DKE215 ch4

4
Fungi, Secondary Productivity,

and Other Fungal – Faunal
Interactions
Fungi are an important component of the food supply to many grazing animals.
How many of us have picked a mushroom in the woods only to find it riddled with
holes and full of fly larvae and other invertebrates? In many European countries,
wild mushrooms are an important component of human’s diet. In recent times,
however, the cultivation of mushrooms by commercial growers has become more
important than personal fungal forays, especially as the commercial production
of mushrooms is independent of season. Indeed, the value of mushrooms as a
food source for humans runs to a sale of approximately 426,625 Mg of Agaricus
and specialty mushrooms in the United States at a sales value of $863 million
(data for the year 2000 –2001, National Agricultural Statistics Service, USDA).
It is therefore not surprising that a number of vertebrate and invertebrate
animals consume mushrooms as part of their diet (Cave, 1997). Not only is the
survival and growth of these organisms dependent upon fungi, but the animals
have effects on the fungi by the dispersal of spores or reduction in the fecundity
of the fungi. In addition to consumption by vertebrates, the unseen grazing of
fungal mycelia by soil fauna is often equally important. Many soil animals are
dependent upon fungi as food or as modifiers of the plant resources, making them
more palatable. We saw earlier that leaf litter in aquatic ecosystems became more
palatable to the “shredder” community as a result of prior colonization and
activity of saprotrophic fungi (Suberkropp, 1992; Graca et al., 1993; Gessner
et al., 1997). It is the fungi that support the populations of many groups of
collembola, mites, and nematodes in soil (Anderson, 2000; Edwards, 2000;
Moore and de Ruiter, 2000; Ruess et al., 2000). In response, these animals exert
their influence on the fungal biomass and community composition. This grazing
Copyright 2003 by Marcel Dekker, Inc. All Rights Reserved.

186 Chapter 4
effect can be significant in regulating the function of the fungal community in

terms of modifying rates of leaf litter decomposition, affecting competition
among fungi for resources, and reducing the efficiency of mycorrhizae to effect
nutrient uptake into host plants.
In the same way that fungi can have both beneficial and detrimental effects
on plants, so too some groups of fungi are pathogens of invertebrates and
vertebrates. Many diseases of fish and humans are fungal, and the role of fungi as
pathogens of invertebrates has been utilized as biocontrol of insect, mite, and
nematode pests of agricultural crops (Larsen et al., 1997; Bird et al., 1998;
Manueli et al., 1999). Recently there has been concern regarding the impact of
fungal pathogens on the populations of tropical frogs (Reed et al., 2000;
Warkentin et al., 2001; Fellers et al., 2001).
In a number of specific instances there have evolved close associations
between animals and fungi. Leaf-cutting ants and termites rely on fungi as a food
source to such a degree that they maintain cultures of specific fungal species,
exclude others, and tend to the growth of their food supply as if it were an
agricultural crop. In other examples, the close association between bark beetles
and the fungi that they transport with them is an essential relationship that permits
the larvae of the beetle to obtain sufficient nitrogen from the tree that they invade
(Ayres et al., 2000). It is thus not possible just to discuss the effects of fungi as
food on the maintenance of animal growth and population size. We must also
consider some of the complex interactions and feedback effects of grazing on the
fungi themselves, as such feedback influences ecosystem processes. The
interactions discussed in this chapter are shown in boldface type in Table 4.1.
4.1 FUNGI AS FOOD FOR SECONDARY

PRODUCERS: POSITIVE IMPACTS ON FAUNAL
PRODUCTIVITY
Fungi are rich in important nutrients, particularly nitrogen, phosphorus, minerals,
and vitamins (Fogel, 1976; Grönwall and Pehrson, 1984) (Table 4.2). Clinton
et al. (1999) measured the nutrient content of fungal fruit bodies (mushrooms of
both mycorrhizal and saprotrophic basidiomycetes) of a Nothofagus forest floor
and showed that all elements other than calcium are more concentrated in fungal
tissue than the forest floor material. This suggests that fungi would be preferred
food resources for many animals. Much of the nitrogen they contain is in complex
forms, however, such as indigestible cell walls (Cork and Kenagy, 1989a), thus
for animals to effectively utilize the nutrients in fungi, they are required to have a
complex community of gut symbionts to assist in the breakdown of these
compounds. Indeed, experiments conducted by Cork and Kenagy (1989b)
showed that the weight of ground squirrels declined when fed entirely upon fruit

Fungal– Faunal Interactions 187
TABLE 4.1 Ecosystem Services Provided by Fungi
Fungal
Ecosystem service functional group
Soil formation Rock dissolution Lichens

Saprotrophs
Mycorrhizae
Particle binding Saprotrophs
Mycorrhizae
Providing fertility for Decomposition or Saprotrophs
primary production organic residues (Ericoid and
ectomycorrhizae)
Nutrient mineralization Saprotrophs
(Ericoid and
ectomycorrhizae)
Saprotrophs
Soil stability Arbuscular mycorrhizae
(aggregates)
Primary production Direct production Lichens
Mycorrhizae
Nutrient accessibility Mycorrhizae
Plant yield Pathogens
Mycorrhizae
Defense against Endophytes
pathogens Saprotrophs
Defense against Endophytes
herbivory Mycorrhizae Pathogens
Plant community structure Plant – plant interactions
Secondary production As a food source Saprotrophs
Mycorrhizae
Population/biomass Pathogens
regulation
Modification of pollutants Saprotrophs
Mycorrhizae
Carbon sequestration and storage Mycorrhizae
(Saprotrophs)
Note: The services that will be discussed in this chapter are in bold face type. Fungal groups in
parentheses are regarded as of lesser importance in that function.
bodies of the hypogeous ectomycorrhizal fungus Elaphomyces granulatus, as

more than 80% of the nitrogen was locked up in complex forms and could not be
made available in the digestive tract of these animals. Fogel and Trappe (1978)
showed that fungi consist of a large amount of water (70 – 94%) and contain fewer

188 Chapter 4
TABLE 4.2 Protein and Mineral Content of a Range of Fungal Species

Used as Food by the Red Squirrel (Sciurus vulgaris )
Fungal species Protein P Ca Mg K Na
Amanita muscaria 25 0.48 0.13 0.04 7.9 0.02

Pholiota sqaurrosa 35 0.96 0.05 0.1 3.1 0.02
Cortinarius delibutus 17 0.55 0.09 0.07 5.4 0.02
C. armillatus 18 0.68 0.11 0.12 6.4 0.02
Gomphidius glutinosus 18 0.56 0.08 0.11 3.8 0.02
Lactarius sp. 16 0.67 0.06 0.12 4.9 0.02
L. torminosus 17 0.46 0.12 0.09 3.0 0.02
L. uvidus 22 0.52 0.06 0.07 3.5 0.03
L. deliciosus 30 0.60 0.06 0.1 2.5 0.02
Russula flava 18 0.29 0.06 0.07 3.9 0.02
Boletus sp. 15 0.53 0.09 0.05 2.2 0.02
B. edulis 30 0.62 0.10 0.12 4.1 0.02
Hydnum repandum 26 0.52 0.16 0.06 4.1 0.03
Elaphomyces granulatus 17 0.21 0.08 0.12 0.6 0.10
Source: Data from Grönwall and Pehrson (1984).
calories per unit weight than nuts, eggs, and meat. Kinnear et al. (1979) provides
figures of fungi having around 40% (by weight) of lipids and 8 – 10% of proteins.
Despite these shortcomings of fungi as high-quality food supplies, however, they
are consumed by a number of vertebrate and invertebrate animals to a greater or
lesser degree.
Some invertebrate animals are entirely fungiverous, whereas others ingest
fungi inadvertently along with plant remains or soil. For a number of vertebrates,
fungi or fungal-based food serves as a primary or temporary food source for times
of the year when little other food is available. For example, the reindeer herds of
Fennoscandia rely heavily on lichens as a food source during the winter months,
without which the populations could not be sustained (Cooper and Wookey,
2001). Mathiesen et al. (2000) showed that more than 25% of the gut contents of
Norwegian reindeer consist of lichens during March. The energy value of this diet
is regarded as good, despite the fact that the structural carbohydrates differ
significantly from plant carbohydrates. The hemicellulose in lichens contains
xylan and lichen starch in b-1-4 and b-1-3 glucoside linkages. It is this factor that
Mathiesen et al. (2000) suggest induces increased bacterial fermentation in
the gut, which results in an increase in the development of food-absorptive
papillae on the gut wall in reindeer fed exclusively with a lichen diet.

4.1.1 Fungi in the Diet of Vertebrates

Claridge and May (1994) reviewed mycophagy in Australian mammals. They
identified 37 species of native and fair species of feral mammals as exhibiting
mycophagy of some sort. The degree of dependency of each animal species on
fungi as a staple or essential part of the diet is difficult to establish. It is estimated,
however, that fungi comprise more than 25% (by volume) of the diet of brush-
tailed potoroo (Potorus longipes ) at all times of the year. Fungi occurred in the
feces of these animals 90% or more at the time during most months and never fell
below 80%. Other animals, such as the smoky mouse (Pseudomus femeus ), relied
on a diet of seeds and moths during the summer months, when fungal fruiting
bodies were unavailable. During the winter, however, the smoky mouse, along
with bush rats (Rattus fuscipes ), relied heavily on fungi. The fungi consumed are
from a wide variety of taxa. Lichenized fungi, however, have rarely been reported
to be consumed by the Australian megafuanal population. Potoroos consume the
most varied fungal diet of any animal (36 fungal taxa), and most of the fungi are
of hypogeal fungi. It would appear that body size limits the diversity of fungal
species eaten, with rats and mice (, 150 g body weight) feeding mainly on
arbuscular mycorrhizal spores of the Endogonaceae (Cheal, 1987). Large
animals, however, such as the feral pig, eat a wide variety of fungal species.
On the island of Svalbard in the Barents Sea, areas that had been free of
reindeer for a number of years now support large herds. As these animals rely on
lichens for a major part of their diet, two aspects of their foraging are posing
severe threats to the lichen community and the sustainability of a viable food
reserve (Cooper and Wookey, 2001). Because of the relatively slow growth of
lichens in this high arctic region, calculated as 2.5 to 10.6 mg g21 wk21 relative
growth rate, the density of reindeer and their grazing activity is likely to outpace
lichen growth. Studies in Finland by Kumpula (2001) show that reindeer
consumed up to 2.6 kg lichens per day during the most intensive digging period
when snow covers the ground. With the assumption that a reindeer grazes an area
of approximately 30 m2 per day during the period of snow cover and calculating
the energy requirements of a reindeer, Kumpula (2001) estimated that each
reindeer requires some 1000 kg ha21 dry weight of lichens to sustain it during the
winter. In addition to the grazing pressure per se, trampling of lichens by the
reindeer herds is an important reason for the decline in both species diversity and
biomass of lichens in areas in which reindeer herd density is high. As Crittenden
(2000) points out, however, there are too few data on the rates of the growth of
lichens to be able to predict large mammal-carrying capacity based on the
reliance of these animals on a predominantly lichen diet. It is interesting to note
that although grazing reduces lichen biomass, the presence of reindeer
significantly increases the lichen nitrogen content from 0.43– 0.91% but no
similar increase in N concentration of Scots pine or Empetrum shrubs, which are

190 Chapter 4
the dominant vegetation of the area (Stark et al., 2000). These authors also noted
an increase in the abundance of bacteria and fungal-feeding nematodes in
reindeer-grazed areas, suggesting a more general increase, in microbial activity
induced by the presence of the reindeer herd.
The abundance of particularly hypogeous (subterranean fruiting) fungi in
forests can be considerable. Fogel (1976) estimated that there could be between
11,052 to 16,753 fruiting bodies produced per ha per year in old-growth Douglas
fir forests in western Oregon. Fruiting accounts for some 2.3 to 5.4 kg ha21 dry
mass of fungus. These fungi have a higher content of nitrogen, phosphorus,
potassium, and micronutrients than epigeous fungi (fungi fruiting above ground),
making them a higher-quality food resource for mammals (Fogel and Trappe,
1978; Trappe, 1988). In comparison with available plant parts, many fungi have
similar food value but less fat content for herbiverous small mammals (Fogel and
Trappe, 1978) (Table 4.3). Fungi thus form a significant proportion of the diet of
these animals (Fig. 4.1).
4.1.2 Fungi in the Diet of Invertebrates

In their reviews of fungivory, both Shaw (1992) and McGonigle (1997)
concentrate on invertebrate consumption of fungi. An older review of
the interactions between fungi and insects by Wilding et al. (1989) describes a
wide variety of interactions with a range of fungal taxa and functional groups.
There are a number of groups of invertebrates that inhabit the mushroom-fruiting
FIGURE 4.1 Percentage contribution of fungi to the annual diet of nine small mammal
species in the Pacific Northwest. Source: Data from Fogel and Trappe (1978).

