FORUM

Mosquito (Diptera: Culicidae) Dispersal—The Long and Short of It

M. W. SERVICE
Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, U.K.

J. Med. Entomol. 34(6): 579-588 (1997)

ABSTRACT A review is presented of all aspects of adult mosquito dispersal, encompassing
transportation of mosquitoes by ships, airplanes and trains, long distance wind-assisted dispersal,
and much shorter almost daily flights that mosquitoes make to locate mates, blood sources,
nectar, oviposition sites, and resting sites. The many definitions and concepts of animal migration
are debated, and instances of so-called mosquito migration, that is long distance wind-assisted
flights, and the ecological advantages and disadvantages of such journeys are examined. It is
concluded that there is little evidence that mosquitoes make purposeful long distanceflightsthat
can be classified zoologically as migration. It is argued that it is better to regard all mosquito
flights as dispersal. Host orientation cues are not discussed, but the contentious idea of a
memorized home range between feeding and oviposition sites is presented.

KEY WORDS mosquito dispersal, migration, flight behavior, home range

ZOOLOGISTS OFTEN DISAGREE about the precise mean- winds should be regarded as vagrants to distinguish
ing of the words dispersal and migration (Johnson them from true migrants, which are individuals
1969, Kennedy 1975, Baker 1980, Lincoln et al. 1982, whose behavior is such that it leads to purposeful
Begon et al. 1986, Service 1993a). Many restrict flights outside their habitat, in other words, migra-
migration to mean seasonal (or occasionally shorter tion. Southwood (1962) suggested that migration
temporal intervals, even diurnal) movements of can be maintained in 2 ways. Obligatory migration
large numbers of individuals, even entire popula- occurs when a species is polymorphic so that in a
tions, from one area to another, and usually with the population some individuals are born to be migrants
original animals (return migration) or their progeny such as certain bruchid beetles. In contrast, facul-
(re-migration) returning to the point of origin (Bak- tative migration is considered to occur when
er 1980, Pomeroy and Service 1986). I strongly sup- changes in environmental conditions trigger behav-
port this definition. Furthermore, studies suggest ioral changes, such as aphids, becoming positively
that true migration is adaptive rather than acciden- phototactic, which leads them to fly upward and
tal and that a purposeful event in the life history of become dispersed by winds.
the animals is involved (Baker 1978, 1982). How- Downwind dispersal, often regarded as migration,
ever, Kennedy (1992) queried whether migration is predominates in small, day-flying insects and has the
intentional and considered much of our interpreta- advantage of a limitless supply of free transport
tion of animal behavior, including migration, to be energy, the wind. It has its downside because insects
falsely rooted in anthropomorphism. Whatever the must go where the wind takes them and a successful
reality, migration permits the exchange of genes outcome is not guaranteed; for many it is a kamikaze
between populations and so creates a diversity of journey. However, Taylor (1973) argued that the
the gene pool, which usually is considered advan- "orientation element in insect migration is of trivial
tageous for thefitnessof a species. But migration can ecological importance," that migration is a system
have its costs. It is naive, for instance, to think that for providing new territories, and that the area cov-
all individuals, especially wind-dispersed insects, ered and linear flight are the relevant parameters. In
will find suitable new habitats for egglaying and contrast, in small, night-flying insects, migration
colonization. seems to be limited because at night atmospheric lift
Many entomologists view insect migration some- is minimal, wind speeds are often reduced, and the
what differently (Southwood 1962, Johnson 1969), boundary layer is deeper. Taylor (1974) argued that
and they seem to have proposed more definitions for nocturnal flight is one of the many behavioral means
migration than those working with vertebrates. that small insects have for avoiding migration.
Southwood (1962) considered insect movements to I do not consider that the more classical defini-
be composed of 2 types, namely trivial movements tions of migration, as commonly applied to verte-
that are restricted to the animal's immediate sur- brates, but also to insects such as some butterflies
roundings and migratory movements that take the that periodically migrate from country to country or
animal away from its population habitat. He also to different continents with a return journey made
proposed that insects accidentally swept along by usually by their progeny, are applicable to mosqui-

