The Hemipteran suborder Prosorrhyncha comprises two groups, the Coleorrhyncha (family Peloridiidae) and the Heteroptera. Like all hemipterans, members of these two groups have elongated mouthparts for sucking fluids; unlike all other hemipterans, many heteropterans (true bugs) suck the fluids of animals—mostly of arthropods but in a few instances of vertebrates. Heteroptera contains 8 infraorders, 79 families, and about 38,000 described species. The families range from the very small (one species) to the very large (>10,000 species), and heteropterans as a group live in all habitable (and many apparently uninhabitable) parts of the world, from deserts to forest canopies, and on and below the sea. Heteropterans feed on all parts of plants (including on fungi and freshwater algae); some are sufficiently serious predators of pests to be biocontrol agents; and a few (bed bugs, triatomine bugs) feed on human blood. As a whole, Heteroptera is the most diverse of all hemimetabolous insect groups. Nevertheless, we know amazingly little about heteropteran biology and ecology, and the more we learn, the greater this diversity is shown to be.
CLASSIFICATION
The classification of the order Hemiptera is confused, sometimes defies the available evidence, and always arouses controversy. That there ts an order Hemiptera, few doubt; moreover, that the group of true bugs, Heteroptera, is a phylogenetically valid taxon, no one doubts. Questions arise, however, concerning what had been considered the other suborder, Homoptera, a group that some (mostly homopter-ists) elevate to ordinal rank; indeed, some homopterists elevate groups within Homoptera to ordinal rank. However, recent work has shown that Homoptera and some of its subordinate groups are paraphyletic (and may not even be monophyletic). As a result, confusion reigns.
The order Hemiptera is characterized by being hemimeta-bolic (three life stages: egg, nymph, adult), having wings (with a few exceptions), and especially in possessing elongated mouthparts (“beak,” or “rostrum”) designed for the piercing of plants or animals and the sucking up of their juices. The Heteroptera differ from the majority of other hemipterans. In these other insects (mostly homop-terans), the forewings are usually opaque (hence, “Homoptera”), but they are half opaque and half membranous in Heteroptera (again, hence the name). The two groups differ also in the apparent location of the mouthparts, which arise from the ventral surface of the head in both groups but, in Homoptera, arise from the back of the head (sometimes appear to arise from the thorax) and, in Heteroptera, arise from the front of the head. In addition, all homopterans, but not all heteropterans, are herbivorous. Nearly all nonheteropterans, except coleorrhynchans, have a filter chamber, which allows water ingested with the dilute plant juices to be ” short-circuited ” in the digestive system for rapid elimination. Heteropterans also differ from homopterans in that many feed on animal juices, a few indeed on the blood of vertebrates (including humans). It is likely that animal-feeding characterized the early heteropterans, although this view is controversial.
There is some confusion over the meaning and extent of “Hemiptera” and over just what a “bug” is. To some, “Hemiptera” refers only to Heteroptera, which is treated as an order the equivalent of Homoptera. To others, including most if not all students of Heteroptera, “Hemiptera” is an order with two suborders, Heteroptera and Homoptera. The features (i.e., synapomorphies) that the two groups share seem to be far more basic and significant than the two groups) differences, a circumstance that is best represented by treating all members of the two groups, Heteroptera and Homoptera, whatever this latter group may in fact contain, as belonging to an order, Hemiptera.
Because the group known as “Homoptera” (= nonheteropteran) is either paraphyletic or not monophyletic, the higher classification of
Hemiptera is in flux. One consequence of the recent analysis of these relationships (based particularly on molecular evidence) has been the recognition of a small formerly homopteran group, Coleorrhyncha, as the sister group of Heteroptera. These two—Coleorrhyncha and Heteroptera—have been placed by some as a single hemipteran suborder, Prosorrhyncha. Although this idea was based on molecular evidence (and therefore likely to be discounted by some), morphological evidence also supports it. This article considers the hemi-pteran suborder Prosorrhyncha. Because the Coleorryncha is very small and of limited distribution, the focus is on Heteroptera.
Coleorrhyncha
The Coleorrhyncha is a group that contains the single family Peloridiidae, which had once been treated as a major homopteran group (Coleorrhyncha) and then as a group equal in taxonomic status to Heteroptera and Homoptera (sensu antiquo) and perhaps “bridging the evolutionary gap” between them.
The dozen or so species of Peloridiidae have a classic Gondwana distribution; they occur in southern South America, New Zealand, and Australia and are associated with southern beech trees (Nothofagus), where they feed probably on moss (like idiostolids, mentioned later under Pentatomomorpha). They are small (2-5 mm long) and flattened, and many have expansions on the head and/or thorax which, semitransparent, are quite beautiful.
Heter optera
All insects are not bugs. Heteropterans, however, are indeed bugs, and so are often called “true bugs” (i.e., “real” bugs, not “faithful” ones). The word bug derives from the Middle English word bugge, meaning a “spirit” or “ghost.” If one awakens in the morning with red itching welts, one clearly has been visited in the night by a malevolent wraith or spirit—that is, by a bugge. This, of course, is correct: one has indeed been visited by a bug, by a bed bug (Cimex lectularius), which has fed and fled, leaving behind a red welt and a mystery. Bed bugs are “bugs” and so, by extension, are all their relatives—all het-eropterans. (The original meaning of bugge is retained in English in such words as bugbear and bugaboo, and in the name of the insect-repelling plant, bugbane. And the scientific name of the bed bug, Cimex lectularius, means “bed bug,” cimex being the Latin for bug, and lectularius describing a small couch or bed. The word “cimex,” by the way, was sometimes used by the Romans as a derogatory epithet.)
The suborder Heteroptera is perhaps the largest of the hemime-tabolous groups (with about 38,000 species, and probably considerably more are undescribed), and also among the most diverse. The group’s diversity is reflected in the variety of organisms fed upon, the variety of habitats lived in, and the variety of habits; these varieties are in turn reflected in the variety of shapes, sizes, and ornamentation found among the Heteroptera. Many heteropterans are aquatic or semiaquatic, and in this feature alone they differ from other hemimetabolans. Many are predaceous (upon other arthropods) and some are hematophagous (upon vertebrate blood), and in this feature too they differ.
Like all hemipterans, heteropterans have elongated mouthparts for piercing organisms and the drawing up of those organisms’ juices; predaceous bugs reduce to juice the soft internal organs of their prey. The organisms fed upon include all terrestrial groups of plants (except perhaps algae; but Corixidae include freshwater algae in their diet), other arthropods, snails (fed upon by some giant water bugs), and of course vertebrate blood.
Heteroptera is further distinguished by having scent glands. These occur on the abdominal dorsum in immatures and on the metathoracic pleura in adults. Nymphs lack the thoracic glands, but the abdominal glands occur in adults usually as nonfunctional scars; however, considerable evidence has accumulated showing that in many heteropteran groups one or more of the abdominal glands are functional in adults as well as in nymphs. Another distinctive feature of heteropterans is the scutellum (“little shield”). This triangular structure (broad base anterior) is a modification of the mes-onotum; it may be quite small relative to the body, or quite large. In a few families and in a few members of a very few other families, the scutellum is large enough to cover the wings and the entire dorsum of the abdomen.
Regarding the general account of heteroperan biology that follows, and also the more specific accounts of the different groups, it cannot be too heavily emphasized very little is known about most heteropterans: many of the generalities given here are based on small samples, and what we do not know far outweighs what we do know. The reader is urged to take all general statements, if not with a pillar, then with several grains of salt.
Predaceous bugs, and those feeding on vertebrate blood, are not particularly host specific, although some degree of specificity may be imposed upon them by their habitats: bat bugs, living in bat caves, are restricted to feeding on bats, although given the chance they may feed on other warm-blooded vertebrates; many triatomine bugs live in or with their vertebrate hosts and are perforce restricted to them. A few predaceous bugs are more clearly host specific: the bed bug (everybody’s favorite heteropteran) lives only with humans and does poorly when fed other kinds of blood; certain minute flower bugs (Anthocoridae) appear to specialize on certain species of scale insects (although here the specificity may be habitat driven, not prey driven); and some predaceous mirids prefer certain species of lace bugs as prey. There are few other examples.
The host specificity of herbivorous heteropterans is in general greater than that of predaceous ones. Not all herbivorous bugs are host specific, and among those that are, the specificity is sometimes at the species-species, or species-genus level (bug-plant), but more commonly at the family group-family group level (e.g., Alydinae and Plataspidae on Leguminosae; Rhopalidae: Serinethinae on Sapindaceae). Many bugs, and family-level groups of bugs, are oligo-or polyphagous. Of course, the heteropterans that compete with humans for their food and are agricultural pests are those that are either host specific on crop species or, although polyphagous, can build up large populations quickly on crops.
Measuring host specificity can be impeded by the willingness of bugs to probe nonhost plants, either to test their suitability as food or merely to get water. Too many host-plant records are of this sort; the best records are those of the feeding of immatures, since imma-tures, being wingless, cannot go elsewhere to better their lot.
Most heteropterans (perhaps two-thirds) are herbivorous. Many pierce plants to their circulatory systems and feed on the contents of phloem or (less often) xylem; a few very small heteropterans feed on plant cell contents. These heteropterans thus feed not unlike most homopterans. However, plant sap is low in nutrients, and many het-eropterans feed on reproductive tissues such as flowers, ovules, and ripe and unripe seeds, which are richer in nitrogen; another group of heteropterans (Miridae and some Tingidae) feeds on somatic tissues that, to the delectation of the bugs, mobilize nitrogen when the host is wounded. A very few heteropterans feed on bryophytes, and a few Tingidae are the only heteropterans to induce plant galls. Many herbivorous bugs, especially in the infraorder Pentatomomorpha, contain bacterial symbionts in gastric ceca or mycetomes; these presumably supply necessary trace nutrients.
As mentioned earlier, several heteropterans may become pests on agricultural crops. In the Old World tropics, cotton stain-ers (Pyrrhocoridae) feed on developing cotton bolls and may allow entrance of destructive pathogens; the bugs) excreta also stain the cotton (hence the bugs) name). Sunn pests, species of the genera Eurygaster and Aelia (Scutelleridae and Pentatomidae), are among the most serious pests of small-grain crops (especially wheat) in a broadband of countries from eastern Europe through the Middle East into western Asia. Chinch bugs similarly afflict wheat in North America, and a close relative attacks lawn and golf course grasses in Florida. Lygus bugs (several species), a leaf-footed bug (Coreidae), and southern green stinkbugs (Pentatomidae) feed on a variety of vegetables and fruits and are pests worldwide (lygus especially in the north-temperate regions). Species of Riptortus and Neomegalotomus (Alydidae) may become pests of legume crops (Fig. 1). Several bur-rower bugs (Cydnidae) are pests of many crops and range grasses, upon whose roots they feed. The red pumpkin bug (Dinidoridae) may seriously damage cucurbit crops in Asia. There are many other major pests, and very many other minor or regionally restricted ones; nearly 1000 are discussed in a recent topic by Schaefer and Panizzi. As the foregoing list suggests, most pests specialize on the plant family to which the crop belongs. A few (e.g., lygus, southern green stink bug, and the leaf-footed bug Leptoglossus gonagra) are exceptions, feeding on many unrelated plants and quickly achieving large destructive populations.
