Isoptera

(Termites)

Class Insecta

Order Isoptera

Number of families 7

Evolution and systematics

Termites make up the order Isoptera, comprising approximately 2,800 described species. The number of described species is thought to be no more than one-fourth to one-half the actual number, but this depends in part on the species concept applied. Some newer phylogenetic species concepts recognize every diagnosable geographically distinct population as a species, whereas the traditional biological species concept includes many geographic forms as subspecies within a smaller number of described species. Irrespective of theoretical issues of species limits, it is widely recognized that certain portions of the termite fauna, such as the New World soldierless termites, have been neglected by systematists, and many parts of the world remain to be thoroughly explored in terms of their termite biodiversity.

Termites are among the most primitive of the terrestrial Neoptera, which also includes the Blattodea (cockroaches) and Mantodea (mantids). These are the most basal of extant orders of winged insects to lay eggs on land, rather than in the water, and all share a similar adaptation for protection of the eggs from desiccation, laying the eggs as a mass encased in a protective secretion called an ootheca. Because of this shared character, these orders comprise a group formerly called the Oothecaria, but now more commonly known as the Dictyoptera.

Recent phylogenetic studies have suggested that the mantids were the earliest offshoot of the Dictyoptera, leaving the cockroaches and termites as sister groups. The most primitive family of the cockroaches, the Cryptocercidae, are the cockroaches most like termites: they eat wood, live in tunnel systems inside logs, have symbiotic flagellates in their hindgut, and live in small subsocial family groups in which the parents share their burrows with one brood of offspring they feed with proctodeal fluids. Likewise, termites in the most primitive family, the Mastotermitidae, are the termites most like cockroaches. Mastotermitidae is represented by only one living species, Mastotermes darwiniensis, the only termite that still lays eggs in an ootheca. It is also the only

termite that has five-segmented tarsi and an anal lobe in the hind wing, characters it shares with cockroaches.

Because of these similarities, it could be argued that termites are actually social cockroaches. However, termites lack the many distinctive features of cockroaches, a wide flattened body with the pronotum expanded over the head as a shield, shortened and thickened anterior wings that barely project beyond the tip of the abdomen, and very spiny legs, and therefore termites seem morphologically simpler and more primitive than cockroaches. The split in their lineages must have occurred very early, so that all extant members of each group form monophyletic clades of equal ordinal rank. Termites are more like stoneflies in that they retain a more primitive cylindrical body form and elongate flying wings. Cockroaches developed a more robust body form suited for a free-living, detrivorous lifestyle; termites pursued a life of tunneling inside wood or soil substrates and developed a more advanced level of family integration. Most systematists prefer to regard cockroaches as having split very early from a common protorthopteroid ancestor, which possessed a mix of characters predefinitive of either order. Hence, cockroaches are not asocial termites, and neither are termites social cockroaches.

The traditional hypothesis of termite origin is that they descended from a common ancestor of the primitive cockroach family Cryptocercidae, which is comprised of the single living genus Cryptocercus, of Holarctic distribution. Cryptotcercids digest wood and live in tunnel systems inside rotten logs. They also display a primitive subsociality in which a reproductive pair of adults share a tunnel system, usually with a single brood of up to about 20 offspring. The mandibles and intestines of cryptocercids are also very similar to those of primitive rottenwood termites in the family Termopsidae. A further similarity is that several genera of symbiotic protozoa are common to the hindguts of these Cryptocercids and primitive termites. However, some studies suggested that Cryptocercids may not be basal within the phylogeny of the cockroach order Blattaria, and therefore, if termites have a shared ancestry with Cryptocercidae, then the termite order Isoptera is cladistically encompassed within the Blattodea, rather than a sister group of the cockroaches. Consequently, termites must be considered a type of derivative social cockroach. The conventional view, reflected by current taxonomy, is that the three orders branched from common ancestors now long extinct, and form distinct and valid independent clades of equal ordinal rank.

The oothecarian orders belong to a larger assemblage called the Orthopteroid insects, which all undergo gradual metamorphosis and possess chewing mouthparts and include the orders Orthoptera (grasshoppers and crickets), Grylloblatta rockcrawlers), Phasmida (walking sticks), Dermaptera (earwigs), Embioptera (webspinners), Zoraptera (zorapterans), and Psocoptera (psocids).