0022-2585/97/0579-0588$02.00/0 © 1997 Entomological Society of America

580 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 34, no. 6

toes. I prefer to describe all flights by mosquitoes, carried by the wind, is purposeful behavior leading
wind-assisted or otherwise, as dispersal, because to potential long distance dispersal. For instance,
there is no convincing evidence that mosquitoes newly emerged adults of a few Aedes species such as
purposely fly high to be swept away to colonize new Ae. taeniorhynchus (Haeger 1960) andAe. cataphylla
territories, or that they, or their progeny, return to Dyar (Klassen and Hocking 1964) have been ob-
their original areas. Nevertheless, a few mosquito served flying steeply upward to 6-12 m before lev-
species, such as Aedes taeniorhynchus (Wiede- eling out and being carried by the wind. Similarly,
mann), are sometimes described as migratory (Pro- Bailey et al. (1965) described newly emerged Cx.
vost 1952), so it seems appropriate to discuss such tarsalis spiraling upwards to 3-5 m (12-15 feet)
flights as well as other terms that have been pro- before being carried downwind when windspeeds
posed to describe mosquito dispersal. were 5.8-6.4 km/h (3-4 mph), or into the wind
With insects, so-called migration usually refers to when speeds were less than this. However, the so-
the mass exodus and wind-assisted flight of adults called migration recorded very occasionally in some
shortly after emergence. Kennedy (1975) pointed species, such as the dispersal of An. pharoensis over
out that nearly all insect migratory flight is by pre- long distances in Egypt seems more accidental than
reproductive females. However, some so-called mi- purposeful and would be regarded by Bidlingmayer
gratory flights in mosquitoes involve older adults, as lacking an objective.
such as have been reported in Anopheles pharoensis Two widely used terms describing insect flight are
Theobald, and sometimes invasions, or suspected appetential and nonappetential (Thorpe 1951, Pro-
invasions, of infected adults have been thought to be vost 1952). The former refers to dispersal or trivial
responsible for disease epidemics (Brooksby 1983). flight, also termed creeping flights or movements by
Clearly, such vectors are not newly emerged indi- Horsfall (1955) and earlier entomologists, that cease
viduals. when certain goals are achieved, such as feeding,
Several workers have described migratory flights sheltering, and egglaying. Such flights are usually
in anophelines searching for overwintering sites. over short distances, such as a few hundred meters,
For example, adults of Anopheles sacharovi Favr although longer flights of ^ 1 km may be necessary
were found in Israel up to 13 km (Kligler 1932) or if hosts and oviposition sites are widely separated.
14 km (Kligler and Mer 1930) from their larval hab- Appetential flights are referred to sometimes as ac-
itats. Anopheles freeborni Aitken were reported to fly tive dispersal because they are selfpropelled and
"many miles" in California (Freeborn 1921, 1932), selfsteered. Nonappetential flights "serve no special
and up to 42 km (26 miles) before hibernation physiological need" (Provost 1952) and are usually
(Rosenstiel 1947). Bailey and Baerg (1967) con- at the mercy of environmental factors, such as wind,
cluded that in the Sacramento valley this species and are characteristically unidirectional. Such
had the following 4 different phases in its life his- flights are sometimes called passive dispersal. Mos-
tory: (1) a summer phase of nonmigratory flights, quito migration is often included in this category.
(2) a fall migratory flight, (3) a quiescent phase (i.e., Haeger (1985) stated that mosquito migrations are
overwintering phase involving virtually no flights), associated always with population outbreaks of mil-
and (4) a spring dispersal phase. In the fall, adults lions of individuals, but I doubt whether this is true.
located most hibernation sites within 8 km (5 miles) There may be low density migration, but because of
of their breeding sites, but flights as far as 28 km the far fewer adults involved, it will not be spec-
(17.5 miles) were sometimes recorded. Bailey et al. tacular and consequently may go unnoticed. Hock-
(1965) also believed that in California Culex tarsalis ing (1953), in his excellent review of insect flight
Coquillett undertook prehibernation flights of at range, was well aware of the controversies concern-
least 17.7 km (11 miles). There are no records of ing the meaning of migration, but the subject re-
gonotrophic dissociation in Cx. tarsalis, but it ap- mains confused.
pears that in some other species, such as An. free- Johnson (1969) debated the many different in-
borni, adults may stop one or more times en route terpretations of insect migration, what constitutes
to take bloodmeals and thereby build up their fat migration, and how it differs from dispersal. He said
reserves (Rosenstiel 1947). Unfortunately, most old that migration is synonymous with adaptive dis-
records are vague in describing mosquito flights, persal, and it differs from accidental or inadvertent
making it difficult to evaluate their significance or dispersal. However, it can be difficult to decide what
advance our understanding of so-called migration. is adaptive. He devotes an entire chapter in his book
Bidlingmayer (1985) characterized mosquito mi- (Johnson 1969) to describing the different classes of
gratory flights as lacking an objective, the absence insect migration, of which he recognizes 3 main
of return flights, and being performed only by newly ones. Class I is migration without any return, and he
emerged adults. Much of this is contrary to the includes Ae. taeniorhynchus in this category when
understanding of many zoologists on the meaning of there is mass exodus of adults from breeding sites
migration. However, it can be argued that changes accompanied by long distance wind-borne flight, up
in mosquito behavior, such as temporary positive to 32 km (20 miles), to blood-feed followed by a
phototaxis, which has sometimes been reported to short distance dispersal to oviposit. Class II is mi-
precede migration and which takes them out of their gration and return within a season, and Johnson
boundary layer into the upper air where they are (1969) includes mosquitoes flying "several miles" to
November 1997 SERVICE-. MOSQUITO DISPERSAL 581