Only a few heteropterans are vectors of plant diseases; one important group is Piesmatidae, one of whose members transmits a
FIGURE 1 An alydid (Neomegalotomus parvus), a soybean pest in Brazil.
serious viral disease to sugar beets. Overall, however, heteropterans are far less important than homopterans as vectors of plant diseases, perhaps because most bugs, unlike many homopterans, do not feed directly in plant cells.
The few bloodsucking bugs may cause damage by withdrawing excessive amounts of blood and thus weakening people who may, in addition, be weakened by disease, or frail in health because very old or very young. Bed bug populations may increase to the point where such damage may occur.
Of the two important groups of bloodsucking bugs, the bed and bat bugs (Cimicidae) do not transmit disease pathogens, although there is some slight evidence that the hepatitis B virus may be transmitted by bed bugs in southern Africa. On the other hand, tri-atomine bugs (Reduviidae, subfamily Triatominae) are vectors of Trypanosoma cruzi. T. cruzi causes Chagas disease, a debilitating and often fatal disease of the New World tropics and subtropics (a handful of cases reported in the United States); major international efforts are now under way to eliminate this disease by eliminating the places where the bugs hide. These efforts have been successful in many areas of South America.
Although most heteropterans having an economic impact on humans are harmful, some are beneficial. Chief among the latter are the predaceous bugs that feed on insect pests. Because predators as a rule are not host specific, there are no one-to-one relationships of predator to prey in Heteroptera or in any other group considered for biological control. Nevertheless, many groups of heteropterans have been studied for, and some successfully used in, biological control programs: asopine pentatomids (Pentatomidae, subfamily Asopinae) against many pests, especially garden pests (indeed, an artificial aggregation pheromone has been developed to “call in” these predators); certain minute flower bugs (Anthocoridae) to combat stored-product pests; some predaceous mirids on vegetable and greenhouse crops; and an array of predaceous bugs in field crops. The one exception— remarkably, considering its wide distribution, its variety and numbers of species, and the size (and presumably appetite) of its members— is the Reduviidae. The biological control potential of this family has been surprisingly little explored. It should also be mentioned that the value of very small predators—Anthocoridae, small mirids, early instars of other predators—is unknown; these feed on arthropod eggs and small instars, whose absence goes unnoticed because their presence was overlooked in the first place.
In 1998 Cohen showed that predaceous bugs feed differently than had been thought: instead of merely sucking up the fluids inside a prey, these bugs inject salivary enzymes that digest all soft tissue; the digested material is then sucked up. This discovery has profound implications for biological control: a single predator will be satiated by a far smaller number of prey than had been believed, and will therefore be less effective in controlling pests. This realization is only slowly making its way into the biological control community.
Of less importance is the control of harmful plants, weeds, by plant-feeding heteropterans: Some tingids have been used in various parts of the world to control (not very successfully) the invasive plant lantana; cactus bugs (Chelinidea, Coreidae) have been tested—with small success—against invasive cactus in Australia; and several other bugs have been and are being tested for possible control of other weeds. So far, no major plant pest has been controlled by a heterop-teran, but the exhaustive study of biology and ecology necessary for success in such an endeavor is only now being undertaken.
Detailed accounts of economically important heteropterans are provided in the topic by Schaefer and Panizzi.
COURTSHIP, MATING, OVIPOSITION
Unlike feeding, the sexual lives of heteropterans show little variety. There is little courtship, although males of several species may fight (usually briefly) for the attention of a female. The sexes are brought together initially probably by sex pheromones and, in a few species, by sex-neutral aggregation pheromones; however, only a tiny handful of species, all of them land bugs, has been shown to have pheromones of both types. Mating occurs end to end or with the male directly or diagonally across the female; the position seems to vary with the family group or even the infraorder of the bugs. Mating may be brief or long; if long, the larger female may move about and even feed, while the hapless male scrambles along behind, walking backward.
Mating by bed bugs and some relatives in Anthocoridae and Nabidae (and, just recently discovered, some Miridae), is (to quote from another context) nasty, brutish, and short. The male mounts the female and, with a scimitar-shaped clasper, pierces the side of her abdomen and deposits sperm; in primitive species this traumatic insemination (as it is called) may occur in various parts of the abdomen, allowing sperm to enter the abdominal cavity; in more advanced species (including the bed bug itself), sperm is deposited in a special patch of tissue. Such insemination leaves small healed wounds in the female’s cuticle; counting these, the number of times an individual has been mated can be determined. Sperm then progresses to a sperm storage organ at the base of the common oviduct.
The internal reproductive structures are very conservative—that is, they resemble those of very many other insects. There is a pair of ovaries or testes, each almost always consisting of seven ovarioles or testicular follicles. Paired ducts lead from them to a common duct, with which may also be associated various glands and (in females) organs for sperm storage. The external genitalia are more complex, consisting in the male of a genital capsule (“pygophore”) containing a pair of claspers and the intromittent organ and, in the female, of a genital chamber into which sperm is deposited and a complex ovipositor designed in some bugs for the laying of eggs on surfaces (“platelike ovipositor”) and, in others, for inserting eggs into crevices or actually into slits in vegetation (“laciniate ovipositor”).
As is true of many other groups, the external genitalia of male heteropterans are usually more complex and varied than those of the female. In Heteroptera as in other groups, genitalia provide very useful characters for taxonomic and phylogenetic studies.
The egg is often the stage that survives inhospitable seasons (winter, dry season), and so eggs are laid where they may best be protected from the elements as well as from predators and parasites. Eggs are laid also where food will be available, because the immatures, wingless (of course), cannot seek food themselves. The latter requirement presents certain difficulties to predaceous bugs, which cannot be certain where prey will occur. Perhaps this accounts for the habitat specificity (resulting in a certain degree of prey specificity) of some predators, as mentioned earlier: predators’ eggs are laid on plants on which certain prey species are host specific; the predator then in turns appears itself to be host specific, on the herbivore. Perhaps.
The egg itself varies considerably in shape from group to group; it may be round or oval, and in stinkbugs especially the eggs are barrel shaped. Each egg bears small openings through which it was fertilized, and many have other small openings for oxygen intake. Carbon dioxide is released through the shell (chorion). The few eggs that have been studied have a complex architecture of the chorion, presumably related both to gas exchange and to maintaining an appropriate humidity balance.
Eggs are laid singly or in small batches (rarely more than 100), and if in batches may be laid apparently at random or in tidy rows,sometimes more than a single egg deep. They may be deposited on surfaces (of leaves, stems or trunks, ground, stones, etc.) or placed into crevices; the crevices may in some groups be created by the female’s ovipositor. The eggs of some mirids and tingids absorb water in the spring, and thus nymphs hatch just as the plant becomes suitable for feeding.
The females of some heteropteran groups (some Tingidae, many— all?—Acanthsomatidae; a few others) guard their eggs and the early immature stages. Guarded eggs have been shown to be less heavily parasitized, and guarded nymphs less heavily preyed upon, than unguarded eggs and nymphs. A single female will lay several batches of eggs. In a few groups [some giant water bugs (Belostomatidae), at least one coreid], females lay eggs on the backs of males. Belostomatid males then aerate the eggs, sweeping fresh water over them; without such aeration, the eggs might die of oxygen lack and/or of fungal infection. In some species each new batch requires a fresh mating; in bloodsucking species each new batch requires a blood meal.
Hatching occurs sometimes through areas of weakness in the egg’s chorion; not all species’ eggs have such areas. In some groups (Pentatomoidea, some Coreoidea, and others?) the new hatchling (first instars) do not feed, although they may take water, and pen-tatomoids may suck up symbionts from the emptied eggs. Nearly all heteropterans have five immature stages (instars) (those that do not, have four; very rarely are there six), and except for blood-feeding bugs, the stimulus to molt from one instar to the next is unknown. Blood-feeding bugs require the stimulation (manifested as a distension of the abdomen) of a blood meal to molt.
As the instars grow larger at each successive molt, the wing pads develop; as these become more and more distinct, one can determine the instar by the degree of their development.
The instars (except sometimes the first one) feed for the most part on the same food as their adults. Exceptions include predaceous bugs, whose smaller instars may take smaller prey (although a group of small instars may attack a single large slow prey, like a caterpillar); and some herbivores, whose instars do not feed on the plants chosen by their adults, probably because of seasonal differences in the plants’ availability, and/or because some plants may provide nutrition to the young and others nutrients needed for reproduction to the adult.
Development (egg to egg) in temperate climes usually takes a year, the egg overwintering or sometimes a mated female (less often, other stages). In regions of less predictable or less severely contrasting seasons, there may be several—rarely, many—generations in a year. Even when there is only one annual generation, however, populations of some pest heteropterans can build up over a very few years.
A distinctive feature is the possession by some heteropterans of a pair of small (micro- or m- ) chromosomes. The sex-determining mechanism is XY, although XO occurs in some groups and, in others (especially the bed bugs, Cimicidae), multiple X chromosomes may occur. The chromosomes are holocentric, and numerical doubling of the autosomal complement has occurred in several groups and, probably, reduction in others.
DISPERSAL
As with all living things, dispersal is an important aspect of heteropterans’ lives, necessary for the leaving of places no longer suitable and for the discovery of places as yet unex-ploited; it is necessary, too, for the finding of nonsibling mates. The wingless immatures depend upon the mother to place them where resources—biotic and abiotic—are suitable for development.
Dispersal for mate finding appears to be far more frequent among bugs than dispersal for the discovery of new habitats, although of course it may often serve both purposes. One important exception
is the dispersal of cotton stainers (Dysdercus spp., Pyrrhocoridae) from areas where high populations have depleted food to new areas, which may include cotton fields. After the move, females resorb the flight muscles, converting the products into eggs; thus such dispersal occurs but once. (Evidence suggests that not all Dysdercus spp. do this.) Another exception may be the moonlit flights of some giant water bugs (Belostomatidae) in Africa; it is not clear that these flights correspond to drying of habitat. Like other insect groups, Heteroptera contains some groups that are drawn to light traps (white or black light) and some groups that are not; no one has listed these groups, much less sought a correlation between being attracted to light and having a propensity to disperse.
Of course, for many heteropterans resources are replenished: for predators, new prey is continually being produced; and many smaller herbivores feed on annual plants that appear and disappear too rapidly for their populations to be seriously reduced. In addition, many herbivorous bugs feed on several different species and turn easily from one host to another. Thus for these bugs, dispersal may at times be necessary, but it is not a constant need.
Far better documented for far more heteropteran species is movement in response to sex pheromones, often produced by both sexes. In addition, aggregation pheromones occur in some species. This type of dispersal is of course a “pull” dispersal, not a “push” dispersal: the insect is drawn toward something rather than being driven away. Nevertheless, like the messengers in Through the Looking-Glass (one to fetch and one to carry), movement toward a conspecific may draw one also to fresher resources. The pheromone of at least one beneficial predaceous bug has been synthesized, patented, and marketed to draw these bugs into users’ gardens.
