The Insects - Outline of Entomology 3th Edition - Chapter 14 ppsx

An African ant-mimicking membracid bug. (After Boulard 1968.) Chapter 14 INSECT DEFENSE TIC14 5/20/04 4:40 PM Page 355 356 Insect defense Although some humans eat insects (section 1.6), many “western” cultures are reluctant to use them as food; this aversion extends no further than humans. For very many organisms, insects provide a substantial food source, because they are nutritious, abundant, diverse, and found everywhere. Some animals, termed insectivores, rely almost exclusively on a diet of insects; omnivores may eat them opportunistically; and many herbivores unavoidably consume insects. Insectivores may be vertebrates or invertebrates, including arthropods – insects certainly eat other insects. Even plants lure, trap, and digest insects; for example, pitcher plants (both New World Sarraceniaceae and Old World Nepenthaceae) digest arthropods, predominantly ants, in their fluid-filled pitchers (section 11.4.2), and the flypaper and Venus flytraps (Droseraceae) capture many flies. Insects, however, actively or passively resist being eaten, by means of a variety of protective devices – the insect defenses – which are the subject of this chapter. A review of the terms discussed in Chapter 13 is appropriate. A predator is an animal that kills and con- sumes a number of prey animals during its life. Animals that live at the expense of another animal but do not kill it are parasites, which may live internally (endo- parasites) or externally (ectoparasites). Parasitoids are those that live at the expense of one animal that dies prematurely as a result. The animal attacked by parasites or parasitoids is a host. All insects are potential prey or hosts to many kinds of predators (either vertebrate or invertebrate), parasitoids or, less often, parasites. Many defensive strategies exist, including use of specialized morphology (as shown for the extraordinary, ant-mimicking membracid bug Hamma rectum from tropical Africa in the vignette of this chapter), behavior, noxious chemicals, and responses of the immune sys- tem. This chapter deals with aspects of defense that include death feigning, autotomy, crypsis (camouflage), chemical defenses, aposematism (warning sig- nals), mimicry, and collective defensive strategies. These are directed against a wide range of vertebrates and invertebrates but, because much study has involved insects defending themselves against insectivorous birds, the role of these particular predators will be emphasized. Immunological defense against micro- organisms is discussed in Chapter 3, and defenses used against parasitoids are considered in Chapter 13. A useful framework for discussion of defense and predation can be based upon the time and energy inputs to the respective behaviors. Thus, hiding, escape by running or flight, and defense by staying and fighting involve increasing energy expenditure but diminishing costs in time expended (Fig. 14.1). Many insects will change to another strategy if the previous defense fails: the scheme is not clear-cut and it has elements of a continuum. 14.1 DEFENSE BY HIDING Visual deception may reduce the probability of being found by a natural enemy. A well-concealed cryptic insect that either resembles its general background or an inedible (neutral) object may be said to “mimic” its surroundings. In this book, mimicry (in which an animal resembles another animal that is recognizable by natural enemies) is treated separately (section 14.5). However, crypsis and mimicry can be seen as similar in that both arise when an organism gains in fitness through developing a resemblance (to a neutral or animate object) evolved under selection. In all cases, it is Fig. 14.1 The basic spectrum of prey defense strategies and predator foraging, varying according to costs and benefits in both time and energy. (After Malcolm 1990.) TIC14 5/20/04 4:40 PM Page 356 assumed that such defensive adaptive resemblance is under selection by predators or parasitoids, but, although maintenance of selection for accuracy of resemblance has been demonstrated for some insects, the origin can only be surmised. Insect crypsis can take many forms. The insect may adopt camouflage, making it difficult to distinguish from the general background in which it lives, by: • resembling a uniform colored background, such as a green geometrid moth on a leaf; • resembling a patterned background, such as a mottled moth on tree bark (Fig. 14.2; see also Plate 6.1, facing p. 14); • being countershaded – light below and dark above – as in some caterpillars and aquatic insects; • having a pattern to disrupt the outline, as is seen in many moths that settle on leaf litter; • having a bizarre shape to disrupt the silhouette, as demonstrated by some membracid leafhoppers. In another form of crypsis, termed masquerade or mimesis to contrast with the camouflage described above, the organism deludes a predator by resembling an object that is a particular specific feature of its environment, but is of no inherent interest to a predator. This feature may be an inanimate object, such as the bird dropping