blood-feed and later to oviposit in this category, tances, and they occur within the so-called bound-
citing as an example Mansonia perturb arts (Walker), ary layer, where the mosquito's flight speed exceeds
which flies up to 3.2 km (2 miles) and 6.0 km (3.75 wind speed and mosquitoes are more or less in
miles) from breeding places to feed and then ap- control of their orientation. When mosquitoes es-
parently returns to oviposit (Snow and Pickard cape from the boundary layer they are no longer in
1957). Anopheles quaclrimaculatus Say and Anophe- charge of their destiny. Although they still beat their
les melas (Theobald) sometimes fly 2-3 km to feed wings, they are at the mercy of the wind. This is
and also could be included in this class. Class III nonappetential flight, and is often called migration.
involves migration to hibernation or aestivation Indeed Taylor (1974) considers that whenever small
sites and return flights at the cessation of these insects cross the boundary layer they become po-
quiescent periods, and this definition would include tential downwind migrants, but I still prefer to term
the prehibernation flights reported for several mos- such flights dispersal, albeit involuntary. However,
quitoes, such as An. freeborni and An. sacharovi. some would argue that wind-dispersed mosquitoes
Johnson (1969) subdivides classes I and III into 5 are not flying, but I think this is a problem of se-
and 3 subclasses, respectively. mantics. Wind-borne mosquitoes are sometimes
Bidlingmayer (1985) classified mosquito flight as carried long distances, especially if there are frontal
migratory, appetential, or consummatory. He de- systems. Drake and Farrow (1988) give a useful
scribed appetential flight as ending directly after the account of the role of weather systems, especially
sought after cues (e.g., host odors, which are usually wind, on the dispersal of insects.
perceived at distances of 10-20 m downwind) are I have not attempted to give a detailed review of
encountered; this phase is equivalent to the search- mosquito dispersal, especially the flight and orien-
ingflightof Gillies and Wilkes (1974). The purpose- tation of mosquitoes to hosts, but to present an
ful flight toward the target is termed consummatory account of the many different types of dispersal and
flight by Bidlingmayer (1985) and approach flight their role in mosquito biology.
by Gillies and Wilkes (1974). In other words, what
is generally called appetential flight is divided into
a searchingflight,upwind or downwind, followed by Long Distance Dispersal
a consummatory or approach flight, upwind if ol- Riding Along with Humans. Slave ships, such as
factory cues are encountered, taking the mosquito the Baltimore Clippers, that raced from West Africa
to the target. Bidlingmayer (1985) noted that con- to the Americas in the shortest possible time to save
summatory flight may occur without any preceding their cargo and escape the slower pursuing war-
appetential flight if hosts enter the arena of the ships, necessarily carried many casks of drinking
mosquitoes' resting sites. water. Such larval habitats must have aided the
I do not think that mosquito flights can be de- spread of Aedes aegypti (L.) and yellow fever and
partmentalized into various categories, it being bet- dengue viruses into the New World (Laird 1989,
ter to regard all flight as a continuum of variable Calder and Laird 1994). Other ships likely trans-
behaviors. I prefer to use the word dispersal to ported Ae. aegypti to various South Pacific islands
describe all movements of adult mosquitoes, and to southeast Asia. In fact, mosquitoes were un-
whether motivated (appetential) or passive (non- known in Hawaii until the 19th century, when the
appetential, e.g., migration), and whether involving sailing ship Wellington is believed to have intro-
a few meters or hundreds of kilometers. It has to be duced Cx. quinquefasciatus in 1826 (Bryan 1934),
admitted that this is contrary to the suggestion of and Ae. aegypti later in that century (Joyce 1961).
Kennedy (1975) that we drop the word dispersal in Similarly, in the 18th and early 19th century whaling