ENEMIES AND DEFENSE
Heteropterans have the same enemies as other organisms: predators that would eat them from the outside and parasites that would eat them from the inside. The major predators—again like other insects’—are insects; vertebrates seem to be less important than they are for some other insect groups. Bugs may be protected from vertebrate predators by the secretions of their metathoracic scent glands, which also (it has been suggested) protect bugs from ants; the experimental work demonstrating these possibilities is scant and mostly anecdotal.
Many bugs are also protected from visually orienting vertebrates by being bad tasting and warningly colored. Aposematic coloration occurs in nearly every group of land bug as an arresting contrast of black and red, yellow, orange, or white; the similarity of color and pattern has little to do with genetic or phylogenetic relatedness, and much to do with the strictures placed on color by limited metabolic pathways, as well as the limits placed on pattern and design by the strictures of small body size. Thus unrelated aposematic bugs may resemble one another merely because the possibilities for variety are few. However, as in other groups of animals, both Batesian and Mullerian mimicry occur in Heteroptera: the edible look like the inedible (Batesian) and the inedible look like other inedibles (Mullerian). Mimetic assemblages occur, although they have been little studied. Certain cotton-stainer relatives (Pyrrhocoridae) and their predators look much like certain Reduviidae. It has been suggested that the reduviids can thus slip unnoticed upon their prey (“aggressive mimicry”). This seems outrageously unlikely: more probably, the group as a whole benefits from a collective aposematism, from which the pyrrhocorids benefit more than they lose from being preyed upon.
Few creatures like to eat ants, and it is not surprising that ant mimicry has arisen often in the Heteroptera. The immatures of some Alydidae resemble specific species of local ants; and as the immatures become larger, they resemble increasingly larger species of ants. One assumes that looking like ants is good; no one has tested the idea.
None of these defenses (except perhaps scent) is especially effective against other insects. More effective (guessing here) are the thickened cuticles of many heteropterans, the coriaceous hemelytra, as well, perhaps, as the enlarged scutellum of several bugs.
Body shape may also play a part: the round sleek surfaces of Canopidae, Plataspidae, Megaridiidae, and a few other heteropter-ans offer the jaws of small predators (especially mandibulate insects) little purchase. And the many small spines of coreid nymphs (and others), and the single large spine of adult Cyrtocoridae and some Podopinae (Pentatomidae), must also prove to be unpleasant surprises to vertebrate predators.
It is difficult to know whether heteropterans are more or less parasitized than other insects. The eggs of certain species are often well parasitized by wasps, and the immatures and occasionally the adults by tachinid files. Two indirect bits of evidence suggest that parasitizing bugs is an old and successful way of life: certain family groups of parasites have evolved that parasitize only heteropterans (Diptera: Tachinidae: Phasiinae; several genera of Hymenoptera). And parental care has evolved several times in Heteroptera, to ward off potential parasites (and predators, but these seem to be a lesser evil).
It has been carefully shown that guarding by parents (usually but not always females) protects certain lace bugs (Tingidae), coreids, and many acanthosomatids from parasitism and preda-tion; and the eggs placed upon the backs of some giant water bugs (Belostomatidae) are protected from fungal parasitism by the water currents generated by the male’s rowing movements.
THE INFRAORDERS AND FAMILIES OF HETER-OPTERA
Cladistic work on the morphology of heteropter-ans has resulted in a new classification into eight infraorders: Enicocephalomorpha, Dipsocoromorpha, Gerromorpha, Nepomorpha, Leptopodomorpha, Cimicomorpha, Pentatomomorpha, and Aradi-morpha. In a commonly accepted (but not thoroughly tested) analysis, each of these infraorders is the sister group of those succeeding. Aradimorpha, the most recently proposed, is not universally accepted.
To some extent, these groupings correspond to earlier ones: Preceding this arrangement, for example, Heteroptera was divided into Hydrocorisae (=Nepomorpha, with some adjustments), Amphibicorisae (=Gerromorpha, with some adjustments), and Geocorisae (the remainder, with some adjustments): “water,” “amphibious,” and “terrestrial bugs,” respectively. The last was divided into Cimicomorpha and Pentatomomorpha, names retained in the new classification with the same family composition (with some adjustments in Cimicomorpha); Aradimorpha was included in the earlier Pentatomomorpha. Each mor-pha name is based on a genus in the infraorder.
The following treatment of infraorders and families of Heteroptera, is presented, once again, with the admonition to recognize that little is known in this area and often details are generalized to an entire family from what is known about a tiny fraction of its members.
Enicocephalomorpha, Dipsocoromorpha These small infra-orders are the most primitive in Heteroptera. The latter is usually assumed to have arisen from the former, but there is some suggestion that each may have arisen separately from one or more related preheteropteran ancestors. Each is small: the two families of Enicocephalomorpha, Aenictopecheidae and Enicocephalidae, contain about 20 and 400 described species, respectively; however, it is probable that several thousand species remain to be described.
The same is true of the Dipsocoromorpha, whose five families are Ceratocombidae (50 described species), Dipsocoridae (30),
Schizopteridae (120), Hypsipteryigdae (3), and Stemocryptidae (1). As in Enicocephalomorpha, there remain to be described many hundreds, if not thousands, of dipsocoromorphan species.
Members of both groups are small (Enicocephalomorpha, 2-16 mm long; Dipsocoromorpha, perhaps the smallest of the heteropterans, 0.4-4 mm long). They are all predaceous (as far as is known) and live in or on the soil surface, in leaf litter, or in the interstices of mosses and similar low-growing plants. Their small size, and their life in a habitat of remarkably small interest to biologists or ecologists, render them apparently rare, but actually locally abundant yet nearly wholly unknown.
This is unfortunate, because not only are these bugs of great ecological interest (as predators—and perhaps scavengers—in an ancient and poorly known habitat), but because many occur worldwide and study would yield valuable biogeographic information. Moreover, since they are the most primitive of heteropterans, careful study should reveal much about the origins of this group, as well as its relationships to certain homopteran groups: some enicocephalomorphans share some genitalic characteristics with some auchenorrhynchous homop-terans; and Aenictopecheidae is defined wholly by plesiomorphies.
Some enicocephalids swarm, either in single-sex or mixed-sex swarms, and have been confused with midges! This statement sums up our knowledge of enicocephalomorphan reproductive biology!
Gerromorpha Members of this infraorder are the semiaquatic bugs whose members live near or on water, but never in it. Several members of several gerromorphan families live near or on the surface of the sea and are among the only heteropterans that are, if imperfectly, marine; halobatines (a subfamily of the Gerridae) may occur many kilometers from land. These gerromorphans are semiaquatic bugs—they do not get wet, except occasionally; and indeed a few live not where it is wet, but where it is merely damp. Like other water-associated animals (e.g., Nepomorpha), gerromorphans are usually dark above and pale below.
All are predaceous, those living on the water surface feeding on land arthropods that fall onto and are caught by the water’s surface film; there is some evidence that these bugs may also feed on aquatic crustaceans that are seized upon rising to the water’s surface. Prey is located by many bugs by ripples caused by its struggling. The bugs probably secrete something unpleasant because they themselves are only occasionally preyed upon by fish.
Many gerromorphans are fully or partly winged, some are wingless, and populations of some are pterygopolymorphic (some members wingless, some winged), a phenomenon that may also vary seasonally. The hormonal and ecophysiological bases for pterygopolymorphism has been studied in a few gerrid species. This variety, as well as variety in diapause physiology, is doubtless related to the temporary nature of the habitat, which may dry up or freeze at various locations and times of the year. In temperate regions, many gerromorphans overwinter in debris away from, but close to, their water habitat.
Because of their ubiquity, and especially because of their tight adaptations to an unusual way of life, gerromorphans (especially gerrids) are being used more and more to work out questions in communication and reproductive evolutionary ecology (including courtship). These efforts are helped of course by the wide interest in aquatic ecology, and by the excellent phylogenetic foundations provided by Andersen in 1982 and much recent work as well.
Being semiaquatic predators, a few gerromorphans have been studied for their ability to control rice pests and the aquatic larvae of biting flies; in each situation, success is at best limited, probably because rice pests do not fall into the water often enough and aquatic larvae do not spend much time at the water’s surface.
There are eight families: Mesoveliidae (35-40 species), Hebridae (150), Paraphrynoveliidae (2), Macroveliidae (3), Hermatobatidae (8), Veliidae (720), Gerridae (620), and Hydrometridae (110-115). Several of these families—or components of them—were once contained within a more exclusive Gerridae or Veliidae, but the thorough phylogenetic studies just mentioned have yielded a firm and stable systematic classification.
The insects range in size from very small (1 mm long) to the aptly named Gigantometra (Gerridae), which is up to 36 mm long. Most gerromorphans are at the small end of the range.
Members of the family Gerridae occur worldwide and are among the most frequently seen and frequently admired inhabitants in—or rather on—bodies of fresh water. As they skate about on the surface, their shadows are patterned dark on submerged objects in the water body. This esthetic appeal, and the bugs’ ability to remain on the water, not in it, have earned them various names, such as “water bugs,” “pond skaters,” “wherrymen” (in Britain), and even “Jesus bugs.”
Their shape is characteristic and easily recognized: the head extends somewhat forward of the eyes, the abdomen is often truncate and its segments compressed, and the middle and hind legs are greatly elongated, sometimes looking as if they had been designed for a larger bug. All legs are used in moving on the water’s surface, and the front legs are short, often stout, and used too for prey capture. The claws of all legs are subapical (not apical, as is usual). Probably this is an adaptation for moving on water surface films— something they do with remarkable speed and agility.
Much work has been done on communication and courtship/ reproduction behavior in a few gerrid species: communication is via wave patterns of surface waves and ripples created by the bugs; these ripples apparently serve several functions, including location and courting of potential mates, defining territories, and perhaps even recognizing conspecifics for the avoidance of cannibalism. The extent to which other gerromorphans use similar signals is unknown, although there is some evidence that a veliid does, and it seems reasonable that other surface skaters would also.
Veliidae (riffle bugs, broad-shouldered bugs) is the largest family; the genus Rhagovelia alone contains more than 200 species. Like gerrids’ claws, veliids’ claws are subapical; the legs are not relatively so long (not greatly surpassing the body), the abdomen is more often elongate, the pronotum is larger (covering the rest of the thoracic terga), and the middle legs’ claws of some veliids are modified into a fanlike structure for pushing against the water’s surface. In general, the veliids are smaller than gerrids: 1-10mm vs. 1.5-35mm in length.
Like gerrids, veliids for the most part occur on the surface of ponds or of the quiet stretches of moving water; also like a few gerrids, some veliids live on ocean surfaces, and others are nearly terrestrial, occurring in damp situations or intertidally, or in mangrove swamps. Veliids too feed on smaller animals trapped in the surface film.
Again like gerrids, veliids can move very quickly, and they move even faster when they secrete from the mouthparts a fluid that lowers the surface tension and causes them to “scoot” away.
