A mole cricket. (After Eisenbeis & Wichard 1987.) Chapter 9 GROUND-DWELLING INSECTS TIC09 5/20/04 4:44 PM Page 217 218 Ground-dwelling insects A 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), and moths (Lepidoptera), may be abundant in litter and soils. For example, in Australian forests and wood- lands, the eucalypt leaf litter is consumed by larvae of many oecophorid moths and certain chrysomelid leaf beetles. The soil fauna also includes many non- insect hexapods (Collembola, Protura, and Diplura) and primitively wingless insects, the Archaeognatha and Zygentoma. Many Blattodea, Orthoptera, and Der- maptera occur only in terrestrial litter – a habitat to which 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. Certain arthropods may be confined to a particular layer or depth and show a distinct behavior and morphology appropriate 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 fur- cula, the characteristic collembolan springing organ. At intermediate soil depths, Hypogastrura has simple eyes, and short appendages with the furcula shorter than half the body length. In contrast, Collembola such as Orchesella that live amongst the superficial leaf litter have larger eyes, longer appendages, and an elongate furcula, more than half as long as the body. A suite of morphological variations can be seen in soil insects. Larvae often have well-developed legs to permit active movement through the soil, and pupae frequently have spinose transverse bands that assist movement to the soil surface for eclosion. Many adult soil-dwelling insects have reduced eyes and their wings are protected by hardened fore wings, or are reduced (brachypterous), or lost altogether (apterous) or, as in the reproductives of ants and termites, shed after the dispersal flight (deciduous, or caducous). Flightlessness (that is either through primary absence or secondary loss of wings) in ground-dwelling organisms may be countered by jumping as a means of evading predation: the collembolan furcula is a spring mechanism and the alticine Coleoptera (“flea-beetles”) and terrestrial Orthoptera can leap to safety. However, jumping is of little value in subterranean organisms. In these insects, the fore legs may be modified for digging (Fig. 9.2) as fossorial limbs, seen in groups that construct tunnels, TIC09 5/20/04 4:44 PM Page 218 Insects 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 to prevent flooding during rain, or the whole nest may be elevated to avoid excess ground moisture. Location and design of the nests of ants and termites is very import- ant to the regulation of humidity and temperature because, unlike social wasps and bees, they cannot ventilate their nests by fanning, although they can migrate 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 organisms living on the soil surface and in litter have longer legs than those found deeper in the ground. Organisms occurring deep in the soil usually are legless or have reduced legs; they are unpigmented and often blind. The organisms depicted are: (1) worker of a wood ant (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 muscid fly (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.) TIC09 5/20/04 4:44 PM Page 219 220 Ground-dwelling insects growth of particular fungi that serve as food (section 12.2.4). Many soil-dwelling hexapods derive their nutrition from ingesting large volumes of soil containing dead and decaying vegetable and animal debris and asso- ciated microorganisms. These bulk-feeders, known as saprophages or 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 possess symbiotic 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 a significant role in structuring soils of the tropics and subtropics. For arthropods that consume humic soils, the subsoil parts of plants (the roots) will be encountered fre- quently. The fine parts of roots often have particular associations with fungal mycorrhizae and rhizobac- teria, forming a zone called the rhizosphere. Bacterial and fungal densities are an order of magnitude higher in soil close to the rhizosphere compared with soil distant from roots, and microarthropod densities are correspondingly higher close to the rhizosphere. The selective grazing of Collembola, for example, can curtail growth of fungi that are pathogenic to plants, and their movements aid in transport of beneficial fungi and bac- teria to the rhizosphere. Furthermore, interactions between microarthropods and fungi in the rhizosphere and elsewhere may aid in mineralization of nitrogen and phosphates, making these elements available to plants; but further experimental evidence is required to quantify these beneficial roles. 9.1.1 Root-feeding insects Out-of-sight herbivores feeding on the roots of plants have been neglected in studies of insect–plant interac- tions, although it is recognized that 50–90% of plant biomass may be below ground. Root-feeding activities have 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), false wireworms (Tenebrionidae), weevils (Curculionidae), scarabaeids, flea-beetles, and galerucine chrysomelids may become evident only if the above-ground plants collapse. 