Physical characteristics

Termites have gradual metamorphosis and branching developmental pathways leading to three or more different terminal castes, hence are polymorphic. In all other insects with gradual metamorphosis, the hatchling's mouthparts harden so that they are able to feed themselves. However, in termites, the eggs hatch to a form called a "larvae," or "white larvae," so called because their mandibles do not harden and darken, thus remaining white. The white larvae are kept together near the eggs in specific areas called nurseries. They are incapable of feeding on wood and are fed by the workers, both on stomodeal regurgitant and the proctodeal liquid which contains the protozoan fauna needed to establish their own stomach colony of digestive symbionts. The larval stage usually lasts for two instars.

The white larvae are a developmental character state that distinguishes the life cycle of all termites from that of all other insects. In most other insects with gradual metamorphosis, the larvae are independent after hatching. By laying small eggs that do not have enough yolk to hatch as independently functional individuals, the queen economizes. The white larvae hatch prematurely, essentially in an embryonic state. The advantage of this for the termite colony is that the queen's investment of yolk per egg is minimized, thereby making it possible for her to maximize the number of eggs she produces. The burden of feeding these tiny white larvae falls to the workers, thus relieving the queen of the physiological cost in yolk investment per offspring. The delegation of care to the workers also helps to promote the queen's fecundity and the colony's fitness. The care of the queen by her offspring, and the care of younger offspring by their older siblings, are hallmarks of termite sociality. While parental care characterizes subsociality, this filial and sibling care, along with the physical expression of these relationships in a polymorphic caste system, underlies eusociality.

In the second developmental instar, young termites face a decisive developmental juncture, at which they are determined either as neuters or as nymphs. Which form they become is visibly expressed in their body form by the third instar. Neuters have a slightly larger head than nymphs, and nymphs have tiny wing buds on the corners of their thoracic segments. Also by the third instar, their mandibles harden and they start to feed themselves, thus acquiring the characteristic abdominal color of their food, which is visible through the semi-transparent abdominal cuticle. In the course of several more molts, neuters become either workers or soldiers and spend the rest of their lives in their home nest. Nymphs, in contrast, grow longer wing pads and accumulate fat with each molt. In their final molt, they grow wings, develop large eyes, and become sexually mature. They then fly from the nest to establish new colonies.

Among soil-inhabiting termites, which all have a true worker caste, the neuter/nymph juncture is irrevocable. The factors influencing this developmental switch between neuters and nymphs appear to be seasonal cues and nutritional factors that influence hormones, and may be mediated by feedback pheromones. In the worker line, they may undergo several more molts before attaining their mature worker size. Male and female workers may all be the same size, or either males or females may be larger, thus forming major and minor workers of different sexes. In addition, workers of certain stages are able to molt via a presoldier stage to a final soldier stage. Soldiers are usually all of one size, but there may be two or three soldier subcastes. Soldier differentiation results from an increase in juvenile hormone released from small paired glands behind the brain, the corpora allata. Soldiers produce an inhibitory pheromone that regulates the worker to soldier ratio.

Instead of developing in the direction of neuter workers and soldiers, larva can develop in the direction of nymphs. In the first several instars, nymphs look about the same as small workers, the only differences are that their heads are slightly smaller and their thoracic segments are pointed at the posterior corners, exhibiting rudimentary wing-bud development. The wingbuds grow larger with each instar, so that by the last instar, large wing pads lay flat over the thorax. Nymphs do not develop until colonies are about five years old, and from that time a cohort of nymphs will develop annually. Nymphs lead relatively pampered lives compared to workers. They rarely, if ever, engage in the tunneling, building, and feeding behaviors that occupy the ever-busy workers. They may circulate in the population with workers, but do not generally participate in work. They feed themselves and also receive food from workers. As their wing pads lengthen, their bodies gradually change color to a milky white, reflecting the tremendous deposition of fatty tissue in their bodies. Their thorax and abdomen grow longer than those of workers.