Veliids may form large assemblages of very many individuals, sometimes almost seeming to cover a stretch of water. What brings and keeps the bugs together is unknown, nor is the advantage of these assemblages clear.
Members of Hebridae are the velvet water bugs, so called because of their coating of fine (presumably hydrofuge) hairs. Quite small (1.23.5 mm long), they are not often collected and live in damp places such as the edges of water bodies, in moss, or in and among waterside vegetation. The family occurs worldwide. Hebrids look somewhat like small veliids, both being somewhat broader and thus relatively shorter than gerrids.
As the names suggest (in English and Latinized Greek), water treaders or marsh treaders (Hydrometridae) walk with measured tread on surfaces close to the water’s edge, and sometimes even on the surface itself. They are classic sit-and-wait predators, motionless for long periods until some small prey comes near. Hydrometrids are elongate insects, small to moderate in size (2.5-20mm or so long); a distinctive feature is the position of the eyes about halfway along the length of the head. The genus Hydrometra, with 80-85 species, is found worldwide, but the rest of the family is tropical.
Mesoveliidae may be the most primitive family in the infraorder, possessing as it does a number of primitive character states and sharing only a few advanced states with other gerromorphans; indeed, the group has at times been excluded from the infraorder, although its inclusion there is now firmly based. Like so many gerromor-phans, mesoveliids are small and pterygopolymorphic (some species); Mesovelia occurs worldwide, but most of the remaining genera are localized. Mesoveliids vary in their habitats: some (many Mesovelia) are active on the water surface, but others live in damp habitats some distance from water; a few are cavernicolous, and a few are intertidal.
The other three families (Paraphrynoveliidae, Macroveliidae, and Hermatobatidae) are small in number of species (113 species in all) and in size (1.5-2.5, 2.5-5.5, and 2.5-4mm long, respectively). The first has so far been found only in southern Africa; the second only in the New World; and members of the third live near coral reefs, where they remain in air bubbles during high tide and feed during low.
Nepomorpha Most of these are the truly aquatic bugs—that is, bugs that actually occur underwater and get wet; the group is the same as the earlier Hydrocorisae (water bugs). Most are predaceous, but corixids are, as a group, more omnivorous. Although nepomor-phans live much of their lives in water, they also are active aerial dis-persers. It is hard to imagine, therefore, why most of these bugs lack ocelli: even if unnecessary below the water’s surface, ocelli ought to be useful in the air (e.g., the riparian families have ocelli). Water bugs range from small (1 mm long, some Helotrephidae) to huge, the largest of the Heteroptera (112 mm long, some Belostomatidae). Like gerromorphans, and for the same reason, most nepomorphans are much paler ventrally than dorsally. Unlike gerromorphans, most (not all) nepomorphans are streamlined, fusiform; those that are not (Gelastocoridae, Ochteridae) are riparian, not wholly aquatic. The antennae of nepomorphans are short and often concealed; hence an earlier name, “Cryptocerata” (“hidden horns”).
Living as most nepomorphans do, underwater, the problem of breathing arises and has been solved in several ways. Two families are nearly terrestrial: Gelastocoridae and Ochteridae live on the edges of streams and breathe like terrestrial bugs. Belostomatids and nepids have extrusible (belostomatids) or permanently exserted (nepids) “airstraps” or siphons, which can be thrust above the surface. Members of the other families rise to the surface periodically to trap air in hydrofuge hairs; oxygen is then taken into the body (much carbon dioxide here as in most animals is released through the body wall); in some groups and to some extent, plastron respiration occurs (i.e., as the oxygen tension in the air bubble drops, oxygen is drawn into the bubble directly from the water). Plastron respiration is so efficient in Aphelocheiridae that these bugs may remain permanently submerged.
Because of these bugs) importance as fish food (and sometimes as human food), because they occur in aquatic habitats, which have always held a fascination for ecologists, biologists, and folks in general, and because some are so large, nepomorphans have probably been better studied as a group than any other infraorder. The literature on the systematics, biology, and ecology of the group and its members is very large.
There are nine families: Corixidae (at least 600 species), Nepidae (225 species), Belostomatidae (150), Naucoridae (nearly 500), Notonectidae (350), Pleidae (40), Helotrephidae (44-120 species: authorities differ), Ochteridae (50-55), and Gelastocoridae (100). All but the last two live below the water’s surface; Ochteridae and Gelastocoridae are riparian (ripicolous).
Corixids (family Corixidae) are the water boatmen, found commonly in ponds, lakes, and (less often) streams throughout the world. More than 600 species make this the largest nepomorphan family. Aspects of their morphology differ so greatly from those of other bugs that Corixidae has sometimes been placed in its own group, separate from other heteropterans. In particular, the labium of the mouthparts is broad and fused to the head, and the foretarsi are modified (enlarged, somewhat flattened, with an array of long setae) for food gathering. Like other nepomorphans, the hind legs are flattened and hairy, for swimming; in particular, corixids look superficially like notonectids, but corixids are flatter and swim rightside up. Under magnification, the dorsum of many corixids has many fine horizontal zigzag and anastomosing pale lines; this feature too distinguishes these bugs from notonectids and, indeed, from other bugs.
Water boatmen are 2.5-15 mm long and occur throughout the world; they live in aquatic habitats of all kinds, including the intertidal. Unlike other nepomorphans, corixids probably feed mostly on algae and (one suspects other small bits of living or dead organic matter). Some are carnivorous, however; indeed, probably many are (only a few have been studied) and are important predators in waters containing few others (e.g., acidified or saline inland waters). Excellent fliers over long distances, water boatmen are often among the first animal colonizers of new aquatic habitats and have even been captured landing on the shiny roof of an automobile in the desert far from the nearest water.
Corixids are of some small importance in feeding on aquatic larvae of noxious dipterans; they are of greater importance as food for commercially valuable fish (and in some cultures, for humans). In addition, they have been used as indicators of organic pollution.
The function of stridulation has been more thoroughly studied in Corixidae than in any other heteropteran group. (The so-called strid-ulitrum on the male’s abdomen is not sound producing but probably aids in clasping the female.)
Superficially similar to corixids are the Notonectidae, backswim-mers [wherrymen (cf. also Gerridae), boat flies] which, however, swim upside down; notonectids swim ventral side up because that is where the buoyant air bubble is. Backswimmers, like water boatmen, are fusiform and also have flattened hirsute hind legs for swimming. However, they have typically heteropteran mouthparts, are wholly predaceous, lack modified foretarsi, and never have the pale irregular linear markings of many corixids. They range from 5 to 15 mm in length. Moreover, unlike corixids, notonectids bite viciously and painfully, as many a hydrobiologist has learned. The largest genus, Notonecta, occurs worldwide, and the other genera are more localized, although sometimes within entire continents.
Like corixids, notonectids are excellent fliers and are also early colonizers of new bodies of water. Some notonectids also may use sound in courtship and mating, but the evidence here is far more slight than that for corixids. Backswimmers inhabit nearly all types of water, although records from saline or near-saline waters are scarce.
These bugs are eager predators and they prey near the water’s surface, whence they may drive their prey, a procedure aided by the bugs’ buoyancy. They feed on other arthropods (and occasionally fish, see later), including small crustaceans and the larvae and pupae of blood-feeding flies. Mosquito larvae and pupae are favored by some notonectids, but over long periods they do not provide consistent biological control; however, female mosquitoes may recognize notonectid-infested ponds and refuse to lay eggs there.
Backswimmers are themselves food for several kinds of fish (good), but may also feed upon fish larvae (bad); however, neither being fed upon nor feeding is of great economic importance.
Pleidae (pygmy backswimmers) and Helotrephidae (no common name) resemble very small (both are about 1^mm long) notonectids; however, pleids lack the flattened hirsute hind legs of notonectids (and helotrephids). Both are oval to globular and very streamlined; helotrephids indeed have head and thorax fused. Like backswimmers, these bugs (both families) swim upside down (although they can at times swim rightside up), and they presumably get oxygen and prey in much the same way as do notonectids. Pleids occur almost exclusively in still waters, permanent or temporary; helotrephids live in almost any kind of water, still, or running, permanent or temporary, hot springs, or water seeps; one species can even wait in the desert for ephemeral waters. Members of both families may be of some small value in controlling mosquito larvae. Pleidae is wholly, and Helotrephidae mostly, tropical.
The giant water bugs comprise the Belostomatidae; here are the largest of Heteroptera, ranging from 9 to 112 mm in length. All are predaceous, and the largest may be important pests in fish hatcheries; one group of species feeds on snails in Africa and is of some value in suppressing populations of snails that carry bilharzia (schis-tosomiasis); the report of a giant water bug attacking baby ducklings may (or may not) be a rural legend. Although active swimmers, belostomatids usually wait on submerged materials to capture prey swimming by. The bugs are attracted to lights, which explains a common name, ” electric light bugs. ”
The belostomatid body is broadly oval and somewhat flattened; the forelegs are modified for grasping, and one claw is reduced. The eighth abdominal tergum is modified laterally into a pair of extrusible airstraps, which can be thrust above the water’s surface and through which air is moved to an air bubble below the wings. In several subfamilies several antennal segments bear fingerlike projections.
Giant water bugs are well known for the remarkably painful “bite” (actually, stab) they can inflict. But they are even better known because females of one subfamily (Belostomatinae) deposit their eggs on the backs of males. The males care for the eggs by swishing water over them; this aerates the eggs and (it has been shown) prevents fungal growth.
These bugs occur throughout the world and are the most diverse in the tropics. In some cultures giant water bugs are dried and eaten; in parts of Asia they are a delicacy.
Closely related to Belostomatidae is Nepidae, the water scorpions; they range in length from 15 to 50 mm. Nepines (subfamily Nepinae) look rather like small belostomatids except for the terminal air siphon, which may be more than twice the body’s length. Ranatrinae also has a long air siphon, and its body is long and very narrow, nearly round in cross section. Like the antennal segments of belostomatids, those of nepids have projections; unlike belostoma-tids, nepids have one-segmented tarsi.
Water scorpions do not swim actively; they are, rather, “sit-and-wait” predators, often sitting patiently on vegetation in quiet ponds until appropriate prey wanders past. They grab the prey swiftly with the forelegs, rather like aquatic preying mantids.
Like Belostomatidae, Nepidae occurs worldwide but is particularly abundant in the tropics.
The toad bugs, Gelastocoridae (6-15mm long), are riparian, not truly aquatic (Fig. 2); they look (at least to the extremely untrained
FIGURE 2 A toad bug, Gelastocoris oculatus (Gelastocoridae), Riverside, CA.
eye) like tiny toads, and they jump. The body is rough-textured and lumpy (“warty”); the eyes large, and the forefemora and foretibiae modified for prey capture. They occur throughout the world, and most species are tropical.
Ochterids (Ochteridae), or velvety shore bugs, are also riparian, living along the margins of water bodies. Unlike most other nepo-morphans, ochterids have antennae that are visible (although small); the bugs are 4-9 mm long; and are mostly but not wholly tropical. With their visible antennae, suboval shape, and often mottled color patterns, ochterids look rather like saldids (see later, under Leptopodomorpha), a leptopodomorphan group that indeed is ecologically replaced by ochterids in the tropics.