resembled by young larvae of some butterflies such as Papilio aegeus (Papilionidae), or an animate but neutral object – for example, “looper” caterpillars (the larvae of geometrid moths) resemble twigs, some membracid bugs imitate thorns arising from a stem, and many stick-insects look very much like sticks and may even move like a twig in the wind. Many insects, notably amongst the lepidopterans and orthopteroids, resemble leaves, even to the similarity in venation (Fig. 14.3), and appearing to be dead or alive, mottled with fungus, or even partially eaten as if by a herbivore. However, interpretation of apparent resemblance to inanimate objects as simple crypsis may be revealed as more complex when subject to experimental manipulation (Box 14.2). Crypsis is a very common form of insect concealment, particularly in the tropics and amongst noctur- nally active insects. It has low energetic costs but relies on the insect being able to select the appropriate background. Experiments with two differently colored Defense by hiding 357 Fig. 14.2 Pale and melanic (carbonaria) morphs of the peppered moth Biston betularia resting on: (a) pale, lichen- covered; and (b) dark trunks. Fig. 14.3 A leaf-mimicking katydid, Mimetica mortuifolia (Orthoptera: Tettigoniidae), in which the fore wing resembles a leaf even to the extent of leaf-like venation and spots resembling fungal mottling. (After Belwood 1990.) TIC14 5/20/04 4:40 PM Page 357 Box 14.1 Avian predators as selective agents for insects reducing as “post-industrial” air quality improves. How- ever, the centrality of avian predation acting as a force for natural selection in B. betularia is no longer so evident. More convincing is the demonstration of directly observed predation, and inference from beak pecks on the wings of butterflies and from experiments with color-manipulated daytime-flying moths. Thus, winter- roosting monarch butterflies (Danaus plexippus) are fed upon by black-backed orioles (Icteridae), which browse selectively on poorly defended individuals, and by black-headed grosbeaks (Fringillidae), which appear to be completely insensitive to the toxins. Specialized predators such as Old World bee-eaters (Meropidae) and neotropical jacamars (Galbulidae) can deal with the stings of hymenopterans (the red-throated bee-eater, Merops bullocki, is shown here de-stinging a bee on a branch, after Fry et al. 1992) and the toxins of butterflies, respectively. A similar suite of birds selectively feeds on noxious ants. The ability of these specialist predators to distinguish between varying pattern and edibility may make them selective agents in the evolution and maintenance of defensive mimicry. Birds are observable insectivores for laboratory studies: their readily recognizable behavioral responses to unpalatable foods include head-shaking, disgorging of food, tongue-extending, bill-wiping, gagging, squawk- ing, and ultimately vomiting. For many birds, a single learning trial with noxious (Class I) chemicals appears to lead to long-term aversion to the particular insect, even with a substantial delay between feeding and illness. However, manipulative studies of bird diets are com- plicated by their fear of novelty (neophobia), which, for example, can lead to rejection of prey with startling and frightening displays (section 13.2). Conversely, birds rapidly learn preferred items, as in Kettlewell’s experiments in which birds quickly recognized both Biston betularia morphs on tree trunks in his artificial set-up. Perhaps no insect has completely escaped the atten- tions of predators and some birds can overcome even severe insect defenses. For example, the lubber grasshopper (Acrididae: Romalea guttata) is large, gre- garious, and aposematic, and if attacked it squirts volatile, pungent chemicals accompanied by a hissing noise. The lubber is extremely toxic and is avoided by all lizards and birds except one, the loggerhead shrike (Laniidae: Lanius ludovicanus), which snatches its prey, including lubbers, and impales them “decoratively” upon spikes with minimal handling time. These impaled items serve both as food stores and in sexual or terri- torial displays. Romalea, which are emetic to shrikes when fresh, become edible after two days of lardering, presumably by denaturation of the toxins. The impaling behavior shown by most species of shrikes thus is preadaptive in permitting the loggerhead to feed upon an extremely well-defended insect. No matter how good the protection, there is no such thing as total defense in the arms race between prey and predator. Henry Bates, who was first to propose a theory for mimicry, suggested that natural enemies such as birds selected among different prey such as butterflies, based upon an association between mimetic patterns and unpalatability. A century later, Henry Kettlewell argued that selective predation by birds on the peppered moth (Geometridae: Biston betularia) altered the proportions of dark- and light-colored morphs (Fig. 14.2) according to their concealment (crypsis) on natural and industrially darkened trees upon which the moths rested by day. Amateur lepidopterists recorded that