Distribution

Termites are predominantly tropical and subtropical insects. Their diversity falls off sharply in temperate regions, and they are absent altogether in boreal and arctic regions. They tend to be most conspicuous in savannas (tropical grasslands), where their mounds often predominate in the landscape. They are more diverse on continents than on islands, and their diversity usually diminishes the more distant the islands are from continents. They are frequently quite diverse in deserts, but in this habitat do not build conspicuous aboveground epigeal nests or mounds.

Habitat

Termites have been called "dwellers in darkness," a reference to their cryptic lifestyle; they always stay inside substrates (either wood or soil), or tunnels, shelter tubes, and nests they construct from soil, feces, and saliva. Even when they forage, they usually do so through tunnels in the soil or under the cover of mud shelter tubes they construct. Other wood-boring insects are generally free living as adults. Indeed, this lifestyle is one of the many important and unique features of termite biology and ecology. This lifestyle partially accounts for the reason why so many people are unfamiliar with termites, and also for why they are so feared as pests.

Only a few termite species have evolved the ability to venture into the open to forage. The only such termites in North America are the narrow-nosed nasute termites of the genus Tenuirostritermes. In this genus, the workers and soldiers are dark bodied, a defense against ultraviolet radiation that they share with other free-foraging species. The only other time termites emerge from the hidden confines of their galleries, tunnels, and foraging tubes, is when they stage their brief annual alate flights.

Most primitive termites are xylophagous, that is they feed on dead wood. However, more advanced termites forage on a much wider array of foods, including fine woody debris, plant litter, leaf litter, dead grass, organic layers of soil, humus, highly decomposed wood, live wood, live herbaceous plants and grass, dung, fungi, fungus gardens, and lichens. Most termites are adapted for hot, warm, and humid climates, and therefore tend to be most abundant at low elevations and in coastal regions.

Behavior

All termites are eusocial. They have a caste system with soldiers, primary reproductives, secondary reproductives, and workerlike pseudergates or true workers, and live in cooperative colonies with long-lived queens and kings. In fact, termites are the only order that is entirely eusocial. The other major cluster of eusocial insects is found in the order Hymenoptera in the suborder Apocita, which includes the stinging wasps, ants, and bees. Within this group of stinging wasps, adult female societies have evolved a dozen or more times.

Two families of termites are socially more primitive than the others, possessing pseudergates or false workers instead of true workers, and may be designated as "pro-social." These are the rotten wood termites (family Termopsidae) and the dampwood and drywood termites (family Kalotermitidae). In these families, instead of an early developmental bifurcation between neuter and nymphal developmental lines, all individuals follow the nymphal line of development. To prevent too many offspring from maturing and leaving the colony as alates, the king and queen physically manipulate some of them by nibbling on the wing pads or hind legs. These minor physical injuries trigger regressive molts, causing such individuals to regress their wing pads and thus delay development for at least one season. In this condition, they are known as pseudergates. They effectively serve as workers, although this developmental condition is not permanent and they can later resume nymphal development and eventually become alates. Because colonies of pro-eusocial termites are confined to individual items of wood, their populations often number only a few thousand individuals, rarely exceeding 10,000.

The next level of sociality exhibited by termites may be termed meso-eusocial. In these termites (most species in the families Mastotermitidae, Rhinotermitidae, and Serritermitidae), a true worker caste is present. In addition, because such termites always have subterranean habits, they can access a larger base of food resources and attain much larger populations. Populations in mature colonies may number from tens of thousands to millions. However, their nest remains a primitive and poorly defined collection of galleries and cells inside a log, stump, or tree trunk. Such meso-eusocial species have frequently evolved a franchising approach to resource acquisition, in which neotenic supplementary reproductives are generated to occupy any suitable new nesting resource, and colonies spread by a creeping process of colony budding.

Because pro-eusocial termites live inside their food source (dead wood), they have no need to recruit, or lay a pheromone trail, to some distant food source. The only recruitment that occurs is that of workers and soldiers to the breach points, so that when galleries break open they are quickly defended by soldiers and repaired by workers. The sternal gland pheromone used for this "breach recruitment" in pro-eusocial termites is hexanoic acid. In contrast, meso-eusocial termites must travel through soil tunnels to find and link their diverse foraging resources, and the sternal glands have evolved a different pheromone, dodecatrienol, for this new function.