TABLE 4.3 Chemical Composition of Fungi in Comparison with Plant Parts and Meat
Protein Fat Carbohydrate Ash
Fungi Agaricus bisporus 50 1.2 — 7

Boletus edulis 33 5 58 7
Clavaria flava 1927 2 47 5
Lactarius deliciosus 19 7 28 6
Lentinus edodes 40 5 54 3
Marasmius oreades 35 3 34 10
Morchella esculenta 12 2 46 10
Saccharomyces cerevisiae 14 1 21 —
Suillus granulatus 21 2 70 6
Suillus gervillei 20 2 64 6
Suillus luteus 17 4 53 6
Trichoderma favovirens 25 — 75 9
Tuber malnosporum 11 2 42 8
Nuts Chestnuts 11 7 72 2
Butternut 28 61 3 3
Black walnut 30 57 6 2
Pecan 10 72 10 2
Hickory nuts 15 68 7 2
Filbert nuts 16 64 12 2
Beech nuts 22 52 19 3
Meat Chipped beef 30 6 1 —
Source: Data from Fogel and Trappe (1978).
structures of basidiomycete fungi. Large, fleshy mushrooms are often heavily

invaded by dipteran larvae. Studies of fly larvae that consume mushrooms have
shown that there is little correlation between the fungi considered poisonous to
humans and those consumed by invertebrates. Indeed, Jaenike et al. (1983) found
that many species of the fly Drosophila were tolerant of the toxic component of
Amanatia spp., a-amanitn. High densities of collembola can often be found
grazing the surface and spores of less fleshy species, such as Laccaria spp.
Hanski (1989) reviewed the interactions between fungi and insects, considering
fungi as insect food. He suggests that the spatial distribution of fungal fruiting
bodies can influence the feeding activities of above-ground fungiverous insects.
In the same way, he suggests that the seasonal appearance of particularly
basidiomycete fruit bodies can influence the growth and development of insect
larvae and consequently the fecundity of the adult insect. This may be a
determining factor in why most fungal-feeding insects are polyphagous rather
than monophagous; they have a greater chance of finding at least one fungal
species fruiting at any time (Table 4.4).

192 Chapter 4
TABLE 4.4 The Degree of Polyphagy in Diptera

Breeding in Nine Genera of the Agaricales
Number of species used as

Fungal genus food by Diptera larvae
Amanita 6
Hygrophorus 4
Cortinarius 5
Russula 17
Boletus 5
Tricholoma 6
Lactarius 14
Suillius 5
Leccinum 5
Small genera 37
Source: Data from Hanski (1989).
It has been shown that not all fungi are equal in either their ability to provide
the necessary nutrients for adequate growth, and also that the specific secondary
metabolites produced by certain fungal species act as deterrents to animal grazers,
thus not all fungi are equally palatable to specific animals. From the limited
evidence in the literature on fungal selection by a variety of faunal groups, it would
appear that there is no consistent pattern in preference of specific species and
avoidance of others throughout all faunal groups. The preferred fungal species thus
varies among animal groups and even among genera and species within the same
faunal taxon. Soil microfaunal feeding preferences have been determined by
numerous feeding trials in the laboratory. Reddy and Das (1983) provided
evidence to suggest that mites showed little food selection when offered single or
mixed cultures of Trichoderma, Cladosporium, and Pythium, whereas collembola
preferred a mixed microfungal diet. In addition, they demonstrated that the
different fungi had different food values, resulting in differences in the total
numbers of animals at the end of a 9-week experiment. Compared to the control
food (agar medium alone), this showed that some fungi were more beneficial for
population growth and others were detrimental (Table 4.5).
Many animals have distinct preferences for certain species of fungi and
dislikes for other species. Their selection must, however, be based upon other
characteristics of the fungi than the poisons that affect humans. Parkinson et al.
(1979) demonstrated that the collembolan Onichiurus amatus actively avoided a
particular basidiomycete fungus that caused its death, even without the fungus
being ingested. Shaw (1988) compared the palatability of a range of
ectomycorrhizal and saprotrophic fungi to the same collembolan species and

TABLE 4.5 The Influence of Three Microfungi on the Numbers of Soil

Arthropods Remaining in Culture After Nine Weeks Compared to Control
Systems Containing Agar Medium Alone
Microarthropod Trichoderma Cladosporium Pythium Control
Mesostigmata 2 3 530 250

Prostigmata 90 25 70 18
Cryptosigmata 3 6 18 5
Total mites 95 34 618 273
Isotomidae 5 5 4 45
Entomobryidae 1 1 — 5
Total collembola 6 6 4 50
Source: Data from Reddy and Das (1983).
concluded that there was a consistent hierarchy of preferences (Table 4.6).

Thimm and Larink (1995) showed that four collembolan species (Folsomia
candida, Onychiurus fimatus, Sinella coeca, and Proisotoma minuta ) out of the
five tested each had a preference for a different species of arbuscular mycorrhizal
fungus. Xenylla grisea, however, did not show a fungal-feeding preference, but
was observed feeding mainly on nonmycorrhizal root tissue.
TABLE 4.6 Hierarchy of Feeding Preferences of the Collembolan Onichiurus

amatus When Offered a Range of Fungal Species Grown in Agar Culture
Mean percentage of fungal Mean fecal count per

Fungal species colony area consumed culture vessel
Marasmius androsaceus 72.2 74.8

Laccaria proxima 41.4 70.8
Lactarius rufus 55.7 64.5
Suillus luteus 50.7 48.9
Mycena galopus 68.2 19.2
Suillus bovinus 18.2 16.6
Rhizpogon roseolus 20.7 13.8
Paxillus involutus 21.3 13.1
Mycena epiterygia 24.2 10.6
Piolithus tinctorius 0.2 2.1
Clitocybe sp. 1.2 1.1
Hebeloma crustuliniforme 1.7 1.0
Source: Data from Shaw (1988).

194 Chapter 4
Nematodes are ubiquitous in soils. Fungiverous nematodes may feed on a

variety of fungal species, and the selection of fungi to eat may be linked to both
the palatability and nutritional value of the fungi. Sutherland and Fortin (1968)
provided a choice of seven ectomycorrhizal fungi to the nematode Aphelenchus
avenae and found that Amanita rubescens provided the best resource for
nematode reproduction. Three species of Suillus, Cenococcum geophilum, and
Russula emetica provided similar nutritional value, but Rhizopogon roseolus had
a negative impact on nematode numbers. Due to the intensity of nematode
grazing on Suillus granulatus, the authors found that this nematode could prevent
the development of mycorrhizal symbiosis with Pinus resinosa when present in a
tripartite association in culture. It is suggested, however, that the grazing pressure
of nematodes is unlikely to be intense enough to reduce the structure or function
of established mycorrhizal associations in natural ecosystems. Ruess and Dighton
(1996) investigated the fungal food preferences of the nematode Aphelenchoides
saprophilus by comparing saprotrophic and ectomycorrhizal fungi. They
concluded that nematode populations from a natural mixed soil community
performed best and with the highest proportion of A. saprophilus in the
community when the nematodes fed on the ectomycorrhizal fungi Lactarius rufus
and Laccaria laccata. In contrast, a sustainable community could not be
maintained on a diet consisting solely of Paxillus involutus (Table 4.7). In a more
comprehensive study of the food value of mycorrhizal fungi, Ruess and Dighton
(1996) offered seven ectomycorrhizal and one ericoid fungal species to pure
cultures of A. saprophilus. Significant differences in final nematode populations
were found for the different mycorrhizal fungi, and the proportion of females
within these populations also varied. Nematodes feeding on Laccaria laccata
TABLE 4.7 Numbers of Mixed Species Populations of Nematodes in Petri Plates

Supporting the Growth of a Range of Saprotrophic and Ectomycorrhizal Fungal Species
Number of
Functional group Fungal species nematodes (%) A. saprophilus
Mycorrhizal Lactarius rufus 25890 99

Laccaria laccata 2633 100
Paxillus involutus 6 50
Saprotroph Agrocybe gibberosa 349 95
Chaetomium globosum 1427 99
Mucor heimalis 24 13
Note: The proportion of the nematode Aphelenchoides saprophilus in the population is given.
Source: Data from Ruess and Dighton (1996).

TABLE 4.8 Influence of Fungal Food Species (Mycorrhizal Fungi) on the Population of
the Nematode Aphelenchoides saprophilus and Percentage of Females in the Population
(Index of Population Fecundity)
Population after 4 weeks Mature females as percentage

Fungal food ( £ 105) of population
Laccaria laccata 2.4 11.4

Cenococcum geophilum 1.5 7.3
Lactarius rufus 1.4 7.8
Hebeloma sacchariolens 0.8 2.8
Paxillus involutus 0.8 5.8
Amanita muscaria 0.7 2.0
Amanita rubescens 0.6 1.3
Hymenoscyphus ericae 2.0 6.8
Source: Data from Ruess and Dighton (1996).
produced the highest proportion of females in the population as well as the largest
population (Table 4.8), suggesting that this fungus was superior to the others for
both the population growth and potential fecundity of the population. In a
subsequent study, Ruess et al. (2000) showed that the diet of Aphelenchoides sp.
was not only mixed, consisting of both ectomycorrhizal and saprotrophic fungi of
various higher taxa, but that the selection of the most favored fungus changed
over time. It was suggested that this shift in food preference might protect the
nematode from an accumulation of toxic compounds accumulated from the
different fungal species.
Not only do fungi provide food for invertebrates, but invertebrate activity
can change the physico-chemical properties of resources in the decomposer system
to improve their exploitation by fungi. We can see in the decomposition of plant
remains that there are close interactions between soil fauna and fungi, which
change as the process of decomposition progresses. In his microscopic study of
pine leaf litter decomposition, Ponge (1990; 1991) showed changes in fungal
species invading pine needles in concert with faunal invasions. This may have been
a result of animals carrying specific fungal propagules with them, but it is more
likely that the physical actions of the fauna in the comminution of the litter altered
its physicochemical properties, thereby altering the competitive abilities among
the fungi for access to those resources. Indeed, Anderson and Ineson (1984)
showed that the decomposition of leaf litter was enhanced in the presence of
isopods, which by comminution of the leaf litter, increased fungal and bacterial
biomass on the litter. Selective grazing on specific, preferred fungi by soil
invertebrates results in changes in the competitive strengths of fungi, thus faunal
grazing can alter the relative abundance of fungal species in the environment.

196 Chapter 4
A particularly good example of altered fungal competition mediated by soil

arthropods is given by Newell (1984a,b). She found that of two saprotrophic
basidiomycete fungi, Onichiurus latus preferred to feed on Marasmius
androsaceous rather than on Mycena galopus. At high collembolan densities,
the intensity of feeding was enough to significantly reduce the growth of
Marasimus to such an extent that Mycena dominated in the leaf litter. In an optimal,
ungrazed system, however, Marasmius had a preferred habitat of leaf litter, while
Mycena preferred a soil habitat. The effect of collembolan grazing was therefore to
shift the mycelial biomass of each fungus to suboptimal niches. As we have seen,
not all fungal species are equal in their physiological attributes, and a change in
species composition can have an effect on fungal-mediated processes in the
ecosystem. These can be seen from examples of grazing on saprotrophic,
mycorrhizal, and pathogenic fungal functional groups, although the functional
effects of these interactions have only been explored to a limited degree.
The interaction between invertebrates and fungi can also be much more
complex that a direct trophic interaction. In addition to the maintenance of a
fungiverous invertebrate population, the fungus may reap benefits from the
interaction. Over time, these close associations may evolve into near mutualisms.
An example of this close association is that described by Bultman et al. (2000). In
this association, the activities of the larvae of the yucca moth (Botanophila files)
act as “pollinating” parasites of the ascomycete fungus Epichloë elymi. Flies
transfer fungal spermatia (gametes) among fungi as they visit their hosts for egg
laying, and the developing fly larvae consume ascospores. The authors measured
the reproductive output of fungi, the amount of feeding by fly larvae on fungal
reproductive tissues, and the mortality of fly eggs and larvae. Contrary to the
expected, the reproductive output of fungi did not decrease with increasing egg
load, but tended to increase as more eggs were laid (Table 4.9). Larval feeding
TABLE 4.9 Relationship Between the

Number of Yucca Moth Eggs Laid on the
Stroma of Epichloë and the Number of
Perithecia Produced by the Fungus
Number of eggs Number of Epichloë

per stroma perithecia
0 10
1 35
2 57
3 75
.3 70
Source: Data from Bultman et al. (2000).

was only weakly associated with the number of eggs on the fungi. The mean
surface area of fungal stromata decreased as egg abundance increased, but the
overall effect of the flies on Epichloe reproduction was positive, as the number of
preithecia increased with an increase in egg number. The fungus therefore
appears not to be vulnerable to overconsumption by the fly larvae, suggesting that
this could be an example of a balanced antagonism. Similar in associations can be
seen in bark beetle – fungal interactions (Norton et al., 2000; Lombardero et al.,
2000) and will be discussed later in this chapter.
4.2 EFFECTS OF GRAZING ON FUNGI AND

