Biologists have become keenly aware that insects possess a remarkable ability to biosynthesize a large variety of compounds for use as agents of chemical defense against their omnipresent enemies. Many of these compounds are unique products (e.g., cantharidin, or Spanish fly, produced by blister beetles) with diverse modes of toxicity against a variety of vertebrate and invertebrate predators. These defensive secretions often originate from unlikely sources that appear to optimize the effectiveness of the chemical defensive systems. Ultimately, for countless species of insects, chemical defense and survival are synonymous.
ECLECTIC ORIGINS, FUNCTIONS, AND RESERVOIRS OF DEFENSIVE COMPOUNDS
It would be no exaggeration to state that the tremendous abundance of insects constitutes the primary food source for diverse vertebrate and invertebrate predators. For insects in a variety of orders, blunting the attacks of their omnipresent predators is identified either with the production of defensive compounds in exocrine glands or with the acquisition of these compounds from external sources. These deterrent allomones sometimes represent novel natural products that have a very limited distribution in the Insecta. In short, exocrine compounds, characteristic of species in orders or genera, have evolved to function as versatile agents of chemical defense.
It has been generally assumed that de novo biosynthesis characterizes the origins of insect defensive compounds. However, recent investigations suggest that novel insect defensive allomones, including the complex amide pederin from staphylinid beetles (Paederus spp.), and unique steroids from dytiscid beetles, are biosynthesized by endosymbiotes. These results raise the question of whether other novel insect allomones, including the terpene cantharidin, and steroids in chrysomelids and lampyrids, may have microbial origins.
Often, however, the deterrent allomones constitute ingested alle-lochemicals such as cardenolides (milkweeds) and toxic pyrrolizidine alkaloids (asters, heliotrope). Furthermore, some of these plant natural products have been metabolized after ingestion into products that are suitable for sequestration and use as deterrents, as is the case for ingested steroids from milkweeds by the monarch butterfly, Danaus plexippus. These compounds are also transferred to eggs to function as effective predator deterrents. In addition, these allelochemicals may be added to the secretions of exocrine glands, further increasing the deterrent properties of these exudates. The dependence on ingested plant natural products of some insect species is further emphasized by the utilization of ” stolen ” defensive exudates that essentially represent mixtures of pure allelochemicals that have been appropriated, unchanged, from their host plants.
In some species, ingested allelochemicals are sexually transmitted by the male as a copulatory “bonus” for the female. For example, the sperm-rich spermatophore of ithomiine butterflies is accompanied by pyrrolizidine alkaloids that provide protection for the female and her eggs. Importantly, this very adaptive system is functional because the spermatozoa are resistant to the well-known toxic effect of these alkaloids.
Some allelochemicals also possess great selective value for insects as antibiotic agents. Alkaloids such as alpha-tomatine, a constituent of tomatoes, reduce the infectivity of bacteria and fungi for lepidop-terous larvae. Other compounds reduce the activity of viruses and in some cases are highly toxic to insect parasitoids.
The defensive value of insect allomones has been further enhanced by the ability of these arthropods to adapt a variety of these natural products to subserve a surprising variety of multiple functions. This phenomenon, semiochemical parsimony, has been particularly emphasized by insect species such as fire ants, whose alka-loidal venoms possess a dazzling variety of pharmacological activities. The same may be said of cantharidin (Spanish fly), the potent vesicant from blister beetles.
Things are seldom what they seem. The sting-associated glands of bees and wasps are obvious candidates for the production of compounds with considerable deterrent activities. These glands have evolved as biosynthetic centers clearly dedicated to the biogenesis of pharmacologically active compounds that can be delivered by the sting in an unambiguous act of defense. On the other hand, some glands clearly identified with nondefensive functions have been adapted by a variety of insect species to function as defensive organs with varied functions. Furthermore, the deterrent efficiency of these secretions may be considerably enhanced by adding repellent plant natural products to the exudates. And insects have not neglected adapting enteric products to discourage their omnipresent predators. If all else fails, many insects eject blood, sometimes fortified with toxic allomones, at their adversaries, with startling results. It is no exaggeration to state for these species, bleeding has often provided an extraordinary means of deterring a variety of aggressive predators.
VARIETY OF SALIVARY DEFENSIVE FUNCTIONS
Salivary Venoms
The spitting cobra, Naja nigricollis. has an insect parallel, both in terms of the general chemistry of the saliva and the ability to accurately
“fire” the venom at a moving target. For example, Platymeris rhada-manthus is a black and orange assassin bug (Reduviidae) that is very conspicuous because of its aposematic (warning) coloration. This insect can eject its saliva for a distance of up to 30 cm, and if this enzyme-rich solution (proteases, hyaluronidase, phospholipase) strikes the nose or eye membranes of a vertebrate, intense pain, edema, and considerable vasodilation may follow. The saliva of P. rhadamanthus is admirably suited to deter vertebrate predators including birds and reptiles. This rapidly acting salivary venom has clearly evolved for predation on invertebrates.
