The decompositional habitat, comprising decaying wood, leaf litter, carrion, and dung, is an integral part of the soil system.. In this chapter we consider the ecology and taxo-nomic ran
Trang 1A mole cricket (After Eisenbeis & Wichard 1987.)
Chapter 9
GR OUND-DWELLING INSECTS
Trang 2A profile of a typical soil shows an upper layer of
recently derived vegetational material, termed litter,
overlying more decayed material that intergrades with
humus-enriched organic soils These organic
mater-ials lie above mineralized soil layers, which vary with
local geology and climate, such as rainfall and
tem-perature Particle size and soil moisture are important
influences on the microdistributions of subterranean
organisms
The decompositional habitat, comprising decaying
wood, leaf litter, carrion, and dung, is an integral part
of the soil system The processes of decay of vegetation
and animal matter and return of nutrients to the soil
involve many organisms, notably fungi Fungal hyphae
and fruiting bodies provide a medium exploited by
many insects, and all faunas associated with
decompo-sitional substrates include insects and other hexapods
In this chapter we consider the ecology and
taxo-nomic range of soil and decompositional faunas in
relation to the differing macrohabitats of soil and
decaying vegetation and humus, dead and decaying
wood, dung, and carrion We survey the importance
of insect–fungal interactions and examine two intimate
associations A description of a specialized
subter-ranean habitat (caves) is followed by a discussion of
some uses of terrestrial hexapods in environmental
monitoring The chapter concludes with seven
taxo-nomic boxes that deal with: non-insect hexapods
(Collembola, Protura, and Diplura); primitively
wing-less bristletails and silverfish (Archaeognatha and
Zygentoma); three small hemimetabolous orders, the
Grylloblattodea, Embiidina, and Zoraptera; earwigs
(Dermaptera); and cockroaches (Blattodea)
9.1 INSECTS OF LITTER AND SOIL
Litter is fallen vegetative debris, comprising materials
such as leaves, twigs, wood, fruit, and flowers in
various states of decay The processes that lead to the
incorporation of recently fallen vegetation into the
humus layer of the soil involve degradation by
micro-organisms, such as bacteria, protists, and fungi The
actions of nematodes, earthworms, and terrestrial
arthropods, including crustaceans, mites, and a range
of hexapods (Fig 9.1), mechanically break down large
particles and deposit finer particles as feces Acari
(mites), termites (Isoptera), ants (Formicidae), and
many beetles (Coleoptera) are important arthropods
of litter and humus-rich soils The immature stages of
many insects, including beetles, flies (Diptera), andmoths (Lepidoptera), may be abundant in litter andsoils For example, in Australian forests and wood-lands, the eucalypt leaf litter is consumed by larvae
of many oecophorid moths and certain chrysomelidleaf beetles The soil fauna also includes many non-insect hexapods (Collembola, Protura, and Diplura)and primitively wingless insects, the Archaeognathaand Zygentoma Many Blattodea, Orthoptera, and Der-maptera occur only in terrestrial litter – a habitat towhich several of the minor orders of insects, the Zor-aptera, Embiidina, and Grylloblattodea, are restricted.Soils that are permanently or regularly waterlogged,such as marshes and riparian (stream marginal) hab-itats, intergrade into the fully aquatic habitats described
in Chapter 10 and show faunal similarities
In a soil profile, the transition from the upper,recently fallen litter to the lower well-decomposed litter
to the humus-rich soil below may be gradual Certainarthropods may be confined to a particular layer ordepth and show a distinct behavior and morphologyappropriate to the depth For example, amongst the
Collembola, Onychurus lives in deep soil layers and has
reduced appendages, is blind and white, and lacks a cula, the characteristic collembolan springing organ
fur-At intermediate soil depths, Hypogastrura has simple
eyes, and short appendages with the furcula shorterthan half the body length In contrast, Collembola such
as Orchesella that live amongst the superficial leaf litter