favor of migration in describing insect flight, and of ships that carried large quantities of drinking water
Baker (1980) who restricts the word dispersal to and increased whaling activities in the Pacific most
describe a scattering of individuals in all directions. likely introduced Cx. quinquefasciatus into several
A word of caution, dispersion should not be con- tropical islands as well as into New Zealand (Calder
fused with dispersal. Dispersion describes the spa- and Laird 1994). Belkin (1962) discussed how the
tial pattern of a population, such as whether animals only way for many mosquitoes to have colonized
exhibit random or aggregated distributions; several various Pacific islands was through dispersal by
mathematical models, like Poisson and negative bi- ships or airplanes. Anopheles albimanus Wiedemann
nomial distributions, have been generated to de- was introduced by steamship into Barbados in 1927,
scribe such patterns. and this resulted in some 1,000 malaria cases, but the
In summary, whether mosquitoes take voluntary mosquito apparently was unable to survive in this
flight, such as to blood feed and oviposit, depends on new terrritory (Hackett 1949). In contrast, An. gam-
endogenous cues and environmental thresholds, biae s.l. invaded and established itself on Mauritius
principally light intensity and temperature, al- in the 1st half of the 19th century. It is believed that
though winds of S3270-l,600 cm/s may inhibit take- the introduction was by ships arriving from main-
off (Bidlingmayer 1985, Klassen and Hocking 1964). land Africa or Madagascar (Bruce-Chwatt 1970). In
Such motivated or goal-orientated (appetential) this former malaria-free island, there followed many
flights are under the control of the mosquitoes and malaria outbreaks including a disastrous one in 1867
generally, but not always, involve only short dis- which caused some 32,000 deaths.
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Either a fast French naval vessel monitoring the last 2 countries was not achieved, although, there
route of the proposed air service from Dakar, Sene- was a small apprehended establishment at Auck-
gal, to Natal, Brazil, or an aircraft pioneering the land, New Zealand, against which prompt control
westbound leg is thought to have transported An. measures were effective (Laird et al. 1994, Laird
gambiae s.l., one of the world's most notorious ma- 1995). Ae. albopictus is a competent experimental
laria vectors, to the latter country, where it estab- vector of many arboviruses in addition to dengue,
lished itself in 1930 (Soper and Wilson 1943). Before and consequently may pose a public health threat
it was eradicated in 1940 by a vigorous and disci- almost everywhere it has been introduced. Some-
plined campaign, there were malaria epidemics in- what similarly, it seems that transportation of used
volving ~300,000 people and 16,000 deaths. During tires across New Zealand has assisted the spread of
1942-1944, Egypt also was invaded by An. arabiensis Ae. notoscriptus within that country (Laird 1995). A
Patton, this time originating from the Sudan, and it good account of how commerce, mainly through
seems likely that airplanes were responsible for this ships and airplanes, has aided the spread of vectors,
introduction. Before the species was eradicated in including mosquitoes, is presented by Laird (1984).
1945 by intensive antilarval operations, there were Wind-Borne. There are many examples of mos-
disastrous malaria epidemics (Shousha 1948). More quitoes being carried long distances by wind (John-
recently and on a much smaller scale, infected ma- son 1969; Service 1980, 1993a) and under little con-
laria vectors, including An. gambiae s.l., have trol of their own. A disproportionate number of such
hitched rides on airplanes and on disembarking at examples are of saltwater species. For example; the
foreign airports transmitted malaria to local inhab- mass exodus and dispersal of Ae. taeniorhynchus
itants. The 1st documented case of so-called airport from salt marshes on the eastern seaboard of the