Naucoridae, which contain the creeping water bugs, or saucer bugs, are 5-20 mm long and elongate-oval, with hidden antennae and enlarged forefemora. They look like small belostomatids; however, naucorids lack airstraps, their eyes are relatively larger than belostomatids’, and their dorsal surface is sometimes mottled.
Two naucorid subfamilies, Aphelocheirinae and Potamocorinae, are often treated as separate families in the recent literature, partly because they have small but visible antennae and other nonnaucorid features. The former subfamily (60 species) ranges in length from 3.5 to 12 mm and contains the best plastron breathers in Heteroptera. So effective in trapping and keeping the air bubble are their hydrofuge hairs that these bugs can remain their entire lives below water, using the bubble as a physical gill. This ability allows aphelocheirines to live deep in the water, a niche unavailable to other aquatic bugs which must surface at least occasionally to replenish their air supply. Aphelocheirinae, like Nepinae, are primarily tropical, but with significant representation in the Holarctic (Nepinae) or Palearctic (Aphelocheirinae) region.
The eight potamocorine species are all Neotropical and look like very small (2.5-3 mm long) naucorids except for the visible if small antennae. Nothing is known of their biology.
Leptopodomorpha With one exception, the families of this infraorder have few species and are poorly known. The family groups in Leptopodomorpha have been arranged variously by various authors. This article follows Schuh and Slater, who in 1995 listed four families: Saldidae (265 + species), Aepophilidae (1), Omaniidae (5), and Leptopodidae (about 40). Most leptopodomorphs live near water, in damp places, and members of the Omaniidae and Aepophilidae are intertidal; many leptopodids, however, live in quite dry habitats. These bugs are small (about 1-7.8 mm long), with large eyes (except Aepophilidae) and a broad head. All are predaceous (as far as is known).
The largest and best-known family is Saldidae, whose members range in length from 2 to 7.8 mm. Known as shore bugs, saldids occur in damp areas near water; they are excellent jumpers, fly readily, and are more difficult to collect than they at first appear to be. The eyes are indented medially (kidney-shaped), and the dorsum of many species is mottled dark and light. The male has a grasping structure on the side of the abdomen. Shore bugs occur mostly in temperate regions (somewhat unusual for heteropterans) and may occur at fairly high elevations or quite far north (e.g., Alaska); a few are intertidal or found in salt marshes.
Aepophilidae and Omaniidae are wholly intertidal. Indeed, the single aepophilid species lives below the water, breathing (like Aphelocheiridae) via plastron respiration with an air bubble permanently trapped in a dense mat of hydrofuge hairs. Omaniids seek prey on exposed rocks at low tide; at high tide they wait in crevices, probably tapping air bubbles for oxygen. Members of both families are very small (2 and 1-2 mm long, respectively), and presumably feed on even smaller intertidal invertebrates. Aepophilids have quite small eyes, as do aphelocheirids, suggesting that a life permanently under erratically moving water is not sight based.
Aepophilus bonnairei occurs in Europe south to coastal North Africa. Omaniids are known from the Red Sea, south to Aldabra on the African coast, and east to Samoa; it seems likely that they occur on the Indian Ocean coast, and on coasts to the east.
Species of Leptopodidae are about the same size as saldids, ranging from about 2 to 7 mm in length. These bugs vary in shape, and males have a grasping organ similar to but different from that of sal-dids. Most species are tropical, and many occur near water, but others are in quite dry habitats. Some have been collected in ant lion pits, which suggests they may be scavengers.
Cimicomorpha This is by far largest of the heteropteran infra-orders, containing as it does Miridae and Reduviidae, the two largest families. Within the infraorder’s 14 families is the widest variety of foods and of habitats: primitively predaceous on other arthropods, three major groups have moved to feeding on vertebrate blood, and others to feeding on plants. Habitats of various cimicomorphans range from human homes and caves to the webs of spiders, embiids, and psocids; one reduviid “fishes” for termites and another is “led” to its food by ants.
The group has long been recognized (before the current classification of Heteroptera) but is held together only loosely by shared advanced character states, not all of which are possessed by all members. The head usually bears some long-socketed hairs (trichobothria) and is usually prominent and extends directly forward; the forewing’s membrane usually has several closed cells, the claws usually lack pads between them; and the eggs often have a characteristic type and arrangement of microstructures. However the sperm storage organ of other heteropterans (the spermatheca) is in cimicomorphs nonfunctional or either greatly reduced or absent. The cimicomorphan families are united by this last character. Moreover, since each family is more or less phylogenetically related to another, the first and last are joined less by their relationship to each other and more by their relationship one at time to those in between (rather like a group of people in a line holding hands).
With its 6700 species, Reduviidae is the second largest of the Heteropteran families; it is also perhaps the most diverse, as is suggested by the 25, or 22, or 21, or 29, or 23 subfamilies—and the confusion over the number! Suggested by the number is the systematic confusion at the higher taxonomic levels, a situation similar to that in the Pentatomidae (another large family) and—until recently—in the Lygaeidae (yet another).
Reduviids, also called assassin bugs, for the fierce way some attack prey, vary greatly in shape and in size, ranging in length from 3^mm to 40 + mm. All (or most) have a short, stubby, slightly curved beak, designed for being stabbed downward through the cuticle of arthropod prey; well-developed eyes (sight-orienting predators); forefemora often enlarged and with spines for prey capture; forewing membrane with two closed cells; glandular setae and a spongy pad on the foretibiae, presumably to help in grasping; paired first-abdominal glands (Brindley’s glands) whose secretion apparently wards off enemies (but, then, what is the function of the metatho-racic scent glands?); and a stridulitrum on the prosternum whose plectrum is on the beak, also presumably to frighten would-be vertebrate predators. Not all reduviids—even not all reduviid subfamilies and tribes—have all these characters, but most species are two to four times longer than wide, with a large head, bulging eyes, and a stout beak. Most assassin bugs are easily recognized.
All reduviids are predaceous, the great majority on other arthropods. There is some degree of specialization: Ectrichodiinae (645 species) on millipedes, Peiratinae (47 species) on hard-bodied prey like grasshoppers and beetles, Harpactocorinae (2060 species) on soft-bodied prey like grubs and caterpillars, Reduviinae (980 species) on social insects, Emesinae (920 species) on flies, and other subfamilies with usually lesser degrees of specialization (but again it must be emphasized: much generalization here is based on scant data).
FIGURE 3 A triatomine, Triatoma protracta (Reduviidae), on a human host, China Lake, CA.
One group, the subfamily Triatominae, feeds upon the blood of vertebrates (mostly warm-blooded vertebrates). These are the only bugs responsible for a human disease (Fig. 3): Chagas disease is a serious trypanosomiasis in the neotropics, costing many deaths every year. Triatomines that live near or in human dwellings are vectors of the protozoan parasite T. cruzi. An intense cooperative effort by Latin American countries and several other national and international agencies is gradually reducing the range of this disease.
Triatomines are large (50-20 mm long, 5-8 mm wide) bugs, usually brown or patterned light and dark brown. They occur throughout the New World tropics and subtropics (including well into the
United States) and the “wild” (sylvatic) ones feed on small mammals (often burrowing rodents) and (some species) on birds. Domestic triatomines live in the thatch or in litter on the floor of dwellings. One genus (Linshcosteus) occurs only in India; a species complex of Triatoma occurs in Malaysia, Indonesia, New Guinea, and surrounding areas; T. rubrofasciata is pantropical (and may be the ancestor of the species in the second group). The possibility that Triatominae is paraphyletic (or polyphyletic)—t hat its members are descended from several different reduviid groups and independently evolved blood feeding—is being investigated.
Certain reduviid species and smaller groups feed rather strangely: An Indian reduviine (Acanthaspis siva) hunts honey bees at their nests, and some neotropical apiomerines, which wait near resin sites for certain bees to arrive to harvest nest-constructing resin, may even release a kairomone to attract the bees, which are eaten; fossil evidence indicates that the latter relationship goes back at least 25 million years. The Indian harpactocorine Lophocephala guerini feeds on the juices emanating from cow feces (or perhaps on arthropods found within?) and is led to this food by ants, which in turn feed upon the bugs) feces. Many emesines live unentangled in spider or psocid webs, and they feed on their hosts or on prey trapped therein. Salyavata variegata (Salyavatinae, neotropical) waits by crevices in termite nests and disguises itself with bits of the nest itself; it eats termites that emerge to repair the crevice and even uses the remains of fed-upon termites as bait to lure more termites out.
Most reduviids actively seek prey and seize it. Some wait where prey is sure to be found (e.g., termite or bee nests); others wait more patiently for less specific prey. Once seized, prey may be fed upon at once or, often, dragged to a secluded spot. Nymphal reduviids may engage in communal feeding: several bugs feeding on a single prey. This occurs in other predaceous heteropterans too, and probably the pooling of saliva with its digestive enzymes is of benefit to all (except the prey). Several reduviids resemble other heteropterans (e.g., aly-dids, pyrrhocorids) and may be associated with them. Some have thought this a ruse to lure these others to their doom (see earlier comments on this “aggressive mimicry”).
Reduviids are abundant in most habitats. They are large and presumably eat a lot. They are aggressive predators. It is therefore surprising that their possibilities as biological control agents have been so little studied (except—recently—i n southern India, as described by Ambrose).
Phymatidae is a family often included in Reduviidae, and as often treated separately. Also known as ambush bugs, phymatids lie in wait for their prey, grabbing them with ferociously enlarged forelegs. In the United States, a common ambush bug is yellowish and lurks in late-summer yellow flowers, waiting for hapless bees and other insects seeking nectar where “rosae … serae morentur” (to twist Horace a bit).
The small family Pachynomidae contains 15 described species of tropical predators. They look like certain nabids and share characters with several different cimicomorphan groups; recently they have been placed as the sibling group of Reduviidae. They and another family, Velocipedidae, are the only cimicomorphans with ventral abdominal trichobothria (long-socketed hairs, regularly arranged), a feature found more commonly in Pentatomomorpha. Pachynomids range from 3 to 15 mm in length. Nothing is known of their biology— not even the immatures (that they are predaceous is inferred from the thick curved beak).
The family Miridae [Capsidae (Britain), plant bugs], with its 10,000 species, contains nearly one-third of all heteropterans. So vast is the family and so diverse in habits and habitats, that it cannot be covered here. Luckily, Wheeler’s excellent topic on the family’s biology is available.
All but one group of mirids lack ocelli (hence the German name Blindwanzen, “blind bugs”); all are relatively small (1.5-15 mm long), delicate in appearance, usually brown or greenish but often brightly and contrastingly colored, and range in shape from elongated to round to myrmecomorphic. Many (most?) have setae on their surfaces, a “break” in the forewing where leathery part (corium) and membranous part meet, one or two closed membranal cells, and asymmetrical genitalia in the male.