the proportion of the dark (“melanic”) carbonaria form dramatically increased as industrial pollution increased in northern England from the mid-19th century. Elimination of pale lichen on tree trunk resting areas was suggested to have made normal pale morphs more visible against the sooty, lichen-denuded trunks (as shown in Fig. 14.2b), and hence they were more sus- ceptible to visual recognition by bird predators. This phenomenon, termed industrial melanism, often has been cited as a classic example of evolution through natural selection. The peppered moth/avian predation story has been challenged for its experimental design and procedures, and biased interpretation. The case depended upon: • birds being the major predators rather than night- flying, pattern-insensitive bats; • moths resting “exposed” on trunks rather than under branches or in the canopy; • dark and pale morphs favoring the cryptic background appropriate to their patterning; • crypsis to the human eye being quantifiable and equating to that for moth-feeding birds; • selection being concentrated in the adult stage of the moth’s life cycle; • genes responsible for origination of melanism acting in a particular way, and with very high levels of selection. None of these components have been confirmed. Evolution undoubtedly has taken place. The proportions of dark morphs (alleles for melanism) have changed through time, increasing with industrialization, and TIC14 5/20/04 4:40 PM Page 358 Secondary lines of defense 359 morphs of Mantis religiosa (Mantidae), the European praying mantid, have shown that brown and green morphs placed against appropriate and inappropriate colored backgrounds were fed upon in a highly selective manner by birds: they removed all “mismatched” morphs and found no camouflaged ones. Even if the correct background is chosen, it may be necessary to orientate correctly: moths with disruptive outlines or with striped patterns resembling the bark of a tree may be concealed only if orientated in a particular direction on the trunk. The Indomalayan orchid mantid, Hymenopus corona- tus (Hymenopodidae), blends beautifully with the pink flower spike of an orchid, where it sits awaiting prey. The crypsis is enhanced by the close resemblance of the femora of the mantid’s legs to the flower’s petals. Crypsis enables the mantid to avoid detection by its potential prey (flower visitors) (section 13.1.1) as well as conceal itself from predators. 14.2 SECONDARY LINES OF DEFENSE Little is known of the learning processes of inexperi- enced vertebrate predators, such as insectivorous birds. However, studies of the gut contents of birds show that cryptic insects are not immune from predation (Box 14.1). Once found for the first time (perhaps acci- dentally), birds subsequently seem able to detect cryptic prey via a “search image” for some element(s) of the pattern. Thus, having discovered that some twigs were caterpillars, American blue jays were observed to con- tinue to peck at sticks in a search for food. Primates can identify stick-insects by one pair of unfolded legs alone, and will attack actual sticks to which phasmatid legs have been affixed experimentally. Clearly, subtle cues allow specialized predators to detect and eat cryptic insects. Once the deception is discovered, the insect prey may have further defenses available in reserve. In the energetically least demanding response, the initial crypsis may be exaggerated, as when a threatened masquer- ader falls to the ground and lies motionless. This behavior is not restricted to cryptic insects: even visually obvious prey insects may feign death (thanatosis). This behavior, used by many beetles (particularly weevils), can be successful, as predators lose interest in apparently dead prey or may be unable to locate a motionless insect on the ground. Another secondary line of defense is to take flight and suddenly reveal a flash of conspicuous color from the hind wings. Immediately on landing the wings are folded, the color vanishes, and the insect is cryptic once more. This behavior is common amongst certain orthopterans and underwing moths; the color of the flash may be yellow, red, purple, or, rarely, blue. A third type of behavior of cryptic insects upon dis- covery by a predator is the production of a startle dis- play. One of the commonest is to open the fore wings and reveal brightly colored “eyes” that are usually concealed on the hind wings (Fig. 14.4). Experiments using birds as predators have shown that the more perfect the eye (with increased contrasting rings to resemble true eyes), the better the deterrence. Not all eyes serve to startle: perhaps a rather poor imitation of an eye on a wing may direct pecks from a predatory bird to a non- vital part of the insect’s anatomy. An extraordinary type of insect defense is the con- vergent appearance of part of the body to a feature of a vertebrate, albeit on a much smaller scale. Thus, the head of a species of fulgorid bug, commonly called the alligator bug, bears an uncanny resemblance to that of a caiman. The pupa of a particular lycaenid butterfly Fig. 14.4 The eyed hawkmoth, Smerinthus ocellatus (Lepidoptera: Sphingidae). (a) The brownish fore wings cover the hind wings of a resting moth. (b) When the moth is disturbed, the black and blue eyespots on the hind wings are revealed. (After Stanek 1977.) TIC14 5/20/04 4:40 PM Page 359 360 Insect defense looks like a monkey head. Some tropical sphingid larvae assume a threat posture which, together with false eyespots that actually lie on the abdomen, gives a snake-like impression. Similarly, the caterpillars of certain swallowtail butterflies bear a likeness to a snake’s head (see Plate 5.7). These resemblances may deter predators (such as birds that search by “peering about”) by their startle effect, with the incorrect scale of the mimic being overlooked by the predator. 