have larger eyes, longer appendages, and an elongatefurcula, more than half as long as the body
A suite of morphological variations can be seen insoil insects Larvae often have well-developed legs topermit active movement through the soil, and pupaefrequently have spinose transverse bands that assistmovement to the soil surface for eclosion Many adultsoil-dwelling insects have reduced eyes and their wingsare protected by hardened fore wings, or are reduced(brachypterous), or lost altogether (apterous) or, as
in the reproductives of ants and termites, shed after thedispersal flight (deciduous, or caducous) Flightlessness(that is either through primary absence or secondaryloss of wings) in ground-dwelling organisms may becountered by jumping as a means of evading predation:the collembolan furcula is a spring mechanism and the alticine Coleoptera (“flea-beetles”) and terrestrialOrthoptera can leap to safety However, jumping is oflittle value in subterranean organisms In these insects,the fore legs may be modified for digging (Fig 9.2) as
fossoriallimbs, seen in groups that construct tunnels,
Trang 3Insects of litter and soil 219
such as mole crickets (as depicted in the vignette of this
chapter), immature cicadas, and many beetles
The distribution of subterranean insects changes
seasonally The constant temperatures at greater soil
depths are attractive in winter as a means of avoiding
low temperatures above ground The level of water in
the soil is important in governing both vertical and
horizontal distributions Frequently, larvae of
subter-ranean insects that live in moist soils will seek drier sites
for pupation, perhaps to reduce the risks of fungal
dis-ease during the immobile pupal stage The
subter-ranean nests of ants usually are located in drier areas,
or the nest entrance is elevated above the soil surface toprevent flooding during rain, or the whole nest may beelevated to avoid excess ground moisture Location anddesign of the nests of ants and termites is very import-ant to the regulation of humidity and temperaturebecause, unlike social wasps and bees, they cannotventilate their nests by fanning, although they canmigrate within nests or, in some species, between them.The passive regulation of the internal nest environ-
ment is exemplified by termites of Amitermes (see Fig 12.9) and Macrotermes (see Fig 12.10), which
maintain an internal environment suitable for the
Fig 9.1 Diagrammatic view of a soil profile showing some typical litter and soil insects and other hexapods Note that organismsliving on the soil surface and in litter have longer legs than those found deeper in the ground Organisms occurring deep in the soilusually are legless or have reduced legs; they are unpigmented and often blind The organisms depicted are: (1) worker of a woodant (Hymenoptera: Formicidae); (2) springtail (Collembola: Isotomidae); (3) ground beetle (Coleoptera: Carabidae); (4) rove beetle (Coleoptera: Staphylinidae) eating a springtail; (5) larva of a crane fly (Diptera: Tipulidae); (6) japygid dipluran (Diplura:Japygidae) attacking a smaller campodeid dipluran; (7) pupa of a ground beetle (Coleoptera: Carabidae); (8) bristletail
(Archaeognatha: Machilidae); (9) female earwig (Dermaptera: Labiduridae) tending her eggs; (10) wireworm, larva of a
tenebrionid beetle (Coleoptera: Tenebrionidae); (11) larva of a robber fly (Diptera: Asilidae); (12) larva of a soldier fly (Diptera:Stratiomyidae); (13) springtail (Collembola: Isotomidae); (14) larva of a weevil (Coleoptera: Curculionidae); (15) larva of a muscidfly (Diptera: Muscidae); (16) proturan (Protura: Sinentomidae); (17) springtail (Collembola: Isotomidae); (18) larva of a March fly(Diptera: Bibionidae); (19) larva of a scarab beetle (Coleoptera: Scarabaeidae) (Individual organisms after various sources,especially Eisenbeis & Wichard 1987.)
Trang 4growth of particular fungi that serve as food (section12.2.4).
Many soil-dwelling hexapods derive their nutritionfrom ingesting large volumes of soil containing deadand decaying vegetable and animal debris and asso-ciated microorganisms These bulk-feeders, known as
saprophagesor detritivores, include hexapods such
as some Collembola, beetle larvae, and certain termites
(Isoptera: Termitinae, including Termes and relatives).