In the pro-eusocial termites, the developmental dichotomy between pseudergates and nymphs occurs late, following wing pad injury, and the differentiation in terms of size and fat body accumulation is negligible. Both pseudergates and nymphs feed for themselves and accumulate fat reserves at about the same rate, and all retain approximately an equal chance of future reproduction. With the transition to meso-eusociality and the early, developmentally controlled bifurcation of neuter and nymphal lines, a true worker caste is defined. Coincident with this is a distinctive differentiation of the workers and nymphs. True workers develop slightly enlarged heads, mainly to house their enlarged mandibular muscles. They also develop enlarged salivary glands to meet the increased demand placed on them for feeding the dependent nymphs.

Nymphs of meso-eusocial termites also undergo a new and distinctive differentiation, which mainly involves a pronounced tendency to accumulate fat and for the abdomen and thorax to grow longer to accommodate these new reserves. Nymphs now become truly nutritional "bank accounts" for the colony. The worker-nymph dichotomy at the pro-eusocial stage is merely one of wing pads, but at the meso-eusocial stage is accentuated by a dramatic differential social/nutritional investment. This is profoundly important, for now the entire termite colony population has split along somatic/generative lines. At the pro-eusocial stage, the vast majority of the population, all but the soldiers, continue to express their development and behavior in a manner which leaves open the possibility of alate differentiation and personal reproduction ( direct fitness). But at the meso-eusocial stage, a large portion of the population, the workers, now pursue a course of development that forecloses the possibility of alate development. At the same time, they express altruistic feeding behaviors toward siblings, thus sacrificing their own reproductive potential to promote the future reproductive potential of their larval siblings. Workers therefore engage in a strategy in which indirect fitness benefits (proxy reproduction by close kin) exceed personal reproduction efforts. Meso-sociality is seen in most species in the families Mastotermitidae, Rhinotermitidae, and Serritermitidae.

The next stage in termite social evolution, meta-eusociality, is characterized by the construction of an organized nest. Two families of termites, the Hodotermitidae and the Termitidae, have achieved meta-eusociality. The nest is usually in the soil and separate from any feeding source. It may be entirely below the surface (hypogeal), or on and above the surface (epigeal). In desert environments, hypogeal nests are often found below large surface rocks (sublithic). Nests may also be attached to the trunks or limbs of trees (arboreal). In wood- or cellulose-feeding species, nests are generally composed of a hardened, pulpy, fecal plaster material called carton, which varies in color from light tan to dark brown. In humus and soil-feeding species, nests are made of a darker "stercoral" fecal material, presumably high in lignins and polyphenols. Other nests are essentially excavations of tiers of galleries in the soil, containing chambers lined with fecal plastering.

With the development of an organized nest, the social life of the colony is transformed. Workers and soldiers must evolve a division of functions between nest tasks and foraging tasks. In all cases, the younger stages are occupied with in-nest tasks, and the older workers and soldiers assume the more perilous tasks associated with foraging at greater distances from the nest. With this age-related polytheism, there is often a division of workers into sex-based size subcastes. In most cases, males become the smaller, minor workers, and females the larger, major workers, but these roles are reversed in the Macrotermitidae. While both sexes may become workers, the soldier caste frequently becomes restricted to one or the other sex, and may become dior trimorphic. Such nests have a distinctive growth pattern of their own, starting as a single chamber (the nuptial cell, or copularium), and growing by the addition and/or reorganization of more cells and diverse tunnels and tiers over time.

The population size of mature nest-building termites is sometimes quite modest and tends to overlap, rather than exceed, the population ranges of meso-eusocial termites. There can be as few as several thousand up to a few million termites, mainly reflecting ecosystem differences in the resource productivity that can be harvested by a population with a central nest. Some meta-eusocial species have evolved interconnected multiple-nest systems (polycalism). These systems are analogous to those of meso-eusocial termites whose colonies spread by budding, and allow meta-eusocial species to achieve populations of several millions.

