed antifeedant activity against
Pieris rapae, the female rice gall midge Orseolia larvae of Agrotis segetum. The antifeedant prop-
oryzae, the citrus leafminer Phyllocnystis citrella, erties of M. azedarach constituents: salannal,
the polyphagous beetle Anomala cupripes, and meliacarpine E, salanin, deacetyl salanin, nim-
the Asiatic corn borer Ostrinia furnacalis. High bolinin B and nimbolidin B were examined with
oviposition deterrence and reduction of adult the larvae of Spodoptera eridania. Meliacarpinin
emergence of the rice hispa and the pulse beetle E showed the most potent activity at 50 ppm,
was detected when exposed to leaf or seed extracts similar to meliacarpinins A-D. Other C-seco
of Chinaberry. limonoids showed only weak activities at 500
The food intake of newly emerged females 1000 ppm. Three trichilin type limonoids from
of the brown planthopper, and the whitebacked the ether extract ofthe root bark of the Chinese
planthopper, Sogatella furcifera, on rice plants M. azedarach L., namely trichilin H, 12-acetyl,
sprayed with M. azedarach seed oil, was reduced and 7,12 diacetyltrichilin B. were found to be
starting from the dosage of 5 mg/plant. The 32P antifeedants active against the Japanese pest
isotope tracer technique was used to verify the Spodoptera exigua.
antifeedant effect of M. azedarach seed oil emul- Meliatoxin A2 isolated from the fruit of
sion against the citrus aphid, Aphis citricola. The M.azedarach induced a significant level of anti-
nymphal period of the cicadellid Nephotettix feedant activity against Spodoptera lituralis lar-
nigropictus was prolonged and mortality was vae, while the meliatoxin B1, lacking the epoxide
obtained when the insects were fed on seedlings ring, was much less active. The salannins and
treated with the oil extract. salannols isolated from M. azedarach have shown
The 0.5% emulsified seed oil extract of M. aze- antifeedant activity toward the Mexican bean
darach gave good control of the orange spiny beetle.
whitefly, Alevrocanthus spiniferus (Quaintance), The two tetranortriterpenoids: 1-cinnamoyl
and its efficacy was comparable to that of the potent melianone and 1-cinnamoyl-3, 11-dihydroxymeli-
acaricides amitraz or cyhexatin in controlling the acarpin were found to have growth inhibitory
856
C Chinaberry, Melia azedarach L., A Biopesticidal Tree

effects for first instar larvae of the Lepidoptera of Melia leaf or fruit. The synthesis of secondary
Heliothis viriscens and S. frugiperda. Other highly plant compound(s) in such undifferentiated cells
oxidized tetranorterpenoids that are azadirachtin ofMelia is clearly occurring. It may be possible to
analogs have impaired metamorphosis of the enhance production of meliaceous allelochemicals
Mexican bean beetle, Epilachna varivestis. in tissue cultures to the extent that culture extracts
could eventually be used for production of botani-
cal insecticides. As an alternative to harvesting an
Integration With Natural Enemies ecologically important tree, cell-culture systems can
be used to provide a continuous supply of those
Adults of the predator Coccinella septempunctata biopesticidal extracts through the propagation of
showed no mortality after being allowed to con- Melia all year round and using them easily and
sume adults of the mustard aphid, Lipaphis erysimi, conveniently.
that had been exposed for 5 h to mustard leaves The different ecotypes of M. azedarach are a
treated with 1.5% alcoholic extract of the drupe of potential natural resource that can be utilized, as
M. azedarach. raw material and extracts, in low-input agroeco-
Leaves infested with Epilachna vigintioc- systems. Cultivation of this meliaceous tree is an
topunctata, and treated with a petroleum ether economically feasible practice, as it is usually
extract of the drupes of M. azedarach, were less planted as a common shade tree. The efficacy of
parasitized by Pediobius foveolatus than the con- M.azedarach extracts might be enhanced by inves-
trol. However, on exposure to parasitization 24 h tigating the timing and frequency of application of
after treatment, larvae were parasitized normally the plant extracts on crops for management of
and the parasites that emerged from treated hosts major economical agricultural pests. These extracts
were normal. could provide a relatively inexpensive and readily
M. azedarach oil did not affect the survival available insecticide to combat the pest resistance
and behavior of the larvae of Coccinella to insecticides.
undecimpunctata, but there was prolongation of Botanical Insecticides
the fourth larval instar while the Aphis gossypii
aphid consumption was unchanged. The oil of
M.azedarach seeds was found to be only slightly References
toxic against the predatory mirid bug Cyrtorhinus
lividipennis and non-toxic against the spider Abou-Fakhr Hammad EM, Zournajian H, Talhouk S (2001)
Efficacy of extracts of Melia azedarach L. callus, leaves
L. pseudoannulata, natural enemy of the white-
and fruits against adults of the sweetpotato whitefly
backed planthopper, Sogatella furcifera, the brown Bemisia tabaci (Hom. Aleyrodidae). J Appl Entomol
planthopper, N. lugens, and the green leafhopper, 125:425488
Nophotettix virescens. A massive dosage of the seed Ascher KRS, Shmutterer H, Zebitz CPW, Nagvi SNH (1995)
The Persian lilac chinaberry tree: Melia azedarach L. In:
oil of M. azedarach applied topically to the wolf Schmutterer H (ed) The neem tree. VHC Publishers,
spider Lycosa pseudoannulata, a natural enemy of New York, NY, pp 602642
the brown planthopper, Nilaparvata lugens, had no Kraus HS, Baumann M, Bokel U, Klenk A, Klingele S, Pohnl
effect on the spider. M, Schwinger M (1987) Control of insect feeding and
development by constituents of Melia azedarach and
Azadirachta indica. In: Schmutterer H, Ascher KRS
(eds) Natural pesticides from the neem tree and other
Potentials in Sustainable Systems tropical plants. Proceedings of the Third International
Neem Conference, Rauiscchholzhausen, Germany, pp
111125
Extracts of tissue culture of Melia have shown repel- Lee MS, Klocke JA, Barnby MA, Yamasaki RB, Balandrin MF
lency to different insect species similar to extracts (1991) Insecticidal constituents of Azadirachta indica
 Chinch Bug, Blissus leucopterus (Say) (Hemiptera: Blissidae)
C 857

and Melia azedarach (Meliaceae). In: Hedin PA (ed)

Naturally occurring pest bioregulators, ACS Sympo-
Chinch Bug, Blissus leucopterus
sium Series 449, pp 293304 (Say) (Hemiptera: Blissidae)
Nakatani M, Huang RC, Okamura H, Naoki H, Iwagana T
(1994) Limonoid antifeedant from Chinese Melia John l. Capinera
azedarach.Phytochemistry 36:3941
University of Florida, Gainesville, FL, USA
Nardo EAB, De Costa AS, Lourencao AL (1997) Melia aze-
darach extract as an antifeedant to Bemisia tabaci
(Homoptera: Aleyrodida). Fla Entomol 80:9294 The chinch bug, Blissus leucopterus, is found
Oelrichs PB, Hill MW, Valley OJ, Macleod JK, Molinski TF through much of the eastern United States and
(1983) Toxic tetranortriterpenes of the fruit of Melia
azedarach. Phytochemistry 22:531534
southern Canada, west to about the Rocky
Tewari GC, Moorthy PNK (1985) Plant extracts as antifeed- Mountains. However, it is absent from the Gulf
ants against Henosepilachna vigintioctopunctata (Fabr- Coast region, where it is replaced by a closely
icius) and their effect on its parasite. Indian J Agr Sci related species, the southern chinch bug, Blissus
55:120124
insularis Barber. The two species have overlap-
ping ranges in portions of the southern states
from North and South Carolina through cen-
China, William Edward tral Georgia and west to Texas. Southern chinch
bug feeds only on lawn and forage grasses,
William China was born in London on Decem- particularly St. Augustine grass, and is not a
ber 7, 1895. His university education was in Lon- food crop pest. Other species of Blissus occur
don and Cambridge, but was interrupted by in both eastern and western states but they
World War I. In that war, he served in France, first are of little consequence. The Blissus spp. may
in the British army, later in the Royal Air Force. have dispersed northwards from South Amer-
He returned to Cambridge University and earned ica, but ifso they apparently dispersed in pre-
a degree in zoology. In January 1922, he was colonial times, as there is no record of their
appointed assistant in the Department of Ento- introduction.
mology of the British Museum (Natural History), The range of B. leucopterus can be subdi-
in 1930 assistant keeper, and eventually in 1955, vided because two discrete subspecies exist; B.
keeper. His subject of research was the taxonomy leucopterus hirtus Montandon in the northeast,
of Hemiptera, in which he eventually published and B. leucopterus leucopterus (Say) in the cen-
265 papers, describing 98 new genera and 248 tral region of the eastern states. In eastern Can-
species. During World War II, he was deeply ada, the New England states, and south to about
involved in temporarily moving the national northern Virginia and eastern Ohio, the north-
insect collections out of London to prevent dam- eastern form, B. leucopterus hirtus, is a pest of
age or loss. His research resulted in his award in lawn grasses, but not of food crops. This sub-
1948 of a D.Sc. degree by Cambridge University. species is also called hairy chinch bug to dis-
He retired in 1970 to a little fishing village in the tinguish it from the food crop-attacking
county of Cornwall, where he died on September subspecies, B. leucopterus leucopterus, which is
17, 1979, survived by his wife Lita and three known simply as chinch bug. Chinch bug
children. occurs from Virginia to Georgia in the east,
extending to South Dakota and Texas in the
west. Chinch bug generally is not damaging
Reference throughout its entire range, and is considered to
be a pest mostly in the midwestern and south-
Knight WJ (1980) Obituary and bibliography. Entomologists western states from Ohio in the east to South
Monthly Magazine 115:164175 Dakota and Texas in the west.
858
C Chinch Bug, Blissus leucopterus (Say) (Hemiptera: Blissidae)

Life History in the third instar, but are difficult to discern. In

the fourth instar the wing pads extend about half
There are at least two generations per year the width (Fig. 47) of the first abdominal seg-
throughout the range of B. leucopterus leucop- ment. In the fifth instar the wing pads extend to
terus. The first generation commences in the the third abdominal segment. The nymphal body
spring with oviposition by overwintering adults, lengths are about 0.9, 1.3, 1.6, 2.1, and 2.9 mm for
usually in April or May. The second generation instars 15, respectively. Nymphs prefer to feed
begins in JuneAugust. Second generation adults in sheltered locations such as curled leaves and
overwinter, often in the shelter of clump-forming on roots, but are often found aggregated on the
wild grasses, dispersing in the spring to early- stem near the base of the plants. When not feed-
season crops, and then in early summer to later- ing they may hide under clods of soil and rub-
developing crops where the second generation bish, or in loose soil.
develops. Generations overlap considerably due The body and legs of the adult are blackish in
to prolonged oviposition, and in the southwest- color (Fig.48). The wings of B. leucopterus leucop-
ern states there is some evidence of a third gen- terus nearly attain the tip of the abdomen, and are
eration. A complete life cycle can occur in 3060 white in color with a pronounced blackish spot
days. found near the center and outer margin of the
The elongate-oval eggs are rounded at one
end, truncate at the other, and measure about 0.85
mm long and 0.31 mm wide. The truncate end
bears three to five minute tubercles, 0.1 mm in
length. The eggs are whitish initially, turning yel-
lowish brown after a few days and reddish before
hatching. Eggs are deposited in short rows at the
base of the plant on roots, on the lower leaf sheaths
and stems, and on the soil near the plant. Females
deposit eggs at a rate of 1520 per day over a 23
week period, producing up to 500 eggs. Duration
of the egg stage is about 16 days at 27C and 8 Chinch Bug, Blissus leucopterus (Say) (Hemiptera:
days at 31C. Blissidae), Figure 47 Adult of chinch bug, Blissus
There are five instars. Duration of the instars leucopterus (Say).
is about 5, 6, 5, 4, and 6 days for instars 15,
respectively, when reared at 29C. Under field
conditions, the development time may be
extended, with a developmental period of about
3040 days normal, and 60 days not unusual.
During the early instars, the head and thorax are
brown, the legs pale. These structures become
darker as the nymphs mature, so that the mature
nymph is blackish. The first two segments of the
abdomen are yellowish or whitish, the remainder
red except for the tip of the abdomen, which is
black. The reddish abdomen becomes progres- Chinch Bug, Blissus leucopterus (Say) (Hemiptera:
sively darker, however, appearing almost black at Blissidae), Figure 48 Fourth instar of chinch bug,
nymphal maturity. The wing pads become visible Blissus leucopterus (Say).
 Chinch Bug, Blissus leucopterus (Say) (Hemiptera: Blissidae)
C 859

forewings. The adult measures 3.54.5 mm in The most important natural mortality factor
length. In the related form called hairy chinch bug, is fungal disease, particularly Beauveria bassiana.
the wings generally are abbreviated, usually not Interestingly, this fungus was intensively redistrib-
extending beyond the middle of the abdomen. uted, particularly in Kansas, during the late 1880s
Hosts of chinch bug consist solely of plants in in an effort to increase suppression. However, it
the family Gramineae, but include both wild and eventually became apparent that the disease spread
cultivated grasses. It is known principally as a pest naturally, and that the effectiveness of the fungus
of such grain crops as barley, corn, millet, oat, rye, was related more to weather than to the efforts of
sorghum, and wheat, but oat is only marginally agriculturalists and entomologists to foster epi-
suitable. However, it also damages forage grasses zootics. The fungus is invasive and pathogenic at
including sudangrass and timothy, and feeds on relative humidities of at least 30100%, but fungal
wild grasses such as foxtail, Setaria spp.; crabgrass, replication and conidia production require humid-
Digitaria spp.; and goosegrass, Elusine indica. ities of at least 75%. Clumps of such bunch grasses
Females select sorghum for oviposition over as little bluestem, Andropogon scoparius, serve to
wheat and corn; barley is intermediate in prefer- harbor not only overwintering bugs, but Beauveria
ence. Crop suitability, as measured by develop- as well, and may be important in initiating fungal
ment time, is similar to oviposition preference. epizootics. The food plant of the chinch bug affects
Numerous natural enemies have been observed. susceptibility to B. bassiana, with a diet of corn
Among avian predators feeding on chinch bugs are and sorghum suppressing fungus development
common birds as barn swallow, Hirundo erythrogas- and bug mortality.
tra Boddaert; horned lark, Otocoris alpestris (Lin- Weather has significant impact on chinch
naeus); meadowlark, Sturnella magna (Linnaeus); bugs. The overwintering period is moderately crit-
redwinged blackbird, Agelaius phoeniceus (Linnaeus); ical. Adults seek shelter in stubble and debris, but
and kingbird, Tyrannus tyrannus (Linnaeus). Insect one of the most favorable locations is among the
predators of special importance are insidious flower stems of bunch grasses. Bunch grasses provide
bug, Orius insidious (Say) (Hemiptera: Anthocori- food in the autumn before the onset of winter
dae), an assassin bug, Pselliopus cinctus (Fabricius) temperatures, and again in the spring before it is
(Hemiptera: Reuviidae), and various ants (Formici- consistently warm and the bugs disperse. Bunch
dae). Ladybird beetles (Coleoptera: Coccinellidae) grasses also serve to break the wind by reducing
and lacewings (Neuroptera: Chrysopidae) frequently desiccation and the severity of the wind, and by
have been observed on plants infested with chinch keeping excessive rainfall from the insects. Thus,
bugs, but their effects are uncertain. in the absence of bunch grasses or similar shelter,
Parasitoids are sometimes found in these survival can be poor. Heavy snow cover is favor-
small insects, but rarely are they considered to be able, keeping the bugs warmer and sheltered from
significant mortality factors. An egg parasite, the drying wind.
Eumicrosoma benefica Gahan (Hymenoptera: Sce- Summertime weather is perhaps even more
lionidae), the nymphal or adult parasite Phorocera critical. Chinch bugs thrive in warm, dry condi-
occidentalis (Walker) (Diptera: Tachinidae), and tions, at least in the midwestern states. Heavy
an unspecified, naturally occurring nematode have rainfall can kill many bugs, and wet, humid
been reported. The egg parasitoid, which is found weather fosters epizootics of fungal disease. In
throughout most of the range of the chinch bug the southwest the situation is different because
and is active during much of the season when dry weather is usually assured, but the absence
chinch bug occurs, was reported to parasitize up ofsummer rain causes premature senescence of
to 46% of the eggs in Nebraska, so it may be of plants, depriving bugs of green food late in the
considerable value in biological control. summer.
860
C Chironomidae

Damage Cultural practices that promote dense growth

and shade will increase humidity and decrease
Chinch bug is a plant sap-feeding insect, causing a chinch bug numbers. Thus, fertilization and irriga-
reddish discoloration at the site of feeding and tion can be detrimental to chinch bug survival.
death of that portion of the plant. Plant growth There is considerable difference among crops in
can be stunted, or plants killed when fed upon by susceptibility to injury, and within crops the level of
large numbers of bugs. Their destructiveness is resistance also is variable. Measurable levels of differ-
attributable, in part, to their gregarious nature. Not ence in bug longevity and development occur when
only do large numbers aggregate on certain plants, they feed on different varieties of wheat, though there
but they also disperse in tremendous numbers is not a practical level of resistance. In contrast, a
from field to field. When plants are infested while resistant variety of sorghum has been identified, and
young, they suffer more damage than if infested there is considerable resistance in grain corn.
later in growth. Turfgrass Insects and their Management
Vegetable Pests and their Management

Management
References
Granular and liquid insecticides are used to pro-
tect plants, particularly plants that are invaded by Leonard DE (1968) A revision of the genus Blissus (Het-
eroptera: Lygaeidae) in eastern North America. Ann
nymphs or adults dispersing from senescent early- Entomol Soc Am 61:239250
season crops. Systemic insecticides can be applied Swenk MH (1925) The chinch bug and its control. Nebraska
at planting time, and either contact or systemic agricultural experiment station circular 28, 34 pp
materials after the crop has emerged from the soil.
Liquid insecticides should be directed to the base
Chironomidae
of the plants, a location favored by the insects.
Historically, most damage occurred when
A family of flies (order Diptera). They commonly
early-season small grain crops matured, and large
are known as midges.
numbers of first generation nymphs dispersed by
Flies
walking to adjacent crops, usually corn. This was
combated by erecting barriers, usually in the form
of a ditch, between crops. Also, some destruction Chironomids as a Nuisance and of
of overwintering bugs in wild grasses was accom- Medical Importance
plished by burning, though it was rarely more than
50% effective. These practices are largely obsolete, Meir Broza
and insecticides are now used effectively. However, University of Haifa, Haifa, Israel
it remains advisable to rotate among susceptible
and nonsusceptible crops, and to grow susceptible Chironomids, the non-biting midges (Diptera:
crops in isolation from alternate hosts. Because Chironomidae) are one of the most important
the combination of small grains and corn leads to groups of insects worldwide in freshwater, aquatic
damage by chinch bugs, it may be desirable to ecosystems. Chironomids can be found on all con-
eliminate one of these crops and thereby eliminate tinents, including Antarctica. They are abundant
an important food from the chinch bug life cycle. in terms of the number of species that are known
In southern states the crop sequence is different, to exist (estimated number between 15,000 and
with both wheat and corn invaded by overwinter- 20,000), their relative biomass or both. They play
ing bugs early in the season. an important role in the decomposition process.
 Chironomids as a Nuisance and of Medical Importance
C 861

Large populations of midges with densities

amounting to several thousand larvae/m2 (usually
on the floor of freshwater habitats) have been
reported. They are a source of economic burden,
nuisance, and health problems. Large midge popu-
lation densities create conflict with nearby human
settlements. This phenomenon is recognized
worldwide, in the United Kingdom, United States,
Japan, Italy, Spain, Israel, New Zealand and Sudan.
Chironomidae (particularly Chironomus)
emerging from polluted natural and man-made
aquatic habitats, near or in urban districts, can
become intolerable (Fig. 49). During the spring
and midsummer, evening breezes carry large
swarms of adult midges to nearby cities and com-
munities where they can become a severe nuisance
to the residents. Adult midges are most active dur-
ing the evening and they may enter the mouth,
eyes and ears, thus limiting evening activities out-
doors and indoors. In 1998, a population estimated
at 4050 billion individuals/night emerged from
200 acres of waste stabilization ponds near Tel
Aviv, Israel. Such swarms may be economically
important due to the damage they can cause to
vessels, pumps and aeroplane engines.
Chironomid larval populations (red-worms)
contaminate municipal drinking water supply
systems. This problem has been reported in the
United Kingdom since the 1970s, in the U.S.A.,
Israel and elsewhere. In both the U.K. and U.S.A., the Chironomids as a Nuisance and of Medical
chironomid inhabiting the water systems was Importance, Figure 49 Nuisance midges: above,
identified as the parthenogenetic species Para- Chironomus sp. female (left) and male (right);
tanytarsus grimmi. After entering the pipe system, below, accumulation of midges on an automobile
the pupal stage circulates in the water and may after only a few minutes of travel.
produce egg masses without emerging as airborne
adults. Because pesticides cannot be used in a such accumulations, greater amounts of energy
water supply, a food-grade coagulant and water may be needed for water transport.
disinfectant were suggested as control agents. Many insect vectors of serious human dis-
Besides the unacceptable appearance of red- eases are flies. This includes nematoceran flies in
worms in the water supply, the larvae also may which the females feed on a vertebrate blood meal.
cause technical problems by blocking water filtra- Chironomids are non-biting midges, and it may
tion systems. In countries where recycled water seem surprising to find that they are of medical
is used for irrigation, the larvae may adhere to significance. However, they are now recognized as
the inner surface of pipes and contribute to the causing severe allergic reactions in humans. The
build-up of biofilm on these surfaces. As a result of most thoroughly investigated case of an allergic
862
C Chitin

disease associated with chironomids comes from Broza M, Halpern M, Teltsch B, Porat R, Gasith A (1998)
Shock chloramination: a potential treatment for
the Sudan. People living south of the Aswan Dam
Chironomidae (Diptera) larvae nuisance abatement in
suffer from the mass emergence of chironomids water supply systems. J Econ Entomol 91:834840
from Lake Nasser. In the dry winds, large numbers Broza M, Halpern M (2001) Chironomids egg masses and
of dead insects are blown into the air, causing Vibrio cholerae. Nature 412:40
allergic reactions such as asthma and rhinitis. The
town of Wadi Halfa located near Lake Nasser has
been particularly plagued since the building of Chitin
thedam on the Nile. A few cases also have been
reported from the U.S.A. For example, an employee A tough insoluble structural polysaccharide mate-
at a hydroelectric plant in Alabama developed rial that comprises variable portions of the insect
seasonal hay fever in response to the mass emer- cuticle. It is a water-insoluble polysaccharide that
gence of chironomids from the dam. It has been forms the exoskeletons of arthropods, and is one
shown that chironomid larval hemoglobin, which of the most widely occurring polysaccharides in
contaminates adults during metamorphosis, is a nature. Chitin molecules are long-chain sugars
potent human allergen. It is believed that midges consisting of N-acetyl-glucosamines attached
are potentially the cause of many allergic reactions together with beta-glucosidic linkages.
worldwide.
As well as causing allergies, midges may play
a role in the maintenance and transmission of Chitinase
infectious diseases. Chironomid egg masses have
been reported to serve as a natural reservoir for An enzyme that degrades chitin.
the cholera bacterium, possibly raising the chi-
ronomid problem from a nuisance level to a life-
threatening hazard. Cholera is a severe diarrheal Chitinous
disease that kills thousands of people each year
and affects the lives of millions of others. The dis- Consisting of, or containing, chitin.
ease is caused by the bacteria Vibrio cholerae,
which is pathogenic to humans only. At present,
the disease is most common in the Indian subcon- Chittenden, Frank Hurlbut
tinent and less developed countries in Asia, Africa
and South America. Frank Chittenden was born in Ohio on November
3, 1858, and grew up in a small town there. He
studied entomology at Cornell University. Next, he
References worked at the Brooklyn Museum and was one of
the founders of the Brooklyn Entomological Soci-
Ali A (1994) Pestiferous Chironomidae (Diptera) and their ety and an editor of Entomologica Americana. In
management. In: Rosen D, Bennett FD, Capinera JL 1891 he was hired by the U.S. Department of Agri-
(eds) Pest management in the subtropics: biological culture (Fig.50) and embarked on his lifes work as
control a Florida perspective, Intercept Ltd, Andover,
UK, pp 487513 an applied entomologist, contributing greatly to
Armitage P, Cranston PS, Pinder LCV (eds) (1995)The Chi- the knowledge of pests of vegetables and stored
ronomidae: the biology and ecology of non-biting products. In 1904 he was awarded an honorary
midges. Chapman & Hall, London, UK, 572 pp
degree of doctor of sciences by Western University
Benke AC (1998) Production dynamics of riverine chirono-
mids: extremely high biomass turnover rates of primary of Pennsylvania. He died in Washington, DC, on
consumers. Ecology 79:899910 September 15, 1929.
 Chordotonal Sensory Organs
C 863

Chlorosis
Yellowing or bleaching of normal green plant tis-
sue, usually caused by the loss of chlorophyll.

Choreutidae
A family of moths (order Lepidoptera). They are
commonly known as metalmark moths.
Metalmark Moths
Butterflies and Moths

Cholinesterase
Chittenden, Frank Hurlbut, Figure 50 Frank
An enzyme that is present in the synapse region of
H.Chittenden.
nervous tissue, and which is necessary for normal
Reference functioning of nerves in animals. Cholinesterase
inhibiting chemicals such as insecticides of the
*Mallis A (1971)Frank Hurlbut Chittenden. In: American organophosphate and carbamate classes disrupt
entomologists. Rutgers University Press, New Bruns- nerve transmission in insects.
wick, NJ, pp 100102

Chlorinated Hydrocarbons Chordotonal Sensory Organs

A class of synthetic insecticides containing chlo- James L. Nation

rine as one of the constituents. Chlorinated hydro- University of Florida, Gainesville, FL, USA
carbon insecticides are typically very persistent
and formerly were used widely for soil and seed Insects have a plethora of sensory organs scattered
treatments. These chemicals also are known as over and within their body. Many of the sensory
organochlorines. structures are mechanical sensors that bend, indi-
Insecticides cating contact with a surface or wind and air move-
ment over the structure. Other mechanoreceptors
detect stress in the exoskeleton, the cuticle, caused
Chloroperlidae by movement of legs, wings, or antennae, and
enable insects to know the position of their body
A family of stoneflies (order Plecoptera). They and limbs. Still others detect vibrations in the sub-
sometimes are called green stoneflies. strate on which the insects may be resting, and
Stoneflies vibrations in the air, which we usually call sound.
Sound detectors are typically called tympanal
Chloropidae organs. The simplest of mechanoreceptors may
consist of a single hair or seta that projects from
A family of flies (order Diptera). They commonly the cuticle surface. Such a simple receptor, usually
are known as frit flies or grass flies. with only one sensory neuron connecting it to the
Flies central nervous system (CNS) is called a sensillum.
864
C Chordotonal Sensory Organs

More complex sensory organs are composed of that different scolopidia might respond to vibra-
many sensilla, i.e., they have many sensory neurons tions of different amplitude according to length.
connecting to the CNS. Although there are numer- The subgenual organ of the American cockroach
ous morphological variations in a mechanorecep- Periplaneta americana is sensitive to vibrations that
tor, from the simple, single hair receptor to very would displace the footof the insect by as little as
complex receptors such as Johnstons organ on the 109107 cm. The subgenual organ generally is less
antennae of most insects, they tend to have certain well developed in Lepidoptera, Hymenoptera, and
common features. Whether one or many, each sen- Hemiptera than in the Orthoptera, and some
sory neuron is enclosed in one to several sheath Hemiptera, Coleoptera, and Diptera do not have
cells, and connected by a relatively long axon to the subgenual organs. Those without a subgenual organ
central nervous system. In mechanoreceptors the display only low sensitivity to high frequency vibra-
dendrites, that part of the sensory neuron nearest tions. Probably all insects have, in addition to the
the site of the stimulus, typically are enclosed subgenual organ, additional more simple chordo-
within a sclerotized cap cell, called the scolopale. tonal sensilla on the legs, particularly at or near the
The scolopale is attached to, or in contact with, the leg joints, and some insects lacking a subgenual
site where stimulation will occur, usually some organ have a similar organ at the distal end of the
internal structure or the cuticular surface. Any tibia that may serve much the same function as the
stretching or movement of the structure to which subgenual organ.
the scolopale is attached will stimulate the den- Johnstons organ is another large complex
drites of the sensory neuron and may set up a series chordotonal organ that typically consists of many
of nerve impulses going into the CNS. If only one scolopidia. Johnstons organ is located between the
sensory neuron and scolopale is present, the single second (the pedicel) and third joints of each
unit is called a scolopodium, or chordotonal sensil- antenna of most adult insects. Some hexapods
lum. These terms are used interchangeably. More (Collembola and Diplura) do not have a Johnstons
complex mechanoreceptors contain many scolo- organ. A simplified form of the organ occurs in
pidia or multiple scolopale units, or chrodotonal some larvae. Johnstons organ responds to several
sensilla, again terms that refer to the same things. kinds of stimuli in different insects, including
The subgenual organ is a complex chordotonal acting as a proprioceptor to indicate movement of
organ composed of multiple scolopidia. The name the antennae, monitoring wing-beat frequency in
subgenual means below the knee, from Latin for relation to flight speed in some Diptera, serving as
knee (genu), and this complex chordotonal organ a gravity indicator, indicating ripples at the water
usually is located near the joint between the femur surface in gyrinid beetles, and functioning as a
and tibia. Subgenual organs may contain as few as sound reception in mosquitoes and perhaps other
three scolopidia in some earwigs (Forficula spp.), insects. With its location in the second antennal
but in most insects usually contains more scolo- segment, Johnstons organ is positioned to monitor
pidia. It acts as a proprioceptor (a receptor of inter- movements of the antennal flagellum, whether due
nal stimuli) and detects vibrations of the substrate to muscles controlled by the insect, or displace-
on which the insect rests. The subgenual organ is ments of the antennae by wind and flight. Radially
especially well developed in crickets (Gryllidae) arranged scolopidia are attached to the wall of the
and katydids (Tettigonidae) and is closely associ- pedicel at one end and to the intersegmental mem-
ated with a tympanal organ, with both organs brane between the pedicel and flagellum. Johnstons
located on the tibia. The two organs have separate organ seems to have reached its apex of develop-
sensory innervation, however, and probably have ment in Chironomidae and Culicidae (Diptera), in
separate functions. In some insects, the scolopidia which the pedicel is much enlarged and filled with
in the subgenual organ vary in length, suggesting scolopidia. It seems to function in successful
 Choriogenesis
C 865

swarming and mating. Male mosquitoes detect the (ii) an air sac or other tracheal structure behind
sound of the female in flight when the arista on the the tympanum, and (iii) sensory neurons orga-
male antenna vibrates in resonance to the wing nized in scolopidia attached to the tympanal mem-
beats. Long hairs on the antennae of males also brane or attached near it, so that they vibrate in
vibrate, causing the flagellum (the major portion of response to the vibrations of the tympanum. Air-
the antenna) to resonate in response to the flight borne sound waves cause the tympanum to vibrate,
sounds of females. Males of the mosquito Aedes and sensory neurons enclosed in the scolopale
aegypti are most sensitive to frequencies from 400 cells detect the vibrations and respond by sending
to 650 Hz, corresponding closely to the natural nerve signals to the CNS. The air cavity or tracheal
wing-beat frequency of females. Johnstons organ sac plays an important role as a resonating cham-
functions as a flight speed indicator in adult Calli- ber. Some insects have a tympanum that can
phora erythrocephala, and probably also in some respond to sound waves striking it from the inside
other insects such as the housefly, honeybee, and of the air chamber as well as from outside; such
related insects. It is probably an important gravity tympanal organs are pressure-difference receivers,
indicator for most insects, enabling them to have a and they are especially sensitive to directionality
sense of their body in relation to horizontal and of the sound. Some tympanal organs have scolo-
vertical planes because the weight of the antenna pidia of different length, suggesting sensitivity to
excites scolopidia depending upon the pull of grav- various frequencies, but function is unproven.
ity relative to the body. Tympanal organs probably evolved from some
Many insects produce sounds, are sensitive to early form of mechanoreceptor, probably a stretch-
sounds, and utilize sounds in courtship, mating, registering proprioceptor, but they evolved inde-
prey location, and predator avoidance. Detection pendently among the seven orders of insects
of high frequency sound waves in the air is accom- having tympanal hearing. In addition to tympanal
plished by a tympanum, a chordotonal organ con- organs, some insects also may hear some sounds
taining scolopidia. Tympanal organs are located at with other organs including Johnstons organ, sub-
various places on the body of insects, including genual organs, scattered simple chordotonal sen-
near the sternum of the first abdominal segment silla, and simple hair sensilla.
of Acrididae (grasshoppers) and Cicadidae (cica-
das), on the tibia of Tettigoniidae (long-horn
grasshoppers) and Gryllidae (crickets), on the tho- References
rax of Notonectidae (water beetles), and on the
thorax or abdomen of some Lepidoptera. Tympa- Bailey WJ (1991) Acoustic behaviour of insects: an evolution-
nal organs are specialized for air-borne sound ary perspective. Chapman & Hall, London, 225 pp
Hoy RR, Robert D (1996) Tympanal hearing in insects. Ann
pressure waves, and permit sound detection over a Rev Entomol 41:433450
relatively long distance. They are sensitive to a Nation JL (2002) Insect physiology and biochemistry. CRC
wide range of frequencies from 2 kHz up to about Press, Boca Raton, FL, 485 pp
100 kHz. Typically in insects, as well as in other Yack JE, Fullard JH (1993) What is an insect ear? Ann Ento-
mol Soc Am 86:677682
animals, tympanal organs are paired. A single pres-
sure receptor is not very efficient at detecting the
directionality of the sound source, but two recep-
tors, preferably well separated from each other, Choriogenesis
can detect directionality by differences in recep-
tion at the two locations. Tympanal ears typically Production of a thin vitelline membrane and cho-
have a minimum of three components, (i) a thin rion by the follicle cell, the last step in production
cuticular tympanum on the cuticular surface, of the egg.
866
C Chorion

Chorion Chromatids

The outer layer of an insect egg. The egg shell. Chromosome components that have duplicated
during interphase and become visible during the
prophase stage of mitosis. Chromatids are held
together at the centromere.
Choristidae

A family of insects in the order Mecoptera. Chromomere

Scorpionflies
A region on a chromosome of densely packed
chromatid fibers that produce a dark band. Chro-
Christophers, (Sir) Samuel Rickard momeres are readily visualized on polytene
chromosomes.
Rickard Christophers was born in Liverpool on
November 27, 1873. He graduated in medicine in
1896, and then spent some time on the Amazon. In Chromosome Imprinting
1898 he joined the Malaria Commission, which
The mechanisms involved in chromosomal
had been established jointly by The Royal Society
imprinting, or labeling of DNA, is associated with
and the (British) Colonial Office; that was the year
methylation of DNA in many organisms. Imprint-
in which final proof was obtained of transmission
ing is a reversible, differential marking of genes
of malaria by Anopheles mosquitoes. In West
orchromosomes that is determined by the sex of
Africa, he concluded quickly that people who sur-
the parent from whom the genetic material is
vive malaria are the main reservoirs of the disease,
inherited.
allowing it to be transmitted by mosquitoes to
uninfected people. After that, he worked in India,
on malaria and the various Anopheles species that
Chromosome Puffs
transmit it, showing that successful control requires
knowledge of the habits and larval habitat of each A localized swelling of a region of a polytene chro-
implicated Anopheles species. He developed stan- mosome due to synthesis of DNA or RNA. Puffing
dards for malarial surveys. He investigated the is readily seen in polytene salivary gland chromo-
anatomy and behavior of mosquitoes, including somes of dipteran insects.
the development of mosquito eggs. Later he worked
at the London School of Tropical Medicine and
Hygiene, and then at Cambridge University. His Chromosomes
landmark book (1960) Aedes aegypti (L.), the
yellow fever mosquito was published when he was Units of the genome with many genes, consisting
87. At the age of 90 he retired and moved to the of histone proteins and a very long DNA molecule;
county of Dorset in the west of England. He died found in the nucleus of every eukaryote.
on February 19, 1978.

Chronic
Reference
In pathology, of long duration; not acute. This is
Gillett JD (1978) Sir Rickard Christophers. Antenna 2:33 usually used to describe a debilitating disease that
 Chronotoxicology
C 867

slowly infects a population as opposed to one that administered a standard dose of potassium cya-
quickly and dramatically infects the population. nide at different times of the day. Within a little
more than a year of Becks report, two papers on
insecticide chronotoxicity appeared in the promi-
Chronic Bee Paralysis nent journal Science. Cole and Adkisson reported
diurnal variations in mortality from a standard dose
A disease of bees caused by a RNA virus (but not a of trichlorfon applied to the beetle, Anthonomus
picornavirus). Symptoms include flightlessness grandis, and Polcik and colleagues, in a paper on
and a distended abdomen. (contrast with acute dichlorvos chronotoxicity to the mite, Tetranychus
bee paralysis) urticae (Koch) posed an important and novel con-
cept that the findings of a marked sensitivity pat-
Chronic Toxicity tern should emphasize the importance of considering
circadian organization [of the pest] in the evaluation
The toxic effect of a chemical following long-term and interpretation of toxicological experiments with
or repeated sublethal exposures. insecticides. Soon, Nowosielski et al. reported daily
changes in susceptibility of the house cricket, Acheta
domesticus (L.) and T. urticae to anesthetics (ethyl
Chronotoxicology ether, chloroform and carbon tetrachloride).
These pioneering papers demonstrated that
Maciej A. Pszczolkowski susceptibility to toxicants fluctuate during the day,
Missouri State University and State Fruit Experi- and are dependent not only on properties of the
ment Station, Mountain Grove, MO, USA toxicant, but also on endogenous rhythmic changes
in pest physiology. One might have predicted that
All eukaryotic organisms, including insects, have by now, monitoring the diurnal susceptibility to
developed rhythmic behavioral, physiological or toxicants (and, in particular, to insecticides) would
biochemical patterns synchronized with particu- be an experimental routine for establishing toxic-
lar periods of the day, to adapt to their ecological ity parameters. However, recent inquiry suggests
niches in the most optimal manner. Those oscilla- that papers on the chronotoxicity of insecticides
tions, circadian rhythms, have evolved with a peri- are rarities.
odicity approximating 24 h, are of endogenous Forty years after pioneering publications
nature and may be adjusted to lighting stimuli. of Beck, Polcik and colleagues and Cole and
Chronotoxicology is the study of the adverse effects Adkisson, Pszczolkowski and associates inspected
of chemicals on living organisms in relation to representative databases (Medline, Toxline, Agri-
their circadian rhythms. In particular, it examines cola, and Internet Database Service-Biological
toxicants chronotoxicity, i.e., periodic changes in Sciences) in search of papers on pesticide chrono-
sensitivity of living organisms to toxicants. toxicity to insects. The search, followed by paper-
to-paper inquiry yielded only 16 reports referring
to diurnal or circadian changes in insecticide tox-
Historical Perspective icity in insects. Four more were found more
recently. Ten of them examined difference between
Circadian changes in sensitivity to toxicants were the highest and the lowest mortality percent after
first reported in mice by Halberg and Stephens as application of a standard dose of insecticide at
early as 1958. Five years later, Stanley Beck showed various times of the day, in the remaining reports
that the German cockroach, Blatella germanica diurnal variations in LD50 were reported. However,
(L.) exhibits a 24-h susceptibility rhythm when even these scanty data show that insect mortality
868
C Chronotoxicology

can be as much as nine times higher than if the

same, standard dose is applied at some other time
or times, and that, depending on the time of test-
ing, the highest LD50 may be up to 7.5 times higher
than the lowest LD50 for the same toxicant.

Coincidence of Insecticide
Susceptibility Rhythms and Other
Biological Rhythms

Theoretically, periodic changes in insecticide sen- Chronotoxicology, Figure 51 Diurnal distributions

sitivity should reflect periodic changes in ratios of of LD50 from DDT versus diurnal changes in
penetration, ratios of detoxification (including respiration and DDT breakdown in WHO strain
metabolism, elimination from hemolymph and of the house fly Musca domestica. Generally,
excretion of a given toxicant), periodic alterations low respiratory rates and low DDT metabolism
at the site of action (for instance, periodic over- or correspond with high tolerance to DDT, and high
underexpression of target receptors) or their com- levels of detoxification correspond with high
binations. This assumption was reiterated in pub- susceptibility to DDT, which is an unexpected
lications devoted to physiological and behavioral correlation. For the sake of clarity, the original
aspects of insect biological rhythms, e.g., in funda- measurements are normalized and expressed
mental Insect clocks. Unfortunately, this hypoth- as percent of the maximum value obtained for
esis did not attract attention of many researchers. diurnal toxicity, respiration and DDT breakdown
Perhaps the most extensive analysis of physio- pattern, respectively. Shaded areas mark the dark
logical and biochemical events that underlie circa- phase of the photoperiod. (Collated and modified
dian sensitivity to an insecticide was research on from Shipp E, Otton J (1976) Circadian rhythms
house fly, Musca domestica (L.). Mean LD50 values of sensitivity to insecticides in Musca domestica
for DDT were established as a function of applica- (Diptera, Muscidae). Entomol Exp Appl 19:163171;
tion time in the house fly, kept in a specific photo- Shipp E, Otton J (1976) Diel changes in DDT
periodic regimen. Flies tested topically with DDT absorption and breakdown rates and respiratory
had a significantly lower LD50 value when treated at rhythm in the housefly, Musca domestica. Entomol
the end of the dark phase, and increased tolerance Exp Appl 19:235242.)
to DDT during the early part of the dark phase. This
distribution was apparently caused by some endog- show an opposite trend: relatively low ratios of DDT
enous oscillations, because the flies kept in total breakdown and respiration correspond with rela-
darkness exhibited similar pattern of DDT suscep- tively high ratios of DDT tolerance, and vice versa.
tibility. This rhythmic response was not caused by Only at 15:00 p.m. high tolerance to DDT is corre-
changes in cuticle permeability to the insecticide, lated with high levels of respiration and DDT break-
for regardless of the time of application, about 40% down. Thus, circadian changes in susceptibility of
of DDT was absorbed within 2 h. However, com- Musca domestica to DDT were generally indepen-
parison of DDT susceptibility rhythm and rhyth- dent of ability to detoxify DDT. Perhaps the oscilla-
mic changes in respiration and DDT breakdown to tions in this insecticide tolerance were caused by
DDE do not support the hypothesis that elevation some alterations at the target site.
of DDT toxicity (Fig.51) was caused by decrease in Time-dependent events in insect systems
dynamics of detoxification mechanisms. The data involved in insecticide toxicity and metabolism
 Chronotoxicology
C 869

may be even more complex, given the mode of

action of insecticide studied. Research on metabo-
lism of di-syston (0,0-diethyl S-2 (ethylthio) ethyl
phosphoditioate) in larvae of Heliothis zea (Boddie)
is a good example. Di-syston requires biological
oxidation to become active; thus, in addition to
periodic changes in ratios of insecticide penetra-
tion, detoxification, or periodic alterations at the
site of action one must consider periodic changes in
activity of oxidative enzymes which are necessary
to activate the insecticide. In this study, the experi-
mental insects were maintained in a specific photo-
periodic regimen (14 h of light- and 10 h of dark
phase) and controls were exposed to constant light.
The treatments aimed to synchronize larval bio-
chemical processes to photoperiod, or keep them
de-synchronized, respectively. In both groups, the
larvae were injected with standard dose of isotope-
labeled insecticide in various times of the day. Chronotoxicology, Figure 52 Diurnal changes
Radioactivity of hydrolytic or oxidative metabolites in oxidation and hydrolysis of isotope-labeled
of di-syston was determined in larval tissues and Di-syston by Heliothis zea last instar larvae.
excreta, 4 h after injection, revealing three distinct Standard doses of this insecticide were applied
rhythms. Oxidation (and therefore toxicity) of di- at various times of the day. Di-syston requires
syston (Fig.52) reached the highest ratios at the end biological oxidation to become insecticidally
of the light phase and at the end of the dark phase active, thus diurnal changes in its oxidation
of the photoperiod, and dropped to the lowest reflect its actual toxic potential. Changes in
values soon after lights on and after lights off. The hydrolysis r eflect dynamics of detoxification.
rhythm of hydrolase activity was bimodal too, with B. Diurnal changes in concentrations of
peaks in the middle of either dark or light phase Di-syston metabolites in excreta of Heliothis
of the photoperiod. The latter rhythm roughly zea last instar larvae. High activity of hydrolytic
corresponded with the rhythm of di-syston metab- enzymes is c orrelated with low concentrations
olite excretion. Control larvae, maintained in desyn- of toxic products of Di-syston oxidation (A) and
chronizing lighting conditions, did not show products of Di-syston detoxification are excreted
rhythmic patterns of di-syston metabolism. immediately (B), showing bimodal diurnal p attern
This work has two important implications. of detoxification. Shaded areas mark the dark
First it shows that sometimes a researcher should phase of the photoperiod. (Modified from Bull
consider at least one more rhythmic organismal DL, Lindquist DA (1965) A comparative study of
event influencing toxic potential of an insecticide insecticide metabolism in photoperiod-entrained
administered at various times of the day; in this and unentrained boll-worm larvae Heliothis zea
case time dependent changes in activation of toxic (Boddie). Comp Biochem Physiol 16:321325.)
properties of the insecticide. Second, it shows that
lighting conditions may influence periodic pity that they did not provide information about
responses to insecticide toxicity (in their study, diurnal changes in mortality of H. zea larvae due
periodic changes in di-syston activation and deg- to di-syston. I am not aware of this information
radation were abolished in constant light). It is a being available in literature.
870
C Chronotoxicology

Because periodic changes in physiological or

biochemical processes are difficult to monitor, a
number of reports have suggested that circadian
rhythms in insect sensitivity to toxicants could be
correlated to locomotor activity rhythms, which
are relatively easy to record. For example, it has
been noted by several investigators that there is a
general trend of a time of greatest susceptibility
occurring at about the time of onset of increased
activity. However, the scanty data published on Chronotoxicology, Figure 53 Diurnal patterns
coincidence of daily changes in susceptibility to of Diazinon toxicity to field populations of adult
insecticide treatment and rhythms of locomotor Diabrotica virgifera virgifera. The p
hotoperiod
activity do not support this assumption. There is shown is the naturally occurring p hotoperiod
no universal rule that would allow predicting the under which the beetles were living when
time of the greatest sensitivity to insecticides by collected. Upper curve shows LD50 distribution
monitoring circadian patterns of locomotor activ- for the population collected in 1968. The lower
ity. It seems that the time of greatest sensitivity curve r eflects susceptibility of the population
depends on the species, mode of treatment and collected 12 months earlier. Only determination
the insecticide tested rather than a specific moment of diurnal LD50 distributions and maintaining the
in the insects activity pattern. same photoperiodic regimen and similar timing
of insecticide treatment allowed d emonstration
of increased resistance to Diazinon (further
Biological Rhythms and Measuring explanations in text). Shaded areas mark the dark
Toxicity Parameters phase of the photoperiod. (Modified from Ball HJ
(1969) Diurnal rhythm of sensitivity to diazinon
Thus, it appears that insect toxicologists should in adult western corn rootworms. J Econ Entomol
concern themselves with not only the usual param- 62:10971098.)
eters of insecticide toxicity, but also with diurnal
distribution of toxicity. At the very least, circadian during that period of time, and only investigation
time of treatment should be indicated in reports on of diurnal pattern of susceptibility revealed increase
mortality tests, particularly if toxicity parameters in resistance against this insecticide.
are used for comparative study of insecticide resis- Precautionary measures should also be taken if
tance. For example, in one study two samples of the insecticide resistance is compared between popula-
beetle Diabrotica virgifera virgifera (LeConte) were tions of the same age, and the same history of toxi-
collected, one in August 1967 and the other 12 cant exposure, but kept under different breeding or
months later, from the same location, which was testing regimens. Because insects are known to syn-
meanwhile exposed to routine sprays with diazi- chronize their endogenous rhythms to exogenous
non. Daily distributions of LD50 (Fig. 53) were stimuli such as photo- or thermoperiod (a phenom-
established for either population of the beetles. If enon called entraining to a rhythm in chronobio-
the author had limited himself to one toxicity assay logical nomenclature) the diurnal distribution of
at 7:00 a.m. in 1967, and one toxicity assay at 11:00 insecticide sensitivity may be synchronized to exter-
a.m. in 1968, he would have probably concluded nal conditions too. This was observed when house
that no resistance has been built up between 1967 flies were reared through multiple generations, each
and 1968. In fact, the field populations of Diabrot- experimental population in a d ifferent photoperiod.
ica increased resistance to diazinon by about 70% Seven different photoperiods were used, including
 Chronotoxicology
C 871

constant light throughout 24-h cycle. In the first set groups treated with trichlorfon in other times of the
of experiments the flies were treated with standard day, marked differences in mortality were observed.
doses of trichlorfon at various times of the day. Next, For instance, in group treated at 4:00 p.m., the
the flies were returned to their respective photoperi- mortality varied from 78 to 95%, depending on the
odic regimens and percent mortality was recorded length of the light phase of the photoperiodic regi-
48 h later. Mortality depended both upon the time of men used. When the flies were exposed to the insec-
treatment commencement and the photoperiodic ticide at 9:00 p.m. the differences were even greater.
regimen the insects were kept in. For instance, mor- In another experiment, the flies were similarly reared
tality from trichlorfon administered at 10:00 a.m. in various photoperiodic regimens, and therefore
almost did not vary, oscillating between 96 and 93 % their endogenous rhythms had synchronized to
regardless of the photoperiod to which the flies were external light:dark oscillations of their specific pho-
synchronized, and maintained in, during the expo- toperiodic regimens. Next, the flies were treated with
sure (Fig. 54) to the insecticide. However, in the various doses of trichlorfon at a fixed time of the
day, corresponding not only to a fixed time of their
own photoperiodic regimen (for instance 9 h after
the onset of light) but also to a fixed time of the
astronomical day (in this case 4:00 p.m.). Subse-
quently the flies were transferred to constant light-
ing conditions, where no oscillating stimuli could
have influenced insects endogenous rhythms. After
48 h of exposure to trichlorfon (Fig. 55), the LD50

Chronotoxicology, Figure 54 Susceptibility of

house flies to standard dose of trichlorfon at
various times of the day as a function of the length
of the light phase of the photoperiod. The flies
were reared in specific photoperiod for several
generations before and during exposure to the Chronotoxicology, Figure 55 Variability of LD50
insecticide. The light in each experimental group from trichlorfon administered at fixed time of
came on at the same time (7:00 a.m.), trichlorfon the day to the flies that had been synchronized
was administered in various times of the day. to v
arious photoperiods before the testing took
The flies tested at 10:00 a.m. exhibited almost the place. The flies were kept in various p
hotoperiods
same mortality ratios regardless of photoperiod for several generations, and then exposed to
they were reared and tested under. The flies the insecticide for 48 h under constant lighting
tested at 4:00 p.m. or 9:00 p.m. showed marked conditions. Beginning of insecticide treatment
variations in mortality from standard dose of commenced 9 h after lights on (4:00 p.m.), in each
trichlorfon, dependent on the photoperiod they group. The flies that had experienced photoperiod
had e xperienced prior to the tests and during light:dark 14:10 prior to the test were markedly
exposure to the insecticide. (Modified from more resistant to trichlorfon than those that
Fernandez AT, Randolph NM (1967) Photoperiodic hadbeen kept in photoperiod light:dark 13:11.
effect on the daily susceptibility of the house fly to (Drawn on the basis of data by Fernandez and
trichlorfon. J Econ Entomol 60:16331635.) Randolph, 1967.)
872
C Chronotoxicology

was calculated. The flies entrained to the photope- be carefully studied before ultimate toxicity param-
riod consisting of 13 h of light phase and 11 h of eters are established and released as a basis for fur-
dark phase were three times more susceptible to ther use. On the other hand, chronotoxicological
trichlorfon than the flies entrained to only slightly experiments are labor expensive and time intensive.
different photoperiod (14 h of light phase and 10 h The scarcity of published data does not allow any
of dark phase). Analogous experiments with DDT, generalization as to methodology of experimenting:
endrin and dieldrin yielded similar results. there is no universal correlation of susceptibility
These remarkable results show that some insects patterns with daily distribution of locomotor activ-
entrained to a photoperiod maintain their charac- ity. Dynamic detoxification processes sometimes do
teristic rhythmicity of detoxification under constant not correlate with toxicity changes in an expected
lighting conditions, and their diurnal distribution of manner; the same photoperiodic conditions may
susceptibility to toxicants are determined by syn- abolish cyclic changes in insecticide metabolism
chronizing stimuli from the past. Entraining, as a (and, presumably, toxicity) in one species, such as H.
feature of circadian organization of insect physiol- zea larvae, or permit changes in susceptibility to
ogy and behavior, clearly should be taken into con- occur in another, such as adult house flies. Research
sideration while planning toxicity tests, but many in insecticide chronotoxicology apparently does not
insect toxicologists do not realize how sensitive to attract funding, and its results are not easy to inter-
entraining insect physiological systems can be. pret, discuss and publish, since there is not much
Insect populations do not need to be exposed literature on this topic. Nor has monitoring the diur-
to certain photoperiodic conditions for several suc- nal distribution of pest susceptibility to insecticides
cessive generations to synchronize their organismal become an experimental routine for establishing
oscillations to external lighting regimen. For insecticide toxicity parameters.
instance, short-lasting exposures to light during Impressive progress in knowledge of insect
the dark phase of the rhythm also effectively syn- toxicology, insecticide resistance mechanisms and
chronize rhythms in adult insects of some species insect chronobiology has been made, but these
(e.g., many dipterans). Such a stimulus may shift the disciplines need integration. Perhaps younger gen-
insect endogenous rhythms by several hours in erations of entomologists will charge themselves
comparison to original pattern of physiological oscil- with such a task.
lations,inducing a response (so-called phase response) Rhythms in Insects
that lasts for days if not weeks under continuous Insecticides
lighting conditions. Even temporary changes in Insecticide Toxicity
insect breeding conditions may have profound Insecticide Bioassays
effects on detoxification rhythms and, consequently,
diurnal distribution of mortality in toxicity tests. References

Bainbridge CA, Margham P, Michael T (1982) Diurnal fluc-

Concluding Remarks tuations in susceptibility to insecticides in several strains
of the yellow fever mosquito (Aedes egypti L.). Pest Sci
An entomologist aware of time-dependent changes 13:9296
Ball HJ (1969) Diurnal rhythm of sensitivity to diazinon in adult
in toxicity of insecticides, toxicants or narcotic western corn rootworms. J Econ Entomol 62:10971098
agents finds himself in a frustrating situation. On Beck SD (1963) Physiology and ecology of photoperiodism.
one hand, it is reasonable to propose that circadian Bull Entomol Soc Am 9:816
Bull DL, Lindquist DA (1965) A comparative study of
organization of mechanisms that underlie insecti-
insecticide metabolism in photoperiod-entrained and
cide uptake, detoxification, action on the target sites unentrained boll-worm larvae Heliothis zea (Boddie).
or at least diurnal distribution of mortality should Comp Biochem Physiol 16:321325
 Cibarium
C 873

Cole CL, Adkisson PL (1964) Daily rhythm in the susceptibil- Chrysomelidae

ity of an insect to a toxic agent. Science 144:11481149
Crystal MM (1969) Changes in susceptibility of screw-worm
flies to the chemosterilant N, N-tetramethylenebis A family of beetles (order Coleoptera). They
(1-aziridinecarboxamide), with time of administration. commonly are known as leaf beetles.
J Econ Entomol 62:275276 Beetles
Eesa NM, Cutkomp LK (1995) Pesticide chronotoxicity
to insects and mites: an overview. J Islam Acad Sci 8 Leaf Beetles (Coleoptera: Chrysomelidae)
(1):2128
Fernandez AT, Randolph NM (1967) Photoperiodic effect on
the daily susceptibility of the house fly to trichlorfon. J
Econ Entomol 60:16331635 Chrysopidae
Halberg F, Stephens AN (1958) 24-hour periodicity in mor-
tality of C mice from E. coli lipopolysaccharide. Fed A family of insects in the order Neuroptera. They
Proc17:439
commonly are known as green lacewings.
Halberg J, Halberg F, Lee JK, Cutcomp LK, Sullivan WK, Hayes
DK, Cawley BM, Rosenthal J (1974) Similar timing of Lacewings, Antlions and Mantidflies
circadian rhythms in sensitivity to pyrethrum of several Natural Enemies Important is Biological
insects. Int J Chronobiol 2:291296 Control
Kermarrec A, Abud-Autun A (1978) Variations de la sensi-
bilit au parathion selon lheure chez Acromyrmex octos-
pinosus Reich (Formicidae, Attini). Ann Zool Ecol Anim
10:2935
Nowosielski JW, Patton RL, Naegele JA (1964) Daily rhythm of
Chrysopolomidae
narcotic sensitivity in the house cricket, Gryllus domesti-
cus L., and the two-spotted spider mite, Tetranychus urti- A family of moths (order Lepidoptera) also known
cae Koch. J Cell Comp Physiol 63:393398 as African slug caterpillar moths.
Polcik B, Nowosielski JW, Naegele JA (1964). Daily sensitivity African Slug Caterpillar Moths
rhythm of the twospotted spider mite, Tetranychus urti-
cae, to DDVP. Science 145:405406 Butterflies and Moths
Pszczolkowski MA, Dobrowolski M, Spencer C (2004) When
did you last test your insects? The forgotten importance
of chronotoxicology. Am Entomol 50:7274
Saunders DS (1982) Insect clocks, 2nd edn. Pergamon Press, Chyromyid Flies
New York, NY, 408 pp
Shipp E, Otton J (1976a) Circadian rhythms of sensitivity to Members of the family Chyromyidae (order
insecticides in Musca domestica (Diptera, Muscidae).
Entomol Exp Appl 19:163171
Diptera).
Shipp E, Otton J (1976b) Diel changes in DDT absorption and Flies
breakdown rates and respiratory rhythm in the housefly,
Musca domestica. Entomol Exp Appl 19:235242

Chyromyidae

Chrysalis A family of flies (order Diptera). They commonly

are known as chyromyid flies.
The pupal stage of a butterfly. Flies

Chrysididae Cibarium
A family of wasps (order Hymenoptera). They The preoral cavity; an external space in front of
commonly are known as cuckoo wasps. the head that is surrounded by the mouthparts but
Wasps, Ants, Bees and Sawflies in front of the true mouth or stomodeum.
874
C Cicada Parasite Beetles

Cicada Parasite Beetles Family Tettigarctidae White

Members of the family Rhipiceridae (order Contains two species in the genus Tettigarcta
Coleoptera). White (Fig.56). The extant members of this family
Beetles are restricted in their distribution to Australia. The
Tettigarctidae exhibit ancestral morphology show-
ing many similarities in their structure to fossil
cicadas. They have a expanded pronotum that
Cicadas (Hemiptera: Cicadoidea)
lacks paramedial and lateral fissures and a prono-
tal collar and conceals much of the mesonotum
Allen Sanborn
along with peculiar wing venation. The mesono-
Barry University, Miami Shores, FL, USA
tum lacks a cruciform elevation. The hind coxae
overhang the abdomen. In addition, both sexes of
The members of the superfamily Cicadoidea West-
the Tettigarctidae have a timbal apparatus but the
wood are four-winged insects with sucking mouth-
structures are poorly developed and they lack
parts that possess three ocelli and a rostrum that
tympana. Males lack an acoustic resonating cham-
arises from the base of the head.
ber in the abdomen. They have recently been
shown to communicate through vibrational rather
than airborne signals.
Classification

The classification within the superfamily has had Family Cicadidae Latreille
a varied history. There have been as many as six
families described within the superfamily. The Members of this family (Fig.57) represent the vast
major characters used to separate these families majority of extant cicadas. Characters that sepa-
are structures of the sound production system, rate members of the family include: a pronotum
e.g., the timbal covers and stridulatory appara- that includes a pronotal collar, paramedial and lat-
tuses. The separation of the two major historical eral fissures and is smaller than the mesonotum;
families was based primarily on the presence or the mesonotal scutellum forms a cruciform eleva-
absence of timbal covers. However, the variation tion; timbals if present only found in males; males
in the timbal cover anatomy is not related to a have an abdominal resonating chamber; both
monophyletic ancestry within the groups. Simi- sexes have tympana. The extant genera have been
larly, the stridulatory structures have evolved as a divided into three subfamilies based on the
means to isolate species reproductively and, there-
fore, appear to have evolved independently more
than once. As a result, the structures of the sound
apparati were a poor choice of characters on
which the higher taxonomy should be based. The
recent analysis of the higher taxonomy of the
Cicadoidea suggests only two families are justi-
fied within the Cicadoidea, the Tettigarctidae and
the Cicadidae.
Order: Hemiptera Cicadas (Hemiptera: Cicadoidea),
Infraorder: Cicadomorpha Figure56Tettigarcta crinita Distant, 1883, a
Superfamily: Cicadoidea member of the family Tettigarctidae.
 Cicadas (Hemiptera: Cicadoidea)
C 875

to the mesothorax and metathorax. The wings can

be hyaline, they may be infuscated, or they may be
opaque or pigmented. Wing venation is another
significant character used in taxonomy. The oper-
cula are another diagnostic character that origi-
nate on the ventral metathorax but extend toward
and often cover large portions of the abdomen.
The abdomen is clearly segmented with the ter-
minal segments modified to form the reproduc-
Cicadas (Hemiptera: Cicadoidea), Figure 57 Cicada tive organs. The genitalia are one of the most
orni Linnaeus, 1758, a representative of the family important structures in identifying species. The
Cicadidae. abdomen of male cicadas is generally hollow and
acts as a resonating organ to increase the song
intensity. In addition, the timbal covers may be
s tructure of the male genitalia, wing venation, tim- found covering the timbal organ of the male.
bal covers, and opercula. It includes the members
of all previously described families except the
Tettigarctidae. Immature Stages

Documented life cycles of cicadas range from 1 to

Chararacteristics 17 years. The life cycle can be variable within a
species and emergence may be determined by
Adults thequality of the food source for the nymph, or all
the individuals of a population may emerge syn-
Cicadas show a large range in adult body size. The chronously as in the periodic cicadas (Magicicada
smallest species have body lengths of 1 cm and spp.). Eggs are laid in twigs or stems of the host
wingspans of <2 cm while the largest species have plants. The nymphs will crawl out of the egg and
body lengths of 7 cm and wingspans of almost 20 fall to the ground after hatching. The nymph will
cm. The body coloration varies from a uniform then burrow into the ground and attach to a root
reddish, green, brown, or black to a mixture of to obtain nourishment. The nymph will construct
colors. The coloration pattern of the pronotum a chamber around the root in which it will grow
and mesonotum is especially useful in determin- and proceed through its hemimetabolous devel-
ing species. The head is dominated by the two opment. When it is mature, the nymph will emerge
compound eyes. Three ocelli form a triangle on from the soil, find a vertical surface on which it
the dorsal surface of the head between the com- can attach and then the adult encloses from it.
pound eyes. This arrangement of the ocelli is one
of the distinguishing characteristics separating
cicadas from other bugs. The antennae are short Natural History
and are located between the postclypeus and the
compound eyes. The mouthparts form a needle- Cicadas are found on all continents except Antarc-
like rostrum that is inserted into plants to obtain tica. They have a broad distribution in the tropical
xylem fluid. The postclypeus houses the pumping and temperate latitudes and can be found wherever
musculature. The thorax is divided into the three permafrost is absent. As is common in the animal
segments characteristic of insects. Each thoracic kingdom, the tropics are rich with species diversity.
segment has a pair of legs and wings are attached There is a correlation between the described cicada
876
C Cicadas (Hemiptera: Cicadoidea)

diversity for particular geographic regions and Agricultural Importance

where cicada taxonomists have concentrated their
efforts during their individual careers either The main source of agricultural damage occurs
through repeated expeditions or by living in a par- when the females oviposit in their host plants.
ticular region. Large emergences of cicadas (i.e., periodic cica-
One of the most distinguishing characteris- das) and their corresponding oviposition can
tics of cicadas is their acoustic behavior. The cause small trees to wilt and small branches to
sounds produced by cicadas are species specific break off trees. In addition, the loss of nutrients to
and are becoming useful tools in species identifi- the host tree in supporting a heavy infestation on
cation. The sounds are generally produced by its roots can lead to decreased growth and fruit
males but females have evolved acoustic responses production. These effects have been well docu-
to male signals. The major male sound production mented in apple orchards located near old growth
system is a timbal organ. The timbal organ is a rib- forests that support a large cicada population.
strengthened, chitinous membrane located in the There are several contact insecticides that can kill
first abdominal segment that is buckled by con- the adults but they cannot be relied upon to pro-
traction of a timbal muscle. Structures such as the tect the trees completely. The slow action of the
abdominal air sacs, opercula, and timbal covers pesticides makes controlling the damage caused
can modify the sound emitted by the cicada. Strid- by the adults difficult. Pruning trees prior to cicada
ulatory apparati have evolved in several genera as emergence decreases the availability of preferred
an accessory sound production system. The strid- oviposition sites. Covering small trees with cheese-
ulatory systems are generally associated with the cloth or some form of netting to prevent access
wings and the mesothorax but a genital system has has been a successful strategy to protect trees par-
also been described. Finally, crepitation is used as ticularly susceptible to damage.
the primary communication signal by two genera Several species around the world have moved
of North American cicadas. The stridulatory and from natural grasses as their host plant to sugar-
crepitation systems permit two way communica- cane. These species decrease the yield of the sugar-
tion between the sexes in contrast to the unidirec- cane fields they infest. A successful control strategy
tional timbal system. has been to till the soil which kills the nymphs.
Birds are major predators of adult cicadas. Adults can also be controlled with contact
Emergences of periodical cicadas represent a insecticides.
superabundant food source and many animals There have been reports of cicadas oviposit-
(e.g., fish, amphibians, reptiles, birds and mam- ing in other food crops such as dates, asparagus,
mals) change their foraging habits to include the citrus trees, cotton, grapevines, etc. These reports
cicadas. Cicada killers (family Sphecidae) are natu- are generally isolated, and cicadas do not appear to
ral parasites that provision their nests with adult be major agricultural pests with the exceptions
cicadas as food for their offspring. Nymphs bur- noted above.
rowing into the ground are prey for ants whereas Sound Production in the Cicadoidea
underground nymphs are prey for animals like
moles and boars. Predators such as spiders, man-
tids, robber flies, and bats also take adult cicadas References
asprey.
There are also several genera of entomopatho- Boulard M (2001) Higher taxonomy and nomenclature of the
Cicadoidea or true cicadas: history, problems and solu-
genic fungi that use cicadas as hosts. Some fungi
tions (Rhynchota Auchenorhyncha Cicadomorpha). Ecole
grow on nymphs (e.g., Cordyceps spp.) while others Pratique des Hautes Etudes, Travaux du Laboratoire Biol-
grow on the adults (e.g., Massospora spp.). ogie et Evolution des Insectes Hemipteroidea 14:148
 Citricola Scale, Coccus pseudomagnoliarum (Kuwana) (Hemiptera: Coccidae)
C 877

Duffels JP (1993) The systematic position of Moana expansa Cimicidae

(Homoptera: Cicadidae), with reference to sound organs
and the higher classification of the superfamily Cica-
doidea. J Nat Hist 27:12231237 A family of bugs (order Hemiptera). They some-
Moulds MS (1990) A guide to Australian cicadas. New South times are called bed bugs.
Wales University Press, Kensington, Australia, 217 pp Bugs
Moulds MS (2005) An appraisal of the higher classification of
cicadas (Hemiptera: Cicadoidea) with special reference Bedbugs (Hemiptera: Cimicidae)
to the Australian fauna. Rec Aust Mus 57:375446
Myers JG (1929) Insect singers: a natural history of the
cicadas. George Routledge and Sons, Limited, London,
UK, 304 pp
Circadian Rhythm

Cicadellidae An endogenous biological rhythm with a recur-

rence of about 24 h. Changes in biological or met-
A family of bugs (order Hemiptera). They com- abolic functions that show periodic peaks or lows
monly are known as leafhoppers. of activity based on or approximating a 24-h cycle.
Leafhoppers This also is known as a circadian clock.
Bugs Biological Clock of the German Cockroach,
Blatella germanica (L.)

Cicindelidae
A group of beetles (order Coleoptera), sometimes Circulative Virus
treated as a separate family, here considered part
of Carabidae. They commonly are known as tiger A virus that systemically infects its insect vector
beetles. and usually is transmitted for the remainder of the
Beetles vectors life.
Tiger Beetles

Cigarette Beetle Circumesophageal Connective

Stored Grain and Flour Insects The bilateral neural connective between the trito-
cerebrum and the subesophageal ganglion. Usu-
ally the alimentary canal passes between the
Ciidae circumesophageal connectives.
Nervous System
A family of beetles (order Coleoptera). They com-
monly are known as minute tree-fungus beetles.
Beetles

Citricola Scale, Coccus

Cimbicidae pseudomagnoliarum (Kuwana)
(Hemiptera: Coccidae)
A family of sawflies (order Hymenoptera, subor-
der Symphyta). This species is a citrus pest in California, USA.
Wasps, Ants, Bees and Sawflies Citrus Pests and Their Management
878
C Citrus Blackfly, Aleurocanthus woglumi (Ashby) (Hempitera: Aleyrodidae)

Citrus Blackfly, Aleurocanthus composed of a scion (the variety) and the root-
woglumi (Ashby) (Hempitera: stock. These two parts are budded or grafted
Aleyrodidae) together, with the goal of combining the best prop-
erties of each to make a tree that produces plenty
This citrus pest is a black-colored whitefly. of quality fruit. The genus Citrus contains many
Citrus Pests and Their Management species and hybrids. Some of the more common
fruits are citron (C. medica L.), sour orange
(C.aurantium L.), pummelo (C. maxima Merril),
Citrus Greening Disease lemon (C. limon (L.) Burm. f.), mandarin or tan-
gerine (types with red-orange skin) (C. reticulata
This psyllid-transmitted disease is a serious haz-
Blanco), common, Mexican, West Indian, or Key
ard to citrus crops.
lime (C. aurantifolia (Christm. et Panz.) Swingle,
Transmission of Plant Diseases by Insects
Tahiti lime (C. latisfolia Tanaka), sweet lime
(C. limettioides Tanaka), grapefruit (C. maxima
Citrus Leafminer, Phyllocnistis var. racemosa, formerly C. paradisi MacFayden),
citrella (Stainton) (Lepidoptera: and orange or sweet orange (C. sinensis (L.) Osbeck).
Gracillaridae) Species in Citrus can readily interbreed or hybrid-
ize. Many combinations are commercially avail-
This leaf-mining caterpillar is a pest of young able, such as tangelo (mandarin X grapefruit),
trees. mandarin lime (lemon X mandarin), and tangor
Citrus Pests and Their Management (mandarin X sweet orange). Other species or
hybrids of Citrus are used as rootstocks.
Citrus Mealybug, Planococcus citri
(Risso) (Hempitera:
Pseudococcidae) History of Citrus

This mealybug threatens citrus crops in USA. Citrus species probably originated in southeast
Citrus Pests and Their Management Asia and India. Various citrus fruits, such as
lemons, limes, and oranges, were cultured in the
Indus Valley over 4,000 years ago. The modern
Citrus Peelminer, Marmara gulosa citrus varieties most likely came from China.
(Guillen and Davis) (Lepidoptera: Conquering armies, traders, and explorers
Gracillaridae) from the Romans to the Arabs to the western
Europeans transported citrus fruits and seeds
This is a minor citrus pest in USA.
from Asia through southern Europe, northern
Citrus Pests and Their Management
Africa and to the New World. Christopher
Columbus brought sour orange, lemon, and
Citrus Pests and their citron seeds when he established colonies in
Management Haiti and the Caribbean. Spanish explorers
brought oranges to St. Augustine, Florida, from
Robert Meagher 1513 to 1565, and Ponce de Leon brought seeds
USDA, Agricultural Research Service, Gainesville, and ordered sailors to plant them wherever
FL, USA theylanded. Grapefruit arrived in Florida much
later, when a grove was planted near Tampa in
Botanically, the genus Citrus L. is an evergreen tree 1823. Spanish missionaries introduced citrus to
in the family Rutaceae. As a commercial tree, it is C alifornia in 1769.
 Citrus Pests and their Management
C 879

Pest Descriptions Pink citrus rust mite, Aculops pelekassi

(Keifer), is similar to citrus rust mites in feeding
This section includes the important mite and and injury. They can coexist on the same leaves,
insect species (Table12, Figs. 5860) that attack but A. pelekassi can develop larger, more damaging
citrus in the continental United States (Arizona, populations earlier in the season. Pink citrus rust
California, Florida, and Texas), though many mites are usually pink and are narrower than citrus
are cosmopolitan. Pest management consider- rust mites.
ations are discussed at the end of this section. Citrus bud mite, Eriophyes sheldoni Ewing,
is primarily a pest of coastal lemons in Califor-
nia. They feed within leaf axil buds and devel-
Acari oping blossoms, causing formation of multiple
buds and abnormal growth of subsequent leaf
Citrus is infested by several groups of mites foliage orflowers.
including rust and bud mites (Eriophyidae), spi- Several other eriophyid mites are pests in
der mites (Tetranychidae), false spider mites other world citrus areas, the citrus grey mite,
(Tenuipalpidae) and broad mites (Tarsonemi- Calacarus citrifolii Keifer, in southern Africa,
dae). Mites have piercing-sucking mouthparts and the brown citrus mite, Tegolophus australis
that physically injure leaves and fruit by remov- Keifer, in coastal New South Wales and Queen-
ing cell contents and by injecting plant toxins sland, Australia.
and viruses. Mite management depends princi-
pally on protecting biological control agents,
secondarily on application of horticultural oils Tetranychidae
to foliage, and as a last resort applications of
miticides. Citrus red mite, Panonychus citri (McGregor),
was recognized as a pest in Florida in 1885, but
was notidentified in Texas until the early 1980s.
Eriophyidae In California, it was initially a pest in coastal
areas, but by the 1930s spread to more inland dis-
Citrus rust mites, Phyllocoptruta oleivora tricts. It is considered a sporadic pest, and occurs
( Ashmead), are small, light yellow, and elon- mostly on lemons and grapefruit. Adult mites are
gated mites. They are serious pests in Florida, red or purple with large pink to white hairs
Texas, and California coastal districts. These (setae) on the body. Adults and immatures feed
mites injure leaves by penetrating the lower epi- on leaves, fruit, and green twigs, but prefer the
dermal layer of cells promoting dry necrotic upper surface of young leaves. Injury to leaves
areas called mesophyll collapse. This russeting and fruit is caused by extraction of chlorophyll.
results in leaf drop, especially during dry peri- This stippling causes a grayish or silvery appear-
ods. Feeding in fruit destroys rind cells and on ance, and severe stippling can lead to mesophyll
oranges this injury is also referred to as russet- collapse. High populations may cause leaf drop
ing. Injury to grapefruit, lemons, and limes dur- and twig dieback, and fruit sunburn in summer.
ing early fruit growth causes silvering of the During dry, cold, windy conditions, high mite
peel and, if severe, results in a condition called populations may cause a condition known as fir-
shark skin. These blemishes lower the grade of ing, blasting, or burning of the foliage. There
fresh fruit, reduce fruit size, and increase fruit are many natural enemies of citrus red mites
drop. There are several natural enemies of citrus including lady beetles (species of Stethorus) and
rust mites including the parasitic fungus Hir- predaceous mites (species in the genera Galen-
sutela thompsonii Fisher. dromus, Typhlodromalus, and Euseius).
880
C Citrus Pests and their Management

Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area affected, and
site of injury
Taxa scientific/Common name Geographic area Site of injury
Arachnida
Acari
Eriophyidae
Phyllocoptruta oleivora (Ashmead) citrus world (humid areas) twigs, leaves, fruit
rust mite
Aculops pelekassi (Keifer) pink citrus rust world (humid areas) twigs, leaves, fruit
mite
Eriophyes sheldoni (Ewing) citrus bud world blossoms, fruit
mite
Tetranychidae
Panonychus citri (McGregor) citrus red world leaves, fruit, green
mite
Eutetranychus banksi (McGregor) Texas western hemisphere leaves
citrus mite
Eotetranychus sexmaculatus (Riley) western hemisphere, Asia leaves
sixspotted mite
E. lewisi (McGregor) Lewis spider mite southern California fruit
E. yumensis (McGregor) Yuma spider mite southern California, Arizona leaves, fruit, green twigs
Tetranychus urticae (Koch) twospotted world leaves
spider mite
T. pacificus (McGregor) Pacific spider mite western U.S. leaves, fruit, green twigs
T. tumidus (Banks) tumid spider mite southeastern U.S. leaves
T. mexicanus (McGregor) Mexican spider southern North America to leaves
mite South America
Tenuipalpidae
Brevipalpus phoenicis (Geijskes) red & world fruit, leaves, twigs
black flat mite
B. obovatus (Donnadieu) privet mite world fruit, leaves, twigs
B. californicus (Banks) false spider mite world fruit, leaves, twigs
B. lewisi (McGregor) citrus flat mite California, Japan fruit, leaves, twigs
Tarsonemidae
Polyphagotarsonemus latus (Banks) broad world leaves, fruit
mite
Hexapoda
Orthoptera
Acrididae
Romalea guttata (Houttuyn) eastern lub- southern U.S. leaves, fruit
ber grasshopper
Schistocerca americana (Drury) American North America leaves, fruit
grasshopper
 Citrus Pests and their Management
C 881

Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area a
ffected, and
site of injury (Continued)
Taxa scientific/Common name Geographic area Site of injury
Tettigoniidae
Scudderia furcata (Brunner von North America leaves, fruit peel
Wattenwyl)
Microcentrum retinerve (Burmeister) eastern U.S. leaves, fruit peel
angularwinged (lesser angle-wing)
katydid
M. rhombifolium (Saussure) broadwinged North America leaves, fruit peel
(greater angle-wing) katydid
Gryllidae
Hapithus agitator (Uhler) restless bush eastern U.S. leaves, small fruit
cricket
Orocharis luteolira (Walker) false jumping southeastern U.S. leaves, small fruit
bush cricket
Isoptera
Rhinotermitidae
Reticulitermes flavipes (Kollar) eastern eastern North America roots, tree bark
subterranean termite
R. hesperus (Banks) western subterranean western North America roots, tree bark
termite
Heterotermes aureus (Snyder) desert southwestern U.S., Mexico roots, tree bark
subterranean termite
Kalotermitidae
Paraneotermes simplicicornis (Banks) southwestern U.S. roots, tree bark
desert dampwood termite
Kalotermes minor (Hagen) common southwestern U.S., Mexico roots, tree bark
drywood termite
Termitidae
Gnathamitermes perplexus (Banks) desert southwestern U.S., Mexico roots, tree bark
termite
Termopsidae
Zootermopsis angusticollis (Hagen) western North America tree bark
common dampwood termite
Hemiptera
Coreidae
Leptoglossus gonagra (F.) citron bug western hemisphere fruit
L. phyllopus (L.) leaffooted bug North America fruit
L. zonatus (Dal.) western leaffooted bug North America fruit
Lygaeidae
Nysius ericae (Schillling) false chinch bug North America, Europe young stems
882
C Citrus Pests and their Management

Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area a
ffected, and
site of injury (Continued)
Taxa scientific/Common name Geographic area Site of injury
N. raphanus (Howard) false chinch bug North America young stems
Pentatomidae
Nezara viridula (L.) southern green stink world young stems and fruit
bug
Cicadellidae
Homalodisca coagulata (Say) U.S., French Polynesia green stems
glassy-winged sharpshooter
Empoasca fabae (Harris) potato world fruit
leafhopper
Flatidae
Metcalfa prunivora (Say) flatid world twigs
planthopper
Psyllidae
Diaphorina citri (Kuwayama) Asiatic citrus Asia, South America, Florida young leaves
psyllid
Aleyrodidae
Aleurocanthus woglumi (Ashby) citrus Asia, western hemisphere, leaves
blackfly world
Dialeurodes citri (Ashmead) citrus whitefly leaves
D. citrifolii (Morgan) cloudywinged Asia, western hemisphere, leaves
whitefly world
Aleurothrixus floccosus (Maskell) woolly leaves
whitefly
Parabemisia myricae (Kuwana) bayberry Asia, Israel, Venezuela, Califor- leaves
whitefly nia, Florida
Siphoninus phillyreae (Haliday) ash world, Arizona, California, leaves
whitefly Nevada
Aphididae
Toxoptera citricida (Kirkaldy) brown citrus world (not Mediterranean), leaves
aphid Florida
T. aurantii (Boyer de Fonscolombe) black world leaves
citrus aphid
Aphis spiraecola (Patch) spirea aphid world leaves
A. gossypii (Glover) melon or cotton world leaves
aphid
A. craccivora (Koch) cowpea aphid world leaves
Margarodidae
Icerya purchasi (Maskell) cottonycushion world leaves, twigs, branches
scale
 Citrus Pests and their Management
C 883

Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area a
ffected, and
site of injury (Continued)
Taxa scientific/Common name Geographic area Site of injury
Coccidae
Coccus hesperidum (L.) brown soft scale world twigs, leaves
C. pseudomagnoliarum (Kuwana) citricola world, California leaves, twigs
scale
Saissetia neglecta (De Lotto) Caribbean world, Florida leaves, twigs, fruit
black scale
S. miranda (Cockerell & Parrott) Mexican world leaves, twigs
black scale
S. oleae (Olivier) black scale world leaves, twigs
Parasaissetia coffeae (Walker) hemispheri- world leaves, twigs
cal scale
P. nigra (Nietner) nigra scale world leaves, twigs
Ceroplastes floridensis (Comstock) Florida world leaves, twigs
wax scale
C. cirripediformis (Comstock) barnacle western hemisphere leaves, twigs
scale
Diaspididae
Aonidiella aurantii (Maskell) California red world leaves, fruit, branches
scale
A. citrina (Coquillett) yellow scale world leaves, fruit
Parlatoria ziziphi (Lucas) black parlatoria world leaves, twigs, fruit
scale
P. pergandii (Comstock) chaff scale world leaves, fruit, branches
Cornuaspis (=Lepidosaphes) beckii (New- world leaves, fruit, branches
man) Purple scale
Lepidosaphes gloveri (Packard) glover world leaves, fruit, branches
scale
Unaspis citri (Comstock) citrus snow scale world branches, leaves, fruit
Chrysomphalus aonidum (L.) Florida red world leaves, green twigs,
scale
Pinnaspis aspidistrae (Signoret) fern scale world leaves, fruit
Pseudococcidae
Planococcus citri (Risso) citrus mealybug world fruit, leaves, twigs
Pseudococcus calceolariae (Maskell) citro- world fruit, leaves, twigs
philus mealybug
P. comstocki (Kuwana) Comstock world fruit, leaves, twigs
mealybug
P. longispinus (Targioni-Tozzetti) long- world fruit, leaves, twigs
tailed mealybug
Maconellicoccus hirsutus (Green) pink Africa, Asia, Australia, Carib- fruit, leaves, twigs
hibiscus mealybug bean, Florida
884
C Citrus Pests and their Management

Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area a
ffected, and
site of injury (Continued)
Taxa scientific/Common name Geographic area Site of injury
Thysanoptera
Thripidae
Frankliniella bispinosa (Morgan) flower southeastern U.S. flowers
thrips
F. kelliae (Sakimura) flower thrips southeastern U.S. flowers
Scirtothrips citri (Moulton) citrus thrips California, Arizona flowers
S. auranti (Faure) citrus thrips southern Africa flowers
S. dorsalis (Hood) citrus thrips Japan, Africa, Florida flowers
S. perseae (Nakahara) avocado thrips California flowers
Heliothrips haemorrhoidalis (Bouch) world leaves, fruit
greenhouse thrips
Chaetanaphothrips orchidii (Moulton) tropics, Florida leaves, fruit
orchid thrips
Danothrips trifasciatus (Sakimura) orchid tropics, Florida leaves, fruit
thrips
Coleoptera
Curculionidae
Diaprepes abbreviatus (L.) diaprepes root Caribbean, Florida roots, leaves
weevil
Pachnaeus litus (Germar) southern blue- Caribbean, Florida leaves, roots, fruit
green citrus root weevil
P. opalus (Oliver) northern blue-green Caribbean, Florida leaves, roots, fruit
citrus root weevil
Artipus floridanus (Horn) little leaf Caribbean, Florida leaves, roots
notcher
Asynonychus godmani (Crotch) Fuller rose world buds, leaves, roots
beetle
Diptera
Cecidomyiidae
Prodiplosis longifila (Gagn) citrus gall Florida, Caribbean, South flowers
midge America
Tephritidae
Anastrepha suspensa (Loew) Caribbean Florida, Caribbean fruit
fruit fly
A. ludens (Loew) Mexican fruit fly southwestern U.S., Mexico to fruit
South America
A. obliqua (Macquart) West Indian fruit fly Caribbean, Texas, Central and fruit
South America
A. fraterculus (Wiedemann) South Ameri- Texas south to Chile and fruit
can fruit fly Argentina
 Citrus Pests and their Management
C 885

Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area a
ffected, and
site of injury (Continued)
Taxa scientific/Common name Geographic area Site of injury
A. serpentina (Wiedemann) sapote fruit Texas south to Argentina fruit
fly
Bactrocera correcta (Bezzi) guava fruit fly southern Asia fruit
B. dorsalis (Hendel) oriental fruit fly Asia and the Pacific fruit
B. tryoni (Froggatt) Queensland fruit fly Australia fruit
B. tsuneonis (Miyake) Japanese orange fly eastern Asia fruit
Ceratitis capitata (Wiedemann) Mediter- world fruit
ranean fruit fly
C. rosa (Karsch) Natal fruit fly throughout Africa fruit
Lepidoptera
Gracillariidae
Phyllocnistis citrella (Stainton) citrus world leaves
leafminer
Marmara gulosa (Guillen & Davis) citrus California, Mexico fruit
peelminer
Tortricidae
Archips argyrospilus (Walker) fruittree North America fruit, leaves
leafroller
Argyrotaenia citrana (Fernald) orange North America, Europe fruit, leaves
tortrix
Megalopygidae
Megalopyge opercularis (J. E. Smith) puss North America leaves, nuisance
caterpillar
Papilionidae
Papilio cresphontes (Cramer) orangedog western hemisphere leaves
P. zelicaon (Lucas) California orangedog western North America leaves
Hymenoptera
Formicidae
Atta texana (Buckley) Texas leafcutting western hemisphere leaves
ant
Solenopsis invicta (Buren) red imported western hemisphere twigs, bark
fire ant
S. geminata (F.) fire ant western hemisphere twigs, bark
S. xyloni (McCook) southern fire ant southern U.S. twigs, bark
Linepithema humile (Mayr) Argentine ant western hemisphere leaves (interferes with biologi-
cal control)
Formica aerata (Francouer) native gray ant western U.S. leaves (interferes with biologi-
cal control)
886
C Citrus Pests and their Management

Citrus Pests and their Management, Table 12 Citrus arthropod pests, geographical area a
ffected, and
site of injury (Continued)
Taxa scientific/Common name Geographic area Site of injury
Gastropoda
Pulmonata
Helicidae
Helix aspersa (Mller) world fruit, leaves, bark

Texas citrus mite, Eutetranychus banksi Adults are various shades of pale amber or green
(McGregor), occurs throughout the Western hemi- with black spots along the lateral margin. Lewis
sphere. It has been a pest in Texas citrus for many spider mite generally damages fruit. Yuma spider
years, but was first detected on citrus in Florida in mite is distributed in the Coachella and Imperial
1951. Since 1955 it has increased in abundance to valleys of California and the Yuma citrus district
where it is the dominant spider mite species. Adults of Arizona. Adults are light straw to dark pink and
are tan to brownish-green with dark green to black are most numerous in winter and late spring. These
spots on the sides. Unlike citrus red mites, Texas mites feed on leaves, fruit and green twigs.
citrus mites have short, stout setae on their upper Twospotted spider mite, Tetranychus urticae
surface. This species is abundant during periods Koch, is a serious pest of many crops but is only an
ofprolonged dry weather. They feed on upper leaf occasional pest of citrus, particularly in the San
surfaces, rarely on the fruit and never on twigs, and Joaquin Valley of California. It first appears on the
their injury is similar to that of citrus red mites. underside of the leaves, but as populations increase,
Sixspotted spider mite, Eotetranychus sexmac- can be found infesting the upper leaf surface and
ulatus (Riley), was first mentioned as a sporadic fruit. Conspicuous webbing similar to that of
pest in Florida in 1886 and continues as a spring Eotetranychus species can occur in areas of heavy
season pest particularly on grapefruit and orange. infestation. As with all spider mites, damage poten-
In California, these mites occur in coastal growing tial of T. urticae varies from citrus species to citrus
areas. Adults are pale yellow to green with one to species, from year to year, and is related to weather
three pairs of dark spots on the upper surface conditions such as heat and to water stress.
which can sometimes be indistinct or missing. Several other Tetranychus species rarely attack
Sixspotted spider mites differ from citrus red mites citrus in the U.S. Pacific spider mite, T. pacificus
and Texas citrus mites in that they feed on the McGregor, is more of a pest of deciduous tree fruits,
lower leaf surface. They initially infest the petiole but has caused damage in the central valleys of
and midvein area, causing a slight depression. At California. Tumid spider mite, T. tumidus Banks, is
higher densities, raised yellow areas develop on present in the southeastern U.S. and T. mexicanus
the upper leaf surface opposite that of the estab- (McGregor) is occasionally a pest of citrus in Texas.
lished lower leaf surface colonies, and severe Worldwide, other members of Tetranychidae
defoliation can follow. are citrus pests. This list includes four Eutetrany-
Two other Eotetranychus species, Lewis spider chus species: oriental red mite, E. orientalis (Klein),
mite, E. lewisi (McGregor), and Yuma spider mite, occurring in the Mideast and Asia, and three Afri-
E. yumensis (McGregor), occur on grapefruit and can species, lowveld citrus mite, E. anneckei Meyer,
lemon in California and Arizona. Lewis spider E. africanus Klein, and E. sudanicus Elb., Eotet-
mite was found on navel oranges in southern Cali- ranychus cendanci Rimando from southeast Asia,
fornia in 1942 and continues to be a pest in the and Schizotetranychus hindustanicus (Hirst) from
southern citrus districts except in desert areas. southern India.
 Citrus Pests and their Management
C 887

Citrus Pests and their Management, Figure 58 Some common insect and mite pests of citrus. Top left,
scanning electron micrograph of citrus rust mite (photo, J. C. Allen); top right, feeding injury (dark areas
where surface temperatures did not inhibit mite feeding) by citrus rust mite (photo, J. C. Allen); second
row left, sixspotted spider mites (photo, J. Knapp); second row right, Texas citrus mite (photo, J. Knapp);
third row left, Diaprepes (citrus root) weevil (photo, J. L. Capinera); third row right, blue-green citrus
weevil (photo, P. M. Choate); bottom left, southern green stink bug (photo, J. L. Capinera); bottom right,
brown soft scale (photo, L. J. Buss).
888
C Citrus Pests and their Management

Citrus Pests and their Management, Figure 59 Some common insect and mite pests of citrus. Top left,
Florida red scale (photo, J. L. Castner); top right, cottony cushion scale adults (on stem) and immatures
(on leaf) (photo, L. J. Buss); second row left, citrus mealybug (photo, J. Knapp); second row right, adult
citrus blackflies (photo, J. Knapp); third row left, immature citrus blackflies (photo, J. Knapp); third row
right, citrus whitefly (photo, J. Knapp); bottom left, brown citrus aphid (photo, P. M. Choate); bottom
right, spirea aphid (photo, J. L. Capinera).
 Citrus Pests and their Management
C 889

Citrus Pests and their Management, Figure 60 Some common insect and mite pests of citrus. Top left,
giant swallowtail, adult form of orange dog (photo, J. L. Castner); top right, orange dog, larval form
of g iant swallowtail (photo, J. Knapp); second row left, adult citrus leaf miner (photo, J. L. Castner);
second row right, leaf mines caused by citrus leaf miner larvae (photo, J. L. Castner); third row left, Asian
cockroach (photo, J. L. Castner); third row right, eastern lubber grasshopper (photo, J. L. Capinera); bottom
left, American grasshopper (photo, J. L. Capinera); bottom right, Mediterranean fruit fly (photo, J. Knapp).
890
C Citrus Pests and their Management

Tenuipalpidae Orthoptera

Four species of false spider mites in the genus Several species of grasshopper, katydid, and cricket
Brevipalpus attack citrus in the United States. cause minor damage to citrus due to feeding with
Three of these, phoenicis (Geijskes), obovatus Don- their chewing mouthparts. These species rarely
nadieu, and californicus (Banks), are cosmopolitan warrant control actions, but when they do foliar
and occur on citrus in most parts of the world. insecticides are employed.
Infestations usually begin in the interior of the
tree canopy on the underside of leaves near the
midrib, but false spider mites are also found on Acrididae
fruit and woody tissue (twigs and branches).
Brevipalpus mites are flat, reddish, and difficult to Two grasshopper species, eastern lubber grasshop-
notice because they are small and slow moving. per, Romalea guttata (Houttuyn), and American
They have a relatively long life cycle compared grasshopper, Schistocerca americana (Drury), are
with other phytophagous mites. Brevipalpus mites sporadic pests in citrus groves. Lubber grasshopper
are economically important because they vector a adults are yellow with red and black markings and
bacilliform virus that causes leprosis. This disease American grasshoppers are light brown with black
can be found on fruit, leaves, and tree branches, markings. Injury is caused by nearly full grown
and is commonly referred to as nailhead rust. The nymphs which feed on foliage and occasionally
fourth species, B. lewisi McGregor, is found in the fruit and the most serious damage occurs when
desert and interior valleys of Californias citrus young citrus trees are defoliated.
growing region. It is a secondary invader that feeds
on rind tissue damaged by other insects. B. phoeni-
cis mites have gained fame lately when it was Tettigoniidae
discovered that they only exist in the haploid state
(one copy of chromosomes). Three species of katydid attack citrus. In Flor-
ida, only broadwinged katydid, Microcentrum
rhombifolium (Saussure), causes economic dam-
Tarsonemidae age. In California, forktailed katydid, Scudderia
furcata Brunner von Wattenwyl, is the species
Broad mite, Polyphagotarsonemus latus (Banks), is that causes damage, although angularwinged
a very important pest of Tahiti lime in Florida and katydid, M. retinerve (Burmeister), is also pres-
an infrequent pest of coastal lemons in California. ent. Katydid feeding resembles that of grasshop-
They are distributed across the world and feed on pers and is mostly restricted to foliage. When
many horticultural plants. Adult females are light fruit rinds are attacked, large, smooth, sunken
yellow, amber, or green with an indistinct white areas on the fruit surface result.
median stripe on the back, and males are similar in
color but without the stripe. Broad mites are found
on newly formed leaves or on young fruit. Heavy Gryllidae
infestations on leaves cause distortion, curling, or
stunting, but the most important damage is russet- Two species of bush cricket, restless bush cricket,
ing on young fruit. Fruit that are severely russeted Hapithus agitator Uhler, and false jumping bush
are not available for the fresh market and must be cricket, Orocharis luteolira Walker, may be present
used for processing. Natural enemies include sev- in large numbers in Florida citrus groves. Both
eral predatory mite species. species feed on small fruit, leaves, and twigs in the
 Citrus Pests and their Management
C 891

lower canopy. Fruit drop and peel blemishes may cover of groves, protection of predators and para-
result in economic damage. sitoids, application of horticultural oils, and foliar
insecticide applications.

Isoptera
Coreidae
Rhinotermitidae
Citron bug, Leptoglossus gonagra F., leaffooted bug,
The only termite species in Florida that attacks cit- L. phyllopus (L.), and western leaffooted bug, L.
rus is eastern subterranean termite, Reticulitermes zonatus (Dal.), are three plant bug species that
flavipes (Kollar). Attack starts below ground where puncture the fruit rind and suck the juices from
they feed on bark and cambium of young trees. underlying vesicles. Citron bug (Figs. 5860) is
They can become serious pests of citrus in groves dark brown to black with the front margin of
where nearby pine woods support large popula- the thorax yellow. Populations build on nearby
tions. Two other species, desert subterranean ter- melons and weeds in the grove during spring and
mite, Heterotermes aureus (Snyder), and western summer, and injury to citrus usually occurs by
subterranean termite, R. hesperus Banks, have fall. Leaffooted bug occurs in Arizona, the Gulf
damaged citrus in California. states, and Florida, where its principle host plants
are thistles (Cirsium spp.). It is dark brown with a
pale yellow line across the wings. Damage by plant
Kalotermitidae bug feeding can cause fruit drop and also may
provide access for various pathogens. Damage is
Desert dampwood termite, Paraneotermes simpli- more common on citrus fruit with thinner rinds.
cicornis (Banks), has damaged grapefruit trees in Western leaffooted bug is primarily a pest of pome-
the Coachella Valley of California by feeding on granates in California, although they will occasion-
the taproot and lateral roots. This species has also ally attack tangerines, oranges, and grapefruit.
damaged young trees in Texas. Common drywood
termite, Kalotermes minor Hagen, has damaged
citrus in California by feeding either below ground Lygaeidae
or above ground by gaining entry through wounds
or crevices. Two other termite species, desert Two false chinch bug species, Nysius ericae (Schil.)
termite, Gnathamitermes perplexus (Banks) (Ter- and N. raphanus Howard, occasionally are very
mitidae), and common dampwood termite, Zoot- destructive to young trees in California. Adults are
ermopsis angusticollis (Hagen) (Termopsidae), small and light to dark gray. Nymphs and adults
occasionally damage citrus in California. sometimes congregate in large numbers on
younger wood.