Although these have not been demonstrated to possesssymbiotic gut protists they appear able to digest cellu-lose from the humus layers of the soil Copious excreta(feces) is produced and these organisms clearly play asignificant role in structuring soils of the tropics andsubtropics
For arthropods that consume humic soils, the subsoilparts of plants (the roots) will be encountered fre-quently The fine parts of roots often have particularassociations with fungal mycorrhizae and rhizobac-teria, forming a zone called the rhizosphere Bacterialand fungal densities are an order of magnitude higher
in soil close to the rhizosphere compared with soil distant from roots, and microarthropod densities arecorrespondingly higher close to the rhizosphere Theselective grazing of Collembola, for example, can curtailgrowth of fungi that are pathogenic to plants, and theirmovements aid in transport of beneficial fungi and bac-teria to the rhizosphere Furthermore, interactionsbetween microarthropods and fungi in the rhizosphereand elsewhere may aid in mineralization of nitrogenand phosphates, making these elements available toplants; but further experimental evidence is required toquantify these beneficial roles
9.1.1 Root-feeding insects
Out-of-sight herbivores feeding on the roots of plantshave been neglected in studies of insect–plant interac-tions, although it is recognized that 50 –90% of plantbiomass may be below ground Root-feeding activitieshave been difficult to quantify in space and time, even
for charismatic taxa like the periodic cicadas (Magicicada
spp.) The damaging effects caused by root chewers and miners such as larvae of hepialid and ghost moths,and beetles including wireworms (Elateridae), falsewireworms (Tenebrionidae), weevils (Curculionidae),scarabaeids, flea-beetles, and galerucine chrysomelidsmay become evident only if the above-ground plantscollapse However, lethality is one end of a spectrum of
Fig 9.2 Fossorial fore legs of: (a) a mole cricket of Gryllotalpa
(Orthoptera: Gryllotalpidae); (b) a nymphal periodical cicada
of Magicicada (Hemiptera: Cicadidae); and (c) a scarab beetle
of Canthon (Coleoptera: Scarabaeidae) ((a) After Frost 1959;
(b) after Snodgrass 1967; (c) after Richards & Davies 1977.)
Trang 5responses, with some plants responding with increased
above-ground growth to root grazing, others neutral
(perhaps through resistance), and others sustaining
subcritical damage Sap-sucking insects on the plant
roots such as some aphids (Box 11.2) and scale insects
(Box 9.1) cause loss of plant vigor, or death, especially if
insect-damaged necrotized tissue is invaded
secondar-ily by fungi and bacteria Although when the nymphs
of periodic cicadas occur in orchards they can cause
serious damage, the nature of the relationship with the
roots upon which they feed remains poorly known (see
also section 6.10.5)
Soil-feeding insects probably do not selectively avoid
the roots of plants Thus, where there are high densities
of fly larvae that eat soil in pastures, such as Tipulidae
(leatherjackets), Sciaridae (black fungus gnats), and
Bibionidae (March flies), roots are damaged by their
activities There are frequent reports of such activities
causing economic damage in managed pastures, golf
courses, and turf-production farms
The use of insects as biological control agents
for control of alien/invasive plants has emphasized
phytophages of above-ground parts such as seeds
and leaves (see section 11.2.6) but has neglected
root-damaging taxa Even with increased recognition of
their importance, 10 times as many above-ground
con-trol agents are released compared to root feeders By the
year 2000, over 50% of released root-feeding biological
control agents contributed to the suppression of target
invasive plants; in comparison about 33% of the
above-ground biological control agents contributed some
sup-pression of their host plant Coleoptera, particularly
Curculionidae and Chrysomelidae, appear to be most
successful in control, whereas Lepidoptera and Diptera
are less so
9.2 INSECTS AND DEAD TREES OR
DECAYING WOOD