The final stage in termite social evolution is ultra-eusociality. Ultra-eusocial termites usually have multiple worker and soldier subcastes and very large nests called mounds. Mound-builders occur in at least one species of Coptotermes, Coptotermes acinaciformis of Australia; the fungus-growing Macrotermitinae in the genera Odontotermes and Macrotermes of Africa and Asia; in the Nasutitermitinae in the genera Syntermes and Cornitermes of South America; some Nasutitermes, including the cathedral-mound building termite (Nasutitermes triodiae) of northern Australia; some Amitermitinae, such as Amitermes laurensis, A. meridionalis, and A. vitosus, of northern Australia; and in Amitermes medius of Panama.

Mounds differ from nests not only in size, but also in having a massive outer wall of soil, usually clay. Because the mounds are so large and conspicuous, the termites must invest much more in fortifying them for defense. Sometimes the larger size also involves the addition of ventilation shafts

and chimneys. In addition, mound builders often store large quantities of food in peripheral storage pits or in storage chambers in the mound itself. Mounds are always long-lived structures, lasting for many decades, if not for centuries. Female reproductives of mound-building termites attain a prodigious size, due to the expansion of their abdomens. They attain a length of 2–4 in (5–10 cm), and have an egg-laying rate and duration exceeding that of all other animals. The larger nests of some arboreal nasutes, such as Nasutitermes rippertii of the Bahamas, could qualify those species as ultra-eusocial. But even relaxing the definition, only a handful of species on each continent and probably no more than 50 to 100 in total can qualify as ultra-eusocial.

The ultra-eusocial grade reflects not only group-level selection leading to an adaptive demography of the population and an efficient subdivision of behavioral tasks among castes, but a quantum advance in the level of internal homeostasis. Ultra-eusocial termites distinctively exceed the most advanced hymenopteran societies, the honeybees and leafcutter ants, in population size and nest scale. Their mound populations typically number into the millions, and their biomass is substantial

due to their larger bodies. But beyond these aspects of scale and biomass, such societies have a permanence and impact on the ecosystems that is exceptional. In the terrestrial landscape, only the relatively recently evolved human civilizations rival the majestic organizational complexity and domineering ecological impact of the ultra-eusocial termites.

Feeding ecology and diet

Termites are detritivores, in other words, they eat dead plant material. Dead plant material contains very little cytoplasm for two reasons: first, because much of the biomass of a plant consists of hollow, water transporting, vascular cells; and second, because when plants or plant parts die slowly, the plant retranslocates its cytoplasmic nutrient reserves to living tissue. Thus, dead wood and withered leaves and grass are mostly composed of plant cell-wall material, which is primarily made up of two types of plant carbohydrate polymers, cellulose and lignin. Plant detritus, therefore, whether large, coarse, and woody or small twigs, leaves, and plant debris, is mainly lignocellulosic matter. This dead plant biomass is high in caloric value, but low in nutritive value.

Lignocellulosic matter is the most abundant material produced annually in the biosphere by photosynthesis. Fungi are the main organisms that consume it, and they are able to do so because their threadlike hyphae have appropriate enzymes, and because the microscopic threads that make up wood-rotting fungi are extremely economical in their nutrient requirements. Vertebrate animals in general cannot derive sufficient nutriment from lignocellulosic matter, and hence almost none, except ruminant ungulates (hoofed animals with complex stomachs such as cows), utilize this abundant matter as food. However, a few groups of insects have evolved as successful detritivores, in all cases by coevolving symbiotic relationships with microbial organisms such as bacteria, protozoa, or fungi (these more primitive organisms have very diverse and useful metabolic machinery).

The main groups of insect detritivores are cockroaches, termites, crickets, flies, and beetles. Termites are the only insect detritivores that are social, leading to a higher level of coordinated foraging and increased foraging reach, and therefore to an extraordinary level of lignocellulosic processing power. Termites also comprise an entire insect order of considerable antiquity (dating perhaps to the late Paleozoic or early Mesozoic periods), and thus their symbioses are coevolved to a high level of integration and efficiency. Furthermore, they have ecologically radiated so that specialist genera exist for virtually every type of plant detritus, wood, humus, and dung, in every stage of decay, in virtually every type of temperate, subtropical, and tropical habitat.