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.) TIC09 5/20/04 4:44 PM Page 220 responses, 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 cause death of fire-damaged trees or those stressed by drought conditions. The role of bark beetles (Scolytus spp., Coleoptera: Curculionidae: Scolytinae) in the spread of Dutch elm disease is discussed in section 4.3.3. Other insect-borne fungal diseases transmitted to live trees may result in tree mortality, and continued decay of these and those that die of natural causes often involves further interactions between insects and fungi. The ambrosia beetles (Curculionidae: Platypodinae and some Scolytinae) are involved in a notable associ- ation with ambrosia fungus and dead wood, which has been popularly termed “the evolution of agriculture” in beetles. Adult beetles excavate tunnels (often called galleries), predominantly in dead wood (Fig. 9.3), although some attack live wood. Beetles mine in the phloem, wood, twigs, or woody fruits, which they infect with wood-inhabiting ectosymbiotic “ambrosia” fungi that they transfer in special cuticular pockets called mycangia, which store the fungi during the insects’ aestivation or dispersal. The fungi, which come from a wide taxonomic range, curtail plant defenses and break down wood making it more nutritious for the beetles. Both larvae and adults feed on the conditioned wood and directly on the extremely nutritious fungi. The association between ambrosia fungus and beetles appears to be very ancient, perhaps originating as long ago as 60 million years with gymnosperm host trees, but with subsequent increased diversity associated with multiple transfers to angiosperms. Some mycophagous insects, including beetles of the families Lathridiidae and Cryptophagidae, are strongly attracted 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 the underside of its pterothorax (Fig. 9.4), from which glandular secretions and material of the ascomycete fungus Trichoderma have been isolated. The beetle probably uses its legs to fill its mycangia with fungal material, which it transports to newly burnt habitats as an inoculum. Ascomycete fungi are important food sources for many pyrophilous insects, i.e. species strongly attracted to burning or newly burned areas or which occur mainly in burned forest for a few years after the fire. Some predatory and wood-feeding insects are also pyrophilous. A number of pyrophilous hetero- pterans (Aradidae), flies (Empididae and Platypezidae), and beetles (Carabidae and Buprestidae) have been shown to be attracted to the heat or smoke of fires, and Insects and dead trees or decaying wood 221 TIC09 5/20/04 4:44 PM Page 221 222 Ground-dwelling insects Box 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 insects because 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 cyst between spring and fall (depending on species) and, in species with males, comes to the soil surface where mating occurs. The female then buries back into the soil, 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 partheno- genetic species, females may never leave the soil. Adult females have no mouthparts and do not feed; in the soil, they secrete a waxy mass of white filaments – an ovisac, which surrounds their several hundred eggs. Although ground pearls can feed via their thread-like stylets, which protrude from the cyst, second-instar nymphs of most species are capable of prolonged dormancy (up to 17 years has been reported for one species). Often the encysted nymphs can be kept dry in the laboratory for one to several years and still be cap- able of “hatching” as adults. This long life and ability to rest dormant in the soil, together with resistance to desiccation, mean that they are difficult to eradicate from infested fields and even crop rotations do not eliminate them effectively. Furthermore, the protection afforded by the cyst wall and subterranean existence makes insecticidal control largely inappropriate. Many of these curious pestiferous insects are probably African and South American in origin and, prior to quar- antine restrictions, may have been transported within and between countries as cysts in soil or on rootstocks. TIC09 5/20/04 4:44 PM Page 222 often from a great distance. Species of jewel beetle (Buprestidae: Melanophila and Merimna) locate burnt wood by sensing the infrared radiation typically pro- duced by forest fires (section 4.2.1). Fallen, rotten timber provides a valuable resource for a wide variety of detritivorous insects if they can overcome 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, either through the possession of cellulase enzymes in their digestive systems and the use of gut symbionts (section 3.6.5) or with the assistance of fungi (section 9.5.3). Cockroaches and termites have been shown to produce endogenous cellulase that allows digestion of cellulose from the diet of rotting