The death of trees may involve insects that play a role in
the transmission of pathogenic fungi amongst trees
Thus, wood wasps of the genera Sirex and Urocercus
(Hymenoptera: Siricidae) carry Amylostereum fungal
spores in invaginated intersegmental sacs connected to
the ovipositor During oviposition, spores and mucus
are injected into the sapwood of trees, notably Pinus
species, causing mycelial infection The infestation
causes locally drier conditions around the xylem,
which is optimal for development of larval Sirex The
fungal disease in Australia and New Zealand can causedeath of fire-damaged trees or those stressed by drought
conditions The role of bark beetles (Scolytus spp.,
Coleoptera: Curculionidae: Scolytinae) in the spread ofDutch elm disease is discussed in section 4.3.3 Otherinsect-borne fungal diseases transmitted to live treesmay result in tree mortality, and continued decay ofthese and those that die of natural causes often involvesfurther interactions between insects and fungi
The ambrosia beetles (Curculionidae: Platypodinaeand some Scolytinae) are involved in a notable associ-ation with ambrosia fungus and dead wood, which hasbeen popularly termed “the evolution of agriculture”
in beetles Adult beetles excavate tunnels (often calledgalleries), predominantly in dead wood (Fig 9.3),although some attack live wood Beetles mine in thephloem, wood, twigs, or woody fruits, which they infectwith wood-inhabiting ectosymbiotic “ambrosia” fungithat they transfer in special cuticular pockets called
mycangia, which store the fungi during the insects’aestivation or dispersal The fungi, which come from awide taxonomic range, curtail plant defenses and breakdown wood making it more nutritious for the beetles.Both larvae and adults feed on the conditioned woodand directly on the extremely nutritious fungi Theassociation between ambrosia fungus and beetlesappears to be very ancient, perhaps originating as longago as 60 million years with gymnosperm host trees,but with subsequent increased diversity associatedwith multiple transfers to angiosperms
Some mycophagous insects, including beetles of thefamilies Lathridiidae and Cryptophagidae, are stronglyattracted to recently burned forest to which they carry
fungi in mycangia The cryptophagid beetle Henoticus
serratus, which is an early colonizer of burned forest in
some areas of Europe, has deep depressions on theunderside of its pterothorax (Fig 9.4), from whichglandular secretions and material of the ascomycete
fungus Trichoderma have been isolated The beetle
probably uses its legs to fill its mycangia with fungalmaterial, which it transports to newly burnt habitats as
an inoculum Ascomycete fungi are important foodsources for many pyrophilous insects, i.e speciesstrongly attracted to burning or newly burned areas orwhich occur mainly in burned forest for a few yearsafter the fire Some predatory and wood-feeding insectsare also pyrophilous A number of pyrophilous hetero-pterans (Aradidae), flies (Empididae and Platypezidae),and beetles (Carabidae and Buprestidae) have beenshown to be attracted to the heat or smoke of fires, and
Insects and dead trees or decaying wood 221
Trang 6Box 9.1 Ground pearls
In parts of Africa, the encysted nymphs (“ground
pearls”) of certain subterranean scale insects are
some-times made into necklaces by the local people These
nymphal insects have few cuticular features, except for
their spiracles and sucking mouthparts They secrete
a transparent or opaque, glassy or pearly covering
that encloses them, forming spherical to ovoid “cysts”
of greatest dimension 1– 8 mm, depending on
spe-cies Ground pearls belong to several genera of
Margarodinae (Hemiptera: Margarodidae), including
Eumargarodes, Margarodes, Neomargarodes,
Porphy-rophora, and Promargarodes They occur worldwide in
soils among the roots of grasses, especially sugarcane,
and grape vines (Vitis vinifera) They may be abundant
and their nymphal feeding can cause loss of plant vigor
and death; in lawns, feeding results in brown patches of
dead grass In South Africa they are serious vineyard