14.3 MECHANICAL DEFENSES Morphological structures of predatory function, such as the modified mouthparts and spiny legs described in Chapter 13, also may be defensive, especially if a fight ensues. Cuticular horns and spines may be used in deterrence of a predator or in combating rivals for mating, territory, or resources, as in Onthophagus dung beetles (section 5.3). For ectoparasitic insects, which are vulnerable to the actions of the host, body shape and sclerotization provide one line of defense. Fleas are laterally compressed, making these insects difficult to dislodge from host hairs. Biting lice are flattened dorsoventrally, and are narrow and elongate, allowing them to fit between the veins of feathers, secure from preening by the host bird. Furthermore, many ectoparasites have resistant bodies, and the heavily sclerot- ized cuticle of certain beetles must act as a mechanical antipredator device. Many insects construct retreats that can deter a predator that fails to recognize the structure as contain- ing anything edible or that is unwilling to eat inorganic material. The cases of caddisfly larvae (Trichoptera), constructed of sand grains, stones, or organic frag- ments (Fig. 10.6), may have originated in response to the physical environment of flowing water, but certainly have a defensive role. Similarly, a portable case of vegetable material bound with silk is constructed by the terrestrial larvae of bagworms (Lepidoptera: Psychidae). In both caddisflies and psychids, the case serves to protect during pupation. Certain insects construct artificial shields; for example, the larvae of certain chrysomelid beetles decorate themselves with their feces. The larvae of certain lacewings and reduviid bugs cover themselves with lichens and detritus and/or the sucked-out carcasses of their insect prey, which can act as barriers to a predator, and also may disguise themselves from prey (Box 14.2). The waxes and powders secreted by many hemipter- ans (such as scale insects, woolly aphids, whiteflies, and fulgorids) may function to entangle the mouthparts of a potential arthropod predator, but also may have a waterproofing role. The larvae of many ladybird beetles (Coccinellidae) are coated with white wax, thus resembling their mealybug prey. This may be a disguise to protect them from ants that tend the mealybugs. Body structures themselves, such as the scales of moths, caddisflies, and thrips, can protect as they detach readily to allow the escape of a slightly denuded insect from the jaws of a predator, or from the sticky threads of spiders’ webs or the glandular leaves of insectivorous plants such as the sundews. A mechanical defense that seems at first to be maladaptive is autotomy, the shedding of limbs, as demonstrated by stick-insects (Phasmatodea) and perhaps crane flies (Diptera: Tipulidae). The upper part of the phasmatid leg has the trochanter and femur fused, with no mus- cles running across the joint. A special muscle breaks the leg at a weakened zone in response to a predator grasping the leg. Immature stick-insects and mantids can regenerate lost limbs at molting, and even certain autotomized adults can induce an adult molt at which the limb can regenerate. Secretions of insects can have a mechanical defensive role, acting as a glue or slime that ensnares predators or parasitoids. Certain cockroaches have a permanent slimy coat on the abdomen that confers protection. Lipid secretions from the cornicles (also called siphunculi) of aphids may gum-up predator mouthparts or small parasitic wasps. Termite soldiers have a variety of secretions available to them in the form of cephalic glandular products, including terpenes that dry on exposure to air to form a resin. In Nasutitermes (Termitidae) the secretion is ejected via the nozzle-like nasus (a pointed snout or rostrum) as a quick-drying fine thread that impairs the movements of a predator such as an ant. This defense counters arthropod predators but is unlikely to deter vertebrates. Mechanical-acting chemicals are only a small selection of the total insect armory that can be mobilized for chemical warfare. 