The primitive groups are predaceous, reflecting the predacity of their infraorder (Cimicomorpha). Many mirids are herbivorous, however, although even many of these have reverted to predacity (“s econdarily predaceous”) . Overall, the percentage of predaceous (and scavenging) mirids is quite high; and many others are omnivorous, supplementing a plant diet with arthropod prey, or vice versa. Moreover, many mirids are cannibalistic. In general, then, a great many mirids are opportunistic feeders and, therefore, may be crop pests under one set of circumstances and useful control agents (of weeds or pests) under other circumstances. However, mirids are small and feed on small prey (eggs, small arthropods). Thus they are rarely seen feeding, and their impact on natural ecosystems and on agroecosystems, although great, is much underestimated (this of course is true of all small predaceous arthropods).
FIGURE 4 A mirid, Onceromepotus nigriclavus, Coachella Valley, CA.
Many mirids (Fig. 4) are somewhat host specific, at least at the bug-species to plant-genus/tribe level. The bugs feed, usually intra-cellularly, on the reproductive parts of plants and on new, still-growing somatic tissues. The bugs’ enzymes cause the plant to mobilize nitrogen to these feeding wounds, which the bugs suck up. Many mirids feed on annual plants, and often on plants that appear only briefly (e.g., early successional plants); the brief presence of such plants, and their great diversity, may help explain the diversity of mirids: this type of association would seem to promote speciation.
Some of the predaceous mirids also appear to be host specific, but the specificity would seem to be more one of habitat than of prey: associated with a particular habitat (rhododendron plants, tree bark), the mirids perforce feed on prey found only there (cf. Anthocoridae). Members of one subfamily, Cylapinae, occur with fungi, and although they may feed on arthropods also found there, at least one species feeds directly on the fungus.
Because of their numbers and diversity, mirids occur throughout the world in all manner of habitats (except aquatic, but some are found in salt marshes). Probably a majority of plant species is fed upon by mirids, and their populations may become high locally; mirids are therefore often the most frequently collected of heteropterans.
As mentioned, the family is very large; one genus (Phytocoris) contains more than 600 species. Eight subfamilies are accepted (but not universally), but it is not surprising that there is less agreement about the number and validity of tribes. Much work is needed on cladistic analyses and higher group systematics of Miridae. And, because of the variety in food preferences, in habitats, in degrees of food and habitat specificity, and in other aspects of their biology, biological and ecological data should be used in these analyses.
Related to the mirids are the Tingidae, known as lace bugs because of the elaborate expansions of the thoraces (and sometimes heads and abdomens) of many of these bugs. Although small (1.510 mm long), these are among the loveliest of Heteroptera; some vaguely resemble large coleorrhynchans, but there is no phyloge-netic relationship.
Because of their often bizarre shape and strange (and attractive) outgrowths, it is not easy to characterize lace bugs. The head is small or of moderate size, the body (when shorn of outgrowths) usually oval. In most tingids the expansions of the thorax conceal the scutel-lum and, in some, a pronotal “hood” may partly cover the head; some species are coleopteroid (forewings completely leathery or hard, and closely appressed; the bug looks beetlelike).
The family, with nearly 2000 species, is distributed worldwide; all tingids are herbivorous, even members of a small subfamily that live in ants’ nests and (probably) feed on rootlets that penetrate therein. As a group, lace bugs prefer woody plants (but there are many exceptions) and are quite host specific, either at the plant-specific or generic level. Species in one genus (Acalypta) are among the few heteropterans that feed on mosses; and members of two other genera (Copium and Paracopium) are the only heteropterans that induce gall formation in their host plants. Tingids’ preference for woody (perennial) plants sets them apart from mirids (which seem to prefer annuals) and perhaps partly explains why there are so many more of the latter.
This feeding preference of lace bugs also explains why so many are pests of ornamental and fruit-bearing shrubs and small trees, where they feed mostly on somatic tissue. Large populations can arise quickly, the buildup aided in part by various defensive mechanisms of the nymphs. These range from maternal care through several defensive pheromones and kairomones, to an array of sharp or defensive-liquid-producing setae on the body. Another strategy is the laying of small batches of eggs in different places, a form of bet hedging (this of course occurs in many other groups). These population buildups often lead to major problems localized in time and space.
Maternal care has been carefully worked out in the genus Gargaphia, especially Gargaphia solani. In this species several females may oviposit in a single cluster, which they then communally guard, as well as the resulting nymphs. This opens up the possibility of “cheating”: a female that lays eggs in the cluster but does not help guard it can thus devote more time and resources to producing more eggs.
One other family of Cimicomorpha is herbivorous: the 19 species of Thaumastocoridae feed on a variety of plants, but many feed on palms, and the name palm bugs has been given to the family. These are small (2-5 mm long) insects, broadly to narrowly oval, and flattened. The external genitalia are much reduced: the ovipositor is gone in females, one or both parameres are gone in males; the genital capsule is highly
asymmetrical. Like tingids, these bugs feed on the cells of plants’ somatic tissues (usually leaves), leaving behind pale spots. Populations occasionally build upon ornamental plants to the point of visible damage. One such culprit is the royal palm bug, Xylocoris luteolus, which may at times cause unsightly damage to a decorative palm.
The approximately 400 species of Nabidae are about 8-12 mm in length and most are slight in appearance, which perhaps accounts for the derivation of their name, damsel bugs. All are predaceous, but some will probe plants, probably for water (none survive on plant food alone). The majority of species seem to prefer seeking prey on low vegetation or in fields, and for this reason nabids are an important component of agroecosystems. Nabids also fly readily and disperse well. As a result, several species are cosmopolitan. One genus (Arachnocoris) lives in spiderwebs, probably stealing prey.
Most nabids are brown or light brown, although a few are black and red. The males of most species have a specialized group of tibal setae which, upon being rubbed across part of the genital capsule, spread an attractant pheromone produced in rectal glands.
In many species copulation is normal, but in some a form of internal traumatic insemination (cf. Cimicidae) occurs, wherein the male aedeagus pierces the wall of the female’s genital chamber and deposits sperm in her hemocoel.
Two small cimicomorph families, Medocostidae (one species) and Velocipedidae (discussed earlier), have been placed in Nabidae from time to time. The arguments for excluding them are slightly more persuasive than the arguments for including them (more persuasive for the first than the second); and the evidence for their phylogenetic relationships is equally insecure.
The single medocostid species is about 9 mm length, elongated oval, and presumably predaceous. It has an unusually long fourth ros-tal (beak) segment and lives under bark in western and central Africa.
Three other small families are Plokiophilidae (a half-dozen or so species), Microphysidae (25-30 species), and Joppeicidae (one species). The first appears to be related to Anthocoridae-Cimicidae, but the relationships of the other two are not clear, their affinities with other groups consisting mostly of character-state losses. All are small (1-3 mm long) and predaceous. Of these, the most interesting are the plokiophilid bugs, which live in webs, one species in those of embiids, where they feed on eggs or dead embiids. Other species live in spiderwebs (like some nabids), where they feed alongside the spider on trapped prey. Microphysids are found on tree trunks, and the joppeicid in dry situations.
Closely related to one another are Polyctenidae (bat bugs) and Cimicidae (bed bugs, although most—like all polyctenids—are ectoparasites of bats). Both groups are well adapted as ectoparasites of vertebrates: They are wingless and flattened, the latter an adaptation both for slipping through the hair or feathers of a host and for expansion of the body during engorgement. Cimicids are temporary ectoparasites, moving onto the host only to feed.
As noted earlier, it is cimicids, the bed bugs, that have given their name to heteropterans: true bugs. The 100 or so species are temporarily ectoparasitic on bats, birds (mostly those that roost in groups), and humans. Of the human bed bugs, C. lectularius (worldwide, especially in cooler regions) and C. hemipterus (tropics), the former is among the very few arthropods associated only with humans (like the house fly and the head/body louse). C. hemipterus, the tropical bed bug, may also be found on bats, but it seems to prefer humans.
These human bed bugs are small (5 mm long), round to broadly oval, flat (except when engorged with blood), and brown; they are well known, to the extent that although no one claims to have seen one, everyone knows someone who has. Because bed bugs are secretive
and feed at night, they are not uncommon but are rarely seen, spending the day hidden in crevices in dwellings and in bedclothes. Despite their ubiquity, they usually do little harm. They spread no pathogen (although they have been implicated in transmission of hepatitis B virus in southern Africa, the evidence offered is at best equivocal), and for the most part they are annoying rather than harmful.
Cimicids that feed on birds can cause harm: some feed on poultry and may take enough blood to decrease egg and meat production; and swallow bugs (genus Oecacious) may cause serious damage to populations of these attractive and useful birds.
It is in the human bed bug that traumatic insemination has been studied in the most detail. The male punctures the venter of the female’s abdomen with his scimitar-shaped left clasper. Sperm are deposited either directly into the hemocoel (more primitive cimicids, some noncimicids) or into a patch of tissue specialized for their reception. In either case, the sperm then travel (for part of their journey, from cell to cell) to the base of the ovarioles, where they are stored; this journey cannot occur if the sperm are not activated by an agent in the seminal fluid. Eggs are fertilized as they pass the storage depot. This process has not been worked out for the majority of traumati-cally inseminated species but is probably the same in broad outline.
Unlike bed bugs, polyctenids live permanently on their bat hosts and are so well adapted to this way of life that they closely resemble not cimicids but bat flies (Streblidae, Nycteribiidae). They are eyeless and have claws and stiff setae “designed” as in other ectoparasites to catch on fur and prevent them from being captured and dragged away by the host. Bat bugs have also carried further the traumatic insemination of their relatives: the female is mated before molting to adult, through the base of the right midcoxa into the hemocoel, whence the sperm move close to the oviducts. Here (apparently) fertilization takes place, and here too occurs not only embryogen-esis but also hatching. Nymphs are then “born,” and because some of these births may occur before the female is adult, they represent a form of pedogenesis (i.e., reproduction by immature stages). The embryos are nourished in part directly from the oviduct wall, and the entire process has therefore been termed pseudoplacental viviparity, a phenomenon that occurs in other groups of insects (cf. the tsetse fly). (It is not clear that mating must occur before molting; presumably an unmated adult female can be mated.)
Bat bugs are 3-5 mm in length and occur in the tropics. As a group they show some host specificity, and it would be interesting to compare their host associations with those of streblids and nycteribiids.
Anthocoridae contains 500-600 species and here includes the subfamilies Lyctocorinae and Lasiochilinae, sometimes treated as separate families. Anthocorids are sometimes called minute pirate bugs, perhaps because they are predaceous and some of the more common ones are picturesquely black and white (like the Jolly Roger). Anthocorids’ eyes are prominent, suggesting they orient to prey visually “up close”; some evidence indicates they are initially attracted by the odor of the leaves on which prey are feeding. The left paramere of the male is in many anthocorids modified for traumatic insemination of the female.
Although small (1.5-6 mm long), anthocorids are efficient predators on small arthropods and upon the eggs and early instars of larger arthropods. They are also abundant in many habitats, and for these reasons are quite useful in biological control. In Europe especially, anthocorids are used for control of pests in such confined growing areas as greenhouses. Some members of the Lyctocorinae live in dry areas and have proven useful in the control of stored-food pests.