pests; in Australia different species reduce sugarcane
yield; and in the south-eastern USA one species is a
grass pest
Plant damage mostly is caused by the female insectsbecause many species are parthenogenetic, or at least
males have never been found, and when males are
present they are smaller than the females There are
three female instars (as illustrated here for Margarodes
(= Sphaeraspis) capensis, after De Klerk et al 1982): the
first-instar nymph disperses in the soil seeking a
feed-ing site on roots, where it molts to the second-instar or
cyst stage; the adult female emerges from the cystbetween spring and fall (depending on species) and, inspecies with males, comes to the soil surface wheremating occurs The female then buries back into thesoil, digging with its large fossorial fore legs The fore-leg coxa is broad, the femur is massive, and the tarsus
is fused with the strongly sclerotized claw In genetic species, females may never leave the soil Adultfemales have no mouthparts and do not feed; in the soil,they secrete a waxy mass of white filaments – anovisac, which surrounds their several hundred eggs.Although ground pearls can feed via their thread-likestylets, which protrude from the cyst, second-instarnymphs of most species are capable of prolonged dormancy (up to 17 years has been reported for onespecies) Often the encysted nymphs can be kept dry inthe laboratory for one to several years and still be cap-able of “hatching” as adults This long life and ability
partheno-to rest dormant in the soil, partheno-together with resistance partheno-todesiccation, mean that they are difficult to eradicatefrom infested fields and even crop rotations do not eliminate them effectively Furthermore, the protectionafforded by the cyst wall and subterranean existencemakes insecticidal control largely inappropriate Many
of these curious pestiferous insects are probablyAfrican and South American in origin and, prior to quar-antine restrictions, may have been transported withinand between countries as cysts in soil or on rootstocks
Trang 7often from a great distance Species of jewel beetle
(Buprestidae: Melanophila and Merimna) locate burnt
wood by sensing the infrared radiation typically duced by forest fires (section 4.2.1)
pro-Fallen, rotten timber provides a valuable resource for a wide variety of detritivorous insects if they canovercome the problems of living on a substrate rich
in cellulose and deficient in vitamins and sterols.Termites are able to live entirely on this diet, eitherthrough the possession of cellulase enzymes in theirdigestive systems and the use of gut symbionts (section3.6.5) or with the assistance of fungi (section 9.5.3).Cockroaches and termites have been shown to produceendogenous cellulase that allows digestion of cellulosefrom the diet of rotting wood Other xylophagous
(wood-eating) strategies of insects include very long lifecycles with slow development and probably the use ofxylophagous microorganisms and fungi as food
9.3 INSECTS AND DUNG
The excreta or dung produced by vertebrates may be arich source of nutrients In the grasslands and range-lands of North America and Africa, large ungulatesproduce substantial volumes of fibrous and nitrogen-rich dung that contains many bacteria and protists.Insect coprophages(dung-feeding organisms) utilizethis resource in a number of ways Certain higher flies – such as the Scathophagidae, Muscidae (notably the
worldwide house fly, Musca domestica, the Australian
M vetustissima, and the widespread tropical buffalo fly,
Insects and dung 223
Fig 9.3 A plume-shaped tunnel excavated by the bark
beetle Scolytus unispinosus (Coleoptera: Scolytidae) showing
eggs at the ends of a number of galleries; enlargement shows
an adult beetle (After Deyrup 1981.)
Fig 9.4 Underside of the thorax of the
beetle Henoticus serratus (Coleoptera:
Cryptophagidae) showing the
depressions, called mycangia, which the
beetle uses to transport fungal material
that inoculates new substrate on recently
burnt wood (After drawing by Göran
Sahlén in Wikars 1997.)