Entspannungschwimmen (Chemically Induced Aquatic Propulsion)
The proteinaceous saliva of the hemipteran Vela capraii has been adapted to promote escape from potential predators in aquatic environments. This aquatic true bug will discharge its saliva onto the water surface, a reaction that results in lowering the surface tension of the water behind the bug and propelling it across the aquatic surface.
Allomonal Pheromones
Many bumble bees (Bombus spp.) scent mark territorial sites with cephalic products that are very odoriferous. The secretions, which originate in the cephalic lobes of the salivary glands, are dominated by terpenes, some of which are well-known defensive compounds. This appears to be an excellent example of semiochemical parsimony, with the males utilizing the compounds both as territorial pheromones and as defensive allomones.
Salivary “Glues”
Termite workers in both primitive and highly evolved genera secrete defensive exudates that are rapidly converted to rubberlike or resinous products that can rapidly entangle small predators such as ants. This conversion frequently reflects the polymerization of salivary proteins that have reacted with p-benzoquinone, a highly reactive defensive product. Similar systems for generating entangling salivas have been detected in a diversity of termite genera, including Mastotermes, Microtermes, Hypotermes, and Odontotermes.
Termites in other genera discharge cephalic exudates that are fortified with toxic terpenes. Species of Nasutitermes and Tenuirostritermes secrete mixtures of compounds that rapidly form a resin that entangles ants and other small predators. The presence of monoterpene hydrocarbons is probably responsible for killing ants, and may function as an alarm pheromone for recruiting termite soldiers.
NONSALIVARY ENTANGLING SECRETIONS
The posterior abdominal tergites and cerci of cockroaches in a variety of genera are covered with a viscous secretion that can act as an entangling glue for small predators. Species in genera as diverse as Blatta and Pseudoderopeltis produce proteinaceous secretions on the abdominal tergites that would be readily encountered by predators pursuing these cockroaches. After seizing the cockroaches, centipedes, beetles, and ants rapidly release their prey while cleaning their mouthparts. The fleeing cockroaches generally have more than ample time to affect their escape.
Aphid species in many genera also utilize an entangling secretion as a primary means of defense. The exudate is discharged in response to a confrontation, often hardening to a waxy plaque on an adversary within 30 s. This defensive behavior, which appears to be widespread in the Aphididae, uses tubular secretory organs, the cornicles, on the fifth and sixth abdominal tergites. The secretions, which are dominated by triglycerides, have been characterized in a range of genera, including Aphis, Myzus, Acyrthosiphon, and Therecaphis. The cornicular secretions are clearly more effective against generalized predators (e.g., ants) than they are against specialized predators (coccinellids, nabids). The secretions also contain alarm pheromones, E-B-farnesene and germacrene A, which release dispersive behavior that may cause aphids to drop off plants.
A variety of glands have been evolved by ants as sources of viscous defensive secretions. Many species in the subfamily Dolichoderinae discharge a pygidial gland secretion that is dominated by cyclopenta-noid monoterpenes such as iridodial, compounds that rapidly polymerize on exposure to air. The viscous polymer effectively entangles small predators such as ants. Myrmicine species in the genus Pheidole also use the pygidial glands as a source of entangling glue and in addition, an alarm pheromone.
DEFENSIVE FROTHS FROM DIVERSE GLANDS
A surprising diversity of defensive secretions has been converted to froths that may literally bathe small adversaries with compounds that seem to adversely stimulate the olfactory and gustatory receptors of their predators. The independent evolution of deterrent froths by moths, grasshoppers, and ants demonstrates that this form of defensive discharge can be highly efficacious in adverserial contexts.
Species in the moth families Arctiidae (aposematic tiger moths), Hypsidae, and Zygaenidae often secrete froths, the production of which may be accompanied by a hissing sound and a pungent odor. The aposematism of these moths is enhanced by secretions discharged from brightly colored areas near or on the prothorax. These secretions do not seem to contain plant natural products but rather, toxic de novo synthesized compounds such as pharmacologically active choline esters.
Frothing is highly adaptive in the ant genus Crematogaster. Workers in this very successful myrmicine genus do not possess a hypodermic penetrating sting, but rather, a spatulate sting that is enlarged at the tip. Venom accumulates at the tip and can be smeared onto small adversaries such as ants, as if with a paintbrush. This mode of administration of venom is obviously identified with a topical toxicant that can penetrate the insect cuticle much as an insecticide does.
Two grasshopper species produce froths that are derived from a mixture of tracheal air and glandular secretion. Both species are eminently aposematic, and this warning coloration is enhanced by a powerful odor emanating from the plant-rich froths of the pyrgo-morphid Poekilocerus bufonius, a specialist milkweed feeder, and the acridid Romalea guttata, a generalist feeder with very catholic tastes.
