The Insects - Outline of Entomology 3th Edition - Chapter 9 ppt

A mole cricket. (After Eisenbeis & Wichard 1987.)
Chapter 9
GROUND-DWELLING
INSECTS
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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,
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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.)
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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.)
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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
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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.
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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.)
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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
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 be
expected 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, molecular
phylogenetic studies of the fungi show domestication
from free-living stocks has taken place several times,
although the ancestral symbiosis is at least 50 million
years old. All but one domesticate belongs to the
Basidiomycetes of the tribe Leucocoprini in the family
Lepiotaceae, propagated as a mycelium or occasionally
as a unicellular yeast. Although each attine nest has
a single species of fungus, amongst different nests of a
single species a range of fungus species are tended.
Obviously, some ant species can change their fungus
when a new nest is constructed, perhaps when colony
foundation 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 its
gardens.
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.)
TIC09 5/20/04 4:44 PM Page 227
228 Ground-dwelling insects
certain rainforest species are estimated to cause up to
80% of all leaf damage and to consume up to 17% of all
leaf production. The system is an effective converter of
plant cellulose to usable carbohydrate, with at 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, 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 is provided by
adults feeding on plant sap from chewed leaf fragments.
Leaf-cutter ants may be termed highly polyphagous,
as studies have shown them to utilize between 50 and
70% of all neotropical rainforest plant species. How-
ever, 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 texture
and latex production by leaves can discourage attines,
and chemical defenses may play a role in deterrence.

However, leaf-cutter ants have adopted a strategy to
evade plant defensive chemicals that act on the digest-
ive system: they use the fungus to digest the plant
tissue. The ants and fungus co-operate to break down
plant defenses, with the ants removing protective leaf
waxes that deter fungi, and the fungi in turn producing
carbohydrates from cellulose indigestible to the ants.
9.5.3 Fungus cultivation by termites
The terrestrial microfauna of tropical savannas (grass-
lands and open woodlands) and some forests of the
Afrotropical and Oriental (Indo-Malayan) zoogeogra-
phic 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 under-
ground structures. Abundance, density, and produc-
tion of macrotermitines may be very high and, with
estimates of a live biomass of 10 g m
−2
, termites con-
sume over 25% of all terrestrial litter (wood, grass, and
leaf) produced annually in some west African savannas.
The litter-derived food resources are ingested, but
not digested by the termites: the food is passed rapidly
through the gut and, upon defecation, the undigested
feces are added to comb-like structures within the nest.
The combs may be located within many small subter-
ranean chambers or one large central hive or brood
chamber. Upon these combs of feces, a Termitomyces
fungus develops. The fungi are restricted to Macro-

termitinae nests, or occur within the bodies of termites.
The combs are constantly replenished and older parts
eaten, on a cycle of 5–8 weeks. Fungus action on the
termite fecal substrate raises the nitrogen content of the
substrate from about 0.3% until in the asexual stages
of Termitomyces it may reach 8%. These asexual spores
(mycotêtes) are eaten by the termites, as well as the
nutrient-enriched older comb. Although some species
of Termitomyces have no sexual stage, others develop
above-ground basidiocarps (fruiting bodies, or “mush-
rooms”) at a time that coincides with colony-founding
forays of termites from the nest. A new termite colony
is inoculated with the fungus by means of asexual
or sexual spores transferred in the gut of the founder
termite(s).
Termitomyces lives as a monoculture on termite-
attended combs, but if the termites are removed experi-
mentally or a termite colony dies out, or if the comb is
extracted from the nest, many other fungi invade the
comb and Termitomyces dies. Termite saliva has some
antibiotic properties but there is little evidence for these
termites being able to reduce local competition from
other fungi. It seems that Termitomyces is favored in the
fungal comb by the remarkably constant microclimate
at the comb, with a temperature of 30°C and scarcely
varying humidity together with an acid pH of 4.1–4.6.
The heat generated by fungal metabolism is regulated
appropriately via a 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 between
termite and fungus seems not to derive from joint
attack on plant defenses, in contrast to the ant–fungus
interaction seen in section 9.5.2. Termites are asso-
ciated closely with fungi, and fungus-infested rotting
wood is likely to have been a primitive food preference.
Termites can digest complex substances such as pectins
and chitins, and there is good evidence that they
have endogenous cellulases, which break down dietary
cellulose. However, the Macrotermitinae have shifted
some of their digestion to Termitomyces outside of the
gut. The fungus facilitates conversion of plant com-
pounds to more nutritious products and probably allows
a wider range of cellulose-containing foods to be con-
sumed by the termites. Thus, the macrotermitines suc-
cessfully utilize the abundant resource of dead vegetation.
TIC09 5/20/04 4:44 PM Page 228
9.6 CAVERNICOLOUS INSECTS
Caves often are perceived as extensions of the subter-
ranean 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 plants, but in deeper
caves there is no plant material other than that origin-
ating from any stream-derived debris. In many caves
nutrient supplies come from fungi and the feces
(guano) of bats and certain cave-dwelling birds, such as
swiftlets in the Orient.
Cavernicolous (cave-dwelling) insects include