wood. Other xylophagous (wood-eating) strategies of insects include very long life cycles with slow development and probably the use of xylophagous microorganisms and fungi as food. 9.3 INSECTS AND DUNG The excreta or dung produced by vertebrates may be a rich source of nutrients. In the grasslands and range- lands of North America and Africa, large ungulates produce substantial volumes of fibrous and nitrogen- rich dung that contains many bacteria and protists. Insect coprophages (dung-feeding organisms) utilize this 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.) TIC09 5/20/04 4:44 PM Page 223 224 Ground-dwelling insects Haematobia 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 ungulates are absent, native dung beetles cannot exploit the volume and texture of dung produced by introduced domestic cattle, horses, and sheep. As a result, dung once lay around in pastures for prolonged periods, reducing the quality of pasture and allowing the development of prodigious numbers of nuisance flies. A program to introduce alien dung beetles from Africa and Mediterranean Europe has been successful in accelerating dung burial in many regions. 9.4 INSECT–CARRION INTERACTIONS In places where ants are important components of the fauna, the corpses of invertebrates are discovered and removed rapidly, by widely scavenging and efficient ants. In contrast, vertebrate corpses (carrion) support a wide diversity of organisms, many of which are insects. These form a succession – a non-seasonal, directional, and continuous sequential pattern of populations of species colonizing and being eliminated as carrion decay progresses. The nature and timing of the succes- sion depends upon the size of the corpse, seasonal and ambient 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, in the substrate immediately below the corpse, or in the soil at an intermediate distance below or away from the corpse. Furthermore, each succession will comprise different species in different geographical areas, even in places with similar climates. This is because few species are very widespread in distribution, and each biogeo- graphic area has its own specialist carrion faunas. However, the broad taxonomic categories of cadaver specialists 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- faction stage begins, followed by a fourth, butyric fer- mentation stage, in which the cheesy odor of butyric acid is present. This terminates in an almost dry carcass and 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 as following “waves” of colonization. The first wave TIC09 5/20/04 4:44 PM Page 224 involves 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 corpse turns rancid, a third wave of species enters this modified substrate, notably more dipterans, such as certain Phoridae, Drosophilidae, and Eristalis rat-tailed maggots (Syrphidae) in the liquid parts. As the corpse becomes butyric, a fourth wave of cheese-skippers (Diptera: Piophilidae) and related flies use the body. A fifth wave occurs as the ammonia-smelling carrion dries 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, which feeds on the dung; (c) pupa; and (d) adult just prior to emergence. (After Waterhouse 1974.) TIC09 5/20/04 4:44 PM Page 225 226 Ground-dwelling insects Cleridae (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 vari- ations in preferences for particular yeasts. The fungal component of lichens is probably used by grazing larval lepidopterans and adult plecopterans. Amongst the Diptera that utilize fungal fruiting bodies, the Mycetophilidae (fungus gnats) are diverse and speciose, and many appear to have oligophagous relationships with fungi from amongst a wide range used by the family. The use by insects of subterranean fungal bodies in the form of mycorrhizae and hyphae within the soil is poorly known. The phylogenetic rela- tionships of the Sciaridae (Diptera) to the mycetophilid “fungus gnats” and evidence from commercial mush- room farms all suggest that sciarid larvae normally eat fungal mycelia. Other dipteran larvae, such as certain phorids and cecidomyiids, feed on commercial mushroom mycelia and associated microorganisms, and may also use this resource in nature. 9.5.2 Fungus farming by leaf-cutter ants The subterranean ant nests of the genus Atta (15 spe- cies) and the rather smaller colonies of Acromyrmex (24 species) are amongst the major earthen construc- tions in neotropical rainforest. Calculations suggest that the largest nests of Atta species involve excavation of some 40 tonnes of soil. Both these genera are mem- bers of a tribe of myrmecine ants, the Attini, in which the larvae have an obligate dependence on symbiotic fungi for food. Other genera of Attini have monomor- phic workers (of a single morphology) and cultivate fungi on dead vegetable matter, insect feces (including their own and, for example, caterpillar “frass”), flowers, and fruit. In contrast, Atta and Acromyrmex, the more derived genera of Attini, have polymorphic workers of several different kinds or castes (section 12.2.3) that exhibit 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) and transport the pieces to the nest (Fig. 9.6b). During these processes, the working ant has its mandibles full, and may be the target of attack by a particular parasitic phorid fly (illustrated in the top right of Fig. 9.6a). The smallest worker is recruited as a defender, and is carried on the leaf fragment. When the material reaches the nest, other individu- als lick any waxy cuticle from the leaves and macerate the plant tissue with their mandibles. The mash is then TIC09 5/20/04 4:44 PM Page 226 [...]