Hemiptera
Pentatomidae
At least 12 families have been documented to
occasionally cause economic damage on citrus, Southern green stink bug, Nezara viridula (L.), is
and some of the most important pests are found in green and is abundant in the fall and early winter.
this group. All Hemiptera have piercing-sucking Although other species of stink bugs attack citrus,
mouthparts, and are usually controlled by this species is usually the only one found in high
improved management of plants in the ground numbers. Most stink bugs breed on a variety of
892
C Citrus Pests and their Management

weed plants. In Florida, this insect is most destruc- Psyllidae

tive to tangerines.
Asiatic citrus psyllid, Diaphorina citri Kuwayama,
was found in southeastern Florida in 1998 and in
Cicadellidae southern Texas in 2001. Its native range includes
much of southern Asia, although it has been found
Glassy-winged sharpshooter, Homalodisca coagu- in Brazil and Honduras. African citrus psyllid, Tri-
lata (Say), is native to the southeastern United oza erytreae (Del Guercio), is the only other psyl-
States, but recently has invaded California. Speci- lid worldwide that is an economic pest of citrus.
mens from a citrus grove in Ventura County were D.citri is a small active insect with a brown, mot-
identified in 1989. This large leafhopper is dark tled appearance and is found on the lower sides of
brown to black with yellowish spots on its head new flush leaves. Damage caused by this insect is
and back. Glassy-winged sharpshooters vector either direct feeding injury resulting from the
the bacterium Xylella fastidiosa which causes withdrawal of fluids from the foliage, development
manyplant diseases. Infections affect the xylem of of sooty mold on leaves, and/or transmission of
the plant and is known as Pierces disease (grape), organisms that cause citrus greening disease,
almond leaf scorch, phony peach disease, alfalfa though this disease is not yet known from Ameri-
dwarf, and oleander leaf scorch. Citrus variegated can populations. Greening symptoms include
chlorosis, a serious disease of oranges in South mottling and yellowing of leaf veins, irregular leaf
America vectored by H. coagulata, is not currently and flower production, abnormal fruit drop, and
present in the U.S. In California, the major an unpleasant flavor in the juice. Asiatic citrus
concernis transmission of Pierces disease in vine- psyllid management in Florida is being conducted
yards. Although the disease has been present in using classical biological control, wherein parasi-
California for many years, glassy-winged sharp- toids from Asia are collected and released.
shooter is a more efficient vector than the native
sharpshooters because of higher mobility and the
ability to occupy a wide range of new habitats and Aleyrodidae
host plants.
Potato leafhopper, Empoasca fabae (Harris), is There are eight whitefly species that are considered
a common insect that attacks over 100 crop plants citrus pests. Whitefly nymphs extract phloem sap
throughout the U.S. It is an occasional pest of cit- from leaf tissues causing leaves to wilt and drop if
rus in California, especially in groves near tomato there are large populations. Feeding on such a sug-
or cotton fields in the San Joaquin Valley. Adults ary liquid diet means that the waste product, hon-
are small, greenish, and very active insects. Potato eydew, is also a very sugary liquid substance. The
leafhopper feeds on fruit by puncturing rind cells, creation of honeydew provides a food source for
causing yellowish to light brown scars. sooty mold fungus which blackens the leaves and
interferes with the trees ability to make food
through photosynthesis. Honeydew also attracts
Flatidae ants, which sometimes interfere with biological
control. The combined effects of feeding by
One flatid planthopper species, Metcalfa prunivora nymphs and associated sooty mold can result in
(Say), is an occasional pest of citrus in Texas. It is death of young trees and serious fruit yield reduc-
grayish-white and feeds on twigs. This insect only tions for producing trees. Fruit that has sooty mold
completes one generation per season. Grapefruit on it ripens later than normal fruit and is also dis-
trees appear to be favored over orange trees. colored. Many of these whitefly species that attack
 Citrus Pests and their Management
C 893

citrus are also pests of horticultural crops in green- California in 1978 and Florida in 1984. Like other
houses in northern states. whiteflies, they have several hosts other than citrus.
Citrus blackfly, Aleurocanthus woglumi Ashby, Adults are small, whitish-yellow insects. Females
is of Asian origin that was first detected in the prefer to lay eggs on young, tender foliage. Several
Western Hemisphere in Jamaica in 1913 and then natural enemies attack barberry whitefly, and the
in Key West, Florida, in 1935. It was rediscovered first populations found in Florida were already
in Ft. Lauderdale, Florida, in 1976 and spread to under natural biological control, apparently because
neighboring citrus-producing counties. It first the parasitoids were introduced with the whitefly.
invaded the lower Rio Grande Valley of Texas in Ash whitefly, Siphoninus phillyreae (Haliday),
1955 on residential citrus, and again in Browns- is a species from temperate and subtropical regions
ville in 1971 in both residential and commercial of Europe, northern Asia and north Africa. It was
groves. Adults are slate-blue with a median white first collected in southern California in 1988, and
band; the abdomen and head are bright red. is now present in Arizona and Nevada. It has arbo-
Females lay eggs on the underside of leaves in a real hosts, including several fruit trees, and in
characteristic spiral pattern. This insect has over Europe this pest causes severe damage to pear and
300 host plants, but citrus is one of its favorites. apple. Adults are small, whitish insects with a light
There is a very successful history of both classical dusting of wax. Natural enemies from Israel and
and augmentative biological control of citrus Italy were imported to California for biological
blackfly through release of two parasitic wasps in control.
many areas of the Western Hemisphere including
Mexico, Florida, and Texas.
Citrus whitefly, Dialeurodes citri (Ashmead), Aphididae
and cloudywinged whitefly, D. citrifolii (Morgan),
are two other Asian pests that invaded Florida in Aphids comprise a large and diverse group of
the late 1800s. In the 1920s, whiteflies were consid- small, fragile insects that are economically impor-
ered the most serious pests of citrus in Florida. tant because of direct damage and transmission of
They can still be a serious pest, although not at the plant diseases. Many species are winged (alate)
same level that they once were. Both species are and wingless (apterae), depending on the season.
found in Texas citrus, and citrus whitefly also is Their biologies are complex because a species may
found in California. Both citrus and cloudywinged contain both sexual and parthenogenetic (able to
whitefly adults are small and white, although reproduce without fertilization by males) forms
cloudywinged adults have a darkened area at the at different times of the season or on different
end of each wing. Many natural enemies are used hostplants.
in biological control of both whitefly species, Brown citrus aphid, Toxoptera citricida (Kirka-
including fungi, predators, and parasitoids. ldy), is one of the worlds most serious pests of cit-
Woolly whitefly, Aleurothrixus floccosus rus. It is found in southeast Asia, southern Africa,
(Maskell), was first found in Florida in the early Australia and New Zealand, South America, the
1900s and also is found in Texas and California. Caribbean, and since November 1995, in Florida.
Adults are yellowish-white and seldom fly. The last These aphids are larger than other species on citrus
nymphal stage (pupa) is surrounded by waxy fila- and have slender antennae. Wingless adults are
ments. Adult females lay eggs in a circle on mature shiny black, while nymphs are dark reddish-brown
leaves. Like other whiteflies on citrus, they are and reproduce parthenogenetically by producing
mostly controlled by natural enemies. nymphs, thus, there are no males and no eggs. They
Barberry whitefly, Parabemisia myricae damage citrus by producing copious amounts of
(Kuwana), is an Asian species first discovered in honeydew so that leaves and fruit become black
894
C Citrus Pests and their Management

with sooty mold. However, their most serious dam- acrosiphum euphorbiae (Thomas), and green
M
age to trees is by vectoring a phloem-limited virus peach aphid, Myzus persicae (Sulzer).
called citrus tristeza closterovirus. This virus causes
tristeza stem pitting disease. One of the most dev-
astating citrus crop losses ever reported followed Margarodidae
the introduction of this aphid into Brazil and
Argentina, where 16 million trees on sour orange Only one member of this family is a pest on citrus.
rootstock were killed. Several different manage- Cottony cushion scale, Icerya purchasi Maskell, is a
ment measures are being studied in Florida, includ- large scale insect originally from Australia but that
ing cultural control through rootstock improvement, has now dispersed throughout the world wherever
biological control, and chemical control. citrus is grown. It was first discovered in California
Black citrus aphid, Toxoptera aurantii (Boyer in 1868 and by the late 1880s was severely damag-
de Fonscolombe), is a related species and is found ing citrus in the southern part of the state. A coc-
throughout the world where citrus is grown. It is cinellid predator from Australia, vedalia beetle
found in all citrus areas of the U.S. It is smaller [Rodolia cardinalis (Mulsant)], was imported to the
than brown citrus aphid, with the adult apterae Los Angeles area and released in 18881889. The
dull black. The antennae and legs appear to be beetle multiplied quickly and the cottony cushion
striped. Black citrus aphid is not a serious pest of scale was brought under control. This was the first
citrus and is either a poor or nonvector of citrus successful use of a classical biological control agent
tristeza. in the U.S. Cottony cushion scale was accidentally
Spirea aphid, Aphis spiraecola Patch (formerly sent to Florida in a shipment of vedalia beetles in
known as A. citricola Van der Goot), is a small 1893. Vedalia beetle provides effective control
green aphid that originated in eastern Asia. It was nearly everywhere. Mature female scales have
found in Florida and California in the 1920s, and bright orange-red, yellow, or brown bodies that are
now is present in Texas. Aphids attack new growth partially covered by wax. The body is also covered
leaves, causing them to curl or roll, and cause dam- by a large, fluted egg sac filled with red eggs. Females
age by retarding the growth of young trees, reduc- are actually hermaphrodites, having the sex organs
ing fruit set, and production of sooty mold. Winged of both males and females. Males are rare and are
forms develop when the aphid colony becomes winged. When females self-fertilize, only hermaph-
crowded or when leaves mature. Spirea aphid rodites are produced, whereas if a hermaphrodite
reproduces parthenogenetically throughout the mates with a male, more males and hermaphro-
season, and may spend the summer on alternate dites are produced. Cottony cushion scales congre-
(non-citrus) host plants. gate along the m idrib of leaves and on trees. They
Melon or cotton aphid, Aphis gossypii Glover, damage citrus by decreasing tree vitality, increas-
is a cosmopolitan pest that feeds upon and injures ing fruit drop and defoliation.
many horticultural and agronomic crops. It is
about the same size as spirea aphid, but on citrus is
generally dark gray or dull black. It infests citrus Coccidae
during the spring flush of growth. Melon aphid
can transmit citrus tristeza virus, but apparently is Unarmored or soft scales are represented by several
not an efficient vector. species on citrus. They have no protective covering
Several other aphid species occasionally are like armored scales but do secrete a wax-like sub-
found on citrus in Florida, including cowpea stance which protects them. Female soft scales do not
aphid, Aphis craccivora Koch, oleander aphid, have wings, but are mobile until eggs start to form.
A. nerii (Boyer de Fonscolombe), potato aphid, Adult males usually have one pair of wings, and dont
 Citrus Pests and their Management
C 895

live very long. Young scales are called crawlers, and is found in the southern citrus districts of Califor-
they either hatch from eggs or are born alive. Later nia and in Florida. This scales appearance is similar
stages produce large amounts of honeydew upon to that of other black scales. Excreted honeydew
which sooty mold fungus grows and, along with supports growth of sooty mold and feeding reduces
armored scales, are among the most serious pests of tree vigor and causes leaf and fruit drop.
citrus in the world. Many parasitoid species attack Four other species of soft scales are occasional
and control soft scales, but ants will protect scale pests in the U.S. Hemispherical scale, Parasaissetia
populations from their natural enemies. coffeae (Walker), is widely distributed across the
Two species of Coccus are citrus pests. Brown world and is found in the coastal sections of south-
soft scale, Coccus hesperidum L., has a worldwide ern California. Nigra scale, P. nigra (Nietner), is a
distribution on a variety of plants. In Florida, it tropical species that is found rarely in California.
is not a pest of concern, but is the most serious Florida wax scale, Ceroplastes floridensis Comstock,
soft scale pest in Texas. The scale body is flat and is an important pest of citrus in the Mideast and
oval, light brown to yellowish. Females give birth Asia, and is occasionally a problem in Florida.
to pale yellow crawlers. Brown soft scale is a more Adults are highly convex, somewhat angular, and
serious problem on young trees due to feeding oval. Males have not been reported. Barnacle scale,
and honeydew production. Mature trees suffer C. cirripediformis (Comstock), is an occasional pest
from reduced vigor, twig dieback, and reduced of citrus in California, Texas, Florida, and Mexico.
fruit yields. There are several parasitic wasps that The thick wax coat is dirty white and is divided
attack brown soft scale. into distinct plates, one on top and six on the side.
Citricola scale, C. pseudomagnoliarum
(Kuwana), is found in California. It is more of a
serious pest in the San Joaquin Valley than other Diaspididae
citrus districts. Young citricola scale are very flat
and more transparent looking than young brown Armored scales are represented by several species
soft scale, while mature citricola scales are gray. on citrus. Females and immature males are covered
Crawlers appear in late April and settle on the by coatings of wax and cast skins (exuviae) of earlier
underside of leaves. By November, they migrate to instars. As crawlers, females insert their mouthparts
twigs, where their development speeds up. By the into the plant and never move again. They will lay
next spring, mature female scales lay eggs which either eggs or live young under the armor (cover),
hatch into crawlers. Damage to citrus is similar to depending on species. Armored scales injure citrus
that of brown soft scale. by feeding, not by production of honeydew and
Three species of black scale, Saissetia, are citrus resulting sooty mold. The level of damage varies
pests. Caribbean black scale, S. neglecta De Lotto, is greatly among armored scale species.
a pest in Florida. Adult females are brown to black California red scale, Aonidiella aurantii
and have a tough circular or hemispherical shell. (Maskell), and yellow scale, A. citrina (Coquillett), are
Two lateral ridges and one longitudinal ridge cre- two armored scales that are major pests in the citrus-
ate an H shaped pattern. Crawlers move from growing districts of California. California red scale is
leaves to small twigs and fruit stems. Females lay found also in Texas, while yellow scale is found in
eggs and usually reproduce without fertilization by Florida. Adult females have circular covers. Imma-
males (parthenogenesis). Mexican black scale, S. ture male covers are more elongated, and adults are
miranda (Cockerell & Parrott), is found in the small, two-winged insects that live for only a few
southern U.S. and Mexico on a wide variety of hours. Females give birth to live young (crawlers),
plants. It is seldom found in Florida. Black scale, which search for locations to settle. California red
S.oleae (Olivier), a pest of olive trees and oleander, scale infest all parts of the tree, including leaves, twigs,
896
C Citrus Pests and their Management

branches, and fruit. Yellow scale is found rarely on are small winged insects. Females lays eggs under
twigs and branches. Plant tissue is injured as a result her scale cover. Purple scales prefer trees with a
of plant fluid removal and injection of toxic sub- dense canopy and infest leaves, wood, and fruit.
stances. Damage is caused by leaf yellowing, leaf On leaves, they cause yellow chlorotic spots which
drop, and fruit drop, and serious damage to trees lead to defoliation. Fruit quality is affected because
occurs when twigs and branches are killed. Biological fruit infested with scales do not change color.
control is an important management tactic used Glover scale, Lepidosaphes gloveri (Packard),
against these scales, with Aphytis and Comperiella also known as long scale, is found in association
parasitoids mass reared and released. with purple scale. It is found in Florida, Texas, and
Black parlatoria or ebony scale, Parlatoria limited areas in California. Adult female covers
ziziphi (Lucas), was discovered infesting citrus in are long and narrow, purplish-brown, with white
southern Florida in 1985. It is considered a major to purple colored scale bodies. They infest leaves,
pest in countries bordering the Mediterranean, twigs, bark, and fruit, and when on woody bark,
tropical Asia, parts of South America, and the orient with the grain of the bark. Parasitic wasps
Caribbean. The female covering is black, generally keep this species under biological
rectangular, and with a fluted surface while the control.
male c overing is white, except at one end, flat, Citrus snow scale, Unaspis citri (Comstock),
and elongate. The armor is almost impossible to was known to infest citrus since 1880, but became
remove from host tissues. Scales infest leaves, an important pest in Florida in the early 1960s.
twigs, and fruit, and because they adhere so Replacement of trees after a severe freeze in 1962
strongly, cause rejection of fresh fruit in markets. brought thousands of infested nursery stock to
Large populations cause chlorosis and early drop groves. Female covers are oyster-shaped with a
of leaves, dieback of twigs and branches, and dis- longitudinal ridge, and are purplish-brown with a
tortion of fruit. gray border. Immature male covers are white with
Chaff scale, Parlatoria pergandii Comstock, a center ridge and fainter ridges on either side.
has a similar distribution as black parlatoria scale, Adult males are winged and yellowish. Although
except that it is also found in the Gulf states. This they infest all parts of a tree, citrus snow scales pri-
is the most common armored scale in Texas. The marily attack the trunk and large branches. Declin-
scale covering is circular to elongated, thin, and ing tree vigor and lower fruit production result
brown to gray. The female body, eggs and crawlers from high populations.
are purplish. Chaff scales often are found in depres- Florida red scale, Chrysomphalus aonidum
sions on fruit or along midribs on leaves, and are (L.), affects citrus in Florida and Texas, but is sel-
also found on tree bark. When fruit mature, areas dom found in groves in California. It was intro-
around the scale remain green, rendering the fruit duced into Florida from Cuba in 1874 and was a
unsuitable for the fresh market. major pest until release of the parasitoid Aphytis
Purple scale, Cornuaspis (=Lepidosaphes) holoxanthus DeBach in 1960. In Texas, California
beckii (Newman), was the most common and red scale and Florida red scale can be misidenti-
damaging armored scale in Florida prior to 1960 fied. Florida red scale female covers are more
and the introduction of a parasitoid (Aphytis lepi- circular, are dark reddish-brown, and have a con-
dosaphes Compere). It is found in Texas and in spicuous light brown nipple. The females body is
more humid areas of California. Adult females are yellow, and the females cover is more easily
curved and oyster-shaped (broad and tapering), removed than those of California red scale. Adult
with a purplish-brown cover and a white scale males are winged insects that fertilize adult
body color. Immature male covers are shorter and females. Females lay eggs which hatch into very
more slender than those of the female. Adult males active, bright yellow crawlers. Unlike other
 Citrus Pests and their Management
C 897

armored scales, Florida red scales attack only native of Asia, is primarily a pest on lemons in the
leaves and fruit. On leaves, they cause yellow chlo- San Joaquin Valley of California. It differs from
rotic spots which lead to defoliation. They also citrus mealybug by having a thicker wax cover and
cause yellow spots on fruit which render it unmar- two spines at the posterior end. The citrophilus
ketable as fresh fruit. mealybug, P. calceolariae (Maskell), and longtailed
Fern scale, Pinnaspis aspidistrae (Signoret), is mealybug, P. longispinus (Targioni-Tozzetti), are
found in Florida, South America, and Japan. Female present in California. Longtailed mealybugs differ
scale covers are pale brown, flat, and pear-shaped. from other species because young are born as
Immature males are white and elongated, resem- active nymphs. They are usually not a problem on
bling male citrus snow scale. They are found only citrus because of the work of natural enemies.
on leaves and fruit. They have a wide host range An exotic species, pink hibiscus mealybug,
and never cause economic damage to citrus. Maconellicoccus hirsutus (Green), is a serious pest
of citrus and other plants in Africa (Egypt), south-
east Asia and northern Australia. It was found in
Pseudococcidae the Caribbean in 1994, in southern California in
August 1999, and just recently in Florida in June
Mealybugs are soft, oval, flat, distinctly segmented 2002. It has a high reproductive rate and infests
insects covered with a white, mealy wax that many horticultural, ornamental, and agronomic
extends into spines (filaments) along the body crops. This mealybug feeds on soft tissues of plants
margin and the posterior end. Unlike scales, and injects a toxin which causes leaf curling and
mealybugs remain motile throughout their life distortion. Feeding also promotes growth of sooty
cycle. Species differ in external appearance by the mold because of honeydew excretion.
waxy covering and the thickness and length of
filaments. Mealybugs injure plants by extracting
sap from trees and secreting large amounts of Thysanoptera
honeydew, which serves as a food source for sooty
mold. Feeding on foliage and twigs reduces the Thrips are a group of small, elongated insects with
vigor of trees and may result in defoliation. Feed- fringed wings. Their mouthparts have been
ing on fruit results in distortions and scars which described as rasping-sucking, but it is likely that
lower the grade of the produce. certain parts pierce rather than rasp leaf and
Citrus mealybug, Planococcus citri (Risso), flower tissue. The majority of thrips species feed
occurs in Florida, Texas, and in the coastal citrus on plants, but some feed on fungus and others are
districts in California. They have pinkish bodies predaceous on small arthropods. Life cycles con-
that are visible under the powdery wax. Adult sist of an egg stage, two larval stages that feed, one
males are winged insects. Eggs are laid in a white prepupal stage that doesnt feed, one non-feeding
cottony mass, and nymphs are light yellow. Citrus pupal stage, and an adult stage that feeds. Several
mealybugs prefer protected areas such as the calyx species are pests on citrus.
of fruit or along the stem. Feeding along the stem
usually results in fruit drop. There are several nat-
ural enemies including pathogens, parasitoids, and Thripidae
the ladybird beetle, Cryptolaemus montrouzieri
(Mulsant). This predator was imported from Two species of flower thrips are found on citrus in
Australia to California in 1891. Florida. Frankliniella bispinosa (Morgan) occurs
Three species of Pseudococcus are citrus pests. throughout the state, while F. kelliae Sakimura is
Comstock mealybug, P. comstocki (Kuwana), a found in central and southern growing areas. Both
898
C Citrus Pests and their Management

species have wide host ranges, but on citrus have to growers is restricted to red grapefruit varieties,
been shown to injure navel and Valencia oranges. but in California greenhouse thrips attack Valen-
Flower thrips migrate aerially during the flower- cia oranges, lemons, and avocados. Feeding
ing cycle from January through April. They have from fruit epidermal cells removes pigment. No
been documented to feed, oviposit, and develop scars or deformities develop, but fruit may be
on various flower parts, such as the ovary, style, downgraded.
petals, anthers, pistil, and calyx. Resulting damage Two other thrips species occur in Florida cit-
is by reducing fruit set. Recently a relationship rus. Chaetanaphothrips orchidii (Moulton) females
between thrips feeding and the fungal pathogen are yellow with distinctive dark banding on the
Colletotrichum acutatum J. H. Simmonds was wings. They are most common on grapefruit and
associated with post bloom fruit drop. are present throughout the year. Fruit injury
Three Scirtothrips species are recognized as resembles that of greenhouse thrips. Danothrips
citrus pests, S. auranti Faure in South Africa, trifasciatus Sakimura is present in low numbers in
S. dorsalis Hood in Japan and Africa, and citrus association with C. orchidii.
thrips, S. citri (Moulton), in California and Ari-
zona. Citrus thrips is an important pest on navel
oranges in the San Joaquin Valley, on desert citrus Coleoptera
including grapefruit and tangerine, and on lem-
ons grown in the coastal districts. They are small, Beetles represent the largest order of insects in
yellowish-orange, and have fringed wings. They number of species. As might be expected, this is an
feed on leaves, young fruit (especially under the extremely diverse group with species that special-
sepals), and green twigs. Leaf injury is along the ize in phytophagy (plant feeding), zoophagy or
midrib or leaf margins, causing leaf deformities, carnivory (feeding on animals, usually as preda-
and injury to fruit is by puncturing epidermal tors or parasitoids), fungivory (fungus-feeding),
cells, leaving uniform scars. Scars in young fruit and saprophagy (feeding on dead material). How-
form a ring around the stem, and as the fruit ever, relatively few species specialize or infest
grows, the ring increases and is found further citrus. The primary family of beetles that attack
from the stem. Natural enemies include several citrus is Curculionidae, the weevils.
predators including mites (Eusieus tularensis Diaprepes weevil, Diaprepes abbreviatus (L.),
Congdon). A fourth species, S. perseae Nakahara, has several other common names such as Apopka
recently was found infesting avocado in southern weevil and sugarcane rootstalk borer weevil. It is
California. It is not known if this Central Ameri- native to the Caribbean, and is only found in the
can native will attack citrus. U.S. in Florida and Texas. It was first reported in
Greenhouse thrips, Heliothrips haemorrhoid- central Florida (Apopka) in 1964 and since has
alis (Bouch), is a New World species that is also spread over the southern two-thirds of the state.
found in Europe, the Mideast and north Africa. Adults are black with white, reddish, or yellowish
In the U.S. it is found in central and southern scales on the wing covers (elytra). This is the larg-
Florida and southern California along the coast. est weevil species that infests citrus in Florida.
Adult females are black with a reticulated body Eggs are laid on new flush leaves that have been
surface and yellow-white legs. Greenhouse thrips clustered or glued together by females using an
develop parthenogenetically. They injure rind tis- adhesive material. Young larvae fall to the soil and
sue by feeding on epidermal cells, which may begin feeding on roots. During the course of its
cause ring spotting or irregular russeting. Injury development, which can last anywhere between
occurs where fruits, fruits and leaves, or fruits 6and 24 months, larvae may consume any part of
and twigs are in contact. In Florida economic loss the trees root system. Diaprepes pupate in the soil
 Citrus Pests and their Management
C 899

and then emerge to find mates. Although adults flightless, and are all female. Unlike the other spe-
fly, they do not disperse far from their emergence cies discussed in this group, A. floridanus has a
site. Adults may nibble or notch the margin of much shorter life cycle. Larvae can complete devel-
leaves, but important injury is caused by larval opment in as little as 35 days. Also unlike the other
feeding. Young trees can be killed by a single larva species, larvae feed only on smaller root parts such
and older trees suffer when major roots or the as pioneer and fibrous sections.
taproot is girdled. Feeding on roots also allows for
the introduction of plant pathogens, which injure
an already stressed tree. There is a considerable Diptera
amount of research being conducted by federal
and state entomologists in Florida in detecting, This large, diverse order contains two families that
controlling, and preventing damage by this insect. attack citrus. Gall midges (Cecidomyiidae) are
Two species of blue-green citrus root weevils infrequent pests of citrus buds and flowers. Fruit
are found in Florida. Pachnaeus litus (Germar) flies (Tephritidae) from the genera Anastrepha,
is found in south-central to southern Florida; Bactrocera, and Ceratitis attack fruits and vegeta-
P.opalus (Oliver) is commonly found in north and bles. Females insert eggs under the skin of fruit
north-central Florida. At least two Pachnaeus spe- and larvae feed within, causing direct injury and
cies also occur in Texas citrus groves. Adults of decay. Fruit fly species are also quarantine pests,
both species are gray-green to aqua and can be where whole loads or even a seasons worth of pro-
separated by structures on the wing covers. Larvae duce may be denied entry within regions of a
are root feeders and will attack all root parts except country or among countries because of the threat
the crown. Adults feed by notching the leaf mar- of infestation.
gins. As with other citrus root weevils, many other
plant species can be used as hosts.
Fuller rose beetle, Asynonychus godmani Cecidomyiidae
Crotch, is found in Florida, Texas and California.
It was reported in Florida in 1916 and has been The citrus gall midge, Prodiplosis longifila Gagn,
known as Pantomorus cervinus (Boheman) and A. is a small black-yellowish fly that attacks citrus,
cervinus (Boheman). Its distribution in Florida tomatoes, potatoes, and cotton in Florida, the
ranges from the southern tip to north-central Caribbean, and South America. Large populations
areas. Adults are brownish-gray, flightless, and are developed in 1984 on limes in southern Florida.
all females that develop parthenogenetically. Eggs Eggs are laid in flower buds and larvae feed on
are usually laid under the calyx of the fruit. Larvae flowers, injuring several flower structures. Larvae
take from 9 to 12 months to develop and feed on complete development, drop to the ground, and
all root parts except for the crown. Fuller rose bee- pupate in the soil. Damage occurs when flowers
tle is not a serious economic pest by itself, but are killed and drop from the tree.
because eggs are laid on fruit, they are a quaran-
tine pest when fruit is to be exported. One man-
agement tactic developed in California is the use Tephritidae
of parasitic nematodes [Steinernema carpocapse
(Weiser)] for biological control. Three genera, Anastrepha, Bactrocera, and Ceratitis,
The smallest root weevil in Florida is the little contain fruit fly species that are considered serious
leaf notcher, Artipus floridanus Horn. This insect citrus pests. Eggs are inserted under the skin of
was reported as early as 1876 and is found mostly various fruits, berries, nuts, and vegetables. Larvae
along the east coast. Adults are grayish-white, then mine the host, promoting decay and causing
900
C Citrus Pests and their Management

the fruit to be unmarketable. Fruit flies are direct Three other Anastrepha species are pests in
pests in countries where they are established, but the Western Hemisphere and are potential pests in
are also regulatory or quarantine pests in coun- Florida if they become established. The West Indian
tries where particular species are not established. fruit fly, A. obliqua (Macquart), is nearly identical
There has been much research worldwide into to A. suspensa and occurs throughout the Carib-
detection or monitoring of adults, and manage- bean, southern Texas, and south to Argentina. It
ment tactics other than insecticide sprays, such was found in Key West in the 1930s during surveys
as bait stations, sterile insect technique (releasing for A. suspensa. It was also eradicated and hasnt
sterile flies to mate with wild flies) and biological been found in Florida since 1935. This species has
control. a long host list, but mangos (Mangifera indica L.)
Species in the genus Anastrepha are New World and guavas can be economically damaged. It rarely
flies that attack tropical and subtropical fruits. The attacks citrus. The South American fruit fly, A.
Mexican fruit fly, A. ludens (Loew), is important in fraterculus (Wiedemann), is economically the most
the United States because it is subtropical rather important species in South America (Brazil, Argen-
than tropical. It is found in southern Texas, Califor- tina, Peru), but is also found in Central America
nia and Arizona, where continuous detection and northward to southern Texas. However, this spe-
eradication programs, such as sterile insect tech- cies may be part of a species complex since speci-
nique, are in place. It was detected in Florida in 1934 mens identified as A. fraterculus vary widely from
and again in 1972, but did not become established. populations in Brazil, Mexico, and Texas. It also has
This relatively large yellow-brown fly is native to a wide host range that includes tropical, subtropi-
Mexico but can be found as far south as northern cal and temperate fruits including sweet orange
South America. In Texas, grapefruit appears to be and peach. The sapote or serpentine fruit fly, A. ser-
the preferred host, and several deciduous hosts such pentina (Wiedemann), is a brown fly that is com-
as peach, pear and apple also can be attacked. mon from southern Texas to Mexico, Central
The Caribbean fruit fly, A. suspensa (Loew), is America and South America. It can be a severe pest
a yellow-brown fly that is native to the West Indies. of ripened sapote (Calocarpum spp.) and sapodilla
This species has an interesting history in Florida. It (Manilkara zapota L.) in Mexico. Although many
was documented in Key West in 1931, although flies are trapped in south Texas, there is only one
was believed to have been established for many record of an infestation in grapefruit.
years. This strain attacked guavas (Psidium gua- Species in the genus Bactrocera (formerly
java L.) and noneconomic fruits but did not infest Dacus) are flies native to Africa, the Mediterra-
citrus. This strain differed from populations found nean, Asia and the Pacific. None of the citrus-in-
in Puerto Rico that did feed on citrus. The Key festing species are currently established on the
West populations apparently were eradicated mainland United States, but several are occasion-
through fruit removal and insecticide sprays and ally trapped in California and Florida. The oriental
died out sometime after 1936. Since 1965, a new fruit fly, B. dorsalis (Hendel), is a variably colored
introduction into Florida spread from southern medium-sized fly that infests fruits and vegetables
areas to central Florida groves. It attacks mature throughout Asia (Pakistan, India, Vietnam, Philip-
and overripe citrus, and its seriousness as a pest is pines, Japan, etc.) and the Pacific, including Hawaii.
still being investigated. Exports require an elabo- It was introduced into Hawaii in the mid-1940s by
rate fly-free zone system that requires several mil- returning servicemen that were stationed on sev-
lion dollars a year to maintain. Even so, in some eral Pacific islands, but has become partially under
years up to 16,000 hectares (40,000 acres) of grape- control through the introduction of parasitoids. In
fruit have been lost to export markets because of Japan, several management tactics including the
fly captures within protocol areas. use of attractant baits and sterile male release has
 Citrus Pests and their Management
C 901

been successful. Guava fruit fly, B. correcta (Bezzi), quarantines, cultural control (waste removal and
is a small, brightly colored, predominately black disposal of culls), release of sterile males, and bio-
fly that occurs in southern and southeastern Asia. logical control. Much research has been com-
Adults have been trapped in California and Flor- pleted designing traps and lures for detection of
ida but it hasnt established. It is a potential pest of Medfly.
citrus, peach, and other subtropical and tropical Two other Ceratitis species are pests in Africa.
fruits. Queensland fruit fly, B. tryoni (Froggatt), is The Natal fruit fly, C. rosa Karsch, is slightly larger
a small brown-yellow fly that is wasplike in appear- than the Medfly and similar in appearance. It is
ance. The distribution of this species includes the distributed throughout sub-Saharan Africa and on
eastern half of Australia, although flies have been the Indian Ocean islands of Mauritius and
trapped in Western Australia, New Guinea, and Runion. This fly overwinters in the adult stage
several Pacific islands. It is a pest of pome and and can withstand below-freezing temperatures. It
stone fruits as well as citrus. Biologically, this spe- attacks many temperate stone and pome fruits
cies is more temperate in distribution and does including peach, nectarine, apricot, apple and pear.
not breed continuously but overwinters as an Although the Natal fruit fly has been intercepted
adult. Japanese orange fly, B. tsuneonis (Miyake), in the United States in produce, it has never been
infests orange, grapefruit and mandarin orange in captured as an escapee. If accidentally introduced,
Japan, southwestern China and probably Taiwan. it could prove to be a serious pest. C. malagassa
There have been no interceptions of this fly in the Munro damages citrus fruit on the island of Mad-
U.S., mostly because of an embargo of citrus from agascar. It has a smaller geographical distribution
infested areas. Changes to the embargo laws may than the other two Ceratitis species discussed.
increase the chances of introducing this pest.
Species in the genus Ceratitis are originally
from sub-Saharan Africa, but now some have a Lepidoptera
worldwide distribution. Mediterranean fruit fly,
Medfly, C. capitata (Wiedemann), is a yellowish There are several families of moths and butterflies
brown fly that is one of the worlds most destruc- that attack the fruit or foliage of citrus. Fruit-
tive fruit pests. It has been established in Hawaii piercing moths (Noctuidae) are pests in southern
since 1910, and has been detected at different Africa, Australia, and east Asia. They include spe-
times in California, Florida, and Texas. For cies in the genera Achaea, Calpe, Emaenas, Ercheia,
instance, Medfly has been detected in Florida 16 Gonodonta, Othreis, and Serrodes. None of these
times since 1929, and only massive and expensive are apparently established in the U.S. Other noctu-
eradication programs have kept it from becoming ids, such as cabbage looper, Trichoplusia ni (Hb-
established in the continental U.S. As with other ner) and beet armyworm, Spodoptera exigua
tephritid fruit flies, eggs are laid slightly beneath (Hbner) can cause considerable damage to nurs-
the fruits surface. Larvae feed within the fruit, ery stock and young citrus. Bollworm, Helicoverpa
and generally the fruit drops to the ground and zea (Boddie), is a pest of citrus in Africa in areas
larvae move into the soil to pupate. Over 260 spe- when cotton is planted nearby, but is seldom a
cies of hosts have been recorded, with peach, nec- problem on citrus.
tarine, orange, grapefruit, apricot, and pear being
some of the Medflys favorites. In addition to the
reduction in citrus yield, infested areas have the Gracillariidae
additional expense of control measures and costly
sorting for fresh and processing fruit. Detection Two species in this family are pests of citrus in the
and control of the Medfly has included trapping, U.S. Citrus leafminer, Phyllocnistis citrella Stainton,
902
C Citrus Pests and their Management

is an Asian species that has recently spread to newly set fruit, and later on mature fruit. Unlike
northern Africa, Central America and the United many tortricids, eggs are generally laid on woody
States. It was found in late May 1993 in Dade tissue. Orange tortrix, Argyrotaenia citrana (Fer-
County, Florida, late August 1994 in the Rio Grande nald), is primarily a pest of Valencia and navel
Valley of Texas, and in 2000 in Imperial County, oranges in southern California. Eggs are laid on
California. Hosts include citrus and related species stems, fruit and upper leaf surfaces, and larvae pri-
within the plant family Rutaceae. Eggs are laid on marily feed on new growth leaves and fruit. Fruit
the underside of leaves and green-yellow larvae feeding is around the sepals and holes can be eaten
enter leaves and begin forming mines. Pupation is in the peel.
within the mine and white and silver-colored adults Several other tortricid species occasionally
emerge during the morning. Injury to foliage and can attack citrus in the United States. These include
fruit can be extensive with large populations, and garden tortrix, Ptycholama peritana (Clemens),
damage is more serious to nursery trees or newly variegated leafroller, Platynota flavedana Clemens,
planted groves. This pest appears to be able to be omnivorous leafroller, Platynota stultana Walsing-
controlled through the use of natural enemies. ham, and western avocado leafroller, Amorbia
Several Asian parasitoid species have been col- cuneana (Walsingham). These species are not spe-
lected from Australia and released in the United cific to citrus and attack several other crops and
States, but native natural enemies also show promise ornamentals. Tortricids found in other citrus-pro-
in reducing populations. ducing countries include Archips occidentalis
Citrus peelminer, Marmara gulosa Guillen (Walsingham) and Tortrix capensana Walker, pests
Davis, has seriously damaged citrus in several in South Africa, Archips rosanus (L.) in Greece,
areas in California including the Coachella and and Epiphyas postvittana (Walker) in Australia.
San Joaquin valleys and Kern County. Larvae bur- Like the other leafrollers, these species have rela-
row within the epidermal surface of the fruit caus- tively wide host plant ranges.
ing serpentine mines. It often attacks fruit located
near alternate hosts such as oleander and willows.
Although it seldom affects more than 5% of the Megalopygidae
fruit, in 2000 citrus peelminer infested almost 70%
of the fruit in some groves. It also expanded its Puss caterpillars, Megalopyge opercularis (J. E.
geographic and host ranges in California. Research Smith) are pests more because of their medical
is now being conducted to see if infested fruit importance than through defoliation. This cater-
imported from Mexico during 1998 included a pillar is the larval form of the southern flannel
new biotype or species of peelminer. moth, which is found throughout the southeast
and into Texas. Human disease from puss caterpil-
lars usually arises from direct contact to their
Tortricidae urticating hairs. Field workers pruning or harvest-
ing fruit are usually the people who come in con-
Two species can cause extensive injury to citrus. tact with these insects.
Fruittree leafroller, Archips argyrospilus Walker,
has been a pest of citrus in California for many
years. This species is widespread across the United Papilionidae
States feeding on a wide variety of hosts. It has
damaged apples in Michigan, New York and Penn- A large number of species of swallowtail butter-
sylvania, and bald cypress in Louisiana. On citrus, fly larvae (orangedogs) feed on citrus foliage
it feeds on spring flush growth of leaves, flowers, throughout the world. Orangedogs are named
 Citrus Pests and their Management
C 903

because when disturbed, larvae stick out orange- Several ant species are problems on citrus
colored osmeteria (scent organs located behind because of their interference in the development of
the head) and give off a strong, disagreeable odor. biological control programs. Argentine ants, Linepi-
Two species are common in the U.S. Giant swal- thema humile (Mayr) (formerly known as Iri-
lowtail, Papilio cresphontes Cramer, is distributed domyrmex humilis), and native gray ants, Formica
throughout the U.S. except in the far west. It is an aerata Francouer, feed on honeydew excreted by
occasional pest of citrus in Florida and Texas, soft scales, mealybugs, whiteflies, and aphids. In this
where young trees in groves or nurseries can be relationship, they protect these species from natural
quickly defoliated. Adults are large dark butter- enemies. They even protect other scales species that
flies with diagonal yellow bars on the forewings. dont produce honeydew, such as California red
Adults can be attracted to plants in butterfly scale, from potential biological control agents.
gardens. Citrus California orangedog or black Gastropoda: Pulmonata
anise swallowtail, P. zelicaon Lucas, is a native
butterfly that feeds on perennial anise (sweet fen-
nel) and citrus. Like other Papilio larvae, these Helicidae
larvae are more damaging to youngtrees.
Although snails are not insects, they can be serious
pests of citrus by feeding on leaves, buds, flowers,
Hymenoptera fruit and bark. The brown garden snail, Helix aspersa
Mller, is a European species that is found in Cali-
This order contains ants, wasps, and bees. Wasps fornia and in most southeastern states. However, it
and bees can be pests when fruit workers contact is not established in Florida. This species is her-
colonies in the field. maphroditic (having both male and female organs),
so during mating mutual fertilization can occur.
Large populations can be found in citrus groves
Formicidae where extensive damage to leaves and fruit may
occur. At one time, snails were only found in Cali-
In the Rio Grande Valley, the Texas leafcutting ant, fornias humid and cool coastal areas, but because of
Atta texana (Buckley), is the most serious ant pest. drip irrigation and no-till weed control, snails are
These reddish-brown ants remove leaves from now found in several citrus-growing districts.
trees to culture fungus for food. In areas of large
colonies, single trees may be defoliated in a single
night. Large areas underground are excavated and Citrus Pest Management
may present problems for farm machinery. Multi-
ple defoliation of young trees can slow growth or Fresh or Processing Market
cause tree death.
Fire ant species in the United States can be One of the most important decisions citrus grow-
citrus pests and include red imported fire ant, ers make at the beginning of a season is whether to
Solenopsis invicta Buren, native fire ant, S. gemi- market their fruit for the fresh market or processed
nata (F.), and southern fire ant, S. xyloni McCook. market. For maximum profitability of fresh market
Fire ants injure trees by attacking twigs, bark, and fruit, a high level of pest control is needed to reduce
leaves, and young trees can be completely girdled. the number of external blemishes. This level of
Young trees also can be damaged when bark quality is not needed for fruit destined for the pro-
beneath tree wraps are injured and provide a point cessing market. Several factors are involved in the
of entry for fungi. decision-making process for market destination:
904
C Citrus Pests and their Management

grove location and accessibility of markets, fruit horticultural techniques to reduce the likelihood
variety grown, grove history for pests, and profit- of pest problems. Several cultural control techniques
ability desired. Growers may decide that their fruit may be completed before or during grove estab-
will be managed for the fresh market, but after lishment, such as site selection, rootstock choice,
spring bloom several abiotic (weather-related) or and the use of virus-free budwood. Techniques
biotic (tree health, disease pressure, high pest den- accomplished after grove establishment include
sities) factors may change that decision. Therefore, tree nutrition, irrigation, plant waste removal,
the market decision that growers make impact the pruning practices, and harvesting practices.
management input in groves. The second management strategy that grow-
ers may employ is biological control, which is
the use of naturally occurring or imported para-
Sampling and Thresholds sitoids, predators, or pathogens to reduce pest
populations. The citrus industry historically has
Citrus growers need to be able to identify and pro- encouraged the use of natural enemies, there-
vide estimates of the numbers of pests and natural fore, many citrus pests are partially or fully under
enemies present in their groves. The frequency and biological control. However, biological control
methods used to sample or monitor for pests and systems are easily disturbed by pesticide use.
natural enemies varies depending on the pest being The third management strategy used by citrus
sampled and the time invested. For instance, it is growers is chemical control. The products that are
suggested that sampling for citrus rust mites be used include synthetic chemicals such as insecti-
every 2 weeks during the season because their pop- cides, acaricides, and horticultural oils, which have
ulations can expand quickly. Most other pests are different ways of killing arthropods (mode of
monitored on a monthly basis. Sampling may action). Biological products such as bacteria, fungi,
involve trees randomly selected for each period or or viruses also are available and can be used in a
permanently designated station trees. Trees that similar fashion as chemicals. Before chemical con-
are randomly selected should be dispersed suffi- trol is used, several factors must be considered. Is
ciently to be representative of the grove. Station the pesticide labeled for use against the target pest
trees are representative trees that are flagged and and is it efficacious? What is the cost effectiveness
visited each sampling period. In both cases, accu- of the product and what are the hazards to natural
rate and descriptive records should be kept. Action enemies, the environment, the fruit, and the appli-
thresholds are pest population densities that, when cators? Finally, what is the impact of the intended
reached, signal to the grower that some type of cor- product on the development of pest resistance. All
rective action is needed. Thresholds for a certain citrus-producing states have guides available each
pest species will vary depending on the fruit mar- season for growers. These guides contain lists of
ket destination, time of season, and abundance of labeled products and directions on how to use
appropriate natural enemies. Thresholds have been them against the important pests in those areas.
developed by entomologists for many of the impor- Each state also has entomologists who compare
tant citrus pests, and are designed to provide the efficacy of new and existing products under
enough time for growers to take corrective action. the conditions of the local growing areas.

References
Management Strategies
Hui S (1999) Sweet oranges: the biogeography of Citrus sinen-
Growers use three general approaches for control sis. Available at http://www.aquapulse.net/knowledge/
of citrus pests. Cultural control is defined as using orange.html. Accessed 4 April, 1999
 Cladogram
C 905

Morton JF (1987) Fruits of warm climates, Media Incorp, Cixiidae

Miami, FL. Available at http://www.hort.purdue.edu/
newcrop/morton/index.html
Reuther W, Calavan EC, Carman GE (eds) (1989) The citrus A family of insects in the superfamily Fulgoroidae
industry, vol 5: crop protection, postharvest technology, (order Hemiptera). They sometimes are called
and early history of citrus research in California. Divi- planthoppers.
sion of Agriculture and Natural Resources, University of
California, 374 pp Bugs
Texas A&M University. Available at http://aggie-horticulture.
tamu.edu/citrus/industry.htm
University of California. UC pest management guidelines
pests of Citrus. Available at http://axp.ipm.ucdavis.edu/
Cladistic Analysis
PMG/selectnewpest.citrus.html
University of Florida. Available at http://creatures.ifas.ufl. A technique that groups taxa based on the relative
edu/ and http://edis.ifas.ufl.edu/MENU_CH5A for recency of common ancestry.
Insect Pests of Citrus and /MENU_CG for Pest Man-
agement Guides

Clade
Citrus Rust Mites (Acari:
Eriophyidae) A monophyletic group of taxa that share a closer
common ancestry with one another than with
Several mites cause russeting of citrus. members of any other group.
Citrus Pests and Their Management

Cladiopsocidae
Citrus Snow Scale, Unaspis citri A family of psocids (order Psocoptera).
(Comstock) (Hemiptera: Bark-Lice, Book-Lice or Psocids
Diaspididae)
This is an important citrus pest in Florida, USA.
Citrus Pests and Their Management
Cladistics
A school of thought that uses only evolutionary
relatedness (phylogenetics) in assigning taxo-
Citrus Stubborn Disease nomic groupings in classification systems.

This is a leafhopper-transmitted disease of

citrus.
Cladogenic Speciation
Transmission of Plant Diseases by Insects
Branching evolution of new species.

Citrus Whitefly, Dialeurodes citri

(Ashmead) (Hemiptera: Cladogram
Aleyrodidae)
A term used two ways by different authors. Either
This was once a very serious pest of citrus, but is a dendrogram (tree) produced using the principle
now considered a minor pest. of parsimony, or a tree that depicts inferred his-
Citrus Pests and Their Management torical relationships between organisms.
906
C Clambidae

Clambidae Abiotic factors that affect insect and mite pop-

ulations include weather (heat, cold, rain, drought)
A family of beetles (order Coleoptera). They com- and other physical factors. Biotic and abiotic con-
monly are known as fringe-winged beetles. trol factors usually act together to limit population
Beetles growth by reducing birth rates or increasing mor-
tality or dispersal, although one may be more
important than the other in certain situations.
Class Most organisms produce more progeny than
the environment can sustain, yet many natural pop-
A major subdivision of a phylum, and containing ulations maintain characteristic densities over long
a group of orders. periods of time. This state of dynamic equilibrium is
Classification achieved by an interaction between the biotic poten-
tial of the species and the resistance of biotic and
abiotic factors in the environment. Some ecologists
Classical Biological Control have focused on the importance of natural popula-
tion regulation by biotic factors (particularly natural
Marjorie A. Hoy enemies), while others have emphasized the impor-
University of Florida, Gainesville, FL, USA tance of abiotic factors (especially weather). Still
other ecologists have emphasized the importance of
Biological control is a method of pest control that interspecific competition in regulating population
employs parasitoids, predators, microbial patho- densities. The relative importance of these factors
gens and, sometimes, nematodes to reduce pest continues to be debated, but it is likely that each is
populations. Pests that are targets of biological con- important and potentially capable of regulating
trol include insects, mites, and weeds. [See the sec- population densities in specific situations. Under
tion on Natural Enemies for a description of natural most circumstances both biotic and abiotic factors
enemies used in biological control programs.] together influence population densities, and it is the
Biological control is part of natural control, degree to which any one factor affects natural con-
which maintains populations within more or less trol in specific situations that differs.
regular upper and lower limits over time. Natural Physical factors generally influence populations
control factors may be biotic (living) or abiotic in a density-independent manner. This means that
(nonliving). Biotic control factors include the the intensity of the effect of physical factors is not
effects of natural enemies, food quantity and qual- related to the target populations density. Thus, a
ity, interspecific and intraspecific competition for severe freeze usually will kill approximately the same
resources, and requirements for space or territory. proportion of large populations as of small popula-
All insects and mites have a diverse array of tions. By contrast, biotic factors may influence popu-
natural enemies. Microorganisms, invertebrates, lation densities in a more density-dependent manner,
and vertebrates all affect them, causing debilita- with their effect increasing in intensity as popula-
tion or death. Pathogens attacking arthropods tions become larger and decreasing in intensity as
include viruses, bacteria and fungi. Many verte- populations decrease. Density-dependent popula-
brates (including birds, lizards, fish and frogs) feed tion regulation acts as a negative feedback process
on pest arthropods. Nematodes belonging to sev- between population density and rate of increase. For
eral families attack insects. However, by far insects example, the availability of plant hosts may exert
are the most numerous and diverse natural ene- density-dependent pressure on insect populations,
mies of other insects, with hundreds of thousands with a small number of plants being sufficient for a
of species feeding on other insects. small population but inadequate for a large one.
 Classical Biological Control
C 907

Parasitoids, predators and pathogens poten- Classical Biological Control

tially are capable of affecting pest populations in a
density-dependent fashion because they can respond This approach involves importing and establishing
to changes in host population density. Some natural natural enemies in order to assist in the long-term
enemies may increase their activities and reproduc- control of newly introduced, foreign pests. Classical
tive rates as the density of their insect host increases, biological control involves a series of steps and
and reduce these activities as the density of their usually takes a number of years. Most programs
hosts declines. If natural enemies increase their require more than 10 years of effort.
numbers with increasing pest/host population den- Classical biological control in the U.S.A. was
sities, this is termed a numerical response. Numeri- demonstrated to be a useful pest management tool
cal responses occur because prey or hosts are readily over 100 years ago after two natural enemies were
available so that the reproductive rates of natural introduced and established in 1888 against the cot-
enemies are enhanced. A functional response is tony cushion scale, Icerya purchasi, in Californias
another important component of a density-depen- citrus industry. The cottony cushion scale was acci-
dent response by parasitoids and predators. A func- dentally introduced into California. It rapidly
tional response is the change in number of prey or established, spread and multiplied. The severe
hosts consumed or parasitized per natural enemy in effects of its feeding on citrus trees threatened the
response to changing prey or host density. Func- survival of the citrus industry. In one of the more
tional responses are influenced by several factors, dramatic classical biological control programs ever
including: (i) rate of successful search, (ii) the recorded, the Vedalia lady beetle Rodolia cardinalis
amount of time the natural enemy and target pest and a fly Cryptochetum iceryae were imported and
are exposed to each other, and (iii) the time spent by released. Within 2 years, these natural enemies had
the natural enemy handling each prey or host. If pest established, multiplied, and spread to reduce popu-
populations increase and, as a consequence, are lations of the cottony cushion scale (Fig.61) to an
more aggregated, natural enemies may not have to insignificant level. These natural enemies have con-
spend as much time searching for prey or hosts. Nat- tinued to provide effective control in California
ural enemies also can increase their functional ever since unless disrupted by applications of pes-
response by consuming only part of their prey at ticides. Furthermore, these natural enemies have
high densities, thus killing more prey per unit time. been distributed to more than 25 additional coun-
tries, where they have established and provided
excellent control of the cottony cushion scale.
Naturally Occurring Biological
Control
Assumptions of Classical Biological
Many insects or mites are not pests because native Control
natural enemies keep them suppressed with no
assistance from humans. Naturally occurring bio- Insects or mites that establish in a new environ-
logical control often is discovered only after natural ment often are much more serious pests than
enemy populations have been disrupted and insect they are in their native range where they are sup-
or mite populations have increased dramatically to pressed by a complex of natural enemies. If a for-
become pests. Biological control also includes an eign pest arthropod evades regulatory and
applied technology through which humans attempt quarantine barriers to become established in a
to restore, enhance, or mimic a natural phenome- new environment and cannot be eradicated, the
non by three basic tactics: classical biological con- feasibility of classical biological control should
trol, augmentation, or conservation. be evaluated immediately.
908
C Classical Biological Control

Cryptochaetum iceryae and

Rodolia cardinalis introduced

Icerya purchasi density Resurgence induced by DDT

Economic injury level

Economic threshold

General
equilibrium
position

1868 1888-89 1892 1947

Classical Biological Control, Figure 61 The cottony cushion scale, Icerya purchasi, increased its
population dramatically after its introduction in 1868 into California citrus groves. In 1888, the
parasite Cryptochetum iceryae and the predator Rodolia cardinalis were introduced. Within a year
after their establishment, they reduced the scale populations below the economic injury level, where it
fluctuated around a general equilibrium position until DDT applications were made in the 1940s, which
allowed a resurgence because the natural enemies were disrupted.

The assumptions of classical biological control owever, if classical biological control is successful,
H
are: (i) pest populations are suppressed by natural it can provide cost-effective and environmentally
enemies in their native land, (ii) pest populations benign pest management for a long time.
have escaped suppression after their introduction
without their natural enemies into a new environ-
ment, and (iii) introduced natural enemies may be Steps in Classical Biological
more effective in a new location if introduced free Control
of their own natural enemies (e.g., predators and
parasitoids may have their own natural enemies Classical biological control involves a series of
that reduce their effectiveness against the target steps, beginning with identifying the pest as native
pest). Another assumption is that the existing natu- or foreign in origin. If foreign, it is important to
ral enemies present in the new geographic envi- identify the origin of the pest, because this area
ronment will be generalists, and therefore less may provide the most extensive array of natural
effective than natural enemies that have specialized enemies for evaluation and possible importation.
on the target pest in their original environment. Once the biology and behavior of the pest
Classical biological control programs typically have been reviewed, specific natural enemies are
require a number of years to execute, and there are no identified as potential targets of a collecting trip.
guarantees that the pest populations will be suppressed Sometimes, a long list of natural enemies is avail-
to a satisfactory level in the new environment. able; sometimes, only a few natural enemy species
 Classical Biological Control
C 909

Classical Biological Control, Figure 62 Endoparasitoid female, Trioxys pallidus (Hymenoptera:

Aphelinidae), inserting an egg into the walnut aphid, Chromaphis juglandicola. (Photo
providedbyJ.K.Clark.)

are known. Typically, only a few species are col- declining, fewer such specialists are being trained
lected, shipped and evaluated further. Once the which could lead to delays or failures in future
natural enemies are obtained and shipped to a classical biological control programs. Taxonomic
quarantine facility, their identity is verified by tax- specialists also can provide information on the
onomic specialists and the colonies are screened host or prey range of the natural enemy, which is
to eliminate undesirable hyperparasitoids (parasi- important when risk assessments are being con-
toids of the primary parasitoid) or pathogens. Per- ducted prior to releasing the natural enemies.
mission to release the natural enemies must be Classical biological control is an important
obtained from state and or federal regulatory component of pest management programs because
agencies after a risk analysis has been conducted. foreign pests invade new environments on a con-
Natural enemies are then mass reared and released tinuing basis. For example, by 1971 at least 1,683
(Figs. 62 and 63) with the goal of permanently species of insects or mites found in North American
establishing them in the new environment to pro- forests, rangelands, or agricultural fields were illegal
vide continuing control of the target pest. aliens. Some were pests, some were beneficial, and
Classical biological control programs are some had no known economic importance. At least
dependent upon having taxonomic specialists to 235 major pests in the U.S.A. are foreign, coming
correctly identify immigrant pests, provide infor- from nearly all geographic regions of the world.
mation on their geographic distribution, and iden- Another 630 foreign arthropod species are listed as
tify natural enemies in the country of origin. lesser pests. In Florida, at least 209 species of foreign
Correct identification (Fig. 64) of pests and their insects have been found since 1970; approximately
origins is important when planning collection 20 are major pests, including the Mexican fruit fly,
trips. Natural enemies also must be correctly iden- Anastrepha ludens, Mediterranean fruit fly, Ceratitis
tified before they can be released from quarantine capitata, Asian tiger mosquito, Aedes albopictus, cit-
into the new environment. Some effective biologi- rus blackfly, Aleurocanthus woglumi, citrus leafminer,
cal control programs have been delayed because Phyllocnistis citrella, Asian citrus psylla, Diaphorina
taxonomic information was lacking or incorrect. citri, brown citrus aphid, Diaphorina citri, and the
Because financial support for systematics is melon thrips, Thrips palmi.
910
C Classical Biological Control

Classical Biological Control, Figure 63 Endoparasitoid female, Cardiochiles diaphaniae (Hymenoptera:

Braconidae), inserting an egg into the melonworm, Hyalinata hyalinata. This parasitoid was introduced
from Colombia, South America into Puerto Rico and Florida, successfully establishing in the former
location.

Based on past history, foreign insect and mite Some classical biological control programs
species will continue to immigrate to the U.S.A. at can be accomplished without a collecting trip; if a
the rate of about eleven species per year. Of the natural enemy has been established in one region,
eleven, seven are likely to be pests of some impor- scientists there can collect it and ship it to a new
tance and about every third year a pest of major region where the pest has invaded. Once the natu-
significance will be discovered. Assuming that few ral enemy has been processed through quarantine,
of these pests can be eradicated, classical biologi- reared and released, it may provide relatively rapid
cal control remains a potentially effective method and inexpensive control (Table 13).
for providing cost-effective pest suppression.
Classical biological control can be effective
against different types of pests. For example, in Cooperation Between Scientists
the continental U.S.A. and Hawaii insects in Aids in Citrus Blackfly Project
the orders Lepidoptera, Coleoptera, Hemiptera,
Hymenoptera, Diptera and Orthoptera have been Classical biological control of the citrus blackfly,
suppressed by arthropod natural enemies in classi- Aleurocanthus woglumi, in Texas and Florida pro-
cal biological control programs. Nearly complete vides an example of highly successful projects that
control was obtained in some cases, while in others benefited from cooperation between scientists in
only partial control was achieved. Sometimes a sin- different regions. The citrus blackfly invaded Texas
gle natural enemy provided substantial control; in in the late 1960s and caused serious damage in citrus
other circumstances several natural enemy species groves there. Eradication efforts began in 1971, but
were required. Effective biological control can be were unsuccessful. Joint efforts between scientists in
achieved with a specific natural enemy in the entire Texas and Mexico resulted in the importation, eval-
geographic region that the pest inhabits in some uation and release of two parasitoids, Amitus hes-
cases, or this natural enemy may be effective only in peridum and Encarsia opulenta, that provided
a limited part of the new geographic distribution. complete biological control of the citrus blackfly.
 Classical Biological Control
C 911

Identify pest as native or foreign

If pest is exotic,
determine geographic
origin

Evaluate information on pests biology & behavior and

natural enemies to define search area

Obtain natural enemies by collaboration &

exchange or foreign exploration

Import natural enemies into quarantine;

evaluate biology & risks; maintain
voucher specimens

Once out of quarantine, evaluate

natural enemy in laboratory, greenhouse
& field cages; develop mass rearing methods

Release into environment;

determine if establishment
occurred

Evaluate efficacy &

benefits : costs

Classical Biological Control, Figure 64 Classical biological control involves a series of steps before a
foreign pest can be controlled by the introduction and establishment of one or more natural enemies.
From start to finish, classical biological control programs require sustained funding and personnel over
several years.

The citrus blackfly subsequently invaded by sooty mold growth. Again, eradication of the
Florida in 1976, and huge populations developed pest was attempted, but after $15 million dollars
rapidly. The honeydew produced by the blackflies had been spent, the blackfly was still present and
caused entire citrus groves to become blackened increasing its distribution.
912
C Classical Biological Control

Classical Biological Control, Table 13 Some cases of successful biological control of pest arthropods by
imported arthropod natural enemies in the Continental USA and Hawaii
Pesta control Crop or host Principal natural enemiesa Project resultsb
(P)=parasitoid C=complete
(Pred)=predator S=substantial
P=partial
Oriental mole cricket, Sugarcane Larra polita (P) P
Gryllotalpa orientalis
alfalfa weevil, Alfalfa Bathyplectes curculionis (P) P-S
Hypera postica Microctonus aethiops (P) P-S
Tetrastichus incertus (P) P-S
American cockroach, Household pest Ampulex compressa (P) P
Periplaneta americana
armyworm, Sugarcane Apanteles militaris (P) C
Pseudaletia unipuncta Archytas cirphis (P) S
Asiatic rice borer, Rice Amyosoma chilonis (P) P
Chilo suppressalis Dioctes chilonis (P) P
Trichogramma japonicum (P) P
asparagus beetle, Asparagus Tetrastichus asparagi (P) P-S
Crioceris asparagi
Australian cockroach, Household pest Ampulex compressa (P) P
Periplaneta australasiae
barnacle scale, Passion fruit Coccidoxenus mexicanus (P) S
Ceroplastes cirripediformis
birch leaf-mining sawfly, Birch, Alder Chrysocharis laricinellae (P) C
Heterarthrus nemoratus Phanomeris phyllotomae (P) C
black scale, Citrus, Olive, Metaphycus helvolus (P) S
Saissetia oleae Ornamentals Diversinervus elegans (P) S
Encyrtus infelix (P) S
Metaphycus luteolus (P) S
Coccophagus capensis (P) P-S
Coccophagus cowperi (P) S
browntail moth, Forest, shade trees Apanteles lacteicolor (P) S
Euproctis chysorrhoea Townsendiellomyia nidicolor (P) S ?
and others
California red scale, Citrus Aphytis lingnanensis (P) P
Aonidiella aurantii Aphytis melinus (P) P
Comperiella bifasciata (P) P
Chinese grasshopper, Sugarcane Scelio pembertoni (P) S
Oxya chinensi
 Classical Biological Control
C 913

Classical Biological Control, Table 13 Some cases of successful biological control of pest arthropods by
imported arthropod natural enemies in the Continental USA and Hawaii (Continued)
Pesta control Crop or host Principal natural enemiesa Project resultsb
(P)=parasitoid C=complete
(Pred)=predator S=substantial
P=partial
Chinese rose beetle, Vegetables, Campsomeris marginella P
Adoretus sinicus ornamentals modesta (P)
Tiphia segregata (P) P
citrophilus mealybug, Citrus, Acacia Coccophagus gurneyi (P) C
Pseudococcus fragilis Hungariella pretiosa (P) C
citrus blackfly, Citrus Amitus hesperidum (P) C
Aleurocanthus woglumii Encarsia opulenta
citrus mealybug, Citrus Cryptolaemus montrouzieri P
Planococcus citri (Pred)
Leptomastidea abnormis (P) P
citrus leafminer, Citrus Ageniaspis citricola (P) S
Phyllocnistis citrella Florida Coconut palm
coconut scale, Telsimia nitida (Pred) S
Pinnaspis buxi
Comstock mealybug, Apple Allotropa burrelli (P) C
Pseudococcus comstocki Pseudaphycus malinus (P) C
cottony cushion scale, Citrus Cryptochetum iceryae (P) S-C
Icerya purchasi Rodolia (=Vedalia) cardinalis C
(Pred)
Egyptian alfalfa weevil, Alfalfa Bathyplectes curculionis (P) P
Hypera brunneipennis
European corn borer, Corn Lydella thompsoni (P) P
OIstrinia nubilalis Macrocentrus gifuensis (P) and P
others
European earwig, Forficula Gardens Bigonicheta setipennis (P) P
auricularia
fern weevil, Native Hawaiian Doryctes syagrii (P) P
Syagrius fulvitarsis Tree ferns
Florida red scale, Citrus Aphytis holoxanthus (P) C
Chrysomphalus aonidum
gypsy moth, Lymantria Forest, shade trees complex of parasitoids, preda- P
dispar tors and pathogens
Japanese beetle, Popillia Turf, pasture, fruits, Tiphia vernalis (P) P
japonica ornamentals
longtailed mealybug, Citrus, Avocado Anarhopus sydneyensis (P) P
Pseudococcus adonidum Cryptolaemus montrouzieri P
(Pred.)
Hungariella peregrina (P) P
914
C Classical Biological Control

Classical Biological Control, Table 13 Some cases of successful biological control of pest arthropods by
imported arthropod natural enemies in the Continental USA and Hawaii (Continued)
Pesta control Crop or host Principal natural enemiesa Project resultsb
(P)=parasitoid C=complete
(Pred)=predator S=substantial
P=partial
Mediterranean fruit fly, Fruits, Coffee Opius tryoni (P) P
Ceratitis capitata Opius fullawayi (P) P
melon fly, Melons Opius fletcheri (P) P
Dacus cucurbitae Cucumber
New Guinea sugarcane Sugarcane Lixophaga sphenophori (P) S-C
weevil,
Rhabdoscelus obscurus
nigra scale, Ornamentals Metaphycus helvolus (P) S
Saissetia nigra
nutgrass armyworm, Sugarcane, pasture a complex of parasitoids P-C
Spodoptera exempta
olive scale, Parlatoria oleae Olive, ornamentals, Aphytis maculicornis (P) S S-C
deciduous fruit Coccophagoides utilis (P)
oriental beetle, Sugarcane Campsomeris marginella P-S
Anomala orientalis modesta (P)
Tiphia segregata (P)
oriental fruit fly, Fruits Opius oophilus (P) S-C
Dacus dorsalis Opius vandenboschi (P) S
oriental fruit moth, Peach, pome fruits Macrocentrus ancylivorus (P) P
Grapholitha molesta
oriental moth, Cnidocampa Shade trees, fruit trees Chaetexorista javana (P) S
flavescens
pea aphid, Alfalfa Aphidius smithi (P) S
Acyrthosiphon pisum
pine tip moth, Pine trees Campoplex frustranae (P) P
Rhyacionia frustrana
bushnelli
pink sugar cane, Sugarcane Anagyrus saccharicola (P) S
mealybug Trionymus
sacchari
purple scale, Citrus Aphytis lepidosaphes (P) S-C
Lepidosaphes beckii
Rhodesgrass scale, Orange grasses Neodusmetia sangwani (P) S
Antonina graminis
San Jose scale, Deciduous fruit Prospaltella perniciosi (P) P
Quadraspidiotus
perniciosus
 Classical Biological Control
C 915

Classical Biological Control, Table 13 Some cases of successful biological control of pest arthropods by
imported arthropod natural enemies in the Continental USA and Hawaii (Continued)
Pesta control Crop or host Principal natural enemiesa Project resultsb
(P)=parasitoid C=complete
(Pred)=predator S=substantial
P=partial
satin moth, Forest trees Apanteles solitarius (P) S-C
Stilpnotia salicis Meteorus versicolor (P) S-C
spotted alfalfa aphid, Alfalfa Aphelinus semiflavus (P) S
Therioaphis maculata Praon palitans (P) S

Trioxys utilus (P) S
southern green stink bug, Vegetables, fruits, Trissolcus basilis (P) S-C
Nezara viridula ornamentals
sugarcane aphid, Sugarcane complex of parasitoids and S
Aphis sacchari predators

sugarcane borer, Sugarcane Lixophaga diatraeae (P) P
Diatraea saccharalis Agathis stigmaterus (P) P
sugarcane leafhopper, Sugarcane and others Tytthus mundulus (Pred) C
Perkinsiella saccharacida
sweet potato leaf miner, Sweet potato Apanteles bedelliae (P) P-C
Bedellia orchilella
taro leafhopper, Taro Cyrtorhinus fulvus (Pred) S
Tarophagus proserpina
torpedo bug planthopper, Coffee, Mango, Citrus Aphanomerus pusillus (P) S-C
Siphanta acuta
walnut aphid, Walnuts Trioxys pallidus (P) P-C
Chromaphis juglandicola
western grape leaf Grape Apanteles harrisinae (P) S
skeletonizer, Sturmia harrisinae (P)
Harrisina brillians
wooly apple aphid, Apple Aphelinus mali (P) S-C
Eriosoma lanigerum
wooly whitefly, Citrus Amitus spiniferus (P) S-C
Aleurothrixus floccosus Eretmocerus paulistus (P) C
yellow scale, Citrus Comperiella bifasciata (P) S-C
Aonidiella citrina

a
Not all examples are cited; success ratings and scientific names of pests and natural enemies vary in different lists.
b
Complete successes (C) refer to complete biological control obtained and maintained against a pest over an extensive
area so that pesticide applications rarely are necessary. Substantial (S) successes include cases in which insecticidal
control is sometimes required. Partial successes (P) are those in which chemical controls are applied, but the intervals
between applications or lengthened or the outbreaks occur less often. ? refers to situations in which the results are
unknown or controversial.
916
C Classical Biological Control

As the result of cooperation between scien- Although classical biological control can yield
tists from Texas and Mexico, A. hesperidum, complete and lasting pest population suppression
E.opulenta, E. clypealis and E. smithi were intro- in a many situations, many past efforts have been
duced into Florida in 1976. Both A. hesperidum only casual or have involved use of an unsuitable
and E. opulenta became established. Amitus natural enemy. In general, relatively little classical
hesperidum provided rapid control of blackfly biological control has been directed against pests
populations, but E. opulenta eventually replaced of range, forage, grain crops or row crops. For
A. hesperidum as the dominant parasitoid after example, of 110 pest species under partial to com-
citrus blackfly populations had been reduced. plete control by classical biological control, only
Both parasitoids are given credit for providing 13 involved pests of row crops. This relatively poor
complete biological control of the blackfly in record has been attributed to the instability of the
Florida by 1981. The program cost approximately row crop environment. Row crops persist only for
$US 2.2 million dollars, but the benefits continue weeks or months, during which time the natural
to accrue, and were estimated to be $9.3 million enemy must discover and move into the crop, find,
in 1980 alone. attack, and build up numbers on the pest, then be
Effective classical biological control depends subjected to abrupt disruption at the end of the
upon the establishment of one or more foreign crop season.
natural enemies in a new environment. Establish- A large number (ca. 40%) of the pests tar-
ment of natural enemies in new environments is geted in classical biological control programs have
not guaranteed, with estimates of successful been scales (Hemiptera), and about 20% have
establishment ranging from 16 to 34%. There is been Lepidoptera, Coleoptera, or Hemiptera other
intense interest in learning how to increase estab- than coccids. Many of the successes have been
lishment rates and the use of climate-matching achieved in warmer climates, particularly in
computer programs may allow scientists to Hawaii and California, although it is likely that
increase the establishment rate. After release, the these successes are due to the extensive efforts
introduced natural enemy must find adequate employed in classical biological control. Other
hosts and other resources as well as suitable cli- trends include an emphasis on employing parasi-
matic conditions in the new environment. Natu- toids rather than predators, with a majority of
ral enemies must be released in adequate successful classical biological control programs
numbers, in a healthy condition, at an appropri- involving highly host-specific natural enemies.
ate time, and in the presence of suitable hosts or Establishment of host-specific parasitoids is con-
prey if establishment is to succeed. sidered to be lower risk than release of natural
In some cases, different populations (biotypes) enemies with a broad host or prey range. Such
of a particular species have different biological host specificity is important in alleviating con-
attributes that make them more or less likely to cerns about unintended effects of these natural
establish and be effective in the new environment. enemies on nontarget native species.
For example, a parasitoid called Trioxys pallidus Successful classical biological control is
originally was collected in France and released in dependent on two critical elements: (i) establish-
California to control the walnut aphid Chromaphis ing the natural enemy in the new environment,
juglandicola. The French biotype established, but and (ii) the efficacy of the natural enemy in the
was only effective in the cooler, more humid new environment. Usually, a particular pest will
coastal areas of California. A biotype of T. pallidus have more natural enemies attacking it than are
from Iran was subsequently established and pro- feasible to evaluate and release. Some guidelines
vided highly effective control of the walnut aphid have been suggested for choosing between differ-
in the hot, dry Central Valley of California. ent natural enemy species to evaluate and release.
 Classical Biological Control
C 917

Potentially effective natural enemies generally Classical Biological Control and the
exhibit as many of the following attributes as Gypsy Moth
possible:
The gypsy moth is an important forest defoliator
Fitness and adaptability in the target environment that was introduced into North America in 1869.
High searching capacity for the target species Large classical biological control projects were
High reproductive rate relative to that of the host initiated during three different intervals, with
or prey the first beginning in 1905 after efforts to eradi-
Synchronization with the host or prey and its cate the gypsy moth were abandoned. That proj-
habitat ect continued through 1914 and the second ran
Host or prey specificity from 1922 until 1933. Efforts intensified again
An ability to increase its effectiveness as the host in1963.
or prey density increases (density-dependent During these three intervals, more than 40
response to the pest) species of parasitoids were introduced into North
America against the gypsy moth; ten established,
A natural enemy that behaves in a density- including two that attack eggs, two that attack
dependent manner can respond to changes in the small larvae, four that attack larger larvae, and two
population density of its host or prey, leading to an that attack pupae. In addition, the predaceous
increasing percentage of kill with increasing host ground beetle, Calosoma sycophanta, and a nuclear
or prey density and a decreasing percentage of kill polyhedrosis virus (a virus specific to the gypsy
with decreasing host or prey density. It is difficult moth) were established.
to document experimentally that, in fact, a natural Despite the effects of these parasitoids,
enemy is behaving in a density-dependent man- predators and pathogens, and the depredations
ner because it is likely that most natural enemy- of a variety of native natural enemies such as
pest interactions exhibit a time lag, and thus are mice, shrews, birds, spiders, stink bugs, hornets,
behaving in a delayed density-dependent manner. preying mantids, ants and bacterial and fungal
Delayed density dependence occurs when the diseases, the gypsy moth continued to expand its
response of natural enemies to the pest population range in North America and cause periodic defo-
is delayed for some reason. liations over thousands of acres of forest and
In many situations classical biological control shade trees.
programs result in substantial pest population Recently, a fungus native to Japan, Ento-
reductions. However, some large, lengthy, and mophaga maimaiga, was found causing dramatic
expensive projects have been unsuccessful for and unexpectedly high levels of mortality to
unknown reasons. As an example, a classical bio- gypsy moth larvae in the northeastern United
logical control project directed against the gypsy States. The mortality was unanticipated because
moth, Lymantria dispar, has been slow to result in the fungus is believed to have been introduced
adequate pest population suppression despite into North America nearly 80 years ago, but was
extensive and long-term efforts involving the not discovered until 1989. No one knows why it
importation and release of predators, parasitoids apparently was ineffective until recently; some
and pathogens. Gypsy moth populations are preyed speculate that the fungus was introduced recently,
on by native natural enemies, including vertebrate although the introduction was not conducted
predators. Despite the effects of native and imported with an established program and did not go
natural enemies, suppression of gypsy moth popu- through risk evaluation.
lations in North America to levels that are consid- Despite the pleasant surprise of discovering
ered acceptable has been slow in coming. another microbial disease agent, it is unclear
918
C Classical Biological Control

whether E. maimaiga, in combination with the variety of farming systems and to sub-Saharan
other exotic and native natural enemies, can pro- climatic conditions. Cassava is estimated to pro-
vide adequate suppression of gypsy moth popu- vide up to 50% of the daily caloric intake of 200
lations in North America. Gypsy moth million people in Africa and, because cassava
populations apparently are influenced by both roots can remain in the ground for up to 2 years,
biotic and abiotic factors, including vertebrate provides an even higher proportion of the diet
and invertebrate natural enemies, weather, host when other crops fail. Cassava is an insurance
tree species, foliage chemistry and plant quality. crop against famine.
Because gypsy moth populations synchronously In the early 1970s, the cassava mealybug
reach outbreak densities over large areas, it is Phenacoccus manihoti was accidentally intro-
possible that a combination of weather and other duced into Africa, probably because quarantines
mortality factors is responsible for the onset of were ignored and planting material was intro-
periodic outbreaks. There is considerable debate duced illegally. The cassava mealybug spread
over the degree and type of control exerted by rapidly across much of the sub-Saharan region
various vertebrate and invertebrate natural ene- of Africa and caused devastating losses
mies, and it is unclear whether establishment of (10100%) by the early 1980s, estimated to be at
additional foreign natural enemies would con- least $2 billion per year.
tribute significantly to suppressing the still- Chemical control was not ecologically, eco-
expanding distribution of the gypsy moth in nomically, or logistically feasible. Famine was pos-
North America. sible if control was not achieved. A breeding
Even in southern Europe, where an extensive program was initiated to develop resistant variet-
array of natural enemies occur and the gypsy moth ies, but this was recognized to be a potential solu-
is a native, gypsy moth populations reach damag- tion that would take at least 1020 years.
ing levels periodically. Thus, the gypsy moth At the same time as the breeding program
appears to represent a foreign pest that may be was initiated, a classical biological control pro-
managed only by a multi-tactic pest management gram was begun. Surveys in Central and South
program. America were conducted for natural enemies of
Sometimes, classical biological control pro- the cassava mealybug and an encyrtid parasitoid
grams can reduce the pest population to a level Apoanagyrus lopezi was introduced, reared and
that can be lived with over a very large area. The released by the Africa-Wide Biological Control
cassava mealybug classical biological control Programme of the International Institute for
program is one of the most successful and large Tropical Agriculture and by national agencies of
scale programs ever conducted. This program many African countries. Subsequent to its first
has gone through all the steps involved, includ- release in 1981 and 1982, A. lopezi has established
ing an economic analysis of the costs and in at least 19 countries and is providing effective
benefits. control of the mealybug throughout most of its
distribution in Africa.
The economic benefits of this classical bio-
Continent-Wide Control of the logical control program were estimated from 1977
Cassava Mealybug in Africa through 2002, using the following very conserva-
tive assumptions: that cassava has a value of US
Cassava, Manihot esculenta, was brought to $60/ton; production would remain stable at 1980
Africa about 300 years ago from South America. levels; an average yield loss of 20% would occur
Cassava serves as a subsistence crop for 200 mil- due to mealybug; and A. lopezi would reduce losses
lion people because it is hardy, and adapted to a due to mealybugs by only 60%; by 2002 other
 Classical Biological Control
C 919

c ontrol methods (plant resistance, integrated pest the specific system. However, as a general rule, the
management programs) would provide effective most effective natural enemies:
control.
An estimated $2,205,000,000 are estimated Exhibit a high degree of prey or host specificity
to have been saved by the introduction of A. lopezi, Have a high relative reproductive rate compared
as compared to the classical biological control to their prey or host, and
program which cost $14,800,000. This produced a Exhibit a tolerance of abiotic factors similar to that
benefit to cost ratio of 149:1, which is unusually of the host or prey
high. The benefits are so high because the pro-
gram was developed quickly, was unusually effec- The host or prey searching ability of arthro-
tive across a wide geographic region, and cassava pod natural enemies has been studied rarely in the
is a very important crop. This estimate demon- field. What we know about their behavior usually
strates how well classical biological control can comes from observations in the laboratory or
work and has encouraged its use against another other artificial situations. Arthropod natural ene-
pest of cassava introduced into Africa, the cassava mies respond to physical and chemical cues from
green mite. the host or prey itself, from its host plant, and from
an interaction of the two.
Prey/host selection has been divided into four
Conservation of Natural Enemies steps: (i) habitat selection, seeking a particular
environment where an appropriate host plant
Conservation of natural enemies involves protect- occurs; (ii) prey or host finding, identifying prey
ing and maintaining natural enemy populations. or host individuals on the plant; (iii) prey or host
Conservation is crucial if either native or intro- acceptance, examining individual hosts or prey in
duced natural enemies are to be maintained in the environment to determine whether to feed on
agricultural crops. Conservation most often or parasitize it; and (iv) prey or host suitability, the
involves modifying pesticide applications. ability of the parasitoid to develop on or within
As a general principle, pesticide applications the host or the predator to feed on the prey.
should be made only when pest populations
exceed specified levels and when no other control
tactic is available. In some cases, changing the Biological Control in Relation to
active ingredients, rates, formulations, timing, Other Pest Management
and/or location of pesticide applications can allow Approaches
natural enemies to remain effective. Maintaining
untreated refuges also protects natural enemy The goal in pest management is to reduce a pests
populations; for example, alternate rows are treated density to a lower density than would otherwise
with pesticides so that the lady beetle Stethorus occur. Fluctuations in density are expected to
punctum can survive to control European red occur over time, which may be either small or
mites, Panonychus ulmi, in Pennsylvania apple large. Ideally, the average density remains below
orchards. the level that causes economic injury. However,
the degree of biological control achieved is not
always sufficient to provide economic pest
Effective Natural Enemies suppression.
The term strategy describes the long-term
The effectiveness of natural enemies in controlling plan or theoretical framework of an operation.
pest populations depends on the characteristics of The term tactics describes the methods used to
920
C Classical Biological Control

attain or fulfill that strategy. There are several mating disruption by release of pheromones, dis-
strategies for managing pests, including: exclu- ruption of normal development of pests after
sion or quarantine of foreign pests, eradication, application of insect hormones, or applications of
suppression of pest populations by plant resis- antifeedant materials. Techniques that are com-
tance, biological control or chemical control, and patible with the use of biological control, or have
integrated pest management (IPM). Within each little impact on natural enemies, are often consid-
strategy, there are various methods or tactics ered biorational.
employed. Under many circumstances, pest managers
Exclusion or quarantines can prevent or delay will need to employ multiple tactics to achieve
the introduction of foreign pests into a new geo- economic suppression of all the pest populations.
graphic region. Eradication of foreign pests by Tactics used in IPM programs include plant resis-
means of pesticide applications, release of sterile tance, biological control, chemical control, cultural
males, or removal of suitable host plants is feasible controls, or biorational controls. How should the
in some circumstances. Plant resistance can pro- pest manager prioritize the pest management tac-
vide substantial to partial suppression of many tics to be evaluated and employed? One principle
insect or mite pests, but resistant plant varieties should be that all tactics considered should be
are not available for all pests. Furthermore, insects examined for their effects on natural enemies.
and mites can evolve resistance to plant resistance The conceptual basis for organizing an IPM
mechanisms. Thus, each strategy is valuable but program with biological control as a key compo-
may be limited in scope. nent was spelled out over 45 years ago. That proj-
Classical biological control can provide ect, designed for California alfalfa, demonstrates
effective suppression of many invasive insects, some of the concepts and complexities of creat-
mites and weeds. However, it is rare that all inva- ing such programs. The spotted alfalfa aphid,
sive pests can be controlled by the importation Therioaphis maculata, invaded California and
and release of natural enemies in classical bio- was detected in 1954. The aphid spread rapidly
logical control programs. Nor is chemical control throughout the state, causing millions of dollars
able to suppress all pests because resistance to of crop loss damage. Shortly after the aphid
pesticides and concerns about damage to the became established, research was initiated to find
environment and health hazards are increasing. or develop varieties of alfalfa resistant to the
As a result, integrated pest management is an aphids; to develop a classical biological control
increasingly important approach; it involves project; and to identify pesticides that would
deploying several approaches, perhaps including control this pest at a reasonable cost. An impor-
the use of transgenic (pest resistant) plants, tant component of the IPM program included
releases of sterile male insects, cultural controls, the introduction and establishment of the spot-
and release of pheromones (chemicals used to ted alfalfa aphid parasitoids Praon pallitans and
communicate between individuals within a spe- Trioxys utilis in a classical biological control proj-
cies, such as mating pheromones), in a harmoni- ect. However, classical biological control was
ous manner to control pests. combined with other tactics to achieve effective
Classical biological control should always be pest management in alfalfa.
considered when a new pest invades because clas- A variety of alfalfa was identified that was
sical biological control generally is compatible able to tolerate feeding by the aphid and several
with nonchemical management tactics in IPM pesticides were found that controlled the aphids.
such as plant resistance, cultural controls, and a Analysis of the effects of insecticide treatments
variety of biorational methods. Biorational pest on a complex of native predators, as well as the
management methods include tactics such as pest introduced parasitoids Praon pallitans and Trioxys
 Classical Biological Control
C 921

utilis, indicated that parasitoids of the spotted Evaluating Classical Biological

alfalfa aphid could survive many pesticides if the Control Programs
parasitoids were in the pupal stage when treated.
Importantly, because the aphid was not the only The degree and quality of evaluations of classical
alfalfa pest and the alfalfa caterpillar Colias eury- biological control programs vary dramatically. In
theme had to be controlled as well, a polyhedrosis some cases, detailed documentation has been pro-
virus was found to be effective in controlling the vided (for example, the cassava mealybug project),
alfalfa caterpillar either alone or in combination but in other cases few records were kept.
with a selective chemical insecticide. Monitoring Classical biological control programs can be
was recognized to be a key component in the pro- difficult to evaluate; sometimes the results are so
gram. Population levels of the alfalfa caterpillar spectacular that assessment appears to be unneces-
and its parasitoid, Apanteles medicaginis, were sary. At the least, however, assessments of pest sta-
monitored regularly and chemical control was tus before and after need to be made, although
recommended only if the pest: parasitoid ratio was such evaluations provide only circumstantial evi-
unfavorable. Thus, both the aphid and the caterpil- dence that natural enemies are effective.
lar could be controlled without disrupting control Designing controlled experiments to docu-
of the aphid by natural enemies. ment the effectiveness of classical biological con-
This project laid out a number of concepts trol is particularly difficult when there are no
that remain central to designing an effective IPM untreated plots because natural enemies have dis-
program in which biological control is a central persed rapidly. Also, low pest populations are diffi-
component. This study defined integrated control cult to monitor. When no reduction in pest
as applied pest control which combines and populations occurs, it is easy to assume that the
integrates biological and chemical control, and natural enemies were ineffective, although the nat-
emphasized that chemical control should be used ural enemies may, in fact, be providing some degree
only as necessary and in a manner which is least of suppression. Partial suppression is even more
disruptive to biological control, cautioning that difficult to evaluate; natural enemies often behave
when chemicals are used, the damage from the differently at high and low host or prey densities.
pest species must be sufficiently great to cover not Identifying the reasons for changes in pest
only the cost of the insecticidal treatment but also population density is difficult because natural
the possible deleterious effects, such as the harm- enemies are but one of the mortality factors
ful influence of the chemical on the ecosystem, influencing populations of pests. Both biotic and
thereby introducing economic and ecological con- abiotic factors influence pests and in many crops
siderations into the pest management equation. several to many species of natural enemies influ-
Thus, biological control and chemical control were ence pest populations, but unraveling the impact
shown to be potentially complementary or, with of each is difficult. Even the simplest ecosystem
adequate understanding, made to augment one is sufficiently complicated that population mod-
another. els developed to describe them are not easily
This project also articulated an important tested in the field.
principle: the ideal pest suppression tactic is not Two questions are often asked when evaluat-
one that eliminates all individuals of the pest while ing natural enemies: (i) are natural enemies con-
leaving all of the natural enemies. Pest elimination trolling a pest, and (ii) how is the control achieved?
would force the host- or prey-specific natural ene- Three major approaches are employed to answer
mies to leave the treated area or starve. The goal the first question. These may be used either singly
should be to suppress pest populations rather than or in combination. Research efforts to answer the
eliminate them. second question are more complex.
922
C Classical Biological Control

Exclude, Eliminate, or Reduce release site can be attributed to the effects of the
Natural Enemies natural enemies. Likewise, prey or hosts can be
added to a field plot and the efficiency of natural
Several exclusion techniques have been employed to enemies can be estimated by changes in pest den-
demonstrate that one or more natural enemies can sity. Direct observation of predation is useful in
control a pest population. A branch, tree, or other identifying prey and predator species; observa-
whole plant can be isolated to prevent movement of tions reveal where and when a predator searches,
natural enemies into the system. Isolation can be which is useful in designing a sampling scheme.
achieved by hand picking, providing sticky barriers Direct observation requires no manipulation of
for nonflying natural enemies, or by cages. The size of the environment and pests or natural enemies can
mesh on cages can be modified to exclude different be added or removed to determine the responses
natural enemies based on size. Evaluation of natural of the natural enemy to changes in pest density.
enemies by exclusion has been most useful when Unfortunately, this method is time consuming and
combined with other evaluation methods such as difficult to employ if the natural enemy is cryptic,
behavioral observations or population sampling. active only at night, or easily disturbed.
Unfortunately, none of these techniques is A variety of biochemical methods also have
completely satisfactory. Cages may alter the micro- been employed to determine whether predators
climate (light intensity, temperature, humidity and are preying on specific prey, including the enzyme-
wind speed) and this change can influence the linked immunosorbent assay (ELISA), precipitin
effects of the natural enemies. For example, cooler tests, polyacrylamide gradient gel electrophoresis,
temperatures can reduce the growth and activity and prey marking by labels.
rates of pests or natural enemies. Few have the time
and patience to hand pick natural enemies, and the
area which can be manipulated by this method is Correlation
relatively small. Most natural enemies are able to
fly over sticky barriers. It is usually difficult to iden- Another approach is to correlate the damage exerted
tify which members of the predator or parasitoid by the pest, or the crop yield, with natural enemy
complex are essential for the suppression of the population levels. If high natural enemy popula-
pest population unless the complex consists of one tions are correlated with low damage levels or high
or a few easily segregated species. crop yields, the natural enemies may be providing
Natural enemies can be eliminated by appli- effective pest suppression. However, correlation is
cation of pesticides that are nontoxic to the pest not causation and other changes in crop manage-
and, if an outbreak occurs subsequently the natu- ment practices such as crop cultivar or cultural
ral enemy or natural enemies can be assumed to methods may influence the amount of damage
have been controlling the pest. This approach was inflicted or the amount of crop yield. Ideally, blocks
accidentally employed when effective control of with the natural enemies of interest are compared
the cottony cushion scale by the Vedalia beetle was to blocks lacking them. However, if the natural ene-
disrupted by application of DDT; this pest has mies are highly mobile, such comparisons may be
been under excellent control for nearly a century possible only for a very short period of time.
and the control agents have been effective when
introduced elsewhere. However, relatively few pes-
ticides are nontoxic to pests, and subtle sublethal Modeling
effects can alter the pests response.
Natural enemies can be added to one plot and There are many kinds of models (including math-
not to another and changes in pest density in the ematical, statistical, simulation, and analytic), and
 Classification
C 923

many uses to which models can be put. Computer classical biological control programs directed
models have been developed which attempt to against invasive insect, mite and weed pests could
forecast and understand pest and natural enemy result in reduced pesticide use, reduced ground
populations. Some models include crop-pest-nat- water contamination by pesticides, reduced nega-
ural enemy interactions with the goal of under- tive effects on nontarget organisms from pesti-
standing the role of natural enemies in regulating cides, reduced pesticide residues on food, reduced
pest densities. crop production costs, improved control of pests,
and increased farm worker safety due to reduced
pesticide use.
Risk Assessments

Classical biological control in recent years is References

receiving increased scrutiny regarding possible
environmental risks associated with the importa- Clausen CP (1978) Introduced parasites and predators of
arthropod pests and weeds: a world review. Agricultural
tion and release of foreign natural enemies.
handbook 480. U.S. Department of Agriculture, Wash-
Claims have been made that parasitoids and ington, DC
predators released into Hawaii have had a detri- DeBach P (ed) (1964) Biological control of insect pests and
mental effect on native butterflies and moths. weeds. Reinhold, New York, NY
DeBach P, Rosen D (1991) Biological control by natural ene-
Unfortunately, it is not clear that the observed mies, 2nd edn. Cambridge University Press, Cambridge,
changes in native insect populations can be UK
attributed to classical biological control because Frank JH, McCoy ED (1992) The immigration of insects to
the critics failed to discriminate between the Florida, with a tabulation of records published since
1970. Fla Entomol 75:128
effects of habitat destruction, pesticide use, and Herren HR, Neuenschwander P (1991) Biological control of
the possible negative effects of released arthro- cassava pests in Africa. Ann Rev Entomol 36:257283
pod natural enemies. The release of the tachinid Huffaker CB (ed) (1971) Biological control. Plenum Press,
New York, NY
parasitoid Compsilura concinnata in the classical
Sailer RI (1983) History of insect introductions. In: Wilson
biological control program directed against the CL, Graham CL (eds) Exotic plant pests and North
gypsy moth is thought to have had negative American agriculture. Academic Press, New York, NY,
effects on native populations of Lepidoptera, pp 1538
van Driesche RG, Bellows TS Jr (1996) Biological control.
including the beautiful native silk moths. Because Chapman & Hall, New York, NY
C. concinnata is known to attack over 200 species
of Lepidoptera, it is unlikely to be considered
suitable for release under current risk assess- Classification
ments in classical biological control programs.
Practitioners of biological control are con- In sampling, this refers to a sampling plan that
vinced that classical biological control of arthro- classifies population density as being either above
pod pests or weeds is environmentally safe and or below some predetermined level (e.g., economic
low risk if carried out by trained biological control threshold), or belonging within some density class
specialists. Concerns about preservation of native (e.g., low, medium, high). Commonly used in pest
flora and fauna have led some to recommend management decision making application (con-
restrictions on the importation of all foreign trast with estimation).
species. In systematics, a natural arrangement of taxa
During the debate on the potential negative that organizes like organisms into categories.
effects of classical biological control, it should be Membership in groups traditionally has been
remembered that the use of natural enemies in based on structural features, but also biological
924
C Classification

features, and increasingly on molecular features. group. Perhaps the only obscure name is Zygen-
Sometimes classification is considered artificial, toma, which was introduced by Carl Brner, in
because the classification is based on features that 1904. He viewed these insects to be an evolution-
are convenient to see or to score, but have no phy- ary bridge or connection between the aptery-
logenetic significance. In contrast, natural classi- gote (wingless) and pterygote (winged) insects,
fications systems rely on features that are shared hence the name.
due to common evolutionary descent. The princi- Subclass Apterygota: Greek a (without) = pteron
pal categories used in classification of insects, in (wings)
descending (most inclusive to least) order, are: Order Archeognatha: Greek archaios
Phylum (primitive)+gnathos (jaw)
Class Order Zygentoma: Greek zyg (bridge)+entoma (in-
Subclass sect)
Infraclass Subclass Pterygota: Greek pteron (wing)
Series Infraclass Paleoptera: Greek palaios (ancient)+pteron
Superorder (wing)
Order Order Ephemeroptera: Greek ephermeros (short-
Suborder lived)+pteron (wing)
Infraorder Order Odonata: Greek odon (tooth) (referring to the
Family mandibles)
Subfamily Infraclass Neoptera: Greek neos (new)+pteron (wing)
Tribe Series Exopterygota: Greek exo (outside) + pteron
Genus (wing)
Species Superorder Plecopteroidea
In practice, all these categories are not often Order Plecoptera: Greek plecos (plaited)+pteron (wing)
used; the most commonly used taxa are class, Order Embiidina: Latin embios (lively)
order, family, genus and species. Other categories Superorder Orthopteroidea
also exist; for example, the class Insecta is some- Order Phasmatodea: Latin phasma (apparition or
times placed in the superclass Hexapoda and the specter)
superphylum Ecdysozoa, and related families are Order Mantodea: Greek mantos (soothsayer)
often grouped into superfamilies. The subclass Order Mantophasmatodea: from Mantodea+Phas-
Pterygota is sometimes divided into two divisions, matodea
consisting of the hemimetabolous orders and the Order Blattodea: Latin blatta (cockroach)
holometabolous orders. Possibly the only level that Order Isoptera: Greek iso (equal)+pteron (wing)
can be assessed objectively is the species. Species Order Grylloblattodea: Latin gryllus (cricket)+blatta
are grouped into genera, genera into families, and (cockroach)
so forth, but taxonomists differ in the importance Order Orthoptera: Greek orthos (straight)+pteron
of characters used to cluster the taxa, so different (wing)
arrangements are possible. The names of most Order Dermaptera: Greek derma (skin) + pteron
orders end in ptera; of families in idea; of sub- (wing)
families in -inae, and of tribes in ini. Order Zoraptera: Greek zoros (pure) + a (with
The classification of insects is often debated, out)+pteron (wing)
but a common arrangement and the derivation Superorder Hemipteroidea
(from Greek or Latin) for the class Insecta fol- Order Psocoptera: Latin psocos (book louse)+Greek
lows. The order names generally are logical if you pteron (wing)
consider the appearance of the insects in that Order Hemiptera: Greek hemi (half)+pteron (wing)
 Classification
C 925

Order Thysanoptera: Greek thysanos (fringed) + groups of arthropods such as the Collembola,
pteron (wing) Diplura and Protura are sometimes considered to
Order Phthiraptera: Greek phtheir (louse)+a (with be insects. Classification systems (Figs.65 and 66)
out)+pteron (wing) are based on morphological similarities (phenet-
Series Endopterygota: Greek endo (inside) + pteron ics) and evolutionary relatedness (phylogenetics),
(wing) as well as comparative anatomy, physiology, and
Superorder Neuropteroidea behavior. Increasingly, the genetic component of
Order Megaloptera: Greek megalo (large) + pteron insects is being used to establish relatedness.
(wing)
Order: Raphidioptera: Greek raphio (a needle; refer-
ring to the ovipositor)+pteron (wing) Characteristics of the Major
Order Neuroptera: Greek neuron (nerve) + pteron Groups
(wing)
Superorder Coleopteroidea The major groups are characterized by a number
Order Coleoptera: Greek coleos (sheath) + pteron of fundamental differences. The members of sub-
(wing) class Apterygota lack wings, possess rudimentary
Order Strepsiptera: Greek strepti (twisted)+pteron abdominal appendages, practice indirect insemi-
(wing) nation, and molt throughout their life, whereas the
Superorder Panorpoidea subclass Pterygota possess wings (or did at one
Order Mecoptera: Greek mecos (length) + pteron time), generally lack abdominal appendages, prac-
(wing) tice direct insemination via copulation, and molt
Order Trichoptera: Greek trichos (hair) + pteron only until sexual maturity is attained.
(wing) Infraclass Paleoptera consists of primitive
Order Lepidoptera: Greek lepido (scale) + pteron insects. The wings cannot be flexed over the back
(wing) when the insect is at rest. The immature stages of
Order Diptera: Greek di (two)+pteron (wing) existing paleopterans live in aquatic habitats. The
Order Siphonaptera: Greek siphon (tube)+a (with Neoptera, on the other hand, are a diverse group of
out)+pteron (wing) relatively modern insects. They can flex their wings
Superorder Hymenopteroidea over the body. They display development in which
Order Hymenoptera: Greek hymen (mem the immatures are similar to the mature form
brane)+pteron (wing) (Exopterygota), or the immatures differ markedly
in appearance from the adults (Endopterygota).
Superorder Plecopteroidea, consisting of
Variations on this System of Plecoptera and Embiidina, is closely related to
Classification superorder Orthopteroidea. Both suborders have
chewing mouthparts; complex wing venation, with
Among the principal variations on this system of the hindwings larger than the forewings; and cerci.
classification are the grouping of Phasmatodea and They differ, however, in that the forewings are not
Mantodea into a single order, Dictyoptera; the thickened, and external male genitalia are lacking.
grouping of Megaloptera, Raphidioptera and The members of superorder Orthopteroidea
Neuroptera into Neuroptera; the splitting of (Polyneoptera) have chewing mouthparts, long
Hemiptera into two orders, Hemiptera and antennae, complex wing venation, large hind-
Homoptera; the grouping of Mallophaga and Sip- wings, thickened forewings, large cerci, and
hunculata into Phthiraptera; and the grouping of nymphs with ocelli. Several orders are considered
Strepsiptera with Coleoptera. Also, some additional to be orthopteroids: Phasmatodea, Mantodea,
926
C Classification

Classification, Figure 65 Diagram of the possible phylogeny of the hexapods, showing relationships
among the major groups (principally insect orders) and the temporal occurrence of major evolutionary
steps in insect structure and development.

Mantophasmatodea, Blattodea, Isoptera, Gryllob- Superorder Coleopteroidea consists of the

lattodea, Orthoptera, Dermaptera, and Zoraptera. orders Coleoptera and Strepsiptera. They are
In many older classification systems, they were all similar in that the metathorax is developed for
considered to be part of the order Orthoptera. flight, and bears functional wings. The forewings
This is a relatively primitive group. of the Coleoptera are reduced to hard wing cov-
Superorder Hemipteroidea (Paraneoptera) is erings, and even more reduced in the Strep-
also a large group, consisting of the orders Psocop- siptera, to small club-like appendages. They
tera, Hemiptera, Thysanoptera, and Phthiraptera. contrast strongly in that the Coleoptera is the
Unlike the Orthopteroidea, they lack cerci, and have largest order, and Strepsiptera one of the smaller
stylet-like structures associated with their mouth- orders.
parts (though in Psocoptera, chewing mouthparts Panorpoidea is another large superorder,
are preserved). Some groups are well designed for consisting of the orders Mecoptera, Trichoptera,
piercing the host and sucking liquids. Though this Lepidoptera, Diptera, and Siphonaptera. They
and the preceding superorders are considered to be share few common characters, however, such as
hemimetabolous, a few members of Thysanoptera a tendency for a reduced meso- and metaster-
and Hemiptera are physiologically holometabolous. num, the media and cubitus of the hind wing
The superorder Neuropteroidea is holome- arise from a common stem, and the terminal
tabolous, and consists of the orders Megaloptera, abdominal segments tend to function as an
Raphidioptera, and Neuroptera. Both aquatic and ovipositor.
terrestrial forms occur in this superorder. The Lastly, the superorder Hymenopteroidea
wings tend to bear numerous cells. consists only of the order Hymenoptera, though
 Classification
C 927

Classification, Figure 66 A recent assessment of phylogenetic relationships within Hexapoda based

on both morphological and some molecular characters (adapted from Wheeler et al., 2001, Cladistics
17:113169).

this is a very divergent, complex group. They bear Each Individual Order
numerous Malpighian tubules, unlike all other Phylum
endopterygotes, which have only four to six tubules. Orders
Also, their wing venation is often greatly reduced. Sampling Arthropods
928
C Clastopteridae

Clastopteridae Clavus

A family of bugs (order Hemiptera, suborder This term has several meanings, including the
Cicadomorpha). angular hind margin of the hemelytra in Hemiptera
Bugs (Fig.67); the club of an antenna; the knob at the
end of the stigmal or radial wing veins in
Hymenoptera; and the rounded or finger-like pro-
Claustral Colony Founding cess in the male genitalia of Lepidoptera.

A process of colony founding in which the initial

reproductives seal themselves of in cells, and pro- Claw
ceed to rear the initial brood using nutrients
obtained from their own tissues. A hollow, sharp, curved organ, located at the tip of
the tarsus (foot).
Legs of Hexapods
Clavate
Thickening toward the tip. This term is usually
Clearwing Moths
used to describe antennae with expanded tips.
(Lepidoptera: Sesiidae)
Antennae of Hexapods
Daniel Potter
University of Kentucky, Lexington,
Clavate Larva
KY, USA
This term is sometimes used to describe a larva
with an enlarged thoracic region, particularly Adults of the family Sesiidae(formerly Aegeriidae)
buprestid, cerambycid, and eucnemid larvae. are called clearwing mothsbecause a part of the
wings, especially the hindwings, lacks overlapping
scales and is therefore transparent. The body typi-
Clavola cally is dark-colored, but most species have con-
trasting yellow, orange, or reddish bands or
The antenna beyond the pedicel. The flagellum. markings on the abdomen, legs, or both. Males
Antennae of Hexapods and females often differ in coloration, and in some

Clavus, Figure 67 Front wing of a bug (Hemiptera: suborder Heteroptera), thickened basally and
membranous distally.
 Clearwing Moths (Lepidoptera: Sesiidae)
C 929

cases the amount of clear area in the wings. Virtually along their inner, rear margin, with a row of tiny
all species are day-flying. The moths may be seen curved spines that interlock with the fold; similar
sipping nectar from flowers or resting on foliage spines along the hindwing costa help to hold the
on sunny days. Many adult sesiids bear a striking wings together. The antennae are simple to bipecti-
resemblance to wasps, especially paper wasps nate, widening gradually and then narrowing again
(Polistes spp.) or yellow jackets. Being moths, they to the tip. The larvae are ivory white or cream-col-
cannot sting; however, this mimicry doubtless dis- ored except for a brownish, sclerotized head and
courages insectivorous birds and other vertebrate lighter thoracic shield. Each thoracic segment has
predators. The moths hovering flight and tendency one pair of small jointed legs. Abdominal segments 3
for some species to move the abdomen in a wasp- to 6, and 10, have fleshy lobes (prolegs), each ending
like posture contributes to the deception. in two transverse bands of tiny hooklike crochets.
Sesiid larvae tunnel in living branches, trunks, Many clearwing species have a 1-year life
root collars, or roots of trees and shrubs, and in canes cycle. Others require two years to complete a gen-
and vines of woody and some herbaceous plants. eration, whereas a few species have two generations
Granular, sawdust-like frass usually is expelled from per year. Winter is spent as a partially grown larva
the site of attack. Damage to the inner bark and within a gallery under the bark of the host plant, or
cambium can contribute to the decline and death of within stems, canes, or roots. Several sizes of larvae
host plants. Some species are economically impor- may overwinter, reflecting the fact that the eggs
tant pests of forest and landscape trees, or fruit crops. from which they eclosed were laid by different
The squash vine borer, Melittia cucurbitae, is a pest females over a number of weeks. Active feeding
of squash, gourds, and pumpkins. A few species resumes in early spring. Some species pupate in
induce plant galls, or feed as inquilines within galls late winter or spring, whereas others feed longer
of other insects. Most clearwing species exploit only and pupate later in the growing season. Before
a few closely-related species of trees, shrubs, or vines pupating, the larva extends its tunnel to the bark
as hosts. A few, such as the dogwood borer, Synathe- surface except for a paper-thin cover. Pupation
don scitula, attack a broad range of plants. occurs within a cocoon made from frass and bits of
The family Sesiidae belongs to the order Lepi- bark or soil held together with silken strands. The
doptera, suborder Ditrysia (Frenatae), and super- pupal stage lasts about 3 weeks. Empty pupal skins
family Sesioidea. Clearwing moths have a world often are left partially protruding from exit holes in
wide distribution with about 170 genera contain- the bark after the moths have emerged.
ing more than 1000 described species. Nineteen Flight activity, mating, and egg-laying by
genera and 155 species of sesiids are known from a particular species usually are finished within 4
North America, including such important pests as to 6 weeks after initial emergence. Adults of differ-
the raspberry crown borer, Pennisetia marginata; ent species emerge at certain times during the
grape root borer, Vitacea polistiformis; squash vine growing season, and their flight activity often is
borer, Melittia cucurbitae; lesser peachtree borer, restricted to a specific time of day. These temporal
Synanthedon pictipes; peachtree borer, Synanthe- differences likely are important for reproductive
don exitiosa; dogwood borer, Synanthedonscitula; isolation, especially since females of a number of
and lilac borer, Podosesia syringae. species emit chemically-similar sex pheromones
Adult clearwings are slender-bodied, small to to attract males.
medium-sized moths, wingspan 1.4 to 4.6 cm. The After mating, females deposit eggs singly in
forewings are narrow, at least four times as long as bark crevices, often around wounds, cankers, or old
wide, with anal veins reduced. The hind wings are larval feeding galleries. They seem to be attracted
shorter and somewhat more broad, with all three to plants that are injured or weakened by root
anal veins present. The forewings fold downward pruning, transplant shock, insect or disease injury,
930
C Cleptobiosis

drought, or other stress factors. Individual females Englehardt GP (1946) The North American clearwing moths
of the family Aegeriidae. Bulletin 190. U.S. National
typically live only about a week, during which they
Museum, Washington, DC
may lay several hundred eggs. Eggs hatch in about Johnson WT, Lyon HH (1988). Insects that feed on trees and
2 weeks, and larvae then bore into the bark and shrubs, 2nd ed. Cornell University Press, Ithaca, New
mine in the phloem and cambium, lengthening and York
Solomon JD (1995) Guide to insect borers of North American
enlarging the tunnel as they grow. Many species broadleaf trees and shrubs. Agricultural Handbook 706.
later enter the sapwood. Branch dieback, limb and USDA Forest Service, Washington, DC. 735 pp
trunk swellings, moist sap spots on the bark, gum Taft WH, Smitley D, Snow JW (1991) A guide to the clearwing
exudates, expulsion of larval frass, or protruding borers (Sesiidae) of the north central United States.
USDA North Central Regional Publication 394
pupal skins all may indicate that borers are present.
Woodpeckers are important in natural con-
trol. Ants, and in some cases field mice, moles and
skunks, prey upon the pupae. Eggs, larvae, and Cleptobiosis
pupae are attacked by various parasitic wasps or
flies. A fungus, Beauveria sp., sometimes infects A relationship in which one species robs the food
and kills the larvae. stores, or scavenges in the refuse piles, of another
In the early 1970s, scientists identified and species but does not nest in association with the
synthesized two major isomeric pheromone host.
components, the Z, Z- and E, Z- isomers of 3,13-
octadecadien- 1-ol-acetate, from the peach tree
borer and lesser peach tree borer, respectively. Sub- Cleptoparasite
sequent field testing soon revealed cross-attraction
of other clearwing species to these pure isomers, An organism that consumes the stored food of
their corresponding alcohols, or to various blends of another from its nest.
these compounds. This breakthrough allowed ento-
mologists to learn more about the flight periods of a
number of clearwing moth species, to survey local Cleridae
sesiid fauna, and to develop effective attractants for
some of the key pest species. A family of beetles (order Coleoptera). They com-
Traps baited with commercial synthetic phero- monly are known as checkered beetles.
mones are used by nursery operators and land- Beetles
scape managers to monitor clearwing moth activity.
This helps them to fine-tune timing of control
actions. Entomologists also are evaluating use of Click Beetles
such attractants for mass trapping or mating dis-
ruption of pests such as peachtree borer in orchards. Members of the family Elateridae (order
The most important management strategy is to Coleoptera).
minimize plant stress, because healthy trees, shrubs, Beetles
and vines are less likely to be attacked by borers.