EXTERNALIZING ALLOMONES BY REFLEX BLEEDING
Many insect species, particularly beetles, externalize their distinctive defensive compounds in a blood carrier rather than discharging them as components in a exocrine secretion.
Cantharidin, the terpenoid anhydride synthesized by beetles in the families Meloidae and Oedemeridae, is externalized in blood discharged reflexively from the femorotibial joints. The repellent properties of cantharidin were established more than 100 years ago, and the ability of amphibians to feed on these toxic beetles, with impunity, has been long known, as well. Cantharidin possesses a wide spectrum of activities, including inducing priapism in the human male, and it has been reported to cause remission of epidermal cancer in mammals. Although its role as a repellent and lesion producer certainly documents its efficacy as a predator deterrent, its potent antifungal activity may protect developing meloid embryos from entomopathogenic fungi present in their moist environment.
Autohemorrhage from the femorotibial joints is widespread in many species of ladybird beetles (Coccinellidae), most of which are apose-matic. The blood is generally fortified with novel alkaloids that are outstanding repellents and emetics (i.e., inducers of vomiting) as well.
Adult fireflies (Photinus spp.) produce novel steroids (lucibufa-gins) that are effective repellents and inducers of emesis in invertebrates and vertebrates. Reflex bleeding from specialized weak spots in the cuticle along the elytra and antennal sockets externalizes these steroids. Sometimes rapidly coagulating blood, free of allomones, is used defensively.
BLOOD AS PART OF A GLANDULAR SECRETION
Often the secretions of defensive glands are fortified with blood. For example, arctiid moths (e.g., Arctia caja) discharge odoriferous froths from prothoracic glands, and these exudates contain pharmacologically active choline esters that are accompanied by blood. A similar system characterizes the pyrgomorphid grasshopper P. bufonius.
NONGLANDULAR DISCHARGES OF PLANT ORIGIN
Certain insects have evolved storage reservoirs for plant natural products that can be discharged in response to traumatic stimuli. The evolutionary development reflects the insect’s appropriation of plant allelochemicals (defensive compounds) for subsequent utilization as defensive allomones. In essence, the insects have sequestered the plant’s defenses and stored them in reservoirs where they are available as defensive agents. This defensive system does not require the evolution of any biosynthetic pathways for the synthesis of compounds stored in nonglandular reservoirs.
Adults of hemipterous species in the family Lygaeidae possess dorsolateral (reservoirs) and abdominal spaces that contain a fluid very similar to that of the proteins in the blood. This fluid sequesters steroids (cardenolides) present in the milkweeds on which these species feed. The cardenolides are about 100-fold more concentrated in the dorsolateral fluid than they are in the blood, and they constitute a formidable deterrent system.
Sequestration of plant natural products in nonglandular reservoirs also characterizes larvae of the European sawfly, Neodiprion sertifer. Feeding on pine (Pinus spp.), these larvae sequester both deterrent mono- and sesquiterpenes in capacious diverticular pouches of the foregut.
PLANT NATURAL PRODUCTS IN EXOCRINE SECRETIONS
Herbivorous insects may incorporate plant natural products into exocrine and nonexocrine defensive secretions. By selectively adding plant repellent compounds to their own deterrent secretions, insects can increase the effectiveness of their own chemical deterrents. These plant-derived compounds are generally unrelated to the constituents in the exudates of their herbivores. In all likelihood, these plant additives may augment the repellency of the deterrents by reacting with olfactory chemoreceptors different from those targeted by the insect-derived repellents.
The large milkweed bug, Oncopeltus fasciatus, in common with many species of true bugs, uses the secretion of the metathoracic scent gland as an effective defensive exudate. Nymphs of this species generate defensive secretions with middorsal glandular fluid. The repellent secretions also contain cardenolides derived from the milkweed host plants of this species.
Similarly, the acridid R. guttata sequesters, in the metathoracic defensive glands, plant allelochemicals that can considerably augment the deterrent effectiveness of the secretion. Unlike O. fascia-tus, R. guttata is a generalist that feeds on and sequesters a potpourri of plant natural products. As a consequence, the compositions of the glandular exudates can be variable, sometimes resulting in secretions that are considerably more repellent than those derived from insects that had fed on a limited number of host plant species.
REGURGITATION AND DEFECATION OF ALLELOCHEMICALS
Enteric defense may be widespread in insects as a means of using the proven repellencies of a variety of plant natural products. In a sense, the intestine is functioning as a defensive organ once repellent plant products have been ingested, and it is likely that the presence of pharmacologically active plant compounds in the intestine renders the insect distasteful or emetic. Therefore, transfer of gut contents to the outside either by regurgitation, or by defecation, as seen in milkweed bugs (Oncopeltus spp.), could actually constitute the externalization of the internal enteric defenses.
Lubber grasshoppers readily regurgitate when subjected to traumatic stimuli and the plant-fortified discharge readily repels ants. The same is true of molested larvae of the lymantriid moth Eloria noyesi which produce a discharge containing cocaine from their host plant.