malaria occurred in France in 1969. Since then the United States, and capture of adults on oil rigs 74 and
phenomenon has been reported in Switzerland, It- 106 km from the coast of Louisiana, and on board a
aly, Belgium, The Netherlands, Spain, and the ship sailing several hundred kilometers from land in
United Kingdom (Holvoet et al. 1983, Blaquez 1987, the East China Sea (Hayashi et al. 1978a, b), recov-
Rosci et al. 1987), and possibly Israel (Shpilberg et ery of the salt marsh species Aedes vigilax (Skuse)
al. 1988). 96.5 km (60 miles) inland in Australia, collection of
From the early days of this century, it has been Aedes sollicitans (Walker), another salt marsh mos-
recognized that trains have carried various mosqui- quito, on board a ship which passed no closer than
toes across continents, such as in India (Senior 177 km (110 miles) to the western seaboard of the
White and Newman 1932) and Africa (Gillies and de United States (Service 1980,1993a for references),
Meillon 1968). But such transportation is not re- and the capture of marked Aedes squamiger (Co-
stricted to anophelines. For example, Aedes noto- quillett) in California 61 km (38 miles) from the
scriptus (Skuse) larvae were commonly found in fire release point (Aarons et al. 1951).
buckets on New Zealand railway stations (Graham I believe that there are 2 reasons why saltwater
1939) in the days of coal-fired steam locomotives, mosquitoes have been considered to disperse fur-
and it is possible that such breeding on stations ther than freshwater species. First, coastal salt
facilitated the mosquito's dispersal to new localities marshes usually are exposed windswept places and
on North Island. Similarly, in Australia, Ae. aegypti mosquitoes in such habitats are more likely to be
also bred in station fire buckets and adult mosqui- carried by the wind than species breeding in shel-
toes were often reported biting passengers on long tered woodland habitats; similarly, mosquitoes
distance trains (Taylor 1943). With the switch from breeding in rural areas generally disperse further
steam to diesel trains,firebuckets were no longer an than those in urban areas. Second, it is easier to
essential part of the equipment at stations, and it pinpoint breeding places of saltwater species caught
appears that the numbers of mosquitoes traveling in inland, and so measure the minumum distance they
trains have been reduced. must have flown, than for freshwater species. With
Like those of other Aedes species, the eggs of the latter it is generally assumed that mosquitoes
Aedes albopictus (Skuse) may remain viable, but have emerged from the nearest suitable larval hab-
dry, in larval habitats for many months or even itat, whereas they may have dispersed from more
years. This mosquito, a dengue vector in rural south- distant habitats, although this is difficult to prove.
east Asia, commonly breeds in discarded motor ve- There are nevertheless records of freshwater Aedes
hicle tires. Used tires shipped from Japan and other species also traveling long distances, such as the
Asian countries to the United States and elsewhere capture of Aedes vexans (Meigen) on an unmanned
for retreading (remolding) have been responsible oil rig 32 km from the shore (Sparks et al. 1986) and
for introducing this mosquito into Albania in 1979, Anopheles pulcherrimus Theobald on a ship lying 25
Texas, United States in 1985 (it has now spread to 25 km (15.5 miles) off the coast of Arabia (Wright
states), and later into Brazil, Mexico, the Dominican 1918). In northeast India, >10 species of Anopheles,
Republic, Bolivia, Guatemala, Cuba (eradicated), Aedes, Mansonia, and Culex, including Cx. quinque-
Italy, Nigeria, possibly Burkina Faso, South Africa fasciatus and Culex tritaeniorhynchus Giles, were
(but breeding populations have not been discov- caught at heights of =»150 m on wind-borne journeys
ered), Fiji, Solomon Islands, Santa Cruz Islands, of an estimated 70—110 km (Reynolds et al. 1996).
Australia, and New Zealand. Establishment in the Ming et al. (1993) considered that Cx. tritaeniorhyn-
November 1997 SERVICE: MOSQUITO DISPERSAL 583