those that seek refuge from adverse external environ-
mental conditions – such as moths and adult flies,
including mosquitoes, that hibernate to avoid winter
cold, or aestivate to avoid summer heat and desicca-
tion. Troglobiont or troglobite insects are restricted
to caves, and often are phylogenetically related to
soil-dwelling ones. The troglobite assemblage may be
dominated by Collembola (especially the family Ento-
mobryidae), and other important groups include the
Diplura (especially the family Campodeidae), orthop-
teroids (including cave crickets, Rhaphidophoridae),
and beetles (chiefly carabids, but including fungivorous
silphids).
In Hawai’i, past and present volcanic activity pro-
duces a spectacular range of “lava tubes” of different
isolation in space and time from other volcanic caves.
Here, studies of the wide range of troglobitic insects and
spiders living in lava tubes have helped us to gain an
understanding of the possible rapidity of morpholo-
gical divergence rates under these unusual conditions.
Even caves formed by very recent lava flows such as
on Kilauea have endemic or incipient species of
Caconemobius cave crickets.
Dermaptera and Blattodea may be abundant in trop-
ical caves, where they are active in guano deposits.
In south-east Asian caves a troglobite earwig is
ectoparasitic on roosting bats. Associated with caverni-
colous vertebrates there are many more conventional
ectoparasites, such as hippoboscid, nycteribid, and
streblid flies, fleas, and lice.

9.7 ENVIRONMENTAL MONITORING
USING GROUND-DWELLING HEXAPODS
Human activities such as agriculture, forestry, and
pastoralism have resulted in the simplification of many
terrestrial ecosystems. Attempts to quantify the effects
of such practices – for the purposes of conservation
assessment, classification of land-types, and monitor-
ing of impacts – have tended to be phytosociological,
emphasizing the use of vegetational mapping data.
More recently, data on vertebrate distributions and
communities have been incorporated into surveys for
conservation purposes.
Although arthropod diversity is estimated to be very
great (section 1.3), it is rare for data derived from this
group to be available routinely in conservation and
monitoring. There are several reasons for this neglect.
Firstly, when “flagship” species elicit public reaction
to a conservation issue, such as loss of a particular
habitat, these organisms are predominantly furry
mammals, such as pandas and koalas, or birds; rarely
are they insects. Excepting perhaps some butterflies,
insects often lack the necessary charisma in the public
perception.
Secondly, insects generally are difficult to sample in a
comparable manner within and between sites. Abund-
ance and diversity fluctuate on a relatively short
time-scale, in response to factors that may be little
understood. In contrast, vegetation often shows less
temporal variation; and with knowledge of mammal
seasonality and of the migration habits of birds, the