FUNGAL-MEDIATED PROCESSES: NEGATIVE
AND POSITIVE FEEDBACKS
4.2.1 Influence of Faunal Grazing on Decomposition
During decomposition, the competition for resources between microbes can be
influenced by the selective grazing of fungi by soil fauna. Decomposition rates
are reduced as the number of fungal species is increased, due to the fact that
metabolic activity of competing fungi is greater than the activity of an equivalent
biomass of a single fungal species (Wicklow and Yocum, 1982; Robinson et al.,
1993). Because of the selective grazing of fungi by soil microarthropods, the
diversity of fungal species effecting decomposition is often reduced (Lussenhop
and Wicklow, 1985).
In agricultural systems with low densities of soil fauna the effect of faunal
reduction was to reduce decomposition (suggesting a synergistic interaction).
Indirect effects of faunal grazing on the decomposition of resources in soil by
faunal grazing of fungi have been shown by Lussenhop and Wicklow (1985).
Measuring the effect of increasing complexity of the saprotrophic fungal
community on rabbit dung, they showed that as species complexity increased
there was less decomposition and lower production of spores. This is similar to
the findings of Robinson et al. (1993), who showed that a significantly higher
level of respiration occurred when fungal species competed for a resource than
could be predicted from the combination of respiration of each fungus. When
Lussenhop and Wicklow (1985) introduced the mycophagous fly larvae of
Lycoriella mali, however, there was a 10% increase in the rate of decomposition
of rabbit feces at high fungal species diversity and a 1500% increase in spore
production. They suggest three possible hypotheses for this effect. First they
suggest that the larvae could directly compete with fungi for water-soluble
compounds and that this competition becomes stronger as the complexity of
fungal interactions increases. Second, larval grazing on mycelia could slow
hyphal growth and thus reduce the chance of competitive interactions to such an
extent that the fungi can invest more resources to decomposition. Third, the larvae

198 Chapter 4
could concentrate enzymes as the number of fungal species increases. The exact
effect of this interaction is unclear, however. In a microcosm experiment,
Nieminen and Setälä (2001) showed that the presence of fungal-feeding
nematodes and bacteria increased the fungal activity in soil. Each factor,
nematodes or bacteria, had similar effects, but the two acting together were not
additive. Nieminen and Setälä suggest that nutrient limitation and the dependence
on fungi in this particular food web configuration contradicted previous studies
that show food chain length is positively correlated with rates of nutrient-cycling
processes.
Changes in the decomposition of plant litter in the absence of soil
arthropods have been documented. For example, Beare et al. (1992) showed that
the removal of soil arthropods reduced leaf litter decomposition by 5% in both
conventional till and no-till treatments of an agricultural experiment. The
increase in fungal biomass resulting from the alleviation of grazing pressure was
correlated to an increase in nitrogen retention (25% higher than plots with faunal
populations intact). It is suggested that this increase in nitrogen content is related
to N immobilization in fungal tissue. Indeed, 85% of the net immobilized
nitrogen was associated with the saprotrophic fungal community. The activities
of soil fauna thus not only moderate fungal growth, but allow greater rates of
nutrient mineralization than when animals are removed, leading to greater soil
fertility.
Lussenhop (1992) reviewed the effects of faunal grazing on fungi on the
rates of plant litter decomposition. Chen and Ferris (1999) showed that the
decomposition of alfalfa residues and cellulose was increased by the presence of
fungal-feeding nematodes. Where the residues were colonized by the favored
fungal food (Rhizoctonia solani ) for nematodes, both nematode populations and
nitrogen mineralization was significantly higher than when the less favored
fungal food (Trichoderma sp.) was available. This suggests that nematode
feeding increased either the biomass or at least the activity of the preferred fungal
food and that this increase in fungal activity was manifested in the increase in an
ecosystem function. In a contrasting forest ecosystem, however, Coleman et al.
(1990) showed that reduction in microbial predators in ecosystems with high
densities of forest soil fauna led to increased decomposition of litter by relief of
grazing pressure.
The differential grazing pressure on different fungal species by soil
invertebrates can have a profound effect on the distribution of fungal mycelia,
and probably on their function as well. It has often been viewed that grazing of
fruiting structures by insects is inconsequential to the survival of the fungal
species. Considering the mass of fungi in relation to the biomass of insects
feeding upon them it was thought unlikely that the dissemination of spores, the
primary purpose of a mushroom, would be impaired, regardless of the intensity of
invertebrate grazing pressure (Hanski, 1989; Courtney et al., 1990). Studies of

the effect of grazing of fruit bodies of the wood-decomposing fungus Coriolus

versicolor (Guevara et al., 2000), however, showed that the ciid beetles,
Octotemnus glabriculus and Cis boleti significantly reduced the fecundity of the
fungus by reducing reproductive potential by 58% and 30%, respectively.
The authors suggest that this reduction in the fitness of the fungus may be
significant in the environment in terms of reduction in colonization potential of
this fungus.
Faunal grazing can have an effect on the nature of the growth pattern of the
fungus. For example, Dowson et al. (1988) showed that arthropod grazing on the
cord-forming fungus Steccherium fimbriatum induced the development of a fast-
growing diffuse mycelium from a slow, dense growth form. Hedlund et al. (1991)
also showed that the collembolan Onychiurus armatus caused Mortierella
isabelina to shift from appressed hyphae to aerial hyphal growth. These changes
in the growth form of the fungus can significantly alter the rate at which resources
are colonized and utilized. The indirect effect of grazing may thus be to alter the
rate of the processes that are carried out by the fungi concerned.
In a study of collembolan grazing in Sitka spruce plantation forests in
England, Newell (1984a,b) found that of two saprotrophic basidiomycete fungi,
Onichiurus latus preferred to feed upon Marasmius androsaceous rather than on
Mycena galopus. At high collembolan densities, the intensity of feeding was
enough to significantly reduce the growth of Marasmius, to such an extent that
Mycena dominated in the leaf litter. It appeared that the two fungi had optimal
habitats based on a vertical separation of resources, however, Marasmius was
found to grow nearer the soil surface than Mycena, but by relieving the grazing
pressure of the collembolan, Marasmius was found to grow readily at greater
depth and Mycena into the less decomposed leaf litter at the soil surface. It was
therefore suggested that the vertical distribution of these two fungal species was
constrained by the effects of collembolan grazing pressure. If this is indeed true,
it would suggest that the fungi are growing in suboptimal habitats and are
probably functioning less efficiently than they would given ideal growth
conditions. The extent to which fauna limit the effectiveness of fungal activity is
not known, however.
The number of fungivorous nematodes in a community can be influenced
by predation on the nematode community (Laakso and Setälä, 1999). In the study
by Laakso and Setälä (1999) the presence of a specialist nematode-feeding mite
(Parazercon radiatus ) reduced the population of both bacterial and fungal-
feeding nematodes by half. The omnivorous mite (Lysigamasus lapponicus ),
however, increased the density of fungal-feeding nematodes over the bacterial
feeders. As a result, the specialist predator reduced nitrogen availability in soil,
whereas the generalist predator caused an increase by stimulating the microbial
community as a whole. The authors thus conclude that these “top-down”
regulation processes are important in driving the ecosystem-level function of

200 Chapter 4
the community. Much more work is required, however, if we are to fully

understand the complexities of these trophic interactions and their impact on
function.
Earthworms are also selective in their feeding preferences for different fungal
species. Brown (1995) cites the work of Cooke (1983) showing selection of certain
fungal species and rejection of others. This selective grazing may alter the species
composition on a decomposing resource by changing the diversity of fungal species
and altering the physiological attributes of that community. Indeed, Tiwari and
Mishra (1993) found greater numbers and diversity of fungi in earthworm casts than
surrounding soil. The changes in species composition of fungal communities can
thus be altered to change the rates of decomposition of resources. The activity of
earthworms often results in a greater comminution of leaf litter, thus increasing the
surface area for attack by saprotrophic fungi. This activity will enhance
decomposition processes. Salmon and Ponge (2001) have shown that earthworm
feces attract entomobryid collembola, which feed on the mucus/urine mixture
contained in the feces. In addition, because of their elevated nutrient loading, these
sites are foci for the development of bacterial and fungal communities. These
conditions lead to the establishment of soil microbial communities that are
beneficial in forming and maintaining soil aggregates that are useful for restoring
degraded soils (Scullion and Malik, 2000; Görres et al., 2001).
In plant canopies herbivorous invertebrates can significantly alter the
physicochemical properties of plant parts by their grazing and production of
exuviae and feces. In particular, aphids produce honeydew (a pure sugar excreta
produced by virtue of the fact that they need to process so much phloem sap to
obtain nitrogen for growth and reproduction that most of the sugar is in excess of
their energy needs) (Dixon, 1973). This sugar is a resource for fungi and bacteria
in the phylloplane, in which all micro-organisms are suspected to be energy-
limited (Stadler and Müller, 1996; 2000). These authors report densities of
bacteria and filamentous fungi of two to three orders of magnitude higher in
honeydew-contaminated leaves than in control leaves. The influence of
honeydew and other resources, such as pollen, on leaf surfaces may have
dramatic effects on fungal biomass and alter leaf surface fungal communities. As
we have seen, the effects of fungal and bacterial communities on leaf surfaces can
directly influence the success of fungal pathogen invasion of the leaf. In addition,
the increased fungal biomass on leaf surfaces can alter the dynamics of nutrient
absorption from throughfall precipitation. Stadler et al. (1998) and Stadler and
Michalzik (1999) showed that the elevation of microbial biomass on leaf surfaces
of Norway spruce trees increased the absorption of nitrogen in the tree canopy by
microbial immobilization. This has a direct affect on the nutrient loading of soil
under the canopy, and consequently on the growth of trees.
As we discussed earlier, edaphic abiotic factors strongly influence the
nature of the fungal communities, effecting decomposition and nutrient uptake by

plants. Because of the unique properties of fungi, we showed that they were
capable of tolerating low moisture levels, particularly in the form of lichens, and
were able to more readily respond to rapid and short-term pulses of moisture than
bacteria. As such, arid and semiarid regions tend to be fungal-dominated
ecosystems (Zak, 1993), and as a result, the soil faunal community is dominated
by fungivores (Whitford, 1989). In these dry ecosystems, Whitford (1989)
suggests that there is indirect evidence that some fungiverous mites can remain
inactive in a state of cryptobiosis. It is well known that a number of nematode
species can exist in a state of anhydrobiosis (Demeure and Freckman, 1981),
which affords them protection during times of desiccation and is a state in which
they can be dispersed by wind (Carroll and Viglierchio, 1981).
Coûteaux and Bolger, (2000) have reviewed the current information on the
effects of climate change, principally elevated CO2, on soil fauna. They come to
the conclusion that there is not enough information to suggest any significant
response patterns in the populations of community structure, but also that because
of the complexity of interactions in soil there may be multiple consequences of
changes in soil faunal activity, including changes in food resources for soil fauna,
consumption of low-quality litter by macrofauna, changes in lifespan due to
elevation of temperature, enhancement of earthworm burrowing activity, and
changes in the species composition of the community due to differential effects of
adverse conditions on different groups of animals. As fungi form a major food
source in soil and there is significant selection of fungal species by soil animals,
either from the saprotrophic or mycorrhizal community, it can be assumed that
because of disturbance, significant changes in either abundance or species com-
position of the fungal community will have a major impact on fungal grazing and
the populations and communities of soil fauna. The interactive effects of climate
change, fungal and fungivore community response to that change, and the sub-
sequent effects on ecosystem process is an area that warrants further investigation.
4.2.2 Influence of Faunal Grazing on Mycorrhizal

Function
Grazing of extraradical arbuscular mycorrhizal hyphae by the collembolan
Folsomia candida was shown to decrease the effectiveness of the mycorrhizal
colonization of leek roots (Warnock et al., 1982). The severing of mycelial
connections between the host plant root and soil reduced the effectiveness of the
mycorrhiza to increase phosphate inflow over and above that of nonmycorrhizal
plants. The addition of moderate densities of the collembolan Folsomia candida
and Tullbergia granulata to field-grown soybean, however, resulted in an
increase of arbuscular mycorrhizal colonization of roots by 40% and in leaf
nitrogen by 5% (Lussenhop, 1996). There were no effects on phosphorus content