14.4 CHEMICAL DEFENSES Chemicals play vital roles in many aspects of insect behavior. In Chapter 4 we considered the use of pheromones in many forms of communication, including alarm pheromones elicited by the presence of a TIC14 5/20/04 4:40 PM Page 360 Chemical defenses 361 Certain West African predatory assassin bugs (Hemiptera: Reduviidae) decorate themselves with a coat of dust which they adhere to their bodies with sticky secretions from abdominal setae. To this under- coat, the nymphal instars (of several species) add vege- tation and cast skins of prey items, mainly ants and termites. The resultant “backpack” of trash can be much larger than the animal itself (as in this illustration derived from a photograph by M. Brandt). It had been assumed that the bugs are mistaken by their predators or prey for an innocuous pile of debris; but rather few examples of such deceptive camouflage have been tested critically. In the first behavioral experiment, investigators Brandt and Mahsberg (2002) exposed bugs to predators typical of their surroundings, namely spiders, geckos, and centipedes. Three groups of bugs were tested experimentally: naturally occurring ones with dustcoat and backpack, individuals only with a dustcoat, and naked ones lacking both dustcoat and backpack. Bug behavior was unaffected, but the predators’ Box 14.2 Backpack bugs – dressed to kill? reactions varied: spiders were slower to capture the individuals with backpacks than individuals of the other two groups; geckos also were slower to attack backpack wearers; and centipedes never attacked back- packers although they ate most of the nymphs without backpacks. The implied anti-predatory protection certainly includes some visual disguise, but only the gecko is a visual predator: spiders are tactile predators, and centipedes hunt using chemical and tactile cues. Backpacks are conspicuous more than cryptic, but they confuse visual, tactile, and chemical-orientating predators by looking, feeling, and smelling wrong for a prey item. Next, differently dressed bugs and their main prey, ants, were manipulated. Studied ants responded to individual naked bugs much more aggressively than they did to dustcoated or backpack-bearing nymphs. The backpack did not diminish the risk of hostile response (taken as equating to “detection”) beyond that to the dustcoat alone, rejecting any idea that ants may be lured by the odor of dead conspecifics included in the backpack. One trialed prey item, an army ant, is highly aggressive but blind and although unable to detect the predator visually, it responded as did other prey ants – with aggression directed preferentially towards naked bugs. Evidently, any covering confers “concealment”, but not by the visual protective mech- anism assumed previously. Thus, what appeared to be simple visual camouflage proved more a case of disguise to fool chemical- and touch-sensitive predators and prey. Additional protection is provided by the bugs’ abilities to shed their backpacks – while collecting research specimens, Brandt and Mahsberg observed that bugs readily vacated their backpacks in an inexpensive autotomy strategy resembling the metabolically expensive lizard tail-shedding. Such experimental research undoubtedly will shed more light on other cases of visual camouflage/predator deception. predator. Similar chemicals, called allomones, that benefit the producer and harm the receiver, play import- ant roles in the defenses of many insects, notably amongst many Heteroptera and Coleoptera. The rela- tionship between defensive chemicals and those used in communication may be very close, sometimes with the same chemical fulfilling both roles. Thus, a noxious chemical that repels a predator can alert conspecific insects to the predator’s presence and may act as a stimulus to action. In the energy–time dimensions shown in Fig. 14.1, chemical defense lies towards the energetically expensive but time-efficient end of the spectrum. Chemically defended insects tend to have high apparency to predators, i.e. they are usually non- cryptic, active, often relatively large, long-lived, and frequently aggregated or social in behavior. Often they signal their distastefulness by aposematism – warning signaling that often involves bold coloring (see TIC14 5/20/04 4:40 PM Page 361 362 Insect defense Plates 5.6 & 6.2) but may include odor, or even sound or light production. 14.4.1 Classification by function of defensive chemicals Amongst the diverse range of defensive chemicals produced by insects, two classes of compounds can be distinguished by their effects on a predator. Class I defensive chemicals are noxious because they irritate, hurt, poison, or drug individual predators. Class II chemicals are innocuous, being essentially anti-feedant chemicals that merely stimulate the olfactory and gus- tatory receptors, or aposematic indicator odors. Many insects use mixtures of the two classes of chemicals and, furthermore, Class I chemicals in low concentrations may give Class II effects. Contact by a predator with Class I compounds results in repulsion through, for example, emetic (sickening) properties or induction of pain, and if this unpleasant experience is accompanied by odorous Class II compounds, predators learn to associate the odor with the encounter. This conditioning results in the predator learning to avoid the defended insect at a distance, without the dangers (to