In termites, three main patterns of endosymbiotic relationships may be outlined. First, all lower termite families have a complex paunch community including flagellate protozoa; second, the fungus-growing Macrotermitinae have lost the flagellate protozoans and instead cultivate a basidiomycete fungus, Termitomyces, as fist-sized lumps called fungus combs; and third, the remaining higher termite subfamilies have also lost the flagellate protozoans (although some harbor amoebae or ciliates) and have instead various segments, chambers, and diverticula of the hindgut in which bacterial cultures are involved in various ways in digestive metabolism.

Among the lower termites harboring flagellate protozoan, three subpatterns may be outlined. First, in the family Mastotermitidae, small gastric ceca (presumably containing bacteria) are present in the anterior midgut and there are blattobacteria in fat body bacteriocytes. A hindgut community of flagellate protozoa, spirochetes, and bacteria is also present. Second, in the families Termopsidae and Hodotermitidae, the blattobacteria are lost, but gastric ceca are present as well as hindgut flagellates. Third, in the families Kalotermitidae, Rhinotermitidae, and Serritermitidae, both the blattobacteria and gastric ceca are lost, and digestion symbiosis is relegated entirely to the community of flagellates, spirochetes, and bacteria in the paunch.

In the Macrotermitinae, digestion is accomplished through an initial rapid pass of the food through the intestines of minor workers, after which it is deposited as "primary feces" on the fungus comb. It is then further degraded by the action of the cultivated fungus, which produces nutrient-enriched conidiophores. The conidiophores are eaten by the termites and fed to the dependent castes, while older workers feed on spent fungus comb. The intestine of termites in the Macrotermitinae does not contain symbionts, instead the midgut is substantially enlarged and the hindgut is short and simple.

The other subfamilies of the higher termites (excluding the Macrotermitinae) have evolved a completely modified hindgut with several new segments, chambers, and diverticula for housing new types of symbionts, mostly bacterial floras of various types. In one such modification, the junction of the midgut and hindgut is a unique intestinal innovation called the mixed segment. This region of the intestine posterior to the midgut is composed of a lobe of mesenteric tissue that forms an elongate diverticulum adjacent to the anterior-most section of the hindgut. The Malpighian tubules, which are involved in nitrogen excretion, form a network of convolutions over the mesenteric lobe of the mixed segment. The exact function of the mixed segment is a subject of much interest and conjecture. It seems likely that it has many functions, including roles in nitrogen excretion, osmotic regulation, and hindgut irrigation, as well as housing bacteria that may be involved in nitrogen recycling.

Another gut modification is the elongation and enlargement of the first chamber of the hindgut as a "secondary crop." Posterior to this is the enteric valve, which, in humivorous species, has evolved a complex armature involving spines, forks, and featherlike structures that projects into the succeeding bacterial pouch and rakes bacteria into the food bolus as it passes through the narrow valve. The bacterial pouch is the modified anterior-most portion of the paunch. In the Cubitermes group of genera from Africa, there is an additional bacterial diverticulum on the paunch. The anterior colon is made up of modified chambers which may bear internal cuticular processes, to which are attached various bacteria of unknown function. Thus, although the structural details vary considerably, in almost every case there are three or more distinct, sequential zones of the hindgut in which the food bolus is sequentially processed by different bacterial communities.

Reproductive biology

In general, termites may be characterized as monogamous. The timing of alate flights within a species is synchronized so that termites from different colonies can meet and form outbreeding pairs. After flight, the termites shed their wings, a process called dealation, and the newly dealated individuals seek a mate. The females in some species call by releasing a pheromone from their sternal or tergal glands. When the male finds the female, there usually ensues a brief chaotic zigzagging run, with the female leading and the male following in close tandem. This tandem run apparently constitutes their courtship. If a female fails to put on a good run, or if a male fails to keep pace, the suitor is rejected. This courtship evaluation must be made within minutes, because termites are extremely vulnerable to predation during this brief period of life outside the colony.

After courtship, pairs seek an appropriate place in the soil or in a crevice, crack, or hole in wood to serve as a copularium. Only after they are sealed inside, and therefore committed irrevocably to each other, do they mate. The copularium is the starting point for the growth of the termite family and the expansion of a new gallery system of the colony. Pairing, and then delaying mating until after the copularium is sealed, ensure lifelong monogamy and mate fidelity. In only a few species, and even then only rarely, do more than one male and female join in forming a copularium. In these species, polygamous associations may be adaptively advantageous in getting the growth rate of the colony off to a faster start. Although much attention has been paid to these exceptional cases of polygamy, they should not overshadow the fact that virtually all species in most cases form monogamous unions.