202 Chapter 4
of the plants or on the root nodule number, however. The effect of collembola on
the increase in mycorrhizal colonization of roots is contrary to the findings of
McGonnigle and Fitter (1987) and Finlay (1985), who showed significant
declines in mycorrhizal colonization of roots. Lussenhop suggests that the density
of animals in his study (6:8 £ 103 animals m2) was considerably lower than in
other studies (17 £ 103 animals m2) and that high phosphate availability may
have made the response of this crop different from the other studies. He suggests
that the relationship between collembolan grazing and mycorrhizal colonization
is curvilinear rather than linear, and that the intermediate densities of collembola
used in his study could induce compensatory growth of fungal hyphae (Bengtsson
et al., 1993) and thus cause an increase in mycorrhizae. In another study of the
effects of collembolan grazing on arbuscular mycorrhizae and consequences for
plant growth, Harris and Boerner (1990) found that the growth of Geranium
robertianum was maximal at low collembolan densities, as compared to either
high densities or the absence of collembola. They noted that the intensity of
mycorrhizal colonization of roots was inversely related to collembolan density,
but that there was no relationship between the intensity of root colonization and
phosphorus inflow into plants, although plants with higher root colonization had
the best growth. The authors suggest that the benefit of mycorrhizal association
may have been through nutrients other than phosphorus (plant tissue
concentrations of other nutrients were not measured) and that at high
collembolan densities collembola diversified their feeding to nonfungal
resources. In addition, although they report that the mycorrhizal colonization
of roots was reduced at all collembolan densities, they did not suggest that
compensatory growth of extraradical hyphae may have occurred at low animal
density, which may have greater benefit for plant growth than the appearance of
fungal structures within the root tissue. Hiol Hiol et al. (1994) performed choice
chamber experiments with the collembolan Proisotoma minuta and ectomycor-
rhizal fungi. They showed that the collembola significantly slowed the growth
rate of Suillus luteus, Pisolithus tinctorius, Thelephora terrestris, and Laccaria
laccata cultures and the development of mycorrhizae of these species on roots of
loblolly pine seedlings. It appears that there are optimal densities of collembola to
stimulate root colonization and possibly plant growth. Bakonyi et al. (2002)
increased the density of the collembolan Sinella sp. in microcosms in which
maize or red fescue were grown in the presence of spores of arbuscular
mycorrhizae. Significant reductions in mycorrhizal colonization were found
where the collembolan density exceeded 0.2 individuals per g of soil, but there
was a significant increase in root colonization by these fungi as collembolan
density increased from zero to 0.2 animals per g (Fig. 4.2).
Although soil animals have been implicated in the reduction of the
mycorrhizal effect of increasing plant growth and nutrient content by their feeding
on extraradical hyphae, Klironomos et al. (1999) suggest that it is highly probable

FIGURE 4.2 The effect of collembolan density on arbuscular mycorrhizal spore density
and colonization of maize roots by mycorrhizae. Source: Data from Bakonyi et al. (2002).
that arbuscular mycorrhizal fungi are rarely grazed upon in natural ecosystems. By
providing the collembolan Folsomia candida with a choice of saprotrophic and
arbuscular mycorrhizal fungi, they concluded that the saprotroph Alternaria
alternata was not only the preferred fungal food but that a diet of exclusively
arbuscular mycorrhizal fungi reduced fecundity to the point at which no eggs could
be produced by the second generation of animals (Fig. 4.3). The assumption from
FIGURE 4.3 Numbers of eggs produced and hatched from first generation collembola
(Folsomia candida ) when fed upon a variety of arbuscular mycorrhizal fungi. Source:
Data from Klironomos et al. (1999).

204 Chapter 4
their study was that there is probably little or no effect of collembolan grazing on
mycorrhizal benefit to host plants, as this functional group of fungi is avoided in
favor of more nutritious saprotrophic species. This finding is in contrast to an
earlier study by Klironomos and Ursic (1998), in which they suggested that despite
alternate food items in the form of saprotrophic conidial fungi, collembola
significantly reduced arbuscular mycorrhizal connections between the root and
soil, thus reducing the beneficial effects of the mycorrhizae on plant growth. The
degree of damage to mycorrhizal hyphae was shown to be a density-dependent
function. These results were obtained in culture conditions, however, and it
remains to be shown if indeed these animals can have a significant effect on
mycorrhizal function in natural systems.
As we have seen, mycorrhizae are capable of altering the chemistry of their
host plants, particularly in terms of their nutrient content. The selection of plant
parts as food for invertebrates is often dependent upon the chemistry of the plant;
it is possible that there could be an influence of the mycorrhizal colonization of
plant roots and the palatability of above-ground plant parts to grazing herbivores.
Goverde et al. (2000) attempted to test this idea using larvae of the common blue
butterfly, Polyommatus icarus, that were fed with sprigs of Lotus corniculatus
(Fabaceae) plants that had been inoculated with one of two different arbuscular
mycorrhizal species, with a mixture of these mycorrhizae, or with uninoculated
plants. Survival of third instar larvae fed with plants colonized by both
mycorrhizae was 3.8 times higher than with a single mycorrhizal species and 1.6
times greater than that of larvae fed with nonmycorrhizal plants. Larvae fed with
mycorrhizal plants had double the weight of those feeding on nonmycorrhizal
plants after 11 days (Table 4.10). These differences are attributable to the
improved chemistry of mycorrhizal plants that had three times higher leaf P
concentration and a higher C/N ratio than the nonmycorrhizal plants.
TABLE 4.10 The Influence of Mycorrhizal Association of Lotus corniculatus on Plant

Chemistry and the Performance of the Herbiverous Lepidopteran Larva Polyommatus
icarus
Leaf chemistry
(mg g21)
Mycorrhizal Larval Larval fresh weight
treatment mortality (%) P N C at 11 days (mg)
Nonmycorrhizal 23 3.9 5.8 40.5 13

Species 1 6 11.9 5.4 43.2 23
Species 2 6 11.6 5.2 43.4 24
Mixture 14 10.7 5.1 43.6 27
Source: Data from Goverde et al. (2000).

Furthermore, larval consumption, larval food use, and adult lipid concentrations
of the butterfly differed between plants inoculated with different mycorrhizal
species, suggesting that herbivore performance is mycorrhizal species-specific.
On the basis that our understanding of the role of mycorrhizae in natural systems
is limited and that evidence indicates that there is much less effect of mycorrhizae
on plant growth in natural systems than could be predicted from laboratory and
greenhouse studies (Rangeley et al., 1982; Fitter, 1985; Sanders and Fitter,
1992a,b), evidence suggesting an effect of mycorrhizae on herbivores could be a
reason for the maintenance of the arbuscular mycorrhizal condition in natural
herbaceous ecosystems. We thus have another example of the indirect effects of
fungi on animal populations (secondary production) by the enhancement of plant
food resource quality by fungal intervention.
It has been noted that the effect of root colonization by a range of
ectomycorrhizal fungal species can alter the species composition of protozoa in
the mycorrhizasphere (Ingham and Massicotte, 1994). Ingham and Massicotte
(1994) showed that different bacterial communities were isolated from roots
colonized by a variety of Rhizopogon species, Thelephora terrestris, and
Mycelium radicis atrovirens, and that the communities were different on
different tree hosts (Fig. 4.4). It is suggested that the different mycorrhizae may
FIGURE 4.4 Principle coordinate analysis of ectomycorrhizae in protozoan species

space, showing the difference in protozoan community structure of different
ectomycorrhizal fungal species on roots of ponderosa pine. Four groupings appear from
this analysis with similar protozoan communities on group 1 [Rhizopogon
subcaerulenscens (Rs), R. ellenae (Re), and R. truncates (Rt)] from group 2 [R.
arctostaphylii (Ra), R. smithii (Rsm), and R. flavofibrillosus (Rf)], from group 3 [R.
vulgaris (Rvu), R. rubescens (Rr), Thelephora terrestris (Thel), and Mycelium radicis
atrovirens (MRA)] from the outlier R. occidentalis (Ro). Source: The data have been
reworked from Ingham and Massicotte (1994), and the first two axes account for 23% and
18.2% of the variation, respectively.

206 Chapter 4
encourage the growth of different bacterial flora, which in turn promote a

different protozoan community. The authors do not, however, present any data to
support the hypothesis of mycorrhizae-inducing bacterial communities that are
unique to the mycorrhizal fungal species.
As it is believed that mycorrhizal plants direct much more of their
photosynthates into the soil than nonmycorrhizal plants, it is anticipated that where
the growth of organisms that are energy-limited, the detrital food web would
benefit from the flow of C through mycorrhizal plants into the below-ground
ecosystem. Setälä (2000) investigated the potential benefit of the presence of
ectomycorrhizal fungi on the roots of Scots pine (Pinus sylvestris ) on fungiverous
and micobiverous representatives of soil mesofauna. Soil was defaunated and then
reinoculated with 10 species of soil bacteria, 11 species of saprotrophic soil fungi,
and pine seedlings, either infected or notinfected with four ectomycorrhizal fungi.
Soil fauna were added with increasing levels of community complexity, including
the omnivorous enchytraeid species Cognettia sphagnetorum, a Collembola
(Hypogastrura assimilis ), and four species of oribatid mites. After 60 weeks, pine
biomass production was significantly greater in the mycorrhizal systems, the total
biomass being 1.43 times higher in the presence than absence of ectomycorrhizal
fungi. Similarly, almost 10 times more fungal biomass was detected on pine roots
growing in the mycorrhizal than in the nonmycorrhizal systems. Despite the larger
biomass of both the pines and their associated fungal community, however, neither
the numbers nor biomasses of the mesofauna differed significantly between the
mycorrhizal and nonmycorrhizal systems (Table 4.11). The presence of
Collembola and C. sphagnetorum had a positive influence on pine growth,
TABLE 4.11 The Effect of the Presence or Absence of Ectomycorrhizal Associations of

Scots Pine Seedlings on the Number of Soil Fauna Supported by Experimental Systems
When the Fauna Are Present as Single Species or as a Mixed Community of All Species
Faunal density (number per experi-

mental system)
Faunal group No mycorrhiza With mycorrhiza
Faunal groups alone Enchytraeid 83 98

Collembola 62 18
Mite 630 1372
Faunal groups in combination Enchytraeid 339 44
Collembola 14 20
Mite 90 1235
Note: There are no statistically significant differences among the number of animals between
mycorrhizal treatments because of the high variance around the mean values.
Source: Data from Setälä (2000).

FIGURE 4.5 Hierachical feeding preference of the collembola, Folsomia candida on

fungi as determined by mean fecal number produced by collembola and percentage
consumption of the mycelial colony provided as a food source. Source: Data from Shaw
(1988).
particularly in the absence of mycorrhizal fungi, whereas oribatid mites had no

effects on pine growth. There was therefore, no simple and direct relationship
between the complexity of the soil faunal community and pine biomass
production. For example, the complex systems with each faunal group present did
not produce more pine biomass than the simple systems in which C.
sphagnetorum existed alone. The results of this experiment suggest that the
short-term role of ectomycorrhizal fungi in sustaining the detrital food web is less
significant than is generally considered to be the case. Schultz (1991) showed that
there was selective grazing between different species of ectomycorrhizal fungi in
pure culture by the collembolan Folsomia candida in the same way as Shaw
(1985; 1988) (Fig. 4.5). The choice of fungal species is not taxonomically
determined, as variation in palatability is seen among members of the same
fungal taxon. In addition, Schultz’s study also showed that the selection of fungi
altered with time when fungi were combined into simple communities and direct
selection between pairs of groups was allowed (Fig. 4.6). The input of plant-
derived below-ground energy fuels detrital food webs. Wardle et al. (1998)
suggest that negative effects on these webs could ensue from global climate
change if the nature of the resources entering the system is altered as a result of
increased net primary production and reduced resource quality of the litter. They
suggest that this detrimental change in energy flow could be mediated through
fungal–faunal interactions (Wall and Moore, 1999).

208 Chapter 4
FIGURE 4.6 Changes in feeding behavior of the collembola Proistoma minuta over time
when offered a choice of food items of the ectomycorrhizal fungi Alpova olicaeotinctus,
Melanogaster tuberiformis, an unknown isolate M-40, or PDA agar in pairwise
combinations. Source: Data from Schultz (1991).
Indirect effects of herbivory can influence fungal communities and biomass.