Trang 8Haematobia irritans), Faniidae, and Calliphoridae –
oviposit or larviposit into freshly laid dung
Devel-opment can be completed before the medium becomes
too desiccated Within the dung medium, predatory
fly larvae (notably other species of Muscidae) can
seri-ously reduce survival of coprophages However, in
the absence of predators or disturbance of the dung,
nuisance-level populations of flies can be generated
from larvae developing in dung in pastures
The insects primarily responsible for disturbing
dung, and thereby limiting fly breeding in the medium,
are dung beetles, belonging to the family Scarabaeidae
Not all larvae of scarabs use dung: some ingest general
soil organic matter, whereas some others are
herbivor-ous on plant roots However, many are coprophages
In Africa, where many large herbivores produce large
volumes of dung, several thousand species of scarabs
show a wide variety of coprophagous behaviors Many
can detect dung as it is deposited by a herbivore, and
from the time that it falls to the ground invasion is very
rapid Many individuals arrive, perhaps up to many
thousands for a single fresh elephant dropping Most
dung beetles excavate networks of tunnels immediately
beneath or beside the pad (also called a pat), and pull
down pellets of dung (Fig 9.5) Other beetles excise a
chunk of dung and move it some distance to a dug-out
chamber, also often within a network of tunnels This
movement from pad to nest chamber may occur either
by head-butting an unformed lump, or by rolling
molded spherical balls over the ground to the burial
site The female lays eggs into the buried pellets, and the
larvae develop within the fecal food ball, eating fine and
coarse particles The adult scarabs also may feed on
dung, but only on the fluids and finest particulate
matter Some scarabs are generalists and utilize
virtu-ally any dung encountered, whereas others specialize
according to texture, wetness, pad size, fiber content,
geographical area, and climate; a range of scarab
activ-ities ensures that all dung is buried within a few days
at most
In tropical rainforests, an unusual guild of dung
beetles has been recorded foraging in the tree canopy
on every subcontinent These specialist coprophages
have been studied best in Sabah, Borneo, where a few
species of Onthophagus collect the feces of primates
(such as gibbons, macaques, and langur monkeys)
from the foliage, form it into balls and push the balls
over the edge of leaves If the balls catch on the foliage
below, then the dung-rolling activity continues until
the ground is reached
In Australia, a continent in which native ungulatesare absent, native dung beetles cannot exploit the volume and texture of dung produced by introduceddomestic cattle, horses, and sheep As a result, dungonce lay around in pastures for prolonged periods,reducing the quality of pasture and allowing the development of prodigious numbers of nuisance flies Aprogram to introduce alien dung beetles from Africaand Mediterranean Europe has been successful inaccelerating dung burial in many regions
9.4 INSECT–CARRION INTERACTIONS
In places where ants are important components of thefauna, the corpses of invertebrates are discovered andremoved rapidly, by widely scavenging and efficientants In contrast, vertebrate corpses (carrion) support awide diversity of organisms, many of which are insects.These form a succession– a non-seasonal, directional,and continuous sequential pattern of populations ofspecies colonizing and being eliminated as carriondecay progresses The nature and timing of the succes-sion depends upon the size of the corpse, seasonal andambient climatic conditions, and the surrounding non-biological (edaphic) environment, such as soil type.The organisms involved in the succession vary accord-ing to whether they are upon or within the carrion, inthe substrate immediately below the corpse, or in thesoil at an intermediate distance below or away from the corpse Furthermore, each succession will comprisedifferent species in different geographical areas, even inplaces with similar climates This is because few speciesare very widespread in distribution, and each biogeo-graphic area has its own specialist carrion faunas.However, the broad taxonomic categories of cadaverspecialists are similar worldwide
The first stage in carrion decomposition, initial decay, involves only microorganisms already present
in the body, but within a few days the second stage,called putrefaction, begins About two weeks later,amidst strong odors of decay, the third, black putre- factionstage begins, followed by a fourth, butyric fer- mentationstage, in which the cheesy odor of butyricacid is present This terminates in an almost dry carcassand the fifth stage, slow dry decay, completes the pro-cess, leaving only bones
The typical sequence of corpse necrophages,saprophages, and their parasites is often referred to asfollowing “waves” of colonization The first wave
Trang 9involves certain blow flies (Diptera: Calliphoridae) and
house flies (Muscidae) that arrive within hours or a few
days at most The second wave is of sarcophagids
(Diptera) and additional muscids and calliphorids that
follow shortly thereafter, as the corpse develops an
odor All these flies either lay eggs or larviposit on the
corpse The principal predators on the insects of the
corpse fauna are staphylinid, silphid, and histerid
beetles, and hymenopteran parasitoids may be
ento-mophagous on all the above hosts At this stage, blow
fly activity ceases as their larvae leave the corpse and pupate in the ground When the fat of the corpseturns rancid, a third wave of species enters thismodified substrate, notably more dipterans, such as
certain Phoridae, Drosophilidae, and Eristalis rat-tailed
maggots (Syrphidae) in the liquid parts As the corpsebecomes butyric, a fourth wave of cheese-skippers(Diptera: Piophilidae) and related flies use the body
A fifth wave occurs as the ammonia-smelling carriondries out, and adult and larval Dermestidae and
Insect–carrion interactions 225
Fig 9.5 A pair of dung beetles of Onthophagus gazella (Coleoptera: Scarabaeidae) filling in the tunnels that they have excavated
below a dung pad The inset shows an individual dung ball within which beetle development takes place: (a) egg; (b) larva, whichfeeds on the dung; (c) pupa; and (d) adult just prior to emergence (After Waterhouse 1974.)