(7n/.v was a highly migratory mosquito and that in the lent support to the much earlier report (later dis-
Shanghai area of China diapausing adults are blown puted as improbable) by Kirkpatrick (1925) that in
southward for at least 35 km, but possibly as far as Egypt this mosquito had dispersed at least 72 km (45
200 km, in the autumn. In the spring, after hiber- miles) on the wind. In contrast there is good cir-
nation, adults travel northward to breed. Reisen cumstantial evidence of older An. pharoensis, in-
(1978) considered that in the Punjab province of fected with malarial parasites, having been carried
Pakistan Anopheles subpictus Grassi became extinct on prevailing winds in Israel for at least 280 km (Z.
regionally in about December because of the onset Saliternik in Garrett-Jones 1962). The sudden out-
of cold or dry weather. However, such areas were break of myxomatosis on Woody Island off the Aus-
repopulated annually at the beginning of the mon- tralian coast was attributed by F. N. Ratcliffe (Gar-
soon rainy season. It appears that winds sweeping in rett-Jones 1962) to mosquitoes having been blown
from the southeast bring with it adults, which rap- at least 320 km from the mainland.
idly colonize the numerous newly created larval It may be argued that distances dispersed are
habitats. In Illinois Horsfall (1954) reported the more a function of local topography and the envi-
rapid dispersal after emergence of Ae. vexans seem- ronment than intrinsic factors. Nevertheless, some
ingly up to 370 km (230 miles) and possibly even up species characteristically will disperse further than
to 740 km (460 miles) from the nearest suitable others, because they breed in exposed areas, and
larval habitats. Although there are several instances because the flight behavior of some species brings
of insects being swept along on frontal systems, very them into contact with the prevailing winds. For
few relate to mosquitoes, but this may be one of example, when species such as Ae. taeniorhynchus fly
them. up at a steep angle to «*12 m (40 feet) shortly after
It would seem that wind often causes a greater emergence in the evenings before leveling out
population loss to coastal saltwater breeding mos- (Haeger 1960), this takes them out of the protection
quitoes than to freshwater species. This is because of the boundary layer and so they are more likely to
mosquitoes blown inland a few kilometers, or out to be swept along by winds, sometimes for long dis-
sea, will be unlikely to return to coastal habitats to tances (Haeger 1960, 1985; Nayar 1985). Such be-
oviposit. However, Provost (1952) believed that havior seems to be a response to high larval density,
most wind dispersal of adult Ae. taeniorhynchus was because in the laboratory temporary larval crowd-
parallel to the coast so contact with breeding sites ing produces a migrant phase in adults. These adults
was maintained. With freshwater species there is a exhibit strong bursts offlightactivity during changes
much greater likelihood that wind-dispersed fe- of light to darkness, which is regarded as equivalent
males will find new larval habitats. Moreover, it to the twilight exodus of adults in nature. Adults
seems likely that freshwater mosquitoes breeding in reared from noncrowded larvae show no such flight
woods and forests are transported less frequently by at changing light intensity (Nayar and Sauerman
wind than species breeding in more exposed habi- 1969). Ecologically it can be advantageous for a
tats, such as grasslands, heathlands, open savannas, population to disperse out of an area when densities
and deserts. For example, with species living in increase to levels where there is fierce competition
desert-type habitats, such as Cx. tarsalis in Califor- for resources, such as food in either the larval or
nia and Anopheles sergentii (Theobald) in Egypt, it adult state. Ae. taeniorhynchus is the mosquito re-
would seem advantageous for adults to disperse ferred to most often as to being migratory.
further than forest mosquitoes because larval hab- Bailey et al. (1965) observed Cx. tarsalis adults
itats in dry areas will be fewer, especially when spiralling upward after emergence to 3.7-4.6 m
many desiccate in the drier months or during years (12-15 feet) before being blown downwind. They
of drought. If so, then there will be less gene flow also believed that in California, Cx. tarsalis migrated
among populations of woodland species than in spe- from the floor of the Central Valley to the surround-
cies, inhabiting open habitats, an interesting ing foothills in the fall as a prelude to overwintering
thought for population geneticists. However, Cau- and that wind assisted this movement; studies in the
sey et al. (1950) recorded various forest mosquitoes San Joaquin Valley would appear to support this
in Brazil dispersing several kilometers, with, for hypothesis (Kliewer et al. 1969). However, as re-
example, Aedes serratus (Theobald) and Psorophora viewed by Reisen and Reeves (1990), later studies
ferox (Humboldt) recaptured 11.5 and 10.8 km, re- have failed to confirm the existence of such seasonal
spectively, from their release sites. It seems, how- migration. Ming et al. (1993) considered that Cx.
ever, that the actual areas dispersed were not so tritaeniorhynchus ascends to ^SO m or more before
much across primary forest, but rather across nu- being blown southward on a migration route from
merous isolated patches of forest interspersed with Shanghai, and Reynolds et al. (1996) reported that
savanna areas. mosquitoes (at least 10 species) caught in nets at
An often quoted example of long distance dis- ==150 m elevation in northeast India had flown to
persal is the invasion in 1942 of army camps in Egypt this height on their own accord as a prelude to being
by vast numbers of An. pharoensis at a time of strong swept many kilometers on the wind. As another
winds. They were considered to be newly emerged example, Klassen and Hocking (1964) showed that
adults originating from at least 29-45 km (18-28 newly emerged Ae. cataphylla, but not older indi-
miles) to the northeast (Garrett-Jones 1950). This viduals, are adapted to take-off in windy weather
584 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 34, no. 6