In a study of the effects of damage to the photosynthetic apparatus of pinyon pine
forest trees by the larvae of the moth Dioryctria albovitella, Gehring and Whitham
(1991; 1994) found that there were trees that were both susceptible and resistant to
moth attack. Reduction in photosynthate supply to roots of susceptible trees by
moth larval grazing significantly reduced the number of ectomycorrhizal root tips
formed on the trees compared to the herbivore-resistant trees. When herbivore
grazing pressure was artificially removed, the mycorrhizal status of susceptible
trees returned to that of resistant trees (Fig. 4.7). The effect of herbivory on
mycorrhizal colonization of pine roots and growth of the host plant was greater in
the stressed environment of an oligotrophic cinder soil than in a more nutrient rich,
neighboring, sandy loam soil (Gehring and Whitham, 1994).
4.2.3 Influence of Invertebrate Grazing on Fungal

Dispersal
McGonnigle (1997) and Dighton et al. (1997) reviewed the literature on the
interactions among different soil faunal groups and fungi. Dighton et al. (1997)
viewed the data with respect to faunal feeding and the ability of the animals to act
as vectors of fungi, actinomycetes, and bacteria in the context of understanding
the potential role of these organisms in the dispersal of genetically modified
micro-organisms. The paper by Dighton et al. (1997) suggests that the most
effective distribution of microbial propagules would be by larger soil organisms,
which are capable of long-distance transport. Of all soil fauna the major

FIGURE 4.7 Degree of ectomycorrhizal colonization of roots of herbivore-resistant and

susceptible strains of pinyon pine (Pinus edulis) under leaf-inhabiting moth herbivore
(Dioryctria albovitella ) attack and of susceptible strains of trees when herbivore pressure
has been artificially alleviated by moth larva removal. Source: Data from Gehring and
Whitham (1991) reprinted with permission from Nature (1991) 353:556 – 557. Macmillan
Publishers, Ltd.
ecosystem engineers (Lawton and Jones, 1995; Lavelle, 1997) are considered to
be the earthworms. As endogeic species, they are able to create burrows, which
facilitate both biotic and abiotic migration of propagules from the surface soil
layers to deeper soil horizons. As epigeic species, they are capable of horizontal
transport of propagules for long distances. Brown (1995) reviewed the effect of
earthworm activity on soil microbial and faunal community diversity. In this
review he suggests the different effects of the varied ecological strategies of
earthworms, depending on the size of the worm, its location in or on the soil
surface, and the degree to which the worm is capable of altering the
environmental conditions. Direct effects on fungi are through ingestion. These
effects may alter the biomass of fungi by direct and indirect grazing, altering
spore viability during passage through the gut of the worm, altering the
environmental conditions by both physical and chemical means to improve or
degrade the quality of microsties for fungal growth, and altering the dispersal
patterns of fungal propagules. Dispersal can be enhanced by transport on or in the
worm or may be reduced as leaf litter is buried and the sporulating fungi have less
ability to disperse from depth in the soil. The role of earthworms in the dispersal
of arbuscular mycorrhizal spores (Reddell and Spain, 1991; Gange, 1993) may be
of importance in enhancing colonization of roots of newly emerging plants in the
community, however. This process is of particular importance during secondary
succession, during which spores from surviving vegetation can be more readily
moved into areas being recolonized by plants than could be achieved via physical

210 Chapter 4
FIGURE 4.8 Colonization of roots of subterranean clover plants planted at 3-cm spacing
by arbuscular mycorrhizae. The mycorrhizal inoculum and earthworms were introduced at
one end of the chamber. Source: Data from Pattinson et al. (1997).
dispersal alone. In more recent studies, however, Pattinson et al. (1997)

demonstrated that in experiments with clover plants, the presence of the
earthworm Aporrectodea trapezoids reduced rather than increased arbuscular
mycorrhizal infection of the host plant because of lateral transport of the
inoculum (Fig. 4.8). They suggest that the activity of the worms disrupted the
extraradical hyphal network of the arbuscular mycorrhizal fungi, preventing
interplant infection by mycelial growth.
Earthworms can transport propagules of saprotrophic, mycorrhizal, and
pathogenic fungi. Moody et al. (1995) showed that earthworms feed preferentially
on leaf material that has been previously colonized by fungi and that they are
selective with respect to the fungal species colonizing the leaf material. They used
straw colonized by each of six saprotrophic fungal species, each of which had
different enzymatic capabilities. They showed that there were broadly similar
feeding preferences among three species of earthworms (Table 4.12). Moody et al.
(1996) also showed that there was differential survival of the fungal spores on
passage through the earthworm gut and that the effect was different between
the earthworm species Lumbricus terrestris and Aporrectodea longa. Fusarium
and Agrocybe failed to survive passage through the gut of Lumbricus, and both
Fusarium and Mucor failed to germinate after passage through the gut of
Aporrectodea, although the germination of spores of Chaetomium globosum was
enhanced after passing through this worm species (Table 4.13). In a detailed study
on the spores of Mucor heimalis Moody et al. (1996) showed that the decline in
spore germination on passage through an earthworm was caused by the action of
intestinal fluid, not the abrasive action of soil particles as they moved through

TABLE 4.12 Mean Number of Straw Baits Inoculated with Different

Saprotrophic Fungal Species Taken by Three Earthworm Species
Number of straw baits taken
Lumbricus Aporecttodea Allolobophora

Fungal species terrestris longa chlorotica
Fusarium lateritium 12.8 7.9 7.4

Mucor heimalis 11.8 6.4 4.5
Trichoderma sp. 10.9 7.0 5.2
Chaetomium globosum 9.2 4.4 0.6
Agrocybe gibberosa 5.8 22 3.3
Sphaerobolus stellatus 3.6 3.0 4.8
Source: Data from Moody et al. (1995).
the gut. Indeed, they established that abrasion by soil particles stimulated spore
germination.
Earthworm casts are localized sites for elevated numbers of arbuscular
mycorrhizal spores and soil nutrients. In an alley-cropping agroecosystem in the
tropics, Brussard et al. (1993) showed that earthworm casts had significantly
higher contents of major plant nutrients derived from the interplanted tree species
than from soil of the inter-row between the crops or from a monocrop (Table 4.14).
This shows that the interaction between diverse resources and soil arthropods can
stimuate leaf litter decomposition by fungi and bacteria to improve soil fertility.
TABLE 4.13 Viability of Fungal Spores After Passage Through the Gut of Two
Earthworm Species
Mean number of viable

spores
Worm species Fungal species Fed to worms In hind gut
Lumbricus terrestris Fusarium lateritium 900 0

Agrocybe temulenta 34 0
Trichoderma sp. 665 8
Aporrectodea longa Fusarium lateritium 237 0
Source: Data from Moody et al. (1996).

212 Chapter 4
TABLE 4.14 Nutrient Content (mg g21) of Earthworm

Casts in Maize—Leucaena Alley Cropping Tropical
Agricultural Ecosystems
Position N P K Ca Mg
Under Leucaena 401 8 42 191 23

Interrow 72 1.4 7.5 27 3
Monocrop 46 2 5.4 19 3
Note: The combined influence of tree derived leaf litter,
consumption by earthworms, and enhancement of decomposition
by fungi and bacteria significantly improve soil fertility.
Source: Data from Brussard et al. (1993).
Gange (1993) showed that earthworm feeding activity is concentrated on dead and
dying root material, and as a result the worms ingest large amounts of arbuscular
mycorrhizal spores. By depositing spores that are still viable in their casts,
earthworms provide local sources of inoculum for establishing plant species. The
number of spores per cast increases as vegetation succession proceeds (Fig. 4.9).
The effect of this process is to enhance the colonization of recruits into the plant
community as succession proceeds by providing available spores in patches of
enriched nutrient status (worm casts), in which the opportunities for seedling
establishment are increased. Doube et al. (1994a,b; 1995) have shown that
earthworms of the genus Aporrectodea are important in assisting plant roots to be
colonized by bacteria (especially species of Pseudomonas ) that are antagonistic to
root pathogenic fungi. They have shown that earthworms can be effective vectors
for these biocontrol bacteria against the take-all fungus, Gaumannomyces
graminis (Fig. 4.10).
FIGURE 4.9 Mean number of arbuscular mycorrhizal spores per unit soil weight
occurring in field soil and in earthworm casts at different ages of succession of a natural
plant community. Source: Data from Gange (1993).

FIGURE 4.10 The effect of the earthworm Aporrectodea trapezoids on the distribution
of the take-all biocontrol bacterium Pseudomonas corrugata in soil placed in a tube with
earthworms and inoculum placed at one end. Source: Data from Doube et al. (1994b).
Dighton et al. (1997), however, point out that a number of smaller soil
fauna have the capacity to transport fungal spores on their body surface and both
spores and hyphal fragments in their gut. It is well known that mites are great pets
of living fungal cultures, causing contamination among Petri plates. Fungal
hyphae and spores are common in the gut of many mite species, particularly the
Cryptosigmata (Mitchell and Parkinson, 1976; Price, 1976; Ponge, 1991).
Collembola are also major fungal transporters in soil. Dispersal can be effected
through carriage on the integument or by passage through the gut of spores and
hyphal fragments (Visser, 1985). Visser et al. (1987) isolated over 100 fungal
species from collembola in an aspen woodland ecosystem. These included
saprotrophic fungi as well as plant and insect pathogens. As Lussenhop (1992)
suggests, however, spores of arbuscular mycorrhizal fungi generally too large to
be dispersed by microarthropods. In contrast to this suggestion, Klironomos and
Moutoglis (1999) showed that the collebolan Folsomia candida could effect
colonization of nonmycorrhizal plants from adjacent arbuscular mycorrhizal
plants. They showed, however, that the effect of collembola differed among
fungal species. Spores of Acaulospora denticulata increased their dispersal
distance by 10 cm in the presence of the collembola, but the dispersal of spores of
Scutellospora calospora was reduced when collembola were present, possibly
because of spore consumption (Table 4.15). Arbuscular mycorrhizal spores may
be transported by ants (Friese and Allen, 1993), which may play an important part
in the colonizing of bare ground by primary plant colonizers (Allen et al., 1984).
Movement of mycorrhizal spores may be greater by ants than it is by earthworms
in some ecosystems (McIlveen and Cole, 1976). Apart from earthworms, the role
of other soil organisms in the dispersal of fungi is little known (Dighton et al.,
1997).

214
TABLE 4.15 Colonization of Nonmycorrhizal Plants by Arbuscular Mycorrhizae When Placed Adjacent to Mycorrhizal Plants and in the
Presence or Absence of the Collembolan Folsomia candida
Time
(weeks)
2 Follsomia candida þFolsomia candida
1 2 3 4 5 6 10 14 1 2 3 4 5 6 10 14
Distance between 5
plants (cm)
10
15
20
25
30
35
40
45
50
Note: Shaded areas indicate neighboring plants that have become colonized as a function of time (X axis) and distance (Y axis).
Source: Data from Klironomos and Moutoglis (1999).
Chapter 4
TABLE 4.16 The Effect of Inoculation of Seedlings of

Ponderosa Pine with Feces of Tassel-Eared Squirrels and Fruit
Bodies of Hypogeous Fungi
Treatment Mycorrhizal number (%) Seedling infection
Feces 5 33.3
Fruit body 3 20
Control 0 —
Source: Data from Kotter and Farentinos (1984).
Dromph (2001) has shown that collembola of the genera Folsomia,

Hypogastura and Proisotoma are able to carry spores of the entomopathogenic
fungi Bauveria and Metathizium on their cuticles and in their gut. Between
8% – 78% of the spores carried on the cuticle and between 53 –100% of the spores
in feces gave rise to cultures of all three fungal species, suggesting that this type
of transport of entomopathogenic fungi could be important. This work only
showed the ability of these fungi to form colonies on agar, however, not in terms
of infecting insect hosts. Similarly, Price (1976) and Shew and Beute (1979)
showed that astigmatid mites had the ability to spread the root pathogenic fungi
Verticillium and Pythium myriotylum by conidia and microsclerotia carried in the
gut.
Spore dispersal of ectomycorrhizal fungi has been observed with vertebrate
vectors. Trappe and Maser (1976) showed that spores of the arbuscular
mycorrhizal fungus Glomus macrocarpus and of the hypogeous ectomycorrhizal
fungus Hymenogaster were dispersed by small mammals (the Oregon vole,
Microtus oregoni, and chickaree, Tamiasciurus douglasi ). A proportion of the
spores survived passage through the gut of the animals and germinated in the
feces. The ability of these animals to effect spore dispersal assists in the
colonization of bare ground by primary colonizing plant species during the initial
phases of plant succession (Trappe, 1988). Similarly, Kotter and Farentinos
(1984a,b) showed that spores of a variety (unspecified) of ectomycorrhizal fungi
were viable and could develop associations with ponderosa pine after passage
through the gut of the tassel-eared squirrel (Scurius aberti ) (Table 4.16). Cázares
and Trappe (1994) provide evidence to suggest that mycophagy of both
hypogeous and epigeous mycorrhizal fungi results in the deposition of viable
spores in feces. They show the appearance of spores of a variety of fungal genera
in the feces of pika, voles, chipmunks, marmots, mountain goat, and mule deer on
the forefront of Lyman Glacier, which strongly suggests that the deposition of
these spores forms an inoculum source allowing colonization of the newly
developing soils by early successional and slow-growing tree species (Abies
lasiocarpa, Larix lyalii, Tsuga mertensiana, and Salix spp). Similar results were

216 Chapter 4
TABLE 4.17 Number of Arbuscular Mycorrhizal Spores Found in

the Feces of Spiny Rats in Neotropical Forests of Central America
Mean number of spores in

AM spore morphospecies 0.05 g fecal material SE
Glomus A 193.6 50.8

Glomus B 373.3 63.3
Glomus C 795.5 119.6
Glomus D 610.1 99.6
Sclerocystis coremioides 34.1 2.5
Source: Data from Mangan and Adler (2002).
reported by Cork and Kenagy (1989b), who demonstrated that spores of the
truffle Elaphomyces granulatus could pass through the gut of ground squirrels
and deer mouse. These spores retain viability in the feces and are thus able to
colonize new seedling plants in a nutritionally favorable environment.
Consumption and dispersal of arbuscular mycorrhizal spores by the Central
American spiny rat (Proechimys semispinosus ) in neotropical forests was shown
by Mangan and Adler (2002) to be maximal during the fall and winter (October to
December). This dispersal was positively correlated to soil moisture (good
growth and germination conditions for the host tress), but unrelated to fruit
availability (other food sources for the rats). These authors also showed that there
was either selection of mycorrhizal spore species or differential survival through
the gut, as the numbers of spores appearing in the feces differed among fungal
species (Table 4.17).
4.2.4 Influence of Invertebrate Grazing on Fungal