Trang 10Cleridae (Coleoptera) become abundant, feeding on
keratin In the final stages of dry decay, some tineid
larvae (“clothes moths”) feed on any remnant hair
Immediately beneath the corpse, larvae and adults
of the beetle families Staphylinidae, Histeridae, and
Dermestidae are abundant during the putrefaction
stage However, the normal, soil-inhabiting groups are
absent during the carrion phase, and only slowly
return as the corpse enters late decay The rather
pre-dictable sequence of colonization and extinction of
carrion insects allows forensic entomologists to
estim-ate the age of a corpse, which can have medico-legal
implications in homicide investigations (section 15.6)
9.5 INSECT–FUNGAL INTERACTIONS
9.5.1 Fungivorous insects
Fungi and, to a lesser extent, slime molds are eaten by
many insects, termed fungivores or mycophages,
which belong to a range of orders Amongst insects that
use fungal resources, Collembola and larval and adult
Coleoptera and Diptera are numerous Two feeding
strategies can be identified: microphages gather
small particles such as spores and hyphal fragments
(see Plate 3.7, facing p 14) or use more liquid media;
whereas macrophages use the fungal material of
fruiting bodies, which must be torn apart with strong
mandibles The relationship between fungivores and
the specificity of their fungus feeding varies Insects
that develop as larvae in the fruiting bodies of large
fungi are often obligate fungivores, and may even be
restricted to a narrow range of fungi; whereas insects
that enter such fungi late in development or during
actual decomposition of the fungus are more likely to
be saprophagous or generalists than specialist
myco-phages Longer-lasting macrofungi such as the pored
mushrooms, Polyporaceae, have a higher proportion of
mono- or oligophagous associates than ephemeral and
patchily distributed mushrooms such as the gilled
mushrooms (Agaricales)
Smaller and more cryptic fungal food resources also
are used by insects, but the associations tend to be less
well studied Yeasts are naturally abundant on live and
fallen fruits and leaves, and fructivores(fruit-eaters)
such as larvae of certain nitidulid beetles and
droso-philid fruit flies are known to seek and eat yeasts
Apparently, fungivorous drosophilids that live in
decomposing fruiting bodies of fungi also use yeasts,
and specialization on particular fungi may reflect ations in preferences for particular yeasts The fungalcomponent of lichens is probably used by grazing larvallepidopterans and adult plecopterans
vari-Amongst the Diptera that utilize fungal fruiting bodies, the Mycetophilidae (fungus gnats) are diverseand speciose, and many appear to have oligophagousrelationships with fungi from amongst a wide rangeused by the family The use by insects of subterraneanfungal bodies in the form of mycorrhizae and hyphaewithin the soil is poorly known The phylogenetic rela-tionships of the Sciaridae (Diptera) to the mycetophilid
“fungus gnats” and evidence from commercial room farms all suggest that sciarid larvae normally eat fungal mycelia Other dipteran larvae, such as certain phorids and cecidomyiids, feed on commercialmushroom mycelia and associated microorganisms,and may also use this resource in nature
mush-9.5.2 Fungus farming by leaf-cutter ants
The subterranean ant nests of the genus Atta (15 cies) and the rather smaller colonies of Acromyrmex
spe-(24 species) are amongst the major earthen tions in neotropical rainforest Calculations suggest
construc-that the largest nests of Atta species involve excavation
of some 40 tonnes of soil Both these genera are bers of a tribe of myrmecine ants, the Attini, in whichthe larvae have an obligate dependence on symbioticfungi for food Other genera of Attini have monomor-phic workers (of a single morphology) and cultivatefungi on dead vegetable matter, insect feces (includingtheir own and, for example, caterpillar “frass”), flowers,