References Clicking by Caterpillars

Although acoustic communication is well known

Eichlin TD, Duckworth WD (1988) Sesioidea: Sesiidae. In RB
Dominick et al (eds) The moths of America north of among certain moths (mostly in the context of
Mexico. Fasicle 5.1. 176 pp detecting ultrasonic cries of insectivorous bats),
 Clover Mite, Bryobia praetiosa Koch (Acari: Tetranychidae)
C 931

acoustic communication is widespread in Lepi- Cloaca

doptera. Vibrational signals are used by some
butterfly and moth larvae in communication The rectum, a common chamber into which the
with mutualistic ants, conspecifics, and pre anus and gonopore open; the vagina.
dators. However, sounds made by at least 12 Reproduction
families, including Tortricidae, Oecophorida, Vagina
Notodontidae, Saturniiidae, and Sphingidae, may
be involved in defense. Saturniid and sphingid
larvae produce audible (to the human ear) clicks Clone
that have been described as cracking or crack-
ling. Closure of the mandibles produces the A population of identical cells often containing
click sounds, and it follows disturbance of the identical recombinant DNA molecules. Also a
larvae as may occur when the insects are grasped group of organisms produced from one individual
or pecked by birds. The clicking sound often pre- cell through asexual processes. The offspring are
cedes regurgitation by the larvae, and regurgita- identical. The word may be used either as a noun
tion is known to be repellent to both vertebrate or a verb.
and invertebrate predators.
Vibrational Communication
Acoustic Communication in Insects
Acoustic Aposematism (Clicking) by
Closed Cell
Caterpillars
A cell bounded on all sides by wing veins.

Reference
Clothes Moths
Brown SG, Boettner GH, Yack JE (2007) Clicking caterpillars:
acoustic aposematism in Antheraea polyphemus and Members of the family Tineidae (order
other Bombycoidea. J Exp Biol 210:9931005 Lepidoptera).
Fungus Moths
Butterflies and Moths
Climatic Release

The release of a population from climatic con- Clothodidae

straints by a favorable change in weather, allowing
it to attain a population increase or outbreak. A family of web-spinners (order Embiidina).
Web-Spinners

Climax
Clover Mite, Bryobia praetiosa
The end point of an ecological successional sequence;
Koch (Acari: Tetranychidae)
the community has reached a steady state.
These clover and grass-feeding mites damage
Cline vegetation and also enter homes, becoming a
nuisance.
A geographic gradient in the frequency of a gene. Mites
932
C Club Fleas

Club Fleas Cluster Fly, Pollenia rudis

(Fabricius) and P. pseudorudis
Members of the family Rhopalopsyllidae (order Rognes (Diptera: Calliphoridae)
Siphonaptera).
Fleas Allen Heath
AgResearch Wallaceville, Upper Hutt,
NewZealand
Clubtails
The name cluster fly (or loft fly) is given to two
A family of dragonflies in the order Odonata: species of Northern Hemisphere blowflies (Cal-
Gomphidae. liphoridae) Pollenia rudis and P. pseudorudis
Dragonflies and Damselflies that preferentially breed in earthworms of the
genera Allolobophora, Eisenia (=Helodrilus) and
Lumbricus. Many other members of the genus
Clumped Distribution breed in earthworms, but so far as is recorded,
only P. rudis and P. pseudorudis invade buildings
A distribution of organisms in which there is in large numbers in autumn, achieving pest sta-
some aggregation of individuals that exceeds tus, leaving again in spring. The identities of
the clumping that would occur randomly. This these flies have been confused until recently.
is the most common distribution displayed by Only in 1985 was Pollenia pseudorudis recog-
insects. nized as distinct from both P. rudis and P.
angustigena, and the previously named P. obscura
was subsumed in P. pseudorudis.
Apart from New Zealand records, there is
Clusiid Flies no clear indication that P. pseudorudis invades
houses elsewhere in the world, because in the
Members of the family Clusiidae (order Diptera).
Northern Hemisphere and Hawaii, only P. rudis
Flies
is recorded as the nuisance species, although it
may just be that no effort has been made to
gauge whether P. pseudorudis is present as well.
Clusiidae It is possible that both species (and perhaps oth-
ers) occur together in houses in North America,
A family of flies (order Diptera). They commonly and perhaps elsewhere, as they do in the wild,
are known as clusiid flies. but possibly because of the P. obscura synonymy
Flies no distinction has been attempted. Lofts are a
common sanctuary, hence one of the common
names, and the flies cling together, often in ropy
Cluster Analysis clusters. They have been described as the most
frustrating of structural insect pests.
A method of hierarchically grouping taxa or First reports of cluster flies as a household
sequences on the basis of similarity or minimum nuisance appeared in the mid nineteenth century,
distance. UPGMA is an unweighted pair group although the first published mention of a fly asso-
method using the arithmetic average. WPGMA is ciated with earthworms was in 1881, when Charles
the weighted pair group method using the arith- Darwin, in his treatise on earthworms reported an
metic average. earlier observation by Perrier.
 Cluster Fly, Pollenia rudis (Fabricius) and P. pseudorudis Rognes (Diptera: Calliphoridae)
C 933

In the 1930s, a link between earthworms and

swine influenza was postulated, with a view that
the virus of swine influenza is a surviving proto-
type of the agent responsible for the great human
pandemic of 1918 and that hogs and earthworms
may serve as the source of future epidemics.
Because of its links with earthworms, the cluster
fly was regarded as a possible vector of human
influenza, an hypothesis that has not been sup-
ported by subsequent research.
The tribe Polleniini to which the cluster flies
belong occurs in four distinct geographical
groups, the Palearctic (with at least 30 species), Cluster Fly, Pollenia rudis (Fabricius) and
the Nearctic and Austro-Oriental regions, each P.pseudorudis Rognes (Diptera: Calliphoridae),
with at least eight species in the genus Melano- Figure 68 A recently emerged cluster fly. Normally
dexia and two in Pollenia. The Australasian and the fly at rest has the wings folded back more than
Oceanian regions have three genera, Anthraco- is shown here, and they obscure the abdomen
myia (which is monotypic), Dexopollenia (five (photo courtesy of Lynnette Schimming).
species) and Pollenia (43 species, the majority in
New Zealand). However, there are still a further buildings that act like large flytraps. In the afternoon
17 species unnamed in New Zealand designated they settle on the upper parts of walls and on roofs,
as species a to species q inclusive. It appears facing towards the setting sun. As the sun sets, the
that only the two Northern Hemisphere (widely flies crawl into any crevice and into roof spaces, and
distributed throughout the Nearctic and Palearc- may enter rooms, using drapes, pictures, etc., as hid-
tic) species, P. rudis and P. pseudorudis, congre- ing places. For a few days, the flies will go back out-
gate in houses, although further work may alter side, and then return at night, but this behavior
this view. Both species have been intercepted in eventually ceases, except if there is a spell of mild
New Zealand, but only P. pseudorudis, which weather during winter. Mild weather will break the
reached New Zealand in the early to mid-1980s, fragile hibernation of the flies and they will become
appears to have established and, over the next 20 sluggishly active. Outside of human habitations, the
years or so, subsequently dispersed throughout overwintering locations of cluster flies are not well
both main islands. known, although they have been recorded from the
In the Holarctic, a P. rudis species group is tunnels made by beetles in timber and fungi and also
recognized, and contains six species of Pollenia: in animal burrows. The flies return to the outside in
P. angustigena, P. rudis, P. pseudorudis, and three spring, again causing a nuisance as they do so.
exclusively in the Palearctic: P. hungarica (Cen- The cluster fly P. rudis is frequently seen in
tral Europe and southern parts of Scandinavia), very large numbers in spring moving over moist
P. longitheca (eastern Mediterranean) and P. grass. The female deposits a batch of eggs on the
luteovillosa (Algeria and Morocco). There is a soil surface and then moves some distance away
seventh species of doubtful status. and deposits another batch, about 100130 eggs
The adult flies (Fig.68) are slow-flying, easily- in all. Three days later the eggs hatch and the lar-
caught insects; they are active in spring and summer vae descend into the soil by following natural pore
in pasture and gardens, and then, as ground tem- spaces, such as gaps between plant stems and soil
peratures begin to drop in autumn (fall), the flies and worm burrows, although not if the latter are
move towards shelter, usually houses or other blocked by casts. It seems the larvae locate a host
934
C Cluster Fly, Pollenia rudis (Fabricius) and P. pseudorudis Rognes (Diptera: Calliphoridae)

by a random locomotion through the soil pores A number of species of worms are variously
rather than following any product of the host. reported as hosts. In Europe, cluster flies attack
Some species of earthworms emerge from their Allolobophora chlorotica, A. (latterly Eisenia
burrows at night and move freely about on the formerly Helodrilus) rosea, and L. terrestris, whereas
surface, and after rain many worms can be seen in North America both of the Allolobophora spp. as
above ground. This surface movement could be a well as A. caliginosa are parasitized. But A. rosea
mechanism that would improve the potential for and A. chlorotica seem to be the most common
cluster fly larvae to encounter potential hosts. hosts in North America; both are surface-dwelling
Adult flies are on the wing from early spring species occurring mainly in the top 10 cm of the
in the Northern Hemisphere (February, March) to soil. In general, attempts to experimentally infest
late autumn (October, November). They are some- worms with P. rudis larvae have met with mixed
times attracted to horse and human feces, but are success and only A. rosea was infested in all
more attracted to meat and fruit, with banana attempts. It is possible to rear P. rudis in the labora-
reported to be especially good bait. tory using A. rosea as a host. Parasitism in the field
Larvae enter the earthworm through almost in North America is said to occur only in A. chloro-
any point in the body wall, but mostly on the dor- tica and A. rosea, although other species (A. caligi-
sal side and sometimes through spermiducal and nosa, L. terrestris, L. rubellus, Eiseniella tetraedra,
other pores. Larvae must penetrate a worm within Eisenia foetida, Octalasium lacteum) in a crushed
3 days after hatching if they are to survive. Pene- form will support first instar larvae. Studies in
tration is attempted under the influence of a sub- Hungary showed that P. rudis, P. pseudorudis and P.
stance present in both the slime and coelomic hungarica could be bred out of A. rosea.
fluid, which has been named penetration-induc- The sexes of overwintering flies are approxi-
ing factor. They have been reported to re-emerge mately equal in numbers and the abdomen of flies
after a short period to produce an opening through at this time is full of fat globules, possibly the rem-
which they protrude the posterior spiracles. It has nants of larval fat bodies. The following spring, the
been reported that during the first two stadia the flies possess a shrunken or desiccated appearance
larva acts as an internal parasite, and during the because the fat has been used up during the winter.
last it feeds on the host from the outside. Larvae It has been reported that there are important
may also leave the host and commence feeding on differences in the life history of P. rudis in Europe
healthier parts of the same worm or on a fresh compared with North America, with the first instar
worm. Up to seven larvae may occur in a single larva as the over-wintering stage in Europe, rather
worm, although a single larva will feed on as many than the adult as in North America. In addition,
as three earthworms, resulting in larger pupae there is only one generation a year reported from
than usual. The larvae can eventually eat the entire Europe. However, apparently there are three species
body of the worm and pupate in the soil nearby. in the rudis species complex in North America and
Development times vary with climatic condi- the life cycle of each may differ. Discrepancies
tions. In Canada, total development time is 2530 between North American and European reports
days at 23C, of which 1114 days are spent in the with regard to cluster fly biology (and coincidentally
pupal stage. There are three or four generations larval morphology) may be because early work may
per year. In Europe, after wintering in a dormant not apply to any rudis group member and it is pos-
state in the body cavities of earthworms, the larvae sible that the authors worked with different species.
molt twice over about a 20 day period and then Enlargement of the distribution of P. rudis
pupariate outside the host. The pupal stage typi- into the Oceanic and Australasian regions has
cally lasts from 32 to 45 days, although it can be as occurred relatively recently, with Hawaii record-
short as 7 days at high temperatures (e.g., 27C). ing its first flies in 1955, with A. caliginosa serving
 Cluster Fly, Pollenia rudis (Fabricius) and P. pseudorudis Rognes (Diptera: Calliphoridae)
C 935

as the host. Pollenia rudis was intercepted at the health nuisance, and a town water supply con-
New Zealand border in 1981. This species does not tained in a large wooden reservoir tank in New
appear to have broached the border, as no speci- Zealand had to be drained after cluster flies set-
mens have been subsequently found in the wild. tled inside and an excess of fecal coliform bacteria
However, in 1984 a species soon to be recognized was found in the water. Invasion of a hospital in
as P. pseudorudis was found in a house in Auck- Europe provoked concern and although no bacte-
land, New Zealand, and over the next 19 years riologically sterile flies could be found, an enrich-
spread throughout the country, but up to 2007 no ment culture technique had to be used to provide
worm hosts have yet been identified. sufficient bacteria for identification. This suggests
During the first 12 years after its discovery in that cluster flies may be a low health threat.
New Zealand, P. pseudorudis populations estab- Keeping cluster flies out of houses can be dif-
lished themselves throughout the North Island, ficult, although finding possible entry points and
being more numerous in some years and districts blocking them with appropriate materials such as
that at other times. Simultaneously, in 1996 with wire mesh can work. The flies are capable of squeez-
the end of this initial expansion period, the first ing through very small crevices, however, and even
South Island populations were recorded. Further the most assiduous search may miss openings. The
expansion in the South Island took place over the principal control method favored by pest control
next 7 years to the southernmost districts. It firms involves insecticide application on outside
appears that P. pseudorudis is not found in either walls of buildings, fogging of interiors, such as roof
Hawaii or Australia at present, although P. rudis spaces, and even treatment of vegetation and soil.
occurs in the former. The clustering habit of adult Overuse of insecticides both inside and outside is
flies would provide an opportunity for them to not a particularly safe option for either humans or
collect in shipping containers and facilitate their other animals. Simply vacuuming flies up as they
trans-hemispheric movement. enter houses is safe and effective, especially because
It might be thought that the large numbers of flies killed by insecticides would have to be cleared
cluster flies appearing each year would have a det- up in some manner in any event.
rimental effect on local earthworm faunas. In
Europe and North America, four species of earth-
worms are used as hosts: A. chlorotica, A. caliginosa, References
A. rosea and L. terrestris. However, there have been
no reports of notable reductions in earthworm Heath ACG, Marris JWM, Harris AC (2004) A cluster fly, Pol-
lenia pseudorudis Rognes, 1985 (Diptera: Calliphori-
numbers or any horticultural consequences. Given
dae): its history and pest status in New Zealand. NZ J
the enormous numbers of earthworms in pasture, Zool 31:313318
variously estimated from 70,000 to around 10 mil- Oldroyd H (1964) The Natural history of flies. Weidenfeld &
lion per hectare, there would seem to be enough to Nicolson, London
Rognes K (1987) The taxonomy of the Pollenia rudis species-
spare for cluster fly population maintenance. group in the Holarctic region (Diptera: Calliphoridae).
Apart from this unresolved question of Syst Entomol 12:475502
whether earthworm numbers suffer as a conse- Thomson AJ (1973) The biology of Pollenia rudis, the cluster
quence of cluster fly activity, the insects evoke fly (Diptera: Calliphoridae). I. Host location of first-in-
star larvae. Can Entomol 105:335341
strong emotional responses in humans and pres- Thomson AJ, Davies DM (1973) The biology of Pollenia rudis,
ent a major housekeeping nuisance. If swatted the cluster fly (Diptera: Calliphoridae). II. Larval feed-
they leave greasy spots. There can also be eco- ing behaviour and host specificity. Can Entomol
105:985990
nomic effects if businesses decide to close because
Yahnke W, George JA (1972) Rearing and immature stages of
of fly activity, and such closures have been the cluster fly (Pollenia rudis) (Diptera: Calliphoridae)
recorded. In addition, there is a potential public in Ontario. Can Entomol 104:567576
936
C Clypeofrontal Suture

Clypeofrontal Suture Coarctate Pupa

The suture marking the division between the A pupa that is enclosed in the hardened shell
clypeus and the epicranium. The clypeal suture. formed by the last larval cuticle. This is usually
called a puparium.

Clypeus Coccidae
A part of the head below the front (Fig. 69) to
A family of insects in the superfamily Coccoidae
which the labrum is attached.
(order Hemiptera). They sometimes are called soft
Head of Hexapods
scales, wax scales, and tortoise scales.
Bugs
Scale Insects and Mealybugs
Coarctate Larva
This term usually is applied to the third phase of Coccinellidae
hypermetamorphic development in Meloidae. At
this point in development, which corresponds A family of beetles (order Coleoptera). They com-
approximately to instar six, the larva typically is monly are known as ladybird beetles.
strongly sclerotized, immobile, and the legs are Beetles
greatly reduced. Sometimes it is used to describe
a larva that is similar to the puparium of a fly, in Coccoidae
which the cuticle of the preceding instar is not
completely shed but remains attached to the pos- A superfamily of insects in the order Hemiptera.
terior end of the body. They sometimes are called scale insects, though

Clypeus, Figure 69 Front view of the head of an adult grasshopper, showing some major elements.
 Cockroaches (Blattodea)
C 937

mealybugs also are found in this superfamily. This rofessor of Entomology and Zoology. But there
P
superfamily contains such families as Margarodi- his wife died giving birth to a second son, who died
dae, Ortheziidae, Kerridae, Coccidae, Aclerididae, at the age of eight, the first son having died in
Cryptococcidae, Kermesidae, Asterolecaniidae, infancy in Jamaica. Later, he took an American
Lecanodiaspididae, Cercoccidae, Dactylopiidae, wife, Willmatte. In New Mexico, he developed an
Diaspididae, Conchaspididae, Phoenicococcidae, interest in wild bees, studied their taxonomy and
Pseudococcidae, and Eriococcidae. behavior, and eventually published description of
Scale Insects and Mealybugs 5,480 new names for species, subspecies and vari-
Bugs eties, together with 146 new names for genera and
subgenera. In 1903 he returned to Colorado and
took a position as Curator of the Museum of Ento-
Cochineal Insects mology at Colorado College. Here, he continued
his work on bees but also developed an interest in
Members of the family Dactylopiidae, superfamily paleoentomology and paleobotany and numerous
Coccoidae (order Hemiptera). other natural history subjects, and even art, poetry
Bugs and politics. He traveled to Europe, Japan, Thailand,
Scale Insects and Mealybugs India, Siberia, Australia, Morocco and other parts of
Lacquers and Dyes from Insects Africa, Canada, and Honduras. Upon retirement, he
divided his time between Colorado and southern
Cockerell, Theodor Dru Alison California. His published works amount to over
3,000 items, in which he described over 7,000 spe-
cies of plants and animals, extant and fossil. He died
Theodor Cockerell was born in London on August on January 26, 1948, in California.
22, 1866, and became interested in natural history
at an early age with parental encouragement. This
interest extended to insects and slugs and snails and Reference
was further encouraged after the death of his father
by a trip to Madeira. Upon finishing school, he was *Mallis A (1971) Theodore Dru Alison Cockerell. In: Ameri-
employed by a flour company, but developed can entomologists. Rutgers University Press, New
tuberculosis. At the age of 20 he sailed to the United Brunswick, NJ, pp 357362
States and journeyed to Colorado to find a climate
that would cure his illness. That climate was benefi-
cial and his health recovered. In Colorado he worked Cockroaches (Blattodea)
on a catalogue of the flora and fauna there, but
returned to London in 1890 to work in the British John L. Capinera
Museum (Natural History). He was invited by University of Florida, Gainesville, FL, USA
Alfred Russel Wallace to help in the preparation of
a new edition of the latters book Island Life. In The cockroaches (also called roaches) are mem-
1891 he was appointed Curator of the Public bers of an ancient order of insects. The order name
Museum (now Institute of Jamaica) in Kingston is derived from the Latin word blatta, or cock-
and became interested in scale insects. Unfortu- roach. They are closely related to the praying man-
nately, his tuberculosis had returned by 1893. For- tids (Mantodea), and often are grouped with them
tunately for him, he was able to trade jobs with (as suborders) to form the order Dictyoptera.
C.H.T. Townsend of the New Mexico College of Though the mantids evolved from the cockroaches,
Agriculture, and he moved to Las Cruces to become they are a specialized group of predatory insects
entomologist at the Experiment Station and that warrant individual recognition. Termites
938
C Cockroaches (Blattodea)

(Isoptera) can also be placed in the order Dicty- moderately long, but some species run quite rapidly.
optera, and are considered by some to be social There are five tarsal segments. Cerci are present,
cockroaches. The order name for cockroaches though varying in length, and consisting of one to
sometimes is given as Blattaria. five segments. Some species burrow, and these are
among the heaviest of the cockroaches. Megoblatta
rhinoceros, for example weighs over 30 g. Burrowers
Classification are often wingless, heavy-bodied, hard, and bear
spines. On the other end of the scale, some cock-
About 4,000 species are found throughout the roaches inhabiting the nests of social insects (mostly
world, though most are tropical. They usually are ants and termites) are only 2.7 mm long. Indeed, it is
grouped into six families. surprising to most people that small species pre-
Order: Blattodea dominate, but they are easily overlooked.
Superfamily: Blattoidea The accessory glands of female cockroaches
Family: Blattidae produce oothecae, or egg cases, which contain few
Superfamily: Blaberoidea to many eggs. The eggs are usually are arranged in
Family: Polyphagidae two rows, and in many cases the ootheca is
Family: Cryptocercidae surrounded by a thick, protective covering. The
Family: Nocticolidae ootheca may be inserted into a protected location
Family: Blattellidae or just dropped by the female in the general envi-
Family: Blaberidae ronment in which she lives, but others carry the
ootheca until the eggs are ready to hatch. Cock-
roaches in the family Blaberidae retain their eggs
Characteristics internally and give birth to living young.
Sexual dimorphism is sometimes quite pro-
The cockroaches are small to large in size, measur- nounced. The sexes are so different in some spe-
ing from about 2 mm to over 60 mm. The largest, cies that they were originally described as separate
Megaloblatta blaberoides, measures 100 mm when species. These differences suggest that competition
the tegmina are included in the measurement, and to win a mate is quite keen. The abdomen of the
has a wing span of 185 mm. They are flattened, oval, female, not surprisingly, is more elongate.
and often dark or reddish brown, though some are As with other hemimetabolous insects
black or green. Species that live under bark or rocks (incomplete metamorphosis), the immatures
sometimes are extremely flattened, though this resemble the adults in general appearance, differ-
degree of compression also is useful for defending ing primarily by the absence of the tegmina and
against attack by ants because the cockroaches cling wings in immatures (nymphs). Immatures also
so tightly and closely that the ants cannot get beneath have poorly developed genitalia, and lack charac-
them to their more vulnerable under-surface. The ters useful for identification. Some are colored
head is concealed (when viewed from above) by the quite differently from the adult stage.
pronotum. Compound eyes are usually present Although we tend to think of cockroaches as
and well-developed, though absent in some cave- nocturnal, some are active during the day. Not sur-
dwelling species and myrmecophiles. The filiform prisingly, their color is quite different. Day-active
antennae are long. They possess chewing mouth- cockroaches often sport bright colors: some are
parts. Both males and females usually bear two pairs brightly colored; others are aposematically colored
of wings, though the front wings are thickened. Both because they are chemically defended; still others
short-winged and wingless species are known. The mimic other species (Batesian mimics). They
cursorial legs are not greatly modified, and only commonly mimic beetles, including such brightly
 Cockroaches (Blattodea)
C 939

c olored species as ladybird beetles (Coccinelli- aforementioned preferences, some cockroaches

dae), carrion beetles (Silphidae), and metallic have not only managed to exploit desert environ-
wood-boring beetles (Buprestidae). Cave-dwelling ments, but have become some of the most abun-
species are typically depigmented, and have a thin dant mesofauna present. Many desert dwellers live
cuticle, elongated appendages and loss of vision. beneath the sand, at least for a portion of the day.
The cockroaches are basically terrestrial They also take advantage of natural burrows cre-
insects, though some semi-aquatic species are ated by rodents and vertebrates. Only a few species
known. Flight is not well known for most species, actually inhabit the water, though many favor the
but most seem to fly poorly, despite the presence water-vegetation interface.
of large wings. The presence of wings is the primi- Cockroaches are usually thought of as scav-
tive condition, and wings have been reduced or engers or omnivores. However, this mostly reflects
lost in many taxa. Those living below-ground or in our knowledge of domiciliary pest species, plus
burrows, galleries or crevices are most prone to the tendency of cockroaches to behave abnormally
winglessness, as are those living in stable habitats. when constrained to the laboratory environment.
The absence of wings in the adult form of some Most display some degree of preference, though
species is associated with retention of juvenile they are by no means highly selective (Table 14).
characters (paedomorphosis). For example, in a natural environment such as a
tropical rain forest, there seem to be three domi-
nant night-time feeding strategies: they forage on
Habitats and Food the forest floor, feeding on decaying vegetation but
also ingesting nematodes, fungi, insects, and other
Cockroaches are found in nearly all habitats, from invertebrates; they emerge from crevices and tree
the forest canopy to the soil, within burrows and holes, ascend to a preferred height in the trees, and
caves, within logs and detritus, and in nests of social feed on material that has fallen onto the leaves or
insects, rodents, reptiles and birds. They are most is growing on the leaves; they emerge from har-
numerous in the hot, humid tropics, between 30N borages and flit about the vegetation irrespective
and 30S. They are also more common at sea level of height, scraping algae and other microvegeta-
(where temperatures are warmer) rather than at tion from the tree foliage, bark, or elsewhere.
high altitudes. In the tropics, there is considerable Cockroaches search actively for food but also use
vertical stratification on trees at night, with most olfaction to locate suitable food. They usually con-
species returning to the ground litter during the sume the food as they find it, though some species
day. The species that inhabit the most elevated por- will transport food elsewhere. They can learn
tions at night are also the best fliers; not surpris- where food is located and return after an absence.
ingly, the flightless species are lowest on the trees. Juvenile cockroaches require more nitrogen than
Favored habitats of cockroaches are dark, do older cockroaches so they initially favor meals
humid, poorly ventilated, and cramped or crowded. from animal or microbial sources. Females con-
Thus, they are commonly found with loose sub- sume more than males. Generally cockroaches are
strate such as leaf litter and clods of soil. Some not thought of as plant pests, but there are impor-
force themselves into small voids such as spaces tant exceptions. In a closed environment such as a
under bark, within the bases of palm trees, or greenhouse, any species can be damaging if they
under rocks. Only a few excavate burrows in wood become sufficiently abundant. Others, such as Pyc-
or compacted soil, but rotting logs are popular noscelus surinamensis and Blatella asahinai, com-
habitats. Caves may or may not be populated. The monly are associated with plant injury, even under
presence of vertebrate guano maintains large field conditions. Cockroaches are quite tolerant of
numbers of cockroaches in caves. Despite the starvation, living from five to over 40 days without
940
C Cockroaches (Blattodea)

Cockroaches (Blattodea), Table 14 Diet of four species of Parcoblatta based on nocturnal observations
(after Gorton REJ (1980) The University of Kansas Science Bulletin 52:2130)
Food source P. pennsylvanica P. uhleriana P. lata P. virginica
Mushrooms + + +
Cambium +
Flower petals +
Moss +
Sap + +
Cercopid spittle +
Live insects +
Bird feces +
Mammal feces +
Mammal cartilage +

water and food. Water is a more critical resource, in locations with these chemicals. The response is
and they can survive longer without food than not species specific: they prefer the chemicals pro-
without water, perhaps 6090 days. Dead conspe- duced by their own species, but will aggregate at
cifics and shed cuticles are a common food sites contaminated by other species, including dis-
resource; not surprisingly, biting and cannibalism tant relatives. Due to their lack of specificity, the
are reported. chemicals are not usually considered to be aggre-
The digestive system of cockroaches is well gation pheromones, but they clearly are a form of
equipped with a diversity of microbiota. The resi- behavior-eliciting chemicals. Other factors such as
dent fauna and flora, plus the microbes ingested acoustic, tactile, visual and olfactory stimuli also
along with food, comprise a rich microbial brew influence aggregation, as do environmental stim-
that enhances fermentation. They also contribute uli such as light, humidity, temperature, and air
cellulases, though endogenous cellulases also movement.
occur. It has been postulated that cellulose inges-
tion indirectly benefits cockroaches by fueling
their microbial gut inhabitants, with the microbes Parental Care
and their products being the primary source of
nutrition. The significance of microbes in the gut Most cockroaches display some form of parental
of cockroaches is seen in the regular copropha- care, though the degree of care differs (Table 15).
gous (feces-feeding) behavior of young cock- Care of eggs is most widespread; carrying and
roaches, which provides an important inoculum hiding oothecae, and defense of oothecae, are
for the young insects. The wood-feeding cock- examples of care. Brooding behavior is a short-
roaches in the family Cryptoceridae are the link to term association of the mother and neonates. In
termites. Not surprisingly, digestion is about the some species, the young cluster around, under
same in cryptocerids and termites, the principal and on the mother, though this behavior may
difference between the two groups being the evo- only persist for about a day. Though often not
lution of a higher level of sociality in termites. lasting long, this behavior allows the cuticle of
Fecal pellets are attractive to cockroaches. neonates to harden. The transfer of gut microbi-
Fecal chemicals function as short-distance attrac- ota also may occur at this time, probably via a
tants and arrestants. Cockroaches may aggregate fecal meal.
 Cockroaches (Blattodea)
C 941

Cockroaches (Blattodea), Table 15 Parental care in cockroaches where offspring are provided with bodily
secretions by adults (adapted from Nalepa, Bell (1997) Social behavior in insects and arachnids)
Offspring
Species Location Food source
Perisphaerus sp. Cling ventrally Hemolymph
Trichoblatta sericea Cling ventrally Sternal exudate
Pseudophoraspis nebulosa Cling ventrally ?
Phlebonotus pallens Under tegmina ?
Thorax porcellana Under tegmina Tergal exudate
Gromphadorina portentosa Abdominal tip of female Secretion from brood sac
Salganea taiwanensis Mouthparts of adult Stomodeal fluids
Cryptocercus punctulatus Abdominal tip of adult Hindgut fluids
Cryptocercus kyebangensis Abdominal tip of adult Hindgut fluids
Blatella vaga Under tegmina Tergal exudate

Sometimes the brooding behavior is direct mineralization of soil, because that is the
extended for a longer period of time, perhaps 2 role of microorganisms. Rather, it is to put the
weeks. Females may accommodate offspring organic material in contact with the microbes.
during this period by allowing young cock- This is done by fragmenting litter, exposing litter
roaches to cling to her body, and some have to microbes, and by transporting microbes to new
evolved external brood chambers under their resources. Cockroaches are less dependent on
wing covers. An example of a higher level of water for functioning than are microbes, and
brood care is found in Thorax porcellana, which microbes in the gut are afforded the correct con-
maintains its young in a brood pouch for about ditions for activity. Also, the fecal pellets produced
7 weeks. It seems that the young feed on a pink- by cockroaches are an important substrate for
ish material secreted by the dorso-lateral regions microbes, and speed the return of above-ground
of the tergites. Parental feeding of young is not productivity to the soil. Microfauna such as mites,
unusual. Usually it is only the female that is springtails, nematodes and protozoa utilize the
involved in parental care. bacteria and fungi growing on the pellets as a
principal food resource. The importance of litter
decomposers for soil formation and enrichment
Ecological Importance is widely acknowledged. What is not known, how-
ever, is the relative importance of cockroaches.
Cockroaches contribute to ecosystem function- We can likely assume that it is quite significant in
ing by breaking down organic matter and aiding tropical forests, but in temperate forests they also
in release of nutrients. They are aided both by are abundant, often comprising about half of the
their endogenous cellulases and their microbial soil macrofauna.
symbionts. Cockroaches can be considered to be
soil fauna, though they rarely are acknowledged
as such. The principal diet of cockroaches is Domiciliary Cockroaches
organic material, and in living and feeding in the
litter, soil and decaying trees, they contribute to Some domiciliary species invade dwellings,
the make-up of the soil. Their role is not in the and a few species are well-adapted to living in
942
C Cockroaches (Blattodea)

buildings and on ships, where they can become than adults, wingless and dark brown in color. Ger-
numerous enough to be considered pests. Lack of man cockroaches are primarily indoor pests. They
hygiene is normally associated with cockroach have strict moisture requirements so they are usu-
infestation in temperate areas, though in tropical ally found in kitchen and bathroom areas. Adults
and subtropical regions cockroaches live out-of- live about 6 months, and during this time the female
doors and invade dwellings irrespective of produces from 4 to 8 oothecae. The female carries
hygiene. Cockroaches often produce an odor that the egg case throughout embryonic development
is unpleasant, and are implicated in a limited (34 weeks) often releasing it from her body only
amount of disease transmission. They are a major hours before the nymphs hatch. Each female pro-
source of allergens. Cockroaches are often the tar- duces about 28 nymphs in each egg case. German
get of chemical suppression efforts, especially in cockroaches are the most prolific cockroach pest
food establishments. Thus, it is not surprising that species, most likely to be insecticide resistant, and
insecticide resistance is widespread in some spe- therefore the most difficult to control.
cies. Cockroaches may be eaten by predatory ver- An increasingly important species is the
tebrates, and parasitized by nematodes and mites, brown-banded cockroach, Supella longipalpa.
but the most important natural enemies are egg Although it is favored by warm climates, it can be
parasitoids. About six families of wasps, but par- quite abundant in more temperate environments,
ticularly Evaniidae and Eulophidae, parasitize and has replaced German cockroach as the domi-
cockroach eggs, sometimes quite effectively. nant pest species in some areas. It is more tolerant
of low humidity than German cockroach, so it is
found inhabiting areas without a ready source of
Cockroaches as Pests water, such as bedrooms and closets. The common
name is most descriptive of the nymphal stage,
Traditionally, efforts to suppress cockroach popu- though even the adult has two dark bands on the
lations in the urban environment have relied almost wings. It lacks the two parallel dark stripes found
exclusively on repeated applications of synthetic on the prothorax of German cockroaches. The
pesticides. However, the chemical approach to female carries an egg capsule with up to 18 eggs
cockroach control has become increasingly less initially, but after a day or two she attaches it to an
popular. This is primarily due to the development object. The incubation period of eggs is about 70
of multi-chemical resistance among German cock- days, and time to complete development is about
roach populations and increased public concern 160 days.
about pesticide exposure in their living environ- Some other pest species include the Ameri-
ment. These two issues have led to development of can cockroach, Periplaneta americana, Australian
less toxic approaches to cockroach management. cockroach, P. australasiae; brown cockroach,
P. brunnea; smoky-brown cockroach, P. fuligi-
nosa; Oriental cockroach, Blatta orientalis; and
The Principal Cockroach Pest the Florida woods cockroach, Eurycotis floridana.
Species These other species of cockroaches (Fig.70) are
much larger and heavier than German and
The predominant pest cockroach species in the brown-banded cockroaches. Adults range in size
world is the German cockroach, Blattella germanica from 3 to 4 cm in length and are reddish brown
(Fig.70). German cockroaches are small, with adults to black in color. Some of these large cockroaches
<1.5 cm in length. They are gold in color and have can live up to 2 years in the adult stage. Adult
two dark longitudinal bands on their pronotum near females can produce an egg case about every 12
the head. Immature German cockroaches are smaller weeks. A typical female will produce about 2080
 Cockroaches (Blattodea)
C 943

Cockroaches (Blattodea), Figure 70 Some common cockroaches: top left, German cockroach, Blatella
germanica; top right, brown-banded cockroach, Supella longipalpa; second row left, American c ockroach,
Periplaneta americana; second row right, Australian cockroach, Periplaneta australasiae; third row left,
smoky-brown cockroach, Periplaneta fulginosa; third row right, Florida woods cockroach, Eurycotis
floridana; bottom left, Oriental cockroach, Blatta orientalis; bottom right, Cuban cockroach, Panchlora
nivea (photos by J. L. Castner, University of Florida).
944
C Cockroaches (Blattodea)

oothecae during her lifetime, each containing and toilets to keep the drain trap filled and off lim-
1520 nymphs. Peridomestic females release the its to cockroaches.
egg case from their body soon after it has devel- Covering vent pipes on the roof with fiberglass win-
oped. They then glue the egg case to a surface, dow screen will prevent cockroaches from migrat-
usually in a hidden, moist area. In contrast, Ger- ing up from sewer connections and gaining ready
man cockroach females continue to carry the egg access to the roof, and hence to attics and windows.
case throughout embryonic development. Groceries, produce and other packaged food prod-
Some cockroaches live both indoors and out- ucts may have been stored in infested locations
of-doors, especially in warm climates, and are before they were purchased. Make an effort to vis-
called peridomestic cockroaches. Peridomestic ibly scan all grocery items for evidence of cock-
cockroaches normally breed outdoors in sewers, roachs before putting them away.
palm trees, tree holes, piles of firewood, water Children can transport cockroaches from school
meters, well pumps, mulch, and flower beds. These to home in book bags and lunch pails. Inspect
cockroaches usually enter homes only occasion- these items on a regular basis.
ally, when foraging for food, water or warmth. In
some situations, however, they will establish breed- Sanitation is critically important. For exam-
ing populations in attics, crawl spaces, wall voids ple, German cockroaches can remain alive for
and other indoor areas. approximately 2 weeks with no food or water and
for 42 days if only water is available. Therefore, it is
important to realize that cockroaches can survive
Management on minute amounts of food such as crumbs, grease
or food residue.
Exclusion and Sanitation
Indoor trash containers should be emptied fre-
Long-term prevention of cockroach infestation is quently, and kept clean both inside and out. Plastic
the best means of ensuring a cockroach free bags lining trash containers can be kept closed
environment. This is most easily accomplished by with twist ties. This will prevent cockroaches from
exclusion (preventing cockroach entry) and being attracted to the garbage area.
sanitation (elimination of cockroach resources). Filled indoor garbage containers should be removed
Not only will these measures prevent a future from the dwelling immediately and placed in out-
infestation, they will also help to reduce an exist- door containers with tight fitting lids or dumpsters.
ing cockroach problem. Methods of preventing Keeping the area around dumpsters or other out-
cockroach entry include: door garbage storage areas clean and free of debris
will also prevent peridomestic cockroach infesta-
Cockroaches migrate easily through multi-unit tions in the area.
dwellings via plumbing and electrical connections. Frequent emptying of sink strainers and running
Sealing gaps around plumbing, wall outlets and of the garbage disposal and will prevent food
switch plates will prevent cockroaches from build up in the sink drain.
migrating from infested units to others. Washing dishes immediately after a meal will pre-
Keep doors and windows closed and screened. vent cockroaches from consuming food residue
Also, caulk cracks and gaps that may allow perido- on dishes. Unwashed dishes are a major source of
mestic cockroaches to invade from outdoors. food for German cockroaches.
Peridomestic cockroaches frequently enter homes Kitchen appliances (toasters, toaster ovens,
by coming up through dry drain traps. Periodi- microwaves, ovens, stoves, and refrigerators)
cally run the water in spare bathrooms, utility tubs should be kept clean and free of food particles
 Cockroaches (Blattodea)
C 945

and grease. Additionally, the areas underneath cockroaches are foraging but the pet is indoors or
and behind these appliances should be kept asleep. Aquariums should have tight fitting lids or
grease and crumb free. screens to prevent cockroach entry.
If pets are present, dry food should be kept in Be careful not to over-water indoor plants, because
resealable containers. Do not leave food and water excess water is available to cockroaches.
out all the time. Feed your pet at particular times Glasses, cups and soda cans containing water or liq-
and clean up after every meal. uid residue are common sources of moisture for
All foods products should be resealed after open- cockroaches. Be sure not to leave these containers in
ing, stored in plastic snap-lid containers, or kept in bedrooms, sinks, on counter tops or other areas. Rinse
the refrigerator. and invert cups and glasses to dry immediately after
Regular sweeping/vacuuming of floors and furni- use, and dispose of soda cans in trash containers.
ture helps to eliminate cockroach food sources. Steps should be taken to eliminate places where
Regular cleaning of food storage areas and shelves water collects outdoors (tires, cans, tree holes, etc.).
not only eliminates spilled or scattered food, but This will not only eliminate cockroach moisture
disrupts cockroach populations that may be using sources but also mosquito breeding habitat.
the area as a harborage.
The third critical element for cockroach sur-
The single most important factor in determin- vival is harborage. By nature, cockroaches avoid
ing cockroach survival is availability of water. Ger- open, well-lighted areas with frequent air move-
man cockroaches live <2 weeks without a supply of ment. They prefer dark, warm cracks and crevices.
free water, even if food is abundant. During periods Excess clutter provides numerous locations suitable
of drought, the incidence of peridomestic cock- for cockroach habitation. The elimination of these
roaches indoors will often increase as these large harborages (clutter) is important in controlling
cockroaches invade structures in search of moisture. infestations. Practices that reduce harborage
Therefore, it is important to eliminate all sources of include:
moisture that contribute to cockroach survival.
Important steps in water management include: Adult cockroaches can fit into cracks only 1.6 mm
wide (about 1/16 of an inch). Any small gap or
Tightening loose pipes, patch plumbing leaks and hole that leads to a void is a prime cockroach har-
replace used washers in the kitchen sink and bath- boring area. Cracks and crevices of this kind
room areas. Outdoor water spigots and sprinklers should be sealed with a tube of caulking.
should also be checked for drips and leaks. Removing clutter (boxes, bags, clothing, toys, food,
Water left in the sink or bathtub after dish washing books, papers, etc.) eliminates cockroach harbor-
or bathing also provides moisture for cockroaches. ages and breeding areas. It is essential to keep all
These sources are eliminated by drying out sinks areas of the home, especially the kitchen and bath-
and bathtubs after use. room, uncluttered and free of useless debris.
A common source of moisture is condensation Outside, remove debris and trash from around the
under the refrigerator. This area should be fre- house.
quently wiped dry or, if possible, a pan should be Stack firewood far away from the house, as this is a
placed under the appliance to collect water. The prime harborage area for peridomestic cockroaches.
collection pan should be emptied frequently. Con- Filling in tree holes with cement also eliminates
densation on pipes (under the sink or in wall voids) peridomestic cockroach harborage.
is also a problem. Insulate these pipes, if possible. Keep shrubbery and ornamentals well trimmed.
Pet drinking dishes and aquariums are also sources In particular, keep palm trees free of loose and
of moisture. Empty pet water dishes at night when dead palm branches and remove all palm debris.
946
C Cockroaches (Blattodea)

Toxicants areas where bait station placement is difficult. The

homeowner will often want the large bait stations
Usually it is desirable to eliminate the need for placed inside the structure in order to kill perido-
toxicants, but this is not always possible. Reduced mestic cockroaches that are caught foraging inside.
chemical control methods currently are available This, however, does nothing about the population of
for indoor and outdoor cockroach control. The cockroaches that continues to breed outdoors.
traditional approach of cockroach control based Outdoor baiting products are used primarily
on application of liquid insecticides to floor, wall, for the control of peridomestic cockroaches. Spread-
and fixture surfaces has been supplanted by more able granular baits or bait stations are the most
selective application techniques. The most recent common formulations used for peridomestic cock-
technological advances in reduced toxic and non- roach control. Spreadable baits are usually applied
toxic cockroach control have been in bait formula- as a perimeter band around a structure, and can
tions, and in insect growth regulators. Other effectively suppress populations and reduce inva-
currently used non-toxic measures include desic- sion rates of households. However, it is difficult to
cating dusts, traps and biological controls. Each of determine the residual longevity of these products,
these treatment methods can contribute to an particularly in areas where precipitation is frequent.
effective cockroach management program. On the Even weatherized baits have difficulty retaining
other hand, although ultrasonic devices are fre- their residual properties where there is heavy rain-
quently advertised as a non-toxic method of cock- fall or irrigation. This is particularly true in the
roach control, extensive research has shown that southeastern United States where precipitation can
these devices neither kill nor repel cockroaches. ruin bait effectiveness in a single day.

Cockroach Baits Insect Growth Regulators

Cockroach baits consist of a toxicant mixed with a Insect growth regulators (IGRs) are a group of
food source. Some baits also contain attractants or compounds that disrupt the normal growth and
feeding stimulants designed to make the bait more development of insects. The IGRs are considered to
attractive to cockroaches than other food sources be reduced-risk tools. They generally have very low
that may be available in the immediate area. Cur- toxicity to mammals because they act by disrupt-
rent indoor bait formulations are applied as dusts, ing the hormonal processes that are specific to
pastes, gels or bait stations. The bait station is one insects. IGRs that mimic the juvenile hormones of
of the more popular application methods for cock- insects are called juvenile hormone analogues
roach baits. This is because the stations are easy to (JHAs). JHAs are chemical compounds with struc-
put out, safe around children and pets and have tural chemistry that is very similar to the hormones
residual activity. Gel and dust bait formulations that the immature cockroach produces naturally.
are formulated for injection into cracks and crev- JHAs interfere with the proper development of last
ices, which reduces the potential contact of people instar cockroach nymphs. Instead of the nymphs
with toxicants, and places the toxicants in areas molting into reproductive adults they molt into
frequented by cockroaches. adultoids, which often have twisted wings and are
Bait stations for peridomestic cockroaches are sterile. Because the adultoids are unable to repro-
simply larger versions of those used for German duce, over the course of time the cockroach popu-
cockroach baiting. The problem with this baiting sys- lation will decline. JHAs are an effective method of
tem is that peridomestic species live and breed out- long term German cockroach control. However,
doors in palm trees, woodpiles, tree holes and other because JHAs eliminate reproduction but do not
 Cockroaches (Blattodea)
C 947

kill existing cockroaches, they are very slow acting cabinets, under and behind the refrigerator, and in
(from 4 to 9 months to achieve control). JHAs are the bathroom. Outdoors, sticky traps are not rec-
often combined with residual insecticides. In this ommended because they tend to capture many
manner most of the population can be eliminated non-target animals (snakes, lizards etc.), and are
quickly by the insecticide, and cockroaches that not resistant to weathering.
survive the insecticide treatment are then sterilized A second trapping method is the use of baited
by the JHA. Insect growth regulators are available jars. Any empty jar (pickle, mayonnaise, peanut
in spray formulations or point source dispensers, butter, etc.) with a rounded inside lip will suffice.
where the IGR is released on a filter paper con- Coat the inner lip of the jar with a thin film of
tained in a permeable plastic station then transmi- Vaseline (to keep trapped cockroaches from escap-
grates throughout the infested area. ing). The jar should then be baited with a quarter
Chitin synthesis inhibitors (CSIs) are another slice of bread soaked in beer (a cockroach favorite).
type of insect growth regulator that is being devel- If beer and bread are unavailable try other foods
oped for use in management programs targeting a like cookies, dog food, apples, etc. The outside of
variety of insect pests. Exposure to CSIs results in the jar should be wrapped in paper towel so cock-
the abnormal molting of nymphs, causing them to roaches have a surface to grasp as they climb up the
die during the molting process. CSIs also cause sides of the jar. To kill trapped cockroaches simply
adult cockroaches to form abnormal egg cases and pour dishwashing detergent into the jar and add
interferes with the hatching process. hot water. The cockroaches can then be dumped
outside or in the garbage. Wash out the jar and
repeat the process every 23 days. Indoor jar traps
Inorganic Dusts should be placed in the same locations as those
listed for sticky traps. When trapping outdoors, jars
Inorganic dusts such as silica gel and boric acid should be placed in trees, tree holes, mulched areas,
have been used frequently for indoor cockroach firewood, near trash cans, compost piles, air condi-
control. The dusts are applied with a squeeze-bulb tioning units and storage sheds. Covering the jars
duster into cracks and crevices under sinks, stoves, with a dome-shaped piece of aluminum foil taped
behind refrigerators, along baseboards, in electri- to the sides will prevent rain from filling the traps.
cal outlets, cabinets and wall voids. Silica gel is Jar traps are very suitable for outdoor use because
simply a finely ground sand-like product that they present little threat to non-target organisms,
adheres to, and absorbs, the protective waxes on and are not easily damaged by weather.
the cockroach cuticle, resulting in cockroach death
from dehydration. Boric acid is a stomach poison
that is picked up by cockroaches walking across Biological Control
dusted areas. The boric acid adheres to the cock-
roach cuticle so when the cockroach grooms itself Natural controls do play an important role in
it ingests the boric acid and soon dies. managing cockroach populations. Natural cock-
roach enemies include wasps, nematodes, spiders,
toads and frogs, centipedes, birds, lizards, geckos,
Traps beetles, mantids, ants and small mammals (mice).
It is very important that these populations of natu-
One of the non-chemical tactics available for ral enemies be maintained to help keep cockroach
reducing a cockroach infestation involves the use populations in check. Often, the importance of
of traps. Sticky traps can be purchased and placed natural enemies in keeping the cockroach prob-
indoors, near the garbage, under the sink, in the lem in check is overlooked.
948
C Cockroaches and Disease

Oothecal Parasitoids Diatomaceous Earth

Baits for Insect Control
Parasitic wasps are an important natural enemy Insecticides
of cockroaches. The wasps are parasitoids of the Insecticide Resistance
cockroach egg case (ootheca) and can have a sig- Urban Entomology
nificant negative impact on outdoor cockroach
populations. Most species of parasitoid wasps are
associated with peridomestic cockroaches. The References
majority of these wasps are minute (15 mm)
and do not sting humans. Peridomestic cock- Arnett RH Jr (2000) American insects, 2nd edn. CRC Press,
roaches like the American and smoky-brown live Boca Raton, FL, 1003 pp
Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches: ecology,
in outdoor harborages such as palm trees, tree
behavior, and natural history. The Johns Hopkins Uni-
holes, and woodpiles. The parasitoids live with versity Press, Baltimore, MD, 230 pp
the cockroaches in the harborage parasitizing Cornwell PB (1968) The cockroach, vol 1. Hutchinson &
their egg cases. When the adult male and female Company, London, UK, 391 pp
Fisk FW (1987) Order Blattodea. In: Stehr FW (ed) Immature
wasps emerge they mate immediately. The female insects, vol 1. Kendall/Hunt Publishing, Dubuque, IA,
then begins to sting other oothecae, laying her pp 120131
eggs inside them. The wasp offspring eat the Miller DM, Koehler PG (1999) Least toxic methods of cock-
cockroach embryos inside the ootheca before roach control. Florida Cooperative Extension Service
Publication ENY-258
hatching. This natural system results in 6070% Roth LM, Willis ER (1960) The biotic associations of cock-
of all cockroach egg cases being parasitized with- roaches. Smithsonian Miscellaneous Collections, vol
out any human interference. 141, pp 1470
Oothecal wasp parasitoids have been tested
for potential indoor use. Domestic populations of
brown-banded cockroaches were successfully Cockroaches and Disease
controlled in a California animal rearing facility
by these wasps. However, it is doubtful that parasi- Gary W. Bennett
toid wasps will ever be reared for commercial use. Purdue University, West Lafayette, IN, USA
Very few individuals would welcome a population
of 200,000 wasps in their home even if they prom- The importance of domestic cockroaches (those
ised to eliminate a severe cockroach infestation. invading our buildings) as public health pests,
Wasp parasitoids are extremely susceptible to especially as vectors of disease, is somewhat uncer-
pyrethroid insecticides. When attempting to elim- tain. Although many pathogenic organisms have
inate an outdoor cockroach infestation, it is impor- been isolated from cockroaches, there is only cir-
tant to realize the insecticide applications in cumstantial evidence to link diseases in human
peridomestic cockroach harborages may not kill beings to the causal agents of those disorders
all of the cockroaches but it certainly will elimi- known to be present on and in cockroaches closely
nate the parasitoids. This can result in future cock- associated with humans (Table16).
roach problems because surviving cockroaches Cockroaches rank with termites as the most
can reproduce unchecked once the parasitoids are important insects found in association with
eliminated. The application of bait around an humans. Cockroaches can be found in most any
infested area is the best way to treat a population place humans inhabit, especially where food is
of peridomestic cockroaches and preserve the stored, processed, prepared, or served. They seek
wasp parasitoids. not only our food, but also putrefied and decaying
Boric Acid matter, virulent discharges, and feces. Cockroaches
 Cockroaches and Disease
C 949

Cockroaches and Disease, Table 16 Pathogens associated with cockroachesa

Pathogen type Pathogen Potentially associated Cockroach species
disease
Bacteria Alcaligenes faecalis wound infection, American, Oriental
gastroenteritis
Bacillus spp. food poisoning, American, Oriental
conjunctivitis
Campylobacter jejuni enteritis American, Oriental
Clostridium spp. gas gangrene, food Oriental
poisoning
Escherichia coli diarrhea, wound infection American, Oriental, German
Klebsiella pneumoniae pneumonia, urinary Unspecified cockroaches
infections
Mycobacterium leprae leprosy German, American,
Australian
Nocardia spp. actinomycetoma American
Proteus spp. wound infection American, Oriental
Pseudomonas aeruginosa respiratory infections, American, Oriental, German
gastroenteritis
Salmonella spp. food poisoning, American
gastroenteritis
Salmonella typhi typhoid Oriental
Streptococcus pneumonia Oriental
pyrogenes
Serratia marcescens food poisoning American, Oriental, German
Shigella dysenteriae dysentery German
Staphylococcus aureus wound, skin and internal German
infections Oriental
Streptococcus faecalis pneumonia American, Oriental, German
Yersinia pestis plague Oriental
Fungi Aspergillus spp. respiratory infections American, Oriental
Helminths Ancylostoma duodenale hookworm American
Ascaris lumbricoides giant human roundworm American
Ascaris spp. roundworm Oriental
Enterobius vermicularis pinworm Oriental, German
Hymenolopsis spp. tapeworm American
Necator americanus hookworm American
Trichuris trichuria whipworm American, Oriental, German
Molds Aspergillus niger otomycosis Oriental
950
C Cockroaches and Disease

Cockroaches and Disease, Table 16 Pathogens associated with cockroachesa (Continued)

Pathogen type Pathogen Potentially associated Cockroach species

disease
Protozoans Entamoeba hystolytica amebiasis Oriental, Australian, German,
American
Giardia spp. giardiasis Unspecified cockroaches
Viruses Poliomyelitis paralytic polio German, American,
brown-banded

a
Extracted from Roth LM, Willis ER (1960) The biotic associations of cockroaches. Smithsonian Institute, Washington, DC,
439 pp

readily move from garbage disposal areas, to sew- filth organisms are found both on their bodies and
ers, to toilets, to food ready for consumption. This within their digestive tracts.
movement creates the opportunity for the con-
tamination of food and food preparation surfaces
with disease-causing organisms. Public Health Importance of
Cockroaches

Important Species Numerous published papers recount the incidence

of cockroaches, their association with disease and
Cockroaches are tropical or subtropical in origin. filth organisms, their production of odorous secre-
Species that have adapted to living indoors origi- tions that can contaminate and affect the flavor of
nated in tropical Africa. Cockroaches probably foods, the socially unacceptable nature of cock-
became domesticated in prehistoric times when roaches in homes, and in some cases, the fear and
humans were cave dwellers. As humans evolved anxiety some individuals have of cockroaches.
to more sophisticated structures, the cockroach These problems are justification for the large sums
also moved, readily adapting to new surround- of money spent each year to control these pests.
ings. Homes, restaurants, hospitals any place
that has warmth, food and water available form
ideal environments for the proliferation of these Domestic Nuisance
pests.
Only a small number of species have moved Cockroaches are among the most common insects
from the fields and forests to take up residence in found associated with humans. They breed in our
our structures. And of these domestic species, the buildings and share our food, water, warmth and
German, Oriental, and American cockroaches are shelter. They consume the same food that we eat, as
the most important species because of their wide well as dead plant or animal materials, leather, glue,
distribution and common occurrence in build- hair, wallpaper, fabrics, book bindings, and feces.
ings. The German cockroach is most often found They contaminate food by crawling around and
in close association with kitchens and other food defecating on it, or by leaving cast skins, empty egg
areas. American and Oriental cockroaches may cases, or dead bodies in foodstuff. They regurgitate
also be found in food areas, but more often are saliva and intestinal fluids from their mouths while
found in basements, sewers, crawl spaces, and out- feeding and deposit fecal droppings as they crawl
door areas. Each of these species is routinely found around on food. The nasty habits of this pestcause
in areas of filth and decaying organic matter. Thus, fear and social embarrassment for homeowners.
 Cockroaches and Disease
C 951

Cockroach Bites German cockroach. The insects were observed run-

ning over the bed clothing and over the children at
Cockroaches have been reported to bite humans, night. Among the cockroaches caught, one was found
although such instances are rare and not serious. to be carrying numerous bacteria identified as Sal-
They have been noted to gnaw on the skin and monella. When the cockroach infestation was elimi-
nails of sailors aboard heavily infested ships. Cock- nated, the food poisoning epidemic stopped
roaches are most likely to nibble on the eyelashes, immediately. Thus, the circumstances were very sus-
fingernails, and toenails of sleeping children and picious, but there was no conclusive evidence that the
the infirm, and in cases of heavy infestations they cockroaches were involved in the disease outbreak.
can cause small wounds on softer skin. It is important to note that over 30 species
of bacteria, most of them potentially pathogenic,
have been found on cockroaches collected from
Accidental Invasion of the Body public buildings, along with numerous viruses,
protozoans, mold fungi, intestinal helminths
Numerous accounts of cockroaches entering the (pinworms, tapeworms, etc.), and secretions
ear, nose, or other body orifices have been recorded. which may have mutagenic and carcinogenic
These invasions usually occur at night when the effects. So there certainly is not a lack of patho-
human host is sleeping and when cockroaches gens found on and in cockroaches.
are most active. There have also been instances of
intestinal invasion by cockroaches, usually in
young children in severely infested living condi- Allergies
tions. As cockroaches forage for food in heavily
infested areas, it certainly is possible for them to Some people are allergic to cockroaches. Cockroach
enter orifices of the body, especially when the per- secretions, body parts, and excrement contain a
son is sleeping and quite still. number of allergens to which many people exhibit
allergic responses, such as skin rashes, watery eyes,
and sneezing. For some very allergic individuals,
Disease Carriers and particularly for those who also have a lung dis-
ease such as asthma, allergic reactions to cockroach
Published papers recount the incidence of cock- allergens can be very serious and even life threaten-
roaches and their association with disease organisms. ing. Cockroach asthma is caused by the inhalation
They document the evidence that cockroaches carry of any one of a number of protein fractions found
pathogens in and on their bodies and in their excreta, in cockroaches that can cause allergies.
but are unable to establish any cause and effect rela- High- and low-molecular-weight proteins that
tionship with disease in humans. So to date, cock- have been isolated from cockroach extracts have
roaches can only be viewed with suspicion. been used to illicit bronchospastic allergy responses
Incriminating evidence is difficult to find link- in humans, with allergies to cockroaches being the
ing cockroaches as vectors of disease outbreaks. second most common allergy in asthmatics (with
There are many anecdotal stories, such as the one even more important sensitivity occurring in asth-
about an epidemic of food poisoning caused by Sal- matic children in severely infested homes). Derma-
monella among children in the nursery of a hospital titis and conjunctival edema also occur in asthmatic
in Brussels. The infection persisted for 2 months, and skin-sensitive populations.
despite isolation of the patients. Cockroaches were Exposure to cockroaches increases the inci-
considered as carriers only after a night nurse drew dence of reaction to cockroach allergens. Sensitivity
attention to an infestation of Blattella germanica, the is quite high among asthmatic children in severely
952
C Cocoon

infested homes. Any conditions favorable to an Cocos nucifera L., feeding in extremely dense
increase in cockroach populations, as well as the lack aggregations that cause scarring and distortion of
of fresh airflow to remove airborne allergens, will the fruits. This mite is the only eriophyid mite that
lead to greater allergy problems. Thus, it is important is a serious pest of coconut palm, and it is consid-
to create living environments free of cockroaches, as ered one of the worst arthropod pests of this palm,
well as those that have a good supply of fresh air. whether grown as a crop tree or as an ornamental.
It is distributed in many tropical countries.
Focus on Sanitation
Distribution
Cockroach infestations do have the potential for seri-
ous health consequences. Acceptable hygiene stan-
The coconut mite was described in 1965 from
dards (including cockroach elimination) must be
specimens collected in Guerrero, Mexico. The
implemented to avoid the social unacceptability of
same year it was found near Rio de Janeiro, Bra-
cockroaches, the potential contamination of food-
zil. Within the next several years it was found in
stuffs, and the health problems that they can cause.
many countries of Tropical America and also in
Cockroaches
West Africa. The native home of the species,
which is especially of interest in searching for
References biological control agents, has been enigmatic.
However, it was recently reported that DNA
Alcamo IE, Frishman AM (1980) The microbial flora of field- sequence data from disparate populations of
collected cockroaches and other arthropods. J Environ coconut mite in the tropics of the Eastern and
Health 42:263266 Western Hemispheres revealed that populations
*Cornwell PB (1968) Diseases. In: The cockroach, vol 1.
from the Americas were the most diverse, while
Hutchinson, London, UK
Ebeling W (1975) Pests on or near food. In: Urban entomol- those from Africa and Southern Asia were virtu-
ogy. University of California, Los Angeles, CA ally uniform. This suggests that the mite evolved
Kang B, Chang JC (1985) Allergenic impact of inhaled arthro- and diversified in the Americas, and spread in the
pod material. Clin Rev Allergy 3:363375
Roth LM, Willis ER (1957) The medical and veterinary impor-
tropics of the Eastern Hemisphere from a single
tance of cockroaches. Smithsonian miscellaneous col- introduction (presumably in West Africa). The
lection, vol 134, pp 1147 coconut mite has not been found in the South
Pacific Region, the original home of the coconut.
Although the coconut mite is apparently
Cocoon
native to the Americas, coconut palms are native
A sheath, usually of silk, formed by an insect larva to the South Pacific. Earlier introductions were
as a chamber for pupation. brought first to the Caribbean Region and then
elsewhere in the American Tropics from West
Africa by Europeans in the 1500s. During this
Coconut Mite, Aceria guerreronis same period, a small population of coconut palms
(Acari: Eriophyidae) was found on the Pacific coast of Panama, but
these are thought to have been introduced natu-
Forrest W. Howard rally or by seafarers from the South Pacific shortly
University of Florida, Ft. Lauderdale, FL, USA before the arrival of the Spanish. As a worldwide
agricultural industry developed around the
The coconut mite, Aceria guerreronis Keifer (Acari: coconut in the 1800s, additional coconut varieties
Eriophyidae), attacks fruits of the coconut palm, were introduced to many localities.
 Coconut Mite, Aceria guerreronis (Acari: Eriophyidae)
C 953

It is not known how long this mite has been Biology and Ecology
associated with coconut, but based on anecdotal
evidence provided by farmers and other observers The mites infest the abaxial (lower) surfaces of the
in various localities of the Americas, local people tepals and that part of the fruit surface that is cov-
had been familiar with the damage typical of this ered by the perianth. They are able to penetrate
mite long before it was discovered and described between the perianth and fruit surface a month
taxonomically. The greatest diversity of cocosoid after the fruit begins development. Prior to this,
palms, i.e., genera related to the monotypic Cocos, the tepals are too tightly appressed to allow entry
is found in South America. It has thus been sug- of the mites.
gested that the original host of the coconut mite The coconut mite has inefficient host-finding
may have been a Cocos relative native to the capabilities that are compensated for by a high
Americas. reproductive rate and rapid development. Presum-
The most dramatic extension of the range of ably, a population on a fruit is initiated by one or
coconut mite in recent years occurred in the late more fertilized females usually from either infested
1990s, when it was found for the first time on fruits on the same palm, perhaps even the same
coconuts in Tanzania (East Africa), India, and Sri raceme, or from a nearby infested palm. The mites
Lanka. feed by piercing the superficial plant tissue to elicit
juices which they then imbibe. A coconut mite
develops from egg to adult in 10 days; thus, popu-
Description lations can build up rapidly. Often, thousands of
mites in each of several aggregations occupy the
The adult female of coconut mite, which is the same fruit. Massive populations of coconut mites
largest stage, is 205255 m long and 3652 m may be present among the tepals and on the fruit
wide. The mites are white and translucent. Like surface beneath the perianth until about the sixth
eriophyid mites in general, they are elongate and month of the coconuts development, after which
possess two pairs of legs, instead of four pairs as populations decline. They are no longer present on
is typical of mites in general. Massive colonies of mature (12-month old) fruits.
the mites, but not individual mites, can be Coconut mites are probably capable of dis-
detected with difficulty with a 10X hand lens. At persing from one palm to the other on air currents
this magnification, the colonies appear as vague or by phoresy (e.g., riding on insects or birds that
silvery patches. visit palm flowers). Where coconut palm plantings
are dense, the mites may disperse to new hosts by
being blown a short distance, and in some cases
Hosts probably crawl from one palm to another on foli-
age that is in contact, ultimately arriving on a fruit.
In nearly all localities where coconut mite is pres- Thus, their potential to spread to new host palms is
ent, its only reported host is coconut palm. Rare greater where the palms are in close proximity. In
exceptions include a record of this mite on fruit densely planted coconut plantations, up to 100% of
of Lytocaryum weddellianum (H.A. Wendland), the palms are often infested, while the percentage
and on queen palm, Syagrus romanzoffiana infested is typically lower in more widely spaced
Chamisso (Glassman), both of which are coco- plantings of coconut palm. However, isolated coco-
soid palms native to Brazil. Coconut palm vari- nut palms may sometimes be highly infested.
eties differ in their susceptibility to coconut Some researchers indicate that the coconut
mite. Almost all varieties have some level of mite is most damaging to palms under dry condi-
susceptibility. tions, i.e., growing in relatively dry regions or
954
C Coconut Mite, Aceria guerreronis (Acari: Eriophyidae)

during the dry season in tropical areas with pro-

nounced wet and dry seasons. Potential explana-
tions for this relationship include that under dry
conditions the perianth may open slightly so as to
allow mites to enter more easily, that the coconut
may develop more slowly and thus remain longer
in a susceptible stage, or that fungi that help regu-
late the mites may be suppressed. However, other
researchers have reported that coconut mite attack
increases in wet periods, or that there is no clear
association between seasonal rainfall patterns and
coconut mite populations.

Damage and Economic Importance

The feeding site of the coconut mite is on the

surface of the meristematic zone of the coconut
fruit. This is a circular whitish zone covered by
the perianth. The fruit expands from this zone,
so that the young fruits of about 2.53.0 cm in
length and diameter develop to the mature coco-
nut of up to 25 cm long during the period of
about 1 year.
An early-stage infestation of a young coco-
nut by coconut mites (Fig.71) is often detectable
as a small pale area, often triangular but some-
times broader, extending on the fruit surface from
beneath the perianth. With exposure to the air,
the pale area turns brown within a few days. The
location of damaged sites on individual coconuts
is partly determined by the arrangement of
tepals of the perianth. Damage tends to be greater
under tepals that overlap adjacent tepals at both
ends, because mites find more space there than
under tepals whose ends are overlapped. As an
infested coconut develops, the tissue extending
from beneath the perianth continues to incur
damage, thus the damaged area eventually c overs Coconut Mite, Aceria guerreronis (Acari: Eriophyidae),
a large portion of the surface. In older damage, Figure 71 (above) A coconut mite, Aceria
the affected surface is suberized (cork-like), with guerreronis; (center) young coconut fruit with early
deep longitudinal fissures which may be inter- damage (pale triangular area) due to feeding of the
sected by horizontal cracks. If intense mite coconut mite, Aceria guerreronis; (below) coconuts
feeding is concentrated on one side of the with suberized surfaces due to feeding of the
fruitmeristem, the fruit may develop unevenly, coconut mite, Aceria guerreronis.
 Coconut Mite, Aceria guerreronis (Acari: Eriophyidae)
C 955

forming a distorted coconut. Highly severe dam- young. Any kind of mechanical damage can
age stunts the fruits. Some observers report that result in browning of the surface of young coco-
damage to young fruits causes excessive num- nuts, but coconut mite damage consistently
bers of them to drop, but other researchers sug- extends from beneath the perianth, which is not
gest that some fruit shedding is normal and in true of other kinds of mechanical damage.
many cases the additional fruit shedding that Colomerus novahebridensis Keifer is an erio-
may be caused by coconut mites may not signifi- phyid mite present in southeast Asia and the
cantly affect yield of copra and other coconut Pacific that causes damage to coconuts that is
products. similar but much lighter and less frequent than
Copra, a main product of the coconut indus- that of A. guerreronis. In Florida, Puerto Rico, and
try, is the white kernel, or coconut meat after it is presumably elsewhere in the Caribbean Region,
dried. In one study, coconut mite damage was Tarsonemus sp. (Acari: Tarsonemidae), causes
found to cause a loss of up to 30% of the copra. damage similar in appearance to early coconut
Other researchers have reported a less serious mite damage. However, this mite is rare, and
impact on copra production. apparently does not remain long on coconut
In many tropical countries, millions of coco- fruits, as the damage never advances beyond the
nuts are sold fresh in roadside stands and farmers early stage. Stenotarsonemus furcatus DeLeon,
markets for coconut water, i.e., the clear liquid in which has been found in association with damage
the coconut that serves as a beverage and is on coconut fruits in Brazil, may be the same or a
sometimes erroneously called coconut milk. (In similar species.
the coconut industry, the latter term applies to the
paste made by grinding the kernel.) Data is not
available on the possible impact of the coconut Management
mite on the production of coconut water, but the
unappealing appearance of mite-damaged coco- Chemical Control
nuts has been shown to adversely affect sales of
this product. Some acaricides have been shown to kill coconut
Coconut palms are an essential feature in mites. However, most chemicals applied topically
the landscape of tropical resort areas, and are had to be repeated indefinitely to maintain control.
treasured by many residents of the tropics. Systemic acaricides might persist longer in the
Damage by coconut mite does not affect the plant, but such chemicals could result in residues
vigor of the palm and the scarred coconuts are in the fruits, and coconuts are harvested through-
not highly noticeable from a distance, but the out the year. Chemical control is perhaps the least
aesthetic damage is important to homeowners viable option for control of coconut mite.
or managers of areas where coconuts are seen
up close, such as in the landscaping around hotel
swimming pools. Mechanical Control
Coconut mite damage can be spotted at a
distance, but must be confirmed by closer exam- A simple mechanical form of control practiced by
ination. At maturity, the surface tissues of a some plantation managers is to prune all of the
coconut dry and become a tan color. Prior to coconuts in all stages of development. This is said
maturing, coconuts are green, yellow, bronze, to result in a plantation free of coconut mites for
apricot, or a blend of these colors, depending on an extended period. However, this method would
variety. Thus, the dark brown color of coconut cause a disruption in the economic benefits of the
mite damage is most noticeable when the fruit is plantation.
956
C Coconut Mite, Aceria guerreronis (Acari: Eriophyidae)

Cultural Control continue to explore the possibilities of biologi-

cal control of coconut mite.
As mentioned above, results of studies of envi- The fungus Hirsutella thompsonii (Fisher),
ronmental factors influencing coconut mite which is widely distributed and known to attack
populations, including wet or dry conditions various species of mites, has been isolated from
and nutrient levels, have been thus far contro- coconut mites in various countries, as has H. nod-
versial. Future research may provide a basis for ulosa Petch in Cuba. Control of several species of
economically feasible cultural control of the mites with fungus has been attempted, but success
coconut mite. has often depended greatly on environmental
conditions. In general, these efforts have been
most successful under humid conditions favoring
Host Plant Resistance the development of the fungi. However, some
recent advances in myco-acaricide development
Common coconut varieties in the Americas, viz., have been encouraging.
Jamaica Tall, Panama Tall, Malayan Red Dwarf, Because coconut mites are almost micro-
Malayan Yellow Dwarf, and Malayan Green scopic and pass almost all of their life cycle in a
Dwarf, are all highly susceptible to coconut mite. cryptic habitat, it appears possible that in some
Some observers have reported that certain variet- regions the mite may be present at undetected lev-
ies of coconut in some countries appear to be els. If such regions were known (e.g., if surveys in
resistant to coconut mite. A highly resistant the South Pacific Region should reveal the pres-
Cambodian variety was reported on a research ence of the coconut mite at extremely low levels),
station in Africa. It was suggested that the spheri- they would be promising sources of effective
cal shape of the fruit of this variety perhaps natural enemies of the coconut mite.
resulted in a very tight perianth that excluded
coconut mites. In a study in St. Lucia, West Indies,
highly spherical coconuts had less coconut mite
References
damage than elongated coconuts on the same
palm. However, extensive damage of coconut mites
Navia D, de Moraes GJ, Roderick G, Navajas M (2005) The
on some spherical-fruited coconut varieties has invasive coconut mite Aceria guerreronis (Acari: Erio-
been observed. phyidae): origin and invasion sources inferred from
mitochondrial (16S) and nuclear (ITS) sequences. Bull
Entomol Res 95:505516
Fernando LCP, Moraes GJ, Wickramananda IR (2002) Pro-
Biological Control ceedings of the international workshop on coconut mite
(Aceria guerreronis), Sri Lanka, 68 January, 2000. Coco-
Predatory mites found beneath the coconut nut Research Institute, Sri Lanka, 117 pp
Howard FW, Abreu-Rodriquez E, Denmark HA (1990) Geo-
perianth and in some cases observed to prey on graphical and seasonal distribution of the coconut mite,
coconut mites have been reported in various Aceria guerreronis (Acari: Eriophyidae), in Puerto Rico
localities. They include Bdella distincta Baker and Florida, USA. J Agr 74:237251
Howard FW, Moore D, Giblin-Davis R, Abad R (2001)
and Balock (Bdellidae); Amblyseius largoensis
Insects on palms. CABI Publications, Wallingford,
Muma, Neoseiulus mumai Denmark, N. paspal- UK, 400 pp
ivorus DeLeon (Phytoseiidae); Lupotarsonemus Moore D (2000) Non-chemical control of Aceria guerreronis
sp. (Tarsonemidae); and Proctolaelaps bickleyi on coconuts. Biocontrol News Inform 21:83N87N
Moore D, Howard FW (1996) Coconuts. In: Lindquist EE,
Bram. (Ascidae). Under natural conditions, Sabelis MW, Bruin J (eds) Eriophyid mites their biol-
predatory mites have a minor effect at best on ogy, natural enemies, and control. Elsevier, Amsterdam,
populations of the coconut mite, but researchers The Netherlands, pp 561569
 Coelomomyces
C 957

Cocoon Breaker as copepods and ostracods. Alternation between

hosts is obligatory, i.e., zoospores produced in mos-
A structure found on Lepidoptera pupae, usually quitoes will not infect other mosquitoes, and zoo-
on the head, that enables the insect to escape from spores from infected microcrustaceans will not
the cocoon. infect other Microcrustaceae. This development of
different parasitic stages within two unlike hosts is
termed heteroecism and was observed in the phy-
Coding Strand topathogenic rust fungi before it was discovered in
Coelomomyces. Heteroecism may be considered
The strand of the DNA molecule that carries the similar to the terms digenetic or heteroxenous, used
biological information of a gene and which is to describe certain protozoa (Amblyospora) that
transcribed by RNA polymerase into mRNA. require two or more hosts for survival. Coelomomy-
ces has not yet been cultured in vitro through its
entire, two-phase life cycle. The in vivo culture of
Codling Moth, Cydia pomonella several species of Coelomomyces has been success-
(Linnaeus) (Lepidoptera: fully achieved by cycling the fungus through its
Tortricidae) respective host systems, which in some cases can be
maintained in small containers.
This is one of the most important pests of apple The occurrence of Coelomomyces epizootics is
fruit. dependent on the presence of both hosts, the relative
Apple Pests and Their Management sizes of their populations, and the age of host mos-
quito larvae. Studies have shown that infection of
anopheline larvae with C. punctatus correlates with
Codon the seasonal abundance of the alternate copepod
hosts, and that early-instar larvae are more readily
A triplet of nucleotides that code for a single infected than those from later instars. In the field, it
amino acid. has been observed that the larvae become infected
primarily at dusk. This is apparently due to the dual
photoperiodicity of gamete release from the alter-
Coelomomyces nate hosts, which, under laboratory conditions, also
occurs at this time. Environmental factors such as
The phylum Chytridiomycota, once considered a pH and temperature of the water appear to be much
member of the Mastigomycotina, is now included less important in infection rates of mosquito larvae
with the Oomycota in the kingdom Protoctista. and in the progress of epizootics of Coelomomyces
Within the Chytridiomycetes, Coelomomyces than the relationship between the two host systems.
(order=Blastocladiales) is the most notable insect Finally, with respect to host range, some species of
pathogen. This genus contains more than 70 species the fungus may infect several genera of mosquitoes,
and has been found worldwide. Coelomomyces is while others are specific for a single species.
unique among the entomopathogenic fungi in that It is significant that under natural conditions,
it requires two different hosts to complete its life mosquito larvae from later instars can become
cycle. The insect hosts are usually mosquito larvae, infected with Coelomomyces. Older larvae particu-
although other dipterans such as black flies and larly are susceptible just after molting, when the cuti-
midges, as well as some backswimmers (Hemiptera), cle is not yet completely hardened. Infection in older
also can become infected. The alternate hosts are larvae and even in some younger instars exposed to
other aquatic arthropods (microcrustaceans) such a low level of inoculum may not necessarily kill the
958
C Coelomomyces

insect. Heavily infected larvae do not pupate and gametangia are bright orange due to the presence of
starve to death due to the depletion of nutritional carotene, and the female gametangia are light amber.
reserves from the fat body by the fungus. In contrast, Both types can occur within an individual copepod,
larvae with light infections may pupate and develop and gametes, i.e., the haploid zoospores released as
into infected adults. The fungal hyphae migrate from products of gametangial cleavages, therefore can
the hemocoel and penetrate the ovaries. Conversion fuse during swarming within the host. Alternatively,
of the fungal hyphae into resting sporangia is appar- gametes may escape from the microcrustacean
ently stimulated by hormones (e.g., 20-hydroxyecdy- cadaver to mate outside the host. The biflagellate
sone) produced by the mosquitoes after a blood zygotes that result from mating of the gametes are
meal; in healthy mosquitoes, the same hormones the infective propagules of mosquito larvae.
influence egg maturation. It has been observed that Susceptibility of mosquito larvae to infection
adult Aedes aegyptii mosquitoes infected with C. ste- by Coelomomyces varies and appears to depend
gomyiae display normal reproductive behavior with upon the ability of the zygotes to attach to host cuti-
respect to copulation, sperm transfer and storage, cle. Attachment of C. psorophorae zygotes to the
and oviposition. However, no eggs are produced cuticle of a susceptible host occurs preferentially at
because oocytes of infected ovaries do not endocy- intersegmental membranes, on head capsules, at the
tose vitellogenin and, as a result, vitellin yolk granules bases of anal gills, and around the anus. Attachment
cannot form. During oviposition, infected females is closely associated with encystment of the zygotes.
therefore discharge piles of Coelomomyces resting Germination is initiated at one end of the cyst, where
sporangia, which fill the ovaries rather than eggs. an appressorium forms and functions in further
Obviously, this provides an excellent means of dis- attaching the cyst to the host. As germination con-
persal of the pathogen to its alternate host. tinues, a penetration tube grows from the appresso-
Meiosis occurs in the germinating, resting spo- rium and traverses the cuticle to the epidermal
rangia, and the wall-less zoospores generated dur- region, where the infecting fungal protoplasts are
ing this reduction division often are referred to as deposited into host cells. After penetration, the thalli
meiospores. Meiospores are posteriorly uniflagel- appearing as irregularly shaped, protoplast-like thalli
late and are released from sporangia in masses cov- (hyphal bodies) invade other larval tissues, espe-
ered by thin vesicles consisting of the inner regions cially the fat body and the hemocoel. There is no
of mature sporangial walls. Meiospores serve as the apparent host hemocytic response to Coelomomyces
infective propagules of the alternate microcrusta- hyphal bodies, at least in the case of C. punctatus
cean hosts. In the case of C. dodgei, the copepod infecting Anopheles quadrimaculatus. This could be
hosts release substances recognized by the meio- due to masking of the fungal surface by host mate-
spores, increasing the probability of their attach- rial or to production of fungal surface components
ment to the host cuticle. Meiospore attachment can which are interpreted as self by host defense cells. As
be consolidated by secretion of adhesive material a Coelomomyces infection progresses within host
from cytoplasmic vesicles. At the time of attach- mosquito larvae, extensive growth and branching of
ment, the meiospores encyst and invade the host hyphae occurs, and resting sporangia, which will
via a penetration germ tube. In C. psorophorae, eventually cleave into the meiospores infectious to
appressoria may be produced and may function as the alternate host, form to complete the life cycle.
an additional mechanism for attachment of the
fungus to host surfaces; attachment of this species
to host Cyclops vernalis takes place primarily in References
intersegmental regions. Meiospores are of opposite
mating types, and each meiospore develops a thal- Federici B (1981) Mosquito control by the fungus Culicino-
myces, Lagendium, and Coelomomyces. In: Burges HD
lus that will form a male or female gametangium (ed) Microbial control of pests and plant disease. Aca-
within the alternate host. In C. dodgei, the male demic Press, London, UK, pp 555572
 Coffee Berry Borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae)
C 959

Lucarotti CJ (1992) Invasion of Aedes aegypti ovaries by la broca del caf, is the most devastating insect
Coelomomyces stegomyiae. J Invertebr Pathol 60:176184 pest of coffee throughout the world. This minute
Travland LB (1979) Structures of the motile cells of Coelomo-
myces psorophorae and function of the zygote in encyst- insect (0.50.8 mm length and 0.2 mm wide) is
ment on a host. Can J Bot 57:10211035 endemic to Central Africa, and has now spread to
Whisler HC, Zebold SL, Shemanchuk JA (1975) Life history most coffee growing regions throughout the world.
of Coelomomyces psorophorae. Proc Natl Acad Sci
Infestation levels can be quite high (e.g., Uganda
72:693696
80%, Colombia 60%, Jamaica 5885%, Tanzania
90%, Malaysia 5090%, and Mexico 60%). It is
striking that out of more than 850 insects reported
Coelopidae on coffee, the coffee berry borer is the only one that
has adapted to use the seed of Coffea arabica and
A family of flies (order Diptera). They commonly
Coffea canephora (=robusta) as its food source.
are known as seaweed flies.
Damage begins when an adult female
Flies
(Fig. 72) bores a hole into the coffee berry and
deposits her eggs; larvae feed on the coffee seed,
lowering its quality and possibly causing abscis-
Coenagrionidae sion of the berry. An interesting aspect of the
insects biology is the highly skewed sex ratio
A family of damselflies (order Odonata). They com-
favoring females (10:1), which contributes to a
monly are known as narrow-winged damselflies.
high reproductive capacity. Wolbachia, a mater-
Dragonflies and Damselflies
nally inherited bacterium known to induce par-
thenogenetic development and skewed sex ratios
favoring females, has been detected in coffee
Coevolution berry borers from 11 different countries.
When larvae molt into adults, they mate with
Reciprocal, adaptive changes in traits of two their siblings inside the berry; therefore, once
populations. females emerge, they are inseminated and ready
to deposit eggs into another coffee berry. In con-
trast to females, males remain in the berry, and
Coffee Bean Rot are unable to fly. Thus, insect development inside
the coffee berry makes this insect very difficult to
Stink bugs introduce fungi into coffee berries control. The highly toxic chlorinated hydrocar-
while feeding. bon endosulfan has been widely used against the
Transmission of Plant Diseases by Insects coffee berry borer but some countries have
banned its use. Also, the insect has developed
resistance to this product. The lack of safe and
Coffee Berry Borer, Hypothenemus effective chemical control strategies has led to
hampei (Ferrari) (Coleoptera: strong efforts by coffee scientists in many coun-
Curculionidae: Scolytinae) tries to develop biological control methods rely-
ing on parasitoids and fungal entomopathogens.
Fernando E. Vega Four of the most common coffee berry borer
USDA, ARS, Sustainable Perennial Crops Labora- parasitoids originate in Africa: two bethylids (Pro-
tory, Beltsville, MD, USA rops nasuta Waterston and Cephalonomia stephan-
oderis Betrem), one eulophid (Phymastichus coffea
The coffee berry borer, Hypothenemus hampei La Salle), and one braconid (Heterospilus coffeicola
(Ferrari), known throughout Latin America as Schmiedeknecht). Some of these have been introduced
960
C Coffee Berry Borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae)

berry borer is being aggressively studied. The

insect has also been shown to be associated with
40 species of fungi in 22 genera. Two nematodes
have been reported as parasites of the coffee berry
borer: Panagrolaimus sp. in India and Metaparasi-
tylenchus hypothenemi in Mexico.
Cultural practices such as complete collection
of berries on the tree and ground immediately after
harvest could greatly reduce coffee berry borer pop-
ulation levels. However, this laborious strategy is not
considered a feasible or cost-effective alternative.
Coffee Pests and their Management

References

Baker PS (1999) The coffee berry borer in Colombia. Final

report of the DFID Cenicaf CABI Bioscience IPM for
Coffee Project, DFID Cenicaf, Chinchin, Colombia,
154 pp
Brun LO, Marcillaud C, Gaudichon V, Suckling DM (1989)
Endosulfan resistance in Hypothenemus hampei
(Coleoptera: Scolytidae) in New Caledonia. J Econ
Entomol 82:13111316
Bustillo PAE, Crdenas MR, Villalba GA, Benavides MP,
Orozco HJ, Posada FFJ (1998) Manejo integrado de
la broca del caf Hypothenemus hampei (Ferrari) en
Colombia. Centro Nacional de Investigaciones de Caf
(Cenicaf), Chinchin, Colombia, 134 pp
Le Pelley RH (1968) Pests of coffee. Longmans, Green and Co,
London, UK, 590 pp
Coffee Berry Borer, Hypothenemus hampei
Prez J, Infante F, Vega FE, Holgun F, Macas J, Valle J, Nieto G,
(Ferrari) (Coleoptera: Curculionidae: Scolytinae), Peterson SW, Kurtzman CP, ODonnell K (2003) Myco-
Figure 72 Adult coffee berry borer, Hypothenemus biota associated with the coffee berry borer (Hypothene-
hampei. Drawing by Ann Simpkins (USDA). mus hampei) in Mexico. Mycol Res 107:879887
Poinar G Jr, Vega FE, Castillo A, Chavez IE, Infante F (2004)
Metaparasitylenchus hypothenemi n. sp. (Nematoda:
in coffee producing countries (e.g., Colombia, Allantonematidae), a parasite of the coffee berry borer,
Jamaica, Mexico) in an attempt to reduce coffee Hypothenemus hampei (Ferrari) (Curculionidae: Scoly-
tinae). J Parasitol 90:11061110
berry borer damage, but their mass production Posada F, Aime MC, Peterson SW, Rehner SA, Vega FE (2007)
remains expensive due to the need for coffee seeds Inoculation of coffee plants with the fungal entomo-
in which to rear the coffee berry borers used to pathogen Beauveria bassiana (Ascomycota: Hypocre-
ales). Mycol Res 111:749758
rear the parasitoids.
Varaprasad KS, Balasubramanian S, Diwakar BJ, Ramarao CV
The most common fungal entomopathogen (1994) First report of an entomogenous nematode,
isolated from the coffee berry borer is Beauveria Panagrolaimus sp. from coffee berry borer, Hypothene-
bassiana, although Isaria fumosorosea, Paecilomy- mus hampei (Ferrari) from Karnataka, India. Plant
Protect Bull 46:42
ceslilacinus, and Metarhizum anisopliae have also Vega F, Benavides P, Stuart J, ONeill SL (2002)Wolbachiain-
been reported to a lesser extent. The use of B. bassi- fection in the coffee berry borer (Coleoptera: Scolyti-
ana as a fungal endophyte to control the coffee dae). Ann Entomol Soc Am 95:374378
 Coffee Pests and their Management
C 961

Coffee Pests and their predatory organisms, which regulate the popula-
Management tions of many pests, represented 42% of the total
of species collected in a coffee plantation. For this
Juan F. Barrera reason, it is important to protect and maintain
El Colegio de la Frontera Sur, Tapachula, Chiapas, the natural enemies of pests, avoiding the indis-
Mexico criminate use of chemical pesticides and some
agronomic practices that are harmful to natural
The perennial and evergreen nature of the coffee control. The goal of this section is to describe the
plant (Coffea spp.) favors attack by a number of biological and ecological characteristics of the
insects and mites (Table 17, Figs. 73 and 74). All main insects and mites of C. arabica L. and
portions of the plants are susceptible to attack, C. canephora Pierre ex Froehner, the damage
and damage may appear at the seed bed, nursery, caused by these pests, their natural enemies, and
plantation, or in the warehouse. Certain pests pest management in coffee growing countries of
affect the coffee plant only temporarily, while oth- tropical America. The pests to be described are
ers live for several generations on the plant. In listed in Table 17, which also includes the parts of
some instances, the attack may cause the death of the plant that are damaged and the development
the plant, but in most cases the pests only weaken stage of the coffee plant that they damage. The cri-
the plant, reducing yield. When the bean is terion applied to include these organisms in the
attacked, quality also may be affected. category of major pests, was that they were
Insects constitute the most numerous group reported in at least one of the manuals on coffee
of coffee pests; of more than 850 species of insects pests that have been published in Brazil, Colom-
that feed on coffee in the world, approximately bia, Costa Rica, Cuba, El Salvador, Guatemala,
200 (23.5%) have been reported in the tropical Honduras, Jamaica, Mexico or Venezuela.
and sub-tropical areas in America. Out of these,
hardly thirty species, mostly indigenous, cause
losses considered important. The pests and the Coffee Berry Borer, Hypothenemus
seriousness of the problems they cause vary from hampei (Ferrari) (Coleoptera:
one country to another, and from one area to Curculionidae: Scolytinae)
another. The coffee pest that is considered the
most important in tropical America is the coffee Distribution
berry borer, Hypothenemus hampei (Ferrari)
(Coleoptera: Curculionidae: Scolytinae), now cos- This is the most serious insect pest of coffee
mopolitan but originating in Africa. The coffee worldwide. It originated in Africa. In the Americas,
leaf miner, Leucoptera coffeella Gurin-Mneville it is found in coffee plantations from Mexico to
(Lepidoptera: Lyonetiidae), and the root mealy- Brazil, including some countries in the Caribbean
bugs (Pseudococcidae) are causing serious prob- region such as Cuba, Jamaica, the Dominican
lems in several countries. Bugs of the genus Republic and Puerto Rico.
Antestiopsis (Pentatomidae), which are very harm-
ful in Africa, have not yet been reported in the
American hemisphere. Damage and Economic Importance
Most of the insects that are found in coffee
plantations are beneficial because they contrib- Coffee berry borer (Fig. 73) is a direct pest
ute to plant pollination, degrade organic matter, because it causes direct damage to the product to
or feed on phytophagous organisms. A study be harvested, the coffee bean. The attacked green,
conducted in Mexico showed that parasitic and ripe and dry fruits or berries usually show a hole
962
C Coffee Pests and their Management

Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of cof-
fee in tropical America
Taxon (scientific and Country where the insect/ Developmental Plant parts affected
common name) mite is reported as coffee stage feeding in/on
pest the plant
Acari: Tarsonemidae
Polyphagotarsonemus latus Brazil Nymph, adult Leaves
(Banks)
Acari: Tenuipalpidae
Brevipalpus sp. Brazil, Jamaica, Mexico Nymph, adult Leaves
Acari: Tetranychidae
Olygonychus coffeae Guatemala, Mexico Nymph, adult Leaves
(Nietner)
Olygonychus ilicis (McGregor) Brazil, Guatemala Nymph, adult Leaves
Olygonychus punicae (Hirst) El Salvador Nymph, adult Leaves
Olygonychus yothersi Colombia, Costa Rica, Nymph, adult Leaves
(McGregor) Venezuela
Coleoptera: Anthribidae
Araecerus fasciculatus All coffee growing coun- Larva, adult Bean
(DeGeer) tries in America
Coleoptera: Cerambycidae
Plagiohammus maculosus Costa Rica, El Salvador, Larva Stem, root
(Bates) Guatemala, Honduras,
Mexico
Plagiohammus mexicanus Mexico Larva Stem, root
Breuning
Plagiohammus spinipennis Mexico Larva Stem, root
(Thomson)
Coleoptera: Curculionidae
Brachyomus quadrinodosus Venezuela Adult Leaves
(Lacordaire)
Cleistolophus similis Sharp Costa Rica Adult Leaves
Compsus sp. Colombia Adult Leaves
Epicaerus capetillensis Sharp Guatemala, Honduras, Adult Leaves
Mexico
Hypothenemus hampei Mexico to Brazil, including Larva, adult Fruit, bean
(Ferrari) Cuba, Jamaica, Dominican
Republic, and Puerto Rico
Lachnopus buchanani Cuba Adult Leaves
Marshall
Macrostylus boconoensis Colombia, Venezuela Adult Leaves
Bordn
Pantomorus femoratus Sharp Costa Rica Adult Leaves
 Coffee Pests and their Management
C 963

Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of
coffee in tropical America (Continued)
Taxon (scientific and Country where the insect/ Developmental Plant parts affected
common name) mite is reported as coffee stage feeding in/on
pest the plant
Pantomorus godmani Brazil Adult Leaves
Crotch
Steirarrhinus sp. Costa Rica Adult Leaves
Xylosandrus morigerus Mexico to Brazil Larva, adult Young stems,
(Blandford) branches
Coleoptera: Scarabaeidae
Anomala sp. El Salvador Larva Root
Dyscinetus picipes Burmeister Cuba Larva Root
Phyllophaga spp. Widely distributed in coffee Larva Root
plantations in America
Phyllophaga latipes (Bates) El Salvador Larva Root
Phyllophaga menetriesi El Salvador Larva Root
(Blanchard)
Phyllophaga obsoleta El Salvador Larva Root
(Blanchard)
Phyllophaga sanjosecola Costa Rica Larva Root
Saylor
Phyllophaga vicina Moser Costa Rica Larva Root
Hemiptera: Aphididae
Toxoptera auranti (Boyer de Tropical and sub-tropical Nymph, adult Leaves, buds and
Fonscolombe) areas of the Old World. other tender parts of
Widely distributed in coffee the plant
plantations in America
Hemiptera: Coccidae
Coccus spp. Mexico Nymph, adult female Aerial part of the
plant
Coccus hesperidum L. Guatemala, Mexico Nymph, adult female Aerial part of the
plant
Coccus viridis (Green) Brazil, Colombia, Costa Nymph, adult female Aerial part of the
Rica, Cuba, Ecuador, El plant
Salvador, Guatemala,
Honduras, Jamaica, Mexico,
Puerto Rico, Surinam,
Venezuela
Parasaissetia sp. Colombia Nymph, adult female Aerial part of the
plant
Parasaissetia nigra (Nietner) El Salvador, Guatemala, Nymph, adult female Aerial part of the
Puerto Rico, West Indies plant
Saisettia spp. El Salvador, Mexico Nymph, adult female Aerial part of the
plant
964
C Coffee Pests and their Management

Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of
coffee in tropical America (Continued)
Taxon (scientific and Country where the insect/ Developmental Plant parts affected
common name) mite is reported as coffee stage feeding in/on
pest the plant
Saisettia coffeae (Walker) Brazil, Costa Rica, Cuba, El Nymph, adult female Aerial part of the
Salvador, Guatemala, plant
Honduras, Mexico, Dominican
Republic, Venezuela
Saisettia olae (Oliver) Brazil, Cuba, Guatemala, Nymph, adult female Aerial part of the
Mexico plant
Toumeyella sp. Venezuela Nymph, adult female Root
Toumeyella liriodendri Guatemala Nymph, adult female Root
(Gmelin)
Hemiptera: Cerococcidae
Cerococcus catenarius Brazil Nymph, adult female Aerial part of the
Fonseca plant
Hemiptera: Diaspididae
Chrysomphalus sp. Guatemala Nymph, adult female Aerial part of the
plant
Chrysomphalus dictyospermi Guatemala Nymph, adult female Aerial part of the
(Morgan) plant
Ischnaspis longirostris Colombia, Cuba, Nymph, adult female Aerial part of the
(Signoret) Guatemala plant
Lepidoshaphes beckii Venezuela Nymph, adult female Aerial part of the
(Newman) plant
Selenaspidus articulatus Colombia, Ecuador, Mexico Nymph, adult female Aerial part of the
(Morgan) plant
Hemiptera: Margarodidae
Icerya purchasi Maskell Venezuela Nymph, adult female Aerial part of the
plant
Hemiptera: Ortheziidae
Insignorthezia insignis Browne Brazil, Colombia Nymph, adult female Aerial part of the
plant
Praelongorthezia praelonga Brazil Nymph, adult female Aerial part of the
(Douglas) plant
Hemiptera: Pseudococcidae
Brevicoccus sp. Guatemala Nymph, adult female Root
Ceroputo sp. Costa Rica Nymph, adult female Root
Dysmicoccus sp. Colombia, Ecuador Nymph, adult female Root
Dysmicoccus bispinosus Brazil, Guatemala, Hondu- Nymph, adult female Root
(Beardsley) ras, Mexico
Dysmicoccus brevipes Costa Rica, El Salvador, Nymph, adult female Root
(Cockerell) Guatemala, Honduras,
Mexico
 Coffee Pests and their Management
C 965

Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of
coffee in tropical America (Continued)
Taxon (scientific and Country where the insect/ Developmental Plant parts affected
common name) mite is reported as coffee stage feeding in/on
pest the plant
Ferrisia virgata (Cockerell) Brazil, Mexico, West Indies Nymph, adult female Aerial part of the
plant
Geococcus sp. Mexico, Venezuela Nymph, adult female Root
Geococcus coffeae Green El Salvador, Guatemala, Nymph, adult female Root
Honduras, Surinam
Geococcus radicum Green El Salvador Nymph, adult female Root
Neochavesia caldasiae Colombia Nymph, adult female Root
(Balachowsky)
Rhizoecus sp. Mexico, Venezuela Nymph, adult female Root
Rhizoecus andensis Hambleton Colombia Nymph, adult female Root
Rhizoecus coffeae Laing Costa Rica Nymph, adult female Root
Paraputo sp. Guatemala Nymph, adult female Root
Planococcus citri (Risso) Brazil, Colombia, Costa Nymph, adult female Root, aerial part of
Rica, Cuba, El Salvador, the plant
Guatemala, Honduras,
Jamaica, Mexico, Puerto
Rico
Planococcus halli Ezzat & Guatemala Nymph, adult female Root
McLonnell
Pseudococcus elisae Guatemala Nymph, adult female Root
(Borchsenius)
Pseudococcus longispinus Guatemala Nymph, adult female Root
(Targioni-Tozzeti)
Pseudococcus jongispinus Mexico Nymph, adult female Aerial part of the
Targioni-Tozzetti plant
Puto sp. Costa Rica Nymph, adult female Root
Puto antioquensis (Murillo) Guatemala Nymph, adult female Root
Rhizoeccus campestris Guatemala Nymph, adult female Root
(Hambleton)
Rhizoeccus caticans Guatemala Nymph, adult female Root
(Hambleton)
Rhizoeccus kondonis Kuwana Guatemala Nymph, adult female Root
Rhizoeccus nemoralis El Salvador, Honduras Nymph, adult female Root
Hambleton
Hymenoptera: Formicidae
Acromyrmex spp. Venezuela Adult Leaves
Acromyrmex coronatus (F.) Brazil Adult Leaves
Acromyrmex octospinosus Trinidad Adult Leaves
(Wheeler)
966
C Coffee Pests and their Management

Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of
coffee in tropical America (Continued)
Taxon (scientific and Country where the insect/ Developmental Plant parts affected
common name) mite is reported as coffee stage feeding in/on
pest the plant
Atta spp. Guatemala, Ecuador, Adult Leaves
Nicaragua, Venezuela
Atta cephalotes (L.) Colombia, Costa Rica, Adult Leaves
Mexico, Surinam, Trinidad
Atta fervens Say Mexico Adult Leaves
Atta insularis Gurin- Cuba Adult Leaves
Mneville
Atta laevigata Smith Brazil Adult Leaves
Atta mexicana (Smith) Guatemala, Mexico Adult Leaves
Atta sexdens (L.) Brazil Adult Leaves
Atta sexdens rubropilosa Brazil Adult Leaves
Forel
Lepidoptera: Apateloididae
Olceclostera moresca Colombia Larva Leaves
(Schaus.)
Lepidoptera Arctiidae
Estigmene acrea (Drury) Colombia Larva Leaves
Lepidoptera: Dalceridae
Dalcera abrasa Brazil Larva Leaves
Herrich-Schaeffer
Zadalcera fumata Schaus Brazil Larva Leaves
Lepidoptera: Elachistidae
Stenoma cecropia Meyrick Colombia Larva Leaves
Lepidoptera: Geometridae
Glena sp. Brazil Larva Leaves
Oxydia spp. Colombia Larva Leaves
Oxydia saturniata Guene Brazil Larva Leaves
Lepidoptera: Limacodidae
Phobetron hipparchia Brazil, Colombia Larva Leaves
(Cramer)
Sibine spp. Colombia Larva Leaves
Lepidoptera: Lyonetiidae
Leucoptera coffeella (Gurin- Widespread wherever Larva Leaves
Mneville) coffee is grown in the
Neotropical area
Lepidoptera: Megalopygidae
Megalopyge lanata (Stoll) Brazil, Colombia Larva Leaves
Podalia sp. Brazil Larva Leaves
 Coffee Pests and their Management
C 967

Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of
coffee in tropical America (Continued)
Taxon (scientific and Country where the insect/ Developmental Plant parts affected
common name) mite is reported as coffee stage feeding in/on
pest the plant
Lepidoptera: Noctuidae
Agrotis spp. Colombia, Costa Rica, Larva Stems of small plants
Ecuador, El Salvador in germinating
seedbeds or recently
transplanted plants
Agrotis ipsilon (Hufnagel) Brazil Larva Stems of small plants
in germinating
seedbeds or recently
transplanted plants
Agrotis repleta Walker Venezuela Larva Stems of small plants
in germinating
seedbeds or recently
transplanted plants
Feltia spp. Costa Rica, El Salvador, Larva Stems of small plants
Venezuela in germinating seed-
beds or recently
transplanted plants
Pseudoplusia includens Honduras Larva Leaves
(Walker)
Spodoptera sp. Colombia, Costa Rica, Ecua- Larva Stems of small plants
dor, El Salvador in germinating
seedbeds or recently
transplanted plants
Spodoptera eridania (Stoll) Venezuela Larva Stems of small plants
in germinating seed-
beds or recently
transplanted plants
Spodoptera frugiperda (Smith) Costa Rica, Brazil Larva Stems of small plants
in germinating
seedbeds or recently
transplanted plants;
leaves
Trichoplusia ni (Hbner) Colombia Larva Leaves
Lepidoptera: Psychidae
Oiketicus geyeri (Berg) Brazil Larva Leaves
Oiketicus kirbyi Brazil, Cuba Larva Leaves
Lucas
Lepidoptera: Saturniidae
Automeris sp. Brazil, Colombia Larva Leaves
Automeris complicata Brazil Larva Leaves
Walker
968
C Coffee Pests and their Management