both predator and prey) of having to feel or taste it. Class I chemicals include both immediate-acting substances, which the predator experiences through handling the prey insect (which may survive the attack), and chemicals with delayed, often systemic, effects including vomiting or blistering. In contrast to immediate-effect chemicals sited in particular organs and applied topically (externally), delayed-effect chemicals are distributed more generally within the insect’s tissues and hemolymph, and are tolerated systemically. Whereas a predator evidently learns rapidly to associate immediate distastefulness with particular prey (especially if it is aposematic), it is unclear how a predator identifies the cause of nausea some time after the predator has killed and eaten the toxic culprit, and what benefits this action brings to the victim. Experi- mental evidence from birds shows that at least these predators are able to associate a particular food item with a delayed effect, perhaps through taste when regurgitating the item. Too little is known of feeding in insects to understand if this applies similarly to predatory insects. Perhaps a delayed poison that fails to protect an individual from being eaten evolved through the education of a predator by a sacrifice, thereby allowing differential survival of relatives (section 14.6). 14.4.2 The chemical nature of defensive compounds Class I compounds are much more specific and effect- ive against vertebrate than arthropod predators. For example, birds are more sensitive than arthropods to toxins such as cyanides, cardenolides, and alkaloids. Cyanogenic glycosides are produced by zygaenid moths (Zygaenidae), Leptocoris bugs (Rhopalidae), and Acraea and Heliconius butterflies (Nymphalidae). Cardenolides are very prevalent, occurring notably in monarch or wanderer butterflies (Nymphalidae), certain cerambycid and chrysomelid beetles, lygaeid bugs, pyrgomorphid grasshoppers, and even an aphid. A variety of alkaloids similarly are acquired conver- gently in many coleopterans and lepidopterans. Possession of Class I emetic or toxic chemicals is very often accompanied by aposematism, particularly coloration directed against visual-hunting diurnal predators. However, visible aposematism is of limited use at night, and the sounds emitted by nocturnal moths, such as certain Arctiidae when challenged by bats, may be aposematic, warning the predator of a distasteful meal. Furthermore, it seems likely that the bioluminescence emitted by certain larval beetles (Phengodidae, and Lampyridae and their relatives; section 4.4.5) is an aposematic warning of distastefulness. Class II chemicals tend to be volatile and reactive organic compounds with low molecular weight, such as aromatic ketones, aldehydes, acids, and terpenes. Examples include the stink-gland products of Hetero- ptera and the many low molecular weight substances, such as formic acid, emitted by ants. Bitter-tasting but non-toxic compounds such as quinones are common Class II chemicals. Many defensive secretions are complex mixtures that can involve synergistic effects. Thus, the carabid beetle Heluomorphodes emits a Class II com- pound, formic acid, that is mixed with n-nonyl acetate, which enhances skin penetration of the acid giving a Class I painful effect. The role of these Class II chemicals in aposematism, warning of the presence of Class I compounds, was considered above. In another role, these Class II chemicals may be used to deter predators such as ants that rely on chemical communication. For example, prey such as certain termites, when threatened by predatory ants, release mimetic ant alarm pheromones, thereby inducing inappropriate ant behaviors of panic and nest defense. In another case, ant-nest inquilines, which might provide prey to their host ants, are unrecognized TIC14 5/20/04 4:40 PM Page 362 as potential food because they produce chemicals that appease ants. Class II compounds alone appear unable to deter many insectivorous birds. For example, blackbirds (Turdidae) will eat notodontid (Lepidoptera) caterpillars that secrete a 30% formic acid solution; many birds actually encourage ants to secrete formic acid into their plumage in an apparent attempt to remove ectoparasites (so-called “anting”). 14.4.3 Sources of defensive chemicals Many defensive chemicals, notably those of phytophagous insects, are derived from the host plant upon which the larvae (Fig. 14.5; Box 14.3) and, less commonly, the adults feed. Frequently, a close association is observed between restricted host-plant use (mono- phagy or oligophagy) and the possession of a chemical defense. An explanation may lie in a coevolutionary “arms race” in which a plant develops toxins to deter phytophagous insects. A few phytophages overcome the defenses and thereby become specialists able to detoxify or sequester the plant toxins. These specialist herbivores can recognize their preferred host plants, develop on them, and use the plant toxins (or metabol- ize them to closely related compounds) for their own defense. Although some aposematic insects are closely asso- ciated with toxic food plants, certain