seasonal variations of vertebrate populations can be
taken into account.
Thirdly, arthropods often are more difficult to iden-
tify accurately, because of the numbers of taxa and
some deficiencies in taxonomic knowledge (alluded
to for insects in Chapter 8 and discussed more fully
in Chapter 17). Whereas competent mammalogists,
ornithologists, or field botanists might expect to iden-
tify to species level, respectively, all mammals, birds,
and plants of a geographically restricted area (outside
the tropical rainforests), no entomologist could aspire
to do so.
Nonetheless, aquatic biologists routinely sample
and identify all macroinvertebrates (mostly insects) in
regularly surveyed aquatic ecosystems, for purposes
including monitoring of deleterious change in environ-
mental quality (section 10.5). Comparable studies of
terrestrial systems, with objectives such as establish-
ment of rationales for conservation and the detection of
pollution-induced changes, are undertaken in some
countries. The problems outlined above have been
addressed in the following ways.
Some charismatic insect species have been high-
lighted, usually under “endangered-species” legislation
Environmental monitoring using ground-dwelling hexapods 229
TIC09 5/20/04 4:44 PM Page 229
230 Ground-dwelling insects
Box 9.2 Non-insect hexapods (Collembola, Protura, and Diplura)
The Collembola, Protura, and Diplura have been united
as the “Entognatha”, based on a similar mouthpart mor-

phology in which mandibles and maxillae are enclosed
in folds of the head, except when everted for feeding.
Although the entognathy of Diplura is thought not to
be homologous with that of Collembola and Protura
(section 7.2), it is convenient to treat these classes
together here. All have indirect fertilization – males
designed with vertebrate conservation in mind. These
species predominantly have been lepidopterans and
much has been learnt of the biology of selected species.
However, from the perspective of site classification for
conservation purposes, the structure of selected soil
and litter communities has greater realized and poten-
tial value than any single-species study. Sampling
problems are alleviated by using a single collection
method, often that of pit-fall trapping, but including
the extraction of arthropods from litter samples by a
variety of means (see section 17.1.2). Pitfall traps
collect mobile terrestrial arthropods by capturing them
in containers filled with preserving fluid and sunken
level with the substrate. Traps can be aligned along a
transect, or dispersed according to a standard quadrat-
based sampling regime. According to the sample size
required, they can be left in situ for several days or for
up to a few weeks. Depending on the sites surveyed,
arthropod collections may be dominated by Collem-
bola, Formicidae, and Coleoptera, particularly ground
TIC09 5/20/04 4:44 PM Page 230
Non-insect hexapods (Collembola, Protura, and Diplura) 231
deposit sperm bundles or stalked spermatophores,
which are picked up from the substrate by unattended

females. For phylogenetic considerations concerning
these three classes, see sections 7.2 and 7.3.
Protura (proturans)
The proturans are non-insect hexapods, with over 600
species in eight families. They are small (<2 mm long) to
very small, delicate, elongate, pale to white, with a fusi-
form body and conically shaped head. The thorax is
poorly differentiated from the abdomen. Eyes and
antennae are lacking, and the mouthparts are entog-
nathous, consisting of slender mandibles and maxillae,
slightly protruding from a pleural fold cavity; maxillary
and labial palps are present. The thorax is weakly devel-
oped, and bears legs each comprising five segments;
the anterior legs are held forward (as shown here for
Acerentulus, after Nosek 1973), fulfilling an antennal
sensory function. The adult abdomen is 12-segmented
with the gonopore between segments 11 and 12, and a
terminal anus; cerci are absent. Immature development
is anamorphic (with segments added posteriorly during
development). Proturans are cryptic, found exclusively
in soil, moss, and leaf litter. Their biology is little known,
but some species are known to feed on mycorrhizal fungi.
Collembola (springtails)
The springtails are treated as non-insect hexapods, but
intriguing evidence suggests an alternative, independ-
ent origin from Crustacea (see section 7.3). There are
about 9000 described species in some 27 families, but
the true species diversity may be much higher. Small
(usually 2–3 mm, but up to 12 mm) and soft-bodied,
their body varies in shape from globular to elongate (as