Coffee Pests and their Management, Table 17 The most common phytophagous insects and mites of
coffee in tropical America (Continued)
Taxon (scientific and Country where the insect/ Developmental Plant parts affected
common name) mite is reported as coffee stage feeding in/on
pest the plant
Automeris coresus Boisduval Brazil Larva Leaves
Automeris illustris Walker Brazil Larva Leaves
Eacles imperialis magnifica Brazil Larva Leaves
(Walker)
Eacles masoni Schaus Ecuador Larva Leaves
Lonomia circunstans (Walker) Brazil Larva Leaves
Orthoptera: Gryllidae
Paroecanthus guatemalae Guatemala, Honduras Adult female Stem, branch
Saussure
Paroecanthus niger Saussure El Salvador, Guatemala Adult female Stem, branch
Orthoptera: Tettigoniidae
Gongrocnemis sp. Guatemala Nymph, adult Leaves, buds, fruit
pulp, beans
Idiarthron atrispinum (Stl) Costa Rica, Guatemala Nymph, adult Leaves, buds, fruit
pulp, beans
Idiarthron subquadratum Colombia, Guatemala, El Nymph, adult Leaves, buds, fruit
Saussure & Pictet Salvador, Honduras, pulp, beans
Mexico

on its apical portion. The hole is located at the which produces ochratoxin A, a potent toxin that
center or ring of the berrys ostiole and the emis- sometimes contaminates green coffee beans,
sion of sawdust can be observed through this roasted coffee, and coffee brews, including instant
hole. Its attack reduces the yield and affects the coffee.
bean quality. Characteristic damage includes
the rotting of developing beans as a result of sap-
rophytic microorganisms that enter through the Description
hole, the drop of young berries due to attack, and
the loss of bean weight due to insect feeding. The The egg is elliptical, crystalline and yellowish
borer can cause bean yield losses of 3035% with toward maturity. Its length varies from 0.52 to
100% of perforated berries at harvest time; nev- 0.69 mm. The larva is white-yellowish, without
ertheless, damage can be greater if harvest is legs, with a C-shaped body and a wide thoracic
delayed. All the commercial coffee varieties and region. The head is light brown, with visible and
species are attacked by this insect. However, it forward-extending mandibles. Visible hairs
shows preference for C. canephora, and its multi- spread over the head and body. Females molt
plication is also higher on beans of this coffee twice and males once. The length of the last lar-
species. Recently it was suggested that H. hampei val instar is from 1.88 to 2.30 mm. The pre-pupa
serves as a vector for Aspergillus ochraceus Wilh., is similar to the larva, but its color is milky-white,
 Coffee Pests and their Management
C 969

Coffee Pests and their Management, Figure 73 Some coffee pests: (a) Coffee berry borer,
Hypothenemus hampei (Curculionidae) infesting a coffee berry; (b) Damage of coffee leaf by coffee
leaf miner, Leucoptera coffeella (Lyonetiidae); (c) Root mealybugs (Pseudococcidae); (d) Scale insects
on coffee leaf (Coccidae).

its body is lesscurved, and it does not feed. The 1.84 to 2.00 mm long. The adult is elongated with
pupa is milky-white and yellowish towards a cylindrical body slightly arched towards the
maturity. Many of the adults characteristics can end of the abdomen. It is about 1.501.78 mm
be seen in the pupal stage. The pupa varies from long and its body is bright black, although
970
C Coffee Pests and their Management

Coffee Pests and their Management, Figure 74 Some additional coffee pests: (a) Coffee branch perforat-
ed by Xylosandrus morigerus (Curculionidae); (b) Coffee stem attacked by a stem borer, Plagiohammus
maculosus (Cerambycidae); (c) Aphids on coffee leaf; (d) Adults of a katydid, Idiarthron subquadratum;
(Tettigoiidae) (e) Oviposition by a bush cricket, Paroecanthus (Gryllidae) on the stem of a coffee bush.
 Coffee Pests and their Management
C 971

yellowish when emerging from the pupa. The adults find refuge in the black, dry berries. Adult
head is ventrally located and is protected by females emerge massively from these old berries
the pronotum. The antennae are elbowed and with first rainfall, initiating the infestation by
clubbed at the ends. Mouthparts are the typical attacking berries from the earliest flowerings of
chewing type and the elytra are convex and pos- the new harvest.
sess longitudinal grooves that alternate with lon-
gitudinal series of bristles. Females have
well-developed wings that allow them to fly, Natural Enemies
while the males wings are atrophied. Females
are easily differentiated from males because they Coffee berry borer is attacked by several natural
are larger. enemies. Four parasitoid species from Africa are
the best known: Prorops nasuta Waterston (from
Cameroon, Ivory Coast, Zaire, Kenya, Tanzania,
Biology and Ecology Togo, Uganda) and Cephalonomia stephanoderis
Betrem (Ivory Coast, Togo) (both Hymenoptera:
Adult females initiate the infestation. In general, Bethylidae), and two solitary ectoparasitoids of
a berry is infested by a single female. If the coffee the larva, pre-pupa and pupa, Heterospillus coffei-
bean is watery or milky, the insect tends to aban- cola Schimideknecht (Hymenoptera: Braconidae)
don it and the bean usually rots. But if the bean (Cameroon, Zaire, Kenya, Tanzania, Uganda) (a
consistency is hard enough, the founding female free-living wasp that deposits a single egg near a
constructs a gallery where she lays the eggs. The borers egg cluster in a recently attacked berry)
eggs are oviposited one by one, forming small and Phymastichus coffea LaSalle (Hymenoptera:
groups within the coffee bean. The female lays Eulophidae) (Togo, Kenya) (a gregarious endop-
from 1 to 3 eggs per day during the first 1520 arasitoid of H. hampei adults which parasitizes
days; afterwards, the egg laying diminishes grad- the borer during the berry perforation). Other
ually. Both the founding female and the larvae parasitoids that have been reported attacking
build tunnels in the bean, where they also feed. H. hampei include Aphanogmus dictyna (Water-
Pupation takes place within the coffee bean ston) (Hymenoptera: Ceraphronidae) (Uganda),
where the larva hatched. The duration of the bio- Sclerodermus cadavericus Benoit (Hymenoptera:
logical cycle, from egg to adult, varies according Benthylidae) (Uganda, Zaire, Kenya), Cephalono-
to the temperature: 21 days at 27C, 32 days at mia hyalinipennis Ashmead (Mexico) and Cryp-
22C and 63 days at 19.2C. As the first adult off- toxilos sp. (Hymenoptera: Braconidae) (Colombia).
spring appear, the population inside an infested In Brazil and Colombia, there are reports of an
bean typically consists of 2530 individuals in undescribed species of Cephalonomia parasitizing
all stages of development, of which there are H. hampei.
approximately 10 females for each male. Mating Some of the predators that have been recorded
is conducted between siblings inside the bean. include Dindymus rubiginosus (F.) (Hemiptera:
The mated females leave the bean where they Pyrrhocoridae) (Indonesia), Calliodes, Scoloposcelis
developed to look for another where they will (Hemiptera: Anthocoridae) (Colombia), and Lep-
oviposit. Several generations occur while berries tophloeus sp. near punctatus Lefkovich (Coleoptera:
are available. After coffee harvest, the borer Laemophloeidae) (Togo, Ivory Coast). However,
continues to reproduce in the non-harvested most of the predators of H. hampei reported
berries located on the plant and on the ground. from around the world (most of them anecdotal
In locations with low rainfall, where there is a records) have been ants (Hymenoptera: Formici-
clearly defined period between harvests, the dae), including Azteca instabilis (F. Smith),
972
C Coffee Pests and their Management

rematogaster curvispinosa Mayr, C. torosa Mayr,

C Management
Dolichoderus bituberculatus Mayr, Pheidole
radoszkowskii Mayr, and Solenopsis geminata (F.). An integrated pest management strategy is used
Unknown species of Azteca, Brachymyrmex, against the coffee berry borer. The principal tactics
Paratrechina, Pheidole, Prenolepis and Wasmannia are cultural control, biological control, use of traps
have been recorded as well. baited with attractants, and chemical control with
Several entomopathogenic fungi attack the cof- synthetic insecticides. Sampling infested berries is
fee berry borer, but Beauveria bassiana (Balsamo) used for pest control decision-making.
Vuillemin is the most common species infecting H.
hampei adults under natural conditions. Other fungi
recorded infecting H. hampei are Fusarium oxyspo- Sampling Infested Berries
rum Schlechtend, F. avenaceum (Fr.) Sacc., Hirsutella
eleutheratorum (Nex ex Gray) Petch., Metarhizium The proportion of infested berries is calculated
anisopliae (Metschnikoff) Sorokin, Nomuraea rileyi based on the following sampling protocol: in an
(Farlow) Samson, Paecilomyces amoenoroseus (Hen- area of 15 ha, 20 uniformly distributed sites are
nings) Samson, P. farinosus (Holm. ex S.F. Gray), P. selected; at each site five coffee plants in a row are
fumosoroseus (Wize) Brown & Smith, P. javanicus selected; 20 berries of each coffee plant are exam-
(Friederichs & Bally) Brown & Smith, P. lilacinus ined (without tearing them off), and the number
(Thom.) Samson, and Verticillium lecanii (Zimmer- of perforated berries is recorded.
man). Some of these fungi, such as M. anisopliae and
P. lilacinus, have been isolated from H. hampei-
infested berries collected from the soil. Cultural Control
Metaparasitylenchus hypothenemi Poinar
(Tylenchida: Allantonematidae), an entomopatho- There are a number of cultural practices that may
genic nematode attacking H. hampei adults, has be used to minimize damage by borers. The ber-
been reported in Mexico and appears to have a ries left on the plant before maturity and on the
wide distribution in coffee plantation in Mexico ground after harvest are collected and boiled for
and Central America 5 min to eliminate the borers in them. This practice
This nematode cause sterility in female bor- is also called manual control or rere. Weeds are
ers. The natural parasitism by an undescribed controlled after the harvest in order to facilitate
species of Panagrolaimus (Rhabditida: Panagro- the collection of berries from the ground and to
laimidae) has been reported in H. hampei in India increase the mortality of H. hampei by dehydra-
and Mexico. M. hypothenemi and Panagrolaimus tion of the berries. The coffee and shade plants are
sp. were found infecting the same H. hampei adults pruned to create less favorable environmental
in Mexico. Species from Heterorhabditidae and conditions for multiplication of the borer. Coffee
Steinernematidae (Rhabditida) are able to infect plant density is decreased because high sowing
H. hampei in the laboratory, but this has not been densities favor infestation. The coffee plants are
observed in the field. fertilized so that they have more uniform flower-
In Colombia, infections in the coffee berry ings. Varieties with the same fruiting pattern are
borer caused by bacteria such as Bacillus sp. and used because the early flowering varieties are an
Serratia sp. were observed. Also, infections of infestation source for late flowering varieties;
proteobacterium Wolbachia in H. hampei adults however, coffee varieties or species which flower
have been reported from samples around the world. earlier or later than the main variety can be used
The microsporidian Mattesia sp. was observed in a as trap crops, if managed properly. The harvest is
population of laboratory-reared insects. conducted as the fruits ripen.
 Coffee Pests and their Management
C 973

Biological Control to sunlight. Early in the morning is the most

effective time to apply it in the field, when the
The natural enemies most often used against borer is starting to penetrate the coffee berry.
the borer in tropical America have been the par-
asitoids C. stephanoderis, P. nasuta and P. coffea,
and the entomopathogenic fungus B. bassiana. Insect Traps
These three parasitoids were introduced to
tropical America from Africa. They are estab- Traps are used for monitoring and control of the
lished in most of the countries where they have coffee berry borer. They are made using 2 L plastic
been released. Nevertheless, classical biological bottles into which one or more windows have
control with these African parasitoids has not been cut to allow the entry of flying females. Bor-
been sufficient to reduce the borer population ers are attracted by a mixture of methanol and
below the economic injury level. Yearly inocula- ethanol (1:1 or 3:1) and they are caught and
tive and inundative releases of parasitoids have drowned in the water placed at the bottom of the
been used with better results. However, inunda- trap. Typically, 1625 traps are deployed per hect-
tive releases are expensive because mass rearing are. Each trap is suspended from a branch of a
methods and facilities have not been developed coffee plant at 1.21.5 m above the ground. Borers
for area-wide releases. Parasitoids are produced captured are removed from the traps and counted
for inoculative releases in laboratories where weekly. The best time to use the traps for H. ham-
the borer is reared mostly in parchment coffee pei control is after the harvest, during the massive
(35% humidity) for use in rearing the parasi- emergence of females from old berries. Better
toids. A rearing system for H. hampei in an arti- results for suppression of insect infestation in the
ficial diet has been developed; however, its next harvest can be obtained by combining the
application for mass production of parasitoids use of traps with strict sanitation.
is not fully employed. An alternative and less
intensive rearing system to produce parasitoids
for inoculative releases is production of the par- Chemical Control
asitoids in rural areas, also known as parasitoid
rural rearing. In this system, the coffee growers There are several chemical insecticides used for
rear the parasitoids at their farms or communi- borer control, among which endosulfan is out-
ties. Such rearing is conducted using coffee standing for its ability to cause high mortality of
berries infested by the borer in the field. Regard- H. hampei. However, this organochlorine insecti-
less of the rearing method used, annual releases cide is being seriously questioned for negative
of parasitoids are needed to manage the borer side effects (it is highly toxic to fish and bees, and
population. it causes secondary pest outbreaks by eliminating
The use of B. bassiana for borer control is the natural enemies); borer resistance (appar-
more developed than is the use of parasitoids. Its ently this pest is not resistant to endosulfan in
success has resulted from the relatively easy tropical America; nevertheless, there is concern
propagation, formulation and application of this about the development of resistance, as in the
fungus. Strains of B. bassiana are commonly case of New Caledonia); and sanctions in the
collected for mass production from infected international market due to the possible presence
H. hampei females in the field. Rice grains are used of residues in the coffee bean. The insecticide
as the propagation substrate for this entomopatho- should only be used if the borer population
gen. The fungus requires high relative humidity for reaches the economic threshold. The best time
germination of the spores and it is very susceptible for spraying is when the adult borer starts
974
C Coffee Pests and their Management

enetrating the fruit, at the so-called semi-con-

p by leaf miner can cause severe defoliation. In
sistency stage of development (about 20% dry Ecuador, defoliation between 70 and 90% has
weight in the bean). This period varies, according been reported on C. arabica and from 30 to 40%
to the temperature, from 90 to 140 days after the on C. canephora. The lack of leaves on the plant
main flowering. Formerly, treatments were reduces the photosynthetic activity, and conse-
throughout the plantation, but now sprays are quently the availability of nutrients for the fruits.
directed only at infested areas. In Brazil, when 9495% of the leaves were mined,
a reduction in yield between 6880% has been
observed.
Coffee Leaf Miner, Leucoptera
coffeella (Gurin-Mneville)
(Lepidoptera: Lyonetiidae) Description

Distribution The egg is oval, translucent yellow and similar to a

flattened volcano in profile. It is 0.28 mm long, 0.18
This species is found in the Neotropics: Mexico, mm wide, and 0.08 mm tall. The larva has a dors-
Central America, South America and the Caribbean oventrally flattened body with a more pro-
region. It is widespread wherever coffee is grown. nounced flattening of the head and the first
thoracic segment. The true legs are found on the
1st, 2nd and 3rd thoracic segments but four pairs
Damage and Economic Importance of prolegs occur on the 6th, 7th, 8th and 13th
abdominal segments. It has four larval instars. The
In some areas of tropical America, the coffee leaf larva attains a length of 4.5 mm. The pupa is white
miner is considered to be the principal insect in the initial stage and ochre towards maturity,
pest of coffee; certainly this is the case in some except for the dorsal portion, which remains white.
coffee-growing areas in Brazil. Leaves are the The pupa is covered by a white cocoon which
only plant organs damaged by this insect. The resembles an elongated H or X. The adult is a
damage is caused by the larva. Four larvae per small moth between 2.0 and 3.0 mm long with its
leaf may cause leaf drop. The affected leaves show body covered by silvery scales. The antennae are
irregular light-brown spots. If the damaged sur- long and thin. The front wings possess a gray oval
face of the leaf is rubbed, the leaf separates into point distally, surrounded by a black line and
two layers and between them is found a small edged by a yellow stripe that extends along the
white worm, from 2 to 5 mm in size. The coffee margin. Males tend to be slightly smaller than
leaf miner lesions may be confused with the females.
symptoms of Anthracnose (Colletotrichum sp.),
but in the latter case the leaf layers do not sepa-
rate when rubbed. Four months after flowering, a Biology and Ecology
reduction in the rate of growth of the coffee ber-
ries and an increase in leaf production take place; The female usually lays its eggs irregularly on the
this allows the plant to compensate for the dam- upper surface of the darkest, most mature leaves,
age caused by the miner. But when the fruit particularly on the middle and lower parts of the
growth starts again, if there is more than one leaf coffee plant. Eggs are laid individually or in small
miner lesion per leaf it will result in economic clusters of up to seven eggs, with a total fecundity
damage. The damage increases if simultaneously that varies between 30 and 80 eggs. Upon hatch-
the plant is under drought stress. Attack of coffee ing, the larva makes a semi-circular cut at its base
 Coffee Pests and their Management
C 975

and penetrates rapidly into the leaf, where it Management

moves about, mining the palisade parenchyma
tissue. When ready to pupate, the fully developed There are several useful approaches to manage-
larva leaves the gallery very early in the morning, ment of coffee leaf miner. population. Sampling is
making a semi-circular cut on the face of the leaf, recommended prior to initiating chemical
through which it slips down by a silk thread control.
which it secretes from the mouth. Cocoon for-
mation and pupation take place on the lower face
of the coffee leaf, often on a curvature of the leaf Sampling Damaged Leaves
or close to a protruding vein. The duration of the
life cycle, from egg to adult, lasts between 25 and The recommended sampling protocol follows:
75 days, depending on the temperature. Several sampling is initiated when the coffee flowers, and
generations occur annually, particularly in coffee is conducted monthly until the berries stop grow-
plantations with full sunlight or only lightly ing. The coffee plantation to be sampled is divided
shaded. The abundance of L. coffeella is signifi- into areas not larger than one hectare. The sam-
cantly affected by the onset of rainfall, and by pling is conducted by selecting a zigzag path
natural enemies, which are very numerous after across the coffee plantation and by selecting 12
the end of the dry season. coffee plants at random. From each coffee plant,
25 leaves are selected at random, and the number
of leaves with mines is recorded. The first two
Natural Enemies pairs of leaves at the tip of the branches are not
sampled.
The coffee leaf miner is attacked by a large
number of parasitoids; predators and some
insect pathogens have also been recorded. More Cultural Control
than 20 morphospecies of parasitoids wasps
(Hymenoptera) have been reported in tropical The shade canopy of coffee plantation should not
America. Eulophidae are the most common par- be trimmed immediately after harvest; it should
asitoids of L. coffeella; this group is largely be thinned only when the onset of the rainy sea-
unknown because keys for neotropical species do son is imminent. Adequate soil fertilization is
not exist. In Mexico, Neochrysocharis was the important. Thick mulch coverage of the soil
genus with the greater number of morphospe- should be maintained. High coffee plant densities
cies, and also the one that was collected most fre- should be avoided. The coffee plant should be
quently. It was followed, in order of abundance, pruned to stimulate vigorous growth. Damaged
by Pnigalio, Closterocerus, and Zagrammosoma. leaves should be collected and placed in contain-
Of two braconids collected in Mexico, Stiropius ers that allow the escape of parasitoids but not of
letifer (Mann) was the most abundant and most the coffee leaf miner.
widely distributed. Wasps (Vespidae) are the most
important predators of coffee leaf miner in Bra-
zil, but in Mexico, the most important predators Biological Control
are ants (Formicidae). The bacteria Pseudomonas
aeruginosa (Schroeter) Migula and Erwinia her- The introduction of natural enemies into new
bicola (Lhnis) Dye, and the fungus Cladospo- areas has not been widely explored. The most
rium sp., have been reported infecting L. important action conducted so far has been to
coffeella. protect the already existing natural enemies by
976
C Coffee Pests and their Management

avoiding the use of broad-spectrum, residual Root Mealybugs (Hemiptera:

contact insecticides. The natural control exerted Pseodococcidae)
by the coffee leaf miners natural enemies varies
from 2 to 70%; however, in most cases it is unnec- Distribution
essary to resort to the use of chemical control.
Regrettably, the use of chemical insecticides may Root mealybugs are found in Neotropical coun-
eliminate a large portion of the beneficial organ- tries where coffee is grown. The principal root
isms, causing pest resurgence and making it dif- mealybugs affecting coffee plants in tropical
ficult to implement control. In certain countries America are shown in Table17.
like Honduras, high and recurring L. coffeella
infestations have diminished significantly when
the use of chemical control is not applied for sev- Damage and Economic Importance
eral years and the beneficial fauna is restored.
This supports the idea that coffee leaf miner con- These insects attack the coffee plant roots and some
trol should not be based on use of insecticides in species also affect the foliage. The foliage of attacked
order to avoid disrupting the actions of parasi- coffee plants appears withered, the color of the
toids and predators. leaves fade, and they have copper, brown or necrotic
edges. Additionally, total or partial leaf drop may
occur. These symptoms are more evident during
Chemical Control the dry season. In case of serious attacks by Dysmi-
coccus bispinosus (Beardly), a thick, cork-like, dark
Numerous chemical insecticides can be used for crust covers the main and secondary roots; the
suppression of L. coffeella and protection of foli- attacked roots lose their absorbent root hairs. Heav-
age. These products include both organophos- ily attacked plants perish. Infestation appears to be
phate and pyrethroid insecticides. They are associated with ants (Formicidae). The symptoms
inexpensive and can be applied at the same time may be confused with the symptoms of fungal
with other agrochemicals, but they are highly diseases and with physiological plant problems.
toxic and they are more likely to cause ecological In the case of Neorhizoeccus coffeae (Laing) and
disturbances. Organophosphorates are often D. brevipes (Ckll.) infestations, the branches turn
applied twice at an interval of 3045 days, with whitish and the affected root seems to be covered
an additional application in cases of severe with flour, the crust separates easily, and consider-
attack. In the case of pyrethroids, one or two able deteriorated tissue appears. The attacked plants
applications at an interval of 4560 days are rec- have little anchorage and are easily dislodged.
ommended. The application of granular insecti- Root mealybugs have become important coffee
cides with systemic action to the soil is also pests in some areas of tropical America during the
recommended in cases where it is difficult to last 20 years. In Guatemala, the most harmful species
apply foliar sprays. Soil applications interfere is D. bispinosus; in Costa Rica, N. coffeae and D. brevi-
much less with the natural enemies of the coffee pes; in El Salvador, D. brevipes, Rhizoeccus nemoralis
leaf miner, and this approach can be used to con- Ham. and Geococcus coffeae Green; and in Colombia,
trol pests and soil diseases simultaneously. Gran- Chavesia caldasiae (Balachowsky). At some coffee
ular insecticides should be shallowly buried at plantations in Colombia, Planococcus citri (Risso) has
the drip line of the plant once a year during the also appeared as a pest, causing up to 30% yield loss
rainy season. Where this type of product is used, in the attacked trees. Other forms of damage caused
it is recommended that harvest occur 90 days by root mealybugs include excessive extraction of
after application. potassium, destruction of the absorbent root hairs,
 Coffee Pests and their Management
C 977

development of small rotting areas which tend to Other species, such as Pseudococcus adonidum (L.)
atrophy, and enhanced entry of plant pathogens. This are oviparous. Females die shortly after the eggs
damage creates a general condition of weakness, slow hatch. Upon eclosion, the small nymphs start look-
growth and plant death in many cases. ing for an appropriate place to settle on the plant
Dysmicoccus brevipes weakens the coffee root; at the selected site, they insert their mouthparts,
plants but it rarely kills them. In Costa Rica, and feed by suctioning the sap from the root. Some
plants with more than 20 mealybugs per liter of of them settle down permanently on a site until they
soil are more susceptible to infection by the fungus reach maturity, and others may change their feeding
Cercospora coffeicola Berk & Cooke. Damage is site by moving short distances. Depending on the
more apparent on nutrient-deficient soils, and type of soil, the humidity, aeration and age of the
where weeds are abundant. Plants in seed beds coffee plant, they usually place themselves between
and tree nurseries are also attacked. The varieties 10 and 60 cm under the soil surface, their popula-
of C. arabica grown in Central America (e.g., tion diminishing as the soil depth increases. Differ-
Caturra, Catua, Bourbon) are susceptible to the ent species prefer different parts of the root. For
mealybug attack, while tolerance has been example, D. brevipes and R. nemoralis prefer the
observed on C. canephora, C. dewevrei De Wild. main and the lateral roots, while G. coffeae attacks
& Durand, and C. excelsa Chev. the absorbent roots; the smaller species attack the
whole root system near the soil surface.
As they feed and develop, the nymphs and
Description adults excrete their characteristic waxy cover and
form compact colonies. Mealybugs excrete sugary
Mealybug eggs are small (0.5 mm). The nymphs are substances (honeydew), which supports the growth
oval, slightly swollen, usually white, yellow or pink- of fungi (i.e., Bornetina), which contribute to for-
colored, and covered by a white waxy-mealy dust mation of the thick, cork-like, dark crust covering
with waxy filaments projecting laterally. The female and sheltering the mealybug colony; a succession of
nymphs molt three times, and the males, contrary crusts give a knotty appearance to the root. The sug-
to the females, form a waxy cocoon in the third ary substances also attract certain ant species, which
instar, where they pupate. The adult females have no live in a symbiotic association (trophobiosis) with
wings and they are similar to the nymphs but larger. the mealybugs. In exchange for the sugary foodstuff,
Smaller species, such as Geococcus and Rhizoecus, the ants give them protection and transportation
are from 1.5 to 2.0 mm long and the larger ones, from one root to another and from one plant to
such as Dysmicoccus and Pseudococcus, are from 2.5 another. The ants that associate with mealybugs in
to 5.0 mm long. Males are white, fragile-looking, South America and in some of the Caribbean
smaller than the females, and they possess a pair of Islands are in the genus Acropyga. In Colombia, the
wings and a pair of terminal filaments. Hope ant (A. robae Donisthorpe) and the Amag
ant (A. fuhrmanni Forel) are associated with N. cof-
feae and C. caldasiae, respectively. In Guatemala, D.
Biology and Ecology bispinosus seems to be associated with the presence
of the ant Solenopsis geminata (F.). P. citri does not
Mealybugs generally live attached to the coffee root, produce large quantities of sugary excretions when
forming numerous colonies. Their reproduction it lives on the plant roots, and is not attractive to
may be sexual or parthenogenetic (partial or total). ants. In certain cases, the mealybugs have lived for
Eggs are laid in groups and covered by a layer of more than a year in the absence of ants.
cotton-like wax or by an egg sac of crystalline wax The life cycle, from egg to adult, requires from
filaments. A single female may deposit 300600 eggs. 30 to 120 days, according to the species and the
978
C Coffee Pests and their Management

temperature. Five generations develop per year in ant nests should be examined critically; from 15 to
the case of D. bispinosus. Root mealybugs develop 20 plants/ha should be checked, paying more atten-
better during the rainy season, particularly in low tion to those that are close to the ant nests and/or
or medium altitude plantations in Central Amer- possess yellow leaves. The surrounding shade trees
ica. Other conditions that favor their development and bushes should also be checked. The plants are
are sandy, acid pH, and medium moisture soils. In checked by moving the stems in all directions in
Colombia, the damage caused by Rhizoecus sp. order to gain visibility of the base of the roots.
seems to increase in old, poorly fertilized planta-
tions, and in Guatemala D. bispinosus is found most
frequently in 15 year-old plantations. Mealybugs Cultural Control
are polyphagous, also attacking other plants such
as shade trees (Inga spp.), cassava (Manihot escu- Mealybugs should not be present in the seed bed
lenta Crantz), sugarcane (Saccharum), banana trees and tree nursery. The limits of any infestation
(Musa), lemon trees (Citrus) and some herbs that sites should be determined and marked. Adequate
grow on the coffee plantation. In Costa Rica, Anred- fertilization should be provided, including
era ramosa (Moq.) Eliasson is an alternate host of addition of organic matter to the soil. Physical
D. brevipes; in El Salvador, D. bispinosus has been conditions of the soil should be improved in
found associated with Lantana camara L. order to avoid floods. Planting coffee trees on
land previously supporting plants that are highly
susceptible to mealybugs (e.g., cassava, sugarcane)
Natural Enemies should be avoided. Alternate host plants should
be eliminated from the plantation. Severely dam-
In general, the literature on coffee mealybugs in aged plants should be removed and burned.
tropical America does not make reference to their
natural enemies. In Cuba, Coccidoxenoides peregrinus
(Timberlake) (Hymenoptera: Encyrtidae) is cited Biological Control
as a solitary, primary endoparasite of the pseudo-
coccid complex in coffee. Other natural enemies This is practically unexplored in the coffee grow-
of mealybugs reported in Cuba are Diadiplosis ing countries of tropical America.
cocci Felton (Diptera: Cecidomyiidae), Leptomastix
dactylopii Howard (Hymenoptera: Encyrtidae)
and Signiphora sp. (Hymenoptera: Signiphoridae). Plant Resistance to Insects

In Guatemala, some research has been conducted

Management which supports the use of plants grafted on resis-
tant rootstocks of C. canephora (genotypes 3757,
There are management options for mealybugs, but 3754, 3751, 3581, 3752 and 3756) and C. dewevrei.
insecticides are normally used once pest popula-
tions develop.
Chemical Control

Sampling Systemic organophosphorate and carbamate insec-

ticides produce good results, although they are
Sampling should preferably be conducted on young expensive. The presence of mealybugs in seed beds
coffee plantations (up to 6 years old). Plants near or on plants younger than 1 year old is sufficient
 Coffee Pests and their Management
C 979

justification for insecticide application. On planta- When Capnodium (sooty mold) and Meliola (black
tions older than 3 years, insecticide application is mildew) fungi grow on the honeydew excreted by
made if more than 1.6 colonies per plant, on average, the scales, they interfere with photosynthesis. Ants
are found. In no case should the damage be allowed are present where scale insects are feeding.
to exceed 25% of the absorbent roots. Insecticides In cases of severe attack, a dirty appearance
are applied on the drip line of the plant if the dam- on the plant, general weakening, growth delay, yel-
age is on the small roots. If the damage is on the lowing and drop of foliage and fruit are observed.
main root a funnel-shaped hole should be made With the articulated scale, Selenaspidus articulatus
around the tree trunk, the insecticide should be (Morgan), old attacks may be recognized because
poured in and the hole should be covered again with the site where the scales were located turns yellow
soil, adding also a layer of dead leaves. Application of or discolored, resembling infection by the coffee
granular insecticides is made at the beginning of the rust fungus (Hemileia vastatrix Berk. and Br.).
rainy season or 3 months before starting the harvest. Some species, such as the green scale, Coccus
viridis (Green), are considered to be quite impor-
tant to coffee production, though some attack a
Scale Insects, Mealybugs and number of different cultivated plants. Severe infes-
Related Foliage Pests (Hemiptera) tations of C. viridis may kill young tree nursery
plants. The incidence of these pests is highest on
Distribution coffee plantations lacking adequate shading.

Different scale insects, mealybugs and related

foliage pests live on the coffee plant. The geo- Pest Description
graphic distribution of some is restricted to a few
countries of tropical America, whereas others The following cases are presented as examples:
are distributed more widely. Some are reported C.viridis adult females are motionless, oval, some-
attacking the coffee plant only in South America, times asymmetric, very flat and pale yellow. They
others only in Central America or the Caribbean have some black spots centrally, and they tend to
(Table 17). be soft and elastic. They are about 2.2 mm wide
and 4.0 mm long. The presence of males is very
rare.Saisettia coffeae (Walker) adult females are
Damage and Economic Importance motionless, almost spherically shaped and dark
brown. They are 2.03.5 mm in diameter. The males
Scale insects, mealybugs and related species attack are winged. P. citri adult females are mobile, oval,
the aerial part of the coffee plant and, in some spe- pale yellow or dark orange, with very clear segments
cies, also the root (e.g., Planococcus citri [Risso]). on the body, and 4.0 mm in size. They are covered
The leaves, fruit, branches and young tissues of with a dusty white glandular secretion except for a
the aerial part of the attacked coffee plant often longitudinal stripe dorsally. They have filaments lat-
support colonies or groups of circular, oval or elon- erally. Males are smaller (1.0 mm), violet to yellow
gated scales, which may be flattened or swollen, in color, and they have well-developed wings.
with a soft or hard consistency. In other cases, colo-
nies of insects have a soft body covered with white,
cotton-like filaments. These insects cause damage Biology and Ecology
by removing large quantities of sap, which causes
plant malnutrition. Also, sticky honeydew and The biology of these insects varies among spe-
blackish molds can be found covering the foliage. cies and can be quite complex. The first instar
980
C Coffee Pests and their Management

has legs and antennae and is very active. To feed, Natural Enemies
the insects attach and insert their mouthparts.
After the first molt, they generally lose their legs These insects are susceptible to a large number of
and antennae and the insect becomes sessile. By parasites, predators and pathogens as natural
then, it begins to secrete a waxy, scale-shaped enemies.
layer that covers the body. In the case of scales of
the family Diaspididae, this layer of scale is
almost always separated from the insects body. Management
Adult females remain under this cover and they
produce their eggs or directly give birth to the Sampling
nymphs therein. The location on the plant, and
the age of the plant they prefer to attack, depends During the dry season, inspections should be con-
on the species of scale: C. viridis is commonly ducted to check for the presence of scales and
located along the leaf veins, on the back of the related species in the coffee plantation, as well as
leaves, on young buds and on seed bed coffee on other plants cultivated nearby or at the same
fruits of nursery plants; S. articulatus is found time.
mainly on the leaves and fruits of production
plants; the round scale, Parasaissetia sp., mostly
attacks the stems and branches of coffee plants
Cultural Control
younger than 1 year; the black scale, Ischnaspis
The nursery shading should be reinforced during
longirostris (Signoret), infests the leaves, branches
the dry season. Affected plants should not be
and fruits of old, poorly attended coffee planta-
transplanted. Weeds should be suppressed. The
tions; Cerococcus catenarius Fonseca gathers in
pests should be kept under control on host plants
the form of a line or chain along the trunks and
existing in or near the coffee plantations. Sanitary
branches; P. citri attacks new branches, leaves,
pruning should be performed to eliminate (by
flower buds, fruit peduncles and fruits; Orthezia
burning) old and unproductive branches infested
spp. attack branches, leaves and fruits, mostly of
by the pests.
robusta coffee in Brazil. The males develop very
much like the females except that in the last
stage, before transforming into adults, they go Biological Control
through a pupal stage; the wings develop exter-
nally over the pupa. Most of the scales reproduce Natural enemies should be protected and pre-
parthenogenetically. Some species are oviparous served, using insecticide only if necessary.
(S. coffeae, S. olae [Oliver]) and others are vivipa-
rous (Coccus hesperidum L.). The total number
of eggs produced per female varies among the Chemical Control
species; for example: C. viridis, between 50 and
600 eggs; Orthezia praelonga Douglas, more than Chemical control is directed only at infested plants,
200 eggs; C. catenarius, about 900; S. coffeae can after checking to determine that the scale colonies
lay up to 1,600 eggs. The complete life cycle, from are alive. For better control, mineral oil is added to
egg to adult, lasts between 40 and 60 days. The the insecticide solution, with applications made
scale insects are more abundant during the dry every 15 days until the problem is corrected. The
season and at the onset of the rainy period. Hard oil should not be used during flowering or during
rains and natural enemies are important factors sunny periods of the day. During the rainy season,
in the mortality of these pests. granulated insecticides may be used.
 Coffee Pests and their Management
C 981

Cutworms and Armyworms Biology and Ecology

(Lepidoptera: Noctuidae)
Adults are moths that are active at night, laying
Distribution their eggs individually (A. ipsilon) or in groups
(S.frugiperda). During the first two larval stages,
These insects are widely distributed in the coffee they feed on leaves that are at soil level, and in
plantations of tropical America (Table 17). the last three they act as cutting worms. During
the day, they remain hidden in the soil. In some
species, such as A. ipsilon, the larvae coil up when
Damage and Economic Importance disturbed. Larvae pupate in the soil.

Cutworms and armyworms constitute an economi-

cally important pest for many crops. Damage is Natural Enemies
caused during the night by the larval stage. The
larvae attack the stems of small coffee plants in ger- There are many natural enemies (parasitoids,
minating beds, seedbeds or plant nurseries, and predators and pathogens) of these pests. In Ecua-
recently transplanted plants. On seed beds and plant dor, the larval parasitoids Bonetia sp. (Diptera:
nurseries, plant damage typically takes the form of Tachinidae) and Chelonus sp. (Hymenoptera:
plants cut at the soil level or slightly above, or Braconidae) and the predatory ground beetle
withered plants. In the case of recently transplanted Calosoma sp. (Coleoptera: Carabidae), are cited.
coffee plants, defoliated and sometimes dead coffee
plants can be observed. Spodoptera frugiperda
(Smith) larvae feed on the stem, causing withering Management
and finally death of the small plants during the first
year of their lives. In other cases, the stem breaks at Sampling
the site of the ring formed by the larval feeding.
When the infestation is severe, many plants are killed Night-time inspection of seedbeds and the young
and re-sowings are needed, which increases the cof- plantations should be made to detect initial
fee plantation set-up costs. Damage is more frequent infestations.
in plantations that are close to fields where corn,
beans, vegetables, cassava or pasture are grown.
Cultural Control
Pest Description
Seedbeds or plant nurseries should be kept clean
The following species are presented as examples: of weeds and dead leaves, since the larvae seek
S. frugiperda the larvae have a well-contrasted, shelter there.
inverted Y on the head; neonate larvae are white
with a black head, but as they grow they turn dark.
Large worms are light brown to dark green in color Mechanical Control
and they are about 4.0 cm long. Agrotis ipsilon (Huf-
nagel) small larvae are brown with paler back Larvae should be eliminated by hand during the
marks, and large ones, which may be as be as large as night-time inspections. Heavy watering should be
4.05.0 cm, are shiny black-gray in color, with a pale applied to get the larvae out of their hiding places,
gray line on the back and black tubercles on each of followed by manual elimination. Light traps can
the segments. be used to capture the adults.
982
C Coffee Pests and their Management

Biological Control mortality of the branches and stems is caused by

microorganisms that invade the plant tissues
Biological insecticides such as Bacillus thuringiensis through the feeding sites formed by the brown
Berliner should be used, particularly at the begin- coffee borer. Ants, termites or mites can be found
ning of infestations, when the larvae are small. in the abandoned galleries. Often the ants cause
the death of branches or stems when enlarging the
Chemical Control abandoned galleries of X. morigerus to construct
their own nests. If death of branches or stems does
Insecticides can be incorporated into the soil, before not occur, the yield is reduced as a result of dam-
or after sowing, for cutworm control. Granular age to the flowering and development of the fruit.
products are used in a preventive manner. The use The symptoms can be observed more frequently
of poisoned baits during the night and dry weather on weak coffee plants, but attacks may also be seen
is also recommended. on the young stems of pruned plantations. This
pest is particularly important in Ecuador. In Mex-
ico, X. morigerus is also an important pest in the
Soconusco region in Chiapas.
Brown Coffee Borer, Xylosandrus
morigerus (Blandford) (Coleoptera:
Curculionidae: Scolytinae) Description

Distribution The egg is oval, white and very small. The larva is
milky white, with a yellowish head, and lacks legs.
This pest comes from the Oriental region, having The pupa is white initially, turning cream to brown
its distribution center in the Indomalayan area. It toward maturity. The adult is cylindrical and from
was detected in the western hemisphere in 1958 1.40 to 1.90 mm long. It is differentiated from
1959, and it is now found from Veracruz, Mexico other species of the same genus by the bright
to Brazil. brown-reddish color, by the stouter body and
because the declivity commencing only on-third
of the elytral length from the base, and by the near
Damage and Economic Importance absence of punctures on the sides of the elytra
(variable). Females have well-developed wings and
Various tree species can be attacked by X. morigerus fly, but males are incapable of flight. Females are
(e.g., avocado, cacao, cedar, coffee). This insect dis- larger than males.
plays a strong preference for attacking robusta cof-
fee, C. canephora. Some reports indicate that it
may also infest C. arabica; however, this has not Biology and Ecology
been confirmed in Mexico. The attacked coffee
plant branches and young stems typically display a Mated females take flight during the day, leaving
few or many holes of about 1.0 mm diameter. the gallery where they developed in search of
Blackening of the tissues may be seen around the branches or stems, which they penetrate to
perforations. A longitudinal cut of an affected construct the new galleries. The female lays
branch reveals a gallery in which the whitish lar- from 20 to 60 eggs in 810 days. X. morigerus is an
vae can be observed, along with reddish brown ambrosia beetle. The adults and larvae get more
adults. The attacked young branches and stems nutrition by feeding on fungi (e.g., Ambrosiaemy-
dry up distally and then die. Apparently, the ces zeylanicus Trotter is reported from Ecuador;
 Coffee Pests and their Management
C 983

Raffaelea tritirachium Batra from Mexico) than ethanol have been used for monitoring flying
from the coffee plant tissues. These fungi grow females in robusta coffee plantations.
inside the gallery, which is inoculated by the found-
ing female. The larvae have three instars. The life
cycle, from egg to adult, is 2040 days. A gallery Cultural Control
may contain more than 80 individuals in all stages
of development. The sex ratio in galleries is female- Infested vegetative material, particularly in
dominated; various studies have found only one young or pruned plantations, should be cut and
male for each 7, 11 or 20 females. Mating occurs burned periodically. Adequate fertilization should
within, or very close to the gallery. Infestation is be applied. Shade of coffee should be regulated by
apparently less evident under drought conditions, pruning. Weeds should be suppressed by shading,
because the ambrosia fungi require moisture. Nev- mulching, use of ground cover, and by selective
ertheless, reports from Ecuador indicate that the weeding by hand.
populations are larger during the dry season of the
year. X. morigerus is a pest which frequently attacks
healthy plants; however, very strong attacks may be Biological Control
observed when the coffee plants have been weak-
ened by droughts, malnutrition, nematode attacks This approach has not yet been attempted for this
and competition with weeds. The attacks may be species.
accompanied by attacks from other Scolytinae.

Chemical Control
Natural Enemies
This is recommended when the beetle population
No native parasitoids of this pest have been has undergone a marked increase and natural and
reported in coffee growing countries in tropical cultural control cannot restrain it. Insecticides are
America. However, it should be mentioned that in useful only when adults are out of the galleries or
Indonesia, a Tetrastichus sp. (Eulophidae) has been are boring on the branches; once they have taken
reported, and also probably a bethylid parasitoid. refuge within the galleries, insecticides have little
In Ecuador, ants (Formicidae) have been recorded or no effect on X. morigerus.
as predators of the brown coffee borer, including
species of Crematogaster, Leptothorax, Pheidole,
Pseudomyrmex and Solenopsis. The entomopatho- Stem Borers Plagiohammus spp.
genic fungus B. bassiana has been reported infecting (Coleoptera: Cerambycidae)
this insect pest.
Distribution

Management Three species of Plagiohammus have been reported

attacking the stem of coffee plants in Mexico and
Sampling Central America. P. maculosus (Bates) has the wider
geographic distribution (Costa Rica, El Salvador,
No sampling methods have been developed in Guatemala, Honduras, Mexico), while P. mexicanus
coffee plantations; however, some studies indicate Breuning and P. spinipennis (Thomson) have
that penetrated branches and stems have an aggre- been recorded attacking coffee only in Mexican
gated distribution in the field. Traps baited with plantations.
984
C Coffee Pests and their Management

Damage and Economic Importance ready to pupate, the larva moves close to the excre-
tory opening, which has been made close to the
A pile of white-yellowish sawdust or powder present ground, and it isolates itself within the stem in a
at the base of coffee plants, at the soil level, in a good chamber surrounded by sawdust. The larval period
indication of infestation by Plagiohammus. Infested lasts from 2 to 3 years. Adults are more visible at the
plants may have a withered, yellow-like and decay- beginning of the rainy season (April through June),
ing appearance. Careful observation at the stem base the period when egg laying occurs. The abundance
may help identify the hole or holes (ca. 5.0 mm in of these cerambycids is higher in high-altitude cof-
diameter), where the sawdust originates. A longitu- fee plantations (>1,000 m) and in places with long
dinal cut of the stem and root may uncover a large, summers or with lack of rain. Abandoned coffee
white or creamy-colored larva with long gallery plantations are more severely attacked.
containing powder; the gallery begins at the stem
and may go as low as the tip of the central tap root.
These borers are one of the most destructive coffee Natural Enemies
plant pests in certain areas of tropical America. The
damage is caused by the larva when it bores into the There is no information on the natural enemies of
stem and the root. The borer attack delays the plant the Plagiohammus spp.
growth and it may cause death directly by damaging
its root, or indirectly, by facilitating stem breakage
following wind action or other factors. Management

Sampling
Description
Coffee plants having sawdust as the base of the
The egg is unknown. The larva is creamy-white, with trunk should be searched for. If damage is recent,
the thorax wider than the abdomen, and legless. Its the sawdust is white or pale yellow.
head is light brown with strong and visible mandibles
extended forward. A well-developed larva is about
4.5 cm long. The pupa is brown and similar in size to Cultural Control
the adult. The adult has an elongated body, cylindri-
cal, from 2.0 to 3.5 cm long by 0.8 cm wide. The body Infested stems should be removed. Adequate
is light brown with two white lines on the prothorax fertilization should be applied. Weeds should be
and with irregular white spots on the elytra. The managed by shading, mulching, ground cover,
antennae are longer than the body (4.0 cm). and mechanical removal.

Biology and Ecology Biological Control

Not much is known about the bionomics of Plagio- This has not been attempted yet.
hammus spp. Adult females lay eggs on the bark of
coffee plant stems, at a height below 30.0 cm. Upon
eclosion, the larva penetrates the stem and bores Chemical Control
longitudinally all the way to the root, while it feeds,
grows and develops. The larvae may be found in the In places where the pest appears yearly, a preven-
stem, from the base to a height of one meter. When tive insecticide application with a brush or a
 Coffee Pests and their Management
C 985

manual pump is recommended, treating from important, because they may cause death of the plants.
the stem base up to 60.0 cm high. Application may The attacks are more severe in plant nurseries, on
be repeated once or twice every 20 days. In order recently transplanted coffee bushes and on 1 year-old
to kill the larva within the stem, a cotton ball plants, although mature plantations may also suffer
soaked in an insecticide can be inserted through the attacks of these pests. In some plantations it is esti-
the respiration and excretion opening made by the mated that 2 or 3% of the transplanted coffee plants
larva, or insecticide solution can be injected into may be lost to white grub attack. Coffee plantations
the opening with a syringe. When treating in this located in the vicinity of pastures are most affected.
manner, the orifice is enlarged, the product is
applied and the orifice is sealed with mud, clay
or any other material that solidifies. This step, Pest Description
though effective, can be expensive due to the labor
it may require. The egg is white; when recently laid, they are elon-
gated, and later on they adopt a round shape. The
larva has a milky-white colored body with a C
White Grubs (Coleoptera: shape, with long thoracic legs covered with hair. The
Scarabaeidae) head is dark or light, with strong mandibles. There
are three larval stages; the last stage grows up to
Distribution 3.54.0 cm long. The pupa is brown-golden in color,
with a size that varies between 1.8 and 2.0 cm. The
Phyllophaga is a well-represented genus of white adult is a strong, heavy bodied scarab. Depending
grubs in coffee plantations in tropical America on the species, they may be light or dark brown
(Table17). In El Salvador, P. latipes (Bates), P. men- or reddish-brown in color, measuring from 0.5 to
etriesi (Blanch) and P. obsoleta (Blanch) are found, 2.5 cm in length; the antennae are enlarged distally,
whereas in Costa Rica P. sanjosecola Saylor and with the apical expansion consisting of several
P. vicina (Moser) are reported. Other white grubs laminated segments. They are able to fly.
recorded in coffee are Anomala sp. (El Salvador)
and Dyscinetus picipes Burmeister (Cuba). Biology and Ecology

Adult females, which have twilight habits, come

out at the beginning of the rainy season and they
Damage and Economic Importance lay their eggs within the first 10.0 cm of depth in
the soil, close to pastures or fodders. The eggs are
White grubs attack the coffee plant root. The damage laid one by one or forming small groups. A female
is caused by larvae that live in the soil and feed on the may lay up to 200 eggs. Small larvae feed them-
root system of the plant. In the seedbed and plant selves with organic matter and small roots, and
nursery, the plants wither and die rapidly; in the when they reach the last development stage, they
coffee plantation, irregular areas on one or several are voracious root eaters. They are found at dif-
coffee plants, usually young, may be observed, which ferent depths, according to the soil temperature
show symptoms of yellowishness, limited growth, and humidity. They are common in areas that
scarce fruits and mummified fruits.When the affected have been gramineous pastures. The larval stage
plants are taken out of the soil, lesions, very few small lasts about 6 months. Pupation takes place in a
roots and partial or total bark peeling on the main chamber or cell located in the soil at a depth
and secondary roots are observed. In some coffee between 10.0 and 20.0 cm. The duration of the
growing areas, these pests can be economically life cycle, from egg to adult, varies from 9 to 10
986
C Coffee Pests and their Management

months. Adults are strongly attracted by artificial manually. Light traps, preferably 40 watt black-
light and they feed from the leaves of some plants, light traps, should be used to capture and eliminate
such as cassava, African oil palm and Erythrina adults. The use of a trap for every 1015 ha is rec-
trees (Fabaceae). ommended, which should be turned on from 18:00
to 21:00 oclock. This procedure has the disadvan-
tage of attracting a number of other night habit
Natural Enemies insect species, which should not be eliminated.

The larval parasitoids Campsomeris, Elis and

Tiphia (Hymenoptera: Scoliidae) have been Biological Control
reported in coffee plantations. Parasitism of bac-
teria Micrococus sp. on larvae and parasitism of Biological control has not been attempted in cof-
fungi Spicaria sp. and Metarhizium sp. on pupae fee plantations.
has been observed. Nematodes as parasites of lar-
vae have been observed as well. A robber fly Diog-
mites species (Diptera: Asilidae) has been recorded Chemical Control
predating larvae in the soil. Several mammal,
reptile and bird species predate on the adults. In the case of plant nurseries and recently trans-
planted coffee plants (<1 year old), one larva per
plant justifies the use of granular insecticides.
Management The application can also be made at sowing time.
With three large larvae or seven small larvae per
Sampling square meter, insecticides are recommended for
young plants. Three year old plants withstand
Root and soil samples at a depth of up to 20.0 cm up to eight larvae; for 4 year-old plants, 1215
should be taken, in order to determine the infes- larvae; well-attended mature plantations with-
tation sources. The samples are taken from three stand up to 20 larvae per coffee plant.
coffee plants, at 30.0 m intervals. On areas <7 ha,
sampling should be taken diagonally and for
larger areas sampling should be taken in parallel. Black Citrus Aphid, Toxoptera
aurantii (Boyer De Fonscolombe)
(Hemiptera: Aphididae)
Cultural Control
Distribution
Weeds should be suppressed principally by
shading, by mulching, by ground cover vegeta- This aphid comes from the tropical and sub-tropi-
tion, by slashing back and by selective weeding cal areas of the Old World. It is widely distributed
by hand. Shade trees should be pruned. in coffee plantations in tropical America.

Physical-Mechanical Control Damage and Economic Importance

During preparation of the seedbed or plant T. aurantii attacks leaves, buds and other tender
nursery, the soil to be used for bag filling should parts of the coffee plant. Coiled, deformed and curled
be sifted, and the larvae found therein killed leaves and tender buds are signs of infestation;
 Coffee Pests and their Management
C 987

also, reduced growth, and leaf and flower drop Natural Enemies
occur. Damage may occur in seedbeds, plant nurs-
eries, and on adult coffee plants. Yellow, green or More than 70 species of natural enemies have been
black insect colonies, more or less round shaped, reported on T. aurantii around the world. In coffee
can be found on the lower surface of foliage. They plantations in tropical America, the following
are easily excited, producing a characteristic noise have been reported: the braconid parasitoids
which may be audible if the colonies are very large. Diaretus sp. and Lysiphlebus testaceipes (Cresson);
The infestation may be accompanied by a fungus, the entomopathogenic fungus Acrostalagmus
called sooty mold, on the foliage, and also by the albus Preuss; the coccinellid predators Hippodamia
presence of ants. In general, this aphid is not very sp. and Cycloneda sp.; the syrphid predators
important as a pest; however, a considerable yield Allograpta sp., Paragus borbonicus Macquart and
reduction may appear when severe and prolonged Baccha clavata Fabricius; and the green lacewing
attacks occur, particularly if the infestation appears predator Chrysopa sp. (Chrysopidae).
during the flowering and fruiting season. The
damage is often more severe in the plant nursery,
on growing plants. T. aurantii is reported to be Management
responsible for the transmission of pathogens to
coffee plants in Costa Rica and Guadeloupe. Sampling

Description Growers are advised to monitor young leaves

throughout the dry season for aphids or damage.
The nymphs are similar to adults, but smaller and
dark-brown in color. The adults have a globoid,
dark green or black body, and they may or may not Cultural Control
have wings; apterous females are larger (2.02.1
mm) than winged ones (1.71.8 mm). They bear a Reinforce shade of coffee plantation during the dry
pair of cornicles on the back of the body. season. Affected plants should not be transplanted.

Biology and Ecology Biological Control

Adult females generally reproduce by parthenogen- It is generally acknowledged that natural enemies
esis and are viviparous. Males are winged and rarely contribute importantly to prevent T. aurantii from
seen. An apterous female may produce 50 female having greater economic impact. Natural enemies
nymphs in 7 days. The life cycle, from nymph to should be conserved.
adult, is 6 days at 25C. These aphids excrete honey-
dew on which the sooty mold fungus grows. The
fungus gives a blackish appearance to the plant. Chemical Control
The honeydew is highly appreciated by ants; hence
the association of ants with aphids, providing them with If chemical control becomes necessary, either
protection and transport to other plants. T. aurantii insecticidal oil or an insecticide may be used.
finds conditions more favorable during the dry sea- Chemical control should only be applied at the
son. When conditions are adverse, winged females first signs of damage during periods of young
are produced in order to disperse and colonize new leaves growth. Young leaves should be completely
plants. Infestations appear in a cyclic manner. moistened after application of chemicals.
988
C Coffee Pests and their Management

Leaf-Cutting Ants, Atta and Pest Description

Acromyrmex (Hymenoptera:
Formicidae) Atta cephalotes (L.) is hereinafter described. Their
colonies contain three castes: queens, males and
Distribution workers. Queens are big (16 mm), with a strong
brown-reddish color, and they have wings (although
Leaf-cutting ants of the Atta and Acromyrmex they lose them after the nuptial flight); also, they
genera are found in Neotropical countries where have a pair of horns on the occipital lobules and
coffee is grown. The principal leaf-cutting ant another pair on the lower part of the head, close
species affecting coffee plants in tropical America to the mandibles. Males are winged but smaller
are shown in Table 17. (13 mm) than the queens, and they do not have the
aforementioned horns. Workers are wingless. Sol-
dier workers present abundant yellowish hair on the
Damage and Economic Importance forehead sides, and they are about 1315 mm long.
Forager workers have less hair and they are about
Leaf-cutting ants attack leaves, tender buds and 910 mm long; fungus-cultivator workers are lighter
flowers of the coffee plant. The leaves of attacked colored and smaller (from 2 to 4 mm).
coffee plants have semi-circular cuts or these plants
are completely defoliated. Leaf fragments dispersed
on the ground are seen around the defoliated plants. In Biology and Ecology
recent attacks, the presence of ants carrying leaf and
flower pieces may be observed. It is possible to detect Atta and Acromyrmex ants are social insects that
earth mounds (nests) nearby or relatively far away. use plant leaves to cultivate symbiotic fungus
Situations in which ants are direct plant pests (Leucoagaricus gongylophorus (Mller) Singer;
are rare; however, in the tropical and sub-tropical Attamyces spp.), which serves as their foodstuff.
areas of America, ants of the Atta and Acromyrmex They form colonies constituted of three castes:
genera can constitute important pests of many cul- queens, males and workers; the latter are sterile
tivated and wild plants. In tropical America, cutting and present acute polymorphism and functions
ants constitute the dominant group of herbivorous (soldiers, foragers, cultivators). The mating of
animals, because they consume much more vegeta- queens with males takes place outside the nest
tion than any other animal group. In the case of during the nuptial flight, at the beginning of
coffee, these ants are generally considered of minor the first rains. Newly mated females dig their
importance. Nevertheless, in some areas like the nests in the soil and begin to cultivate the fungi
Turrialba region of Costa Rica, A. cephalotes attacks which will serve as their food and to lay their
on coffee plants can be severe in monocultures. The first eggs. The eggs give birth to the larvae and
damage is caused by the worker caste when they cut after 4060 days, the first adult workers emerge.
the coffee foliage and flowers with their mandibles. In New colonies have a single tower-like mound of
some Atta species, from 5 to 28 colonies/ha have small size of <200 cm2 in area, and with a small
been observed, with the possibility of having one entrance hole, whereas older colonies are flat-
or more millions of workers in each colony. The tened, with larger entrance holes and a colony
nests they construct may have dimensions that vary surface area >200 cm2. The growth of the colony is
between 30 and 600 m2. From one day to the other, very slow at the beginning, but during the second
one or more coffee plants may be completely defo- and third year it accelerates rapidly and then it
liated by these ants. Coffee plantations near woody diminishes as the colony starts production of
or weedy areas are attacked more commonly. males and winged queens. Towards the end of the
 Coffee Pests and their Management
C 989

third year, the population is enormous, and it is Cultural Control

possible to observe more than 1,000 entrance/exit
holes on the nest. The Acromyrmex nests are Queens should be eliminated at the recently formed
simpler than those of Atta. In order to reach the nests using a grub hoe. Repellent plants (e.g., sor-
plants which serve as their food, the forager work- ghum) should be sown. Because coffee on farms
ers move from the nest, which is often in non- with low vegetational diversity is at greater risk of
cultivated fields, through narrow paths which can attack by A. cephalotes, it is recommended that
go more than 100 m in distance. The workers shade trees be planted in order to increase shade
activity is more intense during the night. levels and therefore to decrease ant colonization.
Also, it may be desirable to plant shade trees that
are palatable to leaf-cutting ants, but that should
Natural Enemies be either not commercially valuable (e.g., Erythrina
poeppigiana [Walp]. Cook, Cordia alliodora (Ruiz
Apparently these ants have few natural enemies. & Pav.) Oken, Swietenia macrophylla King, Cedrela
Several predators, such as birds, toads, lizards and odorata L.), or that are tolerant of ant attack, in
anteaters feed on the queens and males during the order to divert ants from foraging coffee plants.
nuptial flight. In Colombia, other carnivorous ants
have been observed to be predators of leaf-cutting
ants. The importance of all these natural enemies in
Biological Control
regulating leaf-cutting ant populations is unknown.
Some entomopathogenic (e.g., Paecilomyces sp.
and M. anisopliae) and antagonist (Trichoderma
viride Persoon ex Gray) fungal strains have proved
Management
to be successful against leaf-cutting ant colonies in
experimental studies. However, the practicality of
The optimal time of the year to control leaf-cutting
these fungi has not been assessed in commercial
ants has not been determined. However, the nup-
coffee plantations.
tial flight period, a crucial event within the ant life
cycle, should be taken into account. Considering
the ecological importance of leaf cutting ants as
plant population regulators in woody and grazing Chemical Control
areas, and taking into account that in certain areas
they are eaten by humans, it is recommended Insecticides are applied directly through some of
that population regulation, not elimination, be the entrance/exit holes of the nests, taking the
the primary goal. precaution of plugging or closing most of them
before. The ant hill beating procedure may also
be used, which consists of digging in the nest
Sampling with a shovel in order to uncover the ant brood,
and spraying them with insecticide. Also, leaf-
No sampling techniques have been developed for cutting ants can be successfully controlled using
leaf-cutting ants in coffee plantations. The nests can baits containing insecticides. Treatment results
be located by following the narrow paths used by can be improved by basing the amount of insec-
the ants. Ant colony density can be estimated by ticide applied on an estimate of the colony
sampling four 125-m2 plots at each edge of a farm volume, instead of surface colony area. An
(north, west, east and south), and a single 500-m2 experimental study shows that mounds of dump
area in the center of the farm (a total area of 1,000 m2). material can be used as a highly effective
990
C Coffee Pests and their Management

small-scale deterrent to protect Hibiscus plants fungi may be involved in the damage (e.g., Phoma
from defoliation by A. cephalotes, but this method costarricensis Echandi).
has not been tested in coffee.

Description
Long-Horned Grasshoppers or
Katydids (Orthoptera: The eggs of I. subquadratum are brown in color,
Tettigoniidae) elongated, with a hard chorion; they are oviposited
in compact clusters. There are six nymphal instars.
Distribution Newly emerged nymphs are fragile and gray in
color. Nymphs resemble adults, but are smaller,
Two Idiarthron species, I. subquadratum Saussure lighter colored, and lack wings. Nymphs and adults
& Pictet and I. atrispinum (Stl), and one unknown have strong and large mandibles and the antennae
Gongrocnemis species have been reported attacking are very thin and longer than the body. Adults have
coffee in Mexico and Central America; apparently, a heavy set, more or less cylindrical body, greenish,
I. subquadratum is present in Colombia too. Of brown-gray or light gray in color, with females
these, I. subquadratum is the most important katy- from 5.0 to 6.0 cm long. Males are smaller. With
did pest in coffee because very high infestations their thorny, strong and long back legs, they can
have been reported in some coffee plantations in jump. Their ability to fly is limited and in general
ElSalvador and Mexico. Most of the information their movements are clumsy. Females have an ovi-
available on katydids comes from this species. positor, from 1.0 to 2.3 cm long, at the tip of the
abdomen, which looks like a spur or a knife point.

Damage and Economic Importance

Biology and Ecology
Attacked coffee leaves show irregular holes mar-
ginally and centrally; feeding can also be observed Idiarthron subquadratum is arboreal, polyphagous,
on the tender buds, shoots and branch tips. A char- and nocturnally active. Both nymphs and adults
acteristic symptom of katydid damage is the leave their daytime shelters at night and disperse
appearance of green and ripe fruits with damaged by jumping between tree and bush canopies. They
pulp, so that the coffee beans are exposed. The hide in shady places, such as dead leaves, rotten
damage is caused by both the nymphs and adults. trunks and weeds; in particular, they take refuge in
In coffee plantations where heavy attacks of I. sub- plants of wind-breaks, izote (Yucca guatemalensis
quadratum occur, complete destruction of leaves, Baker) barriers, banana plants (Musa spp.) and
buds and small branches, the fall of tender fruits Sanseviera sp. This species feeds on leaves and
and the destruction of fruits can be observed. In fruits of several plants, including coffee (Coffea
general, I. subquadratum is not an economically spp.), banana (Musa spp.), orange (Citrus spp.),
important problem in coffee, although it some- chayote [Sechium edule (Jacq.) Swartz], and pacaya
times may create some concern in certain areas of (Chamaedorea sp.). Mating occurs in plant cano-
Central America and Mexico. In southeastern pies at night or in daytime shelters. Adult females
Mexico (Siltepec, C hiapas), the most critical attack place their eggs in the soil and, in some cases,
period is from June through November. Damage is under the bark. The eggs are placed in a mass
more important in very shaded and abandoned (from 5 to 50), and one female may lay several
coffee plantations. In addition to direct damage hundred. In Siltepec, Chiapas, Mexico, mating
caused by I. subquadratum, plant pathogenic usually occurs in October, and oviposition occurs
 Coffee Pests and their Management
C 991

in November and December. Adults are killed by the insects are killed manually and/or used as food
low temperatures in January and February, and for domestic animals (e.g., chickens and dogs).
eggs undergo diapause. At the beginning of the
rainy season, between May and June, nymphs
emerge and start to feed on coffee plants. Genera- Biological Control
tions are overlapping in warmer regions. The life
cycle from egg to adult is about 80 days at 28C. In Some strains of B. bassiana kill nymphs in the lab-
El Salvador, this pest is especially common in high oratory. However, the use of this biocontrol agent
altitude coffee plantations. has not been attempted in field.

Natural Enemies Chemical Control

Birds, spiders, parasitic nematodes and an unknown When infestations are heavy, the application of
tachinid fly species (Diptera: Tachinidae) have chemical insecticides at the places of refuge is recom-
been reported in Mexico. mended. Toxic baits placed inside the bamboo traps
are also recommended. The most convenient period
for chemical control is 1 month after the beginning of
Management rainfall and before oviposition takes place. Because
high infestations of the pest have been related to low
Sampling populations of natural enemies, insecticide use should
be avoided in order to conserve natural control.
Shelter traps made with a 10-cm-diameter by
30-cm-long bamboo (Bambusa vulgaris Schrad.)
internode closed at one end, can be used for sam-
Bush Crickets, Paroecanthus spp.
pling I. subquadratum. The bamboo traps are
(Orthoptera: Gryllidae)
placed on coffee bushes upon the first rainfall
events, and during daytime are checked every
Distribution
week for captured insects.
Bush crickets appear sporadically, affecting coffee
Cultural Control plants and shade trees in coffee plantations in some
areas of Central America and Mexico. The reported
Weed control should be applied. The shade should species are Paroecanthus guatemalae Saussure
be regulated. Trash and rotten trunks in the coffee (Guatemala, Honduras) and P. niger Saussure (El
plantation should be prevented. Dry banana and Salvador, Guatemala). The Paroecanthus species
plantain leaves should be eliminated. in Mexico remains unknown. Recently, high infes-
tations of bush crickets have been reported in
Honduras.
Mechanical Control

Bamboo traps as described earlier for sampling Damage and Economic Importance
can be used for elimination of I. subquadratum.
The traps are placed in dark spots of the plantation Paroecanthus spp. attack lignified stems and
and in the vicinity of the plants that are normally branches of coffee bushes and shade trees. The
used as refuge. The traps are checked weekly and affected plants show small marks or holes, 3.0 mm
992
C Coffee Pests and their Management

in diameter by 1.0 mm in depth, distributed in line coffee plant. Three or four generations appear
throughout the affected stems and branches. This per year. The attacks are more severe in unshaded
mark along the stem gives it the appearance of a coffee plantations. In Honduras, acute infestations
flute; hence this damage is known as flute disease. have been reported in the dry season in plantations
If the stem or branch bark is lifted right below each located between 900 and 1,250 m above sea level.
hole, an X shaped scar on the wood may be
observed. The damage is caused when the adult
female of the cricket lays its eggs. Heavy attacks of Natural Enemies
the bush cricket (when there are many holes), may
cause physiological disorders in the coffee plant, An egg parasitoid wasp, Acmopolynema sp.
which affects its development. The cricket can be a (Hymenoptera: Mymaridae), has been reported in
pathogen vector, or perhaps the lesions may favor Honduras and Mexico.
the penetration of diseases. A severe infestation can
kill the coffee plant. In Honduras, where high infes-
Management
tations have been reported, the affected plants
develop a yellowish color and they lose leaves and
Sampling
fruits.
Scouting should be conducted to determine the
Description limits of the infestation during the dry season. Upon
detection of damage, the trunk bark should be
The egg is white with elongated shape (1.0 by scratched in search of the insects eggs. If the damage
5.0mm). Nymphs are similar to adults, but their is recent, the perforations are white and unhatched
wings are not well developed and they are smaller eggs shall be observed; if the damage is old, the
than adults. The adult has a cylindrically shaped perforations are dark and the eggs have hatched.
body and is 2.02.5 cm long. The legs are yellowish
in color and the abdomen is dark brown. The Cultural Control
antennae are filiform and their length is almost
twice the size of the body. In the female, the wings Weeds should be controlled within and on the
do not cover all of the abdomen, which at its tip edges of the plantation. Severely damaged plants
shows the cerci and a long pin-shaped ovipositor. should be re-planted, or pruned of the affected
stems, and burned thereafter to eliminate the eggs.
Biology and Ecology

The bush cricket is active at night, while during Biological Control

daytime it takes refuge in dark places in the weeds,
dead leaves and some plants such as bananas (Musa This has not been attempted.
spp.) and izotes (Y. guatemalensis). Only on cloudy
days and when it is very abundant can it be seen
during the day. The female lays about eight eggs in Chemical Control
each oviposition hole, distributing two on each end
of the scar it makes on the wood, in an X shape. In plantations that are close to the affected planta-
The nymphs emerge in about 3 weeks, and they go tions, a preventive insecticide application with a brush
through several molts for 3 months before becom- or a manual pump is recommended, treating from
ing adults. Nymphs and adults can feed from the the stem base up to 60.0 cm high. Application may be
 Coffee Pests and their Management
C 993

repeated once or twice every 20 days. Also, an insecti- species, such as Phobetron hipparchia (Cramer), Sib-
cidal dust can be directed to the main stem, to the soil, ine spp., Olceclostera moresca (Schaus), Megalopyge
and to the plantation edges during the dry season. lanata (Stoll & Cramer) and Automeris sp., among
others, have urticating hairs which cause painful
lesions to anyone touching them. Measuringworms,
Leaf-Eating Caterpillars which are active nocturnally, possess camouflage
(Lepidoptera) which allows them to go unnoticed during the day.
In general, the pupation takes place in the soil. In
Distribution Ecuador, Automeris sp. and Eacles masoni Schaus
appear cyclically during the rainy season. The adults
There is a large and diverse group of leaf-eating or moths have nocturnal habits. Insecticide abuse
caterpillar species in tropical American countries and climatological changes can affect the natural
affecting coffee. The principal leaf-eating caterpil- enemies of leaf-eating caterpillars, so their popula-
lars are shown in Table 17. tions may increase and become damaging.

Damage and Economic Importance Natural Enemies

Coffee bushes affected by leaf-eating caterpillars There are many natural enemies of leaf-eating cat-
show totally or partially consumed leaves. Some- erpillars.Among them,birds,parasitic Hymenoptera
times the fruits are also affected. Eventually, and Diptera, and fungal, bacterial and viral dis-
voracious worms or caterpillar larvae, as well as, eases are notable.
their feces, can be observed. Some of these are
urticating caterpillars. These insects are frequently
mentioned in the coffee pest manuals of South Management
American countries, such as Brazil and Colombia.
Some species even defoliate entire sections of Sampling
the coffee plantation.
Regular inspection of the coffee plantation should
be made to detect initial infestation sources.
Description

As example of leaf-eating caterpillars, Oxidia sp. Mechanical Control

(Geometridae), is described. When small, they are
black, and when large, they are light gray. These The larvae of urticating worms should be elimi-
caterpillars attain a length of 5.06.0 cm. The lar- nated manually using gloves. In the case of mea-
vae are called inchworms or measuringworms. suringworms, the same can be done, but at night.
Adults should be eliminated with light traps.

Biology and Ecology

Biological Control
Adults lay their eggs individually or in groups on the
foliage of various plants. The larvae or worm feeds Bacillus thuringiensis Berliner can be used, partic-
on the foliage. The caterpillar goes through several ularly at the beginning of infestations when the
molts, and as it grows, feeds itself voraciously. Some caterpillars are small.
994
C Coffee Pests and their Management

Chemical Control Biology and Ecology

Some organophosphates and pyrethroids are Adults feed from the foliage of coffee and other
recommended. In general, the use of chemical plants. A distinctive characteristic of these weevils
insecticides is not necessary, because the natural is that when they feel threatened they contract
enemies provide regulation of the populations of their legs and snout and let themselves fall to the
these leaf-eating caterpillars. Thus, it is important to ground where they seemingly disappear. Their
preserve the natural enemies, and use insecticides eggs are laid in the soil and the larvae lead a sub-
only in extreme cases. terranean life (between 10.0 and 20.0 cm deep),
feeding from weed roots, including the coffee plant
root. The weevil populations are higher from June
Leaf Weevils (Coleoptera: through August in Honduras. In Brazil, Pantomo-
Curculionidae) rus leucoloma (Boheman) is more frequent in
the summer and it attacks both C. arabica and
Distribution C. canephora. In Honduras, the most frequent
attacks appear in the highest altitude areas. Very
Various leaf weevils are present in coffee planta- weedy areas favor infestation.
tions in tropical America (Table17).

Natural Enemies
Damage and Economic Importance Predation by assassin bugs (Hemiptera: Reduvii-
dae) is reported in Costa Rica.
Leaf weevils attack the coffee bush leaves. The
leaves show irregular holes, tearing and notches
on their edges, often beginning at the tip and from
Management
the edge towards the vein. The most affected parts
are new leaves and shoots. The damage is caused
Sampling
by the adults, which feed on the coffee foliage. The
attack of these weevils can become important
Tender buds and new leaves of the coffee plants
when they affect the buds of recently pruned plants
should be checked. When the damage only appears
and of trees <1 year old. The lesions caused by
on old leaves and not new ones, no control mea-
this pest on the leaves may favor the infection of
sure should be initiated.
P. costarricensis.

Cultural Control
Description
Weeding should not be complete, so that adult and
Larvae are whitish and legless. The color of adults larvae weevils have a feeding source and abstain
varies according to the species, being off-white from attacking the coffee plants.
(Compsus sp.), light brown with yellow spots
(Macrostylus sp.), grayish, light brown or black
(Epicaerus capetilensis Sharp.) or green. Their size Biological Control
varies from 9.0 to 13.0 mm. The snout is fairly well
developed in these insects. It has not been attempted.
 Coffee Pests and their Management
C 995

Chemical Control 5.0 to 7.0 mm. They have about five molts. Pupal
size varies from 3.0 to 4.0 mm. The adult is oval,
When the populations are large, applications of with an arched body, covered by hairs and with a
insecticides to the foliage and then to the soil are length of 2.54.5 mm. The head has round promi-
recommended. nent eyes, with a short, wide, curved-downwards
snout and the mouthparts distally.

Coffee Bean Weevil, Araecerus

fasciculatus (De Geer) (Coleoptera: Biology and Ecology
Anthribidae)
Adult females lay eggs on the parchment coffee
Distribution grooves, placing one per grain and approximately
three per day. The average number of eggs laid is
Present in all coffee growing countries in America. 52. Larvae create galleries in the seed, and they
pupate there also. The life cycle, from egg to adult,
is 3540 days. Between 55 and 74% of the descen-
Damage and Economic Importance dants are composed of females. Infestation is more
acute on softened coffee beans. Up to ten genera-
Araecerus fasciculatus attacks stored coffee beans. tions are reported per year.
Coffee beans stored in warehouses, coffee mills and
other places used to gather the harvest will show per-
forations and irregular and relatively large galleries
caused by this weevil. Accumulation of a fine
Natural enemies
yellowish powder is also observed. Highly infested
In Colombia, the following natural enemies of
warehouses will have a large number of little beetles,
A. fasciculatus have been reported: Anisep-
+the walls, roofs and windows. This weevil, which
toromalus calanadrae (Howard) (Hymenoptera:
attacks a wide variety of grain in storage, is considered
Pteromalidae), Cephalonomia gallicola (Ash-
as one of the few economically important pests of
mead) (Hymenoptera: Bethylidae), Cheyletus sp.
stored coffee in the American countries, particularly
(Acari: Cheyletidae) and Monieziella sp. (Acari:
in South America. It creates problems in warehouses
Tyroglyphidae).
that store poorly processed coffee containing more
than 12% humidity. The damage is caused by the
weevil larvae, which live in and feed on the grains.
The attack is also favored when the warehouse tem-
Management
perature is higher than 27C and relative humidity is
above 60%. In 6 months of infestation, losses of 30%
Sampling
have been estimated. C. arabica apparently is more
Fortnight visits should be made to the storehouses
susceptible than C. canephora. The fruits that remain
to check the presence of weevils, particularly in the
on the plant after harvest may also be attacked.
wet season and in places with very humid weather.

Description
Cultural Control
The larva is without legs, white, with a C shaped
body and a relatively wide thorax. The head is Adequate fertilizing, harvesting and pulp extrac-
small, light brown in color. They measure from tion should be conducted. Coffee should be stored
996
C Coffee Pests and their Management

with adequate humidity. Warehouses and storage a magnifying glass, little animals moving on the leave
places should be kept clean. Infested lots should be can be observed, and in general, silky threads which
set aside and placed in the sunlight. retain dust and other residues. The damage, which
consists of the destruction of superficial cells of the
leaf, is caused by immature and adult mites when they
Bilogical Control feed. Spider mites may be especially important in
some areas of tropical American countries during
It is not conducted. abnormally dry weather. In severe attacks the leaf
functions are interrupted and they may drop. Leaf
defoliation and yield decreases may occur when more
Chemical Control than 30 mites per leaf are present, particularly under
dry weather conditions. The economic importance of
In the case of preventive treatments and the treat- some species of mites on coffee, for example, Polyphag-
ment of infested lots, fumigation is recommended. otarsonemus latus (Banks) (Acari: Tarsonemidae) in
After fumigation, spraying of a 3-month residual Brazil, is unknown.
effect pyrethroid with motorized equipment is
recommended. The preventive treatment should
be conducted when there are 12 weevils/m2 of Description
sacks. Treatment of the walls, floor and roof of the
warehouse where the coffee is going to be stored is The egg is elliptic or spherical, bright orange, red-
also recommended. dish or red in color, depending on the species. Its
length varies from 0.100 to 0.127 mm. The larva
has three pairs of legs, an almost circular body,
Spider Mites (Acari) and according to the species, orange or yellow col-
ored when hatching, turning green-yellowish as
Distribution they feed. They are from 0.15 to 0.16 mm long.
Nymphs (protonymph and deutonymph) have
At least, six spider mite species have been four pairs of legs, and they are ovoid and about
recorded in coffee in tropical America (Table17). 0.20 mm long. In the deutonymph, which is larger,
Olygonychus (Acari: Tetranychidae) is the most females (0.200.26 mm) can be differentiated from
representative genus. males (0.180.23 mm). Adult females are larger
(0.280.50 mm) and more oval than the males
(0.250.35 mm). Color varies according to the
Damage and Economic Importance species and the sex; however, colors such as red
and orange are blended, and in some cases the
Spider mites attack coffee foliage in all their stages of mites have spots. The broad mite, P. latus, has a
development. Attacked plants present yellowish, white-milky color and it is smaller than the other
brown or copper colored leaves, with more undulated species (0.150.20 mm).
edges. Sometimes the attacked leaves may dry up and
fall. Also, the leaves lose their shine and present a dirty
appearance. The symptoms take place in large patches Biology and Ecology
in the coffee plantation, and more frequently in old,
poorly attended coffee plantations, and near the roads. Adult females reproduce sexually and parthenoge-
These symptoms are easily recognized at a distance. netically. The eggs are laid one by one, preferentially
Upon examination of the upper face of the leave with on the upper face of leaves, close to the veins,
 Coffee Pests and their Management
C 997

although P. latus, unlike the others, prefers the determined by making parallel inspection routes
lower side of the leaves. The eggs may be fixed to 25 m apart from each other, and examining 24
the leaf with the silk threads (cobweb) produced by leaves at random from four coffee plants every 25 m.
the mites and which serves for protection and for
moving from one leaf to another. Unlike the Tet-
Cultural Control
ranychidae, Tenuipalpidae (Brivipalpus sp.) do not
produce silky threads. Egg laying, in the case of
Shade trees should be planted in very sunlit areas.
Olygonychus coffeae (Nietner), occurs at a rate of
Weed control should be conducted. Adequate fer-
46 eggs/day/female for 2 or 3 weeks. Upon eclo-
tilizing should be applied.
sion, the larvae feed from cells that they puncture
with their chelicerae, and in time they become prot-
onymphs and the latter become deutonymphs. At Biological Control
the end of their development, both protonymphs
and deutonymphs go through an inactive stage Not applied.
called quiescence. An accumulation of various
residual materials such as dust and the old exuviae
of spider mites can be observed in the cobweb pro- Chemical Control
ducing species. The egg to adult life cycle varies
from 8 to 28 days, according to the temperature. Some pesticides have a selective action, affect-
Females mate with one or more males, and a male ing only mites, and others (non-selective) kill
may fertilize several females. Females, which are mites and insects. In case of a simultaneous
more abundant than males, disperse from one leaf attack by mites and leaf miners, non-selective
to another and from one coffee plant to another, by products are recommended. However, the over-
the use of silk threads. However, the factors that use of this practice can negatively affect the
contribute the most to dispersion are the wind, beneficial parasitoids and predators. Applica-
humans and other animals. Spider mites prefer to tions should be made only to infested areas.
colonize the sunlit coffee plants and the older leaves, Various pesticides are recommended, making
although in severe infestations they also attack the one application and sometimes a second one. A
young leaves. population of 3040 spider mites per leaf in the
dry season cause defoliation, so this density
must be avoided.
Natural Enemies

Predators such as ladybirds (Coleoptera: Coccinel- References

lidae) and rove beetles (Coleoptera: Staphylinidae)
are reported. However, the literature on coffee pests Barrera JF (ed) (2002) Tres plagas del caf en Chiapas. El
is not clear about the predator species present. Colegio de la Frontera Sur. Mxico, 198 pp
Crdenas-M R, Posada-F FJ (2001) Los insectos y otros habi-
tantes de cafetales y platanales. Comit Departamental
Management de Cafeteros del Quindo. Armenia, Colombia, 250 pp
Castillo-Ponce G, Contreras-J A, Zamarripa-C A, Mndez-L I,
Vzquez-M M, HolgunM F, Fernndez-R A (1996) Tec-
Sampling nologa para la produccin de caf en Mxico. Instituto
Nacional de Investigaciones Forestales y Agropecuarias.
Mxico. 88 pp. Primera reimpresin. Folleto Tcnico
The plantation should be checked during the
Nm 8
summer or dry periods, preferably on roadsides. Coffee Industry Development Company Ltd (1986) Growing
The infestation of a coffee plantation plot is coffee in Jamaica. Jamaica, 103 pp
998
C Cold Tolerance in Insects

Garca-G A, Campos-A O, Barrera-S CA, Meoo-R JE (1998)

Manual de caficultura. Tercera edicin. Asociacin
Classification of Cold Tolerance
Nacional del Caf, Guatemala, 218 pp
Le Pelley RH (1973) Las plagas del caf. Editorial Labor, SA, Insect cold tolerance classifications have tradition-
Barcelona, 693 pp ally been divided into freezing tolerance and freeze
Matiello JB (1991) O caf. Do cultivo ao consumo. Publica-
es Globo Rural. Coleo do Agricultor. Gros. Editora
intolerant strategies. This division has been criti-
Globo, SA, Brasil, 320 pp cized in recent years by a number of investigators.
Muoz-H R (2001) Plagas insectiles del cafeto. In: Manual de The arguments for the classification scheme have
caficultura. Instituto Hondureo del Caf, Honduras, pp depended on the definitions applied to the two
115142
Pliz-S V, Mendoza-M J (1993) Plagas del cafeto. In: Manual terms, and it is how freezing tolerant and freeze
de caficultura. Estacin Experimental Pichilingue. GTZ, intolerant species have been defined that evokes the
FUNDAGRO, Quevedo, Ecuador, pp 144166 controversy. For example, in freeze tolerance, these
insects are said to be capable of withstanding ice
formation in some or nearly all parts of the body
Cold Tolerance in Insects and associated fluids. Most insects in this grouping
usually freeze at temperatures between 5 and
David Rivers 10C, though others require lower temperatures.
Loyola College in Maryland, Baltimore, MD, USA Once frozen, these species can tolerate cooling to
much lower temperatures, and upon thawing, the
Exposure to low temperatures is among the most insects recover and apparently resume normal
important abiotic factors limiting the range of development and behaviors. Some experts, how-
insects in temperate climates. The relationship ever, have contended that this example of freeze tol-
between insects and cold is dynamic, particularly erance is at the extreme end of cold tolerance and
when considering the actual temperature at the only represents insects which are most suited to
surface of the integument versus internal and/or survive low temperatures. An examination of some
ambient conditions, the length of exposure to low 6070 species of insects classified as freezing toler-
temperature, and the degree of temperature fluc- ant has led to the suggestion that there are distinct
tuation over a defined period of time (e.g., day, freeze tolerance strategies that allow insects to be
week or winter season). These issues make it chal- grouped based on supercooling points (SCPs) and
lenging to categorize insect tolerance to a specific lower lethal temperature (LLT): (i) partially freeze
set of temperatures, particularly in terms of sur- tolerant species that survive a small portion of their
vival. As poikilotherms, although some are hetero- body water converted to ice; (ii) moderately freeze
thermic under specific conditions, insects have tolerant species, if the exposure is sufficiently long,
adapted to cold environments resulting in exten- die at temperatures <10 below their SCP; (iii)
sion of locomotor and/or reproductive activity strongly freezing tolerant insect species display LLT
during low temperature exposure, enhancement of twenty degrees or more below their SCP; and (iv)
metabolic rate, and maintenance of a positive freezing tolerant species possess very low SCPs and
energy balance. The implications to many of these freeze at extremely low temperatures. Insects in this
insects are a lengthening of the life cycle and a latter group are capable of surviving at tempera-
requirement for individuals to overwinter one or tures a few degrees below their SCP.
more times. The actual mechanisms associated Insects that are not tolerant of any ice forma-
with these adaptations have received extensive tion in their bodies are generally termed freeze
study in recent years, including attempts to deci- intolerant species. The natural tendency has been
pher the underlying genetic basis of individual to assume that these insects will die if tissues or
and population responses to low temperatures and body fluids freeze, and presumably if they avoid
seasonal change. the frozen state, these insects will survive. Such
 Cold Tolerance in Insects
C 999

classification appears to be an oversimplification of insects are non-hardy since they possess no physi-
the freeze intolerant strategy, because most species ological adaptations to survive low temperatures.
of insects found in temperate regions are suscepti-
ble to injury and possibly death at non-freezing
temperatures. For these insects, the more correct Mechanisms of Cold Tolerance
terminology for their low temperature survival
strategy is freeze susceptible (avoidance). In this Cold adapted insects have developed a complex of
classification, a distinction is made between freez- strategies that allow survival at their physiological
ing and chilling, recognizing that injury and death temperature minimum. These strategies broadly
may result from low-temperature processes occur- include (i) morphological (e.g., melanism, hair/
ring at non-freezing temperatures. Even in this sys- pubescence, reduction in size, physical barriers); (ii)
tem of classification, there is further division in behavioral (migration, opportunistic exploitation,
which freeze avoiding species are distinguished parasitism); (iii) physiological (depression of SCPs,
from those insects susceptible to chilling. Freeze removal or acquisition of ice nucleators); and (iv)
avoidance is defined as both a low temperature biochemical (synthesis of antifreeze proteins and/or
survival strategy and a description of a specific cir- polyhydric alcohols) adaptations. The latter two
cumstance under which the insect will die, that is, adaptations have received considerable attention,
when it freezes. Chill tolerant species possess resulting in a fairly clear picture of the mechanisms
extensive supercooling ability and a high level of characteristically associated with freeze tolerant
cold tolerance, but is distinguished from the freeze versus freeze susceptible strategies. In freeze-tolerant
avoiding insects by displaying some mortality insects, potent ice-nucleating agents are produced or
above the SCP, which in most cases increases with acquired in the extracellular fluids, promoting a pro-
decreasing temperatures and increasing length of tective extracellular freezing at a few degrees below
exposure. Some insects are strongly influenced by zero. Polyhydroxy alcohols (polyols) and sugars
the severity of the preceding winter conditions, accumulate in extracellular fluids to cryoprotect par-
indicating that the cold tolerance of these species is tially frozen tissues. In addition, fat body and local-
not as well developed as those that seem to be inde- ized tissues synthesize antifreeze proteins that
pendent of yearly variations in winter tempera- function to inhibit secondary recrystallization of ice.
tures. These insects are referred to as chill susceptible Collectively, these adaptations sharply drop the lower
and are characterized by extensive supercooling lethal temperature to 40C or below.
that allows them to survive moderate low tempera- Other adaptations used by freeze tolerant
ture exposure (05C), but only brief exposure to insects include changes in membrane composition
temperatures below 5C can induce death. SCPs to maintain the liquid crystalline state at low tem-
are not indicators of cold temperature tolerance in peratures, a process referred to as homeoviscous
these species. The final category of cold tolerance is adaptation. These changes can occur at low temper-
termed opportunistic survival. It is used to describe atures through an increase in points of unsaturation
insects that originate in tropical or semi-tropical along phospholipids fatty acid chains. Membrane
regions, which implies that these species are defi- composition changes have also been shown to occur
cient in cold hardiness adaptations or characteris- by increasing the cholesterol content or changes in
tics, and as such, are not likely to survive at the distribution of phospholipid classes composing
temperatures below the threshold that permits plasma membranes. Changes in membrane compo-
normal metabolism. These insects may have sition are not restricted to freezing strategies and
extensive supercooling but can only survive low can occur with freeze susceptible species as well.
temperatures by opportunistic exploitation of a In contrast, freeze susceptible species gener-
favorable habitat or location. Essentially such ally attempt to remove or inactivate ice nucleators,
1000
C Cole Crops

most commonly through purging the contents of Collectors

the digestive tract. Many of these insects have the
ability to maintain a liquid state at temperatures In an aquatic community, insects that collect fine
well below the equilibrium freezing point (FP) of particles of organic matter from the water.
their body fluids through manipulation of the
colligative properties of their body fluids. This can
be achieved by increasing the solute concentration Coleophoridae
of extracellular fluids (directly or through a reduc-
tion of water mass), accumulation of cryoprotec- A family of moths (order Lepidoptera). They com-
tive polyols and sugars, and through supercooling. monly are known as casebearer moths.
Production of thermal hysteresis factors function Casebearer Moths
to stabilize the supercooled state. Some species Butterflies and Moths
also elicit a rapid cold-hardening (RCH) response
that protects insects against non-freezing (cold
shock) injury. Rapid cold-hardening is a swift Coleoptera
physiological response elicited by exposure to
mild chilling to turn on one or more of the above An order of insects. They commonly are known as
mechanisms to enhance the cold hardiness of beetles.
insects, thereby affording protection from expo- Beetles
sure to subsequent low temperature exposures.
Together, these adaptations contribute to a depres-
sion of the SCP and lower the temperatures that Collecting and Preserving Insects
promote freezing.
Diapause Paul M. Choate, J. Howard Frank
Overwintering in Insects University of Florida, Gainesville, FL, USA
Thermoregulation in Insects
Insects provide many opportunities for biologi-
cal studies, ranging from detailed research to
References casual field observations. Frequently the need
arises for collecting specimens to accurately
Bale JS (1996) Insect cold hardiness: a matter of life and death. identify the species of interest. Collecting tech-
Eur J Entomol 93:369382
Lee RE Jr, Denlinger DL (1991) Insects at low temperatures.
niques and methods of preservation of insects
Chapman & Hall, New York, 513 pp vary considerably. A few of these techniques are
Lencioni V (2004) Survival strategies of freshwater insects in described here.
cold environments. J Limnol 63:4555
Sinclair BJ (1999) Insect cold tolerance: how many kinds of
frozen? Eur J Entomol 96:157164
Zachariassen KE (1985) Physiology of cold tolerance in
insects. Physiol Rev 65:799832 Key elements to successful insect
collecting

Cole Crops Collectors frequently wish to find as many differ-

ent insects as possible. In order to accomplish this,
Crops of the family Cruciferae, such as cabbage, the greater the diversity of collection techniques
broccoli, and collard. Cole crops are also called employed and habitats explored, the greater the
crucifers. diversity of insects that will be collected.
 Collecting and Preserving Insects
C 1001

Most entomology textbooks present an over- transport them as soon as you can. If your objec-
view of collecting and preserving insects for study. tive is to kill them to obtain preserved specimens,
There are two major categories of information kill rapidly to prevent damage.
dealing with these subjects, collecting techniques
and preservation techniques (how to deal with the
insects once collected). Killing Methods

Large specimens typically are killed in a jar with a

Collecting Techniques closely fitting lid using a volatile toxicant such as
ethyl acetate absorbed onto plaster or sawdust or
Collecting techniques are limited only by the cotton. Small specimens may be killed in vials using
imagination of the student or researcher. Practi- the same toxicant. Alternatively, if they will not be
cally any technique will yield a few insects. Here damaged by immersion in liquid, they may be killed
are a few: in 70% alcohol or soapy water. Freezing (several
hours) also is an option, though it may result in
Hand-collecting, turning over logs and rocks and other certain deformities.
objects
Unbaited pitfall traps
Pitfall traps baited with carrion, dung, yeast, or fermen- Recording
ted fruits
Hand-collecting, or use of sweep nets, beating trays, as- Vials or other containers should be labeled in the
pirators field as the specimens are collected. Never use a
Cutting sections of plants to place into containers within ball-point pen for insect labels; if you do not have
which the insects will later emerge, breaking logs a pen with India ink available in the field, make a
apart with an ax or chisel, stripping bark of dead temporary label with pencil. Record at least all the
trees to find subcortical insects information you may eventually need (see section
Hand-held nets below on Labeling specimens).
Passive intercept traps: Malaise and window traps
Attractant traps with mercury-vapor or ultraviolet
light, or carbon dioxide, or specific insect phero- Preserving Insects
mones as bait
For Subterranean Insects Small and soft-bodied insects should be stored in
Sifting soil or debris with a sieve 70% alcohol (either ethanol or isopropanol) in tightly
Placing debris into a Berlese or Tullgren funnel to extract sealed glass vials. Isopropanol (rubbing alcohol) is
insects by heat, or light, or a chemical repellent inexpensive and readily obtained in most countries.
Aquatic nets Ethanol may be subject to excise laws because it may
be used for human consumption, so typically is more
expensive and more difficult to obtain, and there
Living Insects seems to be no point in going to that trouble if
isopropanol can be obtained.A label should be placed
If your objective is to collect insects alive for study in the vial, with information printed or written in
alive, then your best option to prevent damage is insoluble ink. An additional label may be taped to the
to chill them as soon as they are collected. To do outside of the vial. Insect larvae may need brief inser-
this, place them into suitable containers in an tion in boiling water before they are preserved in
insulated chest with ice or other refrigerant, and alcohol, without which they will blacken.
1002
C Collecting and Preserving Insects

Vials

These are available in many shapes and sizes.

Plastic vials are useful in the field because they
are less subject to breakage than are glass vials,
but glass vials are very much preferable for long-
term storage. When specimens are stored in alco-
hol in vials, be aware that the type of vial and
type of stopper is important. Straight-sided glass
vials (shell vials) are thinner-walled and more
fragile than other types. Vials stoppered with
screw-caps or corks will sooner or later allow the
liquid contents to evaporate. Thick-walled glass
vials with necks (homeopathic vials), when fit-
ted with natural rubber stoppers, seem to offer Collecting and Preserving Insects, Figure 75
the greatest permanence, but the rubber will Spreading board used to prepare moths and
eventually crack and decompose. Stoppers of butterflies.
neoprene or other synthetic materials have not yet
shown an advantage over natural rubber. If using increasing in thickness with increase in numeri-
homeopathic vials with rubber or neoprene stop- cal value. Extremely narrow pins are of size 00,
pers, it is important to seat the stopper firmly; and extremely thick pins are of sizes 47 but are
this may be done by inserting a straightened-out longer. Most insects large enough to be pinned
steel paper clip alongside the stopper as the latter may be pinned on sizes 2 or 3. Insects are pinned
is inserted, then withdrawing the paper clip to in specific locations depending on their classifica-
release trapped air. All vials should be checked tion. Large beetles are pinned in the middle of
periodically for leakage and loss of preservative. their right wing cover, close to the front margin.
Other examples of pin positions are included in
the diagrams provided in the accompanying fig-
Mounting Techniques ures. (In the United Kingdom, white brass pins
once were used; their length varied with width).
Different insects require different mounting tech- Minuten pins (from a German adjective meaning
niques. Large moths and butterflies and some minute) are very small, fine pins used for pinning
other winged insects are mounted with wings tiny insects into a small block of pinning mate-
neatly (Fig.75) spread on a spreading board. rial, which is in turn pinned by a standard pin.

Pinning Storage in Transparent Envelopes

Insects of average size usually are mounted on Some Odonatologists (dragonfly collectors) stuff
pins. In many countries, steel pins of 3.5 cm length their specimens into semi-transparent (Glassine)
are used; the best quality is stainless steel with envelopes. This is an alternative to pinning (Fig.76)
nylon heads. Lacquered steel pins may rust, and specimens, saving much museum space. However,
brass pins may corrode (become covered with this is not necessarily the most desirable method
green verdigris) in humid climates. Pin widths are of storage because the specimens are prone to
numerically designated, with standard sizes 03 breakage.
 Collecting and Preserving Insects
C 1003

Collecting and Preserving Insects, Figure 76 Position of pins in various kinds of insects.

Pointing

Insects too small to be pinned safely may be

mounted on cardboard points, glued to the point
on their right side. Points should be bent down
slightly to better attach to the side of each speci-
men. Such points may be purchased, or may be
made by a hand-held device called a point press,
which cuts points (Fig.77) from a sheet of card-
board. Care should be taken not to cover the
underside of the insect with glue, obscuring key
characters. This is the standard mounting tech-
nique in the USA, and it is claimed to be better
because underside characters are visible. However, Collecting and Preserving Insects, Figure 77
there are two major problems: (i) insects thus Examples of how to position mounting point
mounted are very susceptible to physical damage, under right side of insect specimen.
1004
C Collecting and Preserving Insects

and (ii) adhesives used to obtain secure adhesion (2) It is said that such a method of preparation is more
to the small surface may be soluble only in harsh time-consuming. This may be true, but it varies
solvents (benzene, toluene, xylene, acetone, etc.). with the expertise of the preparator. More impor-
Subsequent attempts to dissect soft body tissues tantly, if the specimen is rare and from a distant
are thwarted because these are destroyed. locality, it makes far more sense to spend a few
seconds more to prepare it this way (better-protected)

Card Mounts

Some groups of insects are better mounted on tiny

(Figs.7880) rectangular cards. Cards of standard
sizes are sold by some supply houses. This tech-
nique is popular with European entomologists. It
is claimed to be better because the specimens are
better-protected from physical damage and
because they may be viewed in one plane against
the white background of the card (as contrasted
with specimens that may be drooped over card
points), and because they may later be removed
easily for dissection. Only water-soluble adhesives
should be used. There are perhaps two problems:

(1) The underside characters are not visible without Collecting and Preserving Insects, Figure 79
removal from the card. However, preparators with Card-mounted specimen (European fashion).
a series of specimens available will mount some
dorsal side up, and some ventral side up.

Collecting and Preserving Insects, Figure 80 Large

long-legged flies such as crane flies may need to
Collecting and Preserving Insects, Figure 78 have their body supported with an extra large
Minuten pin used to position small insect above point. Alternatively, the specimen could be place on
piece of cork. This technique is frequently used for a card mount, which will offer much more
delicate flies and very small moths and butterflies. protection from damage by protecting the legs, too.
 Collecting and Preserving Insects
C 1005

than to face the days or weeks and expense nec- however, they are feebly sclerotized or too small,
essary to collect more specimen from the distant they may be mounted (after dehydration through
locality, even assuming that a replacement speci- alcohols to xylene) in a drop of Canada balsam on a
men can be found for a rare species. small celluloid rectangle pinned directly below the
specimen (no cover slip is needed). When specimens
are card-pointed, the usual method is to place them
Adhesives in genitalia vials pinned through the stopper below
the specimen. Such genitalia vials are tiny, of glass or
Many kinds of adhesives are used to secure insects plastic, and contain a cork or stopper of some syn-
to card points. The objective is to secure the insect thetic material; typically, they contain alcohol, glyc-
firmly to the point. It is recommended that only erine, or a mixture of the two. When genitalia almost
water-soluble or alcohol-soluble adhesives be fill the vial, and when such vials are checked fre-
used. When other kinds of adhesives are used, quently for leakage, the method may have merit.
there will arise questions about the necessary sol- Otherwise they can be disastrous: extremely small
vents to remove the specimens (it is virtually genitalia in a vial can be lost when the stopper is
impossible to guess what adhesive some collector pulled, or the vial can leak and desiccate the parts.
may have used and what its solvent is). For speci- Such genitalia vials are to be avoided wherever
mens adhered to card mounts, only water-soluble possible.
adhesives should be used. When card-mounting,
the strength of the adhesive is less important
because much more surface area is used. Many Slides
water-soluble adhesives are available, although
the two most commonly sold in stationery stores Some insect specimens are best mounted on
in the USA are unsuitable, one because it dries microscope slides. These include very small and
hard, cracks and turns brown, and the other soft-bodied insects as well as dissections of insect
because it is not truly transparent and dries from parts. The most permanent mountant available is
the outside inward, forming first a sticky skin. Canada balsam. Some insects (scale insects,
aphids and lice, minute parasitic Hymenoptera,
and many insect larvae) typically are prepared by
Card Mounts, Card Points, and Labels clearing and differential staining before being
mounted on microscope slides.
Use only a heavy weight, high quality, non-yellow-
ing, 100% rag card stock for making these items.
Some years ago, Bristol board, a laminated card, Soft-Bodied Specimens
was recommended. We see no advantage to such
laminated card stock. Because of their hard exoskeleton, very many insects
will maintain their shape when dead and dry. Some,
however, will not they tend to shrivel. Techniques
Genitalia have been developed for maintaining the shape of
dried specimens (one alternative was to preserve
It is often desirable to dissect specimens to make the them in alcohol, another to mount them on micro-
genitalia evident for identification purposes. With scope slides). For decades, the preferred method
card-mounted specimens, the genitalia (if large for preserving large Orthoptera (grasshoppers and
enough and well-sclerotized) may be mounted on crickets), Phasmida (stick-insects) and Mantodea
the same card as the specimen, a great advantage. If, (mantids) was to eviscerate them and stuff their
1006
C Collecting and Preserving Insects

abdomen with cotton before pinning and drying. The top label should contain (i) country, (ii) prov-
For Odonata (dragonflies and damselflies), the ince or state, etc., (iii) township, etc., (iv) route
method was to eviscerate them and stuff a tooth- information when known if the collection was a
pick-shaped object into the abdominal cavity. For result of a route followed, (v) date of collection,
larvae of butterflies and moths (caterpillars), the and (vi) collectors name(s). A second label should
method was to roll the abdominal contents out contain method of collection (bait, technique,
through the anus, then inflate the abdomen (by trap) and habitat. Dates should be written in order
blowing into it) while drying the inflated skin in a day-month-year (the international standard) with
tiny oven. Mosquitoes and some other flies, and month either in letters or in Roman numerals and
Trichoptera, having feeble exoskeletons, could not the year with four digits. For example, a date of
be dealt with by such rough physical methods the 4th of July 2002 should thus be written as
because they are covered in scales, and the scales 4-JUL-2002 or 4-VII-2002, and not as 7/04/02 (as
would be lost by such treatment; they were destined in commonly done in the USA) or as 4/7/02 (as is
to shrivel as they dried. Many of these methods have commonly done in most of the world) or as
now been abandoned because of the availability of 2002/7/4 as is commonly done in the Far East. A
critical-point drying. A critical-point drier is an third label may contain rearing information.
expensive piece of equipment and may be unavail- A fourth label may contain determination infor-
able in some institutions and to amateur collectors. mation, species name, determiner, and date of
determination.