Monogamy is extremely important because it ensures that the growing population is comprised of full siblings. In a monogamous, outbred family, each offspring has exactly 50% of the genome of each parent, and shares with each sibling a 50% chance of having a particular gene in common. In other words, an exact equivalence of relatedness exists among all individuals in the colony. The importance of this is that colony-mates (siblings) are of equal genetic value as potential offspring. Therefore, if a termite has the opportunity, through a redirection of effort, to trade offspring production for sibling production, then it is an even tradeoff. The endo-substrate mode of life tends to enforce monogamous mating, and in consequence yields conditions of high intrafamilial relatedness that are conducive to a re-allocation of effort, away from risky potential offspring toward a secure investment in additional siblings.

Because of these conditions, immature termites in the early stages of social evolution may be thought of as willing helpers for their parents. They were able to trade direct reproduction for equally valuable indirect reproduction, simply by choosing to feed their parents and siblings, in other words, by evolving alloparenting. However, while pursuing this indirect strategy a further selfish reproductive benefit exists, the possibility of inheriting the parental nest when a pseudergate transforms into a neotenic replacement reproductive. That selfish interests still count is evident in the siblicidal battles that occur among replacement reproductives in lower, proeusocial termites. In the family Termopsidae, replacement reproductives soldiers may develop in orphaned colonies, and in this context their hypertrophied mandibles may be turned toward the nasty business of siblicidal neotenic combat, rather than the customary and more noble altruistic function of soldiers as colony defenders. The peculiar occurrence of reproductive soldiers among the ecologically most-primitive rottenwood termites has led to the suggestion that soldiers actually originated, not as colony defenders, but as a selfish adaptation, or "Cainism," an interesting parallel of the Biblical account in which one brother kills the other.

In pro-eusocial termites, the potential for neotenic transformation is present in workers, nymphs, and even presoldiers in some species. This provides great reproductive flexibility for individuals to express their own best situational strategy. In this respect, the pro-eusocial termites are exceedingly interesting, and far from being fully understood. In meso-eusocial termites, neotenic tendencies become more limited and are usually restricted to either the nymphal or worker line. In the Termitidae, where meta-eusociality is the rule, this individual reproductive flexibility is greatly restricted or completely lost. For example, termites in the subfamilies Macrotermitinae and Apicotermitinae do not have neotenics, and replacement reproduction is only possible by unflown alates. Thus, while individual reproductive strategies and a mixed portfolio of indirect and direct reproductive benefits were important in the early stages of termite social evolution, once critical social grades were reached, individual developmental options became rigidly channeled and the reproductive prerogative restricted. Eventually, this resulted in stronger domination by the primary reproductive pair, the king and queen, for whom the colony became merely a somatic extension, serving the reproductive output of their gonads.

Conservation status

No species of Isoptera is known to be threatened. Nevertheless, because of the extensive clearing of tropical forests for timber production and the conversion of much land to intensive agricultural production, it is likely that many termite species have been ecologically marginalized. Ancient termite-mound dominated landscapes are easily obliterated by bulldozers. Because so many insectivorous animals depend on termite populations for food, termite conservation is important and should be given greater attention.

Significance to humans

Termites have traditionally been regarded as pests. Even the ancients recognized termites as the original terminators and destroyers of man's wooden constructs. The name termite derives from the Latin root word "term -es, -in, -it," as in terminal: the end; and terminate: to bring to an end or destroy. Until the 1940s, the only defense against their depredations was good construction and vigilance. But with the advent of synthetic pesticides, an arsenal of poison was unleashed. To destroy drywood termites, chemical fumigants, including the ozone-depleting chemical methyl bromide, were used. For subterranean termites, chemicals such as pentachlorophenol and CCA have been used as wood preservatives, and lindane, aldrin, dieldrin, chlordane, and chlorpyrifos (most of which have now been banned) were used as soil termiticides. Despite some regulatory progress in removing the more hazardous and environmentally persistent synthetic pesticides, many equally toxic compounds remain on the market in both developed and developing countries.