illustrated here for Isotoma and Sminthurinus, after
Fjellberg 1980), and is pale or often characteristically
pigmented grey, blue, or black. The eyes and/or ocelli
are often poorly developed or absent; the antennae
have four to six segments. Behind the antennae
usually there is a pair of postantennal organs, which
are specialized sensory structures (believed by some to
be the remnant apex of the second antenna of crus-
taceans). The entognathous mouthparts comprise
elongate maxillae and mandibles enclosed by pleural
folds of the head; maxillary and labial palps are absent.
The legs each comprise four segments. The six-
segmented abdomen has a sucker-like ventral tube (the
collophore), a retaining hook (the retinaculum), and a
furca (sometimes called furcula; forked jumping organ,
usually three-segmented) on segments 1, 3, and 4,
respectively, with the gonopore on segment 5 and the
anus on segment 6; cerci are absent. The ventral tube is
the main site of water and salt exchange and thus is
important to fluid balance, but also can be used as an
adhesive organ. The springing organ or furca, formed
by fusion of a pair of appendages, is longer in surface-
dwelling species than those living within the soil. In
general, jump length is correlated with furca length,
and some species can spring up to 10 cm. Amongst
hexapods, collembolan eggs uniquely are microlecithal
(lacking large yolk reserves) and holoblastic (with com-
plete cleavage). The immature instars are similar to
the adults, developing epimorphically (with a constant
segment number); maturity is attained after five molts,

but molting continues for life. Springtails are most
abundant in moist soil and litter, where they are major
consumers of decaying vegetation, but also they occur
in caves, in fungi, as commensals with ants and ter-
mites, on still water surfaces, and in the intertidal zone.
Most species feed on fungal hyphae or dead plant
material, some species eat other small invertebrates,
and only a very few species are injurious to living plants.
For example, the “lucerne flea” Sminthurus viridis
(Sminthuridae) damages the tissues of crops such as
lucerne and clover and can cause economic injury.
Springtails can reach extremely high densities (e.g.
10,000–100,000 individuals m
−2
) and are ecologically
important in adding nutrients to the soil via their
feces and in facilitating decomposition processes, for
example by stimulating and inhibiting the activities of
different microorganisms.
Diplura (diplurans)
The diplurans are non-insect hexapods, with some
1000 species in eight or nine families. They are small to
medium sized (2–5 mm, exceptionally up to 50 mm),
mostly unpigmented, and weakly sclerotized. They lack
eyes, and their antennae are long, moniliform, and multi-
segmented. The mouthparts are entognathous, and
the mandibles and maxillae are well developed, with
their tips visible protruding from the pleural fold cavity;
the maxillary and labial palps are reduced. The thorax
is little differentiated from the abdomen, and bears

legs each comprising five segments. The abdomen is
10-segmented, with some segments having small
styles and protrusible vesicles; the gonopore is
between segments 8 and 9, and the anus is terminal;
the cerci are filiform (as illustrated here for Campodea,
after Lubbock 1873) to forceps-like (as in Parajapyx
shown here, after Womersley 1939). Development of
the immature forms is epimorphic, with molting con-
tinuing through life. Some species are gregarious, and
females of certain species tend the eggs and young.
Diplurans are generally omnivorous, some feed on live
and decayed vegetation, and japygid diplurans are
predators.
TIC09 5/20/04 4:44 PM Page 231
232 Ground-dwelling insects
The Archaeognatha and Zygentoma represent the sur-
viving remnants of a wider radiation of primitively flight-
less insects. These two apterygote orders superficially
are similar, but differ in pleural structures and quite
fundamentally in their mouthpart morphology. The tho-
racic segments are subequal and unfused, with poorly
developed pleura. The abdomen is 11-segmented, with
styles and often protrusible vesicles on some seg-
ments; it bears a long, multisegmented caudal appendix
dorsalis, located mediodorsally on the tergum of seg-
ment 11, forming an epiproct extension lying between
the paired cerci and dorsal to the genitalia. In females
the gonapophyses of segments 8 and 9 form an
ovipositor. Fertilization is indirect, by transfer of a
spermatophore or sperm droplets. Development is