Labeling Specimens
Pinning Blocks
Specimens without accurate and complete collec-
tion data are of little value. A proper label contains Supply houses sell blocks on which specimens
locality data, date of collection, collectors name, and labels may be pinned. These achieve a stan-
method of collection, and identification label with dard height for each specimen and label and
determiners name. Additional information may be make a resultant collection appear more uniform.
included (host plant, behavior, etc.). Computer- Unfortunately, we have not seen a block from a
generated laser-printed labels in general seem supply house with more than three steps. If the
entirely adequate. Such labels with a font size of 3 steps are (i) specimen, (ii) dissections of genitalia
or 4 are suitable for pinned specimens. Labels with from the specimen, (iii) locality information,
larger font (10 or 12) can be used in vials with alco- (iv) habitat information, and (v) identification
hol. Most laser-printer inks seem stable in alcohol information, then five steps are needed. The only
(you may want to test labels made with the laser current option seems to be for collectors to man-
printer available to you before relying upon them), ufacture their own pinning blocks (one of us has
and printed labels are far easier to read than are done so).
most hand-written labels, Use them wherever you
can for pinned and alcohol-preserved specimens
(provided that the ink is not alcohol-soluble). Storing Collections

Insect collections require protection from atmo-

Information on Labels spheric conditions such as humidity and pests
capable of destroying specimens. Such pests
Labels for pinned insects should be placed beneath include cockroaches, silverfish, ants, dermestid
specimens, aligned parallel with the insects body. and anobiid beetles, booklice, and mice. Tight
 Collecting and Preserving Insects
C 1007

containers, with a fumigant, will deter most pests. Supply Houses

Be sure not to use chemicals toxic to humans or
pets. The safest method is to store in or donate a Several companies maintain an inventory of ento-
collection to a recognized museum where it will mological supplies and sell by mail order. They
be maintained safely. Museum curators often will sell nets, beating sheets, light traps, vials, pins,
provide space for your materials, hoping that at forceps, lenses, pinning blocks, storage boxes,
some time in the future you will donate your col- cabinets, microscopes, microscope illuminators,
lection to them. microscope slides, preservatives, light traps, nume-
rous other items, and assorted entomological
literature.
Storage Containers and Cabinets

Insect specimens are typically housed in wooden Permits

storage boxes (in the USA called Schmit or
Schmitt or Schmidt boxes) or in cabinets with A very few species of insects have been declared
drawers. The storage boxes have tightly-fitting to be endangered species. They may not be col-
lids, and the floor is lined with a material into lected, even on your own property, without a very
which pins can easily be thrust. Traditionally, hard-to-obtain permit. In many countries, you
this material was cork, usually lined with paper, may collect any other insect (apart from endan-
but now is normally some white synthetic foam. gered species) on your own property, or (with
European cabinets were and are of numerous permission from the landowner) on someone
sizes, each drawer lined with a pinning material. elses property. If the landowner is a government
The disadvantage of the European system is that agency and the property is a park or preserve, you
dozens or hundreds of specimens may have to be may need a written permit from that agency. In a
moved one by one to make way for a few new few countries you may not collect insects of any
specimens. Additionally, drawers of some cabi- kind without a government permit; even if you
nets are exceptionally shallow, allowing vertical use a pesticide to kill pests on your property, and
space only for short pins. In the USA, another along with the pests you kill harmless or benefi-
system arose in which drawers of standard size cial insects, you may not collect any of these
were designed to accept a standard number of insects without a permit. So, be aware of the laws
cardboard unit trays, the unit trays (not the in your country.
drawers themselves) are lined with a pinning
material, and all drawers accept standard 3.5 cm
pins. Unit trays are manufactured in a range of
References
complementary sizes so that a combination of
Hatch M (1926) Concerning the insect collection. Entomol
small and large trays, as need arises, will fit pre- News 37:329332
cisely into a drawer. The trays make it easy to Lehker GE, Deay HO (1969) How to collect, preserve, and
move groups of specimens about a drawer or identify insects. Extension circular 509. Cooperative
from drawer to drawer, and protect specimens Extension Service, Purdue University, Lafayette, IA,
43 pp
from physical damage. The US system was a Ross HH (1962) How to collect and preserve insects. Illinois
good idea, but, unfortunately, the system is at State Natural History Survey Circular 39, Urbana, IL,
least three systems, not one, and developed at 71 pp
Smart J (1954) Instructions for collectors. No 4A Insects. Brit-
competing museums, which differ in dimensions
ish Museum (Natural History), London, UK, 178 pp
of drawers and size of unit trays so that they are Steyskal GC, Murphy WL, Hoover EM (eds) (1986) Insects and
not interchangeable. mites: techniques for collection and preservation. US
1008
C Collembola

Department of Agriculture, Miscellaneous Publication No Colonization

1443, Washington, DC, 103 pp. Available Online at http://
www.sel.barc.usda.gov/Selhome/collpres/contents.htm
The introduction and establishment of a species,
usually a beneficial insect, in a new geographic
Collembola area or habitat.

An order of hexapods in the class Entognatha,

and sometimes considered to be insects. They Colony
commonly are called springtails.
Springtails A group of individuals, other than a mated pair,
which rears offspring in a cooperative manner, and
may construct a nest. (contrast with aggregation)
Colleterial Glands
Female insects commonly secrete glue that Colony Fission
attaches the egg to a substrate. Also secreted in
some cases are jelly-like materials, oothecae, or pods Among social insects, the same as budding: multi-
containing the individual eggs. The glands that plication of colonies by the departure from the
secrete these are known by various names, including parental nest of one or more reproductive forms
accessory, mucous, cement, and colleterial glands. accompanied by workers. Thus, the parental nest
remains functional and new ones are founded.

Colletidae
Colony Odor
A family of bees (order Hymenoptera, superfamily
Apoidae). They commonly are known as plasterer The odor specific to a particular colony. This odor
bees and yellow-faced bees. allows social insects to identify their nestmates
Wasps, Ants, Bees and Sawflies among others of the same species.
Bees Social Insect Pheromones

Collophore
Colorado Potato Beetle,
A tube-like structure located ventrally on the first Leptinotarsa decemlineata (Say)
abdominal segment of springtails (Collembola). (Coleoptera: Chrysomelidae)

Donald C. Weber
Colobathristidae USDA Agricultural Research Service, Beltsville,
MD, USA
A family of bugs (order Hemiptera, suborder
Pentamorpha). Colorado potato beetle is the most important
Bugs insect pest of potatoes in the northern hemisphere.
Larvae and adults feed on potato foliage, and
Coloburiscidae under many agricultural conditions the pest will
completely defoliate the crop if not controlled. It is
A family of mayflies (order Ephemeroptera). also a major pest of eggplant (aubergine) and
Mayflies tomato in some regions, as well as feeding on
 Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae)
C 1009

solanaceous weeds such as horsenettle, Solanum photoperiod, and availability and quality of host
carolinense. Although it is occasionally found on plants. In the spring, overwintered adults emerge
other nightshade crops such as peppers (Capsi- from the soil and begin their search for host plants
cum), tobacco, and husk tomato (Physalis), it can- to feed upon. This commences with walking, but
not complete its life-cycle on these hosts. after a few days beetles may take to flight. The yel-
The original range of Colorado potato beetle low-orange eggs, laid on leaf undersides in masses
was probably restricted to southwestern USA and/ of 2060 (several hundred to a few thousand total
or northern Mexico, where the host plants were per female), soon hatch into leaf-feeding larvae
the spiny nightshade herbs Solanum rostratum which eat about 40 cm2 of foliage. The fourth instar
(buffalobur) and Solanum elaeagnifolium (silver- larva drops to the ground and digs down a few cm
leaf nightshade). The species was described in to pupate in the soil, emerging 1020 days later as a
1824, but the first occurrence on potato was not callow adult. Also a voracious leaf feeder, the imago
reported until 1859 in Nebraska. From there it consumes up to 10 cm2 per day. Depending on food,
spread rapidly, especially eastward, reaching the photoperiod, and temperature, this young adult
Atlantic coast of North America in 1874. By then may mate and reproduce, or after feeding, bury
the potato crop was a staple food, and the spread itself 1050 cm deep in the soil to spend months in
of Colorado potato beetle infestation prompted diapause before emerging the next spring.
early development of arsenical pesticides and In areas where tomatoes abound, it has
application methods in the USA. evolved an improved fitness on this plant, as in the
In 1870, responding in part to the threat of southeastern USA and Uzbekistan. Even where it
Colorado potato beetle introduction, Germany does not thrive on tomato, large numbers may
established the first-ever quarantine law followed damage this valuable crop. In contrast, potato
within several years by other European countries. plants can tolerate light to moderate defoliation at
Following the eradication of numerous isolated certain times of year, but without control, major to
European introductions, its establishment into complete crop loss is common. A typical economic
France in 1921 initiated another rapid geographic threshold is one adult equivalent per plant, where
invasion which now includes all of Europe (except small larvae are counted as equivalent to 1/4 of
for the United Kingdom, Ireland, and Scandina- one adult, and large larvae (3rd and 4th instars)
via), continues through central Asia eastward into equate to 2/3 of an adult. Yield impact is depen-
China, and threatens to spread into east and south dent on timing, variety, and other crop stresses.
Asia, where one-third of the worlds potatoes are In early years, control relied on hand-picking,
grown. The range is now about 8 million km2 in but this gave way to arsenical insecticides and in
North America and a like area in Eurasia. Climati- the 1940s the more powerful synthetic chemical
cally favorable areas not yet infested include east controls. No other agricultural pest better exempli-
Asia, parts of south Asia temperate South America fies evolution of resistance to insecticides. Within
and Africa, Australia and New Zealand. the first decade of DDT use, it was failing against
Colorado potato beetle adults are approxi- Colorado potato beetle in the intensive potato-
mately 10 mm long, convex, with cream-yellow and growing region of Long Island, New York, USA.
black striped elytra, and variable black markings Resistance followed to numerous other chlorinated
(Fig. 81) in the pronotum. Larvae are typically hydrocarbons, organophosphates, carbamates, and
orange with two rows of black lateral spots, and as pyrethroids. This sustained evolution of pesticide
later instars are characteristically hump-backed resistance has prompted development and use of
in shape. Colorado potato beetle overwinters as additional novel chemical controls such as neoni-
the adult in the soil, and has from one to several cotinoids and ecdysteroids, as well as transgenic
generations per year, depending on temperature, crops incorporating high levels of beetle-specific
1010
C Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae)

Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), Figure 81

Colorado potato beetle (a) egg mass, (b) larvae, (c) pupa and (d) adult. (Egg mass photo by D. Weber;
others by Doro Rthlisberger, Zoological Museum, University of Zurich.)
 Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae)
C 1011

Cry3A BT toxins (derived from Bacillus thuringi- threshold, but not reliably in most current crop-
ensis). Transgenic potatoes were developed and ping systems. Predatory stink bugs (Podisus and
introduced as the cultivar Newleaf in the 1990s, Perillus) as well as several species of generalist
later also incorporating resistance to important Coccinellidae and Carabidae, spiders and harvest-
aphid-transmitted potato viruses. Yet this highly men are common predators. During the 1980s, the
effective tactic met with a mixed and then negative egg parasitoid wasp Edovum puttleri was intro-
reception, first because it was introduced con- duced to the USA from Colombia (where it is
temporaneously with an effective and broader- native on L. undecemlineata (Stl)), and enjoyed
spectrum systemic insecticide, imidacloprid, and success as an inundative biocontrol in the high-
later because large multinational processors value eggplant crop. This parasitoid is not winter-
decided that using transgenic potatoes would risk hardy. Rearing efforts ceased with the advent of
consumer opposition across their global markets. the systemic neonicotinoid imidacloprid.
Two years after registration in the US, major buyers Two of the most promising natural enemies
announced plans to discontinue Newleaf purchases, native to North America are quite poorly studied.
and commercial sales have been discontinued. Lebia grandis is a carabid ground beetle predator of
Transgenic technology continues with limited field Colorado potato beetle eggs and larvae as an adult,
trials in eastern Europe, and may be commercialized whose larvae are ectoparasitoids of Colorado potato
in the future. One prerequisite for sustainable use, beetle pupae. The newly hatched larvae locate the
as with chemical controls, is the implementation of Colorado potato beetle host soon after it buries
resistance management plans. itself to pupate, then obtain their entire larval food
Periodic failure of chemical controls has requirement from a single host pupa, emerging
prompted research into a variety of alternatives weeks later as blue-metallic and orange, very
ranging from pedestrian to peculiar. These include mobile and hungry adult predator beetles. Two
native and introduced biological controls, crop species of tachinid parasitoid flies of the genus
rotation, cover crop mulches, trap crops, trenches Myiopharus attack larvae or in the fall even Colo-
to disrupt crop colonization, early planting, late rado potato beetle adults, where they overwinter as
planting, and multi-row propane-fueled flamers an early-instar larva inside their host, then develop
and crop vacuums. Collectively and as comple- and emerge the next season as an adult fly. Beau-
ments to chemical control, these are essential tactics veria bassiana has potential to suppress Colorado
to manage the pest and help avert resistance. potato beetle populations under some conditions,
For an insect that is the focus of thousands of and commercial formulations have been devel-
published scientific articles, there is still surprisingly oped. If the agroecosystem can somehow better
much to learn. In just the past few years, plant-based nurture natural enemies, especially early in the sea-
attractants as well as a male-produced aggregation son before Colorado potato beetle damage the
pheromone, (S)-3,7-dimethyl-2-oxo-6-octene-1,3- crop, then Colorado potato beetle management
diol, have been discovered. The exact role that these may not so frequently require costly and some-
behaviorally active substances will play in Colorado times troublesome insecticidal inputs.
potato beetle management remains to be seen, but Crop rotation is consistently an effective means
perhaps in combination with selective toxins and/or to delay and reduce colonization of overwintered
antifeedants, a push-pull behavioral strategy can adults. But in many cases, land tenure and intensive
succeed in suppressing the Colorado potato beetle culture may prevent farmers from rotating the
instead of whole-field treatments which have his- several hundred meters which constitute an effective
torically failed due to selection of resistance. separation in successive years. Yet even unrotated
Natural enemies of Colorado potato beetle crops are amenable to border treatments, trap crops
may sometimes keep the pest below economic or trenches to thwart beetle colonization, because
1012
C Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae)

many adults overwinter in wooded or other non- Siberia, it buries deeply over winter, while in milder
crop areas adjacent to crop fields. Physical controls areas, it buries less deeply. Some beetles delay
of flaming and vacuuming have enjoyed limited emergence from diapause for years at a time.
success against the pest. Rye straw or other killed Researchers express both reverence and frustra-
cover crops suppress Colorado potato beetle popu- tion at the variability in its behavior.
lations, probably by a combination of abiotic and Just why is the Colorado potato beetle so flex-
biotic effects. One novel cultural-physical control ible in responding to changing ecology and toxi-
uses late-maturing trap crops to attract beetles to cology? The reason may lie in its evolutionary
concentrated overwintering areas which are then history of genetic and biochemical diversity in eco-
stripped of their snow and mulch covering in logical and evolutionary pursuit of toxicologically
midwinter to enhance diapause mortality. complex and ephemeral groups of host plants. This
Colorado potato beetle is one of the most fre- beetle reinforces the need for flexible and integra-
quently used bioassay insects for toxicological and tive thinking in developing pest management strat-
physiological research, and usually the first beetle egies: one tactic alone will not quell it for long.
to be tested with candidate insecticides. It is easily Witness the latest entry, the chloronicotinyl imida-
maintained on a potato diet, hosting few diseases cloprid, starting to fail after about 10 years of inten-
in the lab, and is also amenable to semi-artificial sive use in the eastern USA. Integration of multiple
diet, which aids in precisely controlling its nutri- effective tactics will continue to be essential for an
tion. Colorado potato beetle has played a key role intelligent and sustainable approach to manage-
in development of concepts of host-plant location ment of the formidable Colorado potato beetle.
and selection, host shifts, molecular and popula- Potato Pests and Their Management
tion mechanisms of pesticide resistance, gene flow, Vegetable Pests and Their Management
and integrated pest management. There is also
active research on conventional and engineered
crop resistance, neurophysiology, dispersal behav- References
ior, biochemical and molecular reaction of host
plants to Colorado potato beetle feeding, digestive, Boiteau G, Alyokhin A, Ferro DN (2003) The Colorado potato
microbial and immunological defenses of Colo- beetle in movement. Can Entomol 135:122
Casagrande RA (1987) The Colorado potato beetle: 125 years
rado potato beetle and, of course, novel natural of mismanagement. Bull Entomol Soc Am 33:142150
and synthetic toxins and antifeedants. Chang GC, Snyder WE (2004) The relationship between preda-
Providing sustainable control options requires tor density, community composition, and field predation
of Colorado potato beetle eggs. Biol Control 31:453461
not only laboratory and molecular insights into
Dickens JC, Oliver JE, Hollister B, Davis JC, Klun JA
the mechanisms, but also ecological and behav- (2002) Breaking a paradigm: male-produced aggrega-
ioral insights, especially into the movement of tion pheromone for the Colorado potato beetle. J Exp
beetles within and between fields which could lead Biol 205:19251933
Ferro DN, Logan JA, Voss RH, Elkinton JS (1985) Colorado
to the spread or suppression of pesticide resistance potato beetle (Coleoptera: Chrysomelidae) temperature-
genes in agricultural populations. The quantifica- dependent growth and feeding rates. Environ Entomol
tion of gene flow and frequencies, which in turn 14:343348
depends on selection, dispersal and reproduction, Grapputo A, Boman S, Lindstrm L, Lyytinen A, Mappes J (2005)
The voyage of an invasive species across continents: genetic
provides the basis for rational deployment of refu- diversity of North American and European Colorado
gia in resistance management. Questions of move- potato beetle populations. Mol Ecol 14:42074219
ment are also critical to effective employment of Jermy T (1994) Hypotheses on oligophagy: how far the case
of the Colorado potato beetle supports them. In: Jolivet
crop rotation and pest colonization in a variety
PH, Cox ML, Petitpierre E (eds) Novel aspects of the
of regional cropping systems. In some areas, the biology of Chrysomelidae. Kluwer Academic Publish-
beetle flies frequently. In others, it flies rarely. In ers, Dordrecht, The Netherlands, pp 129139
 Common Stoneflies
C 1013

Hough-Goldstein JA, Heimpel GE, Bechmann HE, Mason CE Common Fleas

(1993) Arthropod natural enemies of the Colorado
potato beetle. Crop Protect 12:324334
Mota-Sanchez D, Hollingworth RM, Grafius EJ, Moyer DD Members of the family Pulicidae (order
(2006) Resistance and cross-resistance to neonicotinoid Siphonaptera).
insecticides and spinosad in the Colorado potato beetle, Fleas
Leptinotarsa decemlineata (Say) (Coleoptera: Chry-
somelidae). Pest Manag Sci 62:3037
Weber DC (2003) Colorado beetle: pest on the move. Pest Common Name
Outlook 14:256259

A vernacular name, reflecting the language of a

Colorado Tick Fever particular country, as opposed to a scientific name,
which is universal.
A viral disease transmitted by ticks in the USA. Common (Vernacular) Names of Insects
Ticks
Common Oviduct
Columnar Cells A median tube (median oviduct) of the female
genital tract (Fig. 82) that leads from the lateral
The tall, and generally most numerous cells, of the
oviducts to the cloaca (vagina).
midgut. They conduct most of the enzyme secre-
Reproduction
tion and absorption of digested products.

Common Sawflies
Colydiidae
Members of the family Tenthredinidae (order
A family of beetles (order Coleoptera). They com- Hymenoptera, suborder Symphyta).
monly are known as cylindrical bark beetles. Wasps, Ants, Bees and Sawflies
Beetles
Common Scorpionflies
Comb
Members of the family Panorpidae (order
A layer of brood cells or cocoons produced by Mecoptera).
social insects and clustered together in a regular Scorpionflies
arrangement.
Common Skimmers
Comb-Clawed Beetles A family of dragonflies in the order Odonata:
Libellulidae.
Members of the family Alleculidae (order Coleoptera).
Dragonflies and Damselflies
Beetles

Common Stoneflies
Commensalism
Members of the stonefly family Perlidae (order
An association between two organisms from dis- Plecoptera).
tant taxa that harms neither and benefits at least one. Stoneflies
1014
C Common Thrips

Common Oviduct, Figure 82 Diagram of female reproductive system, as found in Rhagoletis (Diptera)
(adapted from Chapman, The insects: structure and function).

the USA is monarch butterfly. That name is com-

Common Thrips mon on both counts. But take instead the scarab
species Serica rhypha which has been assigned the
Members of the family Thripidae (order Thysanoptera). invented English language name crooked silky
Thrips June beetle. That common name is unlikely to be
known to more than a handful of people anywhere;
it is a vernacular name that is not commonly used.
Common (Vernacular) Names of Very few vernacular names are common in
Insects the sense of abundantly used and widespread. A
more appropriate term for this entry would be
J. Howard Frank vernacular names, but this expression itself is not
University of Florida, Gainesville, FL, USA common (in the sense of being widely used and
abundant), although it deserves to be so.
There are two meanings of the word common as The English language has a few true common
applied to names. One is that a name is abundant names for insects. Ant, bee, beetle, butterfly, and
or widespread. Quite another is that a name is writ- cricket are some of them. They are old names,
ten in the vernacular language of the place where it having come into use before entomologists began
is used, rather than in Latin. Take, for example, the to classify the five or six million insect species that
species Danaus plexippus whose common name in may exist. In medieval bestiaries, such names were
 Common (Vernacular) Names of Insects
C 1015

used as if they applied to individual species, so very far in listing the 8,800+ species of ants known
that we may read in bestiaries about the habits of worldwide. Even those few names became cumber-
the ant alongside habits of the lion. some for news writers who preferred greater sim-
Entomologists soon realized that they were plification. Thus, the red imported fire ant got
dealing with many species of ants, and by 1990 had simplified to the fire ant (by which the black
described about 8,800 species of them, with the task imported fire ant became downsized).
of description still unfinished. Together, they are There is no hope for systematically providing
classified as the family Formicidae, they have common (vernacular) names for all the approxi-
8,800+scientific species names, and entomologists mately one million insect species that have now
call them the ants. In contrast,the lion of medieval been described (and have scientific names) much
bestiarists remains the one species Panthera leo. less the three to five million that have not yet been
The general public seems to have little grasp of described. Nor is there any point in doing so in
this complexity. News writers, when interviewing English or the worlds other over 900 current writ-
an entomologist about ants, typically insist that the ten languages. The emphasis should instead be on
entomologist provide a common name for what- providing scientific (Latin) names for all species.
ever ant species is being discussed. Then, the news Then we will have at least one name that may be
writer typically uses this common name and used worldwide for each species, as was the intent
writes about it being a variety of ant[s]. By using of scientific names. For any group of people insist-
the expression variety instead of species, the news ing on a name in its own language for some par-
writer seems to be drawing on a medieval classifi- ticular insect species where none exists, one may
cation (that the ant is the classificatory equivalent be invented on the spur of the moment.
of the lion), refusing to acknowledge that there Conventionally, common names are not
may be more than one species of ant. It is a sad capitalized in English. If, however, a proper noun
reflection on public education that news writers (such as a geographical name or the name of a
may have only a medieval knowledge of insect person or a month) is incorporated in that com-
classification and, that with such [lack of] knowl- mon name, then that word (a proper noun) alone
edge, their task is to inform the public. needs capitalization (for example, a June beetle).
Entomologists, when challenged with the ques-
tion of what is the common name of the insect you
are talking about?, invented some names in ver- Vernacular Names Derived from
nacular English. They invented such names as the Scientific Names
wood ant, the carpenter ant, the black imported
fire ant, the red imported fire ant, the Argentine For higher taxa of insects and any other animals,
ant and a few others. But those names do not go there are accepted methods of deriving English

Common (Vernacular) Names of Insects, Table 18 Examples of common (vernacular) names

Classification Name Common name Derived singular Derived plural
1 tribe Brachinini bombardier beetles brachinine brachinines
2 subfamily Cicindelinae tiger beetles cicindeline cicindelines
3 family Culicidae mosquitoes culicid culicids
4 order Plecoptera stoneflies plecopteran plecopterans
5 class Insecta insect insects
6 phylum Arthropoda arthropod arthropods
1016
C Common (Vernacular) Names of Insects

vernacular names (common names) from the standardized common names are useful when
scientific names. The table below gives the scien- communicating with the public and with other
tific name of a tribe, a subfamily, a family, an order, entomologists. The list includes names of species
a class, and a phylum. English vernacular names [that], in most cases, will inhabit the United States,
have been derived as shown. Canada, or their possessions and territories. To
It is unfortunate that the derived vernacular promote adoption of these approved names, the
names in rows 1 and 2 are identical in ending. ESA requires that only they be used in manuscripts
The same method may be used for deriving submitted to that society for publication. More than
vernacular names from all names of higher taxa. 100,000 species of insects inhabit the United States
These derived names are English (not Latin) and are and/or Canada, and far fewer than 2% of species
typically written with all letters in the same case, have been given approved common names.
which is to say that there is no more reason to ESAs printed list of common names was
capitalize the first letter than there is to capitalize the recently supplemented with an online capability by
first letter of the English words bird or cat. Editorial which common names or scientific names may be
guidelines of major entomological journals, with searched (http://www.entsoc.org/pubs/common_
no exceptions, require that they not be capitalized, to names/index.htm). Long delay in implementing
avoid confusion with scientific names. this online search ability, meanwhile requiring pur-
The same method is used to derive vernacular chase of the printed edition, may have contributed
names in other languages using the Latin alphabet, to lack of adoption of the approved names by other
but with twists according to the language in ques- organizations within the United States. For exam-
tion. In French, the singular and plural from Culi- ple, in the mid-1990s, this writer used the ESA-
cidae are culicide and culicides, but many French approved common name for Apis mellifera (honey
texts do capitalize the first letter. In Italian they are bee) in a manuscript submitted as a book chapter
culicido and culicidi, and it seems permissible for publication by a commercial publishing house.
although not required in at least some Italian ento- That name was changed to honeybee by the edi-
mological journals to capitalize the first letter. In torial staff on grounds that honeybee is the house
Spanish they are culcido and culcidos, and the style of that publishing house. Outside the United
tendency, as in English, is not to capitalize the first States, the ESA-approved common names have
letter. In German the plural is Culiciden, and this even less weight, because contrasting common
word must be capitalized because all German names may be commonly used. For example, the
nouns must have the first letter capitalized; the ESA-approved common name for the butterfly
singular should be Culicid (capitalized), but such a Pieris rapae is imported cabbageworm (based
word is avoided by circumlocution. upon the medieval concept that its larva is a worm,
and the more recent concept that it was imported
from Europe [in fact, it probably arrived as an
Official Common Names immigrant, which is to say that it may have been a
contaminant or hitchhiker on some cargo, never
The Entomological Society of America has taken an deliberately imported, but the possibility that it
unusual step of publishing a list of common names. arrived by a combination of winds and flight from
The names selected for this list and their form are Europe or eastern Asia is hard to rule out]) but, in
due to opinions of a committee. By 1989 this list the United Kingdom where it is native, it has been
had a few more than 2,000 common names, and called small white or small white butterfly per-
they applied to selected taxa at various levels from haps since the eighteenth century.
subspecies to class, including some non-insect Australias CSIRO and the Entomological
invertebrates. The list was developed because Society of Canada list common names of insects
 Compound Eyes
C 1017

on websites http://www.ento.csiro.au/aicn and Competitive Displacement

http://esc-sec.org/menu.htp, respectively, with free
public access. Replacement of one species by another. Species
that replace other species typically are ecological
homologues, or nearly so. This also is known as
Reference competitive exclusion.
Gauses Principle
ESA (1989) Common names of insects and related organ-
isms. Entomological Society of America, Lanham,
MD, 199 pp
Complex Metamorphosis
Common Walkingsticks A change in body form in which the insect dis-
plays a striking change in appearance over the
A family of walkingsticks (Heteronemiidae) in course of its development. This is also referred to
the order Phasmatodea. as holometabolous development. The develop-
Walkingsticks and Leaf Insects mental process consists of the egg, larval, pupal
and adult stages. Complex metamorphosis is also
known as complete metamorphosis.
Communal Behavior
Metamorphosis
Incomplete Metamorphosis
A level of sociality less than eusocial behavior. A
type of presocial behavior. It involves members of
the same generation sharing a nest, but without
brood care. Compliance Procedure (for a
Presocial Consignment)
Solitary
Subsocial From a regulatory perspective, this is an official
Communal procedure that is used to verify that a consignment
Quasisocial (usually of plants or other regulated articles) com-
Semisocial plies with stated phytosanitary procedures.
Eusocial Behavior Risk Analysis (Assessment)
Regulatory Entomology
Invasive Species
Community
A group of populations that interact within a
certain geographic area. The biotic portion of Compound Eyes
an ecosystem. This is also called an ecological
community. The principal organs of visual reception in most
insects, consisting of individual functional units
(ommatidia), each of which is marked externally
Companion Planting by a facet. The number of ommatidia present in an
eye varies greatly among taxa. Species with great
The interplanting of repellent and susceptible visual acuity may have thousands of ommatidia
host plants, affording protection to the susceptible per eye, whereas others with poor vision may have
plants. as few as a dozen ommatidia per eye. Compound
1018
C Compsocidae

eyes are very effective at detecting motion, but less other part-time jobs. Now, he was paid as a
suitable for discerning form. Color vision appar- lecturer. He continued his studies and graduated
ently in present in most insects, and polarization in 1874 with a B.S. degree, the only degree that he
of light can be detected by some. ever earned. He continued to lecture at Cornell
Head of Hexapods University and in 1876 was appointed (Fig. 83)
Assistant Professor of Entomology. In 1878 he
married Anna Botsford, one of his students. But
Compsocidae by then he had accepted and acted upon an invi-
tation by Charles Riley to study Alabama argil-
A family of psocids (order Psocoptera). lacea, a pest of cotton, and the following year he
Bark-Lice, Book-Lice or Psocids became Chief Entomologist in the U.S. Depart-
ment of Agriculture. In the winter of 18791880
he began studies of scale insects on citrus in
Compound Nest Florida and continued them in California. He
returned to Washington, was replaced as Chief
A nest containing more than one species of social Entomologist by Charles Riley, who reoccupied
insect. Although there may be intermingling by the position, then returned to academic life at
the adults, the broods are maintained separately. Cornell University. His wife graduated from Cor-
nell in 1885, and by then had taught herself
wood-engraving, which she used with acclaim to
illustrate her husbands (1888) first part of his
Comstock, John Henry An introduction to entomology and other
works. This was followed (1894) by Manual for
Henry Comstock was born on a farm in Wiscon- the study of insects, a book which was so suc-
sin on February 24, 1849. His father, in attempt to cessful that the Comstock Publishing Company
pay off the farms mortgage, decided to search for
gold in California, but died of cholera on the
journey, leaving his mother to support the family.
She became ill after she moved with her son to
New York in 1853, and John was first placed in an
orphanage, then cared for by unsympathetic rela-
tives, then taken in by a farming/sailing family.
He became a cook on sailing ships on the Great
Lakes to earn his living. In 1869 he entered
Cornell University, and in summer 1870, after
reading Thaddeus Harris book Insects injurious
to vegetation he determined to become an ento-
mologist. Unfortunately for him no course in
entomology was being offered at Cornell Univer-
sity, so in summer 1872 he studied entomology at
Harvard University with Hermann Hagen. After
this brief introduction, he returned to Cornell
University and there taught entomology while he
was still a student. Until that time, he had sup- Comstock, John Henry, Figure 83 John Henry
ported himself by working as a laborer and at Comstock.
 Concealer Moths (Lepidoptera: Oecophoridae)
C 1019

was formed, and it continues to this day as a

branch of Cornell University Press and outlet for
major entomological works. Later works (1904)
How to know the butterflies and (1912) The
spider book followed. Anna Comstocks Hand-
book of nature study was published in 1911 and
her Pet book in 1914. His Introduction to ento-
mology was published in full in 1920. He
resigned from his university position in 1913 and
died in 1931, surviving his wife by less than a
year, having suffered a brain hemorrhage in 1926 Concealer Moths (Lepidoptera: Oecophoridae),
and merely existing for the next 5 years. Figure 84 Example of concealer moths
(Oecophoridae), Alabonia geoffrella (Linneaus)
from Italy.
Reference
medium size (580 mm wingspan), with smooth
*Mallis A (1971) John Henry Comstock and Anna Botsford head (rarely slightly roughened); haustellum
Comstock. In: American entomologists. Rutgers scaled; maxillary palpi 34-segmented and
University Press, New Brunswick, NJ, pp 126138
folded over haustellum base (or reduced to one
segment). Maculation varies from somber to
very colorful and iridescent, and variously
Concealer Moths (Lepidoptera: marked; venation (Fig. 84) usually complete
Oecophoridae) (rarely reduced as in such narrow-winged groups
as Stathmopodini). Adults mostly nocturnal but
John B. Heppner some are diurnal or crepuscular. Larvae include
Florida State Collection of Arthropods, many leaf litter feeders, but also leaf tiers, leaf
Gainesville, FL, USA webbers, bark feeders, and a few leafminers, with
a very diverse assemblage of biologies involved.
Concealer moths, family Oecophoridae, are a Host plants include a large number of plant fam-
large family of about 7,550 described species ilies, plus lichens, fungi, and detritus or leaf litter.
from all faunal regions, with most species being Some groups are recorded more on some plants,
from Australia; the actual fauna may well exceed such as Ethmiinae, which have many host records
12,000 species worldwide. There are ten sub in Boraginaceae, and the Australian Hypertro-
families recognized: Depressariinae, Ethmii- phinae, which are mostly on Myrtaceae.
nae, Peleopodinae, Autostichinae, Xyloryctinae,
Stenomatinae, Oecophorinae, Hypertrophinae,
Chimabachinae, and Deuterogoniinae. Many of
References
the subfamilies have at various times been con-
sidered separate families (e.g., Ethmiinae, Steno-
*Common IFB (19941997) Oecophorine genera of Austra-
matinae, Xyloryctinae). Even some of the odd lia. In: Monographs on Australian Lepidoptera 3:1390
tribes of Oecophorinae have been considered (1994); 5:1407 (1997), CSIRO, Canberra
separate families, such as the tribe Stathmopo- *Gaede M (19381939) Oecophoridae. In: Lepidopterorum
catalogus, 88, 92:1476. W Junk, The Hague
dini. The family is part of the superfamily Gele- Gozmny L (2000) In: Microlepidoptera Palaearctica,
chioidea in the section Tineina, subsection Band 10: Holcopogonidae. Goecke & Evers, Keltern,
Tineina, of the division Ditrysia. Adults small to 174 pp, 8 pl
1020
C Conchaspididae

Hodges RW (1974) Gelechioidea. Oecophoridae. In: Domin-

ick RB (eds) The moths of America North of Mexico
Congeners
including Greenland, Fasc 6.2. EW Classey, London,
142 pp, 8 pl Member of the same genus.
Powell JA (1973) A systematic monograph of New World
ethmiid moths (Lepidoptera: Gelechioidea). Smithsonian
Contrib Zool 120:1302
Sattler K (1967) Ethmiidae. In: Amsel HG, Gregor F, Reisser H Congo Floor Maggot,
(eds) Microlepidoptera Palaearctica, vol 2. G Fromme, Auchmeromyia senegalensis
Vienna, 185 pp, 106 pl
*Toll S (1964) Oecophoridae. In: Klucze do Oznaczania
(luteola) (Diptera: Calliphoridae)
Owadw Polski. 27. Motyle Lepidoptera, 35:1174. Pol-
skie Towardzystwo Entomologiczne [in Polish. Engl The larvae of this curious fly feed on the blood of
transl 1975. 176 pp. National Science Foundation, humans and other mammals, though they do not
Washington]
infest the tissues. The normal hosts are warthogs,
hyenas and other animals. Occasionally the females
Conchaspididae deposit eggs on the floor of huts and the larvae live
within the earthen floor or in the bedding of prim-
A family of insects in the superfamily Coccoidae itive habitations in sub-Saharan Africa. The larvae
(order Hemiptera). become active at night, feeding on sleeping inhab-
Bugs itants. They repeatedly feed for periods of 1520
min, and then retreat to their hiding places. Inhab-
itants can avoid this pest by sleeping above the
Conditional Lethal floor, in beds or hammocks.
Myiasis
A mutation that may be lethal only under certain
environmental conditions.
Congener
Conditioned Stimulus
This has several meanings, but generally means an
A stimulus that evokes a response that was previ- organism belonging to the same genus as another
ously elicited by an unconditioned stimulus. organism. Congeners within the same geographi-
cal region tend to compete with one another so
Condyle many adaptations can be observed that mitigate
this pressure on populations. Congenic organisms
A process by means of which an appendage is are organisms with very similar genomes.
articulated at the point of attachment, and partic-
ularly the point of articulation of the mandible
and the head. Conidiophore
A specialized hypha on which one or more conidia
Confused Flour Beetle, Tribolium are produced.
confusum Jacquelin du Val
(Coleoptera: Tenebrionidae)
Conidium
This important grain pest feeds on flour, but not
on whole grain kernels. A sexual fungus spore formed at the end of a
Stored Grain and Flour Insects conidiophore.
 Conservation Biological Control
C 1021

Conifer Bark Beetles Connexivum

Members of the family Boridae (order Coleoptera). In Hemiptera, the junction of the dorsal and
Beetles ventral abdominal plates, which is marked by a
pronounced ridge.

Conifer Sawflies Conopidae

Some members of the family Diprionidae (order A family of flies (order Diptera). They commonly
Hymenoptera, suborder Symphyta). are known as thick-headed flies.
Wasps, Ants, Bees and Sawflies Flies

Coniopterygidae Conservation Biological Control

A family of insects in the order Neuroptera. They Kenneth W. McCravy

commonly are known as dustywings. Western Illinois University, Macomb, IL, USA
Lacewings, Antlions, Mantidflies
Conservation biological control is the implemen-
tation of practices that maintain and enhance the
reproduction, survival, and efficacy of natural
Conjunctiva enemies (predators, parasitoids, and pathogens) of
pests. Natural enemies are important in regulating
A membraneous infolded portion of the body wall populations of many agricultural and forest insect
(Fig.85) that connects two segments. pests. Approaches to conservation of these natural

Conjunctiva, Figure 85 Head and thorax of a grasshopper (Orthoptera).

1022
C Conservation Biological Control

enemies involve avoidance of practices harmful to pests, but are usually very poor environments for
them, as well as adoption of practices that benefit natural enemies. Plowing, mowing, and harvesting
them. Like other animals, insect natural enemies operations, dust from these practices, burning
require food, water, and shelter, and protection of crop residues, and poorly timed irrigation prac-
from adverse conditions. To achieve the goals tices can cause direct mortality of natural enemies.
of conservation biological control, fundamental Of greater importance, however, is the habitat
knowledge of the biology and requirements of disruption associated with these practices. This
natural enemies is needed. disruption can create harsh conditions for natural
enemies. Alternate hosts or prey, nectar and pollen
sources, free water, and refugia are generally found
Practices Detrimental to Natural in greater quantities in habitats with greater diversity
Enemies of vegetation. Microclimatic conditions are gener-
ally more moderate as well. However, increasing
Perhaps the most important rule of conservation reliance on intensive agriculture and forestry prac-
biological control is the physicians maxim, first, tices has tended to decrease habitat heterogeneity
do no harm. Many insecticides can have both as well as genetic diversity of crops. Densities of
direct and indirect effects on natural enemies. parasitoids, as well as parasitism rates of pest
Direct effects include acute or chronic mortality as species, have been found to be higher in mixed
a result of direct contact with pesticides. Direct species habitats and in agricultural field edges near
sublethal effects, such as decreased adult fecundity, mixed species habitats. Avoidance or modification
reduced viability of offspring, and changes in feeding of cultural practices that disrupt natural enemy
habits or other behaviors can also occur. Indirect populations is an important strategy for maintaining
effects can result from mortality in populations natural enemy effectiveness.
of alternate prey or hosts of the natural enemies.
Use of broad-spectrum insecticides that have
detrimental effects on natural enemies can lead to Practices that Enhance Natural
rapid resurgence of targeted pest populations. In Enemy Effectiveness
addition, secondary pest outbreaks (rapid increase
to pest status of populations of non-target arthro- Incorporating practices that are beneficial to
pods) can result if naturally occurring biological natural enemies requires fundamental knowledge
control of these secondary arthropods is disrupted. of natural enemy ecology and life history. These
Use of more selective biorational insecticides, practices can be divided into two broad categories:
or insecticides with short residual activity, can (i) alternate foods or hosts of natural enemies, and
be an effective strategy for conservation of bio- (ii) shelter and refugia.
logical control agents. Timing insecticide applica- Many predators and parasitoids require alter-
tions when natural enemies are absent or in life nate food sources. For instance, certain ladybird
stages that are not susceptible to the insecticide beetles (Coccinellidae), which are important aphid
can also aid in natural enemy conservation. Recent predators, feed on plant pollen before switching to
research involving development of pesticide- aphids. Many adult parasitoids require food in the
resistant natural enemies holds promise as well. form of pollen, nectar, or honeydew. Availability of
Conservation biological control also includes such foods has been found to increase fecundity,
implementation of agricultural and silvicultural longevity, survival, and effectiveness of many spe-
practices compatible with maintenance of natural cies. Availability of plant food sources may also
enemy populations. Monoculture environments increase the host searching efficiency of parasi-
are highly advantageous to many herbivorous toids, since degree of hunger can influence whether
 Conservation of Ground Beetles in Annual Crops
C 1023

the parasitoids spend more time searching for Pickett CH, Bugg RL (eds) (1998) Enhancing biological
control: habitat management to promote natural
hosts or for food. Starved parasitoids have demon-
enemies of agricultural pests. University of California
strated greater attraction to flower odors over host- Press, Berkeley, CA, 422 pp
associated odors. Maintenance of non-crop plants
in or around agricultural fields or forest plantations
can provide these foods, and also harbor alternate
hosts or prey of natural enemies, helping to main- Conservation of Ground Beetles
tain natural enemy populations when pest popula- in Annual Crops
tions are low. Provision of artificial supplementary
food sources has also been shown to increase lon- Fabin D. Menalled, Douglas A. Landis
gevity of some agricultural and forest parasitoids USDA ARS National Soil Tilth Laboratory, Ames,
in the laboratory and field. IA, USA
Natural enemies also require shelter from the Michigan State University, East Lansing, MI, USA
elements. Artificial shelters have been found to
increase winter survival of various peach orchard Ground beetles (Coleoptera: Carabidae) are an
predators, allowing them to provide improved important and diverse group of ground-dwelling
control of early season peach pests. Windbreaks insects with over 2,500 species known from North
and shelterbelts may increase searching efficiency America alone, and more than 40,000 known
and oviposition of parasitoids and predators species worldwide. They occur in many habitats
adversely affected by high winds. Within-field and including forests, riparian areas, grasslands,
border refugia in the form of mixed species habi- orchards, and crop fields. As immatures, carabid
tats can also increase the natural enemy: pest ratio beetle larvae usually live in litter or the upper soil
by providing overwintering and aestivation sites. layers and have ten well-defined body segments
Conservation biological control is likely to tapering towards their posterior end. Adult beetles
increase in importance as agricultural and com- are primarily nocturnal, with a body size ranging
mercial forest systems become more intensively from a few millimeters up to 34 cm. Adult beetles
managed and restrictions on the use of conven- have relatively long legs and are black or dark
tional insecticides increase. It is an approach that reddish, although several species are colored.
requires integration of fundamental insect life Adult and larva beetles feed on insects, snails,
history and natural enemy/pest interactions with slugs, and weed seeds. Because of their voracious
knowledge of the ecology of the systems in which feeding behavior and their abundance in agri-
these interactions take place. This combination of cultural settings, carabid beetles are considered
factors makes conservation biological control important biological control agents with the
research and implementation a challenging, but potential of restricting the abundance of many
potentially rewarding, endeavor. pest species. Among the different pests carabid
beetles are known to consume are: black cutworms,
Agrotis ipsilon Rottemburg; gypsy moth, Lyman-
References tria dispar (Linn); cabbage maggot, Delia radi-
cum (Linn); armyworm, Pseudaletia unipuncta
Barbosa P (ed) (1998) Conservation biological control. (Haworth); European corn borer, Ostrinia nubila-
Academic Press, New York, NY, 396 pp lis (Hbner); western corn rootworms, Diabrotica
Croft BA (1990) Arthropod biological control agents and virgifera virgifera LeConte; and many aphid
pesticides. Wiley, New York, NY, 723 pp
Landis DA, Wratten SD, Gurr GM (2000) Habitat manage- species. Several species of ground beetles are
ment to conserve natural enemies of arthropod pests in omnivorous, consuming not only insects, but also
agriculture. Ann Rev Entomol 45:175201 seeds of common agricultural weeds such as giant
1024
C Conservation of Ground Beetles in Annual Crops

foxtail (Setaria faberi Herm.), velvetleaf (Abutilon i ndirect effect caused by removal of resources and
theophrasti Medicus), redroot pigweed (Amaranthus food. The impact that tillage has on carabid beetles
retroflexsus L.), and common lambsquarters (Che- depends on the species, but it has been found that
nopodium album L.). species diversity and evenness tends to increase in
Due to the potential of ground beetles as bio- reduced tillage fields when compared to conven-
logical control agents, their biology and ecology tionally tilled ones.
have been widely studied. However, ground beetles Cover crops have also been shown to be a
are not commercially available for augmentation suitable habitat management practice to enhance
and several studies have demonstrated that com- ground beetle abundance. Cover crops are crops
mon agricultural practices such as tillage, pesticide not grown for harvest, but rather for other bene-
applications, and harvest reduce ground beetle fits they provide, including protection from soil
abundance and alter carabid beetle community erosion, improving soil structure, supplying soil
characteristics. As a result, pest control by preda- nutrients, suppression of weed germination and
tory ground beetles in conventionally managed weed growth, and contribution to management
annual crop fields is usually diminished. Moreover, of insect pests and plant pathogens. From an
the current tendency of increasing agricultural insects point of view, cover crops can increase
landscape simplification, where farmers manage humidity, reduce temperature, and serve as a host
large monocultures with high mechanical and for alternate prey species. In total, cover crops
chemical inputs, increases the impact of manage- often provide a favorable habitat for generalist
ment practices on carabid beetle survivorship. predators such as carabid beetles. However, it is
In row crop systems, to fully exploit the poten- important to note that the increase in surface
tial of ground beetles as biological control agents, plant material occurring in cover crop systems
it is necessary to generate an environment that may be responsible for a decrease in carabid
allows their survivorship and reproduction. Habi- beetle mobility.
tat management represents a viable approach to Due to the ephemeral characteristics of
reduce the negative impact that several agricul- annual crop systems, it is critical to assure the
tural management practices have ground beetles. overwinter survivorship of ground beetles. Pro-
Habitat management is defined as a series of prac- viding refuge habitats in close association with
tices aimed to alter habitats to improve availability crop fields has been shown to be a promising
of resources required by natural enemies for opti- approach to conserving ground beetles. Examples
mal performance. Several habitat management of refuge habitats include non-crop sites such as
practices have been shown to encourage carabid woodlands, hedgerows, riparian buffers, cross
populations, including no-tillage or conservation wind trap strips, perennial pastures, and grassy
tillage practices, cover crops, and maintenance strips. Crop field edges not sprayed with pesticides
of refuge habitats in close spatial association can also act as refuge habitats for carabid beetles.
with crop fields. The goal of these practices is Refuge habitats benefit carabid beetles through
to provide ground beetles with the ecological several mechanisms. First, refuge habitats provide
infrastructure necessary for their survivorship and suitable overwintering sites for carabid larvae and
reproduction. adults. Several studies have shown that the density
Several studies have evaluated the impact of and diversity of overwintering carabids is higher
tillage on ground beetle abundance and diversity. in refuge strips than in adjacent crop fields. Possible
In general, lower number of individuals are found mechanisms for these differences include a differ-
in conventional tillage than in no-tillage or reduced ential mortality and/or a preferential selection of
tillage systems. This could be due to either a direct habitat. Second, refuge habitats act as a stable
mortality inflicted by soil disturbance, or the resource of food such as aphids and springtails.
 Conservation of Insects
C 1025

This is particularly important early in the growing elements of diversity that enhance ecological ser-
season when prey have not colonized crop fields vices necessary to secure the establishment, sur-
and has been observed to correlate with an increase vivorship, and reproduction of this diverse group
in the weight and reproductive output of female of beneficial organisms. This knowledge should
carabid beetles. Third, refuge strips provide favor- be combined with an understanding of the spa-
able microclimates during hostile weather condi- tial scale over which habitat management oper-
tions such as high temperature and low humidity. ates (within-field, farm-level, agricultural
Finally, refuge habitats protect carabid beetles landscape), any potential negative aspect associ-
from disruptive management practices. If pesti- ated with the addition of new plants into the sys-
cide applications, cultivation, or harvest damage tems (i.e., increasing the risk of pest outbreak or
carabid populations, refuge habitats can serve as weed invasion), and the associated economic
sources of natural enemies that colonize agricul- costs and benefits.
tural fields, inflict mortality on pests, and return to
refuges.
A common denominator among all habitat References
management practices aimed at conserving cara-
bid beetles in row-crops is an increase in the Desnder K, Dufrene M, Loureau M, Luff ML, Maelfait JP
planned biodiversity (organisms purposely (1994) Carabid beetles: ecology and evolution. Kluwer
Academic Publishers, Dordrecht, The Netherlands
included in the agroecosystem by the farmer) Landis DA, Wratten SD, Gurr GM (2000) Habitat manage-
and the associated biodiversity (all soil flora and ment to conserve natural enemies of arthropod pest in
fauna, herbivores, carnivores, etc. that colonize agriculture. Ann Rev Entomol 45:175201
the crop fields (Fig.86) but are not intentionally Lee JC, Menalled F, Landis D (2001) Refuge habitats modify
impact of insecticide disturbance on carabid beetle
established by farmers). However, it is not increas- communities. J Appl Ecol 28:472483
ing diversity per se the final objective of habitat Lovei GL, Sunderland KD (1996) The ecology and behavior
management. A key component is to identify the of ground beetles. Ann Rev Entomol 41:231256
Stork NE (1990) The role of ground beetles in ecological and
environmental studies. Intercept, Andover, UK

Conservation of Insects

Andrei Sourakov, Thomas C. Emmel

University of Florida, Gainesville, FL, USA

Insect conservation is a relatively new concept.

Traditionally, invertebrates are the lowest prior-
ity for conservation organizations due to their
relative inconspicuousness to the public eye and
the lack of showy charismatic flagship species
among the large invertebrate numbers. Even our
most basic scientific knowledge of insects is rela-
Conservation of Ground Beetles in Annual Crops, tively poor. Some taxonomists estimate that there
Figure 86 Anisodactylus sanctaecrusis (F.), a are more than four million insect species alone,
ground beetle commonly found in agricultural but other entomologists believe the number
fields (Drawing by S. Kudrom). could be as high as 50 million. Of these insect
1026
C Conservation of Insects

species, only 510% have scientific names. Even trade is strictly regulated. These include species
for described and well known species, the infor- that are in international trade and are vulnerable
mation on their biology and population dynam- to overexploitation. Regulated trade is allowed
ics is scarce, which makes it harder to determine provided that the exporting country issue a permit
their conservation status. There is also a miscon- that includes a finding that the trade will not be
ception among the general public that a good bug detrimental to the survival of the species or its role
is a dead one, which makes it more difficult to in the ecosystem. This regulation includes a
obtain public money for insect conservation requirement for documentation from the country
projects. of export, monitoring of imports and, in some
At the same time, the roles that the insects cases, export quotas.
play in our lives can hardly be overestimated. They Appendix III. A country may unilaterally
are responsible for reproduction of most plants, (without a vote) list in Appendix III any species
and are essential food sources for many vertebrates which is subject to regulation within its jurisdic-
from fish to birds and even mammals. Though tion for which the cooperation of other Parties is
most pest species indeed belong to the Insecta, needed. Importing countries must check for export
there also are many insect species that keep pests permits for the species issued by the country of
under control through predation and parasitism. origin for Appendix III species.
Though we consider conservation of the pollina-
tors and of the natural enemies to be as essential as
conservation of endangered insect species, here The Importance of Subspecies
we discuss only conservation of endangered
and threatened species, and focus on the diurnal The U.S. Endangered Species Act is written to
Lepidoptera as an example of the problems and allow the preservation of any recognized unique
opportunities inherent in the overall field of insect taxonomic entity, subspecies included. Indeed,
conservation. preserving a subspecies is as important as conser-
vation of a species as a whole. Not only do subspe-
cies frequently turn out to be separate species with
Cites thorough study, but most insect populations thrive
on the gene flow that occurs between populations
The Convention on International Trade in Endan- in the intergrade zones and through migration.
gered Species of Wild Fauna and Flora (CITES) Unique morphological characteristics of subspe-
was signed in 1973 and entered into force in 1975. cies reflect the genetic diversity that allows species
The treaty now has 152 Parties. to survive. These morphological features are often
CITES species are listed in Appendices linked with various ecological and physiological
according to their conservation status. In addi- characteristics. Many local populations go extinct
tion, listed species must meet the test that trade is at one time or another, and such extinction events
at least in part contributing to their decline. are becoming more and more frequent with
CITES regulates international trade in species shrinking of the average population size. Occa-
of animals and plants according to their conser- sional repopulating from an extant neighboring
vation status. population is therefore required for long-term
Appendix I species are species in danger survival of most populations. It is not enough to
of extinction, for which all commercial trade is conserve a species in a single locality, but in as
prohibited. many localities as possible, connected by corridors
Appendix II species are not necessarily threat- of habitat. A distribution range containing as wide
ened with extinction, but may become so unless variability as possible should ideally be designated
 Conservation of Insects
C 1027

in a successful conservation effort. Subspecies, utterfly conservation. By far outweighing all

b
under current legislation, play an instrumental other factors that threaten butterflies (or any
role in achieving these goals. other species) are those of habitat degradation
and pollution, in that order.
The highest diversity of insects on the
Butterflies as an Index Group in planet is found in the Amazonian rainforest, the
Conservation equatorial area which has had no recent major
cataclysms such as glaciation leading to mass
Despite the large numbers of insects that have extinction. Lesser, but nevertheless impressive,
been placed on various lists of threatened or diversity of insects is found in the tropical for-
endangered species, and even larger numbers ests of West Africa, Asia, and New Guinea.
that have already become extinct or are on the Despite the rapid disappearance of these forests,
verge of extinction, by far the most interest and these are not the habitats that contain most of
funding have been attracted by the butterflies. the species placed on the endangered lists.
The latter group accounts for only 20,000 species, Instead, that dubious distinction falls to the
or half a percent of the total insect diversity, but temperate zones. Here, conservation efforts are
there are probably more books written on that much more extensive in the developed coun-
group than on the rest of the insects combined. tries, such as United States, Japan, and the coun-
This popularity, the result of butterflies esthetic tries of Western Europe, where ecological
appeal, is also responsible for the amount of awareness and general education level are
knowledge on them that has been accumulated higher. This creates a misleading impression, as
since the time of Linnaeus, mostly by amateur most of the potentially threatened or truly
naturalists. The last two decades have seen publi- endangered species actually occur in the devel-
cation of books on the butterfly fauna of nearly oping tropical countries.
every country of the world, and there also are Another peculiar phenomenon is that many
numerous books that cover worldwide faunas of species are given preference in being declared
particular groups or different aspects of butterfly endangered because of the demand they attract
biology. These works, combined with the efforts from collectors. Normally, these are the larger and
of hundreds of regional butterfly-enthusiast more attractive species. Even when these species
organizations, provide a significant framework are in decline, this decline is caused by loss of hab-
for conservation. We should note that this knowl- itat, and has little to do with collecting. Habitat, at
edge is far from complete, as life histories and least in the developing countries, often is not pro-
survival requirements are still not understood vided protection from such legislation. The focus
for the majority of species. on collecting occurs mostly because people who
As with many conservation movements, create insect conservation legislation are general
the conservation of butterflies takes many, wildlife biologists, whose primary focus as well as
sometimes contradictory forms. For instance, education and training are in the area of large ver-
some ill-informed people, driven by good inten- tebrate animals.
tions focus their efforts almost entirely on prohibi- Wildlife biologists tend to extrapolate their
tion of collecting. Collecting, however, has been experiences with large vertebrates to insect con-
repeatedly demonstrated to play no important role servation. Thus, they don t take into account that
in endangering butterfly populations. Indeed, even the smallest insect population consists of
quite the opposite is true: collecting is instrumen- thousands of individuals, and that most insects
tal in acquiring scientific information, as well as in reproduce with large numbers of eggs from a
attracting new people into the movement for single female, and have very high biotic potentials.
1028
C Conservation of Insects

The population numbers can naturally vary Case Studies of Four Endangered
tremendously from year to year, which is also Swallowtail Butterflies
rarely taken into account by those monitoring (Papilionidae) from Different
them. The threat from collectors seems obvious to World Regions
vertebrate wildlife biologists because it is parallel
to their experience with hunters and game ani- Ornithoptera alexandrae, New Guinea,
mals. However, it is sometimes enough to just and other birdwing butterflies
mow a meadow or burn the grass in it to destroy
the whole insect population consisting of thou- The first specimen of the Queen Alexandras bird-
sands of individuals: a task that could never be wing, Ornithoptera alexandrae (Fig.87), the largest
even deliberately accomplished by a dozen collec- butterfly in the world, was discovered in New
tors. Nevertheless, over- collecting in rare popula- Guinea at the turn of the century. Recognizing it
tions that are already greatly diminished in size was something new, but always flying high and out
by habitat degradation could be a problem, and of reach, the collector, A. S. Meek, had to fire a shot-
no commercial collecting should be allowed in gun blast at the insect to bring it down in 1906.
such localities. Today, the butterfly persists only in small
Even in the tropics, some habitats are more patches of primary forest left around Popondetta.
threatened and contain more endangered species Population surveys of this species are difficult, as
than others. Mountain chains and the islands cre- adults fly in the canopy. It is extremely local and
ate the conditions of isolation that are often its distribution even before recent habitat destruc-
responsible for new species formation. Moun- tion was apparently restricted, perhaps by host
tains also support a wide variety of unique habi- specificity of the species, which feeds on three
tats associated with elevation change, with related Aristolochiaceae vine species: Aristolochia
correspondingly unique or specialized and highly dielsiana, Paraaristolochia alexandriana and
localized species of plants and animals inhabit- P.meridionaliana.
ing them. In the tropics, these habitats are often Ornithoptera alexandrae has had the legal
claimed for settlements and agriculture because status of Endangered since 1967 in Papua New
they have much more favorable climatic and soil Guinea, and is listed as a CITES Appendix I spe-
conditions than the lowlands. Reforestation in cies. As a result, ironically, it does not enjoy the
such areas, when it occurs, often is conducted protection of habitat that accrues to other Orni-
with exotic fast-growing tree species, such as thoptera species from local people who could be
temperate pines and Australian eucalyptus, which ranching it for sale to collectors, if it were not so
only contributes to exotic replacement and listed. (Papua New Guinea and Australia are now
extinction of the native insect species. The fauna jointly planning a ranching project, which may
of tropical islands, such as those of Oceania, the require re-listing it to Appendix II status.) In
Antilles or Madagascar, are composed of mostly addition, restoration of the rainforest habitat that
endemic species. Some of the most threatened was lost to oil-palm plantations and volcanic
insect species are found on these islands, where devastation (in 1951) is underway, and eventu-
overpopulation of humans often leads to defor- ally O. alexandrae might see removal of present
estation and erosion. Even in the areas where restrictions on its commercial propagation and
population densities are low, the demand for marketing.
cheap timber that can be easily hauled away by Several other species of that colorful butterfly
sea, as well as weakness of environmental laws genus, as well as many other insects of New Guinea,
and governmental corruption, lead to deforesta- are already raised for sale. This activity is under
tion and extinction. the centralized control of IFTA (Insect Farming
 Conservation of Insects
C 1029

Convervation of Insects, Figure 87 Adult of Queen Victorias birdwing, Ornithoptera victoriae (photo by
Andrei Sourakov).

and Trading Agency) at the town of Bulolo. The For example, two birdwing species are found
individual ranching incomes from this activity, exclusively on the Solomon Islands. Smaller than
though low by the standards of the western coun- O. alexandrae, they are nevertheless among the
tries, often exceed the national income average by worlds largest and most beautiful butterflies.
ten-fold. This fact provides strong incentive for Males are valued by collectors for their dazzling
planting host plants and preserving habitat for the coloration, females for their immense size. Queen
species being ranched. Victorias birdwing, Ornithoptera victoriae, dis-
Ranching requires very little effort and no ini- plays different shades of brilliant green, while the
tial investment. Wild female butterflies from the wings of d Urvilles birdwing, Ornithoptera pria-
surrounding forest lay eggs on their respective host mus urvillianus (Fig.88), are sky-blue. The females
plants. Most birdwing species, for example, feed on are colored inconspicuously brown and are slow
the widespread pipe vine, Aristolochia tagala, which fliers that mostly stay inside the forest.
readily grows in small farm plots. Caterpillars are In the Solomons, butterfly specimens are
allowed to feed and pupate freely, while pupae are sold to a middleman in Honiara, who accumu-
collected and brought inside a hut. No cages are lates a sufficient number of butterflies to fill an
used to hold the emerged butterflies or to keep ants order from a Western dealer. Ranchers receive a
and parasitic wasps away because ranchers usually fraction of what a butterfly will be actually sold
do not have money to buy these much-needed sup- for in the developed world. With more coordi-
plies. Instead, they wait for a pupa to turn dark, and nation brought into the program, perhaps by
then watch it closely until the butterfly emerges. the Solomon Islands Development Trust orga-
Then it is killed and papered for sale to IFTA, and nization, some middlemen could be bypassed,
further commercial distribution abroad. and the ranching would become more economi-
Following the example of Papua New Guinea, cally important to the farmers. Now that local
other countries in the region have established people have been introduced to ranching, which
similar programs with different degrees of success. is a much more efficient way of acquiring
1030
C Conservation of Insects

Conservation of Insects, Figure 88 Adult of d Urvilles birdwing, Ornithoptera priamus urvillianus (photo
by Andrei Sourakov).

igh-quality specimens than collecting, the trade

h Homerus swallowtail, Papilio
(and thus conservation effort) is being hampered homerus, Jamaica
by the fact that these birdwings are presently pre-
vented from normal trade in the largest potential This is the largest swallowtail in the Americas.
market in the U.S. by a desire of some CITES offi- Once it inhabited seven of the thirteen parishes of
cials there to punish the Solomon Islands gov- the island of Jamaica in the West Indies, but now it
ernment for not doing enough for conservation. is found only in St. Thomas and Portland parishes
The environmental threat to birdwing survival at the junction of the Blue Mountains and the John
comes from the destruction of their forest habitat Crow Range. In the late 1930s, P. homerus butter-
through logging and slash-and-burn agriculture, flies (Fig.89) were relatively common. By 1945, the
activities which disregard the presence of endan- species was rapidly disappearing from its larger
gered butterflies and for which there is no pun- stronghold in the eastern Blue Mountains. It is
ishment because the local people own the land now one of four endangered swallowtail species
and can develop it as they wish. Without the eco- listed in the IUCN Red Data Book Threatened
nomic impetus to preserve these forests for but- Swallowtail Butterflies of the World.
terfly ranching and other sustainable activities, The rugged Blue Mountains run approxi-
there is no local incentive to resist the lucrative mately one-third the length of the island. The cli-
logging concessions requested by foreign timber mate is uneven throughout the island. For instance,
companies. Thus, outside political pressure in the the northern parish of Portland receives heavy
form of a unilateral U.S. trade embargo, which is rainfall of 381 cm, while the south is much drier
not endorsed by other CITES nations, is having (89 cm). Papilio homerus larvae require humidity
an anti-conservation outcome and inhibiting to be close to 100% to survive. Thus, the species
insect conservation measures undertaken in the only inhabits wet limestone forest at the western
Solomon Islands. end of Jamaica, and lower montane rain forest at
 Conservation of Insects
C 1031

Conservation of Insects, Figure 89 Adult of Homerus swallowtail, Papilio homerus (photo by Thomas C.
Emmel).

the eastern end. The first area is characterized by survival. In 1984 the film Papilio homerus, the
trees such as Jamaican cedar, prickly yellow and vanishing swallowtail, was produced. This film
figs. Secondary succession areas frequently have and other similar publicity efforts over the poten-
bracken ferns and citrus trees. The second area tial national symbol represented by this rare flag-
supports mountain guava, Santa Maria, cobywood, ship species, have created a positive movement of
roadwood and tree ferns. Papilio homerus nor- preservation, culminating in the establishment of
mally occur below an elevation of 1,000 m. Her- Blue and John Crow Mountains National Park in
nandia catalpifolia, locally known as water mahoe 1991, with Papilio homerus as the official symbol
or water wood, and H. jamaicensis (pumpkin of the Park Service. Subsequent educational efforts
wood, suck axe) are the larval host plants, in the have continued annually in Jamaicas elementary
family Hernandiaceae. Ocotea nr. leucoxylon (lob- schools, with written materials on the butterflys
lolly sweetwood in the Lauraceae) may also be life history and the manifold importance of the
used by larvae. montane rain forest habitat to watershed protec-
Forest reserve areas were established in these tion, wildlife, recreation, and tourism-based eco-
mountains, including prohibition of cutting trees. nomic benefits. After Hurricane Gilbert destroyed
However, FIDCO (Forest Industries Development most of the planted Caribbean Pines at the end of
Company), formed by the Jamaican government the 1980s, the establishment of the montane rain
in 1979, began cutting 2,000 hectares of rainforest forest park has allowed natural succession to begin
per year to plant Caribbean Pine to help the char- reclaiming these areas. Fortuitously, Hernandia
coal production industry. With the rapid disap- species are among the foremost recolonizing rain
pearance of the wet streamside rain forests, this forest trees, rapidly increasing the potential habi-
activity presented the major threat to P. homerus tat for the Homerus Swallowtail.
1032
C Conservation of Insects

Parnassius apollo, Europe uarter-mile-wide island, where there are no recent

q
human developments or mosquito control practices.
This is the first butterfly species that was placed on Theannual number of adults flying there has usually
the CITES list for prevention of trade. While hovered at several hundred to as many as a thou-
numerous cases of local extinction are known for sand, though it varies from summer to summer.
the species throughout Europe, none of them has Schaus swallowtail was once widespread
been linked to collecting. Acid rains were blamed throughout south Florida, but its population size
for its demise in the 1970s in Germany and the and distribution have been reduced by the growth
Alps, while around Moscow the mass spraying for of Miami and urbanization of the Keys, and, later,
gypsy moth might be a key factor for its disap- by the spraying of Dibrom and Baytex pesticides.
pearance. Everywhere, habitat loss is also a signifi- Prior to the development of the area, butterflies
cant factor. In our view, one of the weaknesses of migrated freely around the northern Keys and
the current conservation legislation concerning P. mainland. Capture/recapture data shows individ-
apollo (Fig.90) (as well as of all other endangered uals fly as much as 3.5 miles within a few hours.
butterfly species) is that it targets the species rather This movement supported the genetic diversity of
than the habitat. Additionally, this legislation rec- each of the smaller populations, and ensured pop-
ognizes all subspecies of P. apollo as endangered, ulation of new sites and natural repopulation of
despite the fact that many of them, particularly in those suffering a temporary extinction.
Central Asia mountain ranges, are very common. Today, Elliott Key has the only large popula-
Some captive breeding and reintroduction pro- tion of the butterfly, and the area is currently
grams for the endangered European subspecies protected as a part of Biscayne National Park.
are being developed locally. When Schaus swallowtail was recognized as an
endangered species by the U. S. Fish and Wildlife
Service in 1984, a research group from the Uni-
Schaus Swallowtail, Heraclides versity of Florida began looking for ways to secure
aristodemus ponceanus Schaus, its future. Although now protected, the Schaus
Florida swallowtail, even on Elliott Key, remains at risk.
The small size of this sanctuary, and the absence
The Schaus swallowtail is the resident H. aristode- of secure populations outside it, make the Elliott
mus subspecies that is found in South Florida and population vulnerable. Should it be wiped out
the Florida Keys. An assortment of other distinct by an ecological disaster, there would be no
subspecies is found on some of the Bahamian and natural source of Schaus swallowtails to repopulate
Caribbean islands. Only a few of the Keys have the islands.
suitable hardwood hammock habitat today, and Schaus swallowtail shares Elliott Key with two
even fewer support the Schaus butterflies. This is similar-looking swallowtails: the Bahama swallow-
one of the cases where pollution by mosquito con- tail, Heraclides andraemon bonhotei, apparently a
trol practices has evidently contributed signifi- very low-level resident population or an occasional
cantly to the demise of the species. Were it not for visitor, and the Giant swallowtail, H. cresphontes,
this impact since 1972, the population (though which forms a persistent but smaller resident pop-
impaired by the loss of habitat) would be substan- ulation. The Giant swallowtail flies synchronously
tially above present precarious levels. with Schaus, but can easily be identified by its larger
The adult butterflies (Fig. 91) emerge from size and more powerful flight. Schaus swallowtails
their pupae after the first rains in May, following usually have slow fluttering flight to maneuver
a long dry season. The major population is that through the dense jungle of tropical hardwood
on Elliott Key, an isolated, seven-mile-long and hammock while avoiding lethal spider webs. It is
 Conservation of Insects
C 1033

Conservation of Insects, Figure 90 Adult of Parnassius apollo (photo by Alexander Dantchenko).

not uncommon to see a Schaus even backing up, plants and the thick hardwood hammock, which
a rarity among butterflies. While giant swallowtail provides a relatively cool, shady microclimate in
larvae would feed on any citrus (Rutaceae) tree, the hot Keys.
Schaus larvae can complete development only on When Hurricane Andrew hit south Florida
wild lime (Zanthoxylem fagara) and torchwood in August 1992, the hammock on Elliott Key was
(Amyris elimifera). Females especially prize the devastated: no canopy was left to protect the deli-
latter for Therefore, Schaus require these host cate undergrowth of torchwood and wild lime
1034
C Conservation of Insects

Conservation of Insects, Figure 91 Adult of Schaus swallowtail, Heraclides aristodemus ponceanus (photo
by Andrei Sourakov).

from the desiccating rays of the sun. Elliott Keys eggs before dying at an average age of 3.6 days.
wild Schaus population survived Hurricane Most of the eggs in nature are eaten by predators
Andrew in very low numbers (only 17 in 1993), such as ants, or parasitized by wasps. Thus, captive
and was later buttressed by releases of captively propagation can work well with this species. The
reared individuals. Fortuitously, 100 wild Schaus females can easily be hand-paired, and lay eggs on
eggs had been removed to establish a captive either torchwood or wild lime. The young larvae
colony at the University of Florida just 2 months are raised in vials with fresh torchwood leaves, and
before the hurricane. This colony was expanded later can be placed on potted trees. At maturity
to produce several thousands of Schaus swallow- they are transferred back into individual plastic
tails that were then released back in the wild at a cups, in which the larvae pupate. Then, either pupae
series of sites on the south Florida mainland or emergent adults are released into the wild at
and the Florida Keys in 1995, 1996, and 1997. suitable sites.
Capture-recapture data showed (Fig.91) recovery Future studies will tell whether the 13 wild
to about 1,200 adults flying in 1996 and 1997. populations that were established after Hurricane
However, the possible genetic bottleneck that the Andrew through this captive propagation pro-
population went through during the immediate gram are viable. In addition to monitoring the suc-
post-hurricane years could cause serious prob- cess of the introductions, there is a need for
lems for the population in the future. Additionally, continuing the search for remnants of suitable,
a 5-year drought (19982002) in South Florida reintroduction-worthy habitat. The programs sur-
reduced the Schaus populations to, at most, 200 vival greatly depends on funding, which has so far
adults by mid 2002. been provided by the U.S. Fish and Wildlife Ser-
In captivity a female can live up to 32 days and vice and private donations.
lay up to 430 eggs; in nature, she lays at most 80 Endangered Species
 Construction Behavior of Insects
C 1035

References Types of Structure and Nest

Architecture
Collins M, Morris MG (1985) Threatened swallowtail butter-
flies of the world. The IUCN red data book. IUCN, Of the many different types of structures built by
Cambridge, UK, 401 pp
New TR (ed) (1993) Conservation biology of Lycaenidae
insects, some of the simplest structures are the
(Butterflies). IUCN, Gland, Switzerland, 173 pp bubble nests of the froghoppers (Hemiptera).
New TR (1997) Butterfly conservation. Oxford University Bubble nests function in anti-predator defense
Press, Oxford, UK, 248 pp and water conservation and are produced by froth-
Samways MJ (1994) Insect conservation biology. Chapman &
Hall, London, UK, 358 pp ing up secretions of the Malpighian tubules into a
tight bubble mound around the builder.
Another very simple form is the cocoon built
Conspecific by a moth caterpillar preparing for pupation. The
larva finds a spot for this transitional stage to take
Organisms belonging to the same species. place and begins the process of building the
cocoon. The larva has large salivary or labial
glands that produce a remarkable material called
Construction Behavior of Insects silk. This complex protein is drawn from the
glands forming a durable and water resistant
Holly Downing thread. The larva touches the substrate and
Black Hills State University, Spearfish, SD, USA attaches the end of the silk to one side and then
draws out a length of silk in an arch and attaches
One of the most complex and exciting areas of the silk to the substrate on the other side of its
insect biology is that of nest architecture and con- body. Repeatedly attaching and looping over itself,
struction behavior. There are four major groups of the larva creates a covering that will protect and
insects that are well-recognized builders, while attach the denser cocoon pouch on the inside.
there are individual species in other groups that Once the outer layer is in place, the larva will spin
also build structures. The four major groups of silk around and around itself to create the protec-
builders are the Isoptera (termites),the Hymenoptera tive cocoon. In a cocoon of the silkworm moth,
(ants, bees and wasps), the Lepidoptera (butterflies the length of the single thread is 5001,300 m
and moths, though only moths build), and the long. Silk material is made from the threads that
Trichoptera (caddisflies). The moths and caddisflies are unwound from these cocoons. The cocoons
build individual cases, cocoons, or group retreats, are soaked in hot water and the loose outer thread
but the termites, ants, social bees and social wasps is caught on a turning spool. The cocoon unwinds
build the most elaborate structures. Some nests as one very long silk thread. Multiple strands are
are enormous relative to the size of the builders collected at the same time and combined to create
(several miles high if the height is made propor- a remarkably strong thread that can then be dyed
tional to human dimensions), able to maintain and woven into a beautiful cloth. The larvae of
nearly constant temperature and humidity, and able other moth groups, such as the bagworms and the
to withstand years of harsh sun and driving tropical case making clothes moths, build individual silk
rains. Small insect groups that build, or with only a cases with fragments of their food material or
few building species, include the Diptera (flies), vegetation incorporated in the walls. The case is
Embioptera (webspinners), Orthoptera (grass- dragged around, serving to protect the larva as it
hoppers, crickets), Hemiptera (cicadas, hoppers), feeds, and is spun closed during pupation.
Neuroptera (lacewings, antlions, mantispids), and Other Lepidoptera species, including some
Coleoptera (beetles). tent caterpillars, lay their eggs in clusters. When
1036
C Construction Behavior of Insects

the larvae hatch, they work together to spin a that the case takes is species-specific, so the charac-
common retreat. The silk in the walls of the retreat teristics of the case can help in identifying the ani-
is so tightly layered that it takes on an almost mal that made it. Studies have shown that the larvae
leather-like appearance and texture. Some indi- are very careful in their selection of building mate-
viduals are more active foragers and lay down rial, turning each item around repeatedly before
silken trails to foraging locations, which the others rejecting or accepting it. If accepted, the item is
follow. During the day, they return to the safety of then carefully oriented and glued with silk into
the multi-layered retreat that protects them from position. Macronema transversum is a species of
predators and dampens temperature and humid- caddisfly that builds a more elaborate, curved case.
ity fluctuations. This U-shaped case, which has an incurrent funnel
The Embioptera or webspinners are members facing upstream and a smaller excurrent funnel
of a small order of insects, but unique in that they immediately downstream, not only provides a safe
use silk from tarsal glands in their front legs to spin retreat, but also is used to support a web spun
silken passageways. Groups of individuals live across the interior chamber and to filter food par-
together in what becomes a network of galleries. ticles from the water.
The caddisfly larva is the immature form of There are some insects that use the leaves of
the Trichoptera. This insect group is closely related plants to create safe feeding locations for their
to the butterflies and moths, but it has little hairs developing brood. The females of a group of leaf-
instead of scales on its wings. Although the adult is rolling weevils (Coleoptera) first use the mandi-
a terrestrial insect, its immature larva is aquatic, bles at the end of a long proboscis to chew into the
living in streams among the rocks and vegetation leaf petiole just at the base of the leaf. The female
at the bottom. As in the Lepidoptera, this group then moves out on the leaf and begins to break
builds using silk produced by the salivary or labial open the epidermal layer with tarsal claws and
glands. The caddisfly larvae build a variety of struc- mouthparts until the leaf begins to curl with loss
tures, depending on the species. Some build a silken of turgor pressure. The female then aligns herself
web, which they use in straining food from the with the edge of the leaf and using the legs on one
water flowing around them. Others build retreats side, pulls the leaf edge over to begin the tight curl.
by attaching small pebbles (Fig.92) or plant mate- The leaf is rolled to completion and glued tight
rial to silk in a case surrounding their body. As they with anal secretion. During the construction of
grow, they add more building material on the front the curl, the female enters the curl and lays an egg
lip of the case, always keeping it just large enough through a slit she makes in the inner layer. Thus,
to draw back into for safety, but small enough to multiple leaf layers protect the egg, and when it
drag around. The type of material and the form hatches, the larva has a secure feeding spot.

Construction Behavior of Insects, Figure 92 Caddisfly case built of small pebbles and silk by the larva.
They are found in streams and other bodies of flowing water.
 Construction Behavior of Insects
C 1037

Many different types of animals, both verte- Those that build underground burrows to
brate and invertebrate, build burrows, insects protect immature offspring are members of the
included. These burrows may be simple, consisting Orthoptera, Coleoptera and Hymenoptera. Paren-
of a tube dug into the ground with a single chamber, tal care may exist in the form of guarding the bur-
or they may be quite complex in structure. Regard- row, or provisioning the young. In the dung beetles,
less of complexity, the burrows may serve a variety male and female pairs dig out a burrow and then
of functions including predator avoidance, brood pack the end of it with a ball of fresh dung (some
rearing, feeding and vocalization enhancement. collect the dung first, tap it into a ball and push it
Immature cicadas, members of the order with the hind legs to a desirable location where
Hemiptera, live in burrows. The length of the they then cover it with dirt). An egg is laid on the
nymphal stage varies with the species, but may ball of dung, or the ball may be subdivided a num-
extend as long as 17 years. During that time, they ber of times and eggs laid on each of the balls. In
live underground and feed on roots accessed from some species, there is little parental care, while in
their burrows. others, the burrow is defended and the dung ball is
Some members of the order Orthoptera build kept from desiccating and molding. After hatching
burrows, but none more elaborate than that of from the eggs, the young feed on the dung within
the mole cricket, Gryllotalpa vineae. The male of the protective environment of the burrow.
this species builds a burrow with two adjacent, Burrow construction is most elaborate among
horn-shaped entrances. The double-barreled bur- the ants, bees and wasps. In some wasps and bees,
row curves downward where the two entrances multiple chambers are built either singly or in
join in a single, somewhat enlarged passage leading clusters off the main tube, or off branching tubes.
to the deeper blind retreat. The male calls from Each chamber or cell houses one developing larva
the enlarged passage while facing away from the that feeds on food provisioned within the sealed
entrance. He rubs his forewings producing a loud cell. Some species, like Paralastor sp., build a mud
call, which is greatly amplified by the burrow tube elaboration on the burrow entrance that helps
design and can be heard by a person more than prevent parasitoids and predators from entering
400 m away. The call frequency with maximum during the construction and provisioning of cells.
energy is 34 kHz, while the call can reach over In the stingless bees, the nest entrance has wax
100 dB at approximately a half meter above the added to form a chamber for guard bees and a
burrow. landing platform for returning foragers. The large
The antlions of the order Neuroptera build nest chamber houses wax cells where the brood is
prey-capturing traps in sandy soil, which at times reared and the reserves of honey and pollen are
can be spotted along hiking trails. The larva has stored. In these insects, the honey and pollen are
large mandibulate mouthparts and builds its cone- fed to the young and they are progressively provi-
shaped pit by throwing sand up and out of the hole sioned. Tubes leading deeper into the ground pro-
with its flat head and mandibles. It buries itself at vide space for water drainage and garbage
the bottom of the pit and lies in wait for an unsus- disposal.
pecting ant or other small insect to slide down the One group of amazing underground build-
side of the pit. By tossing sand up the edge of ers is the leaf cutter ants, of the tribe Attini. The
the pit, the antlion creates a mini-avalanche that colonies of these extraordinary ants start with
causes the struggling prey to slide further down the founding queen who has been fertilized prior
the side of the pit, whereupon it is bitten and to sequestering herself in a newly formed blind
sucked dry. There is a group of flies, the worm-lion, burrow. She takes a small amount of fungus from
Vermileo comstocki, that also builds a similar trap her parental nest, plants it with a bit of her anal
to catch prey. secretion, and carefully tends this small fungal
1038
C Construction Behavior of Insects

garden. She lays a few eggs, which are destined to The air cools in these outer passageways and sinks
become the first workers for the colony. From downward. The cooler air is then drawn into the
this obscure beginning, the colony grows until it core area as the warm air rises. Millions of workers
has a fully formed caste system with sterile and chambers filled with fungal gardens generate
workers and soldiers numbering in the millions. a great deal of heat, yet the architecture of the
Separate chambers are built to grow fungal gar- mound keeps the temperature constant, within
dens and rear brood. These ants forage for leaves, one degree Celsius.
which they bring back to the colony along cleared The shape of the termite mounds may also
paths. They attach the leaves to the fungal garden, contribute to colony thermoregulation. For exam-
sometimes using small amounts of anal fluid. ple, the mounds of the compass termite stand
Mycelia of the fungus are planted on the leaves about 4 m high and are long and thin. The broad
where they grow and soon cover the entire leaf. surfaces face east and west, while the thin sides
The ants tend the fungal gardens, which in turn face north and south. Thus, during the cool morn-
produce spherical swellings that are eaten by the ings and evenings, there is a broad surface facing
ants. An Atta leafcutter queen is estimated to live the sun to collect solar energy, while during the
ten or more years. By the time her colony is heat of the day, only a narrow surface is exposed to
mature, the nest will have more than several mil- the sun, minimizing the heat uptake. The nests of
lion workers, will have thousands of chambers other species have tall towers or buttresses, which
and over a thousand entrances. Nests have been also help to cool down the nest.
described that reach as deep as 6 m below the There is a group of solitary wasps that are
surface and extend over 100 m2. referred to as mud daubers. This group includes the
Although termite nests typically start out potter wasps, which build single or clusters of small
underground, they are built up with loads of build- mud cells, each one built to house one developing
ing material until they have some structures above offspring and the provisioned, paralyzed insects or
ground. Even the termites with the simplest nests spiders to feed it. In some cases, the pots truly look
have covered passages made by gluing pieces of like a clay pot molded into a jug-shape with an out-
mud together with fecal material. Their building wardly curving lip at the entrance. After the jug has
process includes creating an arch and then extend- been stuffed full with paralyzed caterpillars and an
ing that arch to form the tunnel, which protects egg laid, the jug is sealed with a mud plug. Because
them from predators, the sun and desiccation. The these wasps are small, their nests are often over-
mounds of some termites get to be enormous, with looked, and most homeowners are more likely to
chimneys that extend 910 m above the ground. notice the long mud tubes of the organ-pipe wasp
The mound of Macrotermes bellicosus is one of the (Trypoxylon spp.) (Fig.93) or the large cell clusters
most complex yet described. The mound has a of the common mud dauber (Scelephrons spp.). The
central living area with chambers for the king and organ pipe nest is built by the female, as is typical in
queen, the brood and the fungal gardens (like the the Hymenoptera. She adds mud to form arching
leaf cutter ants). Surrounding this central living mud strips in a long half-tube attached along the
area is an open chamber that allows air to circulate edges to the substrate. The tube is long enough to
around the inner core. The outer protective wall is house approximately six cells. She lines the inside,
filled with passages that act like capillaries and smoothing out the interior walls and adding to
maintain a constant temperature within the the tube along the substrate junction. She then
mound, while decreasing potential water loss from begins the process of provisioning the cells with spi-
evaporation. Warm air, produced by the termites ders, laying an egg on one of the spiders and sealing
and gardens within the core, rises and passes out off the individual cells with mud in sequence down
to the air passages within the outer protective wall. the length of the tube. This is one group in which
 Construction Behavior of Insects
C 1039

Construction Behavior of Insects,

Figure 94 Polistes wasp female building a petiole
and the side of the first cell. Building material
is a combination of plant fibers and glandular
secretion.

by wasps is typically cryptic in that the nests are

thin and built on the underside of tree trunks, or
Construction Behavior of Insects, Figure 93 leaves, or in cavities, have the color of the sur-
Organ-pipe mud dauber female constructing a rounding substrate and are easily overlooked. The
mud tube. She will line the tube and then nests of some social wasps have no enclosing
construct a series of cells down its length. Each cell envelope and are attached to the substrate by a
will be provisioned with spiders, have an egg laid narrow petiole (Fig.94).
on one spider, and be sealed off with a mud wall. The nests of a unique group of wasps, Micro-
The fly in the photograph is a nest parasite of this stigmus, are made using plant hairs from the
wasp. underside of leaves. Microstigmus comes has been
extensively studied; these small (4 mm long) trop-
the male contributes to the process of construction ical wasps begin by locating a nesting spot on the
and brood provisioning by guarding the tube underside of a leaf of a species-specific host plant
entrance from nest parasites that would otherwise in the genus Chryosophila. A single female, or
sneak one or several of their own eggs into the cells. small group of cooperating females, then begins
The male is then well placed to mate with the female to chew up plant hairs in a wide circle. The hairs
when she is ready to lay her eggs. are pulled inward and a growing mound of hairs
Social wasps usually use plant material of wrapped in silk forms around the edge of the cir-
some sort to build aerial or underground nests, cle. The wasp or wasps keep working until a ball
but some species use mud. Each nest is typically of plant hairs and silk is located at the center of
made of one or more combs of hexagonal cells in the area cleared of plant hairs. The base of the ball
rows, and the nest may have one or many enclos- is worked into a long slender spiraling petiole,
ing envelopes. The architecture of the nests made which suspends the ball that will form the actual
1040
C Construction Behavior of Insects

nest. The wasps create an entrance near the base tergites produce bees wax in thin scales. Wax is a
of the petiole and excavate a space called the ves- component of the insect integument. During the
tibule. This will be an area for adult wasps to course of evolution, it is likely that clusters of
gather that is located above the cells. The remaining cells that produced wax for the integument
ball is worked into 114 cells, which are lined with became specialized for greater wax production.
silk and provisioned with Collembola. Although The bees scrape the wax off the wax producing
some Microstigmus are progressive provisioners, surfaces of the abdomen and work it into a ball of
M. comes is a mass provisioner. Prior to laying material for adding to the comb. In some species,
an egg, these wasps stuff each cell with enough the wax is mixed with plant resins to make a mix-
Collembola to supply a developing larva through ture called cerumen. Although wax and cerumen
pupation. The entire nest is only approximately are both water resistant and pliable, cerumen is
1 cm3 in size. more pliable than wax and is used for building
the softer parts of the nest such as the storage
pots and brood cells. In some species, wax is also
Building Materials mixed with other glandular secretions or even
mud. Resins may even be used without the addi-
The study of the building materials that insects use tion of wax to produce supporting pillars and
is still far from complete. There are two key ways protective layers. Thus, construction material for
the building material supports the weight of the bees varies dramatically in the wax content and
structure, (i) compression, in which the nest bears in the nature of the additives, depending on the
the weight of the overlying structure like the bricks species, the component of the nest under con-
in the wall of a building, and (ii) tension, in which struction and the type of support the structure
the weight of the structure is suspended and hangs. provides.
Insects use both methods. Mud is often mixed with water and glandular
Silk, often used in suspension construction, is secretions or fecal material and used in building.
a polypeptide that is highly diverse in structure as Insects building with mud usually use fine, moist
well as in gland of origin when compared across soil. In some species such as the mud-daubing
species. However, in general, it is a remarkable type wasps, the builder vibrates as it collects and applies
of material in that it is extremely light weight yet the mud. This has the effect of suspending the mud
has a tensile strength 23 times that of steel. Its particles and liquefying the material, thus making
strength comes from its structure. Silk, in most it easier to manipulate and shape.
arthropods, is a fibroin a protein with long, un- The use of plant fibers and fragments requires
branching polypeptides. Although the sequence the addition of glandular secretion, as well. Anal-
and make up of the polypeptide chains vary ysis of the building material of Polistes paper
between species, glycine, alanine and serine make wasps shows that the glandular secretion adds a
up about 80% of most types of silk. Crystalline or mix of more than 20 amino acids to the plant
highly organized regions are interspersed with fibers, including glycine, serine, alanine, valine
amorphous or unorganized regions. The organized and proline. The combined material is pliable,
areas have tightly packed polypeptide chains that strong, lightweight and water resistant. Not only
are in tightly linked pleats through hydrogen cross is the glandular secretion added to the building
bonding. The amorphous areas give silk its material, but it also is added to the outer surface
flexibility. of the nest, especially around the petiole and
When building, bees use a second type of comb back. The wasps apply the pure oral secre-
glandular secretion. Epidermal glands along the tion by licking the nest and this often results in a
anterior edges of the abdominal sternites and/or shiny, dark outer layer.
 Construction Behavior of Insects
C 1041

Function and Evolution of Insect

Structures

Protection is the primary function of all insect-

made structures. The structure separates the insect
from the exterior world and thus, may help to
lessen fluctuations in temperature and humidity
and may act as a protective barrier between devel-
oping brood and predators, parasitoids and para-
sites. The bubble nests of the spittle bug, the
caddisfly case, the galleries of the Embioptera and
the towering nests of termites all share the func-
tional role of protection. However, the structures
often have additional functions. For instance, the
bubble nests of the spittle bug help the nymph
avoid desiccation; the caddisfly case assists in feed-
ing in some species, and helps move water over the
gills. As previously described, the termite mound
controls thermoregulation and humidity regula-
tion, and shelters the colony from rain. It provides
Construction Behavior of Insects, Figure 95
housing for the members of the colony and their
Polybia occidentalis nest showing the enclosing
sources of food.
envelope and small entrance hole that aids in nest
One feature of many social insect combs that
defense against ants (photo R. L. Jeanne, Univ.
has attracted attention is the hexagonal array of
Wisconsin).
cells. This pattern of cells occurs in the combs of
honey bees and many social wasps and appears to
be the result of packing circular cells as closely some wasp nests help to insulate the brood on the
as possible with a minimum use of building inside by creating a cushion of air around them.
material. The builders actually build circular cells Nests with no enclosing envelope have a nar-
initially, which are possible to see along the edge of row attachment to the substrate as an anti-predatory
the comb, but as they add on additional cells, the defense. The comb appears to hang from this narrow
adjoining walls straighten out. Once a cell is com- petiole in a precarious manner, but the petiole is
pletely surrounded by other cells, it takes on the strengthened with many layers of glandular secre-
hexagonal shape. Occasionally cells are four- or tion or silk. The narrow petiole provides protection
five-sided, but this occurs when the cell arrange- from marauding ants because it is difficult for them
ment is being adjusted for a confined space, or the to find, and the wasps can defend it both physically
rows of cells are out of alignment. and with applied chemical barriers.
The brood developing in the hexagonal cells It is possible to compare nest structure among
of the comb is a rich food source for a number of groups of related species and formulate hypotheses
predators, both vertebrate and invertebrate. The about the evolution of the different species-
enclosing envelope that the nests of many species specific structures. For instance, in the social
have helps to hide the comb, and the small entrance wasps, all of the variation in nest architecture was
hole is easy to defend against ants (Fig.95), which shown to be a derivation of the basic horizontal
are an important invertebrate predator of social comb (cell openings facing down) hung from the
insect colonies. In addition, the envelope layers of substrate by a somewhat narrowed extension of
1042
C Construction Behavior of Insects

the comb top or back. In one derived set of nests, inherit the design blueprint, and these lead builders
the comb top has become narrowed to form a then direct the construction of others based upon
petiole of variable length and combs take a variety information they have gathered while moving
of angles and forms. Another derived group devel- systematically about the nest. There is again no
oped envelopes that are the extension of the outer evidence supporting this hypothesis, and it would
walls of the outer row of cells of the comb. Petioles be difficult for an individual to compare what
may or may not be present and the envelope serves others are building to a blueprint design of the
to protect the brood from predators. A third group finished product. In all insects studied thus far,
of distinctive nests have narrowed petiole attach- the only direction observed is by the queen or king
ments, multiple combs and a separate envelope (if present), and they simply act as pacemakers.
that is not an extension of the cell walls. It can only A third hypothesis is that each individual
be hypothesized that predation, environmental inherits a construction program of sorts. This pro-
pressures and evolving modifications in the build- gram consists of the steps of construction and a
ing material combined to produce the larger, com- sensitivity to certain cues that regulate that con-
plex nests of the highly eusocial wasps. It has been struction process. When an insect builds, it has no
suggested that the evolution of building material sense of the finished product and is simply
capable of holding together a large nest was a criti- responding to the immediate cues, some of which
cal precursor to the development of highly euso- come from previously completed construction.
cial behavior and large colony size. The building The process of building in response to previous
behavior has had to change as well, because as construction is referred to as stigmergy, a word
nests become larger, more construction material is coined by P. Grass.
needed for the nest attachment and supporting In solitary insects, the building program fol-
walls. As a result, mature nests are often structur- lows a linear series of steps with the completion of
ally quite different from incipient nests. one step triggering the next. Cues associated with
the completion of an act are tested with the addi-
tion of a load. A simple decision is made is the
Regulation of Construction previous step done? If no, add building material in
Behavior the same way as before, if yes, go on to the next
step of construction. By building through a spe-
As shown in previous sections, the nests of most cific set of construction steps and responding in a
insects are species-specific in design and the nests species-specific way to certain cues, the results are
can thus be used to enhance phylogenetic studies. a species-specific nest. Because each individual
There are several hypotheses attempting to explain (Fig.96) is independently responding to the cues
how species-specific construction information is in its surroundings, no coordination among indi-
transmitted between generations. Insects could viduals is necessary.
inherit a blueprint of the finished nest design and With social insects, nests develop over a lon-
then build toward creating a structure that matches ger period of time. Throughout the nesting season,
the blueprint. There is no support for this hypoth- cells are progressively lengthened as the brood
esis, and intuitively one can consider a small ter- grows, entrances, chambers and cells are added,
mite building in the pitch-black galleries of the and petioles and envelopes are enlarged. Although
developing nest and see the difficulty. There is little the building may start out with a linear series of
possibility that such an insect could comprehend construction steps, this soon can no longer
the entire structure and coordinate its construc- describe the process where building can take place
tion with that of many other builders. A second in any of many different sites simultaneously.
possibility is that there are certain individuals that Builders must evaluate competing locations and
 Construction Behavior of Insects
C 1043

non-social. Studies of construction behavior in

different organisms can help identify common
construction mechanisms. Where species differ,
these comparisons can lead to insights into the
evolution and regulation of this behavior.
The building process actually involves two
types of decisions: (i) where to build next, and
(ii) how to shape the building material in that
location. For instance in the paper wasp, Polistes
fuscatus, which builds a comb suspended by a petiole,
brood size and cell mouth angle impact the deci-
sion about which cell to lengthen next, while
the antennae are used to measure the width of
the cell as pulp is added. By constantly rotating the
antennae in adjacent cells, wasps maintain a species-
specific cell diameter. Cut one of the antennae
and the cell wall measurements are altered. Most
behavioral studies of construction have investi-
gated the first type of decision only. The second
type of decision and its relationship with the first
have been studied in only a few insect species and
many questions still remain to be investigated.
Individual building decisions are a part of
the larger phenomenon of colony wide activity. The
Construction Behavior of Insects, Figure 96 regulation of the pace of construction and how
Diagrammatic representation of a the tasks of foraging for water, collecting wood
building program. pulp for building and building itself are partitioned
has been studied in the swarm founding wasps.
Polybia occidentalis has been shown to have com-
choose one site for building. In large complex plex interactions among the builders, pulp foragers
nests, like those built by termites, different areas of and water foragers, with smaller colonies having
the nest have distinct structures added at certain longer queuing delays that result in less efficient
times in the colonys reproductive cycle (e.g., plat- task partitioning. In another swarm founding
forms are built for dispersing reproductive allates.) species of wasp, Metapolybia spp., water or water
This array of different structural components chal- saturation of the colony appears to be a critical
lenges stigmergy because the builders cannot just regulator of task partitioning dynamics, with water
keep building based on previous construction and availability affecting water foraging, pulp foraging,
must switch to different building programs at and consequently, the number of builders.
appropriate times. Thus, building in highly eusocial As it has become clear that among insects,
insects must have a more complex regulatory individuals build by rather simple rules and act
mechanism or additional components to their independently of one another, it has become appar-
building program. Nonetheless, stigmergy has ent that colony wide behavior can be understood
been shown to be an important means for explain- as a culmination of all of these individual building
ing the regulation of construction in a wide array events. Self-organization is an epi-phenomenon
of species, insect and non-insect, social and seen in some aspects of social insect behavior. The
1044
C Construction Behavior of Insects

Construction Behavior of Insects, Figure 97 Some diverse types of insect construction: top left, pa-
per wasp nest showing detail of brood cells; top right, paper wasp nest early in construction showing
early formation of cells; second row left, tubes constructed by subterranean termites to maintain high
humidity as they seek food; second row right, mud dauber nest; third row left, pits for capture of ants
constructed by ant lion larvae; third row right, mound constructed by imported red fire ants; bottom row
left, tent constructed by eastern tent caterpillar larvae; bottom row center, paper wasp nest;
bottom row right, nests constructed by fall webworm larvae. (All photos by J. L. Castner, University
ofFlorida.)
 Contamination
C 1045

honey, pollen and brood storage pattern seen in Matthews RW, Matthews JR (1978) Insect behavior. Wiley,
New York, NY, 507 pp
honey bee combs can be explained through a self-
Ross KG, Matthews RW (eds) (1991) The social biology of
organizing process. Likewise, positive feedback wasps. Cornell University Press, Ithaca, NY, 678 pp
during construction can amplify small differences Turner JS (2000) The extended organism. Harvard University
in worker behavior, and can lead to the distinct and Press, Cambridge, MA, 235 pp
Von Frisch K (1974) Animal architecture. Harcourt Brace
repeated patterns of galleries observed in both ant Jovanovich, New York, NY, 306 pp
and termite nests. Computer modeling studies have
shown that, indeed, relatively simple rules and a
programmed responsiveness to the location and Consumption Efficiency
activity of other colony units within the virtual nest
can lead to clustered building and a chamber pat- The proportion of energy available that is con-
tern of walls and spaces similar to those of real sumed at a trophic level. In the case of herbivorous
nests and other repeating patterns seen in nature. insects, it is the proportion of net primary produc-
Modeling studies have also shown that relatively tivity that is ingested.
small changes in the building program can lead to
pronounced differences in the appearance of nests.
These results suggest a mechanism for the evolution Contact Poison
of the diversity in nest structures observed in nature.
A pesticide that acts after external contact of the
insect with the toxicant, and does not require
Conclusions ingestion to be effective.
Insecticides
Much of behavior is transient, with little in the way
of a permanent record left behind. Construction
behavior (Fig.97), however, does leave physical evi- Contagious Disease
dence behind that has even been fossilized. These
trace fossils include burrow remains, nests and such A disease which is naturally transmitted by hosts
things as the dung balls made by beetles some 3035 of the disease; synonymous with communicable
million years ago. The amazing fact is that fossilized disease.
ant nests from 60 million years ago show little
variation from those seen today, suggesting that at
least some social insects have not changed their
Containment
behavior over extremely long periods of time. Thus,
From a regulatory perspective, containment con-
the complex behaviors associated with insect
sists of phytosanitary measures in and around an
construction have been around for millions of
infested area to prevent spread of a pest.
years. Some of the evolutionary process and the
Risk Analysis (Assessment)
regulation of construction behavior is now under-
Regulatory Entomology
stood, but this area of insect biology remains a vital
Invasive Species
and fertile area for ongoing and future research.