mem-and fruit In contrast, Atta mem-and Acromyrmex, the more
derived genera of Attini, have polymorphic workers
of several different kinds or castes (section 12.2.3) thatexhibit an elaborate range of behaviors including cutting living plant tissues, hence the name “leaf-cutter
ants” In Atta, the largest worker ants excise sections of
live vegetation with their mandibles (Fig 9.6a) andtransport the pieces to the nest (Fig 9.6b) During theseprocesses, the working ant has its mandibles full, andmay be the target of attack by a particular parasiticphorid fly (illustrated in the top right of Fig 9.6a) Thesmallest worker is recruited as a defender, and is carried
on the leaf fragment
When the material reaches the nest, other als lick any waxy cuticle from the leaves and maceratethe plant tissue with their mandibles The mash is then
Trang 11individu-inoculated with a fecal cocktail of enzymes from
the hindgut This initiates digestion of the fresh plant
material, which acts as an incubation medium for a
fungus, known only from these “fungus gardens” of
leaf-cutter ants Another specialized group of workers
tends the gardens by inoculating new substrate with
fungal hyphae and removing other species of
undesir-able fungi in order to maintain a monoculture Control
of alien fungi and bacteria is facilitated by pH
regula-tion (4.5 –5.0) and by antibiotics, including those
pro-duced by mutualistic Streptomyces bacteria associated
with ant cuticle In darkness, and at optimal humidity
and a temperature close to 25°C, the cultivated fungal
mycelia produce nutritive hyphal bodies called
gongy-lidia These are not sporophores, and appear to have
no function other than to provide food for ants in a
mutualistic relationship in which the fungus gains
access to the controlled environment Gongylidia are
manipulated easily by the ants, providing food for
adults, and are the exclusive food eaten by larval attine
ants Digestion of fungi requires specialized enzymes,
which include chitinases produced by ants from their
labial glands
A single origin of fungus domestication might beexpected given the vertical transfer of fungi by trans-port in the mouth of the founding gyne (new queen)and regurgitation at the new site However, molecularphylogenetic studies of the fungi show domesticationfrom free-living stocks has taken place several times,although the ancestral symbiosis is at least 50 millionyears old All but one domesticate belongs to theBasidiomycetes of the tribe Leucocoprini in the familyLepiotaceae, propagated as a mycelium or occasionally
as a unicellular yeast Although each attine nest has
a single species of fungus, amongst different nests of asingle species a range of fungus species are tended.Obviously, some ant species can change their funguswhen a new nest is constructed, perhaps when colonyfoundation is by more than one queen (pleiometrosis).Lateral (horizontal) transfer was observed when a
Central American Atta species introduced to Florida
rapidly adopted the local attine-tended fungus for itsgardens
Leaf-cutter ants dominate the ecosystems in which
they occur; some grassland Atta species consume as
much vegetation per hectare as domestic cattle, and
Insect–fungal interactions 227
Fig 9.6 The fungus gardens of the leaf-cutter ant, Atta cephalotes (Formicidae), require a constant supply of leaves (a) A
medium-sized worker, called a media, cuts a leaf with its serrated mandibles while a minor worker guards the media from a
parasitic phorid fly (Apocephalus) that lays its eggs on living ants (b) A guarding minor hitchhikes on a leaf fragment carried by a
media (After Eibl-Eibesfeldt & Eibl-Eibesfeldt 1967.)