ametabolous and molting continues for life. For phylo-
genetic considerations see section 7.4.1.
Archaeognatha (bristletails)
The bristletails are primitively wingless insects, with
some 500 species in two extant families. They are mod-
erate sized, 6–25 mm long, elongate, and cylindrical.
The head is hypognathous, and bears large compound
eyes that are in contact dorsally; three ocelli are pre-
sent; the antennae are multisegmented. The mouth-
parts are partially retracted into the head, and include
elongate, monocondylar (single-articulated) mandibles,
and elongate, seven-segmented maxillary palps. The
thorax is humped, and the legs have large coxae each
bearing a style and the tarsi are two- or three-
segmented. The abdomen continues the thoracic con-
tour; segments 2–9 bear ventral muscle-containing
styles (representing limbs), whereas segments 1–7
have one or two pairs of protrusible vesicles medial to
the styles (fully developed only in mature individuals).
The paired multisegmented cerci are shorter than the
median caudal appendage (as shown here for Petrobius
maritima, after Lubbock 1873).
Fertilization is indirect, with sperm droplets attached
to silken lines produced from the male gonapophyses,
or stalked spermatophores are deposited on the ground,
or more rarely sperm are deposited on the female’s
ovipositor. Bristletails often are active nocturnally, feed-
ing on litter, detritus, algae, lichens and mosses, and
sheltering beneath bark or in litter during the day. They
can run fast and jump, using the arched thorax and

flexed abdomen to spring considerable distances.
Zygentoma (Thysanura; silverfish)
Silverfish are primitively wingless insects, with some
400 species in five extant families. Their bodies are
moderately sized (5–30 mm long) and dorsoventrally
flattened, often with silvery scales. The head is hypo-
gnathous to slightly prognathous; compound eyes are
absent or reduced to isolated ommatidia, and there
may be one to three ocelli present; the antennae are
multisegmented. The mouthparts are mandibulate, and
include dicondylar (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 muscle-
containing 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 elongate multisegmented cerci are nearly as
long as the median caudal appendage (as shown here
for Lepisma saccharina, after Lubbock 1873).
Box 9.3 Archaeognatha (bristletails) and Zygentoma (Thysanura; silverfish)
TIC09 5/20/04 4:44 PM Page 232
Grylloblattodea 233
Box 9.4 Grylloblattodea (Grylloblattaria, Notoptera; grylloblattids,
ice or rock crawlers)
Grylloblattodea comprise a single family, Grylloblattidae,
containing some 25 described species, restricted to
western North America and central to eastern Asia
including Japan. North American species are particu-

larly tolerant of cold and may live at high elevations on
glaciers and snow banks; East Asian species may live
at sea level in temperate forest. Grylloblattodea are
moderately sized insects (20–35 mm long) with an elon-
gate, pale, cylindrical body that is soft and pubescent.
The head is prognathous, and the compound eyes are
reduced or absent; ocelli are absent. The antennae
are multisegmented, and the mouthparts mandibulate.
The quadrate prothorax is larger than the meso- or
metathorax; wings are absent. The legs are cursorial,
with large coxae and five-segmented tarsi. The
abdomen has 10 visible segments and the rudiments
of segment 11, with five- to nine-segmented cerci. The
female has a short ovipositor, and the male genitalia are
asymmetrical.
Copulation takes place side-by-side with the male on
the right, as illustrated here for a common Japanese
species, Galloisiana nipponensis (after Ando 1982).
Eggs may diapause up to a year in damp wood or soil
under stones. Nymphs, which resemble adults, develop
slowly through eight instars. North American rock
crawlers are active by day and night at low temperat-
ures, feeding on dead arthropods and organic material,
notably from the surface of ice and snow in spring
snow-melt, within caves (including ice caves), in alpine
soil, and damp places such as beneath rocks.
Phylogenetic relations are discussed in section 7.4.2
and depicted in Fig. 7.2.
Fertilization is indirect, via flask-shaped spermato-
phores that females pick up from the substrate. Many

silverfish live in litter or under bark; some are subterran-
ean or are cavernicolous, but some species can tolerate
low humidity and high temperatures of arid areas; for
example, there are desert-living lepismatid silverfish in
the sand dunes of the Namib Desert in south-western
Africa, where they are important detritivores. Some other
zygentoman species live in mammal burrows, a few are
commensals in nests of ants and termites, and several
species are familiar synanthropic insects, living in human
dwellings. These include L. saccharina, Ctenolepisma
longicauda (silverfishes), and Lepismodes inquilinus
(= Thermobia domestica) (the firebrat), which eat mater-
ials such as paper, cotton, and plant debris, using their
own cellulase to digest the cellulose.
beetles (Carabidae), Tenebrionidae, Scarabaeidae, and
Staphylinidae, with some terrestrial representatives of
many other orders.
Taxonomic difficulties often are alleviated by select-
ing (from amongst the organisms collected) one or
more higher taxonomic groups for species-level
identification. The carabids are often selected for study
because of the diversity of species sampled, the pre-
existing ecological knowledge, and availability of
taxonomic keys to species level, although these are
largely restricted to temperate northern hemisphere
taxa.
Studies to date are ambivalent concerning correlates
between species diversity (including taxon richness)
established from vegetational survey and those from
terrestrial insect trapping. Evidence from the well-