References Contamination

Hansell MH (1984) Animal architecture and building behav- Harboring of, or contact with, microorganisms (or
iour. Longman, New York, NY, 324 pp other organisms such as insect parasites).
1046
C Continental Drift

Continental Drift temperatures, and the low temperatures have an

effect on insect mortality, while at other times the
The separation and movement of land masses in controlled atmosphere directly affects the desired
geologic time. insect control. Reported effects of controlled
atmosphere on insect physiology include the
reduction of NADPH levels in hypercarbonic
Controlled Atmosphere (>10% CO2) environments, a reduction in energy
Technologies for Insect Control charge as a result of slower production of ATP, the
production of glutathione is reduced, and the inhi-
Lisa Neven, Elizabeth Mitcham bition of the regeneration of choline to acetylcho-
USDA, ARS, Wapato, WA, USA line under hypercarbonic environments. There is
University of California, Davis, CA, USA also an observed reduction of high temperature
tolerance in insects exposed to anoxic environments.
Controlled atmosphere treatments have been Controlled atmosphere can also mean con-
employed to control stored products pests for cen- trolling the environment surrounding an insect,
turies. The first example is the storage of grains in meaning the temperature, light, humidity, pres-
ancient Egypt, where the cribs were sealed tightly sure, and atmospheric gases. Any postharvest
to prevent the propagation and growth of insects situation allows for the manipulation of the envi-
through the use of lowered oxygen environment. ronment for pest control. Traditionally, controlled
Historically, controlled atmosphere treatments atmospheres means the alteration of atmospheric
were designed to preserve commodity quality dur- gases, such as oxygen and carbon dioxide. This can
ing long-term storage. The secondary effect of be achieved through the use of flow-through sys-
providing some level of insect control was seren- tems in which oxygen is lowered by a nitrogen
dipitous. Sometimes the controlled atmosphere purge and carbon dioxide is increased by injection
provides extra time to store a commodity at low of this gas. The levels of oxygen and carbon dioxide

Controlled Atmosphere Technologies for Insect Control, Table 19 USDA-APHIS approved controlled
atmosphere treatments for fresh fruits as of 2007
Percentage Temperature Heating rate Total
Commodity Pest O2 CO2 C C/hr Time
Apple Codling Moth & 1 15 46 12 3h
Oriental Fruit
Moth
Cherry Codling Moth & 1 15 47 >200 25 min
Western Cherry
Fruit Fly
Cherry Codling Moth & 1 15 45 >200 45 min
Western Cherry
Fruit Fly
Nectarines & Codling Moth & 1 15 46 24 2.5 h
Peaches Oriental Fruit
Moth
Nectarines & Codling Moth & 1 15 46 12 3.0 h
Peaches Oriental Fruit
Moth
 Controlled Atmosphere Technologies for Insect Control
C 1047

Controlled Atmosphere Technologies for Insect Control, Table 20 Some potential controlled atmosphere
treatments to control arthropod pests in fresh fruits and vegetables
Percentage Temperature Time
Commodity Pest O2 CO2 (C) (Days)
Apple San Jose scale <1 >90 >12 2
Apple San Jose scale 0 96 22 1
Apple Codling moth 1.52 <1 0 91
Apple Mites 1.0 1.0 20.8 160
Apple 4 tortricid pests 0.4 5.0 40 >0.6
Asparagus Aphid & thrips 8.4 60 01 4.5
Strawberry Thrips 1.92.3 88.790.6 2.5 2
Sweet potato Sweetpotato 4 60 25 7
weevil
Sweet potato Sweetpotato 2 40 25 7
weevil
Sweet potato Sweetpotato 2 60 25 7
weevil
Table grapes Mites, thrips, 11.5 45 2 13
omnivorous
leafroller
Walnut Codling moth 8.4 60 25 7
Mango Fruit flies
Broccoli Thrips 0.0025
Lettuce Thrips 0.0025

used in controlled atmosphere treatments vary in MAP: Modified atmosphere packaging.

relation to commodity tolerance and insect intol- Vacuum: Reduction of atmosphere through evacuation.
erance. The levels of atmospheric gases necessary Reduction of atmospheric pressures below STP.
to kill a target pest will vary in relation to the pest/ STP: Standard temperature and pressure. Internationally,
commodity complex. the current STP defined by the IUPAC (Internati-
Controlled atmosphere technologies have onal Union of Pure and Applied Chemistry) is an
unique terminology associated with them. Some absolute pressure of 100 kPa (1 bar) and a tempe-
of the important terms/acronyms and their defini- rature of 273.15K (0C).
tions are: Hypobaric treatments: Reduction of atmospheric pres-
sures below STP.
Controlled atmosphere (CA): Alteration of the chemical Hyperbaric treatments: Increase of pressure above STP.
content of the air environment from that normally Film wraps: Plastic impermeable or semi-permeable
experienced at STP. wraps of fresh fruits and vegetables to reduce
Chilling mortality: Death of an organism due to cumu- respiration and dehydration.
lative, non-freezing, low temperature damage. Coatings: Usually wax or shellac type mixtures that
Anoxic: Low oxygen to no oxygen environment. cover fruits and vegetables to reduce respiration
Hypercarbonic: High carbon dioxide environment. and dehydration.
1048
C Controlled Atmosphere Technologies for Insect Control

Low Oxygen at temperatures within the normal growing range

(1040C). High carbon dioxide treatments have
The most common types of controlled atmosphere been shown to be very effective in controlling
treatments are those that employ low oxygen envi- mites and diapausing insects. However, when ele-
ronments. In the case of apples, oxygen levels vary vated carbon dioxide is used in combination with
from 1 to 5%, and carbon dioxide levels can vary low oxygen levels, the results on insect mortality
from 0.3 to 3%. Other treatments use ultra low have been variable. Combination high tempera-
levels of oxygen, such as the case with broccoli, ture and controlled atmosphere treatments used
which employs oxygen levels of 0.0025%. Both of effectively against lepidopteran pests do not work
these treatments are performed at temperatures as effectively against fruit flies. This may be due to
well below 5C. the differences in the respiratory systems and reg-
Low oxygen treatments can be effective in ulatory mechanisms of terrestrial (Lepidoptera)
killing insects provided that the temperature is and semi-aquatic (fruit fly larvae) insects. At low
high enough to put a stress on the metabolic sys- temperatures, near 0C, mortality of the moth
tem of the insect. Reduced O2 consumption leads Platynota stultana is greater with 45 kPa O2+11.5
to a decreased rate of ATP production. As a result kPa O2 (air) as compared with 45 kPa CO2+0.5
of energy insufficiency, the membrane ion pumps kPa O2. In some cases, when only a small amount
fail, leading to K+2 efflux, Na+ influx, and mem- of CO2 is present in an O2-deficient atmosphere, it
brane depolarization. The voltage-dependent Ca+2 can enhance mortality by up to ten-fold.
gates are then opened, causing Ca+2 influx. The Elevated CO2 (hypercapnia) can reduce the
high Ca+2 concentration in the cytosol activates rate of insect respiration. High levels of CO2 can
phospholipases and leads to increased membrane reduce oxidative phosphorylation by inhibiting
phospholipid hydrolysis. The cell and mitrochon- respiratory enzymes such as succinate dehydroge-
drial membranes become further permeable, causing nase and malic enzyme. Reduced oxidative phos-
cell damage or death. phorylation leads to reduced ATP generation,
Omnivorous leafroller pupae use metabolic which in turn leads to a failure of membrane ion
arrest as a major response to hypoxia. The pupaes O2 pumps, membrane depolarization and eventual
consumption rate and metabolic heat rate decrease cell death, as described for hypoxia.
slightly with decreasing O2 concentration until a Elevated CO2 levels can decrease pH through
critical concentration is attained, below which the the formation of carbonic acid. Reduced pH can
decrease become rapid. The critical concentration increase intercellular Ca2+ concentration, which
points are 10, 8 and 6 kPa at 30, 20 and 10C, respec- causes the cell and mitochondrial membranes to
tively. Although the pupaes metabolism decreases become more permeable, suggesting that high CO2
quickly below the critical concentration points, the can increase membrane permeability. High CO2
pupae do not initiate anaerobic metabolism until levels can alter the ratio of pyruvate to lactate by
the O2 concentration is below 2 kPa at 20C. Con- 25% of normal, changing the redox potential and a
centrations of O2 below the anaerobic compensation lesion in the electron transport chain, presumably
point appear to be in the insecticidal range. by a modification in the permeability of mito-
chondrial membranes.

High Carbon Dioxide

Modified Atmosphere Packaging
There are other treatments that use carbon dioxide
levels of 60% or greater, with the oxygen level not Controlled atmosphere can also be achieved
being regulated. These treatments have been used through the use of semi-permeable membranes,
 Controlled Atmosphere Technologies for Insect Control
C 1049

called modified atmosphere packaging, which tolerate this treatment, exposure to insecticidal
reduces the movement of oxygen and carbon diox- atmospheres for this length of time, even at low
ide. Modified atmosphere packaging is generally temperatures, would not be tolerated by many
performed at temperatures between 020C, with fresh commodities.
118% O2, and 010% CO2, and is of a long dura- There has been considerable research on con-
tion, generally weeks to months. Modified atmo- trolled atmosphere at intermediate temperatures
sphere packaging can also be generated using film (1028C), but interest in this approach has been
wraps. Also, film coverings and coatings can form diminishing due to increasing research on high tem-
modified atmospheres in fresh horticultural com- perature CA treatments (4055C). The advantage
modities. These treatments are usually carried out of intermediate temperature controlled atmosphere
at 2027C, for long durations, with variable levels treatments is that they range from hours to days,
of atmospheric gases, depending on commodity much faster than low temperature controlled atmo-
respiration rates and film permeability. The com- sphere treatments. However, high temperature
modity will consume oxygen and increase carbon controlled atmosphere treatments have gained pop-
dioxide during normal respiration processes. Nor- ularity because the treatments are relatively short
mally, the reduction of oxygen and elevation of and easy to apply. High temperature controlled
carbon dioxide are not as severe because there is a atmosphere applies two simultaneous stresses, which
point where either the level of oxygen will no lon- greatly reduces total treatment time and minimizes
ger support commodity respiration or the level of commodity phytotoxicity due to elevated tempera-
elevated carbon dioxide is inhibitory to commod- tures. In fact, high temperature controlled atmo-
ity respiration. Therefore, modified atmosphere sphere treatments may be beneficial for climacteric
packaging often takes longer to kill the target pest. fruits (fruits that continue to ripen after harvest)
because the elevated temperatures knock out many
of the enzymes involved in fruit ripening, and there-
Temperature Combinations fore extends shelf life. High temperature controlled
atmosphere treatments appear to block thermal
Temperature control has been a traditional means acclimation by blocking the synthesis of heat shock
of controlling the environment to affect insect proteins due to lack of oxygen, wherein the elevated
mortality. Typically, low temperature has been the carbon dioxide inhibits respiration and alters inter-
means used to control postharvest pests. Low tem- nal pH, causing systematic breakdown of oxidative
peratures work because they are usually below phosphorylation and electron transport.
the optimal growth and development tempera- Hot water dips not only raise temperature, but
tures of most insect species. Low temperature alter the levels of atmospheric gases in the commod-
causes mortality through cumulative, systemic ity. As temperature rises, oxygen level in the com-
tissue and metabolic damage, and the inability to modity is reduced and carbon dioxide is elevated.
repair that damage. Unfortunately, low tempera- This is due to the interaction of cuticle permeability
ture controlled treatments require a significant and ability of the gases to dissolve in water.
time, measured in days, weeks, or even months,
to affect insect mortality. The advantage of low
temperature controlled atmosphere is that it could Ozone, Other Chemicals and
be applied during marine transit. A 13 day treat- Processes
ment with 45 kPa CO2 (11.5 kPa O2) at 2C or
lower has been developed for control of Pacific Ozone has typically been used for control of post-
spider mite, western flower thrips and omnivorous harvest diseases. However, the advances in ozone
leafroller on table grapes. Although table grapes generation and application of vacuum has allowed
1050
C Controlled Atmosphere Technologies for Insect Control

for treatments to be developed for arthropod inexpensive, and are needed only when the pro-
pests. The problem with ozone is that it is non- tocol calls for CO2 levels higher than the com-
penetrating and can only effectively control exter- modity can produce. Modified atmosphere
nal pests. Also, ozone penetration is inhibited by packaging is found in every aspect of the fresh
water. So, wet commodities are poor candidates food market. Each modified atmosphere packag-
for ozone treatments. In addition, there may be ing system provides an affordable and portable
some problems with ozone if the commodities controlled atmosphere system.
have green stems and leaves. Ozone decomposes
chlorophyll and may cause a bleaching effect of
green commodities. Approved Treatments
Hypobaric treatments have been gaining
popularity. These treatments work by reducing To date there are only a few controlled atmosphere
atmospheric pressures below STP (Standard Tem- treatments in the USDA, APHIS treatment manual
perature and Pressure), and in turn reduce both the (see approved controlled atmosphere table). These
availability of oxygen and the ability of the spiracles treatments were the first to be approved and were
to remain closed. This may cause anoxia and desic- only entered into the Federal Register on April 16,
cation stress, resulting in mortality of the insect. 2007. These treatments employ a combination of
Only recently, hyperbaric or hydrostatic controlled atmosphere (Fig.98) and hot forced air
pressures have been tested for controlling inter- (called CATTS for Controlled Atmosphere Tem-
nal feeding insects. This technology uses very perature Treatment System). Other controlled
high pressures of 10,00080,000 psi, pressures atmosphere treatments have been developed (see
experienced in the deep ocean environments, to potential controlled atmosphere table), but are
disinfest and decontaminate foods. It is not not yet in the APHIS treatment manual.
known how these very high pressures kill insects, Adoption of controlled atmosphere quaran-
but it is presumed that it causes protein denatur- tine treatments by industry has been slow because
ation and wide-scale tissue break-down. of the wide availability of chemical fumigants like
methyl bromide. Although methyl bromide was
identified as an ozone depleter under the Montreal
Machinery Protocol, its use for commodity disinfestations is
still allowed while other uses, such as soil and
The most attractive feature of controlled atmo- structural fumigations, are restricted. The cost of
sphere treatments is the wide range of locations methyl bromide has rapidly increased from US$5
and situations where it can be applied. Controlled for a 100 lb. tank in 1995 to nearly US$1,000 in
atmosphere treatments can be applied in huge 2007. As fumigation costs rise, alternative, non-
warehouses, individual pallets in cold rooms, chemical quarantine treatments will gain industry
specially designed heat/controlled atmosphere support and become more common.
chambers, hot water dipping tanks, shipping con-
tainers in transit, in individual boxes (via modi- References
fied atmosphere packaging), and in individual
fruits (via wraps and coatings). With todays tech- Edwards LJ (1968) Carbon dioxide anaesthesia and succinic
nology, controlled atmosphere is becoming more dehydrogenase in the corn earworm, Heliothis zea.
affordable and portable. Nitrogen generators JInsect Physiol 14:10451048
Fanestil DD, Hastings AB, Mahowald TA (1963) Environ-
needed to form low oxygen environments are
mental carbon dioxide stimulation of mitochondrial
becoming more compact and affordable. Com- adenosine triphosphate activity. J Biol Chem
pressed tanks of carbon dioxide are still relatively 238:836842
 Cooloola Monsters
C 1051

Herreid CF (1980) Hypoxia in invertebrates. Comp Biochem

Physiol (A) 67:311320
Hochachka PW (1986) Defense strategies against hypoxia
and hypothermia. Science 231:234241
Mitcham EJ, Zhou S, Bikoba V (1997) Controlled atmosphere
for quarantine control of pests of table grape. J Econ
Entomol 90:13601370
Neven LG, Mitcham EJ (1996) CATTS (controlled atmo-
sphere/temperature treatment system): a novel tool
for the development of quarantine treatments. Am
Entomol 42:5659
Neven LG (2005) Combined heat and controlled atmosphere
quarantine treatments for control of codling moth,
Cydia pomonella, in sweet cherries. J Econ Entomol
98:709715
Neven LG, Rehfield-Ray LM (2006) Combined heat and
controlled atmosphere quarantine treatment for control
of western cherry fruit fly in sweet cherries. J Econ
Entomol 99:658663
Neven LG, Rehfield-Ray L, Obenland D (2006) Confirmation
and efficacy tests against codling moth and oriental fruit
moth in peaches and nectarines using combination heat
and controlled atmosphere treatments. J Econ Entomol
99:16101619
Neven LG, Rehfield-Ray L (2006) Confirmation and effi-
cacy tests against codling moth, Cydia pomonella, and
oriental fruit moth, Grapholitha molesta, in apples
using combination heat and controlled atmosphere
treatments. J Econ Entomol 99:16201627
Zhou S, Criddle RS, Mitcham EJ (2000) Metabolic response of
Platynota stultana pupae to controlled atmospheres and
its relation to insect mortality response. J Insect Physiol
46:13751385
Zhou S, Criddle RS, Mitcham EJ (2001) Metabolic response
of Platynota stultana pupae during and after extended
Controlled Atmosphere Technologies for Insect exposure to elevated CO2 and reduced O2 atmospheres.
J Insect Physiol 47:40140
Control, Figure 98 A commercial CATTS
(controlled atmosphere temperature treatment
system) can accommodate various types of
produce and packaging, and produce insect-free
products. Convergent Evolution
The evolution of unrelated species or lineages
Fleurat-Lessard F (1990) Effect of modified atmospheres resulting in similar structures and behaviors.
on insects and mites infesting stored products. In:
Calderon M, Barkai-Golan R (eds) Food preservation
by modified atmospheres. CRC Press, Boca Raton, FL,
pp 2138
Friedlander A (1983) Biochemical reflections on a non-chemical
control method. The effect of controlled atmospheres Cooloola Monsters
on the biochemical processes in stored product
insects. In: Proceedings of the third international A family of crickets (Cooloolidae) in the order
working conference on stored product entomology.
Kansas State University, Manhattan, Kansas, pp Orthoptera.
471486 Grasshoppers, Katydids and Crickets
1052
C Cooloolidae

Cooloolidae Copularium
A family of crickets (order Orthoptera). They The initial chamber constructed by a pair of col-
commonly are known as cooloola monsters. ony-founding termites.
Grasshoppers, Katydids and Crickets

Coquillett, Daniel William

Cooties
Daniel Coquillett was born on a farm in Illinois on
A popular term applied to human body lice. January 23, 1856. He collected insects while a
Human Lice youth, and published his first entomological paper
Chewing and Sucking Lice (Phthiraptera) On the early stages of some moths in the Cana-
dian Entomologist in 1880. However, he developed
an incipient tuberculosis, and his parents moved
Coppers
the family to Anaheim, California, in 1882. There,
Some members of the family Lycaenidae (order he began to specialize in flies. His entomological
Lepidoptera). activities drew the attention of C.V. Riley who
Gossamer-Winged Butterflies appointed him as a U.S. Department of Agricul-
Butterflies and Moths ture field agent in 1885. He worked on chemical
control of pest insects (Fig.99) and on part of the
cottony cushion scale biological control program.
Copromorphidae At the same time, he continued his studies of
Diptera, especially bee flies and robber flies. When
A family of moths (order Lepidoptera). They com- C.V. Rileys relationships with California growers
monly are known as tropical fruitworm moths. become strained in 1893, Coquillet was called to
Tropical Fruitworm Moths Washington, DC, and was made an honorary
Butterflies and Moths

Coprophagous
Feeding on fecal material.

Coprophagy
Feeding on dung or excrement by animals. Such
arthropods are said to be coprophagous or
coprophages.
Food Habits of Insects

Coptopsyllidae
A family of fleas (order Siphonaptera). Coquillett, Daniel William, Figure 99 Daniel
Fleas W. Coquillett.
 Corazonin
C 1053

custodian of the Diptera collections in the U.S. moths, but no cardio-stimulating action is found
National Museum. There, he published extensively in any of these other insects. In the sphinx moth,
on Tachinidae, Simuliidae, Culicidae, and other Manduca sexta, this molecule plays a role in con-
flies, eventually describing about 1,000 species. A trolling eclosion. [Thr4, His7]-corazonin occurs
major work was his (1910) Type species of North in the European commercial honey bee, Apis
American Diptera. He died on July 7, 1911, and mellifera, but its function is yet to be elucidated.
his Diptera collection became part of the US The last molecule is [His7]-corazonin that has
National Museum. been identified from a stick insect, a grasshop-
per, and locusts. Immunohistochemical observa-
tions indicate that corazonin is synthesized in
Reference the brain and sent via the axon to the corpus car-
diacum where it is presumably secreted into the
Mallis A (1971)Daniel William Coquillet. In: American ento- hemolymph in some insects. In locusts and
mologists. Rutgers University Press, New Brunswick, NJ, grasshoppers, corazonin induces melanization
pp 389391
and also has other physiological functions, as
described below in association with phase
polyphenism.
Coral Treaders

Members of the family Hermatobatidae (order Role of Corazonin in the Control of

Hemiptera). Body-Color Polymorphism in
Bugs Locusts

In 1921, B.P. Uvarov proposed the phase theory

Corazonin to explain that locusts that had been regarded as
two distinct species (Locusta danica and L.
Seiji Tanaka migratoria) belonged to the same species, which
National Institute of Agrobiological Sciences was designated as L. migratoria. According to
(Ohwashi), Tsukuba, Ibaraki, Japan his theory, locusts display body-color polyphen-
ism in response to population density and some
Corazonin is a neuropeptide that is found in environmental factors. Locusts under low pop-
many insects. It consists of 11 amino acid resi- ulation density are called solitarious phase,
dues, and three molecule types are known whereas those under high population density
(Fig. 100). [Arg7]-corazonin was the first mole- are called gregarious phase. Solitarious nymphs
cule discovered, from the cockroach Periplaneta are uniformly colored. Their body color is cryp-
americana, and is a potent cardio-stimulating tic and assumes green, brown, yellow, reddish,
neuropeptide. It has been found in other species grey, or black depending on the background
including other cockroaches, a cricket, and color of their habitat. In contrast, gregarious

pGlu-Thr-Phe-Gln-Tyr-Ser-Arg-Gly-Trp-Thr-Asn-amide [Arg7]-corazonin

pGlu-Thr-Phe-Thr-Tyr-Ser-His-Gly-Trp-Thr-Asn-amide [Thr4, His7]-corazonin

pGlu-Thr-Phe-Gln-Tyr-Ser-His-Gly-Trp-Thr-Asn-amide [His7]-corazonin

Corazonin, Figure 100 Corazonin molecule types. Different amino acids are emphasized.
1054
C Corazonin

nymphs develop black patterns with an orange Albino nymphs injected with [His7]-cora-
background color. Locusts growing under zonin (Fig.101) develop not only black patterns
intermediate population densities are often but also various other colors depending on the
called transient phase and display intermediate dose and the timing of the injection. Nymphs
body coloration. Juvenile hormone (JH) is with a completely black body color appear if
responsible for the induction of green color. they are injected with a high dose of the neuro-
Because the green body color is common among peptide at the beginning of the previous sta-
solitarious locusts, JH was once believed to con- dium, whereas those injected with lower doses
trol the phase-related body-color polyphenism. at the same stage turn brown, light brown or
The administration of JH to gregarious nymphs yellow in the following nymphal stadium. Uni-
causes them to lose the black patterns and formly reddish body coloration appears in
induces green color, but destruction of the cor- nymphs injected with the hormone shortly
pus allatum, the gland producing JH, does not before the previous ecdysis. These body colors
induce black patterns. An albino mutant strain are similar to those normally observed in soli-
of L. migratoria was used to study the hormonal tarious nymphs of L. migratoria in the field.
control of body color polyphenism. This strain Green solitarious nymphs are brownish or red-
was derived from a laboratory culture in Japan, dish in the ventral side of the body as well as
and the albinism is a recessive trait controlled some portions of the legs. Such body coloration
by a simple Mendelian unit. The possible can be induced in albino nymphs when both JH
involvement of a neuropeptide in the control and corazonin are injected. As previously men-
of body-color polymorphism was noticed in tioned, gregarious nymphs typically develop
L. migratoria in which albino nymphs turned black patterns with an orange background color.
darker after receiving an injection of methanol This type of body coloration can also be induced
extracts of brains and corpora cardiaca taken by injection of [His7]-corazonin at a certain
from normal (pigmented) nymphs. The extracts stage in albino nymphs. It is highly likely that
are heat-stable, but lose the dark-color inducing changes in corazonin concentration control the
activity after incubation with a proteinase. This expression of body coloration in the locust. For
dark-color inducing factor was later demon- a certain type of body coloration to be main-
strated to be identical to [His7]-corazonin. The tained in successive nymphal stadia, the specific
albinism of the above strain is caused by defi- changes in corazonin and JH concentrations
ciency of this neuropeptide. required for the expression would be repeated

Corazonin, Figure 101 Albino Locusta migratoria nymphs. The individual on the right was injected with
corazonin in the previous stadium.
 Corazonin
C 1055

in each stadium. The hormonal induction of

solitarious and gregarious body coloration is
independent of the rearing density.
Other locusts and grasshoppers also show
body-color polyphenism and corazonin appears
to be present in their central nervous system
and corpora cardiaca. Transplantation of their
brain and corpora cardiaca into albino L. migra-
toria induces darkening in the latter. Injection
of [His7]-corazonin causes darkening in all
locusts and grasshoppers so far tested. In the
desert locust, Schistocerca gregaria, and the
American grasshopper, S. americana, [His7]-
corazonin has been isolated and is responsible Corazonin, Figure 102 Effect of corazonin injection
for the induction of black patterns, but not the on morphometric ratios in Locusta migratoria.
background color. An albino strain is known for (Based on data of Tanaka et al., 2002. Reproduced
S.gregaria that is inherited by a simple Mende- with permission of Journal of Insect Physiology.)
lian unit, as in the case for L. migratoria. How-
ever, the albinism in the former is caused by injection of [His7]-corazonin induces morpho-
some unknown mechanism other than defi- metric gregarization in isolated-reared adults
ciency of [His7]-corazonin, because this of L.migratoria and S. gregaria. This gregariz-
neuropeptide is present in this strain. Some ing effect is greater as the injections are made
katydids display body-color variation. The earlier during nymphal development.
albino bioassay suggests that their brain also
contains corazonin or a similar compound, but
injection of [His7]-corazonin has no biological
activity on the body color in the katydids. Effect of Corazonin on the
Formation of Antennal Sensilla

Effect of Corazonin on Body Shape Locusts have several types of sensilla on the
antennae. In S. gregaria and L. migratoria, the
The body dimensions of locusts are affected total number of antennal sensilla is greater in
by crowding. Morphometric ratios (Fig. 102) solitarious adults than in gregarious ones,
of F/C and E/F (F = hind femur length; although the significance of this difference is
C=maximum head width; E=forewing length) unknown. Corazonin causes locusts reared in
are often used to evaluate the degree of gre- isolation to develop fewer antennal sensilla when
garization or solitarization. Gregarious adults injected during the nymphal stage as compared
have a smaller F/C ratio and a larger E/F ratio with oil-injected counterparts, and the total
than solitarious adults. In the laboratory, simi- number of antennal sensilla in the former
lar values can beobtained by rearing locusts in becomes similar to that for locusts reared in
a group or in isolation. Neither JH nor molting groups. Among the four major antennal sensilla
hormone influences these ratios in a consistent (Figs. 103 and 104), basiconic sensilla do not
manner, indicating that these hormones play show a phase-specific difference in abundance.
no major role in the control of phase-related Injection of corazonin does not influence the
changes in body shape. On the other hand, abundance of this sensillum. As in the case for
1056
C Corazonin

Corazonin, Figure 103 Four types of antennal sensilla in Schistocerca gregaria. A: basiconic sensillum
type with high density of pores; B: basiconic sensillum type B with low density of pores; C: c oeloconic
sensillum; D: trichoid sensillum with a terminal pore in the inset. (After Maeno and Tanaka, 2004.
Reproduced with permission of Journal of Insect Physiology.)

morphometric gregarization, the earlier the

injection of corazonin during nymphal develop-
ment the greater the effect on the total abundance
of antennal sensilla in the adult stage.

Corazonins in Other Insects

Corazonins have been chemically identified in

only a small number of species. It is highly
likely that more than three molecular types of
corazonin exist in insects. Immunohistochemi-
cal observations are a powerful tool to visualize
Corazonin, Figure 104 The n umber of sensilla. the presence and localization of corazonin
(After Maeno and Tanaka, 2004. Reproduced with and similar compounds in many species,
permission of Journal of Insect Physiology.) although this technique still requires laborious
 Corazonin
C 1057

Corazonin, Figure 105 Dark-color inducing activity of various organs from a heelwalker,
Hemilobophasma montaguensis when implanted into albino nymphs of Locusta migratoria. (After Tanaka,
2006. Reproduced with permission of Applied Entomology and Zoology.)

procedures. Probably the easiest and fastest (Fig. 105). These observations suggest that
method to detect corazonin is use of the albino corazonin or a similar molecule is widespread
L. migratoria strain as a bioassay. As mentioned in the Insect class including pterygote and
earlier, implantation of a brain or corpora car- apterygote insects except for the Coleoptera.
diaca taken from normal locusts into albino Polyphenism in Insects and Juvenile Hormone
nymphs causes the latter to turn darker. Using (JH)
this method, more than 90 species of insects Phase Polymorphism in Locusts
have been checked. The results indicate that Grasshoppers and Locusts
insects belonging to a total of 19 insect orders
have been shown to have a dark-color inducing
activity (Table21) when their brain or/and cor- References
pora cardiaca were implanted into albino
locusts. This includes both pterygote and Pener MP (1991) Insect phase polymorphism and its endo-
apterygote orders of insects, indicating that crine relations. Adv Insect Physiol 23:179
corazonin or a corazonin-like compound is old Pener MP, Yerushalmi Y (1998) The physiology of locust poly-
phenism, an update. J Insect Physiol 44:365377
in origin. Interestingly, no coleopterans show a Tanaka S (2001) Endocrine mechanisms controlling body-
sign of corazonin activity, which is also sup- color polymorphism in locusts. Arch Insect Biochem
ported by immunohistochemical evidence. Physiol 47:139149
Brains and corpora cardiaca taken from twisted- Tanaka S (2006) Corazonin and locust phase polyphenism.
Appl Entomol Zool 41:179193
winged parasites, Strepsiptera, which are often Uvarov B (1966) Grasshoppers and locusts, vol 1. Cambridge
placed in the order Coleoptera, display a dark- University Press, Cambridge, UK, 481 pp
color inducing activity when implanted into Uvarov B (1977) Grasshoppers and locusts, vol 2. Centre for
Overseas Pest Research, London, UK, 475 pp
albino locusts. Heelwalkers, belonging to a
Veenstra JA (1991) Presence of corazonin in three species
recently discovered new insect order, Manto- and isolation and identification of [His7] corazonin
phasmatodea, also have a positive response from Schistocerca americana. Peptides 12:12851298
1058
C Corbicula

Corazonin, Table 21 A list of insects tested by the Corduliidae

albino bioassay for dark-color inducing activity.
Class Order No. species A family of dragonflies (order Odonata).
testeda They commonly are known as green-eyed
Insecta Thysanura 1/1 skimmers.
Ephemenoptera 2/2 Dragonflies and damselflies
Odonata 3/3
Orthoptera 18/18
Phasmatidae 1/1 Coreidae
Mantophasmatodea 1/1
Dictyoptera 6/6 A family of bugs (order Hemiptera). They some-
times are called leaf-footed bugs.
Dermaptera 1/1
Bugs
Isoptera 2/2
Plecoptera 2/2
Hemiptera 9/9
Neuroptera 1/1 Coreid Bugs and Relatives:
Mecoptera 1/1
Coreidae, Stenocepahidae,
Alydidae, Rhopalidae, and
Trichoptera 6/6
Hyocephalidae (Hemiptera:
Lepidoptera 11/11
Coreoidea)
Diptera 7/7
Hymenoptera 7/7 ngeles Vzquez
Strepsiptera 2/2 Universidad Complutense de Madrid, Madrid,
Coleoptera 0/13 Spain

a
No. of species with a positive response/No. of species
tested. The superfamily Coreoidea of the suborder Het-
eroptera includes principally phytophagous bugs,
but also some coprophagous and carrion feeding
species. Ocelli are present on the head and the
Corbicula antennae are four-segmented (Fig. 106). Usually
their metapleural scent-gland peritremes (plates
A pollen basket. A specialized scopa, or pollen hold- on the metapleural scent glands) are well devel-
ing apparatus, found in bumble bees and honey oped, with showy orifices that emit a strong scent.
bees. The corbicula consists of the broad, concave Coreoidea consists of five families:
hind tibia surrounded by a fringe of long hairs. Order Hemiptera
Suborder Heteroptera
Infraorder Pentamorpha
Superfamily Coreoidea
Cordulegastridae Family Stenocephalidae
Family Coreidae
A family of dragonflies (order Odonata). They Family Alydidae
commonly are known as biddies. Family Rhopalidae
Dragonflies and Damselflies Family Hyocephalidae
 Coreid Bugs and Relatives: Coreidae, Stenocepahidae, Alydidae, Rhopalidae, and Hyocephalidae (Hemiptera: Coreoidea)
C 1059

Coreid Bugs and Relatives: Coreidae, Stenocepahidae, Alydidae, Rhopalidae, and Hyocephalidae
(Hemiptera: Coreoidea), Figure 106 Coreoid bugs: (a) adult red-shouldered bug, Jadera haematoloma
(Rhopalidae) by golden rain tree seed, a favorite food; (b) nymph of J. haematoloma; (c) adult
1060
C Coreid Bugs and Relatives: Coreidae, Stenocepahidae, Alydidae, Rhopalidae, and Hyocephalidae (Hemiptera: Coreoidea)

Stenocephalidae modified hind legs for territorial combat. They show

varied coloration, though in temperate climates they
The small family Stenocephalidae, with two genera are generally brown or gray, and more or less dark. In
and over 30 species, possesses intermediate charac- tropical and subtropical countries, they sometimes
ters between Lygeidae and the Coreidae. This fam- are colorful. In coreids, the head tends to be small in
ily is restricted to the Eastern Hemisphere. The relation to the body and generally is shorter than the
greatest species diversity occurs in the Afrotropical pronotum. The antennae are four segmented. Meta-
Region. Stenocephalids are phytophagous, and pleural scent-gland peritremes are well developed.
often polyphagous. Many species in the Palaearctic Currently, the family is considered to consist
region live in association with Euphorbiaceae. of four subfamilies: Agriopocorinae, Coreinae,
Meropachydinae and Pseudophloeinae. Agriopo-
Stenocephalidae are slender bugs, 816 mm corinae contains Australian coreids that are flat-
long. The head is elongated, subtriangular, with tened and generally wingless. They possess spiracles
mandibular plates longer than the clypeus. The buc- on abdominal segments 2 and 3 that are visible
culae are short and explanate (flat and spreading). from above. The vast majority of coreid bugs are
The antennae four segmented. Metathoracic glands contained on the Coreinae. They display very dif-
are present. The abdominal spiracles are located ferent shapes and sizes. They have a median sulcus
ventrally. Females oviposit on plant surfaces. (groove) on the head in front of the eyes. The tibiae
possess deep grooves on the outer surface. The
abdominal spiracles are not visible from above.
Coreidae This subfamily includes many tribes throughout
the world, but mainly in warmer regions. The
This family consists of over 1,800 species and 250 Meropachydinae include over 12 genera with a
genera, and is worldwide in distribution. Various small head, the hind femora large, and hind tibiae
groups are commonly called leaf-footed bugs, with the distal end produced into a spine or tooth.
squash bugs or pod bugs. The family Coreidae was The abdominal spiracles are not visible from above.
established by Leach in 1815 and included the This subfamily is restricted to the Neotropical
present families Alydidae and Rhopalidae. All of Region. The Pseudophloeinae are relatively small
them plus the Stenocephalidae have numerous in size. Their head does not have a medial sulcus in
veins in the membrane of the hemelytra. front of the eyes, the tibiae are not grooved (sul-
Coreids vary in size from 5 mm to more than 4 cate) on the outer surface, and the abdominal spir-
cm and although most have a robust body, some are acles are not visible from above. This subfamily
thin or display peculiar legs and antennae and even consists of about 28 genera and 165 species, and is
spiny or hairy bodies. In some species, males use the mainly old-world in distribution.

Stenocoris sp. (Alydidae), sometimes known as broad-headed bugs or rice bugs; (d) adult of cactus bug,
Chelinidea vittiger (Coreidae), a species commonly associated with prickly pear cactus
(Optuntia spp.) in North America; (e) adult of squash bug, Anasa tristis (Coreidae), a serious pest of
squash in North and Central America; (f) adult golden egg bug, Phyllomorpha laciniata (Coreidae)
with eggs carried on its back; (g) adult Euthochtha galeator (Coreidae) is found widely in eastern North
America where it occasionally can become a pest, feeding on such plants as oranges and roses; (h) adult
Leptoglossus p hyllopus (Coreidae), one of the most damaging of the leaffooted bugs in North America,
where it feeds on fruits, vegetables, grains and other crops. (photo credits: a, b, d, g, Lyle Buss; f, Arja
Kaitala; c, e, h, John Capinera).
 Coreid Bugs and Relatives: Coreidae, Stenocepahidae, Alydidae, Rhopalidae, and Hyocephalidae (Hemiptera: Coreoidea)
C 1061

Most coreids are phytophagous, feeding on have suggested alternative explanations, such as the
seed or fruit. A few species are considered to be of notion that this behavior results from the egg-laying
economic importance. Cucurbits, various nut and female behaving as an intraspecific parasite.
fruit trees, rice, legumes and greenhouse vegeta-
bles are crops damaged by coreids worldwide.
They even can attack conifers, junipers and Euca- Alydidae
lyptus. Among the economically important species
is the squash bug, Anasa tristis, which occurs from The Alydidae, which are called broad-headed bugs,
Brazil to Canada, and is especially a pest in Mexico are a cosmopolitan family known worldwide. It
and the USA. The genus Leptoglossus has more includes about 42 genera and over 250 species,
than 40 species and variable feeding habits. For- with most living in the subtropical and tropical
merly this genus was restricted to the Western regions. Many alydid nymphs are dark red-brown,
Hemisphere, but there have been introductions to and some adults look like ants or wasps.
Europe (Italy and Spain) and to northern Africa. Alydidae includes three subfamilies: Alydinae
Some species are serious pests, such as the polypha- that feed mainly on Fabaceae, and Micrelytrinae
gous Leptoglossus occidentalis and L. phyllopus. and Leptocorisinae that feed predominantly on
Coreids are not generally thought of as plant grasses. The body and appendages of alydids are
virus vectors, but their feeding secretions can be elongated. The head is subtriangular. The head rela-
toxic, causing phytotoxicity. Also, they are associ- tively broad, with the width greater than half the
ated with the transmission of fungi and other width of the posterior margin of the pronotum. The
pathogens. bucculae is shorter than the antennal insertion. Two
Few behavioral studies have been done on ocelli are present, but they are not found on tuber-
Coreidae, although it is known that some males with cles. The metathoracic glands have distinct external
large femora fight for territory, and that some employ peritremes, and they often produce a foul odor. The
pheromones for sexual attraction or aggregation. Of wing membrane has numerous veins. Some species
special interest is the behavior associated with paren- are economically important, including Leptocorisa
tal care displayed by some coreids. Golden egg bug acuta on Poeacea, and Riptortus linearis and R. ser-
(Phyllomorpha laciniata Villiers) shows a very pecu- ripes on Fabaceae.
liar oviposition behavior. Females can lay eggs on
plants (Paronychia argentea), or on the bodies of
conspecifics of both sexes, where they remain until Rhopalidae
hatching. Egg carrying on P. laciniata has been
known for over a century. It is common to see both The family Rhopalidae includes 20 genera and
males and females carrying 115 eggs/individual about 210 species in two subfamilies: Serinethinae
glued to their backs. The eggs laid on plants experi- and Rhopalinae. These subfamilies are represented
ence high rates of predation and attacks by parasi- in both the Eastern and Western Hemispheres.
toid wasps. However, when the eggs are carried by Rhopalinae are most diverse in the Palaearctic
an adult, fewer eggs are attacked by parasitoid wasps. Region whereas Serinethinae are more tropical in
Female oviposition choice may be adaptive and distribution.
minimizes offspring mortality. The golden egg bug is In Rhopalidae, the clypeus extends beyond the
not unique among insects in the sense that males mandibular plates. Two ocelli are present on tuber-
carry eggs (it is also known in belostomatid bugs) cles. Rhopalidae have greatly reduced metapleural
but rather it is unique because there are different scent-gland peritremes; for this reason they are
explanations for this behavior. Some authors have called scentless plant bugs.The hemelytral membrane
interpreted this behavior as parental care. Others contains numerous veins. The secondary dorsal
1062
C Coremata

abdominal scent gland opens close to that of the Lansbury I (1966) A revision of the Stenocephalidae Dallas
first gland. All of the rhopalids are phytophagous on 1852 (Hemiptera-Heteroptera). Entomologists Monthly
Magazine 101:145160
herbs and woody plants, but are not known to be Mitchell PL (2000) Leaf-footed bugs (Coreidae). In: Schaefer
economic pests of any significance. However, in CW, Panizzi AC (eds) Heteroptera of economic impor-
Florida, USA, the rhopalid bug Jadera haematoloma tance. CRC Press, Boca Raton, FL, pp 337403
Moulet P (1995) Hmiptres Coreoidea (Coreidae, Rhopali-
feeds on golden rain tree, Koelreuteria spp. (Sapin-
dae, Alydidae), Pyrrhocoridae, Stenocephalidae, Euro-
daceae) and other plants in this family, becoming so Mditerranens. Faune de France 81:1336
abundant as to become a significant nuisance Schaefer CW (1965) The morphology and higher classifica-
around homes. Niesthrea lusitanica (Sailer) is bene- tion of the Coreoidea (Hemiptera: Heteroptera). III. The
families Rhopalidae, Alydidae, and Coreidae. Misc Publ
ficial, and is used to control the invasive weed vel- Entomol Soc Am 5:176
vetleaf, Abutilon theophrasti. Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera:
Heteroptera). Classification and natural history. Cornell
University Press, Ithaca, NY, 336 pp
Hyocephalidae Vzquez M (1985) Los Coreoidea ibricos. Tesis Doctoral.
Publicaciones de la Universidad Complutense de
Madrid, 322 pp
The small family Hyocephalidae includes only two
genera and three species from Australia: Hyoceph-
alus aprugnus Bergroth and Moevius with two Coremata
species. The adults are large, elongate, and mostly
dark in color. The head is very extended. The buc- Long eversible tubes found at the tip of the males
culae are enlarged, extending posteriorly to the abdomen is some Lepidoptera (Fig. 107). These
eyes. The gula has a labial groove. The pronotum is structures are inflated pneumatically, and release
trapezoidal. The scutellum is small. Macropterous pheromones. The pheromones released from the
and brachypterous morphs are known. The wing coremata are thought to be aphrodisiacs, and to
membrane contains four veins forming three basal function in courtship.
cells. All spiracles occur ventrally. Hyocephalids
live under stones in sandy and gravelly areas and
may be associated with Acacia and Eucalyptus.
Bugs (Hemiptera)
Paternal Behavior in Heteroptera
Squash Bug, Anasa tristis (Degeer)
(Hemiptera: Coreidae)

References

Brailovsky H (2002) A new species of Maevius Stl from Aus-

tralia and some notes on the family Hyocephalidae
(Hemiptera: Heteroptera). Proc Entomol Soc Washing-
ton 104:4150
Dolling WR (1991) The Hemiptera. Oxford University Press,
Oxford, UK, 274 pp
Gllner-Scheiding U (1983) General-Katalog der Familie
Rhopalidae (Heteroptera). Mitteilungen aus dem Zool-
ogischen Museum in Berlin 59:37189
Coremata, Figure 107 Fully inflated coremata in a
Kaitala A (1996) Oviposition on the back of conspecifics: an
unusual reproductive tactic in a coreid bug. Oikos specimen of a tiger moth (Arctiidae) (photo by
77:381389 A. Sourakov).
 Corn Delphacid, Peregrinus maidis (Ashmead) (Hemiptera: Delphacidae)
C 1063

Corethrellidae The corn delphacid, Peregrinus maidis (Ashmead)

(Fig.109) is known to be a vector of at least two
A family of flies (order Diptera) viral diseases of maize (Zea mays L.), and is of par-
Flies ticular economic importance in the lowland
humid tropics. It has even been suggested that its
introduction into Central America resulted in the
Corioxenidae collapse of the Mayan civilization.
P. maidis is pantropical, having been recorded
A family of insects in the order Strepsiptera from most tropical regions, including the West
Stylopids Indies, Central and South America, Africa, islands
in the Indian and Pacific Oceans, India, Malaysia,
Taiwan, Indonesia, China and Australia. In the
Corium
United States, it has been recorded from Washing-
The thickened basal region (Fig.108) of the front ton, DC, south to Florida, and west to Ohio and
wing in Hemiptera. Texas.
Wings of Insects P. maidis is the only known vector of two
major viral diseases of maize, maize mosaic virus
and maize stripe virus. The former is a tropical and
Corixidae subtropical disease and is found in Hawaii and in
southern Florida. Maize stripe virus, also a tropical
A family of bugs (order Hemiptera). They some- and subtropical disease, has been known to occur
times are called water bugs in southern Florida.
Bugs The corn delphacid feeding causes damage
to corn and sorghum (Sorghum bicolor Moench)
extracting a large quantity of sap and excretion
Corn Delphacid, Peregrinus maidis of honeydew. Both nymph and adult are efficient
(Ashmead) (Hemiptera: vectors of maize stripe and maize mosaic viruses.
Delphacidae) In general, the nymph is a more efficient trans-
mitter than the adult. The virus can be acquired
James H. Tsai in less than an hour. The average incubation
University of Florida, Ft. Lauderdale, FL, USA period of virus in P. maidis is 1014 days,

Corium, Figure 108 Front wing of a bug (Hemiptera: suborder Heteroptera), thickened basally and mem-
branous distally.
1064
C Corn Delphacid, Peregrinus maidis (Ashmead) (Hemiptera: Delphacidae)

depending on age of vector and virus titre in the respective average length of nymphal develop-
infected plant. Once the viruses are acquired by ment on corn, itch grass (Rottboellia exaltata L.),
P. maidis, they are retained for life. Both viruses sorghum (Sorghum bicolor (L.) Moench), goose
multiply in the vector, and only maize stripe grass (Eleusine indica (L.) Gaertn.), barnyard grass
virus is transovarially transmitted by P. maidis. (Echinochloa crusgalli L.), and gamma grass (Trip-
Corn plants and P. maidis can be doubly infected, sacum dactyloides L.) is 17, 18, 20, 25, 27 and 61
bearing both viruses. days. The adult longevity on these respective plants
The life cycle of corn delphacid varies with averages 20, 28, 8, 8, 7 and 43 days.
temperature and host plant. The average develop- The number of eggs laid daily per female on
mental periods at 1032C are 210 days for first corn, itchgrass and gamma grass is 21, 6 and 4
instar nymph, 420 days for second instar, 424 eggs, respectively. The number of eggs per female
days for third instar, 1719 days for fourth instar per life on these three plants averages 612, 146 and
and 413 days for fifth instar. Nymphs undergo 46 eggs.
five instars within the range of 1627C. The adult The eggs are deposited under the epidermal
longevity averages 1097 days for males, and cells along the leaf sheath and midrib. The egg is
19108 days for females, within the temperature lined in one or more rows numbering 47 eggs.
range of 1732C. At 27C, the average number of The egg is elongate and curved with a round pos-
eggs laid per day per female range from 15 to 25 terior end. The average size of egg measures 1.06
eggs and a mean of 605 eggs, ranging from 297 to mm long and 0.28 mm wide. Freshly laid eggs are
938 eggs per female. The preoviposition period translucent white with red eye suffusion at poste-
ranges from 3 to 6 days, and the oviposition period rior end.
ranges from 11 to 48 days. The developmental Young nymphs are mostly aggregated and
period of immature stages is also affected by the feed on the inside of the leaf sheath. It is very
host plants on which they are reared. At 27C, the common to find adults attending the nymphal

Corn Delphacid, Peregrinus maidis (Ashmead) (Hemiptera: Delphacidae), Figure 109 Adult corn
delphacid, Peregrinus maidis (photo J. Tsai).
 Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)
C 1065

aggregations in the field. The average size of the Corn Earworm, Helicoverpa zea
first instar measures 1.4 mm long and 0.4 mm (Boddie) (Lepidoptera: Noctuidae)
wide. The average measurement of second instar
is 1.7 mm long and 0.6 mm wide. The average size John L. Capinera
of third instar is 2.3 mm long and 0.8 mm wide. University of Florida, Gainesville, FL, USA
The fourth and fifth instars measure 2.8 and 4.0
mm long, and 1.2 and 1.7 mm wide, respectively. Corn earworm is found throughout North Amer-
The morphological characters such as number of ica except for northern Canada and Alaska. In the
tarsomeres on metatarsi and the development of eastern United States, corn earworm does not nor-
metatibial spur and wingpad are useful in distin- mally overwinter successfully in the northern
guishing the instars. Both adult males and females states. It is known to survive as far north as about
typically are dimorphic, containing macropterous 40 degrees north latitude, or about Kansas, Ohio,
and brachypterous forms. In rare case, the adult Virginia, and southern New Jersey, depending on
can be completely wingless. the severity of winter weather. However, it is highly
P. maidis can be controlled by the use of pes- dispersive, and routinely spreads from southern
ticides that are routinely used for control of states into northern states and Canada. Thus, areas
lepidopteran pests affecting corn. Most research have overwintering, both overwintering and
emphasis is placed on breeding corn hybrids immigrant, or immigrant populations, depending
resistant to the viral pathogens instead of the on location and weather. In the relatively mild
insect vector. Pacific Northwest, corn earworm can overwinter
Maize (Corn) Pests and their Management at least as far north as southern Washington.

References Life Cycle and Description

Bradfute OE, Tsai JH (1983) Identification of maize mosaic

This species is active throughout the year in tropical
virus in Florida. Plant Dis 67:13391342 and subtropical climates, but becomes progressively
Falk BW, Tsai JH (1998) Biology and molecular biology of more restricted to the summer months with increas-
viruses in the Genus Tenuivirus. Ann Rev Phytopathol ing latitude. In northeastern states dispersing adults
36:139163
Tsai JH (1996) Development and oviposition of Peregrinus may arrive as early as May or as late as August due
maidis (Homoptera: Delphacidae) on various host to the vagaries associated with weather; thus, their
plants. Fla Entomol 79:1926 population biology is variable. The number of gen-
Tsai JH, Wilson SW (1986) Biology of Peregrinus maidis with
erations is usually reported to be one in northern
description of immature stages (Homoptera: Delphaci-
dae). Ann Entomol Soc Am 79:395401 areas such as most of Canada, Minnesota, and west-
Tsai JH, Zitter TA (1982) Characteristics of maize stripe virus ern New York; two in northeastern states; two to
transmission by the corn delphacid. J Econ Entomol three in Maryland; three in the central Great Plains;
75:397400
Tsai JH, Steinberg B, Falk BW (1990) Effectiveness and resid-
and northern California; four to five in Louisiana
ual effects of seven insecticides on Dalbulus maidis and southern California; and perhaps seven in
(Homoptera: Cicadellidae) and Peregrinus maidis southern Florida and southern Texas. The life cycle
(Homoptera: Delphacidae). J Entomol Sci 25:106111 can be completed in about 30 days.

Egg
Cornea
Eggs are deposited singly, usually on leaf hairs
The cuticular part of an eye. and corn silk. The egg is pale green when first
1066
C Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)

deposited, becoming yellowish and then gray with microspines. Although it is easily confused with
time. The shape varies from slightly dome-shaped corn earworm, it rarely is a vegetable pest and never
to a flattened sphere, and measures about 0.50.6 feeds on corn. Close examination reveals that in
mm in diameter and 0.5 mm in height. Fecundity tobacco budworm larvae the spines on the tubercles
ranges from 500 to 3,000 eggs per female. The eggs of the first, second, and eighth abdominal segments
hatch in about 34 days. are about half the height of the tubercles, but in corn
earworm the spines are absent or up to one-fourth
the height of the tubercle.
Larva

Upon hatching, larvae wander about the plant until Pupa

they encounter a suitable feeding site, normally the
reproductive structure of the plant. Young larvae Mature larvae leave the feeding site and drop to
are not cannibalistic, so several larvae may feed the ground, where they burrow into the soil and
together initially. However, as larvae mature they pupate. The larva prepares a pupal chamber 510
become very aggressive, cannibalizing other larvae. cm below the surface of the soil. The pupa is
Consequently, only a small number of larvae (often mahogany-brown in color, and measures 1722
only one) are found in each ear of corn. Normally, mm in length and 5.5 mm in width. Duration of
corn earworm displays six instars, but five is not the pupal stage is about 13 days (range 1025)
uncommon and seven to eight have been reported. during the summer.
Mean head capsule widths are 0.29, 0.47, 0.77, 1.30,
2.12, and 3.10 mm, respectively, for instars 16.
Larval lengths are estimated at 1.5, 3.4, 7.0, 11.4, Adult
17.9, and 24.8 mm, respectively. Development time
averaged 3.7, 2.8, 2.2, 2.2, 2.4, and 2.9 days, respec- As with the larval stage, adults (Fig.110) are quite
tively, for instars 16 when reared at 25C. variable in color. The forewings of the moths usually
The larva (Fig.111) is variable in color. Overall, are yellowish brown in color, and often bear a small
the head tends to be orange or light brown with a dark spot centrally. The small dark spot is especially
white net-like pattern, the thoracic plates black, and distinct when viewed from below. The forewing also
the body brown, green, pink, or sometimes yellow or may bear a broad dark transverse band distally, but
mostly black. The larva usually bears a broad dark
band laterally above the spiracles, and a light yellow
to white band (Fig.111) below the spiracles. A pair
of narrow dark stripes often occurs along the center
of the back. Close examination reveals that the body
bears numerous black thorn-like microspines. These
spines give the body a rough feel when touched. The
presence of spines and the light-colored head serve
to distinguish corn earworm from fall armyworm,
Spodoptera frugiperda (J.E. Smith), and European
corn borer, Ostrinia nubilalis (Hubner). These other
common American corn-infesting species lack the
spines and have dark heads. Tobacco budworm, Corn Earworm, Helicoverpa zea (Boddie)
Heliothis virescens (Fabricius), is a closely related (Lepidoptera: N
octuidae), Figure 110 Adult of
species in which the late instar larvae also bear corn earworm, H elicoverpa zea.
 Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)
C 1067

Corn Earworm, Helicoverpa zea ( Boddie) (Lepidoptera: Noctuidae), Figure 111 Corn earworm larva.

the margin of the wing is not darkened. The hind tobacco, vetch, and wheat. Among field crops, sor-
wings are creamy white basally and blackish distally, ghum is particularly favored. Cotton is frequently
and usually bear a small dark spot centrally. The reported to be injured, but this generally occurs
moth measures 3245 mm in wingspan. Adults are only after more preferred crops have matured. Fruit
reported to live for 515 days, but may survive for and ornamental plants may be attacked, including
over 30 days under optimal conditions. The moths ripening avocado, grape, peaches, pear, plum, rasp-
are principally nocturnal, and remain active through- berry, strawberry, carnation, geranium, gladiolus,
out the dark period. During the daylight hours they nasturtium, rose, snapdragon, and zinnia. In studies
usually hide in vegetation, but sometimes can be seen conducted in Florida, corn earworm larvae fed on
feeding on nectar. Oviposition commences about 3 all 17 vegetable and field crops studied, but corn
days after emergence, continuing until death. Fresh- and sorghum were most favored. In cage tests ear-
silking corn is highly attractive for oviposition but worm moths preferred to oviposit on tomato over a
even ears with dry silk will receive eggs. Fecundity selection of several other vegetables that did not
varies from about 5003,000 eggs, although feeding include corn. Such weeds as common mallow,
is a prerequisite for high levels of egg production. crown vetch, fall panicum, hemp, horsenettle, lamb-
Females may deposit up to 35 eggs per day. squarters, lupine, morningglory, pigweed, prickly
sida, purslane, ragweed, Spanish needles, sunflower,
toadflax, and velvetleaf, have been reported to serve
Host Plants as larval. Crimson clover and winter vetch, which
may be both crops and weeds, are important early
Corn earworm has a wide host range; hence, it is season hosts in Mississippi. Cranesbill species were
also known as tomato fruitworm, sorghum head- particularly important weed hosts in this area. In
worm, vetchworm, and cotton bollworm. In addition North Carolina, especially important wild hosts are
to corn and tomato, perhaps its most favored vege- toadflax and deergrass. Adults collect nectar or
table hosts, corn earworm also attacks artichoke, other plant exudates from a large number of plants.
asparagus, cabbage, cantaloupe, collard, cowpea, Trees and shrub species are especially frequented.
cucumber, eggplant, lettuce, lima bean, melon, okra, Among the hosts are Citrus, Salix, Pithecellobium,
pea, pepper, potato, pumpkin, snap bean, spinach, Quercus, Betula, Prunus, Pyrus and other trees, but
squash, sweet potato, and watermelon. Not all are also alfalfa; red and white clover; milkweed, and
good hosts, For example, a study of relative suitabil- Joe-Pye weed and other flowering plants.
ity of crops and weeds in Texas found that although
corn and lettuce were excellent larval hosts, tomato
was merely a good host, and broccoli and canta- Damage
loupe were poor. Other crops injured by corn ear-
worm include alfalfa, clover, cotton, flax, oat, millet, Corn earworm is considered by some to be the
rice, sorghum, soybean, sugarcane, sunflower, most costly crop pest in North America. It is more
1068
C Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)

damaging in areas where it successfully overwin- spp. (Hymenoptera: Scelionidae), are common egg
ters, however, because in northern areas it may parasitoids. Common larval parasitoids include
arrive too late to inflict extensive damage. It often Cotesia spp., and Microplitis croceipes (Cresson)
attacks valuable crops, and the harvested portion (all Hymenoptera: Braconidae); Campoletis spp.
of the crop. Thus, larvae often are found associated (Hymenoptera: Ichneumonidae); Eucelatoria
with such plant structures as blossoms, buds, and armigera (Coquillett) and Archytas marmoratus
fruits. When feeding on lettuce, larvae may bur- (Townsend) (Diptera: Tachinidae). General preda-
row into the head. On corn, its most common host, tors often feed on eggs and larvae of corn earworm;
young larvae tend to feed on silks initially, and over 100 insect species have been observed to feed
interfere with pollination, but eventually they usu- on H. zea. Within-season mortality during the
ally gain access to the kernels. They may feed only pupal stage seems to be important, and although
at the tip, or injury may extend half the length of overwintering mortality is often very high, the
the ear before larval development is completed. mortality is due to adverse weather and collapse of
Such feeding also enhances development of plant emergence tunnels rather than to natural enemies.
pathogenic fungi. If the ears have not yet produced In Texas, Steinernema riobravis (Nematoda: Stein-
silk, larvae may burrow directly into the ear. They ernematidae) has been found to be an important
usually remain feeding within a single ear of corn, mortality factor of prepupae and pupae, but this
but occasionally abandon the feeding site and parasitoid is not yet generally distributed.
search for another. Larvae also can damage whorl- Epizootics caused by pathogens may erupt
stage corn by feeding on the young, developing when larval densities are high. The fungal patho-
leaf tissue. Survival is better on more advanced gen Nomuraea rileyi and the Helicoverpa zea
stages of development, however. On tomato, larvae nuclear polyhedrosis virus are commonly involved
may feed on foliage and burrow in the stem, but in outbreaks of disease, but the protozoan Nosema
most feeding occurs on the tomato fruit. Larvae heliothidis and other fungi and viruses also have
commonly begin to burrow into a fruit, feed only been observed.
for a short time, and then move on to attack
another fruit. Tomato is more susceptible to injury
when corn is not silking; in the presence of corn, Management
moths will preferentially oviposit on fresh corn
silk. Other crops such as bean, cantaloupe, cucum- Sampling
ber, squash, and pumpkin may be injured in a
manner similar to tomato, and also are less likely Eggs and larvae often are not sampled on corn
to be injured if silking corn is nearby. because eggs are very difficult to detect, and larvae
burrow down into the silks, out of the reach of
insecticides, soon after hatching Moths can be
Natural Enemies monitored with blacklight and pheromone traps.
Both sexes are captured in light traps whereas only
Although numerous natural enemies have been males are attracted to the sex pheromone. Both
identified, they usually are not effective at causing trap types give an estimate of when moths invade
high levels of earworm mortality or preventing or emerge, and relative densities, but pheromone
crop injury. For example, in a study conducted in traps are easier to use because they are selective.
Texas, <1% of the larvae were parasitized or infected The pheromone is usually used in conjunction
with disease. However, eggs may be heavily parasit- with an inverted cone-type trap. Generally, the
ized. Trichogramma spp. (Hymenoptera: Tricho- presence of five to ten moths per night is sufficient
grammatidae), and to a lesser degree Telenomus to stimulate pest control practices.
 Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)
C 1069

Insecticides developing larvae if they are applied to corn silk;

this has application for home garden production
Corn fields with more than 5% of the plants bear- of corn if not commercial production. Soil surface
ing new silk are susceptible to injury if moths are and subsurface applications of nematodes also can
active. Insecticides are usually applied to foliage in affect earworm populations because larvae drop
a liquid formulation, with particular attention to to the soil to pupate. This approach may have
the ear zone, because it is important to apply insec- application for commercial crop protection, but
ticide to the silk. Insecticide applications are often larvae must complete their development before
made at 26 day intervals, sometimes as frequently they are killed, so some crop damage ensues.
as daily. Because it is treated frequently, and over a Trichogramma spp. (Hymenoptera: Trichogram-
wide geographic area, corn earworm has become matidae) egg parasitoids have been reared and
resistant to many insecticides. Susceptibility to released for suppression of H. zea in several crops.
Bacillus thuringiensis also varies, but the basis for Levels of parasitism averaging 4080% have been
this variation in susceptibility is uncertain. Min- attained by such releases in California and Florida,
eral oil, applied to the corn silk soon after pollina- resulting in fruit damage levels of about 3%.
tion, has insecticidal effects. Application of about
0.751.0 ml of oil 57 days after silking can pro-
vide good control in the home garden. Trap crop- Host Plant Resistance
ping is often suggested for this insect; the high
degree of preference by ovipositing moths for corn Numerous varieties of corn have been evaluated
in the green silk stage can be used to lure moths for resistance to earworm, and some resistance has
from less preferred crops. Lima beans also are rela- been identified in commercially available corn.
tively attractive to moths, at least as compared to Resistance is derived from physical characteristics
tomato. However, it is difficult to maintain attrac- such as husk tightness and ear length, which
tant crops in an attractive stage for protracted impede access by larvae to the ear kernels, or
periods. In southern areas where populations chemical factors such as maysin, which inhibit lar-
develop first on weed hosts and then disperse to val growth. Host plant resistance thus far is not
crops, treatment of the weeds through mowing, completely adequate to protect corn from ear-
herbicides, or application of insecticides can worm injury, but it may prove to be a valuable
greatly ameliorate damage on nearby crops. In component of multifaceted pest management
northern areas, it is sometimes possible to plant or programs.
harvest early enough to escape injury. Throughout Vegetable Pests and Their Management
the range of this insect, population densities are Maize (Corn) Pests and their Management
highest, and most damaging, late in the growing
season. Tillage, especially in the autumn, can sig-
nificantly reduce overwintering success of pupae References
in southern locations.
Archer TL, Bynum ED Jr (1994) Corn earworm (Lepidoptera:
Noctuidae) biology on food corn on the high plains.
Environ Entomol 23:343348
Biological Control Capinera JL (2001) Handbook of vegetable pests. Academic
Press, San Diego, CA, 729 pp
The bacterium Bacillus thuringiensis, and stein- Harding JA (1976) Heliothis spp.: seasonal occurrence, hosts
and host importance in the lower Rio Grande Valley.
ernematid nematodes provide some suppression.
Environ Entomol 5:666668
Entomopathogenic nematodes, which are avail- Hardwick DF (1965b) The corn earworm complex. Entomo-
able commercially, provide good suppression of logical Society of Canada Memoir 40, 246 pp
1070
C Cornicles

Neunzig HH (1964) The eggs and early-instar larvae of overwinter on Prunus sp. The northern areas of
Heliothis zea and Heliothis virescens (Lepidoptera: Noc- North America and southern Canada are thought
tuidae). Ann Entomol Soc Am 57:98102
Oatman ER, Platner GR (1971) Biological control of the to be invaded annually, with the timing of invasion
tomato fruitworm, cabbage looper, and hornworms on and the number of subsequent generations in an
processing tomatoes in southern California, using mass area a function of weather. The short life cycle of
releases of Trichogramma pretiosum. J Econ Entomol
64:501506
this aphid, normally 612 days, allows production
of 2040 generations per year in such southern
locations as Texas and about nine generations in
Cornicles Illinois, but fewer further north.
There are 4 instars. The young nymph ini-
Two tubular structures located on the posterior tially is pea green in color, with red eyes and col-
part (fifth or sixth abdominal segment) of an orless antennae and legs, and measures about 0.5
aphids abdomen. They vary greatly in structure, mm long. Body length increases to about 0.9, 1.1,
and are the source of aphid alarm pheromone. and 1.3 mm, the green body color becomes darker,
They are also called siphunculi. and the appendages gain some dark pigmentation
Abdomen of Hexapods as the nymph progresses through instars 24.
Aphids Mean development times are 4.5, 4.5, 4.5, and 4.7
days, respectively, for instars 14 among nymphs
destined to grow into apterae, when cultured at
Corn Leaf Aphid, Rhopalosiphum 11C. The corresponding development times for
maidis (Fitch) (Hemiptera: 19 and 29C are 1.7, 1.8, 1.7, and 1.9 days; and 1.2,
Aphididae) 1.2, 1.5, and 1.7 days, respectively. Development
times for alatae are quite similar, except that instar
John L. Capinera 4 tends to require an additional day.
University of Florida, Gainesville, FL, USA The viviparous females generally are bluish
green, although they become darker with time,
This species may be of Asiatic origin, but now has a some becoming almost black. Fine white powder
world-wide distribution in temperate areas. How- covers the entire body. The winged form (alatae)
ever, corn leaf aphid does not persist in areas with has a black thorax and head, whereas in the wing-
severe winters, so it dies out from cold areas such as less form (apterae) only the head is black (Figs.112
most of Canada, and northern Europe and Asia, and and 113). The winged form also tends to bear three
re-invades large areas of temperate regions annually. black spots laterally on the abdomen, and the base
of the cornicles is enveloped in a small area of pur-
ple or black color. In both female forms the append-
Life History ages are black. The alatae measure about 1.7 mm
long, the apterae about 2.4 mm. The adult male
This species overwinters as viviparous females aphid measures about 1.5 mm long. The head, tho-
(displaying parthenogenetic reproduction) in rax, and legs are black. The abdomen is dark bluish
warm winter areas (such as the southern USA). green, with a dark spot laterally on each segment.
During mild winters, there is evidence that such Corn leaf aphid feeds on numerous grasses in
overwintering may occur in moderately cold winter addition to corn, and is considered to be a serious
regions, too (such as the mid-western USA). Over- pest of cereal grains due to its ability to transmit
wintering does not occur in cold winter areas (such virus diseases. The crops fed upon, in addition
as most of Canada). Oviparous (egg producing) to corn, include barley, chufa, oat, rye, millet,
forms and males are rare, though in Pakistan, eggs sorghum, Sudan grass, and sugarcane. Barley is the
 Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae)
C 1071

most important early season host. While the leaf

blades are rolled, aphid colonies develop within
the furled barley leaves. However, once the corn is
about 30 days old it also becomes very suitable for
aphids; the tassels forming within the furled leaves
are particularly suitable for aphid population
growth. As the tassel extends, aphids disperse over
the entire plant to feed.
Among weeds and prairie grasses known to
Corn Leaf Aphid, Rhopalosiphum maidis (Fitch)
serve as hosts are barnyardgrass, Echinochloa crus-
(Hemiptera: Aphididae), Figure 112 Winged
galli; buffalo grass, Buchloe dactyloides; crabgrass,
female corn leaf aphid, Rhopalosiphum maidis
Digitaria sanguinalis; foxtail, Setaria spp.; grama
(Fitch).
grass, Bouteloua spp.; and Johnson grass, Sorghum
halepense.
These aphids feed on exposed areas of the plant
and often are subject to significant levels of predation
and parasitism. Numerous species of ladybird beetles
attack corn leaf aphid. Despite their abundance, how-
ever, the ladybird beetles generally are numerous and
effective predators only after the aphid populations
attain high and damaging densities. Other common
predators include various flower flies (Diptera: Syr-
phidae), predatory midges (Diptera: Cecidomyiidae),
minute pirate bugs (Hemiptera: Anthocoridae), and
lacewings (Neuroptera: Chrysopidae).
Several wasps parasitize corn leaf aphid.
Lysiphlebus testaceipes (Cresson) (Hymenoptera:
Braconidae) is the most widespread and common
parasitoid, but Aphelinus varipes (Foerster)
(Hymenoptera: Aphelinidae) is an important parasi-
toid in Texas. Other parasitoids include Diaeretiella
rapae (MIntosh) and Ephedrus persicae (Froggatt)
(both Homoptera: Aphidiidae) and Aphelinus
asychis Walker (Hymenoptera: Encyrtidae).

Damage

Corn leaf aphid is commonly found feeding on the

tassel and silk of the corn plant in addition to
the leaves. It interferes with pollen production and
Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) fertilization, resulting in poor kernel fill of the ears.
(Hemiptera: Aphididae), Figure 113 Wingless Infestation also can cause a delay in plant maturity,
female corn leaf aphid, Rhopalosiphum maidis and reduced plant size. Honeydew secreted by the
(Fitch). aphids supports growth of sooty mold fungus,
1072
C Corn Leafhopper, Dalbulus maidis (Delong and Wolcott) (Hemiptera: Cicadellidae)

causing an unsightly appearance of the ears and virus, but incidence of aphids and disease increase
interfering with photosynthesis in small grains. In thereafter. Little work on the management of corn
general, crop plants are very tolerant of aphids, and leaf aphid as a virus vector has been reported, other
only extremely dense infestations cause injury. If than the assessment of corn varieties for resistance.
soil moisture conditions are inadequate, however, Maize (Corn) Pests and their Management
then the damage by the aphids is increased, and
yield reductions are more likely. References
The ability to transmit plant viruses greatly
exacerbates the damage potential of this aphid. Sev- Capinera JL (2001) Handbook of vegetable pests. Academic
eral diseases, including barley yellow dwarf, beet Press, San Diego, CA, 729 pp
yellows, cucumber mosaic, lettuce mosaic, maize Kring TJ (1985) Key and diagnosis of the instars of the corn
leaf aphid Rhopalosiphum maidis (Fitch). Southwest
streak, maize dwarf mosaic, and maize stripe are
Entomol 10:289293.
transmitted. Even in crops not successfully colo- Straub RW (1984) Maize dwarf mosaic virus: symptomatol-
nized by the aphids, corn leaf aphid is implicated in ogy and yield reactions of susceptible and resistant
the transmission of numerous stylet-borne viruses. sweet corns. Environ Entomol 13:318323
Straub RW, Boothroyd CW (1980) Relationship of corn leaf
aphid and maize dwarf mosaic disease to sweet corn yields
in southeastern New York. J Econ Entomol 73:9295
Management Wildermuth VL, Walter EV (1932) Biology and control of the
corn leaf aphid with special reference to the southwest-
ern states. USDA Technical Bulletin 306, 21 pp
Sampling for corn leaf aphids on young leaf tissue
is usually done by visual examination of the whorls.
As the aphids disperse from the whorls, they are
readily apparent on other plant structures. As pop- Corn Leafhopper, Dalbulus maidis
ulations increase and honeydew accumulates, (Delong and Wolcott) (Hemiptera:
remote detection of aphid populations is possible Cicadellidae)
by examination of photographs taken by aircraft
using infrared-sensitive film; sooty mold growing James H. Tsai
on honeydew impedes the reflectance of infrared University of Florida, Ft. Lauderdale, FL, USA
radiation. It is advisable to monitor populations in
barley early in the season, as incidence in this The corn leafhopper, Dalbulus maidis (Delong and
favored crop may reflect potential incidence in Wolcott) is found only in subtropical and tropical
corn later in the season. Populations of alate aphids areas of America. Its host range is limited to maize
may be monitored with yellow water pan traps or and its relatives.
sticky traps, though aphids collected on sticky Maize (Zea mays L.) is one of the major cereal
traps are often damaged and difficult to identify. crops; it ranks third in production following wheat
Systemic insecticides applied to the young and rice with an average of 380 million tons pro-
plants or to the soil soon after plant emergence from duced annually on 120 million ha by 53 countries.
the soil are particularly effective at controlling It is the worlds most widely grown crop in almost
aphids. They may be killed by contact insecticides all tropical areas of the world including tropical
as well, though the increase in crop yield does not highlands over 3,000 m in altitude, to temperate
justify spraying on some low value grain crops. areas as far north as the 65th latitude. In tropical
Early plantings can escape injury, especially in and subtropical areas of America, maize is often
northern areas where aphids do not overwinter. In infected with at least three serious phytoplasmal
New York, for example, corn planted before June 10 and viral agents. They are known as corn stunt
escape injury by corn leaf aphid and maize dwarf spiroplasma (CSS), maize bushy stunt phytoplasma
 Corn Leafhopper, Dalbulus maidis (Delong and Wolcott) (Hemiptera: Cicadellidae)
C 1073

(MBP) and maize rayado fino virus (MRFV). These per day per female averages 4 eggs at 16C, and 15
three pathogens are all transmitted by D. maidis in eggs at 27C. The number of eggs laid per female per
a persistent manner. However, the former two life averages 402 eggs at 16C and 611 eggs at 27C.
pathogens are known to multiply in the D. maidis. Other plants such as Tripsacum dactyloides L.,
In Florida, corn plants often have been infected by Tripsacum sp., Rottboellia exaltata L., Secale cerale
any two of these pathogens. Occasionally, multiple L., and Avena sativa L. can be used as temporary
pathogens can be found in the same corn plants in feeding hosts, but not for rearing hosts. Besides
the field. CSS can be acquired by D. maidis in 15 corn, T. dactyloides var. meridonale is suitable for
min. All these pathogens require a protracted incu- continuous rearing of D. maidis. Eggs are mainly
bation period in the vector, ranging from 14 to 21 deposited in the mesophyll tissue of the midrib. The
days, depending upon the isolate and titre of patho- egg is elongate, and curved with a round posterior
gen, and biotype and age of vector. end. The average size of egg measures 1.04 mm long
The life cycle of D. maidis varies with tempera- and 0.25 mm wide. Young nymphs often are found
ture and host plant. In general, nymphs undergo five aggregating more on leaves than stems. The average
instars; an additional instar is often noted. The aver- size of instar I through V measures 0.87 mm long
age developmental times for first through fifth instars and 0.27 wide, 1.14 mm long and 0.37 mm wide,
range from 12 to 34 days at 10C, 6 to 13 days at 16C, 1.69 mm long and 0.49 mm wide, 2.14 mm long
3 to 4 days at 27C and 2 to 4 days at 32C. The adult and 0.62 mm wide, 2.82 mm long and 0.81 mm
(Fig.114) longevity averages 67 days for males and wide, respectively. The average size of male and
38days for females at 10C, 107 days for males and female measures 2.80 mm long and 0.81 mm wide,
52 days for females at 16C, 78 days for males and 3.18 mm long and 0.88 mm wide, respectively.
and 30 days for females at 27C, and 16 days for males D. maidis can be controlled by the use of pesticides
and 10 days for females at 32C. There is a minimum that are commonly used for control of lepidopteran
of one day preoviposition period, and it is affected by pests of corn.
rearing temperature. The number of eggs oviposited Maize (Corn) Pests and their Management

Corn Leafhopper, Dalbulus maidis (Delong and Wolcott) (Hemiptera: Cicadellidae), Figure 114 Adult corn
leafhopper, Dalbulus maidis (photo J. Tsai).
1074
C Corn Stunt

References Juvenile Hormone

Reproduction
Falk BW, Tsai JH (1998) Biology and molecular biology of Corpus Cardiacum
viruses in the Genus Tenuivirus. Ann Rev Phytopathol Nervous System
36:139163
Nault LR, Bradfute OE (1979) Corn stunt: involvement of a
complex of leafhopper-borne pathogens. In: Maramoro-
sch K, Harris KF (eds) Leafhopper vectors and plant dis-
ease agents. Academic Press, New York, NY, pp 561586
Corpus Cardiacum (pl., Corpus
Tsai JH (1987a) Bionomics of Dalbulus maidis (DeLong and Cardiaca)
Wolcott). A vector of mollcutes and virus (Homoptera:
Cicadellidae). In: Maramorosch K, Raychaudhuri SP Small organs between the corpus allata (Fig.115)
(eds) Mycoplasma diseases of crops: basic and applied
aspects. Springer-Verlag, New York, NY, pp 209221
that releases PTTH to the hemolymph.
Tsai JH (1987b) Mycoplasma diseases of corn in Florida. In: Endocrine Regulation of Insect Reproduction
Maramorosch K, Raychaudhuri SP (eds) Mycoplasma Reproduction
diseases of crops: basic and applied aspects. Springer- Corpus Allatum
Verlag, New York, NY, pp 317325
Tsai JH, Falk BW (1988) Tropical corn pathogens and their Nervous System
associated vectors. In: Harris KF (ed) Advances in dis-
ease vector research. Springer-Verlag, New York, NY,
pp 177201
Tsai JH, Steinberg B, Falk BW (1990) Effectiveness and resid- Corpus Pendunculatum
ual effects of seven insecticides on Dalbulus maidis
(Homoptera: Cicadellidae) and Peregrinus maidis
(Homoptera: Delphacidae). J Entomol Sci 25:106111 A portion of the protocerebral region of the brain,
also called mushroom bodies. The size of the cor-
pus pendunculatum is correlated with the occur-
Corn Stunt rence of complex behaviors in insects, and seems
best developed in social insects.
A disease transmitted by leafhoppers to maize (corn).
Nervous System
Transmission of Plant Diseases by Insects
Learning in Insects
Corn Leafhopper, Dalbulus maidis
Learning in Insects: Neurochemistry and
Localization of Brain Functions
Corpora Pedunculata
The mushroom bodies of the brain. These are large
bilateral integrative centers located in the protoce- Corydalidae
rebrum. They are thought to function in olfactory
learning. A family of insects in the order Megaloptera.
Nervous System They commonly are known as dobsonflies and
fishflies.
Alderflies and Dobsonflies
Corpus Allatum (pl., Corpora
Allata)
Corylophidae
Small endocrine glands behind the brain (Fig.115),
with nervous connections to the brain, and the A family of beetles (order Coleoptera). They com-
source of juvenile hormone. monly are known as minute fungus beetles.
Endocrine Regulation of Insect Reproduction Beetles
 Cosmet Moths (Lepidoptera: Cosmopterigidae)
C 1075

Corpus Allatum (pl., Corpora Allata), Figure 115 Cross section showing the relationships of the principal
endocrine glands with the brain (adapted from Chapman, The insects: structure and function).

Cosmetic Damage are used: Antequerinae, Cosmopteriginae, and

Chrysopeleiinae. The family is part of the super-
Superficial injury that affects the appearance, and family Gelechioidea in the section Tineina, sub-
hence the value of a crop, though leaving the quan- section Tineina, of the division Ditrysia. Adults
tity and nutritional value unaffected. small (632 mm wingspan), with head smooth-
scaled; haustellum scaled; labial palpi recurved;
maxillary palpi 4-segmented. Wings very linear
Cosmet Moths (Lepidoptera: and with long fringes on hindwings. Maculation
Cosmopterigidae) varies greatly (Fig. 116) but many have various
spots or lines, often with metallic-iridescence.
John B. Heppner Adults mostly diurnal, but some are crepuscular.
Florida State Collection of Arthropods, Larvae mostly leafminers or needleminers, but
Gainesville, FL, USA some are borers of various plant parts; a few are
predaceous on Hemiptera. Hosts are varied but
Cosmet moths, family Cosmopterigidae, total many records are for Leguminosae. Ovovivipary
over 1,540 species worldwide, but the extant fauna has been recorded in a few species. Some eco-
may encompass 3,500 species. Three subfamilies nomic species are known.
1076
C Cosmopolitan

Costa
The basal segment of the leg, articulating with the
body. Also the thickened anterior-most vein that
forms the anterior margin of the wing.
Legs of Hexapods

Cosmet Moths (Lepidoptera: Cosmopterigidae), Costal Break

Figure 116 Example of cosmet moths
(Cosmopterigidae), Ithome concolorella A section of the costal vein where the sclerotiza-
(Chambers) from Florida USA. tion is weak or absent, and the vein appears to be
broken.
Wings of Insects
References

Clarke JFG (1965) Cosmopterigidae. In: Clarke JFG (ed) Costal Cell
Catalogue of the type specimens of Microlepidoptera
in the British Museum (Natural History) described by
Edward Meyrick, 5:471559. British Museum (Natural
The wing space between the costal and subcostal
Hisory), London veins.
Hodges RW (1978) Gelechioidea. Cosmopterigidae. In: Wings of Insects
Dominick RB (eds) The moths of America north of
Mexico including Greenland. Fasc. 6.1. E. W. Classey,
London, 166 pp, 6 pl
Mariani M (1935) Monografie sulle Cosmopteryx d Europa. Costal Margin
Giornale del Sciencia Naturale Economica Palermo
38:154 (1934)
The anterior margin (Fig.117) of the wing.
Riedl T (196269) Matriaux pour la connaissance des
Momphidae (Lepidoptera) palarctiques. Polski Pismo Wings of Insects
Entomologica, 32:6975 (1962); 33:101106 (1963);
35:419468 (1965); 36:7584 (1966); (B) 12:115118
(1966); 37:2546 (1967); 39:635923 (1969) [mostly
Cosmopterigidae]
Costs and Benefits of Insects
John L. Capinera
University of Florida, Gainesville, FL, USA
Cosmopolitan
Insects (arthropods) have a well-deserved reputa-
Distributed throughout the world, or nearly so. tion for significant economic and ecological effects,
but there tends to be over-emphasis on negative
effects and under-emphasis on beneficial effects.
Cossidae The emphasis on negative effects results from well-
known insect competition with humans for food
A family of moths (order Lepidoptera). They com- and fiber resources, and the role of insects in trans-
monly are known as carpenterworm moths, goat mitting diseases to humans, domesticated and
moths, and leopard moths. wild animals, and to crop and forest plants. The
Carpenterworm Moths negative effects of insects are due not only to their
Butterflies and Moths direct damage (usually by feeding) and indirect
 Costs and Benefits of Insects
C 1077

Archetype tracheation of wing pad

basal fold
fulcrum
costal margin Sc1 Sc2
(1C) h (2C) (Scr) R1
Sc
+ + (Sc) R2
R R1
(2R1)

RS
(1R1)
r
M R2+3 (R2)
(R) R4+5
+
(1R3 ) R3
Cu
+

s (2R3)
1+2 r-m apex
axilla P


(R5)
(M) 3+4 (R4) R4
(1M2)
(M1)
m-cu m R5
(3A) (M4 ) M1
(2M2)
+ +
2J + 1A (M3)
3A + (Cu) M2
+ 2A
1J
M3
(P)
(Cu1)
(2A) apical
M4
(1A) margin
3A Cu1
P Cu2
jugal fold 2A
1A anal notch
jugal notch anal margin anal furrow

jugum vannus remigium

Archetype wing venation

Costal Margin, Figure 117 Hypothetical ancestral pattern of wing venation.

effects (often by transmission of plant and animal The Negative Effects of Insects on
diseases), but by the costs of preventing or reduc- Crops and Livestock
ing damage (Table 21). There is a rich literature
purporting to provide documentation of losses Yield Loss
attributable to pests, though some of it has been
challenged. In contrast, the beneficial effects are The reduction in crop yields and costs of prevent-
less well documented. In part, there has not been ing damage attributable to insects are notoriously
much incentive to document the beneficial effects difficult to obtain. Even in the USA, where consid-
of insects. However, the under-appreciation of erable efforts to estimate loss have been made,
insects is also due to the difficulty in assigning there is considerable variation among loss esti-
monetary value to the benefits derived from insect mates, and concern about their reliability. Studies
pollination (next to items of commerce such as of the major crops conducted in the USA indicate
silk and honey, probably the best-documented that without insecticides, 50% or more of the
benefit), the decomposition of plant materials and major crops could be lost to insects. Generally,
animal dung, the biological suppression of pest crop losses in the USA due to insect and mite pests
insects and weeds, and the role of insects in recre- (with pest control practices) are estimated to be
ation, or as food for fish and other wildlife. The 1315%, a value of perhaps $35 billion annually
benefits of insects as food for humans, and in pro- (1998 estimate). In developing countries, however,
duction of silk, shellac, and pigments is worth losses are greater, usually 2030% of preharvest
mentioning, but small in comparison to some yield, and then additional losses during storage.
other benefits. The cost of pesticides for prevention of crop
1078
C Costs and Benefits of Insects

Costs and Benefits of Insects, Table 21 Losses associated with some nonindigenous pests in the USA
(adapted from Pimentel et al. 2000). NA signifies information not available
Type of organism Losses ($ millions) Control costs ($ millions) Total costs ($ millions)
Plants
Purple loosestrife NA 45 45
Aquatic weeds 10 100 110
Melaleuca tree NA 36 36
Crop weeds 23,400 3,000 26,400
Pasture weeds 1,000 5,000 6,000
Turfgrass weeds NA 1,500 1,500
Mammals
Wild horses and burros 5 NA 5
Feral pigs 800 0.5 800.55
Mongooses 50 NA 50
Rats 19,000 NA 19,000
Cats 17,000 NA 17,000
Dogs 250 NA 250
Birds
Pigeons 1,100 NA 1,100
Starlings 800 NA 800
Reptiles and
amphibians
Brown tree snake 1 4.6 5.6
Fishes 1,000 NA 1,000
Arthropods
Imported fire ant 600 400 1,000
Formosan termite 1,000 NA 1,000
Green crab 44 NA 44
Gypsy moth NA 11 11
Crop pests 13,900 500 14,400
Turfgrass pests NA 1,500 1,500
Forest pests 2,100 NA 2,100
Molluscs
Zebra mussel NA NA 100
Asian clam 1,000 NA 1,000
Shipworm 205 NA 205
Microbes
Crop plant pathogens 21,000 500 21,500
Turfgrass pathogens NA 2,000 2,000
Forest plant pathogens 2,100 NA 2,100
 Costs and Benefits of Insects
C 1079

Costs and Benefits of Insects, Table 21 Losses associated with some nonindigenous pests in the USA
(adapted from Pimentel et al. 2000). NA signifies information not available (Continued)
Type of organism Losses ($ millions) Control costs ($ millions) Total costs ($ millions)
Dutch elm disease NA 100 100
Livestock disease 9,000 NA 9,000
Human disease NA 6,500 6,500
All organisms 136,630

damage in the USA is estimated at $3 billion been used, but it likely underestimates the effects
annually (2003 estimate). Because about 40% of of nonindigenous species, which often account
pests are nonindigenous, their contribution to the for disproportionately large amounts of damage.
loss is estimated at about $15 billion. However, For example, of the total crop losses attributable
nonindigenous pests are more likely to be serious to arthropods in three states of the USA, Hawaii,
pests than are indigenous species, so this is likely Florida and California, the proportions due to
an underestimate of the effects of invaders. Also, nonindigenous species are estimated to be 98, 95,
considerable effort is directed to preventing move- and 67%, respectively, much higher than the pro-
ment of pests from country to country, and in portions of species that are nonindigenous.
eliminating (eradicating) or suppressing newly The effects of nonindigenous insects are much
arrived pests, so these costs should be added to the greater than the simple monetary loss. For exam-
losses associated with nonindigenous species. The ple, the woolly adelgid, Adelges piceae (Ratzeburg)
losses to livestock are estimated to total an addi- (Hemiptera: Adelgidae), has killed about 90% of
tional $9 billion annually. Fraser fir (Abies fraseri) trees in the southern
Appalachian Mountains, disrupting local ecosystems
and leading to local shifts in avifauna. In New
Nonindigenous (Invasive) Pests England, the occurrence of gypsy moth defolia-
tion in oak-dominated forests is apparently con-
The monetary cost of only the nonindigenous tributing to the decline in abundance of Saturniidae
insect pests affecting the USA was estimated in and other large summer moths, although it is
2000 to total about 15% of the total cost of nonin- debatable whether the decline is due to loss of
digenous organisms. The effects of nonindigenous favored food, enhanced abundance of generalist
weeds, mammals, and plant pathogens were each parasitoids, or nontarget effects of gypsy moth
estimated to be greater than the effects of insects, suppression. Although biodiversity is obviously
but insects reportedly accounted for more loss affected, it is not possible to affix a monetary value
than birds, reptiles and amphibians, fishes, mol- to these changes.
luscs, livestock diseases, and human diseases.
Monetary loss due to nonindigenous arthropods
is considered to be about $16 billion in both the Pesticides
USA and in India, and is variously considered to
represent 4060% of the losses due to arthropods. An important negative effect of pests is the cost of
Sometimes the damage attributable to nonindig- preventing their damage. These costs include the
enous species is partitioned according to propor- economic, environmental, and health effects of
tions of indigenous and nonindigenous species pesticides. The world market for pesticides is esti-
in the pest species assemblage. This approach has mated at about $31 billion (2005 estimate). The
1080
C Costs and Benefits of Insects

USA is the biggest market, both in terms of costs mites, and many ticks can cause paralysis of mam-
(33%) and amount of active ingredients applied mals. Predation of ground-nesting bird nestlings,
(22%). After North America, the next biggest con- sea turtle eggs, and other small wildlife by red
sumer of pesticides is Southeast Asia, followed by imported fire ant, Solenopsis invicta Buren, is of
Europe, South America, and finally Africa and the considerable concern in the southeastern USA, as
Middle East. However, herbicides are used more is predation by Argentine ant, Linepithema humile
extensively than insecticides. The use of insecti- (Mayr) (formerly Iridomyrmex humilis Mayr), on
cides, as measured by amount of active ingredient, the west coast of the USA.
is about 20% of all pesticide use. In North Amer-
ica, insecticide use in agriculture has been decreas-
ing for some time due to both the shift to products Disease Transmission
that are effective at lower rates of application, and
the recognition that overuse of insecticides has Of particular importance to wildlife is the trans-
many detrimental effects. In many other areas of mission of diseases by arthropods. Eastern equine
the world, however, insecticide use continues to encephalitis is an example of a common wildlife
increase. The cost of insecticides used worldwide disease transmitted by mosquitoes. Found in east-
is $7.7 billion (2005 estimate), about 25% of the ern North America and south to Argentina and
cost of all pesticides. For comparison, the cost Peru, the disease is due to a virus that is harbored
of other pesticides (in $ billions) is herbicides, most commonly in passerine and other perching
14.8; fungicides, 7.5; and other, 1.1. Nearly every- birds, which serve as the amplification hosts. Mos-
where, the agricultural sector is the principal quitoes feeding on these birds when they are vire-
consumer of pesticides. In the USA, for example, mic obtain high concentrations of virus in the
agriculture uses about 77% of the pesticides ingested blood, and in turn become infected. Upon
applied, whereas the urban pest control industry feeding on other birds, the mosquitoes transmit
(structural, building interiors, and landscape) and the disease. Wildlife differ greatly in susceptibility.
government use about 14%, and consumer use Nonindigenous species such as pheasants, chukar
(self-applied home and garden) is only about 9%. partridge, and pigeon are most susceptible, but an
endangered native bird, whooping crane, readily
succumbs to the disease. Symptoms of infection
The Negative Effects of Insects on can include lethargy and lack of coordination;
Wildlife surely such animals are more susceptible to preda-
tion even if they survive infection. Other examples
Biting and Stinging of diseases affecting wildlife include tularemia
(rabbit fever) caused by Francisella tularensis,
Insects can be detrimental to wildlife due to direct which is transmitted by tick and insect bites and
effects (biting, stinging, disease transmission) or infects over 100 species of mammals and 25 spe-
indirect effects (nontarget effects of insecticides). cies of birds; bubonic plague caused by Yersinia
Blood feeding by mosquitoes (Diptera: Culici- pestis, which is transmitted by fleas to rodents,
dae), deer flies (Diptera: Tabanidae), ticks rabbits and other mammals; Lyme disease caused
(Acarina: Ixodida) and other wildlife parasites by Borrelia burgdorferi, which is transmitted by
undoubtedly causes considerable annoyance, and Ixodes ticks to deer, mice, bats, squirrels, weasels,
sometimes determines suitability of habitat or and others, including reptiles and birds; and West
affects feeding behavior. For example, birds have Nile virus caused by a flavivirus, and which is
been known to abandon their nests and fledglings transmitted by mosquitoes to 250 species of birds
due to the abundance of blood-feeding ticks or and 18 species of mammals.
 Costs and Benefits of Insects
C 1081

Pesticides later, or eggs left unhatched or nestlings left to

starve. Organophosphate and carbamate insecti-
Insects can be considered detrimental to wildlife cides are most commonly implicated.
by virtue of stimulating use of insecticides; expo- The use of persistent lipophilic insecticides,
sure to pesticides can be deleterious to all wildlife, which tend to accumulate in animals that are
but particularly to birds. A simple example is higher on the food chain, has long been known to
the presence of seed-feeding flies, Delia spp. affect hatching success in predatory birds (rap-
(Anthomyiidae), which damage crop seeds planted tors). The widespread use of DDT, in particular,
in the spring. To prevent damage by insects while was linked to production of abnormally thin egg
the seed is germinating, coatings containing insec- shells and subsequent declines in successful rap-
ticides are commonly applied to seeds before they tor reproduction. DDT and related products
are planted. Seed treatment with insecticides (and interfere with calcium metabolism. Less well
often fungicides) not only protects the germinat- known, but not at all surprising, are the effects of
ing seed, but if the insecticide acts systemically it DDT and dicofol on alligators. Male alligators
may also impart protection to young plants, par- living in Lake Apopka, Florida, have low testos-
ticularly from piercing-sucking insects such as terone levels. Lake Apopka was the site of a DDT
aphids. Unfortunately, birds will often feed on and dicofol (which is closely related to DDT)
seeds that have been recently planted, and thereby spill, and the insecticides had estrogen-like
ingest a lethal dose of insecticide. Another prob- effects, resulting in feminization of the males.
lem results from broadcast application of granular The penises of male alligators were 25% smaller,
insecticides to the soil surface. Probably because bone density was affected in females, and egg
sand is sometimes consumed by birds to aid in hatching was reduced. Alligator numbers plum-
grinding up seeds, birds sometimes feed on granu- meted in the years after the pesticide spill. DDT
lar insecticide, again resulting in bird mortality. was widely used before its adverse effects were
Lastly, application of liquid insecticides sometimes fully appreciated, and though its use is prohibited
results in a lethal dose of insecticide being applied in many areas of the world, it remains in use else-
directly to wildlife. Though this seems unlikely, where due to its effectiveness, persistence, and
when aircraft are used to apply insecticides, exten- low cost. Birds that migrate long distances may
sive land area is treated quickly and wildlife may move into and out of countries where DDT is
not have adequate time to escape. Not only are used, so it remains a continuing threat even where
crop fields treated, but often adjacent border areas it is not currently used. The benefits of DDT to
(hedge rows, fence rows, irrigation ditches, road humans are not trivial, especially in countries
margins) are treated deliberately or inadvertently. plagued by malaria and other mosquito-vectored
In the case of nestling birds, there is no opportu- diseases, so there remains considerable interest
nity to avoid exposure. There is also a problem in continuing its use. Consequently, there is
with birds flying into fields that were recently extensive literature for and against DDT.
treated, perhaps to feast on dying insecticide-con- Although the use of DDT has attracted con-
taining insects, thereby ingesting a lethal dose of siderable attention as a disruptor of wildlife pop-
insecticide. Other vertebrates are not immune to ulations, its direct toxicity is quite limited. Certain
such poisoning, but it is most pronounced in avi- cyclodiene insecticides, particularly heptachlor,
fauna and fish. The United States Fish and Wildlife dieldrin and aldrin, are similarly persistent and
Service estimates that over 670 million birds are more toxic. Indeed, it is the cyclodiene insecti-
exposed to pesticide on farmlands in the USA, and cides that accounted for most of the direct mor-
that about 10% die immediately as a result. This tality to birds in the 1950s1960s, not DDT.
does not include those that are sickened and die Generally, use of DDT, cyclodienes, and similar
1082
C Costs and Benefits of Insects

lipophilic products that accumulate in wildlife The Negative Effects of Biting Pests
has declined greatly. Where use of these products and Vectors of Human Disease
has been reduced, wildlife populations have
recovered. Many people are killed annually by diseases that
Pesticide use also affects wildlife indirectly, are vectored by arthropods, and even more suf-
and these indirect effects may be more impor- fer chronic infections that impair their ability to
tant than the direct exposure of wildlife to insec- work efficiently and live normal lives. Probably
ticides. One important indirect effect is the the top arthropod-transmitted diseases are
depletion of insect populations caused by insec- malaria, leishmaniasis, sleeping sickness, lym-
ticide use. Broad-spectrum insecticides cause phatic filariasis, and dengue. These also are
treated fields to become almost sterile, and if the among the most important diseases in tropical
products are persistent the fields may remain areas of the world. Some of the important arthro-
depleted of insect life for weeks. Birds will pod-transmitted diseases, the vector, and human
attempt to compensate for loss of insect food by pathogen are:
foraging elsewhere, but there are limits as to how African relapsing fever (Ornithodorus spp. (Borrelia spp.)
far they can fly and then return regularly to a Amoebic dysentery (Musca domestica) (Entamoeba
nest with food for nestlings. If the distance is too histolytica)
great, the nest will be abandoned. Due to the Chagas disease (Triatoma spp.) (Trypanosoma cruzi)
high cost of insecticide development and regis- Cholera (flies) (Vibrio cholerae)
tration, agrochemical companies favor develop- Dengue (Aedes aegypti) (virus)
ment of broad-spectrum products because, once Encephalitis (mosquitoes) (virus)
registered, they can be used extensively and gen- Epidemic fever (Pediculus humanus) (Rickettsia
erate large profits before the patent expires. The prowazeki)
nonselective nature of such products is particu- Epidemic relapsing fever (Pediculus humanus) (Borre-
larly damaging to bird populations; if only the lia recurrentis)
pests were affected, some insect fauna would Filariasis (mosquitoes) (Wuchereria bancrofti)
remain to support bird life. Sleeping sickness (Glossina spp.) (Trypanosoma spp.)
Another indirect effect of pesticides on wild- Leishmaniasis (Phlebotomus spp.) (Leishmania spp.)
life is the change in floral diversity (loss of edible Loasis (Chrysops spp.) (Loa loa)
weeds, weed seeds, or fungi, and also depletion of Lyme disease (ticks) (Borrelia burgdorferi)
habitat or cover) caused by herbicide (and to a Malaria (Anopheles spp.) (Plasmodium spp.)
lesser degree by fungicide) application. Grass and Murine typhus (Xenopsylla cheopis) (Rickettsia typhi)
weed seed can be an important food resource, Onchocerciasis (Simulium spp.) (Onchocerca volvulus)
and clean culture of crops though beneficial in Plague (Xenopsylla cheopis) (Pasturella pestis)
terms of plant growth efficiency, energy efficiency Rocky Mountain spotted fever (ticks) (Rickettsia ri-
and water conservation can greatly reduce food ckettsii)
abundance for bird life. This problem is exacer- Scrub typhus (Trombicula spp.) (Rickettsia tutsuga-
bated by the ever-increasing scale (field size) in mushi)
agriculture, which usually results from merging Trench fever (Pediculus humanus) (Rickettsia quintana)
smaller fields, reducing crop heterogeneity, and Tularemia (Chrysops spp.) (Francisella tularensis)
in destroying hedge-row and other border area Typhoid fever (flies) (Salmonella typhi)
habitat. The results of the combined effects are Yaws (flies) (Treponema pertenue)
often dramatic. In Britain, for example, two-thirds Yellow fever (Aedes aegypti) (virus)
of farmland bird species have shown declines in Likely the most important arbovirus is
abundance. dengue, which is found throughout the world in
 Costs and Benefits of Insects
C 1083

tropical areas. According to the USAs Centers The Negative Effects of Urban
for Disease Control and Prevention (CDC), as (Structural, Household, and
of 2005 tens of millions of people were being Landscape) Pests
infected, and tens of thousands of people were
contracting dengue hemorrhagic fever. Though Urban pests are among the most important
dengue usually is not lethal, the closely related because they affect so many people, not only
but more severe dengue hemorrhagic fever can those in rural/agricultural environments. Also,
be very dangerous, often resulting in mortality the pesticide market for structural, household
of about 5% of its victims. Yellow fever remains and landscape pests is large and unusually lucra-
an important arbovirus in the tropics, with per- tive for pesticide companies. Thus, pesticide use
haps 200,000 cases per year, and 30,000 deaths. is actively promoted at the same time that major
Similarly, Japanese encephalitis causes about efforts are under way to reduce pesticide use in
40,000 cases per year, inflicting 1015,000 crops. In some cases there is justification for pest
deaths annually in Asia. West Nile virus recently control in the urban environment, particularly in
gained access to North America, and though the case of termite and red imported fire ant con-
only a few thousand people have contracted this trol. Other examples of important urban pests,
disease thus far, like other encephalitis diseases, and the basis of their importance, include cock-
survivors often suffer significant neurological roaches (mostly a sanitation issue), flies (sanita-
impairment. Malaria remains the most impor- tion), household ants (sanitation), stored grain
tant insect-vectored disease, infecting 300500 insects (sanitation), carpet beetles and clothes
million people per year, and resulting in about moths (damage to wool products), lice and fleas
one million deaths per year. The economic and (human and pet health), and turf and ornamental
sociological consequences of this disease are plant pests (aesthetics).
devastating. Termites can be extremely destructive by
Domestic animals are a very important source attacking wood buildings, compromising their
of food and companionship for humans, and they structural integrity. Even buildings constructed
also can succumb to diseases transmitted by largely of concrete can be damaged because sub-
arthropods. Among the important diseases of terranean termites will tunnel over concrete to
domesticated animals, the vector, and the animal get to wood roof supports, and because drywood
pathogen are: termites and some subterranean termites will
African horse sickness (Culicoides spp.) (virus) alight on roofs and attack from above. In addi-
Anthrax (Musca domestica) (Bacillus anthracis) tion to structural materials, damage may be
Blue tongue of sheep (Culicoides spp.) (virus) inflicted to cabinetry, furniture, and wood panel-
Cattle filariasis (blackflies) (Onchocerca gutturosa, etc.) ing and trim. Damage by termites is a severe
Dirofilariasis (mosquitoes) (Dirofilaria spp.) problem in all but the northernmost climates, but
Fowl spirochaetosis (Dermanyssus gallinae) (Borrelia is especially acute in warmer areas because ter-
anserina) mites are active for longer periods of time. The
Heartwater of cattle (Amblyomma hebraeum) (Rickett- economic effect of termites is estimated at $56
sia ruminantium) billion per year (2006 estimate) in the USA, with
Mal de caderas (Stomoxys calcitrans) (Trypanosoma most of the damage occurring in the warm-
equinum) weather, southern states from Florida to Califor-
Nagana (Glossina spp.) (Trypanosoma spp.) nia, and also in Hawaii.
Surra (Tabanidae) (Trypanosoma evansi) Arthropods living indoors, such as house dust
Texas cattle fever (Boophilus annulatus) (Babesia mites and cockroaches, can be an important source
bigemina) of allergens. Cockroach allergens are proteins shed
1084
C Costs and Benefits of Insects

by cockroaches, and also found in their feces. Expo- mostly dependent on insects, and bees in particu-
sure by children to cockroach allergens is believed lar, for successful pollination. Notable among
to be a major risk factor for asthma. Currently, about crops requiring pollination are most fruits and
20% of American children are allergic to cockroach nuts, many vegetables, and a few field crops. The
allergens, and asthma rates are particularly high in grain crops, including corn (maize) are wind-pol-
inner-city areas where cockroach problems fre- linated. Wild pollinators can be quite important
quently occur. Such children miss more school and for plants requiring insect pollination, and may be
have more hospitalizations for asthma. Cockroach completely effective for isolated plants or small
allergy is not limited to children, however. In addi- fields. However, in modern crop production the
tion to allergy/asthma issues, about $200 million is high density of crops and the long distance of
expended annually in the USA for cockroach sup- crops from uncultivated areas may limit the ability
pression in homes and businesses, particularly in of wild pollinators to effectively provide pollina-
the food/restaurant industries. tion of crop plants. Therefore, hives of bees (usu-
Red imported fire ant, Solenopsis invicta Buren ally Hymenoptera: Apidae and specifically Apis
(Hymenoptera: Formicidae), is an interesting and mellifera) are often moved adjacent to the crops
complex case because not only is it a very impor- requiring pollination. In the USA, about 2.5 mil-
tant urban pest, but it also affects agricultural and lion hives were rented for pollination services in
natural environments, and even has beneficial 1999, clearly indicating the importance of pollina-
aspects. A native of South America, it entered the tion. Nearly 85% of the rentals occurred in only
USA without its natural enemies and has prolifer- seven crops (in descending order of importance):
ated largely unchecked. Because it stings, it threat- almond, apple, melons, alfalfa seed, plum/prune,
ens the lives of people, pests, livestock and wildlife. avocado, and blueberry.
The economic effect in the USA is estimated at $5.6 Estimates of the dependence of crops on
billion per year, with the principal impacts being to pollination, and the proportion of pollination
residential households ($3.6 billion), disruption of accomplished by wild pollinators versus domes-
electric and communication systems ($637 mil- ticated honey bees, are shown in Table 22. Note
lion), crop destruction ($428 million), golf course that dependence varies considerably from crop
damage and treatment ($318 million), and effects to crop, and even within related crops (e.g., com-
on schools and school yards ($130 million) (2004 pare grapefruit to lemon, which are both citrus
estimates). Other ants can be a nuisance, and car- crops). The value of pollination is estimated at
penter ants can cause structural damage, but none over $3 billion in the USA alone (2001 estimate),
approach the impact of S. invicta. On the other though there are earlier estimates of $5.7 billion
hand, S. invicta is an effective predator of insects, in pollination benefits. Though this is a small
and in some cropping systems such as sugarcane, value relative to the total value of crops, these
this species contributes significantly to the biologi- insect-pollinated crops account for important
cal suppression of other pest species. diversity in our diet. Imagine subsisting on corn,
wheat and barley, spiced up with an occasional
potato; a bland diet, indeed! The benefits of fruit
The Benefits of Pollination and and vegetables are considerable, both for nutri-
Honey Production tion and appetite.
However, some caution should be used in
Pollination interpreting pollination data. Sometimes insect
pollinated crops can be produced without pol-
Pollination is accomplished by insects, vertebrates lination. Thus, with asparagus, carrots and
(birds and bats), and wind, but certain crops are alfalfa (for example) a crop can be obtained in
 Costs and Benefits of Insects
C 1085