Pathogens
As worms often have higher rates of feeding at or adjacent to roots, it is not
surprising that they can be involved in the activities of root pathogenic fungi.
These interactions are not as simple as would be predicted by logic, however,
Clapperton et al. (2001) showed that the presence of earthworms reduced the
severity of symptoms of the take-all disease (Gaeumannomyces gramminis ) on
wheat. This was not due to a reduction in the abundance of fungi, but to an
increase in fungi in the earthworm-colonized system. As well as increasing
fungal biomass, earthworms also stimulate an increase in bacterial populations. It
is suggested that the effect of earthworms on this pathogen is indirect and
mediated through changes in the microbial community by as yet unknown
mechanisms. It could be hypothesized, however, that an increased diversity in

the microbial community would increase the abundance of bacteria that are
pathogenic to fungi and increase fungal – fungal competitive interactions.
In an indirect way, soil fauna may influence the severity of a plant fungal
disease by using invertebrates as vectors of biocontrol agents. Doube et al.
(1994a,b; 1995) showed that the earthworms Aporrectodea spp. could be used to
transport Pseudomonas bacteria to root surfaces to protect against the take-all
fungus (Gaumannomyces graminis ).
In addition to the interactions among fungi and insect pathogens, soil fauna
may also modify the efficacy of plant fungal pathogens. Recently, Sabatini and
Innocenti (2000) studied the feeding preference of collembola on soil-borne plant
pathogenic fungi. They determined that all of the tested species of collembola
(Onychiurus amatus, O. tuberculatus, and Folsomia candida ) preferred
Fusarium culmorum mycelia, although mycelia of both Gaeumannomyces
graminis and Rhizoctonia cerealis in the mixed culture continued to be grazed at
a lower intensity and were capable of sustaining collembolan growth on their
own. They showed that the fungus Bipolaris sorokinaianum was lethal to all
collembolan species, however.
It can thus be seen that the dispersal of mycorrhizal spores by animal
vectors can be an important component in the provision of fungal inoculum
potential to sites in which vegetation regeneration is occurring. Use of this
information could be made in restoration sites, in which the development of
microhabitats suitable for small mammal refuges could enhance propagule
dispersal and thus increase the rate of primary succession. In general, however,
we do not know enough about the dynamics of fungal spore dispersal by
invertebrates or the significance of faunal grazing on fungi below ground.
From the few studies that have shown the propensity of soil animals to carry
fungal spores or hyphal fragment, there appears to be the possibility of these
animals carrying beneficial organisms to improve plant production by
supplying inocula of mycorrhizal fungi or to deliver mycoparasitic fungi and
bacteria to plant roots to reduce fungal pathogens (Doube et al., 1994a,b;
1995). These interactions among fungi, bacterial, and soil animals therefore
requires further investigation.
4.3 SPECIFIC FUNGAL– FAUNAL INTERACTIONS

4.3.1 Ant and Termite Fungus Gardens
Soil fauna cause significant physical disturbance of soil as well as changes in
the soil chemistry by the introduction of feces, leaf litter, and so on. Due to the
aggregated distribution of most soil fauna, these activities increase the
heterogenetity of the soil ecosystem. An example of such activity and its
influence on fungi can be seen from the study of western harvester ants

218 Chapter 4
TABLE 4.18 The Effect of the Harvester Ant

(Pogonomyrmex occidentalis ) Activity on Root Length and
Arbuscular Mycorrhizal Colonization of Roots of Sagebrush
Community Plants
(%) Root colonized

Total root length (cm) (cm)
Site Mound Off mound Mound Off mound
1 49 52 34 25
2 23 118 20 11
3 127 160 27 18
4 150 180 16 12
5 255 355 21 15
Source: Data from Snyder and Friese (2001).
(Pogonomyrmex occidentalis ) in arid and semiarid ecosystems in North America.

Snyder and Friese (2001) show that the activities of these ants create nests at
densities up to 30 ha21, where each nest represents an area of soil disturbance and
enrichment. They found that the density of sagebrush (Artemesia tridentata ) roots
was similar in and off nest mounds, and that the root length colonized by arbuscular
mycorrhizaa was similar. The intensity of root colonization was higher within the
nest (Table 4.18), however. Given that nests are typically enriched in nutrients
(MacMahon et al., 2000) it is surprising that there is not a greater difference in
mycorrhizal colonization of roots or root length in response to this enrichment
(Pregitzer et al., 1993; van Vuuren et al., 1996; Tibbett, 2000).
Of all the close associations among fungi and animals, the interaction
between leaf-cutting ants and termites and their fungus gardens is an important
illustration of the role of fungi in the maintenance of an insect population. This
association is so close that many regard it as a true symbiosis, as the ants and
termites selectively allow certain fungi to colonize and grow on the leaf pieces to
provide food for their colony. Indeed, the dominant mycelium in termite nests
appears to be Termitomyces sp., which is maintained in abundance by the
constant care of the termites in the face of a greater competitor, Aspergillus. This
balance is probably actively maintained by these animals because Aspergillus is
less palatable or has lesser food value than Termitomyces (Cherrett et al., 1989;
Wood and Thomas, 1989).
Bass and Cherrett (1996) found that there is a close relationship between the
activities of the small worker ants of the colony “minima” workers and the
production of food rewards (staphylae) produced by the fungus. The abundance of
these staphylae appears to increase in smaller passages in the colony, where only

the minima workers can gain access. Indeed, activity of ants can alter the local
fungal flora. Ba et al. (2000) showed that the fire ant imported into the United States
from South America develops a unique yeast flora in its brood chambers. The close
association between Macrotermitinae and the fungus Termitomyces was reviewed
by Wood and Thomas (1989), and they showed that the digestive processes of
termites is almost entirely dependent upon the symbiotic association with the
fungus, without which wood could not be converted into a form that could be
assimilated by the termite. Similarly, Cherrett et al. (1989) described the
mutulaistic association in leaf-cutting ants. The fungus Attamyces bromatificus has
never been found outside the nests of leaf-cutting ants. The ants carry a fungal
inoculm to new nests in an infrabuccal pocket, a small cavity at the esophageal
opening to ensure colonization of new food reserves in the new colony. Korb and
Linsenmair (2001) showed that the availability of food is a limiting resource for
large colonies of the fungus-cultivating termite Macrotermes bellicosus in two
habitats in the Comoé National Park (Ivory coast). The aggregation of smaller
colonies in the savannah region was probably associated with the availability of
trees to provide leaves for the cultivation of fungi. This patchy distribution is also
related to the availability of appropriate microclimatic conditions for fungal
production, which seems to be more important for young colonies. The lower
density of larger colonies in the high forest suggests a more stable environment and
stable humidity for the cultivation of fungi compared to the savannah ecosystem, in
which smaller colonies are more widely dispersed.
4.3.2 Bark Beetle –Fungal Interactions

The close association between wood-decomposing fungi and bark and
ambrosia beetles, the evolution of the symbiotic relationship, and the
physiology and behavior of the organisms involved has been reviewed by
Beaver (1989). The bark beetles mainly feed on phloem which is of relatively
high food value, whereas the ambrosia beetles feed on xylem, which requires a
greater dependence on the fungal symbiont to improve the resource quality of
the wood by partial decomposition and incorporation of nitrogen. Beaver
(1989) discusses the importance of the mycangium, a specialized appendage
on the insect’s leg for the transport of the fungal partner, as the adult beetles
have relatively little fungal material in their gut when they hatch and disperse
from the tree in which they develop. In some instances there may be a
tripartite interaction among plants, animals, and fungi. One of these
interactions that has recently come to light and has ecosystemwide influence
is the link among (1) mites, (2) specialized invaginations or tufts of hair on
leaf surfaces providing refugia for mites (acarodomatia), and (3) plant
pathogenic fungi. By manipulating access to diomatia by tydeid mites
(Orthotydea lambi ), Norton et al. (2000) observed the density of domatia per

220 Chapter 4
leaf and the incidence of grape mildew caused by Uncinula necator. They
showed that the activity of mite mycophagy at high domatia densities
significantly reduced the incidence of mildew on the plants.
Another complex interaction among fungi, arthropods, and plants can be
seen in the blue stain fungus Ophiostoma minus, the mycangial fungi
Ceratocystiopsis ranaculosus and Entomocorticium sp., southern pine beetles
(Dendroctonus frontalis ) a phoretic mite (Tarsonemus spp.,) and pine trees
(Lombardero et al., 2000). Ceratocystiopsis ranaculosus is carried in specialized
structures (mycangia) of the female bark beetle, and the fungus is necessary for the
developing beetle larvae. Ayres et al. (2000) showed that the action of the fungus,
when decomposing live phloem, doubles the nitrogen content of the wood/fungal
matrix (from 0.4 – 0.86% N) (Fig. 4.11). This provides the developing beetle larvae
with a nutrient-enhanced food supply, allowing for faster growth rates and more
rapid maturation. The beetle also inadvertently carries the fungus O. minus,
however, but on its body surface, not in the mycangia. Similarly, the Tarsonemus
mite is inadvertently transported between tress by the bark beetle and has its
highest population growth when feeding on O. minus or C. ranaculosus, but not on
the other mycangial fungus, Entomocorticium sp. Ophiostoma minus is
antagonistic to the growth of the bark beetle, so development of the two
mycangial fungi into wood provides food for developing beetle larvae, but also
provides fungal competition against O. minus. The high growth rate of the mite
when feeding on Ceratocystiopsis reduce the growth of this fungus, allowing
greater wood colonization by O. minus, and hence greater antagonism with the
developing beetle population. There thus exists an indirect negative effect of
FIGURE 4.11 Concentrations of nitrogen (solid bars) and phosphorus (hatched bars) in
phloem of Pinus taeda trees with or without infestation of Dendroctonius frontalis and its
associated mycangial fungi. Blue stain is where the bark is also infected with the blue stain
fungus Ophiostoma minus, which inhibits the growth of the mycangial fungi. Source: Data
from Ayres et al. (2000).

a phoretic mite on the population of a bark beetle that appears to be regulated by

induced changes in competitive abilities between fungi.
Similarly, other bark beetles and wood wasps are vectors of other fungal
pathogens of trees. Redfern (1989) discussed the role of the bark beetle Ips
cembrae in transmitting the fungal disease Ceratocystis lariciola and the wasp
Urocerus gigas in transmitting Amylostereum chailletii, both of which cause
dieback and death of larches. The degree of damage to the tree by fungal
pathogens introduced by both the bark beetle and the wood wasp appears to be
density-dependent. Where the population of the insects is high and causes severe
attack of the tree, tree death is a likely outcome. Where insect density is low, the
effect of the fungus is relatively minor (Fig. 4.12).
4.4 FUNGI AS ANIMAL PATHOGENS: NEGATIVE

IMPACTS ON FAUNAL PRODUCTIVITY
In addition to the positive effects of fungi on vertebrates in terms of providing a
consistent or intermittent food source, fungi can have detrimental effects on
animal populations. There are many fungal diseases of humans and other
vertebrates that are particularly critical when they infect individuals with
compromised immune systems. Details of some of the important human fungal
pathogens can be seen in texts such as those by Bulmer (1989); Evans and
Richardson (1989). A discussion of these pathogens is outside the scope of this
book, however. Many of these disease are not fatal on their own, but can exert
enough influence on the health of their host to reduce growth and fecundity,
which has consequential effects on the population of the animal.
Such pathogenic fungi can have negative effects on insect populations. In
her presidential address to the Mycological Society of America, Blackwell (1994)
discussed the evolution and life histories of some of these strange members of the
Laboulbenales that are carried by and negatively affect many arthropods.
Although these fungi are small and often obscure, they may have important
effects of insect populations and are being investigated as possible biocontrol
agents (Charnley, 1997; Leite et al., 2000; Freimoser et al., 2000). Charnley
(1997) discussed the effect of these fungal pathogens, which are able to breach
the insect defenses of an exoskelton and a variety of immune responses. Charnley
(1997) lists some 20 commercial products, containing the five most commonly
used insect pathogenic fungi (Verticillium lecanii, Metarhizium anisopliae,
Bauveria basiana, B. brongniartii, and Paecilomyces fumosoroseus ) for use
against a variety of plant insect groups. Johnson and Goettel (1993) report that
the application of spores of Beauvaria bassiana in fallow fields reduced the
population of grasshoppers by 60% and 33% within 9 and 15 days, respectively,
after application. The incidence of fungal disease in the insects declined from

222 Chapter 4
FIGURE 4.12 Interactions among the bark beetle, Ips cembrae, the wood wasp,
Urocerus gigas, and the two larch fungal pathogenic fungi, Ceratocystis lariciola and
Amylostereum chailletti, showing how the severity of the diseases depends on interactions
between the two insects. Source: From Redfern (1989).
70% 2 days after spore application to 41% by 13 days, and subsequently to 5%

after 19 days. Pickford and Riegert (1964) showed that the fungus
Entomophthora grylli caused an almost complete eradication of the grasshopper
Cammula pellucida in Saskatchewan in 1963. The high incidence of this fungus
was correlated to unusually high precipitation and high humidity in June and July
of that year, compared to the long-term average and previous 2 years, which
favored fungal growth and reproduction.