insects can produce their own toxins. For example, amongst the Coleoptera, blister beetles (Meloidae) synthesize cantharidin, jewel beetles (Buprestidae) make buprestin, and some leaf beetles (Chrysomelidae) can produce cardiac glycosides. The very toxic staphylinid Paederus synthesizes its own blistering agent, paederin. Many of these chemically defended beetles are aposematic (e.g. Coccinellidae, Meloidae) and will reflex-bleed their hemolymph from the femoro-tibial leg joints if handled (see Plate 6.3). Experimentally, it has been shown that certain insects that sequester cyanogenic compounds from plants can still synthesize similar compounds if transferred to toxin-free host plants. If this ability pre- ceded the evolutionary transfer to the toxic host plant, the possession of appropriate biochemical pathways may have preadapted the insect to using them subsequently in defense. A bizarre means of obtaining a defensive chemical is used by Photurus fireflies (Lampyridae). Many fireflies synthesize deterrent lucibufagins, but Photurus females cannot do so. Instead they mimic the flashing sexual signal of Photinus females, thus luring male Photinus fireflies, which they eat to acquire their defensive chemicals. Defensive chemicals, either manufactured by the insect or obtained by ingestion, may be transmitted between conspecific individuals of the same or a different life stage. Eggs may be especially vulnerable to natural enemies because of their immobility and it is not surprising that some insects endow their eggs with chemical deterrents (Box 14.3). This phenomenon may be more widespread among insects than is recognized currently. 14.4.4 Organs of chemical defense Endogenous defensive chemicals (those synthesized within the insect) generally are produced in specific glands and stored in a reservoir (Box 14.4). Release is through muscular pressure or by evaginating the organ, rather like turning the fingers of a glove inside- out. The Coleoptera have developed a wide range of glands, many eversible, that produce and deliver defensive chemicals. Many Lepidoptera use urticating (itch- ing) hairs and spines to inject venomous chemicals into a predator. Venom injection by social insects is covered in section 14.6. Chemical defenses 363 Fig. 14.5 The distasteful and warningly colored caterpillars of the cinnabar moth, Tyria jacobaeae (Lepidoptera: Arctiidae), on ragwort, Senecio jacobaeae. (After Blaney 1976.) TIC14 5/20/04 4:40 PM Page 363 364 Insect defense In contrast to these endogenous chemicals, exogenous toxins, derived from external sources such as foods, are usually incorporated in the tissues or the hemolymph. This makes the complete prey unpalatable, but requires the predator to test at close range in order to learn, in contrast to the distant effects of many endogenous compounds. However, the larvae of some swallowtail butterflies (Papilionidae) that feed upon distasteful food plants concentrate the toxins and secrete them into a thoracic pouch called an osmeterium, which is everted if the larvae are touched. The color of the osmeterium often is aposematic and rein- Box 14.3 Chemically protected eggs males to the females via seminal secretions, and the females transmit them to the eggs, which become distasteful to predators. Males advertise their possession of the defensive chemicals via a courtship pheromone derived from, but different to, the acquired alkaloids. In at least two of these lepidopteran species, it has been shown that males are less successful in courtship if deprived of their alkaloid. Amongst the Coleoptera, certain species of Meloidae and Oedemeridae can synthesize cantharidin and others, particularly species of Anthicidae and Pyro- chroidae, can sequester it from their food. Cantharidin (“Spanish fly”) is a sesquiterpene with very high toxicity due to its inhibition of protein phosphatase, an import- ant enzyme in glycogen metabolism. The chemical is used for egg-protective purposes, and certain males transmit this chemical to the female during copulation. In Neopyrochroa flabellata (Pyrochroidae) males ingest exogenous cantharidin and use it both as a precopulat- ory “enticing” agent and as a nuptial gift. During courtship, the female samples cantharidin-laden secretions from the male’s cephalic gland (as in the top illustration, after Eisner et al. 1996a,b) and will mate with cantharidin-fed males but reject males devoid of cantharidin. The male’s glandular offering represents only a fraction of his systemic cantharidin; much of the remainder is stored in his large accessory gland and passed, presumably with the spermatophore, to the female during copulation (as shown in the middle illustration). Eggs are impregnated with cantharidin (probably in the ovary) and, after oviposition, egg batches (bottom illustration) are protected from coccinellids and probably also other predators such as ants and carabid beetles. An unsolved question is where do the males of N. flabellata acquire their cantharidin from under natural conditions? They may feed on adults or eggs of the few insects that can manufacture cantharidin and, if so, might N. flabellata and other cantharidiphilic insects (including certain bugs, flies, and hymenopterans, as well as beetles) be selective predators on each other? Some insect eggs can be protected by parental pro- visioning of defensive chemicals, as seen in certain arc- tiid moths and some butterflies. Pyrrolizidine alkaloids from the larval food plants are passed by the adult TIC14 5/20/04 4:40 PM Page 364 [...]