Costs and Benefits of Insects, Table 22 The value of crop production in the USA resulting from
pollination, 20012003, in relation to the source of pollinators (adapted from Losey and Vaughn, 2006)
Crop Mean annual Dependent on Domesticated Indigenous Mean value
value pollination (%) nonindigenous bees (%) from indig-
($millions) bees (%) enous bees
($ millions)
Fruits and nuts
Almond 1120.0 100 100 10 158.51
Apple 1585.1 100 90 20 4.2
Apricot 30.0 70 80 10 38.24
Avocado 382.4 100 90 10 2.31
Blueberry, wild 23.1 100 90 10 19.29
Blueberry, 192.9 100 90 10 0.31
cultivated
Boysenberry 3.9 80 90 10 0.31
Cherry, sweet 290.6 90 90 10 26.15
Cherry, tart 56.3 90 90 10 5.07
Citrus
Grapefruit 278.4 80 90 10 22.27
Lemon 286.1 20 10 90 51.50
Lime 2.0 30 90 10 0.06
Orange 1713.6 30 90 10 51.41
Tangelo 10.8 40 90 10 0.43
Tangerine 112.0 50 90 10 5.60
Temple 6.1 30 90 10 0.18
Cranberry 159.7 10 90 10 15097
Grape 2774.8 10 10 90 249.73
Kiwifruit 16.7 90 90 10 1.50
Loganberry 158.0 50 80 20 15.80
Macadamia 31.1 90 90 10 2.80
Nectarine 121.2 60 80 20 14.54
Olive 66.5 10 10 90 5.99
Peach 487.9 60 80 20 58.55
Pear 263.9 70 90 10 18.47
Plum & prune 197.8 70 90 10 13.85
Raspberry 95.8 80 90 10 7.19
Strawberry 1187.6 20 10 90 213.77
Vegetables
Asparagus 164.3 100 90 10 16.43
Broccoli 543.4 100 90 10 54.34
Carrot 575.5 100 90 10 57.55
1086
C Costs and Benefits of Insects

Costs and Benefits of Insects, Table 22 The value of crop production in the USA resulting from
pollination, 20012003, in relation to the source of pollinators (adapted from Losey and Vaughn, 2006)
(Continued)
Crop Mean annual Dependent on Domesticated Indigenous Mean value
value pollination (%) nonindigenous bees (%) from indig-
($millions) bees (%) enous bees
($ millions)
Cauliflower 219.8 100 90 10 21.98
Celery 256.5 100 80 20 51.30
Cucumber 379.5 90 90 10 34.16
Cantaloupe 401.0 80 90 10 32.08
Honeydew 94.1 80 90 10 7.53
Onion 808.0 100 90 10 80.80
Pumpkin 75.5 90 10 90 61.16
Squash 192.3 90 10 90 155.76
Vegetable seed 61.0 100 90 10 6.10
Watermelon 315.9 0.7 0.9 0.1 22.11
Field crops
Alfalfa hay 7212.8 100 95 5 360.64
Alfalfa seed 109.0 100 95 5 5.45
Cotton lint 3449.5 20 80 20 137.98
Cotton seed 689.3 20 80 20 27.57
Legume seed 34.1 100 90 10 3.41
Peanut 793.1 10 20 80 63.45
Rapeseed 0.3 100 90 10 0.03
Soybean 15095.2 10 50 50 754.76
Sugar beet 1057.3 10 20 80 84.58
Sunflower 312.7 100 90 10 31.27
Total 3074.13

the absence of pollinators, but they require pol- require the presence of pollinators. In contrast,
linators for propagation (seed production). A for other crops (e.g., apple, avocado, and blue-
relatively small area of carrots, if properly pol- berry) every fruit harvested requires visitation
linated, can produce enough seed for all the car- by an insect pollinator.
rots grown as vegetables. In the case of alfalfa, We take for granted that pastures and prai-
the crop can be harvested several times per year, ries will be populated by wildflowers. A spring
and for several years, before replanting. The walk through woodlands is a wonderful way to
extreme case is asparagus, which is normally see small herbaceous plants in their full glory.
harvested for a decade before replanting. Thus, And what would a tropical landscape be with-
although the existence of these crops (and many out a profusion of flowers? Without insects to
others) is dependent on insect pollination, the perform pollination services, these and many
production of any particular field may not other environments would seem sterile, lacking
 Costs and Benefits of Insects
C 1087

in the bright colors we normally expect in our The Benefits of Animal Dung
landscapes. Most plants that produce colorful Decomposition
flowers do so to attract insects, and without
these pollinators the plants would decline or Although it is difficult to estimate the benefits of
disappear. Biodiversity would decline tremen- insect decomposition of plant products, in a quali-
dously, and highly coevolved systems, such as tative sense it is certain that insects speed up plant
some orchids, would certainly disappear. It is matter decomposition, allowing more light to
difficult to assign economic or even aesthetic reach the forest floor and increasing the rate of
values to the loss of insect pollination, but it nutrient recycling. By hastening the demise of
certainly would represent a very different world senescent vegetation, especially trees, insect
than we now enjoy. decomposers allow the forests to boost productiv-
ity. Averaged across ecosystems, insects consume
about 5% of available (not including woody tis-
Honey sues) biomass. Thus, herbivores can affect ecosys-
tem productivity by regulating the rate of energy
Honey is an important by-product of pollina- input. Saprophytic species (feeding on feces and
tion. At one time, honey production was more honeydew) cannot directly affect primary produc-
important; farmsteads routinely produced their tivity, but can regulate it indirectly by affecting the
own supply of sweetener from their own hives. rate of nutrient recycling. Feces and honeydew
Later, an industry grew up to supply honey, often allow premature release of nutrients, boosting
manned by migratory beekeepers who kept hun- nitrogen flow to the plants.
dreds or thousands of hives and followed the One aspect of decomposition that has been
availability of nectar for their bees. While this studied is consumption of dung by insects, par-
still occurs to some extent, in many instances the ticularly by dung beetles (Scarabaeidae: Scarabaei-
importance of honey has been supplanted by nae). Cattle produce large quantities of dung,
other sweeteners (from sugar cane, sugar beet, or about 9,000 kg (about 21 cubic meters) per animal
corn). Nevertheless, honey production is an per year. Scarab beetles are quite efficient at decom-
important supplement to pollination services for posing this waste, which otherwise smothers
many beekeepers, and the only product for some. vegetation, fouls vegetation leading to avoidance
The value of honey produced in the USA was by grazing animals, and ties up nitrogen in an
$157 million in 2005, coming from 2.4 million unusable form. Decomposition also reduces the
colonies. But about 60%of the honey consumed breeding of parasites and nuisance and biting flies
in the USA was imported from other countries, that would otherwise breed in the dung.
so this value underestimates its importance. The accelerated decomposition of dung by dung
World honey production in 2005 was estimated beetles in the USA is estimated to provide at least
by the Food and Agriculture Organization of the $380 million in benefits annually (2006 estimate).
United Nations to be slightly over 1.4 billion kg. The economic benefits attributable to specific actions
Production has increased steadily over the last include reduction in fouling of forage, $122 million;
decade or so, with most of the increases coming reduced volatilization of nitrogen, $58 million;
from Asia and South America, while honey pro- reduced parasitism, $70 million; and reduced num-
duction in the USA continues to decline, along bers of pest flies, $130 million. Dung beetle activity is
with the number of beekeepers and colonies of not as great in the USA as it is in many other coun-
bees. It is difficult to estimate the value of honey tries due to the animal husbandry practices of the
throughout the world due to differing curren- USA. Specifically, large numbers of cattle are pas-
cies, but it likely was about $3 billion in 2005. tured in feedlots (beef cattle) or on concrete (dairy
1088
C Costs and Benefits of Insects

cattle) rather than on rangeland, and dung beetles do is available to plants and thus functions as a fertil-
not inhabit these areas. Also, over half of the cattle in izer. The difference is considerable, about an 80%
the USA are treated with avermectin pesticides to difference in nitrogen content. The enhanced plant
control parasites, and the avermectin residues in the growth associated with incorporation of dung into
dung inhibits development of dung beetles. Thus, the the soil by dung beetles is estimated to increase
benefits due to dung beetles are likely considerably available forage by about $58 million per year in
greater in countries that maintain their livestock in the USA. As in the previous example, this is only
pastures or do not treat with avermectins. true if the stocking rate is adjusted appropriately
The benefit of dung beetles is perhaps best to take advantage of the additional forage.
seen in Australia, a continent that lacked mam- The availability of dung allows survival of
mals (and mammal dung) until cattle were intro- parasites and pests, and reducing the longevity of
duced during settlement by Europeans in 1788. the dung should reduce survival of the parasites
The abundance of cattle in Australia (about 20 and pests as well. The economic benefits have been
million currently) produces an abundance of dung calculated to be $70 million and $380 million per
that is slow to decompose, which allows bush fly, year, respectively, in the USA. As noted earlier,
Musca vetustissima Walker (Diptera: Muscidae), however, avermectins are widely used in the USA,
to breed in huge numbers in the dung. Marsupial so the benefit of beetles might be better in regions
dung, the natural food source of bush fly, is much not using these pesticides. Also, these calculations
smaller and tends to dry out quickly and become are based only on beef cattle, but benefits also
unsuitable for fly larvae. To deal with the reduc- accrue to other livestock such as dairy cattle, horse,
tion in pasture by the slowly decomposing dung, goats, and sheep, so these certainly are low esti-
and to reduce fly breeding, many species of dung mates of the economic benefit of dung beetles.
beetles from Africa and Europe were introduced.
The result has been an 80% reduction of bush flies.
This approach has only recently been extended to The Benefits of Insects for
target dog dung, a problem in urban areas. Recreation
Losses attributed to forage fouling are derived
from the concept that cattle will not, or cannot, con- Insects are quite important as food for wildlife pop-
sume forage covered with dung. Studies conducted ulations that, in turn, support recreational activities
in California, USA, determined that the presence of such as hunting, fishing, and wildlife viewing. The
dung beetles would increase the decomposition rate importance of insects relative to wildlife popula-
of dung by about 20%. Projected over cattle on pas- tions is often overlooked, except for freshwater fish,
ture and rangeland throughout the country, it is where there is considerable appreciation for the role
possible to estimate a $122 million saving due to of insects in supporting fish populations. The
dung beetles. This assumes that stocking rates are importance of wildlife in technologically advanced
optimized to use all food. However, this is not always countries is often limited mostly to recreation, and
a realistic assumption. The California data may not the analyses reported below (2005 estimates) relate
be applicable universally. In Australia, for example, only to such values, and are limited to calculations
the benefits are much greater because dung reten- made only for the USA. However, in some parts of
tion time was reduced from as long as four years to the world wildlife is an important part of the human
as little as 48 h. diet, so the effects of insects would be proportion-
Drying of dung causes marked reduction of ally greater in such locations.
its inorganic nitrogen content, with the nitrogen Small game, but not large game, is often criti-
being released into the atmosphere. In contrast, if cally dependent on insects for food. Chicks of such
the dung is incorporated into the soil, the nitrogen popular game birds as pheasant, quail and grouse
 Costs and Benefits of Insects
C 1089

cannot survive without insects as a nutritional assess the benefits of natural biological control.
resource. Therefore, the economic effects of insects, However, it has been estimated that 65% of insects
based on the proportion of expenditures related to are being maintained in a non-damaging status
hunting these birds, is about $1.48 billion annually relative to their host plants by the action of natural
in the USA (Table 23). Waterfowl also eat insects, enemies, and only about 7% attain damaging levels
but to a lesser degree than the terrestrial species. (the others do not feed on plants). In the USA, the
Thus, the economic effect of insects as food for benefit (in 2005) of beneficial insects (predators and
waterfowl is estimated at only $0.58 billion. Other parasitoids) to cropping systems has been calculated
vertebrates that are popular with hunters, such as to be about $4.5 billion annually, whereas the
squirrels and raccoons, also consume insects as benefits due to the actions of other factors (insect
part of their diet, but their contribution to the diseases, weather, etc.) working in conjunction with
hunting economy has not been calculated. beneficial insects totals about $13.6 billion.
The majority of freshwater fish are insectivo-
rous, so the entire value of the freshwater fishing
(recreational fishing) economy can be attributed Other Benefits of Insects
to insects (Table 24). This value is $27.9 billion.
Although saltwater fish are not normally thought Silk production (sericulture)
of as insectivorous, about 25 species spend part of
their life in freshwater habitats where they feed on Silk is produced by special glands (generally modi-
insects. If the proportion of the marine fisheries fied salivary glands) in the larvae of some Lepi-
(commercial fishing) due to these species is calcu- doptera, and by other structures in some immatures
lated, it represents about $0.22 billion. and adults of mites and spiders. Only moth larvae,
Wildlife watching is an important form of however, have been exploited by humans for their
recreation, and birdwatching is central to wildlife ability to produce silk commercially. The silk natu-
observation. Wildlife viewers often also appreciate rally serves various functions, such as larval disper-
opportunities to view small mammals, reptiles and sal in the wind, leaf rolling, anchoring of pupae, and
amphibians, which often use insects as well, and construction of cocoons. It is this latter function,
many make efforts to view insects. Nevertheless, which consists of production of a single long strand
the benefits of wildlife watching are calculated of silk, which allows the silk to be unwound from
only on the basis of birdwatching, and only on the the pupal case and harvested.
basis of species of North American birds that are In different parts of the world, various species
primarily insectivorous. Thus, this is a very con- have been used to produce silk, but generally it
servative estimate, but still accounts for an eco- involves insects of the superfamily Bombycoidea,
nomic impact of $19.8 billion. and particularly Bombyx mori L. Silk has been har-
vested by humans from Bombyx mori at least since
2600 b.c. It was one of the first, and most valuable,
The Benefits of Biological Control trade commodities between China and Europe.
by Insects Though originating in China, once the insect was
smuggled out of China it was quickly spread around
As noted previously, insecticides are often used to the world, where its cultivation was limited only by
suppress pests and their damage, and this is a costly the ability to produce mulberry trees, its natural
undertaking. However, pest control would be vastly host. Besides China, Japan and India are the most
more expensive were it not for control of insects by important production centers. Now it can be pro-
their natural enemies, principally other insects. As duced on artificial diet as well. Silk is a valuable
with other estimates of insect effects, it is difficult to commodity, valued at over $1 billion annually.
1090
C Costs and Benefits of Insects

Costs and Benefits of Insects, Table 23 Insectivory in North American bird species (adapted from Losey
and Vaughan, 2006)
Order Common name No. No. primarily No. partially No. not
species insectivorous insectivorous insectivorous
Gavliiformes Loons 5 0 5 0
Podicipediformes Grebes 7 5 2 0
Procellariiformes Tubenoses 6 1 4 1
Pelicaniformes Pelicans & allies 11 0 5 6
Ciconiiformes Herons & allies 20 5 12 3
Phoenicopteri- Flamingos 1 1 0 0
formes
Anseriformes Waterfowl 44 19 24 1
Falconiformes Vultures, hawks, 31 3 18 10
& falcons
Galliformes Quail, grouse & 22 2 20 0
allies
Gruiformes Cranes & allies 13 8 5 0
Charadriiformes Shorebirds & 108 51 22 35
gulls
Columbiformes Pigeons & doves 11 0 3 8
Cuculiformes Cuckoos & 6 6 0 0
roadrunners
Strigiformes Owls 19 6 11 2
Caprimulgi- Goatsuckers 8 8 0 0
formes
Apodiformes Swifts & 20 6 14 0
hummingbirds
Trogoniformes Trogons 1 1 0 0
Coraciiformes Kingfishers 3 0 1 2
Piciformes Woodpeckers 22 22 0 0
Passeriformes Perching birds 285 251 34 0

Total 643 395 180 68
% 61 28 11

Shellac of shellac. Laccifer lacca Kerr is the species most

commonly cultured for this purpose. India pro-
Several scale insects (Hemiptera: Kerriidae) can be duces the largest proportion of the shellac on the
grown on trees in Southeast Asia and used as a world market, though production has fallen greatly
source of lac, a resin that is the principal ingredient due to the availability of synthetic resins.
 Costs and Benefits of Insects
C 1091

Costs and Benefits of Insects, Table 24 Value of commercially landed fish that rely on insects as a critical
nutritional resource (adapted from Losey and Vaughan, 2006)
Species Fish weight (kg landed) Fish value ($)
Alewife 1,675,935 384,968
Mullet, striped 15,473,230 9,504,673
Mullet, white 509,887 241,064
Mullets 444,000 310,680
Mummichog 4,590 13,221
Perch, white 2,482,006 1,082,354
Perch, yellow 1,714,342 2,914,078
Salmon, chinook 27,345,066 32,633,445
Salmon, chum 92,031,758 16,900,456
Salmon, coho 32,256,133 15,261,440
Salmon, Pacific 176 538
Salmon, pink 334,080,474 24,758,990
Salmon, sockeye 184,505,904 109,897,597
Shad, American 2,074,686 1,190,072
Shad, gizzard 5,306,259 700,916
Shad, hickory 88,339 23,199
Smelt, eulachon 1,081,152 160,842
Smelt, rainbow 489,467 730,685
Smelts 480,212 150,728
Suckers 157,164 45,384
Tilapias 5,482,778 1,223,061
Trout, lake 558,129 228,773
Trout, rainbow 308,306 189,625
Walleye 25,810 42,396
Whitefish, lake 8,604,823 6,048,110
Total 224,637,295

Dyes produce a bright red dye that once was very popu-
lar, declined in importance as synthetic materials
Commercially important dyes have been extracted became available, and now is becoming more
from insects. Probably best known is cochineal dye, popular again as a natural dye. It also is useful in
obtained from the bodies of cochineal scales, cosmetics and food. Lac dye is a byproduct of shel-
Dactylopius coccus (Hemiptera: Dactylopiidae). lac production. It has been used as a skin cosmetic,
Cultivated on Opuntia cactus, it can be used to in medicine, and for dyeing wool, silk and leather.
1092
C Costs and Benefits of Insects

Human and Animal Food because higher animals often suffer from boredom
in a zoo environment, and it is healthy to provide
Insects are not ordinarily a major source of nutri- variety and diversion, which can be provided in the
tion for humans in western societies. In some form of live insects. Thus, large mobile insects such
societies, however, insects are consumed if they as grasshoppers provide diversion as well as nutri-
are especially available or provide needed nutri- tion for some zoo animals, including monkeys.
tion during times of famine (e.g., locusts in Lastly, but importantly, insects are used as a lure
Africa), or as part of cultural tradition (e.g., as a (bait) for fishing, as some fish take live insects pref-
condiment canned grasshoppers in Southeast erentially. The same insects used for pet food tend
Asia or Maguey worms in Mexico). In Africa, to be used as fish bait.
Asia, Oceania, and Latin America it is not unusual
to find a great diversity of insects in local market-
places, and in some countries children are espe- Medical Treatment
cially likely to eat insects opportunistically.
Insects are good sources of proteins, lipids, and Though more widely used for medical treatment
vitamins, but it is difficult to raise them economi- in ancient societies, insects retain some uses in
cally. Thus, they tend to be eaten opportunisti- contemporary treatment of human ailments,
cally rather than cultured. The economic value of most notably for apitherapy (bee venom therapy)
insects as food has not been assessed, but likely is and for maggot therapy. Apitherapy is sometimes
relatively low. In a few societies, insects have been recommended for rheumatic diseases, including
prized as food. For example, the emperor Mont- arthritis and multiple sclerosis. Traditionally,
ezuma and the Aztec kings who preceded him bees were stimulated to sting the affected area,
prized the eggs of aquatic Hemiptera (called but injected venom is now also used as a form of
ahuahutle), where it was the equivalent of cav- treatment. Bee venom is also applied topically in
iar, and transported at great effort and expense to creams, liniments and ointments. Maggot ther-
Tenochtitlan for ceremonies. Surely if more of apy is more well-founded scientifically, and takes
the worlds leaders would set an example of con- advantage of the propensity of some fly larvae
suming insects, others would be induced to fol- (usually Lucilia maggots) to feed on dead and
low, setting the stage for a new insect-based food decaying flesh, but to avoid feeding on living tis-
industry! sue. Thus, live maggots are introduced to wounds
Insects often are useful for maintenance of of humans or pets to clean out necrotic tissue.
pets, as they are readily accepted and nutritious. Also, maggots excrete products that inhibit
Easily cultured insects are most generally used, growth of microbes that lead to infection of liv-
including house cricket, Acheta domesticus; meal- ing tissue and stimulate regrowth of healthy tis-
worm, Tenebrio molitar; waxworms, Galleria mello- sue. More commonly used prior to the advent of
nella; and various flies (Muscidae and Calliphoridae). modern antibiotics (the 1940s and 1950s), mag-
They are most often used as food or a food supple- got therapy continues to be used for wounds that
ment for amphibians, reptiles and birds, but rodents display difficulty in healing, and with the emer-
and some small mammals also accept them. They gence of antibiotic-resistant bacteria, there is
are sold in various forms at pet shops, including potential of renewed interest by the medical
alive, dried, and frozen. In recent time, dehydrated community.
insects have been included in some types of wild Apiculture
bird food, although this is still relatively unusual. Pollination and Flower Visitation
Also, zoos often seek live insects for their exhibit Bees
animals, both due to their nutritional value and also Ants
 Cotton Leafworm, Spodoptera littoralis (Boisduval)
C 1093

Invasive Insects morbidity among inner-city children with asthma.

NEngl J Med 336:13561363
Natural Enemies Important in Biological
Southwick EE, Southwick L Jr (1992) Estimating the eco-
Control nomic value of honey bees (Hymenoptera: Apidae) as
Insecticides agricultural pollinators in the United States. J Econ
History and Insects Entomol 85:621633
Ware GW, Whitacre DM (2004) The pesticide book. Meis-
Lyme Borreliosis terPro Information Resources, Willoughby, OH
Eastern Equine Encephalitis
West Nile Fever
Plague: Biology and Epidemiology Cost-Benefit Analysis
Silkworms
Eri Silkworm An assessment of the total costs of an activity in
Sericulture comparison to its total benefits. Although envi-
Shellac ronmental and societal aspects may be considered,
Lacquers and Dyes from Insects all costs and benefits are usually expressed in mon-
Entomophagy: Human Consumption of etary terms.
Insects
Maggot Therapy Cotton or Melon Aphid, Aphis
Midges as Human Food gossypii Glover (Hemiptera:
Native American Culture and Insects Aphididae)
Nutrient Content of Insects
This species is an important pest of crops and has
a wide host range.
Aphids
References Melon Aphid, Aphis gossypii

Cox C (1991) Pesticides and birds: from DDT to todays poi-

sons. J Pestic Ref 11:(4)26 Cotton Leafworm, Spodoptera
DeFoliart GR (1989) The human use of insects as food and
as animal feed. Bull Entomol Soc Am 35:(1)2235
littoralis (Boisduval)
DeFoliart GR (1999) Insects as food: why the western atti-
tude is important. Annu Rev Entomol 44:2150 John L. Capinera
Hill DS (1997) The economic importance of insects. Chap- University of Florida, Gainesville, FL, USA
man and Hall, London, UK
Hodkinson ID, Hughes MK (1982) Insect herbivory. Chap-
man and Hall, London, UK This insect occurs in Africa, Madagascar, Europe
Lind PM, Milnes MR, Lundberg R, Bermudez D, Orberg J, and the Middle East. A very similar but allopatric
Guillette LJ Jr (2004) Abnormal bone composition in insect, Spodoptera litura (Fabricius) (taro caterpil-
female juvenile American alligators from a pesticide-
polluted lake (Lake Apopka, Florida). Environ Health lar or tobacco cutworm), is found in Asia, Austra-
Perspect 112:359362 lia, and the Pacific region. For many years these
Losey JE, Vaughan M (2006) The economic value of ecologi- two species were thought to be the same, and
cal services provided by insects. Bioscience
although they have been considered to be separate
56:311323
Pimentel D, Lach L, Zunia R, Morrison D (2000) Environ- species by most authorities since 1962, confusion
mental and economic costs of nonindigenous species lingers. Other common names applied to S. littora-
in the United States. Bioscience 50:5365 lis include Egyptian cotton leafworm or Egyptian
Rosenstreich DL, Eggleston P, Kattan M, Baker D, Slavin RG,
Gergen P, Mitchell H, McNiff-Mortimer K, Lynn H,
cotton worm, tomato caterpillar, tobacco caterpil-
Ownby D, Malveaux F (1997) The role of cockroach lar, and Mediterranean climbing cutworm, just to
allergy and exposure to cockroach allergen in causing name a few.
1094
C Cotton Leafworm, Spodoptera littoralis (Boisduval)

Life History The appearance of adults are typical of

Spodoptera moths, with the forewings bearing
The number of generations displayed by this brown, yellow and white markings, and the hind
species depends on temperature. In southern wings white with a narrow brown margin. The
Europe, for example, three generations are com- wing span is about 3044 mm. It is nearly identi-
monly observed, whereas in Egypt seven genera- cal to the yellowstriped armyworm, S. ornithogalli
tions are not unusual. Warm, but not excessively (Guene), of North America. Adults are active at
hot, weather favors this species. Development dusk and during the evening. They mate immedi-
ceases when temperature are less than about ately upon emergence and can begin to deposit
10.5C. This species lacks the ability to diapause eggs within two days of mating, though some-
and is intolerant of cold winters, so in Europe, times several days elapse before egg deposition.
for example, it occurs regularly only in the south- The adults are short-lived, rarely surviving seven
ernmost regions. days under warm conditions, though persisting
Eggs are spherical, somewhat flattened, and for three weeks under cool conditions. Sex pher-
measure about 0.41.0 mm in diameter. They are omones are produced and have been identified
deposited in clusters of 100300 eggs, in fairly for use in traps.
regular rows comprising three layers, and covered Many naturally occurring biological control
with whitish scales from the abdomen of the agents have been identified, especially parasitoids
female moth. The eggs are yellowish or green ini- (Braconidae, Encyrtidae, Tachinidae, and Ichneu-
tially, but turn black before hatching. Eggs persist monidae) and general predators. Several disease
for 23 days in the summer, but considerably lon- agents, including a baculovirus, microsporidia, fungi,
ger under cooler condition, up to 25 days. Females and nematodes have been observed.
have been shown to produce 15002000 eggs.
Larvae initially are pale green with black
Damage
heads. The older larvae are more variable, often
appearing gray, brown or almost black and with
dark markings. The latter instars bear triangular Cotton leafworm, like most Spodoptera species, is
spots laterally on each body segment, and dorsal highly polyphagous. It attacks nearly 90 species of
stripes. They attain a length of 4050 mm. Young importance in 40 plant families, including virtually
larvae feed in groups, but after the third instar all vegetables; many flowers; avocado, citrus, and
they disperse and become solitary. Normally there mulberry trees; coffee; grapes; field crops such as
are six instars. Larvae are inactive during the day, alfalfa, clover, cotton, grain amaranth, peanut, rice,
with the older instars seeking shelter in the soil soybean, sugarcane, and tobacco; and many other
but the younger larvae remaining motionless on plants. Larvae feed on the foliage and the fruits or
the foliage. Larval development may require only pods of plants. It is considered to be an extremely
1218 days under hot conditions, but requires up damaging agricultural pest where it occurs.
to 85 days under cool conditions.
Larvae burrow into the soil to a depth of
35 cm in preparation for pupation. Pupae are Management
dark red to reddish brown, and are found in cells
buried in the soil. The pupae are 1520 mm in Insecticides are commonly applied for control of
length, and the last segment bears two hooks. this insect, particularly in cotton. However, it
Pupal development time is only 510 days under can be managed by using Bacillus thuringiensis,
warm conditions, but requires up to 30 days under insect growth regulators and slow-release phero-
cool conditions. mones, thereby preserving natural enemies.
 Cover, Border and Trap Crops for Pest and Disease Management
C 1095

When management procedures are used in an Cottony Cushion Scale, Iceryi

integrated manner, the number of chemical purchasi Maskell (Hemiptera:
insecticide applications can be greatly reduced. Margarodidae)
Insecticide resistance is a frequent problem
when insecticides are used excessively. Not all This is an important citrus pest if predators are
strains of Bacillus thuringiensis are effective. absent.
Taro Caterpillar or Tobacco Cutworm, Citrus Pests and their Management
Spodoptera litura (fabricius) (Lepidoptera: Scale Insects and Mealybugs (Coccoidae)
Noctuidae) Hemiptera
Yellowstriped Armyworm, Spodoptera orni- Area-Wide Pest Management
thogalli (Guene) (Lepidoptera: Noctuidae)
Fall Armyworm, Spodoptera frugiperda (J.E.
Smith) (Lepidoptera: Noctuidae) Cover, Border and Trap Crops for
Beet Armyworm, Spodoptera exigua (Hbner) Pest and Disease Management
(Lepidoptera: Noctuidae)
Vegetable Pests and their Management O. E. Liburd, T. W. Nyoike, C. A. Scott
University of Florida, Gainesville, FL, USA

References Natural pest control provides a safer and more

sustainable approach for managing pest popula-
Baker CRB, Miller GW (1974) Some effects of temperature tions. This type of control relies heavily on com-
and larval food on the development of Spodoptera litto-
ralis. (Boisd.) (Lep., Noctuidae)Bull Entomol Res plex communities, natural enemies and the
63:495511 integration of cultural tactics including the use of
*CABI and EPPO (1997) Spodoptera littoralis and Spodoptera mulches, trap crops, cover crops and other
litura. In: Quarantine pests for Europe, 2nd edn. CABI
mechanisms that modify insect behavior to reduce
International, Wallingford, UK, pp 518525
Kehat M, Gordon D (1975) Mating, longevity, fertility and the effect of insect herbivores on crop plants. This
fecundity of the cotton leaf-worm, Spodoptera littoralis. is also called ecological management. Two
(Boisd.) (Lepidoptera: Noctuidae) Phytoparasitica hypotheses have been proposed to explain the
3:87102
reduction in herbivore damage in complex crop
communities. The natural enemies hypothesis
Cotton Stainers proposes that more diverse food sources (nectar,
pollen, prey host species) allow for the establish-
Members of the family Pyrrhocoridae (order ment of higher densities of predators and para-
Hemiptera). sites, which regulate pest populations in diverse
Bugs habitats. Secondly, the resource concentration
hypothesis predicts that herbivores will not want
to remain in sparsely populated plant stands
Cotton Whitefly, Bemisia tabaci because fewer resources are available.
Gennadius (Hemiptera: Conventional pest control programs rely
Aleyrodidae) heavily on monoculture environments with high
usage of broad-spectrum pesticides. However,
This species is also known as sweetpotato whitefly total reliance on chemical tactics to control pests
and silverleaf whitefly, and is a serious pest world- can lead to resistance of arthropod pests, reduc-
wide. tion in natural enemies, and resurgence of pest
Whiteflies (Hemiptera: Aleyrodidae) populations. In addition, this strategy is harmful
1096
C Cover, Border and Trap Crops for Pest and Disease Management

to the environment and it increases the cost of pro- the fruit and vegetable industry. One common
duction. These effects have led to the search for example of an organic mulch is living mulch. A liv-
other management alternatives, which are sustain- ing mulch is a minor crop that grows within a major
able and cost effective. Such practices include use of crop. Living mulches are low-cost alternatives to
mulches, cover crops, trap crops and border crops. synthetic mulches and are safe for the environment.
Common living mulches include buckwheat,
Fagopyrum esculentum Moench, white clover, Trifo-
lium repens L., and wheat, Triticum aestivum L. Liv-
The Role of Mulches for ing mulches (Fig. 119) reduce the number of insect
Suppression of Pest Populations herbivores that alight onto crop plants. This is
accomplished by modification of insect behavior.
Mulching is the art of using soil barriers to improve For instance, alate aphids locate their hosts by con-
plant growth. This helps to reduce arthropod pest trasting the soil background with the green color of
populations, disease symptoms and regulate soil the foliage. The establishment of living mulches will
temperatures. Generally, there are two types of alter the appearance of the soil surface, subsequently
mulches, which can be used to suppress pests: reducing the image that is recognized by aphids. In
organic and synthetic (Figs.118 and 119). addition, living mulches provide supplemental
resources that support higher numbers of natural
enemies (Fig.118) contributing to pests regulation.
Living mulches have also been shown to reduce the
Organic mulches number of whiteflies, delay the onset of insect-
borne viruses and increase yields in vegetable plants.
These types of mulches are composed of lawn clip- It is, however, important to select the appropriate
pings, leaves, straw, sawdust, bark nuggets, wood living mulch suited for the crop to be planted and
chips, brown paper and living mulches. They are the pest to be controlled. In some instances compe-
used extensively in the production of ornamental tition between the crop and the living mulch can
landscape plants but high usage also occurs within result in reduced yields.

Cover, Border and Trap Crops for Pest and Disease Management, Figure 118 Occurrence of natural
enemies in plots containing the living mulch buckwheat, Fagopyrum esculentum, compared with plots
treated with synthetic mulch; note greater abundance in the presence of living mulch.
 Cover, Border and Trap Crops for Pest and Disease Management
C 1097

Cover, Border and Trap Crops for Pest and Disease Management, Figure 119 Types of mulch: (above)
living mulch: buckwheat intercropped with zucchini squash; (center) zucchini squash growing on
reflective plastic mulch; (below) Sunn hemp cover crop in an organic field in Citra, Florida.
1098
C Cover, Border and Trap Crops for Pest and Disease Management

Synthetic Mulches abundance by providing supplemental resources

(food, water, and overwintering sites).
Various colors of synthetic mulches including In temperate climates, cover crops are usually
clear, white, black, yellow and silver-colored plas- winter annuals that are planted in late summer to
tic (Fig. 119) are used commercially to grow give soil cover during the winter. Barley, Hordeum
vegetable crops. In semi-tropical regions, con- vulgare, and rye, Secale ceceale, are excellent exam-
ventional growers use white in the summer, white ples of winter grass-like cover crops whereas hairy
on black (white top surface with black bottom) in vetch, Vicia villosa, is a very common winter
the fall, and black in the winter and early spring. legume cover crop.
Black mulches increase soil temperatures during Summer grass-like cover crops include sor-
the cool season and white mulches reduce soil ghum, Sorghum bicolor, and sudan grass, Sor-
temperatures during the warm season. Ultravio- ghum sudanense, whereas leguminous summer
let light (UV)-reflective mulches, used by some cover crops include cowpeas, Vigna unguiculata,
growers, have the added benefit of reducing pests sunn hemp, Crotalaria juncea, and velvet bean,
and the occurrence of viral diseases. They can Mucana deeringana. In the United States, sum-
reduce abundance of whitefly and aphid vectors mer cover crops are planted in June, July and
that transmit viruses such as tomato spotted wilt August and are termed warm-season crops. In
virus and mosaic virus among various vegetable well-managed orchards, the combination of
crops. UV-reflective mulches work by reflecting leguminous and graminaceous cover crops can
short-wave light, which repels incoming insect provide improved cover crop benefits as opposed
herbivores, thus reducing their potential for to using only one pure stand cover crop.
alighting on crop plants. However, these mulches Cover crops are an important part of sustain-
lose their effect on insects once the reflecting able organic agriculture and provide good poten-
surfaces are covered by the crop canopy. UV- tial for managing economically important pests.
reflective mulches have an added advantage of Crops that produce high glucosinolate levels have
increasing plant vigor and growth, which eventu- been effective in reducing nematode populations
ally results in increased yields. However, they do when they are incorporated into the soil and
not decompose easily in the environment, which allowed to decompose. For instance, residues of
may limit their use in some farming systems. nematode-resistant radish proved to be effective
in suppressing the sugarbeet nematode, Heterodera
schachtii. A significant decline in the nematode
The Role of Cover Crops in population as well as the rate of nematode infec-
Suppressing Pest Populations tion has been observed in sugarbeet crops when
fodder radish, Raphanus sativus L., and white mus-
Cover crops can be annual, biennial or perennial tard, Sinapsis alba L., were used as cover crops.
herbaceous plants grown singly or within mixed
stands throughout the year to cover the bare soil.
Cover crops become green manures when they are The Role of Barrier or Border Crops
plowed back into the soil specifically to improve in Suppressing Pest Populations
soil nutrient quality. In addition to suppressing
weeds and nematode populations, cover crops can Barrier or border crops have been used as a cul-
influence insect population dynamics by diverting tural strategy for reducing pest populations for
generalist pests, confusing specialist pests, reduc- more than half a century. It involves establishing
ing the success of the pest by changing the quality another minor crop on the perimeter of the main
of the host plant, and by increasing natural enemy crop for pests and disease suppression. Several
 Cover, Border and Trap Crops for Pest and Disease Management
C 1099

theories have been suggested to describe the the invading moths are attracted to the blos-
mechanisms by which barrier crops reduce pest soms of the older plants. Squash can also be
populations. Barrier crops reduce pest and related planted in conjunction with tomato to protect
problems (incidence of pepper veinal mottle virus against silverleaf whitefly, Bemisia argentifolii,
disease) by acting as a physical barrier for vectors. because squash is more preferred. In both cases,
However, factors including plant height can affect however, the squash must be sprayed with insec-
the effectiveness of the barrier crop. Barrier crops ticide or destroyed before the insects disperse to
also may act as a sink for virus invading new the main crop.
environments. For instance, aphids landing on the
barrier crop will lose their virus charge while
probing, consequently preventing them from Economics of Sustainable
transmitting diseases. Agriculture

Ecological management of arthropod and nema-

The Role of Trap Crops in tode pests is a practical sustainable approach to
Suppressing Pest Populations achieving effective pest control while protecting
the environment. The primary economic focus of
Trap crops are plants grown before or with the sustainable agriculture is the input cost savings
main crop to attract pests from the main crop from reduced pesticide usage and fertilizer appli-
into a smaller area (the trap crop). Trap crops are cations. In some instances, it can be less expensive
the more-preferred host when grown with the since many of the tactics employed (mulching,
main crop. The ecological behavior of the target cover crops, trap crops, etc.) are not imported and
pests should be considered when selecting the are tied directly into daily farming activities. Also,
trap crop. In addition, the agronomic compatibil- incorporating leguminous cover crops into differ-
ity between the main crop and trap crop should ent cropping systems may decrease the amount of
be known to prevent competition for natural N applications, and the energy needed for crop
resources (nutrients and water). Trap crops can production. However, this may not necessarily
increase the efficiency of control by concentrat- result in increased profits for farmers because of
ing the pests in one location and by applying a two important factors affecting the profitability of
chemical treatment without spraying the main cover crops: (i) the ability to improve crop yield,
crop, or by destroying the trap crop and associ- and (ii) the establishment cost of the cover crop.
ated pests through tillage or burning. It is also Overall, more research is needed to determine the
possible to release biological control agents into long-term profitability of these sustainable
the trap crop, using it as a nursery for beneficial practices.
organisms that will then spread into the main
crop. The overall cost of management can be sig-
nificantly reduced because pesticide treatments References
or other management tactics are only applied to
areas on the trap crop, where the pest congre- Alegbejo MD, Uvah I (1986) Effect of intercropping pepper
with tall crops on the incidence of pepper veinal mottle
gates. Monitoring the pest population density on virus disease on pepper. Niger J Entomol 7:8287
the trap crop is necessary in order to prevent the Cradock RK, da Graca JV, Laing MD (2002) Studies on the
pest from migrating to the main crop. control of virus diseases in zucchini crops. S Afr J Sci
98:225227
Planting a few rows of squash ahead of the
Csizinszky AA, Schuster DJ, Kring JB (1995) Color mulches
main planting can be used to protect from pick- influence yield and insect populations in tomatoes.
leworm, Diaphania nitidalis, infestation because JAm Soc Hortic Sci 120:778784
1100
C Cover Crops

Frank DL, Liburd OE (2005) Effects of living and synthetic winter season to improve soil condition), to sup-
mulch on the population dynamics of whiteflies and press weeds, or to harbor beneficial insects.
aphids, their associated natural enemies, and insect-
transmitted plant diseases in zucchini. Environ Entomol Cover, Border and Trap Crops for Pest and Dis-
34:857865 ease Management
Hilje L, Costa HS, Stansly PA (2001) Cultural practices for
managing Bemisia tabaci and associated viral diseases.
Crop Prot 20:801812
Liburd OE, Frank DL (2007) Synthetic and living mulches for Coxa
control of homopteran pests and diseases in vegetables.
In: Saxena G, Mukerji KG (eds) Management of nema- The basal-most segment of the insect leg (Fig.120),
tode and insect-borne plant diseases. The Haworth Press
Inc., New York, NY pp 6786 attaching to the thorax.
Lu Y, Watkins B, Teasdale JR, Abdul-Baki AA (2000) Cover Legs of Hexapods
crops in sustainable food production. Food Rev Int
16:121157
Smith HA, Koenig RL, McAuslane HJ, McSorley R (2000)
Effect of silver reflective mulch and a summer squash
trap crop on densities of immature Bemisia argentifolii
Crab Lice, Phthirus pubis
(Homoptera: Aleyrodidae) on organic bean. J Econ (Linnaeus) (Phthiraptera:
Entomol 93:726731 Pthiridae)
Zitters AT, Simons JN (1980) Management of viruses by alter-
ation of vector efficiency and by cultural practices. Annu
Rev Phytopathol 18:289310
These lice infest the genital regions of humans.
Human Lice

Cover Crops
Crabronidae
Cultivation of a second type of crop, principally
to improve the production system for a primary A family of wasps (order Hymenoptera).
crop (e.g., legumes or rye maintained during the Wasps, Ants, Bees and Sawflies

Coxa, Figure 120 Leg of a beetle (Coleoptera: Scarabaeidae) leg showing its component parts, and a
close-up of one type of beetle tarsus (foot).
 Crane Flies (Diptera: Tipulidae and Others)
C 1101

Cranberry Fruitworm, Acrobasis transverse suture between mesonotal prescutum

vaccinii Riley (Lepidoptera: and scutum, or roughly at the level of the wing
Pyralidae) bases. Three other, relatively small families share
this characteristic. The Tanyderidae, or primitive
This is a pest of blueberries in eastern North crane flies, have five branches of the radial vein
America. reaching the wing margin. Tipulidae have four or
Small Fruit Pests and their Management fewer. Trichoceridae, or winter crane flies, possess
ocelli, while tipulids have none. Ptychopteridae,
or phantom crane flies, have a single anal vein in
Cranberry Girdler, Chrysoteuchia each wing, compared to two in Tipulidae.
topiaria (Zeller) (Lepidoptera: Most adult crane flies are slender-bodied, with
Pyralidae) elongate, membranous wings and conspicuously
long, slender legs (Fig.121). People not familiar with
This species affects both cranberries and insects often mistake crane flies for large mosqui-
turfgrass. toes. In fact, the colloquial term gallinipper has
Small Fruit Pests and their Management been applied to both crane flies and mosquitoes.
However, no crane flies are able to bite. Insize, crane
flies range from two species of Holorusia (originally
Cranberry Tipworm, Dasineura Ctenacroscelis) of southeastern Asia, with a wing
oxycoccana (Johnson) (Diptera: span of over 100 mm, or Holorusia hespera in west-
Cecidomyiidae) ern United States, with approximately a 70 mm wing
span, to the tiny Tasiocera ursina, with wingspread
Cranberry tipworm affects both cranberries and of only 4.55.0 mm, smaller than that of mosqui-
blueberries. toes. Wings of many crane flies are unmarked except
Small Fruit Pests and their Management for the somewhat darkened stigma, while many
other species have the wings spotted, transversely

Crane Flies (Diptera: Tipulidae

and Others)
George W. Byers
University of Kansas, Lawrence, KS, USA

Largest of the families of true flies (Order Diptera)

in number of known species, the crane flies (Fam-
ily Tipulidae, of suborder Nematocera) are abun-
dantly represented on all continents except
Antarctica. Some 15,000 species have been named
and described, more than 10,000 of these through
the work of one man, Prof. Charles P. Alexander, of
the University of Massachusetts. Over 1,600 spe- Crane Flies (Diptera: Tipulidae and Others),
cies are known from North America. Figure121 Adult male of Tipula sp., dorsal aspect.
Crane flies can be differentiated from most Body length 18 mm, wing length 21 mm. Legs are
other nematocerous flies by the presence on the arranged unnaturally to show relative lengths of
dorsum of the thorax of a broadly V-shaped, segments.
1102
C Crane Flies (Diptera: Tipulidae and Others)

banded, or with a mottled or clouded pattern of

brown, gray or black. The slender legs of some spe-
cies are banded with dark brown, while those of oth-
ers may be partially white (for example,Brachypremna Crane Flies (Diptera: Tipulidae and Others),
or some Hexatoma). While most kinds of flies, Figure122 Larva of Tipula sp., left lateral aspect.
indeed most insects, have the trochanter firmly Body length 29 mm.
attached to the adjacent femur, the legs of crane flies
are readily broken off between trochanter and femur, head, variously sclerotized according to the species,
possibly so that a leg seized by a predator can quickly can be withdrawn into the thoracic segments. The
be shed, to spare the fly. larvae occur in a great variety of moist to wholly
The adult life of most crane flies is brief. The aquatic, even marine intertidal microhabitats.
adults emerge from the pupal skin, often at night in Those of aquatic species may be found in decom-
order to have the body hardened, the wings fully posing plant material near the shore or in shallow
extended and the insect capable of flight by sunrise water near sandbars. Larvae in aquatic situations
when birds and other predators become active. may respire by means of a pair of large spiracles on
Males usually appear a night or two before females. the ninth abdominal segment that are raised to the
Males of many species form swarms to which surface from time to time. Others have such spira-
females are attracted. Following mating, females dis- cles but appear to obtain sufficient oxygen through
perse and oviposit. Oviposition is often completed the skin. A few (e.g., larvae of Antocha and Hes-
in two or three nights. Thus, an adult life of a few peroconopa) have a closed tracheal system and lack
days is ordinarily adequate. Adults of Chionea, ren- spiracles. Most aquatic tipulid larvae leave the
dered inactive by night time chill, and forced to seek water to pupate. While some aquatic and semi-
shelter from severe cold, may survive a few weeks. aquatic larvae are detritivores, many others are car-
The adults of most crane flies do not feed but nivorous. The larvae of Pedicia, Limnophila and
subsist on energy acquired and stored by the larva. Hexatoma, for example, feed on midge larvae, other
Those of a few, such as species of subgenus Ger- insect larvae and other small, aquatic invertebrates.
anomyia of the large genus Limonia, possess elon- Terrestrial crane fly larvae may occur in and feed
gate mouthparts or a proboscis and are known to upon rotting wood, fungi, or decomposing plant
obtain nectar from certain flowers. debris, in mosses and liverworts, among rootlets of
grasses and other plants, and a few (e.g., Cylindro-
toma) feed on leaves of herbaceous plants. The only
Ecology larval Tipulidae that are of direct economic impor-
tance are those that eat rootlets of range-land
Adult Tipulidae are most often found in low, leafy grasses or seedling crops (particularly some spe-
vegetation in shaded, somewhat damp areas, such as cies of Tipula and Nephrotoma).
along small woodland streams. However, there are
a few species living in grasslands or even in semi-
desert habitats. At temperate latitudes, they are usu- Geological Record
ally the most common in spring and late summer
and may have two annual generations. Adults of The oldest fossil remains described as Tipulidae
Chionea, virtually wingless and almost spider-like in are of upper Triassic age, perhaps 180 million years
appearance, may be found on the surface of snow, in old. In North America, the earliest remains, simi-
winter, in Eurasia and North America. lar to modern Tipulidae, are in the fine-grained
The larvae of crane flies are subcylindrical and shale of the Green River formation, of the Eocene
somewhat tapered toward the ends (Fig.122). The age, approximately 50 million years old. The Baltic
 Crapemyrtle Aphid Sarucallis Kahawaluokalani (Kirkaldy) (Hemiptera: Aphididae)
C 1103

amber of northern Europe, which is upper Eocene feeding exclusively on species of Lagerstroemia.
to Oligocene in age (about 45 million years old), Interestingly, other aphid species are not known to
contains numerous species of crane flies, preserved attack or infest crape myrtles. Crape myrtles are
in fine detail. popular ornamental plants throughout tropical
and subtropical areas of the world. Because aphids
can be extremely difficult to detect on plants dur-
Taxonomic Divisions ing shipping, S. kahawaluokalani has been trans-
ported throughout the world on shipments of crape
The family Tipulidae has been divided into three myrtle. When aphid numbers are high, S. kaha-
subfamilies, Tipulinae, Cylindrotominae and Limo- waluokalani damages crops via a fungus that grows
niinae. Most large crane flies belong to the Tipuli- on its excrement. Several insect predators attack
nae, but there are a few large Limoniinae. For crapemyrtle aphids, but most are unable to provide
identification keys (North America), see Alexander permanent control of aphid populations.
1942 (somewhat revised and reprinted in 1966) or Crapemyrtle aphids (Fig.123) reproduce at an
Alexander 1967. In fairly recent years, European astonishing rate, giving the impression that an infes-
authors have elevated these three subfamilies and tation suddenly occurred overnight. Each adult S.
tribe Pediciini of Limoniinae to full family status. kahawaluokalani gives birth parthenogenetically to
several offspring per day, and the growth of crape-
myrtle aphid populations is further accelerated by
References the process of telescoping generations. Partheno-
genesis is a form of asexual reproduction where off-
*Alexander CP (1942) Family Tipulidae. In: The Diptera or spring are produced without mating. Furthermore,
true flies of Connecticut. Connecticut State Geological crapemyrtle aphids are viviparous, meaning they
and Natural History Survey, Bulletin 64, pp 196509
Alexander CP (1967) The crane flies of California. Bull Calif
give live birth to their offspring. Telescoping gener-
Insect Survey 8:1269 ations refers to the process in which nymphs or
immature aphids begin to develop offspring inside
of them before they become adults. In many aphid
Cranium species, a nymph that is developing inside of its
mother has already begun to develop offspring
The head capsule of an insect.
Head of Hexapods

Crapemyrtle Aphid, Sarucallis

kahawaluokalani (Kirkaldy)
(Hemiptera: Aphididae)

John J. Herbert, Russell F. MizellIII

University of Florida, Quincy, FL, USA

The crapemyrtle aphid, Sarucallis kahawaluokalani

(Kirkaldy), is native to Southeast Asia but may be Crapemyrtle Aphid Sarucallis Kahawaluokalani
found anywhere that crape myrtles, Lagerstroemia (Kirkaldy) (Hemiptera: Aphididae), Figure 123
spp,. are grown. With the exception of henna and Winged adults and nymph of crape myrtle aphids,
pomegranate, S. kahawaluokalani is host specific, Sarucallis kahawaluokalani.
1104
C Crapemyrtle Aphid Sarucallis Kahawaluokalani (Kirkaldy) (Hemiptera: Aphididae)

inside of itself. Telescoping generations allows Successful reproduction and development are
aphids to reproduce immediately upon becoming dependent on the assimilation of nutrients. Crape-
an adult, and S. kahawaluokalani give birth within a myrtle aphids acquire their nutrition by feeding on
few hours of reaching the adult stage. Crapemyrtle the phloem sap of their host plant. Phloem is rich
aphids exhibit a life cycle that is more complex than in sucrose and other sugars, but contains low con-
simple parthenogenesis, and under some environ- centrations of amino acids. In addition to having
mental conditions, crapemyrtle aphids practice small amounts of amino acids, phloem does not
sexual reproduction. contain all of the amino acids required for success-
The life cycle of S. kahawaluokalani begins ful growth, development, and reproduction. Crape-
when overwintering eggs hatch in the spring. Aphids myrtle aphids have evolved several mechanisms to
hatching from overwintering eggs are all female, and circumvent the disadvantages of feeding on
such mature wingless stem mother aphids that hatch phloem. To obtain the necessary quantity of nutri-
from overwintering eggs are called fundatrices (sin- ents, aphids feed on large volumes of phloem and
glular, fundatrix). Fundatrices reproduce through use a special filter chamber in the gut to remove
parthenogenesis, giving rise to a second generation necessary nutrients. Furthermore, aphids harbor
known as virginoparae. Virginoparae reproduce endosymbionts within the gut that manufacture
through parthenogenesis and subsequent genera- amino acids that are required by the aphid but not
tions of aphids throughout the summer are also present in the phloem. The most common endo-
called virginoparae. In late summer and early fall, symbiont of aphids are members of the genus
virginoparae produce a special generation of aphids Buchnera. Phloem contains large quantities of
known as sexuparae. Sexuparae give birth to both sucrose, which causes it to be a hypertonic solu-
male and female aphids. The female aphids of this tion. Thus, even though aphids feed on a liquid diet,
generation are known as oviparae, and after mating they are confronted with the problem of becoming
with males, oviparae deposit their eggs on the dehydrated from their source of food. Aphids can
branches of crape myrtle. Eggs are deposited in loose overcome this is by changing simple sugars into
clusters within the crevices of bark and remain on more complex sugars, which in turn lowers the
the plant until the following spring when the eggs osmotic pressure by creating fewer sugar molecules
hatch and the cycle restarts. per molecule of water. Feeding on large quantities
Nymphs of S. kahawaluokalani are yellow in of phloem, followed by filtering and changing of
color with black hair-like projections protruding sugar composition, creates a large amount of
from their abdomen. Adult S. kahawaluokalani are unused sugar and water. Crapemyrtle aphids
yellow, mottled with black spots, and have two large excrete unused or transformed sugars, along with
black tubercles that project from their dorsum. Many water, from the anus in a droplet known as honey-
aphids produce winged adults for dispersal, but usu- dew. To avoid becoming coated and entangled in
ally do so in response to overcrowding of the host sticky honeydew, crapemyrtle aphids forcefully
plant or a sudden drop in host plant quality. Sarucal- eject honeydew away from their feeding site. Hon-
lis kahawaluokalani is unusual among aphids in that eydew can be easily spotted in the field as a shiny
all adults, except for oviparae, are winged and capa- sticky substance on the leaves of crape myrtles.
ble of dispersing. Fecundity and development of S. Honeydew is rich in sugars and promotes
kahawaluokalani are dependent on ambient tem- the growth of fungi and other microorganisms.
perature, and under optimal conditions, S. kaha- The honeydew of S. kahawaluokalani promotes
waluokalani adults can produce over six offspring the growth of an undescribed black sooty mold in the
per day, and nymphs can mature in as little as five genus Capnodium. Capnodium sp. can turn the
days. Adults can live up to 21 days, producing more entire plant an unsightly black color, detracting
than 150 offspring within their lifetime. from the visual aesthetics. Furthermore, thick
 Crawler
C 1105

carpets of Capnodium sp. interfere with photosyn- Craw, Alexander

thesis, causing the abscission of leaves and in some
cases complete defoliation of the plant. Established Alexander Craw was born on Ayr, Scotland, on
plantings of crape myrtle do not show signs of August 3, 1850. He emigrated to California, USA,
long term damage and bloom beautifully the fol- when he was 23, and by 1875 was placed in charge of
lowing year. Damage to crape myrtles is influenced a very large orange grove near Los Angeles. He helped
by crape myrtle cultivar and interactions with D.W. Coquillett in investigations of chemical control
aphid natural enemies. of the new pest cottony cushion scale. He was the
Crapemyrtle aphids are attacked by a variety first to suggest use of natural enemies for control of
of insect predators, but are not known to harbor this pest when chemicals failed. In 1890, he was
any parasitoids. Lacewings (Chrysopidae), flower appointed quarantine inspector at the port of San
flies (Syrphidae), lady beetles (Coccinellidae), Francisco by the California Board of Agriculture,
and other generalist predators feed on crapemyrtle and it was he who developed and put into practice
aphids, especially when other prey are scarce. the principles of horticultural quarantine. In 1904 he
Predatory and parasitic hymenoptera of other accepted a position as Superintendent and Inspector
insect pests feed on honeydew, allowing them to of the Hawaiian Board of Agriculture and Forestry in
search for prey over greater distances. Because Honolulu, where he remained until his death in 1908.
crapemyrtle aphids do not cause permanent Most of his publications were about control of pests
damage to crape myrtles, and provide food for and about exclusion of new pests by quarantine, but
insect natural enemies, the use of chemical pesti- he did describe a few new species of insects.
cides is strongly discouraged. If aphids reach high
populations and control is necessary, the use of
soapy water or power washing is usually suffi- Reference
cient for removing aphids from a particular plant.
These methods are less harmful to insect natural *Essig EO (1931) Craw, Alexander. In: A history of entomol-
enemies and help contribute to biological and ogy. The Macmillan Company, New York, NY, pp
593595
natural control of crapemyrtle aphid and other
insect pests.

Crawler
References
Whitney Cranshaw
Alverson DR, Allen RK (1991) Life history of the crapemyrtle Colorado State University, Ft. Collins, CO, USA
aphid. Proc SNA Res Conf 36:164167
Alverson DR, Allen RK (1992) Bionomics of the crapemyrtle Crawler is the active stage of an insect immediately
aphid (Homoptera: Aphididae). J Entomol Sci
27:445457
after egg hatch (first instar) found among certain
Dixon AFG (1998) Aphid ecology. Chapman and Hall, insects in the order Hemiptera. The term crawler is
London, UK, 300 pp most commonly used to describe first instar scale
Mizell RFI, Schiffhauer DE (1987) Seasonal abundance of the insects, but may also describe similar stages found
crapemyrtle aphid, Sarucallis kahawaluokalani, in rela-
tion to the pecan aphids, Monellia caryella and Monelli- among mealybugs and whiteflies. The crawler stage
opsis pecanis and their common predators. Entomophaga is noted for mobility allowing distribution within
32:511520 and among host plants. Many species that have a
Mizell RF, Knox GW (1993) Susceptibility of crapemyrtle,
crawler period (e.g., Diaspididae and Aleyrodidae)
Lagerstroemia indica L., to the crapemyrtle aphid
(Homoptera: Aphididae) in North Florida. J Entomol subsequently produce (Fig. 124) immature stages
Sci 28:17 that move little, if at all, following the crawler period.
1106
C Crawling Water Beetles

Crawler, Figure 124 Cottony cushion scale adults and crawlers. The adults (large with a white, fluted,
waxy secretion on the stem) are easily observed, whereas the small crawlers (small i nsects along the
mid-vein on the leaf) are harder to detect. (Photo by Lyle Buss, University of Florida.)

In management of insects, the crawler stage is often close association of humans with livestock, par-
one that is targeted for control because crawlers are ticularly horses and mules.
small and have a relatively thin wax coating that
makes them easier to kill with pesticides.
Creeping Water Bugs
Crawling Water Beetles Members of the family Naucoridae (order
Hemiptera).
Members of the family Haliplidae (order Bugs
Coleoptera).
Beetles
Cremaster

Creeping Myiasis In Lepidoptera, a process at the tip of the abdomen,

usually bearing spines or hooks, by which pupae are
Infestation of humans by bot fly larvae that ulti- suspended from silk attached to a substrate surface.
mately cannot complete their development and
perish in the abnormal human host. The larvae
typically die in the first instar after burrowing Crenulate
beneath the skin, causing little serious injury but
causing itching and creeping eruptions. Species of A tem used to indicate a wavy or scalloped
Gasterophilus are usually implicated, and follow appearance.
 Cresson, Ezra Townsend
C 1107

Crenulate Moths (Lepidoptera: Host plants in several plant families, including

Epiplemidae) Bignoniaceae, Caprifoliaceae, Olacaceae, Oleaceae,
Rosaceae, Rubiaceae, and others.
John B. Heppner
Florida State Collection of Arthropods,
Gainesville, FL, USA References

Crenulate moths, family Epiplemidae, total about *Boudinot J (1982) Insectes Lpidoptres Epiplemidae. In:
632 species worldwide, with most being Neotropi- Faune de Madagascar. 60:155. Paris: Off. Rech. Sci.
Tech. Outre-Mer, France
cal (230 sp.) and Indo-Australian (301 sp.). The * von Dalla Torre KW (1924) Epiplemidae. In: Lepidoptero-
common name for the family refers to the often rum catalogus. 30:157. W. Junk, Berlin.
scalloped, or crenulate, margins of the wings. Two *Holloway JD (1998) Subfamily Epipleminae. In: The moths
subfamilies are known: Auzeinae, with about 25 sp. of Borneo, 8:7882, 92132, pl.1, 68. Malayan Nature
Society, Kuala Lumpur (Malayan Nature Journal, 52).
(mostly Indo-Australian), and Epipleminae for all Seitz A (ed) (191233) Familie: Epiplemidae. Die Gross-
others. The family is in the superfamily Uranioidea, Schmetterlinge der Erde, 2:277280, pl. 48 (1912);
in the section Cossina, subsection Bombycina, of 2(suppl.):171172 (1933); 6:11411170, pl. 169172
(1930); 10:577600 (1929), 601604, pl. 5859 (1930);
the division Ditrysia. Adults small to medium size
14:390394, pl. 67 (1928). A. Kernen, Stuttgart
(947 mm wingspan), with head scaling normal; *Stehr FW (1987) Epiplemidae (Geometroidea). In: Imma-
labial palpi upcurved; haustellum naked; maxillary ture insects [1], 507. Kendall/Hunt, Dubuque
palpi minute, 1-segmented. Wings (Fig.125) trian-
gular, typically with distinct marginal emargin-
ations and marginal points, and forewing tip often Crepuscular
somewhat falcate; hindwing generally rounded to
triangular and also usually with emarginations and Organisms in which the period of activity is twi-
marginal points or tail-like projections. Macula- light, either pre-dawn or dusk.
tion mostly shades of brown with few markings
and hindwings usually matching the forewing col-
oration; rarely more colorful; some are leaf-like. Cresson, Ezra Townsend
Adults nocturnal. Larvae leaf feeders or webbers.
Ezra Cresson was born on June 18, 1838, in Penn-
sylvania, USA. He attended public schools in
Philadelphia through the eighth grade, but then
had to drop out to help support the family. Little
of his paid employment was in entomology, and
one of his positions was as clerk in the treasurer s
office of the Pennsylvania Railroad Company,
another was as secretary to a wealthy patron of
the Philadelphia Academy of Sciences, and a third
was with a fire insurance company. His interest in
insects was kindled by his future father-in-law,
James Ridings. He, Ridings, and George Newman,
Crenulate Moths (Lepidoptera: Epiplemidae), in 1859, were the founding members of an ento-
Figure 125 Example of crenulate moths mological society which, in 1867, changed its
(Epiplemidae), Epiplema castanea Warren from name to the American Entomological Society, and
Taiwan. is now the oldest existing entomological society
1108
C Cretaceous Period

in the United States. The society, under its original Crickets

name, began in 1863 to publish Proceedings of
the Entomological Society of Philadelphia. Cres- Certain members (suborder Ensifera, superfamily
son was one of the society members who set the Grylloidae) of an order or insects (Orthoptera).
type for the printing: this was truly an in-house Grasshoppers, Katydids and Crickets
publication. In that first issue of the Proceedings
appeared Cresson s Catalogue of the Cicindeli-
Criddle, Norman
dae of North America, after which he confined
his own publications to works on Hymenoptera.
Norman Criddle was born in Addlestone, Surrey,
Between 1861 and 1882 he published 66 papers
England, on May 14, 1875 and moved to Canada
on Hymenoptera including catalogs and descrip-
in 1882 with his parents. The Criddle family estab-
tions. In 1901 his collection, including 2,367 type
lished a homestead in Aweme, Manitoba. From
specimens representing 3,511 species, was pre-
his early childhood, Criddle had a strong interest
sented to the American Entomological Society.
in flora and fauna. This was expressed, in part, by
He died on April 19, 1926. Two of his five children
drawing and painting, which he developed to
displayed a strong interest in entomology. These
great proficiency. His artistic skills were discov-
were Ezra T. Cresson, Jr., who specialized in Dip-
ered only after he developed a poison bait, a mix-
tera, and George Binghurst Cresson, who special-
ture that came into wide use for grasshopper
ized in ants.
control during periodic outbreaks on the Cana-
dian prairie. The bait brought the attention of
Dominion Entomologist James Fletcher, who
Reference came to admire Criddles artistic and entomologi-
cal abilities. They coauthored a publication on
*Mallis A (1971) Ezra Townsend Cresson. In: American
entomologists.Rutgers University Press, New Bruns-
weeds in Canada in 1905. This pioneer entomolo-
wick, NJ, pp 343348 gist received a government appointment in 1913,
and investigated the cause of grasshopper plagues,
attributing them to cycles of weather correlated
Cretaceous Period with changes in the numbers of sunspots. Over
the years, he also came to mentor several of Mani-
A geological period at the end of the Mesozoic era, tobas foremost entomologists. His entomological
extending from about 170 to 65 million years ago. interests extended well beyond grasshoppers, of
Geological Periods course, and he was a major proponent of under-
standing the biology of insects as a basis for their
control. Norman Criddle received an honorary
Cribellum degree in Agriculture from the Manitoba Agricul-
tural College shortly before his death on May 4,
In spiders, a sieve-like structure found just in front 1933 in Brandon, Manitoba.
of the spinnerets.

Crimean-Congo Hemorrhagic
Cribrate Fever
This describes a structure or surface that is pierced This virus affects humans, and is transmitted by
by narrowly spaced small holes, resembling a sieve several species of ticks.
or strainer, or that functions as a sieve. Ticks
 Crop Diversity and Pest Management
C 1109

Cristate Crop diversity can take many forms. Traditional

farming systems in the tropics are often character-
A term used to indicate the presence of a high ized by intercropping, in which different crops are
ridge or crest. arranged in alternating rows, or mixed together
without regard to row. Mixed cropping systems in
both temperate and tropical regions can resemble a
Critical Period mosaic-like patchwork of distinct crops. Trees,
hedgerows, cover crops and even weeds can increase
The notion that the brain is needed for a period the plant diversity on a farm. Modern examples of
of time (the critical period) if the insect is to crop diversity include the intentional mixing of
develop properly. The brain synthesizes PTTH resistant and non-resistant wheat hybrids for Hes-
that activates the prothoracic gland to secrete sian fly management in the midwest of the USA.
ecdysone. Removal of the brain after PTTH pro- Several hypotheses have been put forward to
duced (after the critical period) does not disrupt explain why pest damage is sometimes less in
development. polycultures, as mixed cropping systems are called.
The enemies hypothesis, defined by Root, sug-
gests that polycultures offer greater resources than
Crochets monocultures to parasitoids and predators in the
form of nectar and pollen, alternate hosts and prey,
The minute hooks found on the prolegs, mostly of and habitat. Populations of natural enemies are
caterpillars. They usually are arranged in rows or hypothesized therefore to be more stable in mixed
circles. cropping systems than in simple ones, and so bet-
ter able to keep herbivore populations below eco-
nomically damaging levels.
Crop Diversity and Pest A complementary idea put forward by Root is
Management the resource concentration hypothesis. This pro-
poses that resources provided by a crop are more
Hugh Smith easily exploited by herbivores when concentrated
Hawaii Agriculture Research Center, Aiea, in a uniform stand. It may become more difficult for
HI,USA the herbivore to find and exploit the crop when it is
mixed with other crops. This is because the vola-
Contemporary theories concerning the relation- tiles, appearance, and leaf characteristics of non-
ship between crop diversity and arthropod dam- host plants may interfere with the host-finding
age originated from observations made during the mechanisms of certain arthropods. According to
early decades of the twentieth century in temper- the resource concentration hypothesis, once an
ate tree plantations and mixed farming systems in herbivore has found a suitable host within a poly-
the tropics. Seminal studies of insect damage on culture, within-stand effects such as shading,
collards by Pimentel and Root provided a broad increased humidity, and the presence of non-host
ecological framework for examining arthropod crops may influence the arthropod to feed and ovi-
damage under mixed and simple cropping sys- posit less than it would in a monoculture, and to
tems. The classic experiments of Risch and Bach in emigrate from the crop patch sooner than it would
Costa Rica demonstrated that the relationship from a large uniform stand.
between mixed cropping systems and pest damage Trap cropping is another form of polyculture
is ultimately determined by the specifics of arthro- that has been used to reduce pest damage. The pest
pod behavior. is drawn away from the crop being protected by
1110
C Crop Diversity and Pest Management

the presence of a more attractive crop the trap monophagous chrysomelid were reduced in polycul-
crop. Trap crops are often sprayed with pesticides ture because they tended to emigrate more quickly
to keep pest populations from building up and from the mixed stands. Arthropods with sensitive
moving on to the main crop. host-finding mechanisms may be more easily
Neither the enemies hypothesis, resource con- deterred by the presence of non-host plants than
centration hypothesis or trap cropping has been arthropods that do not rely on specific visual or olfac-
shown consistently to predict how an arthropod tory host-finding cues. Highly mobile insects such as
will behave in a mixed cropping system. In the certain grasshoppers or beetles may abandon a patch
1970s, mathematical theories were proposed to in which suitable hosts are hard to find more quickly
suggest that diverse systems should be more stable than weak fliers such as whiteflies or thrips.
than simple ones, and therefore that polycultures Host-finding, mobility, and host range also
should experience less pest damage than monocul- influence how natural enemies will behave in a
tures. The misconception that crop diversity in complex cropping system. Generalist predators and
itself reduces pest damage has persisted in spite of parasitoids are probably better adapted than spe-
the fact that it is inconsistent with empirical obser- cialized natural enemies to search the varied visual
vation. Stability is not a characteristic of most and olfactory landscape presented by a polyculture.
annual cropping systems, which tend to begin and Like monophagous herbivores, natural enemies
end with the complete destruction of all vegetation with a narrow host range may be more efficient
in the field. Whether one or several crops are grown when searching in a uniform environment.
in the field in the interim may have little bearing on By influencing probing behavior, mixed crop-
the long-term stability of the cropping system. ping systems may also affect the transmission rates
Reviews of the literature indicate that in over of insect-vectored diseases. For example, crop
fifty percent of the cases studied, intercropping combinations that encourage vectors of non-
reduced arthropod damage compared to monocul- persistent viruses such as aphids to probe more
ture. Fifteen to eighteen percent of the time, damage frequently and for a shorter duration may increase
was worse in intercropped systems, and in twenty the likelihood of non-persistent virus transmis-
percent of the cases the results were variable. A sig- sion. By contrast, the transmission of persistent
nificant trend revealed by reviews of the intercrop- viruses tends to require longer probing periods,
ping literature is that damage by monophagous and so might be reduced by a cropping environ-
insects tends to be reduced in polyculture, while ment that stimulates vectors such as whiteflies to
damage by polyphagous insects is more likely to be probe for shorter periods.
increased or unaltered in mixed cropping systems. Recent efforts in biological control have empha-
Under traditional mixed cropping conditions in sized the introduction of perennial refugia or nurs-
Costa Rica, densities of a monophagous species of ery crops for natural enemies in and around cropped
leaf beetle are reduced under polyculture, while areas. This is a form of polyculture. Refugia crops
densities of a polyphagous leaf beetle species are are planted to maintain stable populations of natural
not reduced. Studies such as this indicate that the enemies in a cropping system by providing habitat,
damage caused by an arthropod species in polycul- pollen, nectar, and alternate victims, so that preda-
ture will be determined by the quantity and quality tors and parasitoids will be available near the crop to
of host plants in the mix rather than by crop diver- suppress incipient pest populations. Region-wide
sity in the taxonomic sense. approaches to managing major pests such as white-
In addition to host range, the host-finding flies and certain Lepidoptera have included the
mechanisms and the mobility of an arthropod establishment of refugia for natural enemies.
willdetermine how its behavior is influenced by a Standard methods of field research that have
given polyculture. In Costa Rica, populations of a been established for studying and managing pest
 Cross-Resistance
C 1111

populations in large monocultures may require Root R (1973) Organization of a plant-arthropod association
in simple and diverse habitats. The fauna of collards.
modification for use in complex polycultures. Con-
Ecol Monogr 43:95124
ventional field plot research designs require repli-
cation under uniform conditions that are often
difficult to achieve in a heterogeneous environ-
Crop
ment. The reduction of field plot variability required
for standard statistical analysis is also difficult to A portion of the foregut in the alimentary canal of
accomplish in polycultures, which are by definition insects. The crop receives the insects meal, and in
highly variable environments. Elucidation of the insects that feed only infrequently it may be greatly
relationship between polyculture and pest man- expanded to accommodate the occasional meal.
agement may require the adaptation of multiple Although lined with a thick lining that inhibits
regression methods and spatial diversity analysis. digestion, in some insects the digestive enzymes
Similarly, methods for establishing scouting secreted from the mouth or regurgitated from the
protocols and calculating economic injury levels midgut pass into the crop and perform partial
have been designed to address pest behavior in digestion.
homogeneous environments, and may require adap- Alimentary Canal and Digestion
tation for mixed cropping systems. The population
dynamics and feeding behavior of both herbivores
and natural enemies may be different on a crop Crop Loss Assessment
when that crop is grown in polyculture as opposed
to monoculture. The resources that can be allocated This refers to the procedure for assessing arthro-
to scouting and managing the pest complex of a pod impact on crop yield and quality.
crop that represents only one component of a diverse Methods of Measuring Crop Losses
farm may differ from the resources available to man-
age the pest complex of a large monoculture.
Crop Residue
References
A portion of the crop that is not harvested, and
Andow D (1991) Vegetational diversity and arthropod popu- usually is returned to the land by tillage or as
lation response. Annu Rev Entomol 36:56186 mulch.
Bach CE (1980) Effects of plant density and diversity in the
population dynamics of a specialist herbivore, the
striped cucumber beetle, Acalymma vittata. Ecology
61:15151530 Crossing Over
Bach CE (1980) Effects of plant diversity and time of coloni-
zation on an herbivore-plant interaction. Oecologia
The reciprocal exchange of polynucleotides
44:319326
Pimentel D (1961) Species diversity and insect population between homologous chromosomes during
outbreaks. Ann Entomol Soc Am 54:7686 meiosis.
Risch SJ (1980) The population dynamics of several herbivo-
rous beetles in a tropical agroecosystem: the effect of
intercropping corn, beans and squash in Costa Rica.
JAppl Ecol 17:593612 Cross-Resistance
Risch SJ (1981) Insect herbivore abundance in tropical mon-
ocultures and polycultures: an experimental test of two In pest management, the resistance of a pest popu-
hypotheses. Ecology 62:13251340
lation to a pesticide to which it has not been exposed
Risch SJ, Andow D, Altieri MA (1983) Agroecosystem diver-
sity and pest control: data, tentative conclusions, and that accompanies the development of resistance to
new research directions. Environ Entomol 12:625629 a pesticide to which it has been exposed.
1112
C Cross-Striped Cabbageworm, Evergestris rimosalis (Guene) (Lepidoptera: Pyralidae)

Cross-Striped Cabbageworm, 1873! One can only wonder at what he might have
Evergestris rimosalis (Guene) accomplished had he not died so young. The insects
(Lepidoptera: Pyralidae) that he collected in the Azores are in the Natural
History Museum (London), whereas his Coccinelli-
This is an important crucifer pest in the southern dae and Erotylidae are in the Museum of Compara-
USA. tive Zoology, Harvard University.
Crucifer Pests and their Management
Reference
Cross Vein *Essig EO (1931) Crotch, George Robert. In: History of ento-
mology. The Macmillan Company, New York, pp
Short crosswise veins between the lengthwise wing 598600
veins and their branches. Most insects have only a
few cross veins, but the netwinged species have
numerous cross veins. Crowson, Roy Albert
Wings of Insects
Roy Crowson was born in the county of Kent,
England, on November 22, 1914. He graduated
Crotch, George Robert from University College, London, in 1936, and
then began anatomical research on Coleoptera. He
George Crotch was born in Cambridge in 1842 and worked as assistant curator of the Tunbridge Wells
obtained his undergraduate education at Cambridge Museum until World War II, when he served in
University. While still a student he was deeply the Royal Air Force. In 1948, he joined the Depart-
involved in collecting insects. By the time he received ment of Zoology of Glasgow University. Numer-
an M.A. degree (1863) he had concentrated on ous publications on structure of beetle adults and
Coleoptera, and he published a Catalogue of British larvae followed, with more on classification, until
Coleoptera. The next year he collected insects in the his death. Major works were a series called The
Canary Islands and, on return to England, obtained natural classification of the families of Coleoptera
a job in the university library at Cambridge. In 1865 which (1955) were republished as a book, a (1971)
and 1870 he made collecting trips to Spain, and book Classification and biology, and a (1981)
meanwhile had published several entomological book The biology of the Coleoptera. He died on
papers including works on Coccinellidae and Eroty- May 13, 1999, survived by his wife, Betty.
lidae and had become sub-editor of Zoological
Record. In the autumn of 1872 he sailed to the USA
and traveled overland to California in the spring of Reference
1873. A collecting expedition to British Columbia,
Wheeler Q (2000) Professor Roy Albert Crowson 19141999.
Oregon and parts of California followed. In the
Coleopterists Bull 54:120121
autumn of 1873 he returned to Philadelphia (his
point of arrival in the USA), having accepted an
appointment from Louis Agassiz to curate insects in
the Museum of Comparative Zoology at Harvard Crucifer
University. However, he had been infected with con-
sumption (tuberculosis), of which he died on June A plant in the family Cruciferae, such as cabbage,
16, 1874. Despite his travel and illness, he published broccoli, or collard. Crucifers also are called cole
eight papers on North American Coleoptera in crops.
 Crucifer Pests and their Management
C 1113

Crucifer Flea Beetle, Phyllotreta In the more northern latitudes, the cabbage looper
cruciferae (Goeze) (Coleoptera: populations become more variable and the imported
Chrysomelidae) cabbageworm becomes the dominant species. Both
the cross-striped cabbageworm and the cabbage
This species is a pest of several crucifer crops. webworm are generally localized, occasional pests.
Flea Beetles (Coleoptera: Chrysomelidae)

The Imported Cabbageworm, Pieris

Crucifer Pests and their rapae (L.) (Pieridae)
Management
The imported cabbageworm was first discovered in
Loke T. Kok North America in 1860 when a single specimen was
Virginia Polytechnic Institute and State Univer- captured in Quebec. Nearly 30 years later, it had
sity, Blacksburg, VA, USA spread north to Hudson Bay, south to the Gulf of
Mexico, and west to the Rocky Mountains. It now
Crucifer crops are members of the family Cruciferae occurs throughout most of North America. It spends
and include cabbage, cauliflower, Brussels sprouts, the winter as a cocoon in or near crucifer crops. In
broccoli, rape and mustard. Grown commercially or spring, the white adult (Fig.126) butterfly emerges.
as garden vegetables, they attract a large number of The male butterfly has one black spot and the female
insects. Since the common crucifer crops are intro- has two black spots on each front wing. After mat-
duced vegetables, most of the insect feeders origi- ing, the female lays eggs within 24 h of emergence.
nated in Europe or are species native to the United Eggs are laid singly on the underside of the outer
States that feed on a wide range of plants. The impor- leaves of the plant. They hatch into caterpillars in
tance and abundance of a given insect species four to eight days. The caterpillars molt four times
changes with location. Insects attacking crucifers and pass through five stages in 1233 days. The dark
can be divided into three groups: (i) leaf or foliage velvety green caterpillars (Fig.127) have a faint yel-
feeders, (ii) sap feeders, and (iii) root feeders. low stripe down the back and along the sides. They
feed voraciously on leaves and reach 25 mm in
length. When full grown, the caterpillar changes into
a cocoon. Each cocoon changes to an adult butterfly
Leaf or Foliage Feeders: in 820 days. The butterfly lives for approximately
Caterpillars and Flea Beetles three weeks. Females generally lay 200300 eggs.
They generally have two to four generations a year,
Caterpillars of moths, skippers, and butterflies in the but as many as six generations have been observed
order Lepidoptera are important leaf feeders. The in the southern portions of its range. A tiny wasp
adults have four large wings usually covered with parasite, Cotesia glomerata (L.) (Hymenoptera: Bra-
brightly colored scales. The most common are the conidae), attacks the first three caterpillar stages. It
cabbage looper, the imported cabbageworm, and the lays 2050 eggs into a caterpillar. The eggs hatch into
diamondback moth. Two others with potential of parasite grubs that feed within the caterpillar. When
becoming major pests are the cross-striped cabbage- the parasite grubs complete feeding on the caterpil-
worm and the cabbage webworm. The rank of spe- lar, they emerge as a group from the late fifth stage of
cies importance generally varies with latitude. In the the caterpillar, and spin yellow cocoons. The cater-
more southern areas of the United States, the cab- pillar dies. Cotesia rubecula (Marshall) is an exotic
bage looper is the most abundant, followed by the solitary wasp that is a close relative of C. glomerata.
imported cabbageworm and the diamondback moth. It generally attacks the first three caterpillar stages,
1114
C Crucifer Pests and their Management

Crucifer Pests and their Management, Figure 126 Imported cabbageworm adult.

but it kills the imported cabbageworm caterpillar of leaves, hatch in three days into caterpillars. The
soon after it molts to the fourth caterpillar stage. The caterpillar eats holes in leaves and reaches (Fig.128)
single C. rubecula grub inside it exits, and spins a full size in two to four weeks. The green caterpillar
white cocoon. Another parasitic wasp, Pteromalus forms a characteristic loop as it moves. It reaches
puparum (L.) (Hymenoptera: Pteromalidae) attacks 40 mm long when full grown and has a thin white
the cocoon stage of the imported cabbageworm. P. line along each side of the body and two near the
puparum is a gregarious internal parasite of the middle line of the back. It spins a cocoon and passes
imported cabbageworm, attacking the newly formed the winter in this stage. It emerges as an adult in
cocoon. The parasitic grubs develop within the host spring. There are three to six generations a year. A
and emerge as adult wasps through a small hole cut parasitic fly, Voria ruralis (Falln) (Diptera: Tachin-
in the cocoon case. idae), attacks the caterpillar. There are three para-
sitic wasps that attack the cocoon stage: Gambrus
ultimus (Cresson), Stenichneumon culpator cincti-
The Cabbage Looper, Trichoplusia ni cornis (Cresson), and Vulgichneumon brevicinctor
(Hbner) (Noctuidae) (Say) (Hymenoptera: Ichneumonidae).

The medium sized adult moth (Fig.128) is grayish

brown, about 25 mm long, with wing span of 38 Diamondback Moth, Plutella xylostella
mm. There is a silver figure 8 design near the center (L.) (Plutellidae)
of each front wing. The back wings are light brown
with a dark margin. In spring, about 300 eggs laid The diamondback moth is a cosmopolitan insect.
by a female singly on the upper and lower surfaces It is slender and grayish brown, 8.5 mm long, with
 Crucifer Pests and their Management
C 1115

Crucifer Pests and their Management, Figure 127 Imported cabbageworm caterpillars.

wing expanse of about 14 mm. When folded, the The full-grown caterpillar (Fig.129) is yellowish
wings display three diamond-shaped yellow spots green with erect long black hairs. It forms a fine
along the line where the wings meet. The colors of white mesh cocoon and the adult emerges in about
the female are lighter, and the markings less dis- a week. There are four to six generations a year in
tinct than the males. The back or hind wings have North America depending on temperature. In the
a fringe of long hairs. The moth passes the winter tropics, there can be as many as 1518 generations
under leaves. In spring, the moth lays an average of a year. The most common parasite of the caterpil-
160 small yellowish-white eggs that hatch in three lar is a wasp, Diadegma insulare (Cresson)
to five days. The greenish caterpillars feed on the (Hymenoptera: Ichneumonidae), that is capable of
leaves and complete development in 1030 days. killing up to 70% of the caterpillars.
1116
C Crucifer Pests and their Management

Cross-striped Cabbageworm, Evergestis side separating the gray from the yellow. The
rimosalis (Guene) (Pyralidae) cocoon stage lasts for 910 days, before changing
into the adult. There are three to four generations
The adult is a small yellowish brown moth(Fig.130) a year. This insect has the potential to be a very
with a dark patch towards the end of the front serious and destructive pest of crucifer crops in
margin of the front wing. The female lays about 80 the eastern United States. The young caterpillars
eggs in small overlapping masses on the host plant feed on leaves but the mature caterpillars migrate
leaf. The eggs are yellow, flattened, and hatch in to the heart or head of the plant and can riddle the
three to seven days. There are four caterpillar head with feeding holes making the plant unmar-
stages that complete (Fig. 131) development in ketable. It is naturally kept in check by a parasitic
617 days and change into a cocoon. The caterpil- wasp, Cotesia orobenae Forbes (Hymenoptera:
lar is gray on the back and yellow on the lower Braconidae), that feeds on the caterpillar. Indis-
side, with a broad distinctive black band on each criminate use of insecticides that kill off the para-
site will result in outbreaks of the cross-striped
cabbageworm.

Cabbage Webworm, Hellula rogatalis

(Hulst) (Lepidoptera: Pyralidae)

The cabbage webworm is a sporadic but destruc-

tive pest of crucifer crops in the southeastern
United States. It is potentially the most serious pest
of broccoli. The front wing of the moth is light
brown and gray. The newly emerged adults start
laying eggs in three to four days and can deposit
Crucifer Pests and their Management,
up to 161 eggs per female. Newly laid eggs are
Figure128 Cabbage looper adult.
yellowish green, and turn pink as they mature.

Crucifer Pests and their Management, Figure 129 Diamondback moth caterpillar.
 Crucifer Pests and their Management
C 1117

Crucifer Pests and their Management, Figure 130 Cross-striped cabbageworm adult.

Crucifer Pests and their Management, Figure 131 Cross-striped cabbageworm caterpillars.

Most of the eggs are laid on the upper surface of roll up. They also spin webs among the rolled
the leaf, and hatch in three to eight days. There are leaves. The webs protect them from insecticide
five caterpillar stages and they complete develop- sprays. The last two caterpillar stages feed on the
ment in 1535 days. The first two caterpillar stages leaf and midrib, breaking it into two. The caterpil-
mine the leaf between the upper and lower leaf lar moves to the heads after eating the leaves. The
surface (Fig. 132). The larger caterpillars feed on cocoon stage lasts for 717 days before changing
the underside of the leaf causing them to curl and to adult. The adult lives for 1125 days. There are
1118
C Crucifer Pests and their Management

Crucifer Pests and their Management, Figure 132 Cabbage webworm damage.

one to two generations per year. It is difficult to Flea Beetles (Coleoptera: Chrysomelidae)
control cabbage webworms because the caterpil-
lars are protected and there are no effective para- Flea beetles are small elongate, oval, black bee-
sites that attack them. tles of 1.63.2 mm with back legs enlarged for
jumping. When disturbed, they jump up resem-
bling fleas bouncing up and down, hence their
Occasional Caterpillar Pests common name, flea beetles. The adult beetle is a
general feeder of leaves, leaving tiny pits or
Caterpillars that are occasional or minor pests small holes. When they are present in large
include the corn earworm Helicoverpa zea (Bod- numbers, their feeding can cause pitted areas
die) (Lepidoptera: Noctuidae); fall armyworm, and numerous holes on leaves. There are two
Spodoptera frugiperda (J. E.Smith) (Lepidoptera: common species among crucifers, the potato
Noctuidae); green cloverworm, Plathypena scabra flea beetle Epitrix cucumeris (Harris) and
(Fabricius) (Lepidoptera: Noctuidae); yellow- the tobacco flea beetle Epitrix hirtipennis
striped armyworm (Lepidoptera: Noctuidae), and (Melsheimer). Eggs of flea beetles are very tiny
southern cabbageworm, Pontia protodice (Boisdu- and difficult to see. The potato flea beetle scat-
val & LeConte) (Lepidoptera: Pieridae). Severe ters its eggs in the soil close to roots of host
feeding on the leaves by these caterpillars results plants. The tobacco flea beetle eggs are laid in
in loss of crop yield. All plant stages, from seedling batches or clusters. They hatch in about 10 days
to heading, are susceptible to attack. Before a man- into whitish, slender, cylindrical worms that
agement program is initiated, it is important to feed on the roots of weeds and crucifer plants.
have an understanding of the occurrence of the The worms or grubs usually do not cause as
individual species and their life stages during the much damage as the adults. When full grown in
growing season. about four weeks, the worms are 3.28 mm long,
 Crucifer Pests and their Management
C 1119

and have tiny legs and brownish heads. They and cauliflower are a few of the economically
change into the cocoon stage that lasts for 710 important crops attacked by this pest. It also has
days before emerging as adults. There are usu- been found on many wild plants, allowing the
ally one to two generations a year. Flea beetles bugs to survive when crucifers are not present.
are very common on new plantings and can The number of harlequin bug generations per
cause severe damage to young seedlings or year varies by location. There are two genera-
plants. They often infest weeds near crucifer tions in the north and up to five generations in
crops and move onto young plants. Heavy infes- the South. In the North, the adult finds shelter in
tations cause young plants to dry up. cabbage stalks, grass or other debris. In the
South, the insects feed and breed during the
entire year. The adults become active in spring
Sap Feeders: Harlequin Bugs, when they start feeding on weeds, and are ready
Aphids to lay an average of 150 eggs when garden plants
or crucifers are available. The tiny white eggs
Harlequin bugs and aphids are the most serious that look like kegs are laid mostly on the under-
sap feeders of crucifers. They can be especially side of leaves in two rows. There are normally 12
damaging to young plants that cannot withstand eggs per batch, and each egg has two broad black
as much damage as the larger plants. Thus, they are loops. They hatch in 429 days, depending on
often serious pests during the early plantings or temperature into young (nymph) bugs. The
transplantings of crucifers. Both the adults and young bugs molt after five days. Each developing
young nymphs suck sap from the plants. bug molts four times and passes through five
nymphal stages in about 45 days to reach the
adult stage. Feeding damage results in death of
Harlequin Bug, Murgantia histrionica young plants. The younger plants succumb to
(Hahn) (Heteroptera: Pentatomidae) feeding injury sooner than the older plants. Time
to death is shorter when larger numbers of har-
The harlequin bug (Figs.133 and 134) is an exotic lequin bugs feed together on the same plant.
pest originating in Central America. It was first
recorded in the United States in 1864. It passes
the winter south of the 40N latitude. Individu- Cabbage Aphids, Brevicoryne brassicae
als found north of the 40N latitude most likely (L.) (Hemiptera: Aphididae)
are carried by wind currents or are due to sea-
sonal migration. It was considered the most Cabbage aphids are green, soft-bodied insects often
destructive insect pest of crucifers in the referred to as plant lice because of the large numbers
United States before the use of synthetic and their rapid rate of reproduction. They are 1.6
insecticides because it is capable of destroying 3.2 mm in length. They feed by inserting their sharp
entire crops. After the advent of synthetic insec- needle-like stylets in their beaks into plant tissues
ticides, the importance of the harlequin bug and suck sap from the plant.Affected leaves (Fig.135)
declined. However, the harlequin bug has often curl and crinkle or become deformed. During severe
caused substantial damage in crucifers during infestations, they cover the whole plant, causing the
the past decade when insecticides were not used. plant to wilt and die. Infested plants that survive are
The harlequin bug has a wide host range and has shorter and grow more slowly, and cabbage heads
been reported to feed on over 50 species of that are formed are light in weight and are not suit-
plants, including crucifers. Cabbage, collards, able for marketing. The aphid can reproduce by nor-
broccoli, Brussels sprouts, kale, mustard, turnip, mal sexual reproduction and asexually without
1120
C Crucifer Pests and their Management

Crucifer Pests and their Management, Figure 133 Harlequin bug adults on rape.

mating. Sexual reproduction occurs in the fall when maggots of the flower (syrphid) fly. These usually
winged males and females are formed. These are the keep the aphid population down. During heavy
fall migrants that leave the summer host. The winged infestations, chemical sprays or insecticidal soaps
females produce wingless females that mate with the may have to be used. For chemical sprays to be effec-
males of the previous generation. After mating, the tive, they have to reach the underside of the leaves
true female lays small black fertilized eggs in a shel- where the aphids usually lodge.
tered place to pass the winter. From these eggs rise
the stem mother the next year. The eggs hatch into
small nymphs (young aphids) and grow to full size Root Feeder: Cabbage Maggot
as stem mothers with warmer weather. These stem
mothers are wingless. Each can reproduce without Cabbage Maggot, Delia radicum (L.)
mating and gives rise to 50100 eggs that hatch (Diptera: Anthomyiidae)
while they are still inside the stem mother and
emerge as active nymphs in 714 days. These young This is a serious pest in the northern states above
nymphs can reproduce just like their stem mothers 40N latitude, and in Canada. The adult fly resem-
within a week. Each generation takes about a month. bles a housefly and is dark ash gray in color, but is
The number of generations depends on tempera- smaller, 6.4 mm long. It lays its eggs in cracks and
ture, and in the far south, they continue to breed crevices in the soil near the roots. The eggs hatch
yearround. Several natural enemies feed on aphids. in three to seven days into small maggots. The
The most common predators are grubs and adults maggots feed on the roots of crucifers below
of ladybird beetles and green lacewings, and the ground level and thus are not easily seen. Small
 Crucifer Pests and their Management
C 1121

Crucifer Pests and their Management, Figure 134 Harlequin bug nymph.

Crucifer Pests and their Management, Figure 135 Cabbage aphids.

1122
C Crypsis

roots are entirely eaten and larger roots show feed- that it is difficult to discern from its background.
ing tunnels caused by the maggots. Heavy feeding The advantage of crypsis in most animals is that it
causes the plant to wilt and become stunted. Such gives protection against predators that detect prey
plants have a sickly color. The maggots are white, by eyesight. For example, many green caterpillars
6.48.5 mm and without legs, and feed for three to are camouflaged on leaves, giving them protection
four weeks to reach full size. They move away from against insectivorous birds. Some predators are
the root to the soil and form a brown casing called also cryptic which enables them to get close to
the puparium within the top few inches of the soil. prey that detect predators visually. For example, a
The puparium stage lasts for two to three weeks. lion or a leopard crouching in yellow-brown grass
The adult fly that emerges begins laying eggs. There is well camouflaged so its prey may inadvertently
are two to four generations a year. The winter is wander close to it. Among arthropods, the flower
passed in the quiescent pupa stage inside the mantids Pseudocreobotra and Hymenopus, and the
puparium casing. To control this fly, it is best to crab spider Misumena (Thomisidae), are all cryp-
cover the seedbeds of crucifers with thin cloth or tic when resting on flowers while waiting to grab
fine mesh gauze. Insecticidal drenches also can be insects that visit the flower for nectar or pollen.
used at the time of planting or transplanting. Crypsis here could be both a defense against pred-
ators (Figs.136 and 137) and also an aid for cap-
turing insects that visit the flowers but do not see
References
them. However, it has not been demonstrated that
fewer insects visit flowers with conspicuous rather
Chamberlin JR, Kok LT (1986) Cabbage lepidopterous pests
and their parasites in southwestern Virginia. J Econ than with cryptic predators on them, so this sug-
Entomol 79:629632 gestion remains unproven.
Kok LT, Acosta-Martinez JA (2001) Development of Cotesia The simplest form of camouflage involves the
orobenae Forbes (Hymenoptera: Braconidae) in its host,
Evergestis rimosalis (Guene) (Lepidoptera: Pyralidae).
animals color matching that of its background,
J Entomol Sci 36:916 e.g., green lacewings, Chrysopa (Neuroptera), on
Kok LT, McAvoy TJ (1989) Fall broccoli pests and their para- green leaves or transparent mosquito larvae in the
sites in Virginia. J Entomol Sci 24:258265 plankton of ponds. However, birds and some other
Lasota JA, Kok LT (1989) Seasonal abundance of imported
cabbageworm (Lepidoptera: Pieridae), cabbage looper vertebrate predators have excellent eyesight and
(Lepidoptera: Noctuidae), and diamondback moth can recognize a simply camouflaged insect either
(Lepidoptera: Plutellidae) on cabbage in southwestern by the shadow on its lower surface or by its char-
Virginia. J Econ Entomol 82:811818
acteristic outline. Two evolutionary responses of
Ludwig SW, Kok LT (2001) Harlequin bug, Murgantia histri-
onica (Hahn) (Heteroptera: Pentatomidae) development cryptic insects to such predators are countershad-
on three crucifers and feeding damage on broccoli. Crop ing and disruptive coloration.
Prot 20:247251 Green grasshoppers are cylindrical so, when
Mays WT, Kok LT (1997) Oviposition, development, and host
preference of the cross-striped cabbageworm (Lepi-
sunlight comes from above, the ventral surface
doptera: Pyralidae). Environ Entomol 26:13541360 will be in shadow and hence appear to be darker
green than the dorsal surface. Countershaded
grasshoppers are paler green ventrally so that this
Crypsis shadow is reduced and the crypsis is improved
because the animal appears uniformly green in
Malcolm Edmunds side view. Green hawkmoth caterpillars usually
University of Central Lancashire, Preston, UK rest upside down under leaves and stems and have
reversed countershading with the upper ventral
Crypsis is a Greek word meaning camouflage. An surface dark green and the lower dorsal surface
animal that is cryptic is one that is camouflaged so pale green.
 Crypsis
C 1123

Crypsis, Figure 136 The eyed hawkmoth (Smerinthus ocellata) larva showing reverse countershading.
When the larva rests in its normal orientation (left), the body appears flat due to the lighter coloration
of the dorsal surface of the insect. When the twig bearing the larva is inverted (right), the larva becomes
very conspicuous as the sun shining on the light dorsum increases the contrast between the insects
dorsal and ventral surfaces (photos by M. Edmunds).

Crypsis, Figure 137 Shorthorn grasshoppers mating, with disruptive black markings that break-up the
body outline and conceal the eye (photo by M. Edmunds).

Many green grasshoppers have black streaks eyes are possibly a feature by which vertebrate pred-
and stripes on their bodies which draw the eyes of ators can recognize an otherwise well camouflaged
predators to these marks rather than to the contour insect. One way of concealing the eye is for disrup-
of the insect. These are disruptive colors. Similar dis- tive lines to pass through it so that attention is drawn
ruptive markings occur in caterpillars, shield bugs away from the eye to the line which does not look
and many other cryptic insects. Large compound like insect prey. Disruptive eyestripes occur in many
1124
C Crypsis

grasshoppers. It is probable that disruptive colors straight line like a broken twig. Stick insects (Phas-
increase the probability that a prey insect will not be mida) and some praying mantids (e.g., Danuria,
found by a predator, but this has not been demon- Heterochaeta, Angela) also have slender bodies and
strated experimentally. appropriate resting postures such that they closely
Crypsis can also be perfected by morphologi- resemble sticks, while leaf insects (Phasmida) and
cal adaptations, e.g., by flattening of the body so some mantids (Choerododis, Phyllocrania), butter-
there is no ventral shadow, or by resembling a spe- flies (Kallima), and grasshoppers (Zabilius) closely
cific part of the environment, such as a stick or a resemble individual leaves. Some caterpillars rest
leaf. Some (Figs.138 and 139) green lycaenid cat- conspicuously on the upper surfaces of leaves and
erpillars, the green Australian mantid Neomantis closely resemble black and white bird droppings.
(both on green leaves) and the brown mantis Theo- Since insectivorous birds normally ignore drop-
pompa and bug Dysodius (both on bark) are all pings this probably gives good protection. How-
flattened so there is no ventral shadow. Other ever, as the caterpiller grows it becomes too large
insects have excrescences that break up the body to mimic a bird dropping. The final instar of the
outline, e.g., the grass-living mantis Pyrgomantis alder moth (Apatele almi) is black and yellow
and the grasshopper Cannula are both long and (either aposematic or mimicking a wasp), that of
slender with a pointed vertex on the head so they Trilocha kolga changes to resemble the brown and
resemble a blade of grass, while the mantids Phyl- black feces of a large lizard or bird. In Oxytenis
locrania and Hemiempusa both have foliose excres- naemia the final instar resembles brown leaf detri-
cences (leaf-like outgrowths) on the legs and head tus fallen from the canopy, while in species of Pap-
(Fig.140). ilio it is disruptively colored green and black and
Looper caterpillars of geometrid and noctuid no longer rests on top of leaves. There is also a
moths are usually brown with minute legs which cicada, Ityraea, where a cluster of insects resembles
are barely visible close to the head, and a slender, a spike of flowers. These highly specific resemblances
cylindrical body that may be rugose like the bark have been called stick mimicry, leaf mimicry, bird
of a twig. They rest with the posterior claspers dropping mimicry, etc. However, since they have
gripping a branch and the body extended in a presumably evolved from simple camouflage by

Crypsis, Figure 138 The brown chrysalis of the hawkmoth, Atemnora westermanni, resembles a dead leaf
lying amongst brown leaves on the forest floor of Ghana (photo by M. Edmunds).
 Crypsis
C 1125

Crypsis, Figure 139 The mantid, Neomantis australis, from Queensland, Australia, shows cryptic green
coloration and a flattened body that reduces shadow (photo by M. Edmunds).

predator selection progressively eliminating the Given a choice of resting on a white surface with
more easily found insects, they are probably better vertical or horizontal black tape strips, Sargent
considered as extreme forms of crypsis, and Cott found that significantly more insects rested with
called them examples of special resemblance. the markings parallel to the strips (p<0.001) giving
A cryptic insect is only well camouflaged when excellent camouflage, but equal numbers rested
on the correct background, but if it moves some- sideways and vertically (with head up or down), so
where else or if the background changes it is imme- the moth adjusts its resting position to coincide
diately vulnerable to predation. Many cryptic with the strips. When the experiment was repeated
insects move until they find a suitable background with the strips covered with acetate so that there
on which to rest, typically one on which they are was no difference in texture, the resting positions
cryptic. Thus, when the polymorphic grasshopper of the moths were random with respect to the
Acrida turrita was given a choice of backgrounds, strips, with equal numbers facing sideways and
significantly more green than yellow insects rested vertically, so Sargent concluded that the resting
on a green background and significantly more position of this moth is determined by tactile rather
yellow than green insects rested on a yellow back- than visual stimuli. The noctuid moth Catocala
ground (p<0.001 in both cases). Similar background ultronia normally rests with the head down and the
choice occurs in other polymorphic grasshoppers markings parallel with vertical ridges on the bark.
and in praying mantids, resulting in green insects In a similar experiment, significantly more insects
tending to rest on green substrates and brown ones rested with their markings aligned to the strips giv-
to rest on brown substrates. Bark-resting moths ing good camouflage (p<0.05), and almost all
with disruptive markings adopt resting postures moths rested head vertically down rather than hor-
which align their markings with similar marks on izontally (p<0.001). The resting positions were
the tree. The geometrid moth Melanolophia cana- unchanged if the strips were covered with acetate,
daria normally rests sideways with its markings so in this species, resting posture is innate and not
running vertically parallel to striations in the bark. modified by substrate pattern or texture.
1126
C Crypsis

Crypsis, Figure 140 The brown leaf mimicking preying mantid, Phyllocrania paradoxa, rests on brown
dead vegetation in Ghana. Note the frills on head, body, and legs which break up the outline of the
insect (photo by M. Edmunds).