documented British biota suggests that vegetational
diversity does not predict insect diversity. However, a
study in more natural, less human-affected environ-
ments in southern Norway showed congruence
between carabid faunal indices and those obtained by
vegetational and bird surveys. Further studies are
required into the nature of any relationships between
terrestrial insect richness and diversity data obtained
by conventional biological survey of selected plants
and vertebrates.
TIC09 5/20/04 4:44 PM Page 233
Box 9.6 Zoraptera
These insects comprise the single genus Zorotypus,
sometimes subdivided into several genera, containing
just over 30 described species found worldwide in trop-
ical and warm temperate regions except Australia. They
are small (<4 mm long) and rather termite-like. The head
is hypognathous, and compound eyes and ocelli are
present in winged species but absent in apterous
species. The antennae are moniliform and nine-
segmented, and the mouthparts are mandibulate, with
five-segmented maxillary palps and three-segmented
labial palps. The subquadrate prothorax is larger than
the similar-shaped meso- and metathorax. The wings
are polymorphic; some forms are apterous in both
sexes, whereas other forms are alate, with two pairs of
paddle-shaped wings with reduced venation and
smaller hind wings (as illustrated here for Zorotypus
hubbardi, after Caudell 1920). The wings are shed as in
ants and termites. The legs have well-developed coxae,

expanded hind femora bearing stout ventral spines, and
two-segmented tarsi, each with two claws. The 11-
segmented abdomen is short and rather swollen, with
cerci comprising just a single segment. The male
genitalia are asymmetric.
The immature stages are polymorphic according
to wing development. Zorapterans are gregarious,
occurring in leaf litter, rotting wood, or near termite
colonies, eating fungi and perhaps small arthropods.
Phylogenetically they are enigmatic, with a probable
relationship within the Polyneoptera (see section 7.4.2
and Fig. 7.2).
Box 9.5 Embiidina or Embioptera (embiids, webspinners)
There are some 300 described species of embiids
(perhaps up to an order of magnitude more remain
undescribed) in at least eight families, worldwide. Small
to moderately sized, they have an elongate, cylindrical
body, somewhat flattened in males. The head is prog-
nathous, and the compound eyes are reniform (kidney-
shaped), larger in males than females; ocelli are absent.
The antennae are multisegmented, and the mouthparts
are mandibulate. The quadrate prothorax is larger than
the meso- or metathorax. All females and some males
are apterous, and, if present, the wings (illustrated here
for Embia major, after Imms 1913) are characteristically
soft and flexible, with blood sinus veins stiffened for
flight by hemolymph pressure. The legs are short, with
three-segmented tarsi; the basal segment of each fore
tarsus is swollen and contains silk glands, whereas the
hind femora are swollen with strong tibial muscles. The

abdomen is 10-segmented, with only the rudiments of
segment 11; the cerci comprise two segments and are
responsive to tactile stimuli. The female external geni-
talia are simple, whereas the male genitalia are complex
and asymmetrical.
During copulation, the male holds the female with his
prognathous mandibles and/or his asymmetrical cerci.
The eggs and early nymphal stages are tended by the
female parent, and the immature stages resemble the
adults except for their wings and genitalia. Embiids live
gregariously in silken galleries, spun with the tarsal silk
glands (present in all instars); their galleries occur in leaf
litter, beneath stones, on rocks, on tree trunks (see
Plate 4.1, facing p. 14), or in cracks in bark and soil,
often around a central retreat. Their food comprises
litter, moss, bark, and dead leaves. The galleries are
extended to new food sources, and the safety of the
gallery is left only when mature males disperse to new
sites, where they mate, do not feed, and sometimes are
cannibalized by females (see Plate 4.2). Webspinners
readily reverse within their galleries, for example when
threatened by a predator.
Phylogenetic relations are discussed in section 7.4.2
and depicted in Fig. 7.2.
TIC09 5/20/04 4:44 PM Page 234
Dermaptera (earwigs) 235
Box 9.7 Dermaptera (earwigs)
small and leathery, with smooth, unveined tegmina; the
hind wings are large, membranous, and semi-circular
(as illustrated here for an adult male of the common