... derived from the leaves that they eat, within a diverticulum of their fore gut and ooze this strong-smelling, distasteful fluid from their mouths when disturbed (Fig 14. 7) 14. 5 DEFENSE BY MIMICRY The theory of mimicry, an interpretation of the close resemblances of unrelated species, was an early application of the theory of Darwinian evolution Henry Bates, a naturalist studying in the Amazon in TIC14 5/20/04... build-up of pressure in the reaction chamber, which closes the one-way valve from the reservoir, thereby forcing discharge of the contents through the anus (as shown by the beetle directing its spray at an antagonist in front of it) This relieves the pressure, allowing the valve to open, permitting refilling of the reaction chamber from the reservoir (which remains under muscle pressure) Thus, the explosive... they enter wounds caused by the mandibles The metapleural TIC14 5/20/04 4:40 PM Page 373 Further reading 373 rectum depicted in both side and dorsal view in the vignette for this chapter The aposematic yellow-and-black patterns of vespid wasps and apid bees provide models for hundreds of mimics throughout the world Not only are these communication systems of social insects parasitized, but so are their... produced as the pent-up elastic energy is released from the tightly appressed mandibles (Fig 14. 10a) In Capritermes and Homallotermes, the mandibles are asymmetric (Fig 14. 10b) and the released pressure results in the violent movement of only the right mandible; the bent left one, which provides the elastic tension, remains immobile These soldiers can only strike to their left! The advantage of this defense... because the aposematic signal aimed at the observer is diluted as the chances increase that the observer will taste an edible individual and fail to learn the association between aposematism and distastefulness The mimic gains both from the presence of the protected model and the deception of the observer As the mimic’s presence disadvantages the model, interaction with the model is negative The observer... mimicry of ants Annual Review of Entomology 38, 351–79 Moore, B.P & Brown, W.V (1989) Graded levels of chemical defense in mimics of lycid beetles of the genus Metriorrhynchus (Coleoptera) Journal of the Australian Entomological Society 28, 229–33 Pasteels, J.M., Grégoire, J.-C & Rowell-Rahier, M (1983) The chemical ecology of defense in arthropods Annual Review of Entomology 28, 263– 89 TIC14 5/20/04... Although the social insects have some of the most elaborate defenses seen in the Insecta, they remain vulnerable For example, many insects model themselves on social insects, with representatives of many orders converging morphologically on ants (Fig 14. 12), particularly with regard to the waist constriction and wing loss, and even kinked antennae Some of the most extraordinary antmimicking insects. .. outlet of Dufour’s gland enters the sting base ventral to the venom duct The products of this gland in eusocial bees and wasps are poorly known, but in ants Dufour’s gland is the site of synthesis of an astonishing array of hydrocarbons (over 40 in one species of Camponotus) These exocrine products include esters, ketones, and alcohols, and many other compounds used in communication and defense The sting... (cycloalexy) Some larvae lie within the circle and others form an outer ring with either their heads or abdomens directed outwards, depending upon which end secretes the noxious compounds These groups often make synchronized displays of head and/or abdomen bobbing, which increase the apparency of the group Formation of such clusters is sometimes encouraged by the production of aggregation pheromones by early... workers and are of such a size that the head of a single major worker (soldier) can seal it; in others such as the myrmecine Zacryptocerus, the entrances are larger, and a formation of guarding blockers may be required to act as “gatekeepers” A further defensive strategy of these myrmecines is for the head to be covered with a crust of secreted filamentous Fig 14. 9 Nest guarding by the European ant . produces a build-up of pressure in the reaction chamber, which closes the one-way valve from the reservoir, thereby forcing discharge of the contents through the anus (as shown by the beetle directing. distastefulness. The mimic gains both from the presence of the protected model and the deception of the observer. As the mimic’s presence disadvantages the model, interaction with the model. penetration of the acid giving a Class I painful effect. The role of these Class II chemicals in aposematism, warning of the presence of Class I compounds, was considered above. In another role, these

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