In natural ecosystems, entomopathogenic fungi may be important density-

dependent population regulators (Kamata, 2000). Hajek and Leger (1994)
reviewed the literature on the biology and ecology of entomopathogenic fungi.
Blakwell (1994) has specifically reviewed the literature on the Laboulbenales.
Kamata (2000) considered the effect of the pathogenic fungus Cordyceps
militaris in conjunction with avian predators, parasitoids, and abiotic factors on
the population of the beech caterpillar Syntypistis punctatella. He concluded that
the periodic population fluctuations of these larvae were caused by delayed
density-dependent regulators. The fungus was the prime suspect. This causal
agent was suspected as the disease started to induce population decline before it
reached outbreak densities, but the delayed induced defensive response of the
trees was not as closely related to the changes in the insect population (Fig. 4.13).
Cordyceps is also reported as frequently occurring on insects in tropical forest
FIGURE 4.13 Model of the regulation of the population dynamics of the beech
caterpillar Syntypistis punctatella by the delayed induced defensive response (DIR) of the
beech trees and other density-dependent factors. The main correlation between caterpillar
density and a regulator appears to be with insect diseases, which are mainly fungal.
Source: Data from Kamata (2000).

224 Chapter 4
ecosystems (Evans, 1982). Evans (1982), however, stated that pathogenicity of

this fungus was not tested. There was circumstantial evidence, however, that
suggests that Cordyceps is one of the most common pathogens of arthropods. The
sudden decline in the population of gypsy moth Lymantria dispar in Appalachian
forests in 1996 was reported to be due to the high abundance of the fungus
Entomophaga maimaiga (Butler and Strazanac, 2000), again showing how this
fungus could be important in regulating insect populations. The incidence of
fungal disease may be related to environmental conditions, however. Hicks et al.
(2001) showed that there was a significant increase in entomopathogenic fungi in
warm, wet conditions. During these weather events the populations of pine
beauty moth in Scottish lodgepole pine forests were reduced mainly by fungal
pathogens, whereas at other times predators were the main regulators of moth
populations.
The isolation and culture of insect and other arthropod pathogenic fungi
(Leite et al., 2000; Freimoser et al., 2000) may ultimately be useful in the
discovery and use for the biocontrol of human pests. Onofre et al. (2001) have
tested two isolates each of two species of entompathogenic fungi against the
bovine tick Boophilus microplus. The fungus Metarhizium flavoviride proved to
be more effective against adult ticks, reducing both larval emergence from eggs,
and reproductive efficiency, than M. anisopilae (Table 4.19).
Mankau (1981) mentions nematode-trapping fungi that occur in the
rhizosphere of plants such as Arthrobotrys dactyloides, Dactylaria brochopaga,
TABLE 4.19 Mean Lethal Dose (LD50) and Conidial Density of the
Entomopathogenic Fungi, Metarhizium flavoviridae and M. anisopliae,
Required for Control of the Engorged Tick Boophilus microplus
Mean percentage control (C%)
M. flavoviride M. anisopliae
21
Conidia ml CG-291 MF-3 CG-30 CG-46
0 0 0 0 0
104 10.7 23.7 3.1 10.3
105 54.6 50.9 5.1 32.4
106 57.3 45.7 19.5 31.9
107 77.9 63.2 51.6 54.8
108 75.9 66.8 57.2 60.0
LD50
Conidia ml21 3.4 £ 105 4.2 £ 105 2.3 £ 107 1.4 £ 107
Source: Data from Onofre et al. (2001).

Monacrosporium ellipsosporum, and M. gehyropagum. These fungi, he suggests,

are in the prime position to predate plant parasitic nematodes. Although research
has suggested the potential of these fungi as biocontrol agents for plant
pathogenic nematodes, there has been limited success in their use. Nematode egg
parasitic fungi, such as Rhopalomyces elegans, and cyst pathogenic fungi,
Verticillium and Cylindrosporium species, may also be important in regulating
nematode densities. Studies suggest that 14 –50% of cysts and 70– 90% of eggs
of nematodes may be infected with pathogenic fungi. There appears to be little
information regarding the effects of these fungal pathogens on nematode
population regulation, however.
Fungal diseases have been reported as important regulators of anuran
populations (Kaiser, 1998; Morell, 1999; Lips, 1999; Reed et al., 2000;
Warkentin et al., 2001; Fellers et al., 2001). Widespread records of frog
population decline in Panama have been reported by a number of authors. Lips
(1999) showed data reporting an increase in the number of dead frogs found in
her surveys over recent years. Necropsies of all dead frogs showed skin
abnormalities, especially around the mouth, consistent with fungal pathogens.
Previously, Kaiser (1998) had reported an increase in the incidence of a chytrid
fungal disease of frogs in Panama. Also, a chytrid, Batrachochytridium
dendrobatidis, has been found in Australia, where it has been reported to be the
major mortality factor in motorbike frogs (Morell, 1999). It is believed that
climate changes are one of the reasons for the increase in the incidence of skin
infections caused by this fungus, which can be considered to be an “emerging
infectious disease” (Reed et al., 2000). These chytrids have caused oral
deformities of up to 41% of larval mountain yellow-legged frogs (Rana mucosa )
in the Sierra Nevada of California (Fellers et al., 2001). Reed et al. (2000)
reported the occurrence of a variety of Chlamydia species that causes respiratory
disease of up to 90% of African clawed frogs (Xenopus tropicalis ) imported into
the United States. One breeding colony lost 90% of its individuals within 4
months because of this fungal infection. The fungal infection is not confined to
adult and larval frogs. Warkentin et al. (2001) showed that a filamentous
ascomycete fungus was found on 7% of the egg clutches of the Panamanian red-
eyed tree frog (Agalychnis callidryas ) and accounted for 40% of egg deaths
(Fig. 4.14).
Similarly, aquatic fungi, particularly members of the Phycomycetes, are
important pathogens of freshwater fish. Ogbonna and Alabi (1991) isolated
some 24 fungal species from fish in a Nigerian freshwater pond. With an
increasing development in fish farming in this country, the authors discuss
the greater need for evaluating the species of fungi responsible for infecting
fish, their relative pathogenicity, the need to find either chemical or
biological methods of control, as this developing economy could be of
importance to the country as a whole.

226 Chapter 4
FIGURE 4.14 Percentage of red-eyed treefrog egg mortality in laboratory-cultured egg

masses when infected by a pure culture of an ascomyete fungus inoculm introduced by
contaminated eggs, and from a natural population. Source: Data from Warkentin et al.
(2001).
4.5 FUNGAL– FAUNAL INTERACTIONS IN

AQUATIC AND MARINE ECOSYSTEMS
The role of fungi in aquatic ecosystems has been reviewed by Wong et al. (1998).
They suggest that some 600 fungal species are associated with aquatic
ecosystems and that their function ranges from saprotrophs to pathogens of both
plants and animals. In aquatic ecosystems interactions among fungi and
leaf-shredding fauna (Amphipoda, Isopoda, Diptera, Plecoptera, and Trichop-
tera) have been studied (Suberkropp, 1992). It has been suggested that fungal
degradation of the leaf litter “conditions” the leaf material to make it more
palatable for faunal grazing. These fungi alter the palatability of the litter
resource, alter its chemical composition, and appear to increase its food value.
Indeed, Bärlocher and Kendrick (1975) regard aquatic hyphomycetes as
intermediaries in the energy flow in stream ecosystems. They showed that the
amphipod Gammarus increased in weight faster in relation to the amount of food
ingested when provided by the fungi Humicola, Anguillospora, Clavariopsis,
Tricladium, or Fusarium, compared to a diet of elm or maple leaves.
The selection of leaves varies among animal species, the animals are
selective in the choice of fungal colonizers of the leaf material. Although the larvae
of Tipula spp. do not select leaves that have been colonized by fungi, other
shredder species do select colonized leaves. The amphipod (Gammarus

pseudolomnaeus ) has been shown to be selective among fungal species colonizing

leaf litter by favoring leaves colonized by some fungal species and not by others.
Gammarus pseudolimnaeus has been shown to have greater growth on leaves
colonized by four fungal species than six other fungal species. Trichopteran larvae
have also been shown to have significantly improved rates of growth on leaf litter
colonized by fungi than on uncolonized leaves. Contrary to the reports of
Bärlocher and Kendrick (1975), however, Suberkropp (1992) suggests that it is not
the fungus per se that elicits greater productivity of animals. Suberkropp (1992)
cites work showing that certain animals, such as the amphipod Gammarus and the
isopod Asellus, grew better on leaves colonized by fungi that when fed with the
fungi alone or the leaf litter alone. There is thus the suggestion of some synergistic
benefit. The mechanism for this, however, is unclear, as estimates show that fungal
biomass accounts for 1 – 5% of the detrital biomass in aquatic ecosystems. Fungi
make up 90 –95% of the microbial biomass on decaying leaves, however, which
suggests that bacteria are possibly less important as decomposers, at least in the
initial stages of leaf decomposition. This fungal biomass has been shown to be
insufficient to account for the increased rate of respiratory loss of carbon from
fungal colonized leaves. The fungal contribution to respiration accounts for
1 –57% of the total carbon respired. The most logical mechanism for enhanced
growth of animals grazing on fungal-colonized leaf litter is that the biochemical
changes in leaf chemistry caused by fungal attack improve the availability of
essential nutrients (particularly nitrogen) and readily assimilable energy sources.
In a study of the decomposition of alder and willow leaves in streams, Hieber and
Gessner (2002) showed that the shredder community counted for 64% and 51% of
the leaf litter mass loss for alder and willow, respectively. Fungi accounted for 15%
and 18% mass loss, respectively, and that for bacteria was only 7% and 9%,
respectively. Within this community of organisms, fungi were found to compose
95 –99% of the total microbial biomass, which is in line with values reported in
other studies. (See above.) Although fungi appear to dominate in these ecosystems,
Wong et al. (1998) conclude that we still know relatively little about the diversity
and functional role of these fungi.
In contrast to the terrestrial ecosystem, there is little evidence suggesting a
faunal grazing effect on the fungal community structure or biomass. Suberkropp
(1992) cites work showing that leaves incubated in fine mesh bags supported a
more diverse fungal community with a lower mass-specific sporulation rate than
leaves incubated in coarse mesh bags. This indicates a reduced biomass of fungi
under potentially higher grazing intensity, the stimulation of sporulation under a
more stressed (grazed) environment, and selective feeding by fauna or
differential resistance to grazing within the fungal community, leading to a
reduced fungal diversity in more heavily grazed conditions.
Fungi are important in marine and estuarine ecosystems. Although
information on their diversity, biomass, and function is limited and less than