Many anthocorid species seem to be habitat specific. One impressive example is Elatophilus, whose species are found on the trunks
of north-temperate pines, where they feed on Matsucoccus scale insects; the specificity appears to be one of habitat, not prey. Other anthocorids live on the trunks of other trees, feeding there on small homopterans and sometimes bark beetles.
Also known as flower bugs (again perhaps for their daintily contrasting colors), a few anthocorids—mostly of the large and widespread genus Orius—live on annual plants; but this is not the most important habitat of anthocorids. Most species (as far as is known: not very far) live on tree trunks, some in leaf and other ground litter and the bases of grass clumps, and some in natural accumulations of seed or berries (and in the nests of rodents that have carried these foods in—perhaps evolutionarily en route to living where grain is stored). Because of the considerable value of these bugs in biological control, the literature on their biology is vast. Unfortunately, the literature is concerned with relatively few species, and the biologies of most are wholly unknown. It is known that some species (perhaps many?) supplement their diet with pollen; and at least one may be entirely herbivorous.
Pentatomomorpha This is the second largest of the heterop-teran infraorders. Unlike the others, it (and Aradimorpha) is primitively herbivorous: that is, the ancestor, or the earliest members, of the infraorder, were themselves almost certainly feeders on plant juices. With few exceptions, members of Pentatomomorpha feed on plants. The exceptions are certain Rhyparochromidae that feed on vertebrate blood; members of Geocoridae, which prey on small arthropods as well as plants; a very few Pyrrhocoridae that may be either obligate or facultative predators (it is not always clear which); and Pentatomidae of the subfamily Asopinae, all of whose members are predaceous. For the most part, pentatomomorphs feed on the nitrogen-rich reproductive parts of plants: flowers, ovules, and ripe and unripe seeds. Many, however, feed on plant somatic tissues.
Pentatomomorphs range from the very small (some Lygaeoidea) to the largest of the land bugs. The beak is long, extending usually at least to the mesosternum and sometimes beyond the abdomen; the abdomen’s venter bears a regular number of regularly arranged socketed setae. Associated with the metathoracic scent gland opening is one or more raised structures, and the shape is rounded to narrowly oval (rarely long and thin).
Pentatomomorpha contains five superfamilies—six if one includes Aradoidea. (The recent elevation of this group to infraorder level has not met with universal acceptance, and in this article “Aradoidea” is treated as the infraorder Aradimorpha).
The Idiostoloidea contains two families, Idiostolidae (four species) and Henicoridae (one species); the latter was until recently considered to be a subfamily of Lygaeidae (in the broad sense, as discussed shortly). In some features (e.g., abundance of trichobothria), Idiostoloidea appears to be the most primitive of the pentatomo-morphan superfamilies; however, in Henry’s analysis, this group is the sister group of the families formerly included in Lygaeidae. The biology of Idiostoloidea is not known, although specimens have been captured on the ground, not up on plants. Idiostolids are associated with the moss and litter of southern beech (Nothofagus) stands, and may indeed feed on mosses. The superfamily has a Gondwana distribution occurring in southern South America and in Australia (see also Coleorrhyncha, earlier).
Until recently most members of the superfamily Lygaeoidea were classified in the family Lygaeidae. However, it had long been recognized that the members of this family were not all closely related and that indeed Lygaeidae was paraphyletic and, probably, polyphyletic: that is, Lygaeidae did not include all descendents from the common ancestor,
and indeed different members of Lygaeidae were descended from several different ancestors. In 1997 T. J. Henry applied cladistic analysis to Lygaeidae, as well as to related families, and presented a new classification of the members of the former Lygaeidae. This classification, which has been generally (but not universally) accepted, is used here.
The family Lygaeiodea (sensu Henry) now consists of 15 families: Artheneidae, Blissidae, Cryptorhamphidae, Cymidae, Geocoridae, Heterogastridae, Lygaeidae (sensu strictu) , Ninidae, Oxycarenidae, Pachygronthidae, Rhyparochromidae, Berytidae, Colobathristidae, Malcidae, and Piesmatidae. The last four had already been treated as separate families in the old Lygaeoidea. The superfamily contains roughly 4400 species, most of them in the former “Lygaeidae.”
Lygaeoids are relatively small heteropterans (1-20 mm long); the largest are the milkweed bugs, several of which are common in North America. Milkweed bugs are Lygaeidae (sensu strictu), and many are warningly colored because they are distasteful. Of greater importance are the chinch bugs (Blissidae); all feed on grasses, and several are serious pests of graminaceous crops (wheat, sugarcane, rangeland and lawn grasses, etc.) (Fig. 5). Several other families are of some economic importance (Geocoridae, one of the few facultatively predaceous groups in Pentatomomorpha, in biological control; some Colobathristidae on sugarcane).
FIGURE 5 A lygaeid, Wekiu bug, Nysius wekiuicola. feeding on Calliphoridae.
Members of the largest lygaeoid family, Rhyparochromidae, with nearly half the superfamily’s species, feed on fallen seeds; for this reason they are called seed bugs, a name that by extension is often applied to lygaeoids generally. Members of other lygaeoid families feed on seeds still attached to plants, and others feed directly on somatic tissues (mostly leaves, sometimes in vascular tissue, sometimes in plant cells).
Members of the rhyparochromine tribe Cleradini, and one species in the tribe Udeocorini, feed on vertebrate blood, and it has been suggested they might be able to vector T. cruzi, the pathogen of Chagas disease (see Reduviidae).
There are two families in the Pyrrhocoroidea, the Largidae and Pyrrhocoridae. The first contains about 120 species, and a few are excellent ant mimics. The Pyrrhocoridae, with one exception, occurs only in the Old World. The exception is Dysdercus ( Fig. 6 ), with some 85 species in both the Old and New World tropics; these species are
FIGURE 6 Dysdercus cingulatus (Pyrrhocoridae) on a cotton leaf, Tha Wong Pha, Nan Province, Thailand.
FIGURE 7 Mesquite bug (adult), Thasus neocalifornicus.
frequently pests of cotton crops. Exclusive of Dysdercus, there are about 225 species in the family. Both families are tropical or, in a few species, subtropical.
Of the five families in the superfamily Coreoidea (Coreidae, Alydidae, Rhopalidae, Stenocephalidae, and Hyocephalidae), the first is by far the largest in number of species (1800-1900) and in size; indeed, members of the neotropical coreid genus Thasus may be the largest land heteropterans known (Fig. 7); up to 40 mm in length, being exceeded in this respect only by some giant water bugs (Belostomatidae). The other families are smaller in numbers and size: Alydidae (about 250 species), Rhopalidae (somewhat more than 200), Stenocephalidae (about 30), and Hyocephalidae (3). All are phytophagous.
Members of Coreidae are sometimes called leaf-footed bugs because several species, occurring in several apparently unrelated tribes, have hind tibial expansions (and sometimes antennal expansions) as adults, as nymphs, or as both; their function is obscure, although they may serve to deflect the attacks of birds. Males of several groups of coreids have enlarged hind femora, which are used to defend territories from other males. The nymphs of several species are gregarious, and it would be interesting to learn whether this gregariousness occurs in species whose males are territorial. The coreid head is small relative to the body (cf. Alydidae), and the bugs’ length ranges from about 6 to 40 mm.
Members of the family feed up on plants, some species on ripening seeds and other reproductive parts, and many species on the juices from vascular tissue. Varying degrees of host specialization occur in the family, from mono- through oligo- to polyphagy. Some species feed on cucurbits (hence another common name, squash bugs). Some unrelated coreid groups (Pseudophloeinae, and three coreine tribes) are among the few heteropteran family groups to have broached the defenses of the Leguminosae and to have radiated upon these plants. Several of these bugs are serious pests of legume crops (e.g., pigeon pea) in the Old World tropics.
The males of one species, Phyllomorpha laciniata. are heavily spined and, somewhat like some giant water bug males, carry among the dorsal spines their females’ eggs.
Alydidae—called broad-headed bugs because the head is relatively wide (it also resembles an ant’s)—comprises three groups. The subfamily Alydinae is another group specializing on legumes, upon whose ripening seeds the bugs feed. Several species are pests of legume crops (e.g., soybean, pigeon pea) in the tropics. Immature alydines mimic ants, often successfully enough to fool heteropterists; some species mimic small species of ants as early instars and other larger ant species when older (Fig. 8 ).
FIGURE 8 Broad-headed bug (nymph), probably Megalotomus quinquespinosus (Alydidae). Note ant mimicry.
Some members of the second alydid group (Micrelytrinae: Micrelytrini) mimic ants both as adults and as nymphs. The biology of this pantropical tribe is almost completely unknown, although one species may become abundant on range grasses in northern South America. It has been speculated that many micrelytrines are grass feeders (on grass seeds?), as are members of the other tribe (Leptocorisini) of Micrelytrinae.
All members of Leptocorisini feed on grasses, as far as is known. Some species (genera Leptocorisa, Stenocoris” are elongated and are often serious pests on rice in the Old World. Leptocorisines feed on the rice panicles and, when rice of the appropriate stage is not available, rice bugs feed on wild grasses found nearby. These grasses thus serve as a reservoir for the rice pests; some leptocorisines prefer these grasses to rice, however.
Members of Rhopalidae are called scentless plant bugs because all are herbivorous and the external opening of the metathoracic scent gland is small and placed more ventrally (hence harder to see) than are the openings of other bugs. Rhopalids are not scentless, however, and indeed the scents of a few species have been analyzed.
The subfamily Serinethinae (60-65 species, mostly tropical and subtropical) includes the box elder bug (Fig. 9), which in North America sometimes seeks warmth in houses in late fall. Serinethines feed on sapindalian plants and occasionally become minor pests on these ornamental plants. The 150 or so members of the subfamily Rhopalinae are more drab than the red and black Serinethinae, and far more of them occur in the Holarctic region. They feed on a variety of plants and rarely become pests even locally. At least one species has helped biologically control a weed, velvetleaf, in the United States.
FIGURE 9 Box elder bugs (adult and nymphs), Boisea trivittatus (Rhopalidae: Serinethinae).
Stenocephalidae occurs in the Old World tropics, with a few members in the Palearctic region; the single species on the Galapagos Islands may have been introduced by ship from Africa. Stenocephalids feed on euphorbs, as far as is known. The family is of interest because it possesses certain features of Coreoidea (many) and of Lygaeoidea (ovipositor type, egg type); the phylogenetic significance is unclear.
The three species of Hyocephalidae are all Australian. The family is related to Stenocephalidae, and both families seem to be primitive in the Coreoidea. Little is known of hyocephalid biology except that some occur under stones, where they apparently feed on fallen seeds. Both stenocephalids and hyocephalids are relatively large (8 – 15 mm long) and slender.