Some cryptic insects can change color during the winter on deciduous shrubs. However,
(Fig. 141) so that they match their background, with a long photoperiod (i.e., in summer), pupae
but this change usually takes several days or occurs were usually brown on thick branches but green
only when the insect moults. Some swallowtail on thin twigs, giving good camouflage both on
and other butterfly pupae can be either green or brown branches and on green twigs close to green
brown, usually matching their substrate. Details leaves. Final instar poplar hawkmoth caterpillars
vary in different species, but in Papilio polyxenes (Laothoe populi) can be green or white depending
short daylength induces most caterpillars to turn on whether they are resting on green or white-
into brown pupae which are well camouflaged leaved food plants. When reared on two different
 Crypsis
C 1127

Crypsis, Figure 141 This satyrid butterfly, Paralaza nepalica, from Nepal blends into a sandy background
(photo by A. Sourakov).

plants significantly more sibling poplar hawk cat- insect is cryptic in the peppared moth (Biston bet-
erpillars on green leaved Salix fragilis became ularia), caterpillars of the pine looper (Bupalus
green rather than white while significantly more piniarus) and poplar hawkmoth (Laothoe populi),
reared on white-leaved Populus alba became white. grasshoppers (Acrida turrita), and praying man-
Similarly, various grasshoppers and praying man- tids (Mantis religiosa). Experiments have also
tids can begreen or brown depending on whether shown that countershaded green pastry prey were
their substrate is green or brown. In all examples found significantly less often by wild birds than
that have been studied, the specific cue that deter- were uniformly green prey, so demonstrating the
mines which color the insect becomes is not sub- selective advantage of countershading.
strate color but some other factor such as humidity It is tempting to ask why, if crypsis is of such
(in the mantid Miomantis paykullii and the grass- great advantage to an animal, many more animals
hopper Syrbula admirabilis), light intensity (in the are not cryptic. The main reason is because cryptic
mantid Sphodromantis lineola), or substrate reflec- animals must remain motionless, and adaptations
tance (in the hawkmoth Laothoe populi). that perfect crypsis may conflict with other essen-
Finally, there is abundant experimental evi- tial activities such as feeding, escape by running or
dence that crypsis does indeed reduce predation flying, or finding a mate. However, predators can
on insects. Most experiments involve placing some become more proficient at finding cryptic prey by
insects on a background where they are camou- developing a searching image for specific insects.
flaged and others on one where they are conspicu- One evolutionary response to this aspect of preda-
ous and then exposing them to predators either in tor behavior is for the prey to evolve several differ-
the laboratory or in the field. Polymorphic insects ent color forms (polymorphism) such that the
are especially good experimental subjects because density of each morph remains low and the preda-
the two morphs can be placed on two backgrounds, tor must acquire several different searching images
one of which matches the color of each morph. if it is to fully exploit the prey population. Cryptic
Experiments of this type have shown the selective polymorphic insects occur among grasshoppers
advantage of resting on a background where the (Acrida), mantids (Mantis, Sphodromantis),
1128
C Cryptobiosis

hemipterans (Philaenus spumarius), caterpillars When the rainy season comes and the pool fills
(Bupalus piniarus, Herse convolvuli), and moths with water, they may revive after rehydration. The
(Biston betularia). desiccated larvae also become resistant to extreme
temperature conditions. So far, 17 years is the lon-
gest record of dormancy for this insect. When
References given water, the larvae quickly become active, usu-
ally within one hour, with no ill effects.
Cott HB (1940) Adaptive coloration in animals. Methuen, Slow dehydration is more beneficial for the
London, UK, 508 pp insect than rapid dehydration. Larvae make tubes
Edmunds M (1974) Defence in animals: a survey of anti-
predator defences. Longman, Harlow, UK, 357 pp
by incorporating detritus and soil with their
Edmunds M, Evans DL, Schmidt JO (eds) (1990) Insect sticky saliva. The tube serves not only as a physi-
defences. State University of New York, Longman, Har- cal barrier against enemies and aids in feeding,
low, UK, pp 321 but also reduces the dehydration rate. In the
Edmunds M, Dewhirst RA (1994) The survival value of coun-
tershading with wild birds as predators. Biol J Linn Soc absence of tubes, larvae do not survive rehydra-
51:447452 tion. During the dehydration process, larvae
Edmunds M, Grayson J (1991) Camouflage and selective pre- accumulate large amounts of trehalose (up to
dation in caterpillars of the poplar and eyed hawkmoths
20%), which provides effective protection against
(Laothoe populi and Smerinthus ocellata). Biol J Linn
Soc 42:467480 desiccation because of its high capacity for water
Wickler W (1968) Mimicry in plants and animals. Wieden- replacement and vitrification. Although mem-
feld & Nicholson, London, UK, 255 pp branes are impermeable to trehalose, a trehalose
transporter is expressed in the fat body, allowing
trehalose production and transport into the
Cryptobiosis hemolymph. Trehalose also serves to protect pro-
teins and cell membranes. Late embryogenesis
Takashi Okuda abundant (LEA) proteins occur in the dehydrat-
National Institute of Agrobiological Sciences, ing larvae, preventing protein aggregation when
Ohwashi, Tsukuba, Japan concentrated upon desiccation. The anhydrobi-
otic larvae attain tolerance to several extreme
Cryptobiosis is defined as the state of organism conditions to such an extent that they can revive
when it shows no visible signs of life and when after expose to -270 to+103C, irradiation up to
its metabolic activity becomes hardly measur- 9 k Gy, and submersion in pure ethanol.
able, or comes reversibly to a standstill. Crypto-
biosis is a generic term for ametabolism, and
can be further divided into five categories based
References
on factors inducing them: cryobiosis (induced
Clegg JS (2001) Cryptobiosis a peculiar state of biological
by freezing), thermobiosis (low and high tem- organization. Comp Biochem Physiol B 128:613624
peratures), osmobiosis (high osmolarity), anhy- Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis.
drobiosis (lack of water) and anoxybiosis (lack Annu Rev Physiol 54:579599
of oxygen). Kikawada T, Minakawa N, Watanabe M, Okuda T (2005)
Factors inducing successful anhydrobiosis in the African
So far, the African chironomid Polypedilum Chironomid Polypedilum vanderplanki: Significance of
vanderplanki is the only insect species exhibiting the larval tubular nest. Integr Comp Biol 45:710714
cryptobiosis (anhydrobiosis, in this case). The lar- Kikawada T, Saito A, Kanamori Y, Nakahara Y, Iwata
K,Tanaka D, Watanabe M, Okuda T (2007) Trehalose
vae of this chironomid live in small and shallow
transporter 1, a facilitated and high-capacity trehalose
rock pools. When the pool dries up during the dry transporter, allows exogenous trehalose uptake into
season, the larvae become completely desiccated. cells. Proc Natl Acad Sci USA 104:1158511590
 Csiki, Ern; (Ernst Dietl)
C 1129

Watanabe M, Kikawada T, Yukuhiro F, Okuda T (2002) Mecha- which, in addition to the endospore, produce
nism allowing an insect to survive complete dehydration a discrete, characteristic crystal or crystal-like
and extreme temperatures. J Exp Biol 205: 27992802
Watanabe M, Nakahara Y, Sakashita T, Kikawada T, Fujita A, inclusion in the sporulating cell.
Hamada N, Horikawa D, Wada S, Kobayashi Y, Okuda T
(2007) Physiological changes leading to anhydrobiosis
improve radiation tolerance in Polypedilum vander-
planki larvae. J Insect Physiol 53:573579
Csiki, Ern; (Ernst Dietl)

George Hangay1, Otto Merkl2, Gyz Szl

Cryptoceridae 1
Narrabeen, New South Wales, Australia
2
Hungarian Natural History Museum, Budapest,
A family of cockroaches (order Blattodea). Hungary
Cockroaches
Ernst Dietl was born on the October 22, 1875
at Zsilvajdejvulka, Hunyad Shire, Transylvania,
Cryptochetid Flies Hungary, today Vulcan, Romania. In 1897 he
graduated at the College of Veterinary in Buda-
Members of the family Cryptochetidae (order pest and shortly afterwards gained employment
Diptera). in the Hungarian National Museums Zoological
Flies Collections as assistant curator. He was mainly
responsible for the library and the beetle collec-
tion. In 1898 he changed his original German
Cryptochetidae name to the Hungarian Csiki. He remained in
the service of the museum until his retirement in
A family of flies (order Diptera). They commonly 1933, eventually ascending to the position of
are known as cryptochetid flies. Departmental Head or Director. After his retire-
Flies ment he withdrew from active work for a few
years but as World War II ended, he returned to
the museum as an outside consultant to continue
Cryptophagidae with his entomological activities. In 1953, at the
age of 78 he received the Doctor of Biological Sci-
A family of beetles (order Coleoptera). They
ences degree. He has passed away in Budapest, on
commonly are known as silken fungus beetles.
the 7th of July 1954. Ern Csiki was probably the
Beetles
first Hungarian museum entomologist who could
devote his entire active life to his chosen group of
Cryptorhamphidae insects, the Coleoptera. During his years the
museums beetle collection grew from 120,000 to
A family of bugs (order Hemiptera, suborder well over one million specimens. This unprece-
Pentamorpha). dental growth was partially due to the personal
Bugs collecting activities of Csiki which yielded more
than 60,000 beetles and partially to the fact that in
those years the museum had sufficient funds for
Crystalliferous purchasing valuable collections. One of the most
notable acquisitions was Reitters European and
Producing or bearing crystals. This term is applied Asian collection, containing over 200,000 speci-
to a number of Bacillus and Paenibacillus species mens and more than 5,000 types. Ern Csiki was
1130
C Ctenidium (pl . ctenidia)

one of the most prolific Hungarian coleopterists, Cubitus

describing more than 400 species, publishing 451
works containing over 9,000 pages. He had a wide The fifth longitudinal wing vein. It extends from
interest, although the Carabidae was his favorite the wing base and usually is two-branched before
group. His major work, Die Kferfauna des Kar- reaching the wing margin.
paten-Beckens, 1946 is still considered a funda-
mental monograph of the Central-European
Carabidae. He was a major contributor to the
Cuckoo Bees
Junk- Schenkling Coleoptorum Catalogus. He
Members of the family Anthrophoridae (order
wrote 4,748 pages for the volumes published
Hymenoptera, superfamily Apoidae).
between 1910 and 1940. During his life he received
Bees
numerous awards and prizes, and earned the
Wasps, Ants, Bees, and Sawflies
respect of all his colleagues. In the Second Dis-
trict of Budapest, where he lived, a street was
named Beetle Street, (Bogr utca) in honor of Cuckoo Wasps
Ern Csiki.
Members of the family Chrysididae (order
Hymenoptera).
References Wasps, Ants, Bees, and Sawflies

Sachtleben H (1955) Gestorben Dr. Ern Csiki. Beitrge zur Cucujidae

Entomologie 5:454
Szkessy Vilmos (1954) Dr. Ern Csiki (18751954). Folia
enomologica hungarica (S. N.) 7:120 A family of beetles (order Coleoptera). They com-
Szkessy Vilmos (1955) Csiki Ern emlkezete. llattani monly are known as flat bark beetles.
Kzlemnyek 45:710 Beetles

Cucurbit
Ctenidium (pl. ctenidia)
A plant in the family Cucurbitaceae, such as
A comb-like structure found on any part of an
cucumber, squash, and watermelon.
insect, but particularly the comb of flat spines
found in fleas and certain beetles.
Cucurbit Yellow Vine Disease

Ctenoplectidae This disease occurs in North America, and squash

bug is thought to be the vector.
A family of wasps (order Hymenoptera). Transmission of Plant Diseases by Insects
Wasps, Ants, Bees, and Sawflies
Culicidae
Ctenostylidae A family of flies (order Diptera). They commonly
are known as mosquitoes.
A family of flies (order Diptera). Mosquitoes
Flies Flies
 Cultivation
C 1131

Culicifuge C. clavisporus germ tubes through host cuticle

takes 618 hours. Melanized areas can form in the
A mosquito repellent. This term is derived from cuticle around the advancing hyphae, and the fun-
the family name for mosquitoes (Culicidae) and gus is then forced to grow around this resistant
the Latin verb fugere (to flee). material. As in the cuticle, zones of melanization
also can develop in the hypodermis. Cylindrical
blastospores form by budding from the hyphae
Culicinomyces clavisporus and circulate in the hemolymph. Mycelial forma-
tion follows, and conidiophores eventually grow
One species of the genus Culicinomyces, C. clavispo- out through the thorax, abdomen, mouthparts,
rus, includes Australian, American and Canadian and bases of antennae. A dense layer of conidia is
strains isolated from the mosquitoes Anopheles hilli, produced on the cadaver; however, the degree of
A. quadrimaculatus, and Culiseta inornata, respec- sporulation depends upon the time of larval death.
tively. The fungus is able to infect mosquito genera If the larvae die before they are completely filled
that transmit diseases in higher animals (e.g., with mycelia, external conidia may not form. It is
Anopheles, Culex, and Aedes). Culicinomyces clav- speculated that toxins released by the high con-
isporus also is pathogenic to some other aquatic centration of penetrating hyphae contribute to
dipteran larvae in the families Chironomidae, Cer- such rapid larval death because normally, up to
atopogonidae, Simuliidae, Syrphidae, and Ephydri- one week is required for larvae to succumb to a
dae. The three strains vary with respect to colony Culicinomyces infection.
morphology, conidial development, and growth
rates in different media; all three exhibit conidial
dimorphism, with the smaller type of conidia References
more abundantly produced in the Australian and
American strains. In addition, conidia can be gen- Cooper RD, Sweeney AW (1986) Laboratory studies on the
erated on polyphialides, phialides with more than recycling potential of the mosquito pathogenic fungus
Culicinomyces clavisporus. J Invertebr Pathol 48:152158
one neck, in all of the isolates. The gray-white colo- Goettel MS, Sigler L, Carmichael JW (1984) Studies on the
nies can appear more darkly pigmented in all of the mosquito pathogenic hyphomycete Culicinomyces clav-
strains depending upon culture conditions. Culi- isporis. Mycologia 76:614625
cinomyces has been targeted as a potential biocon- Sweeney AW, Inmann AO, Bland CE, Wright RG (1983) The
fine structure of Culicinomyces clavisporus invading
trol agent because it is easily cultured under surface mosquito larvae. J Invertebr Pathol 42:224243
or submerged conditions, and because it can recycle
within mosquito populations. Recycling is due to
the formation of external spores on dead, infected Cultivar
larvae which infect later generations of larvae either
from the same genus or a different one. An agricultural plant variety or strain developed
Culicinomyces clavisporus is unusual because for specific horticultural properties.
its submerged conidia are produced both in vitro
and in vivo, and it invades host larvae through the
digestive tract (foregut) rather than the outer Cultivation
integument. Ingested conidia adhere to the cuticle
of the digestive tract via their sticky outer coating. A tillage operation used to prepare land for culti-
This bonding between the conidia and host epicu- vation. Cultivation also disrupts pest populations,
ticle is strong enough to resist mechanical disrup- including weeds and soil insects.
tion by movements of the gut wall. Growth of Cultural Control of Insect Pests
1132
C Cultural Control of Insect Pests

Cultural Control of Insect Pests potential termite-infested wood around homes,

and composting garden debris to eliminate pests.
John All Pest endurance practices are methods
University of Georgia, Athens, GA, USA designed to aid commodity tolerance of pests
without economic damage. Examples of agricul-
Cultural control is using the production or utiliza- tural methods that stimulate optimum health and
tion methods of a commodity with a concern for vigor in crops for tolerance of insect injury include
insect management. Cultural control practices are using vigorous seed, good seedbed preparation,
usually multipurpose technical procedures that optimal fertilization, irrigation and weed control,
create environments that either avoid high-risk thinning, pruning, etc.
situations for infestations or develop unfavorable Pest preventive maintenance practices are
conditions for pests. The operations are often the procedures that keep commodity environments
foundation of preventive control strategies in inte- clean and free of materials where pests can build
grated pest management (IPM) programs. Cul- up and methods that ensure rapid movement of
tural controls are not usually intended to suppress commodities through production, storage, and
insect outbreaks, but are designed to prevent infes- shipment in order not to allow time for pests to
tations from developing. These control methods increase.
are usually inexpensive because they are generally Crop and cultivar selection is choosing crops
necessary for producing or using a commodity and cultivars with consideration of their suscepti-
often with pest management as a secondary prior- bility or resistance to the insect pests, along with
ity. Designing and implementing cultural control high yield, produce quality, and other desirable
in IPM programs may call for greater professional agronomic characteristics. It is using adapted
competence, because greater knowledge of insect crops and cultivars that have the greatest profit
biology and behavior is usually required as com- potential with the least hazard for insect problems.
pared to other insect management methods (e.g., Crop and cultivar selection includes the use of
control with insecticides). Patience and persever- insect resistant varieties (including insecticidal
ance are important because the preventive nature transgenic plants), but it also includes decisions to
of cultural control tactics often does not show tan- avoid high-risk crops or cultivars that could pro-
gible results other than a lack of pest problems on duce insect outbreaks. Examples include use of
a commodity. Several cultural control methods are cotton and corn varieties that express insecticidal
frequently combined with other pest management Cry proteins derived from the bacterium Bacillus
techniques in IPM programs for a commodity. thuringiensis Berliner or the use of wheat contain-
Examples of cultural control methods used ing native resistant genes to the Hessian fly, May-
independently or in concert with other insect etiola hibiscella (Swazey).
management tactics in IPM programs are: Crop rotation is switching plant species within
Sanitation is destroying the habitat associated an environment in order that a resident insect pop-
with a commodity so that insect pests are deprived ulation which is adapted to one of the crops cannot
of shelter, protection from natural enemies, over- survive when the other is planted into the field. An
wintering sites, etc. Sanitation also refers to meth- example would be using corn and soybean as field
ods that destroy or remove insects directly from crops in alternate years so that larvae of western
the commodity environment. Examples include corn rootworm, Diabrotica virgifera virgifera
destruction of infested weeds and crop debris in LeConte, cannot survive the shift from host corn to
and around crop fields, use of vacuums and/or non-host soybean. Crop rotation is applicable to
high pressure water or air to clean machinery in other situations such as in greenhouses, plant nurs-
food processing areas and warehouses, removal of eries, etc. and can be used during the same year in
 Culture of Natural Enemies on Factitious Foods and Artificial Diets
C 1133

fields where multicropping is used. Crop rotation is insect pests and useful insects which falls into
also applicable for stored products as when soy- the realm of economic or applied entomology. The
bean and corn are alternated in grain bins to dis- second is the study of the biology of insects for
courage the build up of granary weevils, Sitophilus the sake of knowing without practical application,
spp., and meal moths, Pyralis farinalis L. which is generally referred to as basic entomology.
Disruption of phenological synchrony is However, recently a distinct field of entomology
interfering with a pest populations natural asso- has been recognized called cultural entomology.
ciation with susceptible growth stages of a crop. Cultural entomology is the study of the influence
Alternating planting and harvest dates and using of insects and other terrestrial arthropods in lit-
cultivars of desirable maturity are ways that crop erature, languages, music, the arts, interpretive his-
growth can be manipulated to avoid peak levels of tory, religion, and recreation. Because the term
pests during the season, for example, early plant- cultural is narrowly defined, some aspects nor-
ing of sweet corn to avoid high populations of mally included in studies of human societies are
corn earworm, Helicoverpa zea Boddie, and fall excluded. Thus, ethnoentomology, which is con-
armyworm, Spodoptera frugiperda (J.E. Smith). cerned with all forms of insect-human interac-
Deception and concealment practices is using tions in so-called primitive societies, is not
lures, trap crops, or polyculturing crops to either completely synonymous with cultural entomol-
decoy or hide a commodity from infestations. Exam- ogy. For example, practical uses of insects such as
ples include placing Japanese beetle, Popillia japon- entomophagy as part of the diet, in pharmacology,
ica Newman, traps in the backyard to help lure adults or in other wholly practical uses of insects, are not
away from landscape plants; using an early maturing the subject matter of cultural entomology. Where
soybean cultivar around the periphery of a soybean primitive societies have employed insects in cul-
field as a trap crop for stinkbugs, Nezara spp.; and tural activities such as art and religion, ethnoento-
companion planting various herbs and aromatic mology and cultural entomology overlap.
plants to hide garden plants from pests.
Cover, Border and Trap Crops for Pest and
Disease Management Reference

Hogue CL (1987) Cultural entomology. Annu Rev Entomol

References 32:18199

All JN (1999) Ruberson JR (ed) Handbook of pest manage-

ment. Marcel Dekker Inc., New York, pp 395415
Rabb RL, (1984) Defoliart GK, Kennedy GG, Huffaker CB, Culture of Natural Enemies on
Rabb RL (eds) (1984) Ecological entomology. Wiley, Factitious Foods and Artificial
New York, pp 697728 Diets
Rajendran B, Pimentel D (ed) (2002) Encyclopedia of pest
management. Marcel Dekker, Inc., New York, 929 pp
Patrick De Clercq
Ghent University, Ghent, Belgium
Cultural Entomology
The use of arthropod predators and parasitoids
Ron Cherry in augmentative biological control programs
University of Florida, Belle Glade, FL, USA necessitates the availability of cost-effective mass
rearing systems, allowing the production of large
Entomology has long been concerned with two numbers of beneficials at the lowest possible
general areas of study. The first is the study of price.
1134
C Culture of Natural Enemies on Factitious Foods and Artificial Diets

In many cases, suppliers of beneficial arthro- of the greater wax moth, Galleria mellonella (for
pods must resort to employing so-called natural several ichneumonid, braconid and tachinid para-
rearing systems. Here, the beneficial is cultured on sitoids and for predatory stink bugs), and of the
its natural host or prey, which itself is maintained yellow mealworm, Tenebrio molitor (e.g., for redu-
on one of its food plants. Natural rearing systems viids and predatory stink bugs). Trichogramma
can be economically viable, like the production of wasps can also be successfully mass produced on
the parasitoid, Encarsia formosa, on tobacco plants eggs of the rice moth, Corcyra cephalonica and a
infested with the greenhouse whitefly, Trialeurodes number of silkworms, such as the Chinese oak
vaporariorum. In many cases, however, the neces- silkworm, Antheraea pernyi. Commercial suppli-
sity to maintain three trophic levels (natural ers routinely use astigmatid mites such as Tyroph-
enemy, host and hosts food plant) leads to prob- agus putrescentiae and Carpoglyphus lactis as prey
lems of discontinuity and the high costs of rearing for culturing a number of phytoseiid mites. Some
facilities and labor result in a high price of the non-insect materials also may hold promise for
natural enemies, making them more expensive use as foods in insect mass culturing. It has been
than chemical controls. Costs may be lowered shown that the anthocorid Orius laevigatus and
when the herbivorous host used for natural enemy the mirid Macrolophus caliginosus can be reared
production can be reared on an artificial diet in on cysts of the brine shrimp, Artemia franciscana,
lieu of plants, which is the case for many lepi- with similar developmental and reproductive suc-
dopteran larvae. cess as on Ephestia kuehniella eggs. Given that
Costs may be further reduced when natural Artemia cysts are at least an order of magnitude
enemies can be produced on unnatural or facti- cheaper than flour moth eggs, they may be an eco-
tious hosts that are easier and less expensive to nomically viable alternative food for the mass
rear than the natural host. Factitious hosts are propagation of these heteropteran predators and
organisms that are not normally attacked by the possibly other predaceous insects.
beneficial, mostly because they do not occur in its The availability of an artificial diet that sup-
natural habitat, but do sustain its development. ports the growth and reproduction of a natural
Eggs of the lepidopterans Ephestia kuehniella and enemy offers a further alternative for the rational-
Sitotroga cerealella, are routinely used in the com- ization and automation of mass rearing proce-
mercial production of various natural enemies dures. Ideally, biochemical analyses of the natural
including coccinellid beetles, lacewings, preda- food along with studies of the digestive and
ceous heteropterans, and egg parasitoids of the absorptive physiology of the insect should be used
genus Trichogramma. Hatching of the eggs is pre- as guidelines for diet definition, but in fact, many
vented by gamma- or UV-irradiation or by freez- successes with artificial diets were based on a
ing. Although these moths are easily produced on mere trial-and-error approach. A nutritionally
inexpensive foods (wheat flour or grains), there adequate artificial diet should contain the basic
are substantial monetary investments for the nutrients (proteins or amino acids, lipids, carbo-
mechanization of rearing procedures and for the hydrates) in appropriate proportions. In addition,
health care of workers (repeated inhalation expo- some specific minor components may be needed
sure to scales is known to cause allergies). Because as growth factors, like sterols, vitamins, minerals
of a continuously high demand, this has led to and nucleic acids. Further, the diet has to be for-
high market prices especially for Ephestia kuehn- mulated and presented in a manner that makes it
iella eggs, amounting to $800 to $1,200 (U.S.) per acceptable for feeding or oviposition. Therefore,
kilogram by the end of the 1990s. Other insects physical properties such as shape, hardness, tex-
that are frequently used as factitious food in com- ture, homogeneity and water content are impor-
mercial insectaries and research labs include larvae tant considerations. Inert filling or gelling agents,
 Culture of Natural Enemies on Factitious Foods and Artificial Diets
C 1135

like agar, cellulose and gelatin, have been used to Promising results have also been obtained with
obtain adequate consistency mainly in diets for artificial diets for hymenopterous egg and pupal
insects with chewing mouthparts. Several materi- parasitoids and for tachinid larval parasitoids.
als have been used to wrap or encapsulate liquid Endoparasitoids (i.e., parasitoids which develop
and semi-liquid media, like paraffin, Parafilm and inside their hosts) are generally more difficult to
certain polymeric coatings. Measures can be taken rear on artificial media than ectoparasitoids or
to prevent spoilage of the food by micro-organisms. predators; for the larvae of endoparasitoids, the
This can be done by adding anti-microbial or diet is not only their food, but also their living
anti-fungal agents (provided they are non-toxic environment. In diets for endoparasitoids, oxygen
to the insect), by adjusting pH or by sterilizing supply, osmotic pressure and pH are major con-
thediet. cerns. The situation is even more complex for
Artificial diets have been classified in three koinobiontic endoparasitoids. These parasitoids
general types: (i) holidic diets, in which all ingre- do not immediately paralyze or kill their hosts,
dients are known in chemical structure, (ii) meridic allowing them to continue to develop for some
diets, which have a holidic base supplemented time after oviposition. As a consequence, the devel-
with one or more unrefined or chemically oping parasitoid larva has strong physiological
unknown substances (e.g., liver extracts, yeast interactions with the still living host, that often
products), and (iii) oligidic diets, which are mainly supplies it with specific growth factors. Finally,
made up of crude organic materials (like meat understanding interactions with microbial symbi-
diets). It is, however, not always easy to discrimi- onts may be the key to success in developing
nate between these three diet types and, in fact, anadequate artificial food for a number of ento-
only a complete description of its composition is mophagous insects.
able to fully characterize an artificial diet. A more The main concern for natural enemies pro-
relevant criterion to categorize a diet is the pres- duced on artificial (or factitious) food is their
ence or absence of insect components. Many quality as biological control agents. Artificially fed
artificial diets still contain host materials to fulfill natural enemies may diverge biologically from
the need for certain growth factors, or to supply their naturally fed counterparts and may have
feeding or oviposition stimuli. Insect additions impaired abilities to find or kill their natural host.
can vary from small quantities of host hemolymph Biological, biochemical, physiological and behav-
to whole host bodies. Supplementing artificial ioral parameters can be used to assess the fitness
diets with insect materials again implies the depen- of an artificially reared beneficial in the laboratory,
dence on parallel host cultures, which may lead to but excellent field performance against the target
an increase in production costs. In some cases, pest remains the ultimate quality criterion. In the
however, insect components are inexpensive and early 1990s, Trichogramma egg parasitoids were
easy to obtain, like the hemolymph from silk- already being produced on artificial eggs at an
worms in the silk-producing areas of Asia and industrial scale in China; the parasitoids were
Latin America. As an alternative to hemolymph or being released on thousands of hectares resulting
host extracts, insect cell cultures have been used in excellent control of different lepidopterous crop
to serve as a source for essential host factors in pests. In the United States and Europe, biocontrol
theartificial rearing of certain parasitoids. companies have also started to integrate artificial
A number of arthropod natural enemies have diets in their production process and some benefi-
been reared with variable success on artificial cials are at least partially being reared on artificial
media. Several predatory heteropterans, chrysopids foods.
and coccinellids have been reared for consecutive Augmentative Biological Control
generations on diets devoid of insect materials. Rearing of Insects
1136
C Cuneus

References Curculionidae

Arijs Y, De Clercq P (2001) Rearing Orius laevigatus on cysts A family of beetles (order Coleoptera). They com-
of the brine shrimp Artemia franciscana. Biol Control monly are known as snout beetles or weevils.
21:7983 Beetles
Cohen AC (2004) Insect diets. Science and technology. CRC
Weevils, Billbugs, Bark Beetles and Others
Press, Boca Raton, FL, 324 pp
Etzel LK, Legner EF, Bellows TS, Fisher TW (eds) (1999) (Coleoptera: Curculionidae)
Handbook of biological control. Academic Press, San
Diego, CA, pp 125197
Grenier S, De Clercq P, van Lenteren JC (eds) (2003) Quality Curculionoid Larva
control and production of biological control agents.
Theory and testing procedures, CABI Publishing, Wall-
ingford, UK, pp 115131 A larval body form that is robust, C-shaped, with a
Thompson SN (1999) Nutrition and culture of entomopha- well-developed head. It is found in the weevils
gous insects. Annu Rev Entomol 44:561592 (Curculionidae) and the first instar of Bruchidae
Waage JK, Carl KP, Mills NJ, Greathead DJ, Singh P, Moore RF
(both Coleoptera).
(eds)(1985) Handbook of insect rearing, vol I. Elsevier,
Amsterdam, The Netherlands, pp 4566

Curran, Charles Howard

Cuneus Howard Curran was born in the province of Ontario,
Canada, on March 20, 1894. He became interested in
In Hemiptera, the small triangular area at the end insects by the age of seven and built a collection, but
of the corium on the hemelytra. In Odonata, the left school at the age of 12. He worked in the news-
small triangular structure (Fig.142) between the paper-publishing business, at first in his fathers
compound eyes. office and later in the province of Saskatchewan. In
1915 he was employed as an assistant in the Domin-
ion Entomology Branch at Vi0neland Station,
Ontario. He went to Europe with Canadian troops
Cupedidae in 1917, served in France in Word War I, was
wounded and invalided out. He returned to Vineland
A family of beetles (order Coleoptera). They com- Station in 19191921, and in 1921 received a B.S.A.
monly are known as reticulated beetles. degree from Ontario Agricultural College (now the
Beetles University of Guelph). At the college, he met C.J.S.

Cuneus, Figure 142 Front wing of a bug (Hemiptera: suborder Heteroptera), thickened basally and
membranous distally.
 Curtonotid Flies
C 1137

Bethune, who encouraged his interest in Syrphidae.

At the annual meeting of the Entomological Society
of America in Toronto in 1921, he was encouraged
to apply for a fellowship at the University of Kansas
for graduate studies. This he did, was successful, and
obtained his M.Sc. degree in 1923 with a thesis on
North America Syrphidae in partial fulfillment of
the requirements. Meanwhile, in 1922, his fathers
firm began printing The Canadian Entomologist. In
19231928, Howard was entomologist in charge of
Diptera and stored products insects, and published
many papers in the pages of The Canadian Ento-
mologist. In 1928 he joined the staff of the American
Museum of Natural History, rose in its ranks, retired
in 1960, and then became Curator Emeritus. He
received a D.Sc. degree from the University of Mon- Curtis, John, Figure 143 John Curtis.
treal in 1933 after a thesis The families and genera
of North American Diptera. His primary entomo- years he developed a talent for drawing, and began
logical contribution was the description of 2,648 to collect butterflies. In 1807, he began to work
taxa in 62 families of Diptera. From the 1940s, he for a solicitor. However, through contact with
undertook much consulting work and his output insect collectors, he found employment as cura-
of publications lessened. After retirement, he tor and illustrator of insects. After some 12 years
moved to Florida and was appointed entomologist he began work on his series of books on British
with the University of Florida Agricultural Experi- entomology, whose first part was published in
ment Station at Leesburg. He died in Leesburg on 1824, with the last, part 16, in 1839. These works
January 23, 1972, survived by his second wife, Ethel, were illustrated by his 769 magnificent color
and three children. plates. He also (1829) published A guide to an
arrangement of British insects. In 1841 he
became editor of the insect part of Gardeners
Reference Chronicle and wrote over 100 articles for it,
under the pseudonym Ruricola. He died on
Arnaud PH, Owen TC (1981) Charles Howard Curran (1894 October 6, 1862, in London.
1972). Myxia 2:120

Reference
Cursorial
Herman LH (2001) Curtis (Ruricola), John. Bull Am Mus Nat
Adapted for running. This term is used to describe Hist 265:5658
legs adapted for running.

Curtonotid Flies
Curtis, John
Members of the family Curtonotidae (order
John Curtis (Fig.143) was born in Norwich, Eng- Diptera).
land, on September 3, 1791. During his school Flies
1138
C Curtonotidae

Curtonotidae the epicuticle and epidermis are always present.

During molting, the inner layers of the new
A family of flies (order Diptera). They commonly cuticle (the future exocuticle and endocuticle)
are known as curtonotid flies. are not sclerotized into distinct layers, and is
Flies called the procuticle, but this is a temporary
condition.
Juvenile Hormone
Cushman, Robert Asa

Robert Cushman was born in Massachusetts on Cuticulin

November 6, 1880. He studied at the University of
New Hampshire and at Cornell University. In 1906 The very thin outer layer of the epicuticle. Cuticu-
he was employed by the U.S. Department of Agri- lin is a tough, insoluble and inelastic layer of cross-
culture and worked in part on applied entomology linked protein and lipid molecules.
(boll weevil, pests of fruits, pests of grapes) and on
taxonomy (ichneumonid and chalcidid wasps). He
was active in the Entomological Society of Wash- Cutworm
ington, and its president in 1925. He died in Cali-
fornia on March 25, 1957. Any of a number of caterpillars in the family Noc-
tuidae that hide in the soil, feeding there or emerg-
ing at night to feed on foliage or seedlings.
Reference Potato Pests and their Management
Vegetable Pests and their Management
*Mallis A (1971)American entomologists. Rutgers University Maize (Corn) Pests and their Management
Press, New Brunswick, NJ, pp 372373

Cutworm Moths
Cuticular Lipids
Members of the family Noctuidae (order
Lipids comprise an important component of the Lepidoptera).
cuticle of insects. Owlet Moths
Metabolism of Cuticular Lipids Butterflies and Moths

Cuticle Cuvier, (Baron) Georges Lopold

Chretien Frdric Dagobert
The noncellular outer layer of the integument,
which is the outer covering of an insect. The Georges Cuvier was born in Montbliard, at that
cuticle serves as the exoskeleton, the site for time in Wrttemberg (later absorbed into France,
muscle attachment and a barrier against preda- and now in Germany) on August 23, 1769. He was
tion, parasitism, and infection by pathogens. The therefore born a Wrttemberger and became
cuticle consists of several layers, including the French. Actually, he was christened Jean Lopold
epicuticle, exocuticle, and endocuticle (Fig.144). Nicolas Frdric Cuvier, but after the early death
The exocuticle or endocuticle may be reduced of his elder brother, Georges, he was renamed
oreven absent on some parts of the insect, but Georges. He studied theology and anatomy in
 Cycloalexy
C 1139

Epicuticle
Exocuticle
Pore canal
Endocuticle
Schmidts
layer
Epidermis
Basement
membrane

Cuticle, Figure 144 Cross section of the insect cuticle and epidermis (adapted from Chapman, The
insects: structure and function).

Stuttgart. In 1795 he moved to Paris and was Cyclical Polymorphism

employed as assistant in comparative anatomy at
the Jardin des Plantes (later known as Musum A complex life cycle characterized by the occur-
National d Histoire Naturelle). Much later he rence of several to many morphs. Many morphs
became professor at the Collge de France and are seasonally related, and are most clearly mani-
chancellor of the Universit de Paris. His contri- fested in aphids, which produce various forms of
butions to entomology consisted of his first small winged and wingless, a nd asexual and sexually
publications, and the entomological part of his reproducing forms, over the course of a season.
(17991805) work Leons d anatomie compare. Aphids
The entomological part of his (1816) book Rgne Polyphenism
animal was written not by him, but by Latreille. Polyphenism and Juvenile Hormone (JH)
He had great influence on zoological anatomy, Phenotypic Plasticity
but little directly on entomology. Much of his
influence, however, was by his stance that animal
species are immutable they do not evolve. Thus, Cyclidiidae
his ideas contrast with those of Lamarck, who
believed that evolution does take place, but by A family of moths (order Lepidoptera) also known
heredity of acquired characters. They contrast as giant hooktip moths.
just as much with the later ideas of Charles Dar- Giant Hooktip Moths
win about evolution. Cuviers ideas were adopted Butterflies and Moths
by Louis Agassiz (see above). He was made grand
officer of Frances Legion d Honneur in 1826.
He was made a peer of France (Baron) in 1831 by Cycloalexy
the king Louis Philippe. He died in France on
May 13, 1832. Pierre Jolivet
Paris, France

Reference Cycloalexy is a form of gregarism, and involves

group reactions. The name is derived from the Greek
Tuxen, SL (1973) Smith RT, Mittler TE, Smith CN (eds) His-
kuklos=circle and alexo=I defend, I protect. It is
tory of Entomology. Annual Reviews Inc., Palo Alto, CA, the attitude adopted at rest by some insect larvae,
pp 95117 both diurnal and nocturnal, in a tight circle when
1140
C Cyclo-Developmental Transmission

either the heads or ends of the abdomen are juxta- (Fig.145). Also, reciprocal altruism may take place
posed at the periphery, with the remaining larvae at when the inner and outer larvae exchange positions.
the center of the circle. It can also be namedthe ring However, this interpretation has been challenged. In
defense behavior. Coordinated movements such as Australian sawflies in the genus Perga (Perga dorsalis
the adoption of threatening attitudes, regurgitation, Leach), some 20% of the larvae preferentially occupy
reflex bleeding and biting are used to repel predators the outer positions in the resting colony and appear
or parasitoids. If for anyreason, the circle is broken, to lead the foraging expeditions. Leaders are quick to
ants or pentatomids can easily catch some larvae. regain outer positions if removed and placed in the
The system is more efficient against predators than center of the colony. So there seem to be differences
against parasitoids that have all found a way to turn in the dispersal behavior of larvae in time and space.
the defense. Cycloalexy has analogy in vertebrates, Small colonies of larvae sometimes show
penguins and muskoxen, for instance, living in non-viability (e.g., pergids). However, when larvae
familial groupsand sometimes adopting a circular of Coelomera spp. (Coleoptera: Chrysomelidae)
formation of males protecting the young and females on a leaf of a Cecropia tree are divided into two or
from potential predators. Cycloalexy is mainly known three subgroups, those groups seem as efficient as
among Coleoptera: Chrysomelidae, (Cassidinae, big ones in repelling predators.
Chrysomelinae, Criocerinae), Coleoptera: Curculioni- Gregarious Behavior in Insects
dae, sawflies, and several other insect orders (Diptera,
Ceratopogonidae, Neuroptera, Lepidoptera, etc.).
References
Generally, the individuals in a colony disperse
to feed upon foliage by night (or by day when they
Jolivet P, Vasconcellos-Neto J, Weinstein P (1990) Cycloalexy:
rest during the night), one behind the other, to a new concept in the larval defense of insects. Insecta
reaggregate before dawn. In Pergidae, to reaggre- Mundi 4:133141
gate the larvae communicate by means of low fre- Vasconcellos-Neto J, Jolivet P (1988) Une nouvelle stratgie
de dfense: la stratgie de dfense annulaire (cycloalexie)
quency vibrations created by tapping the uropod chez quelques larves de Chrysomlides brsiliens. Bul-
upon the substrate. Paropsine (Coleoptera: Chry- letin Societ Entomologique France 92:291299
somelidae) larvae in Australia also tap the substrate Vasconcellos-Neto J, Jolivet P (1989) Ring defense strategy
with the abdomen to reunite the dispersed colony. (cycloalexy) among Brazilian chrysomelid larvae (Col.).
Entomography 67:347354
All the insects demonstrating cycloalexy are sub- Verma KK (1996) Cycloalexy in leaf-beetles (Col. Chrys.).
social in the larval stage and also often exhibit Insect Environ 2:8284
maternal care of eggs and larvae. Some cycloalexic Weinstein P (1989) Cycloalexy in an Australian pergid sawfly
(Hym. Pergidae). Bull R Belg Entomol Soc 125:5360
leaf beetles like Platyphora in Brazil are viviparous.
Weinstein P, Maelzer DA (1997) Leadership behaviour in
When dropped one by one by the mother, the sawfly larvae, Perga dorsalis. Oikos 79:450455
larvae congregate immediately.
Cycloalexy, like maternal care, can only be the
result of a long evolutionary history. The behavior Cyclo-Developmental
efficiently protects the larvae during their most Transmission
vulnerable periods (at rest, during molting). How-
ever, the defense is not always perfect. Trigonalyid Transmission of an arthropod transmitted disease
parasitoids have succeeded in having their eggs wherein the causal organism undergoes cyclical
swallowed by the sawfly larvae, thus obviating the changes but does not multiply in the body of the
need to confront the defensive ring. arthropod vector.
Younger larvae sometimes seem to be protected Mechanical Transmission
inside the circle, and this could be interpreted as Cyclo-Propagative Transmission, and
altruism on the part of the larvae at the periphery Propagative Transmission
 Cyclo-Developmental Transmission
C 1141

Cycloalexy, Figure 145 Cycloalexy:(a) Third instar of Platyphora conviva Stl, 1858 (Coleoptera:
Chrysomelinae). Rupture of the cycloalexic ring and predation by a bug of one larva. (photo
J.Vasconcellos-Neto, 1986.) Itatiaia National Park, RJ, Brazil. (b) Eggs of Coelomera lanio Dalman
Coleoptera: Galerucinae), laid on the underside of the folioles of Cecropia adenopus (Cecropiaceae).
The newly hatched larvae will aggregate. (photo Jolivet, 1990.) Viosa, MG, Brazil. (c) First instar larvae
of Coelomera lanio Dalman (Coleoptera: Galerucina). Cycloalexic ring. (photo Jolivet, 1990.) Viosa,
MG, Brazil. (d) Second instar larvae of Coelomera lanio Dalman (Coleoptera: Galerucinae), on a leaf of
Cecropia adenopus. The ring has been doubled. (photo Jolivet, 1990.) Viosa, MG, Brazil. (e) Third instar of
Coelomera lanio Dalman (Coleoptera: Galerucinae), on a leaf of Cecropia adenopus. The cycloalexic ring is
near to be broken and the larvae to go feeding (Coleoptera: Galerucinae). (photo Jolivet, 1990.) Viosa,
MG, Brazil. (f) Cycloalexic ring of Platyphora conviva Stl (Coleoptera: Chrysomelinae). First instar. The
larvae have covered themselves with the hair of the underside of the leaves for extra protection. (photo
J. Vasconcellos-Neto, 1986.) Itatiaia National Park, RJ, Brazil.
1142
C Cyclo-Propagative Transmission

Cyclo-Propagative Transmission Cyphoderidae

Transmission of an arthropod transmitted disease A family of springtails in the order Collembola.
wherein the causal organism undergoes cyclical Springtails
changes and multiplies in the body of the arthro-
pod vector.
Mechanical Transmission Cypselosomatid Flies
Cyclo-Developmental Transmission, and
Propagative Transmission Members of the family Cypselosomatidae (order
Diptera).
Cyclorrhapha Flies

A term sometimes applied to the higher flies (Dip-

tera), usually treated as an infraorder, and also Cypselosomatidae
known as Muscamorpha. The cyclorrhaphous Dip-
tera differ from the other (lower) flies in that pupa- A family of flies (order Diptera). They commonly
tion and the formation of the adult form occur are known as cypselosomatid flies.
within the old, hardened third instar cuticle. Flies
Flies (Diptera)

Cyclotornidae Cyrtocoridae
A family of moths (order Lepidoptera) also known A small family of bugs in the order Hemiptera,
as Australian parasite moths. suborder Heteroptera. It is treated by some as a
Australian Parasite Moths subfamily of Pentatomidae.
Butterflies and Moths Bugs

Cydnidae
Cystocyte
A family of moths (order Hemiptera). They some-
times are called burrower bugs. A type of hemocyte, also known as coagulocytes,
Bugs that participates in the coagulation process of
hemolymph.
Cylindrical Bark Beetles Hemocytes of Insects: their Morphology and
Function
Members of the family Colydiidae (order Coleoptera).
Beetles
Cytochrome
Cymidae
The complex protein respiratory enzymes occur-
A family of bugs (order Hemiptera, suborder ring within plant and animal cells in the mito-
Pentamorpha). chondria, where they function as electron carriers
Bugs in biological oxidation.
 Cytosol
C 1143

Cytoplasm Cytoplasmic Polyhedrosis Virus

The fluid components of the cell, outside the An RNA virus associated with inclusion bodies
nucleus. found in cytoplasm of cells.

Cytoplasmic Incompatibility
Cytosol
Reproductive incompatibility between two popu-
lations caused by factors that are present in the The fluid portion of the cytoplasm, excluding the
cytoplasm. Often associated with microorganisms. organelles in a cell.
D

Dactyl Dahlbom, Anders Gustav

A tarsal segment, after the first segment, that Anders Dahlbom was born in Ostgothland,
is expanded and finger-like in appearance. The Sweden, on March 3, 1806. He studied in Lund
dactyls on the front legs of mole crickets and earned a doctorate in philosophy in 1829.
(Orthoptera: Gryllotalpidae) are an adaptation Then he became an instructor in natural history
that facilitates the insect burrowing, mole-like, and preparator in the zoological museum in Lund
though the soil. in 1830. Three promotions made him professor of
Mole Crickets and their Biological Control entomology in Lund in 1858. He explored his
Grasshoppers, Katydids and Crickets native Sweden to collect zoological specimens
and also traveled abroad to Germany and Denmark,
and there visited museums. He married Wilhelmine
Krey, and they had six children. His area of
research was the taxonomy of Hymenoptera.
Dactylopiidae
His first two publications appeared in 1829, and
were monographs on pompilid wasps and chry-
A family of insects in the superfamily Coccoidae
sidid wasps. For almost 30 years he maintained an
(order Hemiptera). They sometimes are called
output of books and papers on Hymenoptera
cochineal insects.
while maintaining correspondence with entomol-
Bugs
ogists in his own country and in Britain, France,
and Germany. He died in Lund on May 6, 1859.

Daddy Long-Legs Reference

Anon (1859) Nekrolog Entomol Ztg (Stettin) 20:337340

This term is applied to several arthropods, princi-
pally craneflies (Diptera: Tipulidae), spider-like
harvestmen (Arachnida: Opiliones or Phalang- Dalceridae
ida), and several true spiders in the family Pholci-
dae (Arachnida: Aranea), but most often Pholcus A family of moths (order Lepidoptera). They com-
phalangioides. What they all have in common is monly are known as tropical slug caterpillar moths.
that they have long, slender legs; otherwise, they Tropical Slug Caterpillar Moths
are not closely related. Butterflies and Moths
1146
D Dampwood Termites

Dampwood Termites Order: Diptera

Superfamily: Empidoidea (exclusive of Dolichopo-
A group of termites in the families Kalotermitidae didae)
and Rhinotermitidae that are known to attack Family: Empididae
moist dead wood. Subfamily: Empidinae
Termites Subfamily: Hemerodromiinae
Subfamily: Clinocerinae
Family: Atelestidae
Damsel Bugs Subfamily: Nemedininae
Subfamily: Atelestinae
Members of the family Nabidae (order Family: Hybotidae
Hemiptera). Subfamily: Trichininae
Bugs Subfamily: Ocydromiinae
Subfamily: Oedaleinae
Subfamily: Tachydromiinae
Damselflies Subfamily: Hybotinae
Family: Brachystomatidae
Certain members (suborder Zygoptera) of an Subfamily: Trichopezinae
order of insects (order Odonata). Subfamily: Ceratomerinae
Dragonflies and Damselflies Subfamily: Brachystomatinae
Together these families include nearly 4,500
described species worldwide and comprise a
Dance Flies, Balloon Flies, morphologically diverse array of taxa, although
Predaceous Flies (Diptera: Homalocnemis, Iteaphila, Anthepiscopus and
Empidoidea, Exclusive of Oreogeton are still unplaced to family within this
Dolichopodidae) classification. The vast majority of species are
predators as adults with the few exceptions being
jeffrey m. cumming1, bradley j. sinclair2 obligate flower-feeding groups that consume pol-
1
Agriculture and Agri-Food Canada, Ottawa, ON, len as their only protein source. They are found in
Canada a variety of forested and open habitats where they
2
Canadian Food Inspection Agency, Ottawa, ON, breed in moist soils, decaying wood, dung, and in
Canada aquatic habitats. All known larvae appear to be
predators on invertebrates.
The dance flies, balloon flies and other preda-
ceous flies that have traditionally been placed in
the family Empididae are now classified in four Distinguishing Characters
families of Empidoidea along with the long-
legged flies of the family Dolichopodidae. With Most adult Empidoidea (exclusive of Dolichopo-
approximately 11,400 described species and didae) can be easily differentiated from the very
many more undescribed species, the Empidoidea similar Dolichopodidae by their lack of green
are one of the largest superfamilies of Diptera metallic body coloration. However a few non-
and the most diverse lineage of predaceous flies. dolichopodid Empidoidea (e.g., most Lamprempis)
The four families that were formerly classified as are metallic green and some dolichopodids are
the single family Empididae are listed below with not metallic. However, all Dolichopodidae have
their included subfamilies. the Rs wing vein originating at or near the level of
 Dance Flies, Balloon Flies, Predaceous Flies (Diptera: Empidoidea, Exclusive of Dolichopodidae)
D 1147

crossvein h and have crossvein r-m situated in the a one-segmented palpus, and a labrum that is usu-
basal fourth of the wing, unlike other Empidoidea ally armed at the apex with paired epipharyngeal
that have the Rs vein originating well distal to the blades. The chaetotaxy (bristling) of the head is
level of crossvein h and have crossvein r-m distal limited, and usually includes a pair of ocellar bris-
to the basal fourth of the wing. In addition, male tles, postoculars, and sometimes additional verti-
dolichopodids have their terminalia rotated for- cal bristles.
ward beneath the preceding segments of the abdo- The thorax is generally rectangular in dorsal
men, unlike other empidoids. Some bee flies outline and is extended anteriorly in some groups.
(Bombyliidae) and asiloid groups (e.g., therevids The mesonotum is nearly flat to greatly arched
sensu lato) can also be confused with non- and dome-like. The chaetotaxy of the thorax
dolichopodid Empidoidea, but these flies gener- includes notopleurals and scutellars, and various
ally have a larger anal (cup) cell that reaches, or other dorsal bristles depending upon the group,
nearly reaches, the margin of the wing and they and the acrostichal and dorsocentral setae tend
lack any predaceous modifications on either the to be differentiated. The wings are of varied shape
legs or mouthparts. A few platypezid cyclor- and size, sometimes broadened, sometimes nar-
rhaphan flies (e.g., Microsania) can also be con- rowed, rarely reduced, with the alula and anal
fused with non-dolichopodid Empidoidea, but lobe often lacking. The wing color varies from
their arista is comprised of three articles rather clear to darkened, and is seldom patterned with
than two, and the acrostichal setae are uniserial markings. The wing venation is exceedingly var-
rather than biserial or absent. ied from relatively complete to markedly reduced.
The anal cell is closed and never reaches the wing
margin. The legs are varied in length, thickness
Morphology Adults and armature, and often at least one pair bears
raptorial modifications. The legs are sometimes
Adult Empidoidea (exclusive of Dolichopodidae) sexually dimorphic, with rows of pinnate bristles
are small to medium-sized flies (112 mm) that in females and clasping or glandular structures
are darkish to light in color and are rarely metallic in males. The empodium between the claws is
green (Fig. 1). The head is variously shaped, but is usually setiform, but is pulvilliform in some
not large and is usually narrower than the thorax. aquatic groups.
The compound eyes are generally large, with the The abdomen is subcylindrical and usually
males often holoptic (i.e., eyes meeting above in elongate, with at least some tergites bearing
the middle of the head) and the females dichoptic abdominal plaques. The male terminalia are either
(i.e., eyes separated). However in some groups unrotated or twisted 4590 to the right. The male
the males are dichoptic, and in one major lineage genital capsule is symmetric or asymmetric and
(the Hybotinae) the females are also holoptic like has a lever-like ejaculatory apodeme that usually
the males. The antenna consists of a scape, pedi- articulates ventrally against the base of the phal-
cel, postpedicel (1st flagellomere) and a stylus. lus. The female terminalia are with or without
The pedicel is usually without the thumb-like spine-bearing acanthophorites and there is one
conus seen in most cyclorrhaphan flies that inserts spermatheca internally.
into the postpedicel. The postpedicel appears as a The family Empididae (Fig. 1a) includes small
single article that is variously shaped. The stylus is to relatively large flies (212 mm in length) that
usually comprised of two articles, is short to elon- usually have fairly complete wing venation, with
gate, and is either apical or more dorsally situ- vein R4+5 often forked and cell dm usually present.
ated on the postpedicel, such that it appears The prosternum is enlarged to form a precoxal
arista-like. The proboscis is short to elongate, with bridge and the legs are usually strong, long and
1148
D Dance Flies, Balloon Flies, Predaceous Flies (Diptera: Empidoidea, Exclusive of Dolichopodidae)

Dance Flies, Balloon Flies, Predaceous Flies (Diptera: Empidoidea, Exclusive of Dolichopodidae), Figure 1
Representative Empidoidea (a) Empis aerobatica (Empididae); left male, right female, center balloon
with prey (a midge) attached, USA (photograph by Eric Fisher); (b) Acarteroptera licina
(Atelestidae); female feeding on flower, Chile (photograph by Stephen Marshall); (c) Platypalpus
holosericus (Hybotidae), female, Canada (photograph by Stephen Marshall); (d) Ceratomerus sp. (virgatus
group) (Brachystomatidae), female, New Zealand (photograph by Stephen Marshall).

slender without a fore tibial gland. The male ter- The family Hybotidae (Fig. 1c) includes very
minalia are unrotated and the cerci are often small to medium-sized flies (19 mm) that gener-
enlarged and developed for clasping. The female ally have reduced venation, with vein R4+5
abdomen is telescopic and pointed apically, and unbranched and cell dm often absent. Usually at
lacks acanthophorite spines on tergite 10. least one set of legs (fore, mid, or hind depending
The Atelestidae (Fig. 1b) are small flies (24 on the group) is raptorial and a fore tibial gland is
mm) with venation characterized by an unbranched present. The male terminalia are normally twisted
vein R4+5 and a relatively long anal cell. They lack 4590 to the right and are often asymmetric. The
predaceous modifications on the mouthparts (i.e., female abdomen is telescopic and lacks acan-
epiphyngeal blades) and the legs are not raptorial. thophorite spines on tergite 10.
The fore tibial gland is also lacking. The male The Brachystomatidae (Fig. 1d) are small to
terminalia are unrotated and the gonocoxal apo- relatively large flies (211 mm) that tend to have
demes are distinctively elongated. The female fairly complete wing venation, with vein R4+5 often
abdomen is telescopic and lacks tergite 10. forked and cell dm always present. The legs are
 Dance Flies, Balloon Flies, Predaceous Flies (Diptera: Empidoidea, Exclusive of Dolichopodidae)
D 1149

usually strong, long and slender and lack a fore spines along the dorsal surface of each abdominal
tibial gland. The male terminalia are unrotated segment with the terminal segment ending in a
(asymmetrically twisted to the left in some Tricho- pair of strong hooks.
pezinae), and the ejaculatory apodeme is plate-like
and narrowly fused to the base of the phallus. The
female abdomen is truncate, and usually bears a Ecology
fringe of setae along the posterior margin of tergite
7 as well as acanthophorite spines on tergite 10. The Empidoidea (exclusive of Dolichopodidae)
represent a large group of predaceous flies, includ-
ing a few flower-visiting species. They are often
Morphology Immatures found in various forest habitats, on leaves, tree
trunks, damp depressions and aquatic vegetation,
The immature stages of all Empidoidea are poorly and are a dominant component of running water
known, but larvae are generally maggot-like with habitats such as streams and seeps. However, some
reduced head sclerites and a unique mandible taxa are associated with more open areas such as
made up of four to six components. Non- agricultural fields, grasslands, marshes, coastal
dolichopodid empidoid immatures are known for zones and beaches. Many groups exploit a variety
relatively few groups, but for those that are known of habitats for completion of their life cycles, using
the larvae possess either an amphipneustic, metap- different sites for larval development, swarming
neustic, or apneustic respiratory system depend- and mating, and adult feeding. Adults capture
ing on the taxon. Prolegs are generally present on various arthropod prey, including small to medium-
some abdominal segments of aquatic or semi- sized Diptera, Hemiptera, Thysanoptera, Lepi-
aquatic groups, whereas creeping welts tend to be doptera, Trichoptera, Hymenoptera, Neuroptera,
present on the abdominal segments of more ter- Ephemeroptera, Plecoptera, Coleoptera, Collem-
restrial taxa. bola, and Acari. Because of their vast species
Unlike Dolichopodidae, most other empidoid diversity and wide habitat range, predaceous
larvae do not appear to spin a cocoon before empidoid flies are important natural and poten-
pupating. There is a single report of a cocoon hav- tial biological control agents of various pest
ing been spun by a larva of a species of Drapetis insects.
(Tachydromiinae). However, no cocoon was spun A number of adult non-dolichopodid Empi-
by a larva in the related genus Megagrapha that doidea also visit flowers (Fig. 1b), presumably in
was observed pupating, suggesting that cocoon most cases to obtain nectar, but at least a few
production is not common to all Tachydromiinae groups (e.g., Iteaphila, Anthepiscopus, Anthalia,
as has been speculated. Allanthalia and Euthyneura) obtain all their pro-
Non-dolichopodid empidoid pupae vary con- tein requirements by feeding on pollen.
siderably depending on the genus and the habitat Larvae are generally found in damp soil, rot-
they occupy. Some genera (Drapetis, Megagrapha) ten wood, dung, running water, seeps and tidal
possess a pair of lengthened anterior respiratory zones, depending on the group. They appear to be
organs that arise from the anterior dorsal surface predaceous on various arthropods, particularly
of the thorax, whereas others (Hemerodromia, other Diptera larvae.
Chelifera) possess lengthened lateral abdominal As a group, Empidoidea have the potential to
respiratory processes; Neoplasta has both types of be useful bioindicators for conservation pro-
lengthened respiratory processes. Several aquatic grams and for site quality assessment. Fifteen
genera (Oreogeton, Hemerodromia, Clinocera, species of non-dolichopodid Empidoidea have
Roederiodes, Wiedemannia) have relatively stout been listed in the Red Data Book as critically
1150
D Dance Flies, Balloon Flies, Predaceous Flies (Diptera: Empidoidea, Exclusive of Dolichopodidae)

endangered, endangered or vulnerable in Great Diversity, Evolution and

Britain, whereas 33 species have been listed for Distribution
Northern Belgium. Due to their predominantly
predaceous habits, they are normally not consid- The Empidoidea (exclusive of Dolichopodidae)
ered to be threatened unless their breeding are worldwide in distribution and comprise
biotopes or microhabitats are endangered. approximately 4,500 species classified in over 160
genera. In addition, numerous fossil genera and
species have been described from several Meso-
Mating Behavior zoic and Tertiary deposits, particularly in amber
inclusions from Lebanon, Spain, New Jersey,
Many species of non-dolichopodid Empidoidea Myanmar (Burma), Siberia, Canada, the Baltic
mate on the ground or on vegetation (e.g., Region, Dominican Republic and Mexico. In
Hemerodromiinae, Clinocerinae, Tachydromii- terms of generic diversity, the entire group is
nae and Hybotinae) while others gather in aerial richest in western North America, southern
mating swarms (Atelestinae, Ocydromiinae, Africa, New Zealand and southern South
most Empidinae, and many Trichopezinae). The America. This is also reflected in species diver-
synchronized movement of adult flies within sity, where non-dolichopodid Empidoidea are
these mating swarms is the basis for the com- seemingly more diverse in temperate rather than
mon name dance flies. In a few genera, such as tropical regions.
Trichina (Trichininae), Oedalea (Oedaleinae) The Empididae are a large family of well over
and Bicellaria (Hybotinae), aerial aggregations 2,000 described species worldwide that include
have been observed even though mating appar- the Empidinae, Hemerodromiinae, and Clinoceri-
ently takes place on the ground. These aerial nae, as well as the Ragas group, Hesperempis group,
aggregations that occur without mating have Philetus and Brochella. The monophyly of this
been termed relict swarms. diverse heterogeneous family is still somewhat
Members of one large subfamily, the uncertain. The immature stages of Clinocerinae
Empidinae, transfer nuptial gifts from male to and most Hemerodromiinae are aquatic whereas
female during courtship and mating. Depending the immature stages of the other groups are pri-
on the species, these nuptial gifts include prey, marily terrestrial.
various types of inedible objects, and/or secreted The Atelestidae are a small distinctive family
balloons (Fig. 1a), which is why the entire group of nine extant species that are classified in four
is sometimes referred to as balloon flies. Within genera. The Palaearctic genus Nemedina is assigned
the Empidinae mate choice is generally made by to its own subfamily Nemedininae whereas the
females that visit male-dominated swarms. Males other genera Atelestus (Palaearctic), Meghyperus
in these species compete for females using these (Holarctic) and Acarteroptera (Chilean) belong
nuptial gifts, often enhanced with various to the Atelestinae. The immature stages of
secondary sexual characters. However, many Atelestidae are unknown, but are believed to be
species of Empidinae exhibit sex-role reversed terrestrial.
courtship behavior where females gather in The Hybotidae are a diverse family of approxi-
swarms to await males that choose their mates. mately 2,000 described species currently classified
Females of these species exhibit many different into five subfamilies, namely the Trichininae,
secondary sexual characters used in courting Ocydromiinae, Oedaleinae, Tachydromiinae, and
males, such as enlarged wings, pinnate leg scales, Hybotinae. The family is well defined by several
eversible abdominal pleural sacs and silvery synapomorphies and its monophyly is not in doubt.
abdomens. All of the included subfamilies are virtually
 Darkling Beetles (Coleoptera: Tenebrionidae)
D 1151

c osmopolitan in distribution, except for Trichini- Dark Mealworm, Tenebrio

nae andOedaleinae, which are essentially Holarc- obscurus Fabricius (Coleoptera:
tic. The entire family is terrestrial and many species Tenebrionidae)
are found in some of the driest habitats occupied
by empidoid flies. This is a stored grain insect, and very similar to the
The Brachystomatidae are a moderate-sized more common yellow mealworm, Tenebrio moli-
family of about 150 described species worldwide. tor Linnaeus.
The family includes the nearly cosmopolitan Stored Grain and Flour Insects
Trichopezinae with 14 recognized genera, the Darkling Beetles
Southern Hemisphere Ceratomerinae with three
currently recognized genera, and the primarily
Holarctic Brachystomatinae with three genera. Darkling Beetles (Coleoptera:
The monophyly of this morphologically diverse Tenebrionidae)
family is based primarily on synapomorphies
associated with modifications of the female ter- charles a. triplehorn
minalia. Based on limited information obtained The Ohio State University, Columbus, OH, USA
from rearing records and habitats occupied by
adults, the immature stages of Brachystomatidae The family Tenebrionidae belongs to the suborder
are believed to include both terrestrial and aquatic Polyphaga of the order Coleoptera (beetles). The
representatives. superfamily Tenebrionoidea includes the families
Flies Anthicidae, Colydiidae, Melandryidae, Monomi-
dae, Salpingidae, Mycetophagidae, Tetratomidae,
Mordellidae, Rhipiphoridae, Prostomidae, Syn-
References chroidae, Oedemeridae, Stenotrechelidae,
Meloidae, Mycteridae, Ciidae, Boridae, Pythidae,
Chvla M (1983) The Empidoidea (Diptera) of Fennoscandia Aderidae, Scraptiidae, Archeocrypticidae, and
and Denmark. II. General Part. The families Hybotidae, Zopheridae, as well as the large family
Atelestidae and Microphoridae. Fauna Entomol Scand Tenebrionidae.
12:1279
Collin JE (1961) Empididae. British flies, vol 6. University Order: Coleoptera
Press Cambridge, UK, 782 pp Suborder: Polyphaga
Cumming JM (1994) Sexual selection and the evolution of Superfamily: Tenebrionoidea
dance fly mating systems (Diptera: Empididae; Empidi-
Family: Tenebrionidae
nae). Can Entomol 126:907920
Cumming JM, Sinclair BJ (2007) Family Empididae. In: Brown Tenebrionidae are the fifth largest family of
BV, Borkent A, Cumming JM, Wood DM, Woodley Coleoptera with 14,641 species worldwide and
NE, Zumbado M (eds) Manual of Central American 1,345 occurring in the United States. These num-
Diptera, vol 1. NRC Research Press, Ottawa, Canada (in
press)
bers are low since in the past three decades, many
Sinclair BJ, Cumming JM (2006) The morphology, higher- changes have been made in the classification of
level phylogeny and classification of the Empidoidea the family and many new taxa have been described.
(Diptera). Zootaxa 1180:1172 The Zopheridae and Archeocrypticidae have been
Smith KGV (1969) The Empididae of southern Africa (Dip-
tera). Annals Natal Mus 19:1342 removed and given family status, and the former
Steyskal GC, Knutson LV (1981) Chapter 47. Empididae. In: families Alleculidae and Lagriidae are now con-
McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, sidered subfamilies within Tenebrionidae. Adding
Vockeroth JR, Wood DM (eds) Manual of Nearctic
species from those two groups raises the total
Diptera, vol 1. Agriculture Canada Monograph 27,
Biosystematics Research Institute, Ottawa, Canada, world species to 16,267 with 1,540 in the United
674 pp States. The current classification recognizes twelve
1152
D Darkling Beetles (Coleoptera: Tenebrionidae)

subfamilies worldwide, eleven of which occur in their resemblance to the larvae of Elateridae which
the United States. are known as wireworms. Both do similar damage
Tenebrionidae is one of the most highly to underground portions of plants. The most con-
evolved and diverse families of Tenebrionoidea spicuous difference between them is that tenebri-
and, indeed, in the order Coleoptera itself. It is a onid larvae have a less flattened head and unfused
difficult group to characterize because of the labrum. Larvae of elaterids usually have the labrum
many exceptions that exist in most characters. absent or fused with the clypeus, forming a median
Discounting the exceptions, the following com- sclerotized projection called anasale.
bination of morphological characters separate
adult tenebrionids from other Tenebrionoidea:
tarsal formula 5-5-4; procoxal cavities closed; Habitats
antennae eleven-segmented and inserted under
lateral expansion of the genae; abdomen with There are few macrohabits from which tenebrion-
basal three visible sterna connate, 4 and 5 ids are excluded. In the deserts of the world, they
movable. are among the most conspicuous occupants, some-
times occurring in enormous numbers. All of
them have evolved remarkable water conserving
Adults mechanisms, and survive principally on metabolic
water derived from their foods. Essentially all of
The length of adult tenebrionids ranges from these desert dwellers lack metathoracic wings and
slightly more than one to more than 60 mm. While are therefore flightless. The elytra usually are fused,
the popular concept of the family is somber color- forming a subelytral cavity, and the integument is
ation (shades of black or brown), there are some thick, both factors helping to control water loss
(i.e., Strongylium, Cuphotes, Poecilisthus, Pla- through the spiracles.
tydema) that are vividly colored. There are many Desert tenebrionids escape the extreme day-
species in a number of different subfamilies which time temperatures of arid regions by hiding under
lack metathoracic wings (sometimes there are debris or in mammal burrows, venturing out only
apterous and alate members within the same at dusk. They are probably not truly nocturnal but
genus, and occasionally even within a population opportunists, taking advantage of cooler night-
of a single species (i.e., Blapstinus). The elytra usu- time temperatures. The experienced darkling bee-
ally completely cover the abdomen but in some tle collector works mostly atnight.
(i.e., Corticeus, Phaleria) the pygidium is exposed. At the other extreme are many genera, rich
in species, which inhabit moist environments
throughout the world. Genera such as Strongylium,
Immature Stages Helops, Tarpela and Statira are almost entirely
confined to tropical and subtropical regions and
Tenebrionid larvae are usually elateroid (wireworm- are more diurnally active.
like) or C-shaped, elongate and cylindrical, 540 Several genera in the tribe Phaleriinae (e.g.,
mm in length, hard-bodied, with five-segmented Phaleria, Chaerodes) are found only on ocean
thoracic legs. The head is exserted with a frontocly- beaches where they congregate beneath organic
peal suture present. The apical abdominal segment debris. There are a number of interesting rela-
is usually rounded or triangular, urogomphi, con- tionships between tenebrionids and other insects.
cave plates, or other armature present or absent. Members of the genus Corticeus inhabit the gal-
The larvae of some tenebrionids (e.g., Eleodes) leries of bark beetles (Scolytinae) and others (e.g.,
are sometimes called false wireworms because of Araeoschizus, Bycrea) occur in ant nests.
 Darlington, Jr., Philip J
D 1153

Many species are subcortical but usually Doyen JT, Lawrence JF (1979) Relationships and higher clas-
sification of some Tenebrionidae and Zopheridae
occur under bark of a number of tree species.
(Coleoptera). Syst Entomol 4:333377
There are few that are host specific and none are Doyen JT, Tschinkel WR (1982) Phenetic and cladistic rela-
defoliators. At least one species, Palembus ocularis tionships among tenebrionid beetles (Coleoptera). Syst
Casey, appears to be intimately associated with a Entomol 7:127183
Watt JC (1974) A revised subfamily classification of Tenebri-
plant, Tamarindus indica, and another, Sciophagus onidae (Coleoptera). NZ J Zool 1:381452
pandanicola (Boisduval), occurs on Pandanus in Watt JC (1967) A review of classifications of Tenebri
Hawaii. Those are exceptions. onidae (Coleoptera). Entomologist,s Monthly Maga-
There are a number of genera in several widely zine 102:8086
separated phylogenetic groups (e.g., Bolitotherus,
Rhipidandrus, Neomida, Platydema) which inhabit
fungi. It appears that both the larvae and adults Dark-Winged Fungus Gnats
feed directly on the fungi.
A number of darkling beetle species live in Members of the family Sciaridae (order Diptera).
caves or rock fissures and apparently nowhere Flies
else. Some (e.g., Alphitobius laevigatus (Fab.),
Zophobas spp.) often are associated with bat
guano in caves. Darlington, Jr., Philip J

Philip Darlington was born in Philadelphia, USA,

Food on November 14, 1904. The family moved to the
state of Connecticut, and Philip spent the rest of his
Darkling beetles are mostly omnivorous and only life in the New England states (Connecticut, Massa-
a few appear to be host specific. Many species (e.g., chusetts, Maine, New Hampshire and Vermont)
Eleodes, Blapstinus) are root feeders. Wherever except when he was on field trips or in military ser-
stored grain products are stored, a number of cos- vice. His parents were interested in nature, which
mopolitan tenebrionids are secondary pests. None influenced Philip in his career. In 1922, he entered
of them are able to attack unbroken grain kernels Harvard University, gained a first degree and contin-
but feed on ground or milled farinaceous materi- ued to graduate school, gaining a Ph.D. in 1932. An
als; these insects are collectively known as bran explanation for his lengthy studies is that he took the
bugs. The genera Tribolium, Gnatocerus, Palorus, year 19281929 to work in Colombia for the United
Sitophilus and Latheticus are secondary pests of Fruit Company. Ostensibly he worked as entomolo-
cereal products throughout the world. All of these gist to solve a problem in applied entomology. He
are thought to be of tropical origin and probably returned to Harvard University with a large collec-
were fungus feeders originally. They tend to favor tion of insects and bird skins. Then he worked on
stored products that are not in the best condition his Ph.D. dissertation on carabid beetles of New
(wet, moldy, etc.). Hampshire. But in 19311932 he joined an expedi-
tion, led by W.M. Wheeler, to Australia, from which
he returned with an extraordinarily large collection
of insects plus 341 specimens of mammals. On his
References
return to Harvard University, he was appointed
assistant curator of insects. During the next few
Doyen JT (1972) Familial and subfamilial classification of the
Tenebrionoidea (Coleoptera) and a revised generic clas- years he made several expeditions to the West Indies,
sification of the Coniontini (Tentyriinae). Quaestiones collecting insects and other animals in the high
Entomol 8:357576 mountains of the Greater Antilles. In 1940 he was
1154
D Darners

appointed curator of Coleoptera, and 2 years later he Darwin, Charles

married Elizabeth Koch. However, in World War II
he enlisted in the U.S. Army and served in a malaria Charles Darwin was born in Shrewsbury, England,
survey in New Guinea, the Bismarck Archipelago, on February 12, 1809. He was educated at Shrews-
and the Philippines. He returned to Harvard Uni- bury Grammar School, Edinburgh University
versity in 1944. Other collecting expeditions fol- (18251827), and Cambridge University
lowed, such as to the southern extremes of South (18281831), obtaining B.A. and M.A. degrees. His
America in 19621963, but he was also appointed real interest at Cambridge was in collecting insects,
Alexander Agassiz Professor of Zoology at Harvard especially beetles. Then he served as naturalist
University. His published works were on zoogeogra- aboard H.M.S. Beagle during that ships round-the-
phy and natural selection, mimicry, and taxonomy. world cruise in 18311836. Insects were prominent
His three books were (1957) The geographical dis- among the organisms that he observed and collected,
tribution of animals, (1965) Biogeography of the but many of the new species that he collected were
southern end of the world, and (1980) Evolution not named by him, but by specialists (C.C. Babing-
for naturalists In recognition of his works he was ton, F.W. Hope, W.W. Saunders, J.O. Westwood, and
elected to the (U.S.) National Academy of Sciences, G.R. Waterhouse). He did spend 8 years
to the American Academy of Arts and Sciences, and (18461854) monographing barnacles (Cirripedia).
was awarded two Guggenheim fellowships. He died His leaving of the descriptive work on insects to
on December 16, 1983. specialists allowed him to concentrate on produc-
ing his greatest works, The origin of species (1859)
and The descent of man (1871). He died on April
References 19, 1882, in the county of Kent.

Ball GE (1985) The contributions of Philip J. Darlington, Jr. to

the study of carabid beetles in the Americas and a References
bibliography of his publications. In: Ball GE (ed)
Taxonomy, phylogeny and zoogeography of beetles and
ants. A volume dedicated to the memory of Philip Remington JE, Remington CL (1961) Darwins contributions
Jackson Darlington, Jr. (19041983). Dr W. Junk (Series to entomology. Ann Rev Entomol 6:112
Entomologica vol 33), Dordrecht, xiii + 514 pp Smith KGV (1982) Charles Darwin and the Royal Entomo-
Brown WL (1985) Philip Darlingtons contributions to evolu- logical Society of London. Antenna 6:200201
tionary theory. In: Ball GE (ed) Taxonomy, phylogeny
and zoogeography of beetles and ants. A volume dedi-
cated to the memory of Philip Jackson Darlington, Jr.
(19041983). Dr W. Junk (Series Entomologica vol 33),
Dordrecht, xiii + 514 pp
Darwinism
Carpenter FM (1985) Philip Jackson Darlington, Jr.: A bio-
graphical sketch. In: Ball GE (ed) Taxonomy, phylogeny This term is synonymous with the Theory of Natu-
and zoogeography of beetles and ants. A volume dedi- ral Selection, which explains that speciation results
cated to the memory of Philip Jackson Darlington, Jr.
(19041983). Dr W. Junk (Series Entomologica vol 33),
from differential survival and reproduction in
Dordrecht, xiii + 514 pp response to selective forces (both biotic and abi-
otic). Organisms that are well adapted to selective
forces can survive and reproduce, with the prog-
Darners eny of these survivors likely inheriting these adap-
tations. In contrast, organisms that are not well
A family of dragonflies in the order Odonata: adapted to these same selective forces may not
Aeshnidae. survive or reproduce, leading to their elimination
Dragonflies and Damselflies and loss of progeny. Thus, small mutations interact
 Date Palm Stem Borer, Pseudophilus testaceus Gah. (=jebusea hammershmidti Reiche)(Coleoptera: Cerambycidae)
D 1155

with these selective forces and allow organisms to infestation than young trees. Infestation is more
change over time. serious in neglected farms and the potential
Darwin, Charles damage could reach up to 90% in humid areas.
The main damage symptoms caused by this pest
are the cylindrical, oblique emergence holes of
Dascillidae the adults made when the beetles emerge after
burrowing in the trunk of the palm trees.
A family of beetles (order Coleoptera).
Beetles
Biology

Date Palm Stem Borer, The life cycle of the date palm stem borer is 1 year
Pseudophilus testaceus Gah. in most cases, but sometimes a single generation
(=Jebusea hammershmidti Reiche) may take longer. Adults are active from April to
(Coleoptera: Cerambycidae) July. The number of eggs per female varies from 30
to 150. The eggs are laid singly under the frond
yousif aldryhim base with an incubation period of up to 2 weeks.
King Saud University, Riyadh, Saudi Arabia The larvae feed first on the frond base and then
bore into the stem (trunk) of the tree where they
The adult date palm stem borer is 2140 mm in spend the winter months. The larvae have four to
length and the females usually are longer than the five instars in about 10 months. The larvae con-
males. The beetle is reddish brown in color and the struct an oval pupal cell 2530 mm long and 1015
body is covered by short pubescence. The eyes are mm wide, and the pupal stage lasts about 3 weeks.
perspicuous. The antennae have twelve segments
and are as long as the body. The hind margin of the
last sternite is straight in the male and round with Control
a small depression in its middle in the female. The
eggs are white and elongated, measuring about Pest control measures are mainly focused on the
3.54.3 mm long and less than 2 mm wide. The adults. Light traps are recommended to capture
larvae are long and cylindrical, about 4550 mm adults and to provide notice to farmers about the
in length, light in color with dark brown heads, presence and density of this pest. The capture rate
and are legless with well-formed dorsal pseudo- is the highest from early-May to mid-June. If the
pods. The pupae are 3645 mm in length. pest is causing serious economic damage, dusting
with contact insecticides is recommended. The
growing point of the tree and the base of the fronds
Geographic Distribution are the preferred site for insecticide application.
The fungus Beauveria bassiana yielded promising
The date palm stem borer is found in India, Iraq, results, experimentally, against the larvae in Iraq.
Iran, Saudi Arabia, the Gulf States and Egypt.

References
Symptoms and Economic
Importance Talhouk N (1984) The most common agricultural pests in
Saudi Arabia. Ministry of Agriculture and Water, 121 pp
(in Arabic)
This pest is more serious in humid areas than Hussain A (1974) Pests of date palm trees and dates in Iraq.
dry ones. Older trees are more susceptible to Baghdad University, 190 pp (in Arabic)
1156
D Davis, William Thompson

Hammad SM, Kadous AA (1989) Studies on the biology and DDT

ecology of date palm pests in the eastern Province of
Saudi Arabia. Research Grants Program, Technical
Report No. 25. KACST, Riyadh, Saudi Arabia, 142 pp This is an acronym for dichloro-diphenyl-
trichloroethane, more correctly known as 2,2-bis-
(cholorophenyl)-1,1,1-trichloroethane), a compound
Davis, William Thompson first synthesized in 1873 but not used as an
insecticide until much later. It was not until 1939
William Davis was born in New York on October that the Swiss chemist Paul Mller discovered its
12, 1862, and developed an interest in natural his- insecticidal properties, and Geigy Chemical Com-
tory, encouraged in entomology by Augustus Grote. pany began producing it for control of insect pests.
He had no college education, but went to work at This product, though not universally effective, was
the age of 20 as a clerk. He joined the Brooklyn much more effective than any previous insecticide
Entomological Society and the New York Entomo- and revolutionized chemical-based insect man-
logical Society and obtained an education by learn- agement. It proved very effective in control of
ing from other members and by his own medically important insects and saved thousands
observations. His special interest was in cicadas, of civilian and military lives in wars ofthat era by
and he named and described more than 100 of the improving sanitation and blocking disease trans-
roughly 170 species known in America north of mission by insects during and following warfare.
Mexico. He traveled little, but obtained specimens In the crop production sector, DDT also created a
from all over the USA by purchase. At the age of 46, new level of expectation among producers and
he retired from his job, having been able to save consumers, who came to expect higher crop yields,
enough money, and spent the rest of his life on his and undamaged and uncontaminated produce.
hobbies, mainly entomology, but including other DDT is an organochlorine insecticide, and is
areas of natural history, as well as history. He and related to dicofol (a miticide) and methoxychlor
Charles Leng together wrote two books on the (an insecticide) among other products. Its major
history of Staten Island, the second of which (1930) breakdown products are DDD and DDE, although
appeared in four volumes. He was a major donor of DDD was registered as an independent insecticide.
funds to the Staten Island Institute of Arts and Sci- DDT has low volatility, is insoluble in water, but is
ences, and left the type specimens of the insects soluble in nonpolar solvents. It degrades under
he described to the American Museum of Natural alkaline conditions, but is relatively stable in sun-
History. He married in 1900, but his wife died 13 light. Like most insecticides of the era and since, it
months later. He died on J anuary 22, 1945. affects transmission by nerves. Specifically, it dis-
rupts sodium ion channels resulting in spontane-
ous firing of nerves, leading to spasms and death. In
Reference terms of acute toxicity, it is only moderately toxic to
mammals, though very toxic to many insects and
Mallis A (1971) Willian Thompson Davis. In: American ento-
some other aquatic organisms such as crayfish and
mologists. Rutgers University Press, New Brunswick, NJ,
549 pp shrimp. In some cases, it apparently caused acute
mortality to birds.
Most importantly, DDT was very persistent,
Day-Degree with a half-life of 3060 days in water and 215
years in soil. Persistence was useful in protecting
A physiological unit combining temperature and against insect damage, but proved to be a feature
time, and used to measure and predict growth of that allowed accumulation of DDT or its DDD and
organisms. Also commonly called degree-days. DDE products in animal tissues. Because predators
Bioclimatic Models in Entomology tend to be long-lived and consume numerous prey
 Debach, Pau l Hevener
D 1157

over time, they were exposed tolarge quantities of Dealation

DDT and it products, and itpersisted in their bod-
ies and built to high concentrations. Exposure to Among social insects, the removal of the wings by
these chemicals was associated with egg thinning the reproductives during or after the nupital flight,
in several raptors such as peregrine falcon, bald and prior to colony founding.
eagle, and brown pelican. Calcium deposition was
found to be impaired when birds were exposed to
DDT. The thin eggs could not support the chicks,
Death Feigning
resulting in high mortality and rapid population
decline in these and some other birds. This led the
A behavior displayed by defenseless insects when
United States Environmental Protection Agency to
threatened or disturbed, wherein they become
ban the use of DDT in the USA in 1972, though left
inactive and appear to be dead.
open was the possibility of its use for medical
emergencies. Many other countries followed the
lead of the USA, and DDT use has declined in
much of the world, though it remains available and Death-Watch Beetles
popular in some countries. With the re-emergence
of malaria and some other tropical arthropod- Members of the family Anobiidae (order
borne diseases as serious problems for humans in Coleoptera).
warm areas of the world, a resurgent interest in Beetles
DDT for use against mosquitoes is developing. The
evidence for DDT causing health problems in
humans, particularly cancer, is weak. Debach, Pau l Hevener
Insecticides
Costs and Benefits of Insects Paul DeBach was born in the state of Montana,
USA, on December 28, 1914. With his parents, he
moved to California at an early age. His univer-
Dead-End Hosts
sity training began at the University of California
at Los Angeles, but he transferred to the Berkeley
Hosts that do not allow amplification of a disease,
campus, and completed his B.A. degree in ento-
thereby interrupting transmission, and serving as
mology in 1938. Next, for his graduate studies, he
an end point in the disease cycle. This is usually
moved to Riverside, worked with H.S. Smith, and
used in the context of arboviruses.
was awarded a Ph.D. degree in 1940. His first
Amplification Hosts
appointment was with the U.S. Public Health
Service (19421943) in malaria control, and his
Dead Log Bark Beetles second was with the U.S. Department of Agricul-
ture (19431945) in control of whitefringed bee-
Members of the family Pythidae (order tle. After World War II, he returned to California
Coleoptera). as assistant entomologist with the Department of
Beetles Biological Control, Citrus Experiment Station, of
the University of California at Riverside. He
Dealate remained there for the rest of his career. He orga-
nized the first formal courses there in biological
An individual that has shed its wings, usually after control. His major research was on homopterous
mating. This is common among some groups of pests of California citrus. He undertook foreign
social insects. exploration for biological control agents. To
1158
D Decomposer Insects

c onduct his work, he needed reliable identifica- bacteria exist, most producers are plants. Green
tions of pests and biocontrol agents alike and, plants use solar energy and fix CO2, producing
when these could not be obtained rapidly from organic compounds rich in energy. Most of this
taxonomists, he undertook the taxonomy him- accumulated energy will get used in the ecosystem
self, focusing on minute wasps, and published by respiratory processes and other vital functions,
(1979) a monograph on the genus Aphytis. His whereas some organisms of the community such as
work also included artificial selection of more the consumers and decomposers will use the energy
efficient strains of biocontrol agents. Together accumulated by other organisms.
with Carl Huffaker, he developed the University The consumers are heterotrophic organisms
of California International Center for Biological that obtain food from producers or from other
Control. Again with Carl Huffaker, he developed consumers, with the possibility of several levels of
an Integrated Pest Management Program complexity inside an ecosystem. Primary consum-
designed to develop pest management strategies ers feed directly on the producers. Secondary con-
with minimal use of chemical pesticides, in which sumers feed on primary consumers, etc. Finally,
18 universities and the U.S. Department of Agri- we have the decomposers, saprophytic organisms
culture collaborated. He published more than feeding on dead matter or decaying remains
200 papers and four books. The (1964) Biologi- derived from producers and consumers. Thus, the
cal control of insect pests and weeds that he organic matter synthesized by producers goes on
edited with Carl Huffaker and to which he con- to other levels of organisms across the trophic
tributed key chapters was for years the leading chains, though much of the energy will be used in
textbook on biological control. He died in respiratory processes at all levels.
California in February 1992. In these trophic processes, an important ele-
ment to take into account is that the decomposers
operate at all the levels. Thus, all energy not used
Reference by the consumers and producers, as well as that
accumulated in excretory products, is used by the
Gordh G, Huffaker CB, Luck RF (1992) Paul Hevener DeBach, decomposers and recycled into the ecosystem.
Biological control: Riverside. Available at http://sunsite. This process constitutes the energy cycle, and good
berkeley.edu:2020/dynaweb/teiproj/uchist/inmemo
riam/inmemoriam1993 (accessed Aug 2002)
functioning and subsistence of the ecosystems
depends on effective energy cycling.
In a terrestrial ecosystem, more than 90% of
the organic matter synthesized by the green plants
Decomposer Insects remains unconsumed, and it passes to the level of
decomposers as plant material decaying on soil,
eduardo galante, together with the remains of animal corpses, and
Ma Angeles Marcos-Garcia the excretory products of all levels.
Universidad de Alicante, Alicante, Spain The process of decomposition is one of the
most important events in the functioning of eco-
In any natural or semi-natural habitat, three types systems. Decomposition can be defined as the
of organisms exist: producers, consumers and process by means of which a dead organism or its
decomposers. Good functioning of the ecosystem remains are broken down into the parts or ele-
will depend on their suitable action and interaction. ments that comprise it, and at the end of the pro-
Organisms capable of catching energy and synthe- cess the animal or plant remains will have gradually
sizing organic matter from inorganic compounds disintegrated until their structures cannot be rec-
constitute the producers. Though chemosynthetic ognized, and their complex organic molecules will
 Decomposer Insects
D 1159

have fragmented. This involves a complex process mechanisms out of the initial source (dragging by
in which biotic and abiotic agents interact within wind and water, or direct action of animals such as
the ecosystem. To sum up, the decomposition pro- burial, ingestion, movement, etc.). It is important
cesses cause the liberation of energy and mineral- to note that nutrients released by decomposers
ization of chemical nutrients, turning the organic constitute a food source for numerous animal spe-
matter into inorganic elements. cies, extending the cycle by means of incorpora-
In the process of decomposition, there are tion of the nutrients into tissues, and eventually
two phases, sometimes difficult to distinguish, that constituting new corpses and excrements.
we could call destruction and degradation of The groups of arthropods involved in the pro-
the organic matter. The process of destruction cesses of decomposition of animals and plants
refers to the initial phase of the decomposition remains belong to many taxa (Fig. 2). They are
cycle and is characterized by breaking down the considered to be mesofauna when their size ranges
organic remains by mechanical means so that at between 100 and 200 mm (such as mites (Acari),
the end of this process small-sized particles are springtails (Collembola) and small insects), or
obtained. During this initial phase both abiotic macrofauna when they are larger, such as some
(rain, wind, temperature, etc.) and biotic elements beetles (e.g., Scarabaeidae, Geotrupidae or Silphidae),
(decomposer fauna) play an important role. In the Diptera larvae (e.g., Muscidae, Sarcophagidae,
second phase, degradation of the organic matter Scatophagidae or Calliphoridae), centipedes
occurs, resulting in the disintegration of the small (Diplopoda), woodlice (Isopoda), etc. All these
particles into molecules, producing CO2, H2O and groups are responsible for the fragmentation of
mineral salts as final products. plant or animal remains, contributing to the dest
The destruction phase also results in disper- ruction phase. They contribute both to the
sion of the organic matter, because the small redistribution of the organic remains and forma-
resulting particles can be taken by means of diverse tion of soil elements. These groups of arthropod

Decomposer Insects, Figure 2 The arthropods involved in the process of decomposition of animal and
plant remains belong to such taxa as Diplopoda (1 and 2), Isopoda (3), Collembola (4), Diptera larvae (5),
Coleoptera (6), Acari (7).
1160
D Decomposer Insects

decomposers are present in nearly all terrestrial Another important group in the degradation
habitats, and generally in very high numbers. In of plant remains is woodlice (Isopoda), which also
some cases, millions of individuals belonging to possess symbiotic microorganisms in their intes-
hundreds of species have been identified in just tine that allows them to degrade cellulose.
one square meter. Especially in temperate areas, Not all arthropods assimilate cellulose by
arthropods are the major decomposers, playing a means of symbiotic bacteria, but they make use of
very important role in degradation of waste. woody materials that are pre-digested by extraint-
Thanks to the action of the arthropods during the estinal microorganisms. Included in this group are
initial phase of fragmentation, organic remains some species of springtails such as Tomocerus
can be degraded, and eliminated from the soil (Collembola), ambrosia beetles (Coleoptera:
surface. Curculionidae Scolytinae), ants of the genus
When a suitable community of decomposers Atta (Hymenoptera: Formicidae) and termites
exists, it prevents the appearance of potential bot- (Isoptera) that cultivate fungi.
tlenecks in the recycling of basic elements in the All plant remains do not always present the
ecosystem. Thus, when entomofauna capable of same difficulty of digestion for arthropods. Fruits
acting effectively on plant and animal remains are extensively exploited by arthropods, thanks to
does not exist in a terrestrial ecosystem, serious the existence of yeasts that enhance fruit decom-
alterations in the ecosystem arise, with a reduction position, allowing many arthropods such as flies
in energy flow and great loss of biodiversity. (Drosophila is probably the best known example)
and wasps (Hymenoptera: Vespidae) to feed into
the product resulting from the fermentation. Nev-
Decomposers of Plant Remains ertheless, a fact that must be remembered is that
the relationship between micro-organisms (bacte-
Arthropods play an important role in degradation ria, fungi and protozoa) and plant remains is very
processes of plant remains. Nevertheless, most close, and therefore, in most cases it is inevitable
lack the ability to develop enzymatic processes for that the arthropods consume both resources
degrading the fundamental components of any simultaneously. In some cases, the ingested bio-
plant: lignin and cellulose. Degradation of cellu- mass of micro-organisms is more important nutri-
lose requires the presence of the enzyme cellulase, tionally than the ingested plant remains.
which most arthropods lack. Many insects have
solved this problem by means of mutualistic rela-
tions with micro-organisms, having bacteria or The Entomofauna of Excrement
symbiotic protozoa in the intestinal tract. Others and Corpses
take advantage the cellulase produced by external
microflora. Among the well-known insect decom- The studies of ecosystems have generally paid
posers are termites (Isoptera) and cockroaches preferential attention to the decomposition pro-
(Blattodea). The termites possess symbiotic bacte- cesses of vegetative remains, due to the importance
ria and protozoa, and in their absence wood can- that litter has in the composition of the soil and
not be assimilated by these insects. the contribution of its nutrients. The process of
In many ecosystems millipedes (Diplopoda) decomposition of carrion and dung, though some-
have special importance as decomposers. These times not well known and little studied in many
arthropods, which specialize in leaf litter con- ecosystems, is also important.
sumption, sometimes are abundant, concentrated To understand the processes of degradation
in relatively small areas, and active during a great of corpses and excrements, and the attractiveness
part of the year. of this decaying matter to arthropods, we must
 Decomposer Insects
D 1161

consider that they are very rich resources of not more than one insect generation). Carrion and
organic components that have very special micro- dung are special microhabitats characterized fun-
climatic conditions. Dung and carrion represent damentally by their rapid ecological successions,
not only a rich source of energy, but also a very being extremely ephemeral micro-ecosystems that
specialized habitat that is exploited, in most cases, are rapidly destroyed by the action of the arthro-
by very specific entomological fauna. This fauna pods that colonize them. Arthropod species are
obtains food either directly, such as in the case of sometimes very abundant in these resources, and
the coprophages and carrion-eating arthropods, thousands of individuals belonging to a set of
or indirectly, such as in the case of the predators arthropod decomposers may be attracted to an
that feed on the decomposers. isolated unit. For example, more than 100 species
It is generally difficult to establish the limits of of arthropods belonging to 16 orders and 48 fami-
an arthropod community, but when we study car- lies have been found in just one rabbit corpse, or
rion or dung we meet a perfectly defined ecologi- 16,000 dung beetles found in elephant dung.
cal unit, limited in both space and time. Carrion The arthropods involved in succession vary
(Fig. 3) and dung present many special character- according to geographical areas, even in places
istics that influence the composition and dynam- with similar climates. Also, the number of indi-
ics of the set of species using them. These resources viduals and the species colonizing these micro-
constitute isolated microhabitats inside an ecosys- habitats vary enormously from one patch to
tem in which they are deposed, forming a patchy another, and also through time. Typically, these
system. These microhabitats are relatively small in species are more or less aggregated in these lim-
size (except for corpses of large vertebrates), rich ited resources, with interspecific differences in
in nutrients, and with a short existence (generally foraging and breeding behavior. The aggregated

Decomposer Insects, Figure 3 Adult and larva of a blow fly (Diptera: Calliphoridae) on a lizard cadaver.
Blow flies constitute the first wave of insects colonizing corpses.
1162
D Decomposer Insects

spatial distribution and resource partitioning the entomological fauna of excrement are found,
allow a great number of decomposer species to especially between the excrement of carnivores
coexist in an ecosystem, but great differences in and those of herbivores. This occurs because the
numbers of individuals and species composition composition of nutrients is totally different
are generally found among similar amounts of between carnivore and herbivore excrement.
carrion or dung. However, the broad taxonomic While the excrement of herbivores contains a great
categories of carrion or dung specialists are simi- number of vegetative components that are little
lar worldwide. changed from the plants ingested (8075% of the
Sometimes it is difficult to discern whether ingested weight), the digestive system of carni-
the arthropod fauna involved in decomposition vores is much more efficient and the excrements
processes contributes directly to the recycling of contain less organic matter suitable for exploita-
organic matter or, as in leaf debris systems, they tion by arthropod species. The fauna feeding on
make the substrate more available to the microor- the carnivore excrement is generally depauperate,
ganisms (bacteria and fungi) considered by some and decay often results exclusively from the actions
authors to be the true decomposers. The action of of microorganisms.
the larvae of flies and other insects, for example,
produces liquefaction of corpse tissues, preparing
the substratum for the intervention of microbial Decomposers of Corpses
decomposers. On the other hand, the mechanical
action associated with removal of excrement by Arthropod species attracted to corpses change
beetles, and in making tunnels by both beetles and according to the ecosystem and environmental
fly larvae, enhances microbial activity. The existing conditions. The importance of necrophagous
studies show that the action of decomposer spe- arthropods is not only the ingestion of carrion, but
cies of arthropods and microorganisms is comple- also in making the carrion available to microor-
mentary, but not purely additive. ganisms. Many insects, principally fly larvae, secret
Vertebrates are often considered to be impor- enzymes directly into the carrion, producing liq-
tant scavengers, and many species feed on carrion. uefaction of the tissues. Likewise, adult and larval
Vertebrates may not distinguish between freshly beetles, and fly larvae, make tunnels through the
killed prey and a freshly dead animal, and many carrion, increasing aeration and microbial activity.
predators eat both of them. It is not easy to know The dominant groups, both in number of individ-
how much organic matter is recycled in this man- uals and diversity, are dipterous and coleopterous
ner, but depending on the period of the year, many species. Also, in geographic areas where ants are
of the small animal corpses can be totally destroyed abundant, the corpses are removed rapidly by
by scavengers. However, during summer and these insects, specially the corpses of invertebrates.
autumn in temperate regions, and in the rainy Nevertheless, the arthropods involved in this pro-
period in tropical areas, corpses are rapidly colo- cesses, and the intensity of the action of these ani-
nized by arthropods. As a result, rapid decay is mals, vary according the spatial location of the
observed, with the vast majority of carrion being corpse, type of soil and depth of burial. The num-
consumed by various arthropod species, princi- ber of insects living in carrion diminishes with
pally fly larvae. depth of burial.
The process of decomposition among excre- The arthropods colonizing corpses form
ment and corpse systems varies as a result of the a sequential succession of groups and species
particular composition of the remains, which that depends on the size of the carrion, and on
attracts its own specialist community of arthro- the climatic and edaphic conditions of the area
pod decomposers. Likewise, differences between where they live. Very few species are widespread
 Decomposer Insects
D 1163

throughout the world, and each geographical Diptera are more abundant from early summer to
area and ecosystem has its specialist species feed- mid autumn in temperate regions, and also in the
ing on carrion. rainy season in tropical areas.
The colonization of a corpse is a sequence of The biology of all the Diptera species is simi-
arthropods arriving as successive waves at the car- lar. Females of blow flies and house flies lay eggs or
rion. The form, nature and timing of the succession drop live larvae on to the surface of the fresh
depend on the geographic area, the surrounding corpses, generally at the base of the hairs or near
non-biological environment, and the size of the to the natural holes. Such natural openings facili-
carrion. The first waves involve blow flies (Diptera: tate the penetration of larvae into the inner regions
Calliphoridae) and house flies (Diptera: Muscidae) of the corpse. The ovoviparous females of sar-
arriving for a few hours to oviposit or drop live cophagids are less fecund than blow flies and
larvae. Later, there is a second wave of sarcophagid house flies, and do not deposit all their larvae in
flies (Diptera: Sarcophagidae) that together with the same carrion, rather distributing them evenly
species of calliphorid and muscid flies, deposit among several corpses. Development of fly larvae
their eggs or live larvae on the corpse. The larvae is normally very fast (36 days during the favor-
of these flies are, in turn, consumed by larvae and able periods of the year) and pupation takes place
adults of predatory beetles living in corpses. away from the corpse, in the soil surrounding it.
Staphylinids (Coleoptera: Staphylinidae), histerids Sometimes the mature larvae may migrate more
(Coleoptera: Histeridae) and silphids (Coleoptera: than one meter from the carrion. Ten to 30 days
Silphidae), all are predators of flies, though they after pupation, the new adults emerge and fly off to
also feed on carrion. When the viscera decompose search for new corpses, starting a new life cycle.
and the fat of the corpse turns rancid, a third Among Coleoptera, a principal group in many
wave of insects starts, with some species of phorids temperate ecosystems is Silphidae (e.g., Nicropho-
(Diptera: Phoridae), drosophilids (Diptera: Droso rus, Silpha). It is a group specifically adapted to liv-
philidae) and hover flies of the subfamily Eristali- ing in carrion and its action is comparable to that
nae (Diptera: Syrphidae) arriving. The fourth wave of the Diptera. The adults of Nicrophorus species
consists of cheese skipper species (Diptera: show a very special biology. When a species of this
Piophilidae) and related families of flies. Finally, a genus arrives at the fresh corpse, the male and
fifth wave occurs, the larvae and adults from some female bury the carrion (Fig. 4) underground,
groups of beetles such as dermestids (Coleoptera: thereby reducing the risk of colonization by other
Dermestidae), trogids (Coleoptera: Scarabaeoidea: insects. Once the carrion is safe in the burial cham-
Trogidae) and clerids (Coleoptera: Cleridae) and ber, and the beetles have copulated, they make the
tineid caterpillars (Lepidoptera: Tineidae) that eat corpse into a ball. The eggs are deposited into a
keratin and feed on the remaining hair and short chamber above the carrion ball. The female
feathers. makes a conical depression on the top of the ball,
Diptera are among the most important and defecates and regurgitates droplets of partially
decomposers, especially some of the Calliphoridae digested food, and stridulates, attracting the larvae
(e.g., Lucilia, Calliphora, Chrysomyia, etc.), fol- to the depression in the carrion. The female, and
lowed by some Muscidae (e.g., Fannia), and Sar- sometimes the male, give parental care and pro-
cophagidae (e.g., Sarcophaga). Though the adults vide food by regurgitating into this depression.
feed on the fluids of the corpse, the larvae are the Thus, they ensure the survival of the offspring and
true decomposer organisms, secreting enzymes avoid predation and competition.
directly into the carrion and helping with the liq- In tropical forests, many species of Scarabaei-
uefaction of the corpse tissues while assisting the dae are attracted to both carrion and dung.
increase of microbialactivity. These families of Availability of resources for dung beetles in most
1164
D Decomposer Insects

Decomposer Insects, Figure 4 Male and female Nicrophorus (Coleoptera: Silphidae) burying a mouse
corpse underground. These insects are specifically adapted for living in carrion.

Neotropical forests is low because of the low den- and house flies (Muscidae). The adults of the
sity of large mammals and the low availability of lesser-sized families such as Psychodidae, Scatop-
any particular type of dung. This absence can sidae, Sciaridae, Phoridae, Sepsidae and Sphaero-
probably be attributed to the absence of suitable ceridae come to the corpse in the last phase of
numbers of large herbivores in the forests of Cen- decomposition, after the corpse has been aban-
tral and South America, and the few natural pas- doned by the larvae of the first colonizing flies.
tures of this region (except where cattle have been Their larvae leave the corpse to pupate away from
introduced). In African forests, where large herbi- the larval site, normally in the ground or substrate
vores are present in relatively large numbers, many below carrion. The development of larvae is tem-
dung beetles specialized in the use of excrement perature dependent, and knowledge of the larval
may be found. cycle and its relationships at different tempera-
tures, can be used to estimate the age a cadaver.
Forensic entomology is an important instrument
Forensic Entomology in criminal investigation; however, wemust take
into account that each succession will consist of
Knowledge of the succession of species taking different species in different geographical regions.
place in a corpse following death has been used in This is true even in sites with similar climatic
studies of forensic entomology. This rather con- conditions, because few species are widespread
sistent succession has been used for medical legal in distribution, and each area may have its own
analyses to estimate the time elapsed since death carrion-feeding species. Nevertheless, the broad
of an animal. The study of arthropod species from taxonomic levels of decomposers of carrion are
a cadaver gives us information about the location, constant worldwide. Also, some differences may
time, and conditions to which the corpse was be found as a result of variation in ambient tem-
exposed bef