European earwig, Forficula auricularia) and when at rest
are folded fan-like and then longitudinally, protruding
slightly from beneath the tegmina; hind-wing venation
is dominated by the anal fan of branches of A
1
and
cross-veins. The abdominal segments are telescoped
(terga overlapping), with 10 visible segments in the male
and eight in the female, terminating in prominent cerci
modified into forceps; the latter are often heavier,
larger, and more curved in males than in 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 bur-
row 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 is attained after four or five molts.
The two parasitic groups (of uncertain rank), Arixeniina
and Hemimerina, exhibit pseudoplacental viviparity
(section 5.9).
Earwigs are mostly cursorial and nocturnal, with
most species rarely flying. Feeding is predominantly on
dead and decaying vegetable and animal matter, with
some predation and some damage to living vegetation,
especially in gardens. Some are commensals or
ectoparasites of bats in south-east Asia (Arixeniina) or
semi-parasites of South African rodents (Hemimerina):
earwigs in both tribes are blind, apterous, and with

rod-like forceps. The forceps of free-living earwigs are
used for manipulating prey, for defense and offense,
and in some species for grasping the partner during
copulation. The common name “earwig” may derive
from a supposed predilection for entering ears, or from
a corruption of “ear wing” referring to the shape of the
wing, but these are unsupported.
Phylogenetic relations are discussed in section 7.4.2
and depicted in Fig. 7.2.
The earwigs comprise an order containing some 2000
species in about 10 families found worldwide. They are
hemimetabolous, with small to moderately sized (4–
25 mm long) elongate bodies that are dorsoventrally
flattened. The head is prognathous; the compound
eyes may be large, small, or absent, and ocelli are
absent. The antennae are short to moderate length and
filiform with segments elongate; there are fewer anten-
nal segments in immature individuals than in the adult.
The mouthparts are mandibulate (section 2.3.1; Fig.
2.10). The legs are relatively short, and the tarsi are
three-segmented with the second tarsomeres short.
The prothorax has a shield-like pronotum, and the
meso- and metathoracic sclerites are of variable size.
Earwigs are apterous or, if winged, their fore wings are
TIC09 5/20/04 4:44 PM Page 235
236 Ground-dwelling insects
Box 9.8 Blattodea (Blattaria; cockroaches, roaches)
The large coxae abut each other and dominate the
ventral thorax. The abdomen has 10 visible segments,
with the subgenital plate (sternum 9) often bearing one

or a pair of styles in the male, and concealing segment
11 that is represented only by paired paraprocts.
The cerci comprise from one to usually many segments.
The male genitalia are asymmetrical, and the female’s
ovipositor valves are concealed inside a genital
atrium.
Mating may involve stridulatory courtship, both sexes
may produce sex pheromones, and the female may
mount the male prior to end-to-end copulation. Eggs
generally are laid in a purse-shaped ootheca compris-
ing two parallel rows of eggs with a leathery enclosure
(section 5.8), which may be carried externally by the
female (as illustrated here for a female of Blatella
germanica, after Cornwell 1968). Certain species de-
monstrate a range of forms of ovoviviparity in which a
variably reduced ootheca is retained within the repro-
ductive tract in a “uterus” (or brood sac) during embryo-
genesis, often until nymphal hatching; true viviparity is
rare. Parthenogenesis occurs in a few species. Nymphs
develop slowly, resembling small apterous adults.
Cockroaches are amongst the most familiar insects,
owing to the widespread human-associated habits
of some 30 species, including Periplaneta americana
(the American cockroach), B. germanica (the German
cockroach), and B. orientalis (the Oriental cockroach).
These nocturnal, malodorous, disease-carrying, refuge-
seeking, peridomestic roaches are unrepresentative of
the wider diversity. Typically, cockroaches are tropical,
either nocturnal or diurnal, and sometimes arboreal,
with some cavernicolous species. Cockroaches include