228 Chapter 4
that for terrestrial and aquatic ecosystems, there is evidence to suggest that they
play a role in supporting faunal populations. Fungal biomass in the decomposing
material in salt marsh ecosystems is also important for the sustaining invertebrate
herbivore populations. The amphipod (Ulorchestia spartinophila ) has been shown
to have complex dietary requirements and appears to grow best and produce the
most offspring when fed on decaying leaves containing a high fungal biomass.
Kohlmeyer and Kohlmeyer (1979) show a table of 107 fungal species
isolated from decomposing wood in marine habitats. These include 73
Ascomycotina, two Basidiomycotina, and 29 mitosporic species. As in terrestrial
ecosystems, the low resource quality of wood appears to encourage tight linkages
between fungi and fauna for its decomposition. Evidence suggests that wood-
boring marine mollusks preferentially settle and feed on wood that has previously
been colonized by fungi and partially decomposed rather than invading fresh
wood. The associations have become so tight that, for example, the wood-boring
crustacean the gribble (Limnoria tripunctata ) has increased longevity when
feeding on wood colonized by fungi. More important, it is incapable of
reproduction on any substrate unless marine fungi are included as part of its diet.
This may be due to the enhanced availability of proteins, essential amino acids,
and vitamins, which are unavailable in the absence of fungi.
Fungi are major pathogens of marine animals (Hyde et al., 1998).
Mitosporic fungi have been shown to cause disease of crustaceans (Smolowitz
et al., 1992) and to cause damage to corals (Raghukumar and Raghukumar, 1991)
and juvenile clams (Norton et al., 1994). Norton et al. (1994) isolated demati-
atious fungal hyphae (Exserohilum rostratum and Curvularia spp.) from mantle
and shell of juvenile Tridacna crocea clams where they were associated with
decline in health. Many oomycetes are highly destructive pathogens in finfish,
mollusks, and shellfish (Noga, 1990). Very few fungi have been reported as
pathogens of marine plants, although some have been observed on leaves and
roots of mangrove. Many marine algae are susceptible to fungal pathogens,
however, primarily with chytrids and oomycetes. The impact of these pathogens
on production and fitness of their hosts has not been adequately investigated.
Certainly, Hyde et al. (1998) conclude in their review that the role of fungi in this
ecosystem requires considerably more research than has hitherto been devoted to
it. Although numerous fungal species have been isolated from marine habitats,
their function is largely unknown. Similarly, Wong et al. (1998) state that the role
of fungi as plant pathogens in aquatic ecosystems appears to be minor, but that
many fungi are pathogenic to animals. Citing the work of Thomas (1996), they
show that fungi are pathogens of fish, turtles, tadpoles, adult anurans, and many
invertebrates. There are, suggestions that fungi may potentially be used as
biocontrol agents for mosquitoes.
Like many terrestrial and aquatic arthropods, marine isopods contain fungi
in their gut to assist in the breakdown of plant food. Cafaro (2000) showed that

several genera and species of Patagonian intertidal isopods contained

Trichomycets of the genus Palavascia. A variety of gut symbionts, including
the cultured fungus Termitomyces, are found in the gut of termites for the same
reason (Wood and Thomas, 1989). In aquatic ecosystems, trichomycetes are also
found as endosymbionts in black fly larval guts (Beard and Adler, 2002). These
authors showed that there were significant differences in the abundance of
different fungal species among seasons, within sites, and among sites, although
no reason was given for the between-site differences. Beard and Adler (2002),
however, demonstrated than new recruits to the black fly larval population
rapidly became colonized by Harpella melusinae, suggesting a strong
dependence on this fungus as a gut symbiont.
4.6 SUMMARY AND CONCLUSIONS

As a component in the ecosystem, fungi are a good food resource for grazing
animals. Numerous vertebrate and invertebrate animals consume either the
fruiting structures or mycelia of fungi as the main component of their diet, or
more usually, as part of their diet. The fact that mushroom collecting and
consumption is a tradition in many European countries is testament to their food,
medicinal, and cultural value (Hudler, 1998). Indeed we point out in this chapter
that the cultivation of mushrooms for human consumption is a multimillion dollar
industry in the United States alone. It is thus not surprising that many animals use
fungi as a food source.
For vertebrate animals, the consumption of fungi for food is often part of
their diet. This part is especially important at times of the year when other foods
are scarce. In artic regions, for example, when the ground is snow-covered there
is little vascular plant food available. At this time, reindeer forage for lichens as
their main food source. In the same way, other vertebrates around the world,
particularly small mammals, make use of fungi at times when other food sources
are depleted or fungi are abundant. Many small mammals also forage below
ground for hypogeous fungi, whose spore dispersal is dependent on these
creatures. The degree of dependence of many animals on fungi as a food source is
still not entirely clear. What would be the impact on faunal populations and
communities of the removal of fungi from ecosystems?
For invertebrates, both the fruiting body and the mycelium form a food base.
The nutritional value of this food item is high, especially for certain groups, such as
nematodes. We have documented above the role that fungi play in the maintenance
of populations of fungivorous nematodes and that by selectively feeding on
specific fungal species the proportion of females in the population, their fecundity,
and hence the size of subsequent populations, can be strongly influenced (Ruess
and Dighton, 1996; Ruess et al., 2000). Soil arthropods are also somewhat

230 Chapter 4
dependent on fungal mycelia for their growth and development. Without fungi
many collembola and mite populations would be reduced in the soil.
As animals graze on fungi, they are able to affect the rate of fungal-
mediated ecosystem processes. The rate of decomposition of leaf litter is affected
by the rate of colonization of the litter by fungi. The rate of colonization can be
helped by the invasion of soil animals by the physical breakdown of leaf litter into
smaller parts (comminution) and the active transport of fungal inocula (spores of
hyphal fragments) into the leaf litter by animals (Ponge, 1990; 1991). The actual
effect of grazing on fungal mycelia can significantly alter its growth. Intense
grazing reduces hyphal growth, whereas moderate rates of grazing can stimulate
compensatory growth and actually increase fungal growth. This latter effect can
help fungi to grow and colonize new resources. As we have seen above, however,
like humans, animals are selective in what they eat. Selection of preferred fungal
species can benefit the animal by having a higher nutritional value than other
species or by avoidance of poisonous secondary metabolites. This selection
cannot be seen in the same way as fungal toxicity to humans, as many fungi that
are poisonous to us are the preferred choice of many invertebrates, which will
consume the fungi with no apparent harm! Selection of one fungus compared to
another provides an asymmetric selection pressure on the preferred fungal
species. Under intense grazing pressure, the growth of the preferred fungus will
decline in relation to the less preferred fungus. Grazing selection and intensity
can thus alter the outcome of competition of fungi within the community. A
classic example of this is given above, where the preferred grazing of Marasmius
and rocaceous over Mycena galopus by the collembolan Onychiurus armatus
resulted in both fungal species being displaced from their optimal habitat in the
forest floor of a Sitka spruce stand (Newell, 1984a,b). The impact of changes in
the distribution of fungi in the decomposer community can affect the rate of
decomposition of leaf litter and the rate of mineralization of nutrients. How
important are fungal grazers to the decomposition process? Given observations of
the feeding behavior of collembola in rhizotrons (Lussenhop, personal
communication, 2002) it would appear that collembola spend a great deal of
time grooming and then wandering around “nibbling” at fungal hyphae rather
than consuming large quantities at once. How important is their grazing, given
that once a fungal hyphum has been severed its translocatory function is
inhibited?
In the same way that soil fauna selectively graze saprotrophic fungi, they
also selectively consume mycorrhizal fungi. Again, given that a severed hyphum
is useless for the transport of water or nutrients to a host plant, how important is
the grazing of mycorrhizal mycelia to plant growth and fecundity? Much
information is given above on the detrimental effect of faunal grazing on
mycorrhizal fungi. Much of this information, however, has been gained from
studies in the greenhouse or laboratory or in the field at unrealistic densities of

animals. How important is this grazing in natural ecosystems? Is it enough to

cause significant decline in plant yield? Could this grazing be selective enough to
affect one plant species to a greater extent than another, thus altering plant
community structure?
It was mentioned above that animals are able to carry fungal propagules
either on their bodies or in their gut. This ability to transport fungal propagules is
important in spreading inocula through the ecosystem. It is so important that some
fungal groups have evolved to rely on faunal dispersal of their spores. Hypogeous
fungi, such as truffles, rely entirely on small mammals to consume the fruit body
and disseminate spores in their feces. Other fungi, such as the members of the
Phallales in the Gasteromycetes, have involved sticky, malodorous spore masses
that attract flies, which then disperse the spores. The dispersal of fungal propagules
can be important in providing, for example, mycorrhizal inoculum for plants
invading bare ground during primary or secondary succession. This aspect is
discussed in greater detail in the next chapter. Fungal spores can survive passage
through the guts of earthworms and soil arthropods, thereby being spread to new
resources, such as new organic sources for the saprotrophic fungal community or
roots for the mycorrhizal fungal community. Indeed, we have seen that some
animals, particularly earthworms, have potential as delivery systems of pathogenic
fungi to sites in which other pests reside in soil, and thus help in biological control
(Doube et al., 1994a,b; 1995).
During evolution, the close association between animals and fungi has
occasionally grown to be so close that the two are inseparable. Some species of
ants and termites rely on fungi as a food source to such an extent that they
actively cultivate the preferred fungal species within their colony’s nest. By
selective grazing, the most nutritious fungal material is fed to the developing
young. The colonies of fungi are also cleaned of any contaminating fungi that are
either less palatable or that may compete against the preferred fungal species. In
order to decompose high C:N ratio plant material of plant materials containing
high levels of lignin, fungal-derived enzymes are often necessary. In addition to
providing these enzymes, fungi are also able to translocate nutrients (particularly
nitrogen) into such recalcitrant plant materials. It is for this reason that we think
that bark beetles carry fungi in a specialized structure, or mycangium, on their
legs. The fungi decompose the wood in the phloem of the tree, translocate into
this wood nitrogen from more N-rich surrounding plant material, and make this
resource more palatable and nutritious for the developing beetle larvae. As we
note above, however, there may be more complex interactions with many more
players in the game. How many different scenarios are there in nature that make
use of multispecies interactions in the same way as that of bark beetle, phoretic
mite, and two competing fungi (Lombardero et al., 2000)?
Thus far we have seen that fungi are important as food sources for the growth
of faunal populations and that animals can help to alter fungal communities to either

232 Chapter 4
benefit or harm ecosystem processes. Fungi also act in a negative way on animal
populations. Almost all animals are subject to attack by pathogenic fungi. In some
animals the effect of a fungal pathogen is more dramatic than others. In particular,
entomopathogenic fungi that attack insects can be of importance in natural
ecosystems as regulators of populations. The effect of fungi appears to follow the
rules of density-dependent interactions, whereby the effect of the fungus on the
population is maximal when the animal population is at its peak (Kamata, 2000).
When environmental conditions are favorable for fungal growth, these pathogens
can cause devastating effects on a host animal. It is for this reason that many of these
fungi are being investigated as biocontrol agents of pests of crop plants. We outline
an interesting case in which nematode-trapping fungi can be introduced into
pastures through the feces of cattle to such densities that they significantly reduce
the population of juvenile forms of gut parasitic nematodes that reside in the soil.
The effect of these fungi significantly reduces the incidence of gut parasitic
nematodes in cattle and thus improves the yield of cattle and their products.
Fungal pathogens of frogs and fish can cause major declines in populations,
and fungal diseases of economically important mollusks, particularly bivalves,
can have serious economic impacts. From the perspective of conserving
biodiversity in the tropics, the decline in anuran populations due to fungal
pathogens is disturbing. Given the scenario of climate change producing
conditions conducive for fungal growth, how much more important will fungal
diseases of animal become?
From the information provided in this chapter we may conclude that
Rayner’s statement that fungi regulate populations of organisms is true for animals.
The degree to which fungi are involved in different groups of animals is variable,
and for some groups is largely unknown. Where fungi are not directly involved in
regulating the population of animals, either for the benefit or detriment of the
population, interactions among fungi and animals can take a multitude of forms and
have significant effects on ecosystem processes. One problem that we still face is
trying to interpolate to the real world from studies conducted under unrealistic
conditions. The effects of interactions among fungi and fauna seen in contrived
studies may not resemble those actually occurring in nature. This problem is not
confined to the study of fungi, but is common in many ecological studies.
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4

Fungi, Secondary Productivity,

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effect can be signiﬁcant in regulating the function of the fungal community in

4.1 FUNGI AS FOOD FOR SECONDARY

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TABLE 4.1 Ecosystem Services Provided by Fungi

Soil formation Rock dissolution Lichens

bodies of the hypogeous ectomycorrhizal fungus Elaphomyces granulatus, as

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TABLE 4.2 Protein and Mineral Content of a Range of Fungal Species

Fungal species Protein P Ca Mg K Na

Amanita muscaria 25 0.48 0.13 0.04 7.9 0.02

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4.1.1 Fungi in the Diet of Vertebrates

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4.1.2 Fungi in the Diet of Invertebrates

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Protein Fat Carbohydrate Ash

Fungi Agaricus bisporus 50 1.2 — 7

structures of basidiomycete fungi. Large, ﬂeshy mushrooms are often heavily

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TABLE 4.4 The Degree of Polyphagy in Diptera

Number of species used as

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TABLE 4.5 The Inﬂuence of Three Microfungi on the Numbers of Soil

Microarthropod Trichoderma Cladosporium Pythium Control

Mesostigmata 2 3 530 250

concluded that there was a consistent hierarchy of preferences (Table 4.6).

TABLE 4.6 Hierarchy of Feeding Preferences of the Collembolan Onichiurus

Mean percentage of fungal Mean fecal count per

Marasmius androsaceus 72.2 74.8

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Nematodes are ubiquitous in soils. Fungiverous nematodes may feed on a

TABLE 4.7 Numbers of Mixed Species Populations of Nematodes in Petri Plates

Mycorrhizal Lactarius rufus 25890 99

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Population after 4 weeks Mature females as percentage

Laccaria laccata 2.4 11.4

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A particularly good example of altered fungal competition mediated by soil

TABLE 4.9 Relationship Between the

Number of eggs Number of Epichloë

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4.2 EFFECTS OF GRAZING ON FUNGI AND

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the effect of grazing of fruit bodies of the wood-decomposing fungus Coriolus

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the community. Much more work is required, however, if we are to fully

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4.2.2 Inﬂuence of Faunal Grazing on Mycorrhizal

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TABLE 4.10 The Inﬂuence of Mycorrhizal Association of Lotus corniculatus on Plant

Nonmycorrhizal 23 3.9 5.8 40.5 13

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FIGURE 4.4 Principle coordinate analysis of ectomycorrhizae in protozoan species