and fly up at a steep angle until reaching =4 or 8 m lease point, whereas in the same country Self et al.
where they are blown along by the wind. However, (1971) found that 98% of marked and released adults
none of 11 species investigated in the laboratory, of this species were caught within 56 m (61 yards)
including Ae. vexans, Psorophora confinnis (Lynch of the release site. In Florida, female Cx. nigripalpus
Arribalzaga), and Cx. nigripalpus, showed increased marked and released were recaptured at a maximum
flight activity at the onset of darkness when their distance of 1.2 km, 82.4% being caught within a
larvae experienced temporary overcrowding. How- radius of 0.4 km (Nayar et al. 1980).
ever, when larvae of Ps. confinnis, Culex nigripalpus It often is recommended that a 2-km wide "barrier
Theobald, Cx. quinquefasciatus, and An. quadri- zone" surround or isolate areas targetted by malaria
maculatus were reared under conditions of tempo- control programs (Service 1993b), because for prac-
rary overcrowding, adults had increased flight ac- tical purposes this is considered to be the maximum
tivity during the first 3 d after emergence (Nayar distance anophelines will fly, the numbers of mos-
and Sauerman 1973). quitoes breeding outside the control area and in-
Other so-called migratory flights have been re- vading it are minimal. In India, for example, Russell
ported in Ae. vexans (Clarke 1943), Ps. confinnis et al. (1944) found that Anopheles culicifacies Giles
(Horsfall 1942), Ae. vigilax (Hamlyn-Harris 1933), dispersed a maximum of 2.4-2.8 km (1.5-1.75 miles);
Aedes dorsalis (Meigen) (Rees 1945), and An. albi- later, in Sri Lanka, Rawlings et al. (1981) caught
manus (Curry 1934), and also see Johnson (1969), nearly all marked An. culicifacies within the village
and Service (1980) for other examples. in which they were released, just 2-7% were caught
Whether or not some mosquito species are inher- in a neighboring village 2 km away. Similarly Reisen
ently dispersive and others not remains debatable. and Aslamkhan (1979) estimated that in Pakistan
the average distance flown by Anopheles stephensi
Liston was only 165 m. An. albimanus usually dis-
Short Distance Dispersal perses just a few kilometers or less (Frederickson
Although long distance dispersal, like all extremes 1993), but Curry (1934) considered that in Panama
and records, attracts most attention and has curi- adults flew up to 19-32 km (12-20 miles) from their
osity value, short distance dispersal is undoubtedly breeding places just before to the rains, but much
the norm in mosquito biology. This type of dispersal shorter distances at other times of the year. How-
(appetential flight) is sometimes referred to as ac- ever, reviews of flight ranges of anophelines by
tive dispersal to distinguish it from passive dispersal Eyles (1944) and insects in general by Hocking
(nonappetential flight), which is applied to carriage (1953) show that only a few Anopheles have been
by any other means, such as by wind, airplanes or recorded as traveling 25 km or more, whereas Aedes
ships. species frequently have been reported to fly greater
Mosquitoes need to disperse for 5 primary rea- distances (Hocking 1953 for references).
sons: to find (1) resting sites, (2) mates, (3) nectar
sources, (4) blood sources, and (5) oviposition sites.
If these are close, then little dispersal is needed. For Home Range
example, adults of An. quadrimaculatw in the In Papua New Guinea, Charlwood et al. (1988)
United States and An. melas in West Africa usually collected Anopheles farauti Laveran species number
disperse only a few hundred meters, but Eyles et al. 1 from 2 villages 4 km apart; Agan is a village with
(1945) recorded flights of 3 km by the former spe- known breeding places just 200 m away and Maraga
cies when females had to cross a wide uninhabited is a village with the nearest breeding place over 1 km
swamp to find hosts. In The Gambia, Giglioli (1964, away. Adults were bloodfed, marked with colors,
1965) found that An. melas regularly commuted and released in the village of capture or in the village
1.6-4 km (1-2.5 miles) from its breeding sites in from which they were not collected. Analysis of
mangrove swamps to feed on villagers and then marked mosquitoes recaught at human bait in both
return to lay eggs. villages indicated that nondisplaced mosquitoes dis-
A review of the literature (Service 1993a) shows persed less after release than those taken to a
that the maximum distance flown by mosquitoes, strange village and released. This was interpreted as
based mainly on capture-mark-recapture methods, gravid mosquitoes having "learnt" their local geog-
is usually just 1-5 km, with about half of the records raphy and flying more or less directly to larval hab-
being <1 km. These were the furthest distances itats when released in their native villages, but such
recorded, and many more mosquitoes are caught a memorized home range was of no help in locating
within much smaller distances from their release breeding places when they were released in the
sites. It is notable that the longest distancesflownby alien village. However, Kennedy (1992) argued that
Ae. aegypti are usually just a few hundred meters. we need to exercise caution in interpreting animal
For example, in Kenya Trpis and Haiisermann behavior in terms of human emotions and purposes,
(1986) found that the maximum distance flown by and probably would query whether mosquitoes can
a marked female in 24 h was 154 m, and that 60.0% develop a search image and act on it.
had moved to houses just 11-50 m away. In Myan- In a completely different situation in England,
mar, Linquist et al. (1967) located >80% of marked mark-recapture experiments and direct observa-
Cx. quinquefasciatus 55 m (60 yards) from the re- tions on host-feeding by Aedes cantans (Meigen)
November 1997 SERVICE: MOSQUITO DISPERSAL 585