Pentatomoidea is a well-defined superfamily, although there is some disagreement (not to say confusion) about the higher classification of the groups within: some heteropterists treat some groups as tribes, subfamilies, or even families, and others treat them differently. The taxonomic limits of Pentatomoidea are clear and agreed upon; and there is general agreement that the various tribes, and so on, are indeed worthy of suprageneric rank: the level of that rank is sometimes argued. A forthcoming catalog of the largest family, Pentatomidae (by D. A. Rider), will help settle some of these questions.
In general, pentatomoids are larger than many other bugs. Most (but not all) have five-segmented antennae (hence the name); most other heteropterans have four. Most are also wider than many other heteropterans, and, ranging in length from about 4 to 30 mm, many pentatomoids appear somewhat “squat.” Quite a few are very brightly colored. All except one subfamily (Pentatomidae: Asopinae) are herbivorous; the superfamily contains general feeders and quite host-specific ones. Within both groups are some serious pests of crops, and asopines have shown some success in biological control.
The largest family, Pentatomidae, whose approximately 4500 species make it slightly larger than Lygaeidae (in the old sense, as discussed earlier), occurs abundantly throughout the world. One species, the southern green stinkbug, Nezara viridula, is cosmopolitan, feeds on just about anything green, is a major pest in some areas and a minor one in many others, and in Asia has several striking color varieties. This species has been so widespread for so long that its place of origin remained unknown until recently: it probably arose in or near Ethiopia.
Pentatomids are for the most part relatively large, ranging in length from 8 to 20 mm. They are also herbivorous, with the exception of one subfamily (Fig. 10). Most of the few pentatomids whose feeding habits are known are polyphagous; some feed more narrowly. Members of one group, related to Aelia, feed on grasses; and several species of Aelia itself are serious pests of small-grain crops (Sunn pests, as discussed shortly in connection with ” Scutelleridae ” ). Pentatomids are among the most serious pests of soybean worldwide: when a new area opens up to soybean production (e.g., southern Brazil several years ago, central Brazil a few years ago), local legume-feeding or poly-phagous pentatomid species rapidly become soybean pests. Because of the family’s size and the number of crops its members feed on, Pentatomidae is one of the most important heteropteran families.
FIGURE 10 Adult predaceous pentatomids (Eocantheconafur-cellata) feeding collectively on a caterpillar (Eupterote mollifera) in southern India.
The subfamily Asopinae is predaceous, a fact easily recognized by its members’ short stubby beak, well designed for stabbing into prey. Asopines are useful in biological control, and one (Perillus bioculatus) specializes on the Colorado potato beetle and related chrysomelids; the red of this bug is derived from ingested pigment of the beetle prey.
Many pentatomids are green or (more often) brown, perhaps as camouflage on plants and ground (some feed up on plants and hibernate or estivate on the ground). However, quite a few are brightly and contrastingly colored and are presumably aposematic. Many pentatomids live on tree trunks and indeed may be the most common group of herbivorous bugs to use this habitat; it is not clear what they feed on, perhaps mosses and other epiphytes and perhaps (occasionally) these bugs can penetrate through to the tree’s cambium.
Most pentatomids are somewhat broad and flattened, but some (like the grass feeders) are more or less elongated. Some members of Podopinae are almost globose and may bear thornlike spines dor-sally (see also Cyrtocoridae).
Various degrees of parental care have arisen in this family (or have been retained from parentally caring ancestors; the point is controversial) and in other pentatomoid families (and elsewhere, rarely). For the most part, this care protects eggs and early instars from parasitism and predation. In many species, however, this effort denies the female an opportunity to feed and, as a result, she produces fewer eggs or batches of eggs than her less caring sisters. The significance of this trade-off remains to be worked out for most species.
Scutelleridae contains 400-500 species in which the scutellum is greatly extended to cover the abdomen (hence the common name, shield bugs); these bugs range from 5 to 20 mm in length and are somewhat more globose than pentatomids (although some of the more spectacular ones are broadly elongate). Several species are brilliantly colored (one genus is Chrysocoris, or golden bug), either in solid sometimes iridescent colors (blues, violets, reds) (Fig. 11) or in bold patterns of spots and stripes. These are among the most beautiful of heteropter-ans and, in some cultures, considered to be among the most tasty. Most however are drab brown or tan, the color sometimes patterned.
Despite their relatively large size and often striking appearance, shield bugs remain poorly known biologically, and very poorly known
FIGURE 11 Coleotichus blackburniae (Scutelleridae).
ecologically. The females of a few care for their young, as do those of a few other pentatomoid families. All scutellerids are herbivorous, and a few are pests of several crops. One group is particularly important.
Several species of Eurygaster are very serious pests of small-grain crops in a broad swath from eastern Europe through the Middle East (where they are the most serious) into eastern Asia. In the spring, these Sunn pests move from upland wild plants down to the fields with the young grain; there they feed first on the young shoots and then on seeds. In late summer or early fall, they move back into the hills and mountains, sometimes undertaking a trip of many miles. Crops may be completely destroyed over a very large expanse.
The family is represented throughout the world, but members of each of the four subfamilies are concentrated in different continents, with a few representatives in one or two other continents (the historical biogeography of the family is needed; the pretty ones are all tropical or subtropical).
Acanthosomatids (Acanthosomatidae; there is no common name) look much like pentatomids, but are somewhat larger (7-20 mm long) and more elongated. Their tarsi have only two segments, and the bugs have several other advanced features. The latest revision (1974) recognizes about 45 genera; there are about 200 species, although no one has listed or cataloged them. As far as is known, acanthosomatids feed on woody plants (trees and shrubs). Maternal care by the females of several species has been thoroughly studied; as in Pentatomidae, protection is provided eggs and early instars against predators (chiefly ants) and parasites; the body-jerking and wing-fanning movements are so strong that small predators may actually be hurled from the leaf.
The 250 species of Tessaratomidae are in general larger (15-26mm long), and paleotropical (a few species in neotropics) (Fig. 12). The second abdominal spiracle is exposed, and a projection from the mesosternum extends anteriorly sometimes beyond the tip of the beak. One tessaratomid, the bronze orange bug (Musgraveia sulciventris), is a frequent pest on citrus in Australia.
Possibly related to this family is Dinidoridae, whose 85-90 members are also large (10-30 mm long) and robust, and whose distribution is roughly that of Tessaratomidae. Here too the second abdominal spiracle is exposed (although this may in both families be plesiomorphic); and often the pro- and mesosternum bear a midline groove. Dinidorids in general prefer cucurbits as food, and one species, the red pumpkin bug, Aspongopus (formerly Coridius) janus, is a pest in India on cucurbit crops.
FIGURE 12 Tessaratomid nymph (Tessaratomidae), Umphang, Tak Province, Thailand.
Urostylinae and Saileriolinae, the two subfamilies of Urostylidae, share several features but look very different and differ considerably in general appearance and in other morphological features; most urostylids are Asian. Urostylines (80-90 species) are elongated, (4-15mm long) and look more like coreids than pentatomoids. Saileriolines are small (2.5- 3.8 mm long), more pentatomoid in shape, and with the anterior part of the forewing (the corium) less “leathery” than in most heteropterans. Some urostylines occasionally attack ornamental trees; in great numbers they may become a problem. One early (and successful!) control method was the use of gunpowder.
Cydnidae (burrower bugs) is the only heteropteran group most of whose members live below ground, sometimes several feet below the surface. Most cydnids are dark brown or black, 1.5- 25 mm in length (most in the range of 5-12mm), and have a wing striduli-trum. Their smooth bodies, flattened heads, and strong forelegs are adapted to digging; so also probably is the coxal “comb” (not a “coxcomb”), an array of stout setae perhaps used for cleaning soil particles from the antennae. The foretibiae of one subfamily (Scaptocorinae) are greatly developed for digging. There are four subfamilies: Sehirinae (60 species), Thyreocorinae (5), Corimelaeninae (200), and Parastrachiinae (2). All live above ground. Females of the Sehirinae and Parastrachiinae care for their eggs and early instars. The Thyreocorinae and Corimelaeninae have sometimes been grouped as a single family; and the two Parastrachia species are large and brightly red and black and have recently been elevated to family rank.
The remaining 350 species are subterranean, feeding on roots. They may at times become serious, although localized, pests of both crops and rangeland grasses.
Cydnidae may be phylogenetically close to the “base” of the Pentatomoidea and may also be related to the group of small families described next.
Within the Pentatomoidea is a number of small families, mostly restricted to the neotropics [Cyrtocoridae (11 species), Canopidae (8), Megarididae (16), Phloeidae (3)] or to Australia [Aphylidae (2 species), and Lestoniidae (2)]. Plataspidae (500 species, a very rough estimate) is primarily paleotropical, but a few species occur in the Palearctic region. Characteristic of many of these families are small size and a rounded globose body, with forewings and/or scutellum enlarged (and often ornamented) to cover the entire abdomen. The cyrtocorid scutellum bears a stout impressive spine. Some (all?) may be related to Cydnidae and to Scutelleridae and as, Schuh and Slater say, the phylogeny and biogeography of these groups need to be worked out. Of phylogenetic importance too is the primitive family Thaumastellidae, whose few members live in southern Africa.
Aradimorpha This infraorder contains two families, Aradidae (1800-2000 species, worldwide) and Termitaphididae (9 species, pantropical). These families were included in Pentatomomorpha, from which Aradimorpha probably evolved.
Aradimorphans are very flattened, and (most striking) their feeding stylets are very long, very narrow, and stored coiled within the head. Termitaphidids are small (2-3 mm long), wingless, eyeless, and ovipositorless; they live in termites’ nests and probably feed, like ara-dids, on fungal mycelia.
Most flat bugs (Aradidae) are larger (3-11 mm long) and live under the bark of dead or dying trees, a habitat to which their flat body and shortened legs and antennae fit them; other aradids live in the litter of the forest floor; and a few live in termites) nests, or vertebrates’ burrows. All these places are closely confined and thus both temperature and humidity vary little, conditions conducive to the growth of fungi, within whose long tubular mycelia the flat bugs feed. This way of life is unique to aradids, which have successfully exploited it (as witness the many aradid species).
One species is an exception: Aradus cinnamomeus (actually, a three-species complex) feeds on the circulatory tissues of living pines (and occasionally Larix), and in central and eastern Europe can become a serious pest. Some other aradids also may feed on tree fluids, but the frequency of such feeding, the number of species that so feed, and the phylogenetic significance of such feeding are all unexplored.
ENVOI
Heteroptera not only comprises the most species of any hemime-tabolous group (except perhaps the paraphyletic “Homoptera”) but contains the most biological, structural, and ecological diversity. It is a measure of this diversity, this evolutionary versatility, that so many ecological niches are filled by bugs. From the Alaskan cold to the webs of embiids to the bottoms of streams and the surface of the sea, and to the beds of people, heteropterans live where few other insect groups (and no other hemimetabolans) occur. Moreover, a vast number of heteropterans remain to be described, many from unusual habitats (tree canopies, leaf litter); and the biologies of most het-eropterans remain to be worked out. The diversity we see, although great, is less than the diversity to be discovered. Why this group of insects should be so diverse cannot be answered here. But that it is so diverse explains the group’s great and continuing fascination.