... least 45% of the original cellulose of fresh leaves converted by the time the spent substrate is ejected into a dung store as refuse from the fungus garden However, fungal gongylidia contribute only a modest fraction of the metabolic energy of the ants, because about 95 % of the respiratory requirements of the colony is provided by adults feeding on plant sap from chewed leaf fragments Leaf-cutter ants... utilize the abundant resource of dead vegetation TIC 09 5/20/04 4:44 PM Page 2 29 Environmental monitoring using ground-dwelling hexapods 9. 6 CAVERNICOLOUS INSECTS Caves often are perceived as extensions of the subterranean environment, resembling deep soil habitats in the lack of light and the uniform temperature, but differing in the scarcity of food Food sources in shallow caves include roots of terrestrial... (double-articulated) mandibles, and five-segmented maxillary palps The legs have large coxae and two- to five-segmented tarsi The abdomen continues the taper of the thorax, with segments 7 9 at least, but sometimes 2 9, bearing ventral musclecontaining styles; mature individuals may have a pair of protrusible vesicles medial to the styles on segments 2–7, although these are often reduced or absent The paired... (After Eibl-Eibesfeldt & Eibl-Eibesfeldt 196 7.) 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 undesirable... have shown them to utilize between 50 and 70% of all neotropical rainforest plant species However, as the adults feed on the sap of fewer species, and the larvae are monophagous on fungus, the term polyphagy strictly may be incorrect The key to the relationship is the ability of the worker ants to harvest from a wide variety of sources, and the cultivated fungus to grow on a wide range of hosts Coarse... Press, Cambridge Eisenbeis, G & Wichard, W ( 198 7) Atlas on the Biology of Soil Arthropods, 2nd edn Springer-Verlag, Berlin Hopkin, S.P ( 199 7) Biology of Springtails Oxford University Press, Oxford Lövei, G.L & Sunderland, K.D ( 199 6) Ecology and behaviour of ground beetles (Coleoptera: Carabidae) Annual Review of Entomology 41, 231–56 Lussenhop, J ( 199 2) Mechanisms of microarthropod– microbial interactions... McGeoch, M.A ( 199 8) The selection, testing and application of terrestrial insects as bioindicators Biological Reviews 73, 181–201 Mueller, U.G., Rehner, S.A & Schultz, T.R ( 199 8) The evolution of agriculture in ants Science 281, 203 9 New, T.R ( 199 8) Invertebrate Surveys for Conservation Oxford University Press, Oxford North, R.D., Jackson, C.W & Howse, P.E ( 199 7) Evolutionary aspects of ant–fungus... microfauna of tropical savannas (grasslands and open woodlands) and some forests of the Afrotropical and Oriental (Indo-Malayan) zoogeographic regions can be dominated by a single subfamily of Termitidae, the Macrotermitinae These termites may form conspicuous above-ground mounds up to 9 m high, but more often their nests consist of huge underground structures Abundance, density, and production of macrotermitines... females Copulation is end-to-end, and male spermatophores may be retained in the female for some months prior to fertilization Oviparous species lay eggs often in a burrow in debris (Fig 9. 1), guard the eggs and lick them to remove fungus The female may assist the nymphs to hatch from the eggs, and may care for them until the second or third instar, after which she may cannibalize her offspring Maturity... protecting the membranous hind wings; each tegmen lacks an anal lobe, and is dominated by branches of veins R and CuA In contrast, the hind wings have a large anal lobe, with many branches in the R, CuA, and anal sectors; at rest they lie folded fan-like beneath the tegmina Wing reduction is frequent The legs are often spinose (Fig 2. 19) and have five-segmented tarsi The large coxae abut each other and . complex circulation of air through the passageways of the nest, as illustrated for the above-ground nest of the African Macrotermes natalen- sis in Fig. 12.10. The origin of the mutualistic relationship. nature. 9. 5.2 Fungus farming by leaf-cutter ants The subterranean ant nests of the genus Atta (15 spe- cies) and the rather smaller colonies of Acromyrmex (24 species) are amongst the major earthen. refuse from the fungus garden. However, fun- gal gongylidia contribute only a modest fraction of the metabolic energy of the ants, because about 95 % of the respiratory requirements of the colony