solitary and gregarious species; Cryptocercus (the
woodroach) lives in family groups. Cockroaches mostly
are saprophagous scavengers, but some eat wood and
use enteric amoebae to break it down. Cryptocercus,
uniquely in Blattodea, utilizes flagellate internal protists
to digest cellulose.
Phylogenetic relations are discussed in section 7.4.2
and depicted in Figs. 7.2 and 7.4. Evidence presented
in earlier editions of this textbook suggested that
Cryptocercus convergently acquired its termite-like
features, such as sociality and digestion of cellulose, via
protists. Now this similarity appears to reflect actual
relationships, with Isoptera having arisen from within
Blattodea (Fig. 7.4). Although this renders the latter
paraphyletic, we continue to use “Blattodea” until these
relationships are confirmed.
The cockroaches make up an order of over 3500
species in at least eight families worldwide. They are
hemimetabolous, with small to large (<3 mm to
>100 mm), dorsoventrally flattened bodies. The head is
hypognathous, and the compound eyes may be moder-
ately large to small, or absent in cavernicolous species;
ocelli are represented by two pale spots. The antennae
are filiform and multisegmented, and the mouthparts
are mandibulate. The prothorax has an enlarged,
shield-like pronotum, often covering the head; the
meso- and metathorax are rectangular and subequal.
The fore wings (Fig. 2.22c) are sclerotized as tegmina,
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.
TIC09 5/20/04 4:44 PM Page 236
FURTHER READING
Blossey, B. & Hunt-Joshi, T.R. (2003) Belowground herbivory
by insects: influence on plants and aboveground herbi-
vores. Annual Review of Entomology 48, 521–47.
Dindal, D.L. (ed.) (1990) Soil Biology Guide. John Wiley & Sons,
Chichester.
Edgerly, J.S. (1997) Life beneath silk walls: a review of the
primitively social Embiidina. In: The Evolution of Social
Behaviour in Insects and Arachnids (eds. J.C. Choe & B.J.
Crespi), pp. 14–25. Cambridge University Press, Cambridge.
Eisenbeis, G. & Wichard, W. (1987) Atlas on the Biology of Soil
Arthropods, 2nd edn. Springer-Verlag, Berlin.
Hopkin, S.P. (1997) Biology of Springtails. Oxford University
Press, Oxford.
Lövei, G.L. & Sunderland, K.D. (1996) Ecology and behaviour
of ground beetles (Coleoptera: Carabidae). Annual Review of
Entomology 41, 231–56.
Lussenhop, J. (1992) Mechanisms of microarthropod–
microbial interactions in soil. Advances in Ecological Research
23, 1–33.
Further reading 237
McGeoch, M.A. (1998) The selection, testing and application
of terrestrial insects as bioindicators. Biological Reviews 73,
181–201.

Mueller, U.G., Rehner, S.A. & Schultz, T.R. (1998) The evolu-
tion of agriculture in ants. Science 281, 203–9.
New, T.R. (1998) Invertebrate Surveys for Conservation. Oxford
University Press, Oxford.
North, R.D., Jackson, C.W. & Howse, P.E. (1997) Evolutionary
aspects of ant–fungus interactions in leaf-cutting ants.
Trends in Ecology and Evolution 12, 386–9.
Paine, T.D., Raffia, K.F. & Harrington, T.C. (1997) Inter-
actions among scolytid bark beetles, their associated fungi,
and live host conifers. Annual Review of Entomology 42,
179–206.
Resh, V.H. & Cardé, R.T. (eds.) (2003) Encyclopedia of Insects.
Academic Press, Amsterdam. [Particularly see articles on
cave insects; soil habitats.]
Stork, N.E. (ed.) (1990) The Role of Ground Beetles in Ecological
and Environmental Studies. Intercept, Andover.
Villani, M.G. & Wright, R.J. (1990) Environmental influences
on soil macroarthropod behavior in agricultural systems.
Annual Review of Entomology 35, 249–69.
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