combined with identification of bloodmeals from hibernation sites 13-22.5 km away. There is in fact
blood-engorged females caught resting amongst little evidence that migratory flights of Ae. taenio-
vegetation showed the following pattern of move- rhynchus, or other so-called migratory species, are
ments (Renshaw et al. 1994). Adults emerged from adaptive, although they may be.
numerous ponds in wood A, but because of the lack We are hampered in our study of mosquito dis-
of hosts they flew out at night from the wood across persal by poor methodology. For example, although
a road to feed on sheep and cattle in fields ^200 m capture-mark-recapture experiments can give infor-
away. After blood feeding the mosquitoes sheltered mation on dispersal within the boundary layer,
in the nearest suitable vegetation next to their many mosquitoes, sometimes millions, usually have
blood-feeding grounds, that is in wood B. However, to be marked before even a few are captured. In fact,
because there were no ponds in this wood they
returned to wood A to oviposit. Although mark- a high recapture rate usually suggests that there is
recapture studies showed that this series of events little dispersal from the release site. It is much more
occurs, there is no information on what proportion difficult to detect, let alone measure, wind-borne
of females undertake these journeys or how often dispersal that carries mosquitoes escaping from
they repeat them during subsequent gonotrophic their boundary layer long distances, especially those
cycles. mosquitoes that are flying at great heights. Further-
Apart from these studies there appear to have more, it can be statistically dangerous to interpret
been no others providing evidence of a memorized the behavior of a population on just a few recap-
home range in mosquitoes, although the phenom- tures. There are many other problems with inter-
enon! of learning local geography occurs in other preting mark-recapture data, but these have been
insects such as termites, bees, and butterflies. adequately discussed elsewhere (e.g., Southwood
1978, Pedgley 1983, Service 1993a). Nevertheless,
Discussion mark-recapture techniques can sometimes provide
valuable information, such as showing whether
The dispersal of mosquitoes, especially over long there is much interchange between resting popu-
distances, is important for understanding disease lations in different houses or animal shelters, or
epidemiology as well as for formulating the most between different outdoor resting sites.
appropriate control strategy. There are several in- A new approach for studying dispersal involves
stances, although admittedly mostly based on cir- using polymerase chain reaction techniques to bio-
cumstantial evidence, that some outbreaks of ma- chemically fingerprint adults from different sites to
laria, yellow fever, dengue, Rift Valley fever,
Japanese encephalitis (Pedgley 1983, Sellers 1983) determine gene flow, and consequently dispersal,
and myxomatosis (Garrett-Jones 1962) may have between them. However, although this approach
been the result of invasions of wind-borne infected might indicate the absence of dispersal, I doubt
mosquitoes (Pedgley 1983, Sellers 1983). It perhaps whether the extent of dispersal between popula-
should be noted that these involved not newly tions can be estimated by evidence of similarity in
emerged adults, but older ones that usually are not gene frequencies. In other words, just a single non-
associated with so-called migrations. It would seem native female mosquito that produces progeny will
that such dispersal is most likely accidental. introduce genes into a new area, as will the invasion
A zoologist could argue that mosquitoes migrate of hundreds of foreign mosquitoes.
when they fly in search of hosts, return to the same The quantitative study of mosquito dispersal
general area in which they emerged to lay eggs, then dates back to Ross (1905,1911) who suggested that
repeat these purposeful journeys. In fact, Hocking mosquitoes dispersed randomly and that most flights
(1960) implied that migration covered host-seeking were short, at a low level, and were geared to finding
flights by mosquitoes. However, most culicidologists hosts, mates, and oviposition sites. He considered
would term these as appetential flights and there- that such flights were under the control of the mos-
fore not migratory. Migration means many things to quito, and that wind was unimportant in transport-
many people, but I believe that many long distance ing them. We now know that this is partially incor-
wind-borne flights are accidental and not adaptive rect, yet we still know embarassingly little about the
and cannot be regarded as migration. day-to-day flights and dispersal of mosquitoes going
Most records citing migration in mosquitoes refer about their business. During a mosquito's life there
to either their mass exodus, such as Ae. taeniorhyn- may be many different kinds and combinations of
chus, from breeding places, or to prehibernation flights. Such as exploratory ones against or with the
flights as documented in An. sacharovi in Israel and wind in the 1st stages of host-seeking, then upwind
An.freebomi in California, but these 2 types of flight
flights to the host, accidental wind-borne flights
are different. The former involves newly emerged
females, whereas flights in search of overwintering over short or sometimes longer distances, and more
sites are apparently undertaken by older adults that rarely purposeful long distance dispersal on the
bloodfeed before, or at intervals during, their jour- wind. In conclusion, it is better to describe all mos-
neys. Moreover, hibernation-destined adults (e.g., quito flights as dispersal and to avoid the term mi-
An. sacharovi) can take up to 2 wk to arrive at gration which implies a more purposeful journey.
586 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 34, no. 6

Acknowledgments Drake, V. A., and R. A. Farrow. 1988. The influence of

atmospheric structure and motions on insect migration.
I would like to thank Marshall Laird for giving valuable Annu. Rev. Entomol. 33: 183-210.
comments on an early draft of the manuscript. I am in- Eyles, D. E. 1944. A critical review of the literature
debted to the generosity of the Entomological Society of relating to the flight and dispersion habits of
America which made it possible for me to accept an in- anopheline mosquitoes. U.S. Public Health Bull. Wash.
vitation to present a talk on mosquito dispersal, on which
this article is based, at their annual meeting in Louisville, 287: 1-39.
KY in December 1996. Eyles, D. E., C. W. Sabrosky, and J. C. Russell 1945.
Long range dispersal of Anopheles quadrimaculatus.
Public Health Rep. 60: 1265-1273.
Frederickson, E. C. 1993. Bionomics and control of An-
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