However, there are hopeful signs of progress in termite pest management. These include heating, liquid nitrogen, microwaves, and electrical treatments for drywood termites; baiting and trap-treat-release systems for subterranean termites; and borates as wood preservatives. These newer control techniques offer the promise of effective control with greatly reduced hazard of human exposure and environmental contamination with synthetic pesticides. So far, even with these controls, urban pest termites appear to be holding their own, and even if completely eradicated from the urban environment, will likely persist in natural environments.

With so much emphasis on termite elimination, termite conservation has been given relatively little attention, even though numerous studies document that termite biodiversity is negatively impacted by intensive agriculture and forest clearing. In tropical areas, termites have been estimated to constitute up to 75% of total insect biomass and 10% of total animal biomass. No other taxon, except perhaps earthworms, represents such an major component of tropical ecosystems. Therefore, their conservation is vital to the operational integrity of ecosystems, including trophic relationships, soil microstructure and processes, and major flows of energy and nutrients in biogeochemical cycles. The danger is that, with effective baits, "control measures" might be implemented against termites as management tools in forestry, agriculture, or range management. This could be devastating, not only for termites, but for the ecosystems in which termites are keystone organisms.

Since termites are major converters of lignocellulosic matter to animal biomass, it would seem that they have potential for improving human utilization of lignocellulosic residues and wastes. Examples of such materials include scrap lumber and sawdust from saw mills; agricultural residues such as straw, bean pods, and sugar cane pulp; and animal dung from dairies and feed lots. Termites might be cultivated on such wastes and then harvested as feed for aquaculture or poultry production. The chemical energy in lignocellulosic wastes is usually dissipated to carbon dioxide by microbial degradation. By feeding such waste materials to termites, vast amounts of biochemical energy could be channeled into food production. Because termites have symbiosis with nitrogen fixing bacteria, they possess the rare metabolic machinery needed to convert plant cell wall matter into animal biomass. The substantial flow of plant biomass through termite intestines represents a significant pathway in the terrestrial carbon cycle that humankind has yet to productively tap into. Termites could be important organisms for humans to learn how to cultivate. The promise of large-scale termiticulture, however, will require much more research on termite physiology, nutrition, and respiration before many technical obstacles are overcome.

Species accounts

List of Species

West Indian powderpost drywood termite

Cryptotermes brevis

family

Kalotermitidae

taxonomy

Termes brevis Walker, 1853, Jamaica.

other common names

English: Furniture termite.

physical characteristics

Alates medium size, 0.4–0.5 in (10–12 mm) from head to tip of wings; median vein curving forward to meet anterior margin in outer one-third of wing; yellow brown. Soldiers have distinctive phragmotic (pluglike), deeply wrinkled head with high frontal flange; short mandibles.

distribution

The most widespread termite species. Regarded as a "tramp" species because easily spread in any item of wood furniture, in the wooden spars, masts, and planking of ships, in wooden pallets, and dunnage (packing material in ships). Native to the West Indies, widely distributed on wood sailing ships after discovery of New World. Now established in most oceanic archipelagos, including the Canary Islands, New Caledonia, the Hawaiian Islands, Bermuda, the Azores, Brazil, Australia, South Africa, and most of the Gulf Coast cities of the United States, especially peninsular Florida.

habitat

Usually found in urban areas in structural timbers of houses, in furniture, and in boats. Rarely occurs in natural settings, prefers drier wood found in human habitation. Also requires humid air and is usually only found in coastal and island localities.

behavior

Colonies typically small with only a few thousand individuals, but infested structures may have numerous colonies. Each colony occupies galleries extending a few meters in length. Fecal pellets distinctively shaped, short, six-sided cylinders. Infestation usually detected by piles of fecal pellets which termites dump out of galleries through small round "kick holes" quickly sealed with fecal plaster.

feeding ecology and diet

Xylophagous, survives in variety of woods, particularly sound hardwood and softwood timbers, needs very dry and sound wood.

reproductive biology

Colonies pro-eusocial, headed by primary reproductives or secondary neotenic replacement reproductives. Neotenic reproductives develop quickly when primaries are removed and engage in lethal fighting until single reproductive pair is

reestablished. In Florida, alates fly between dusk and dawn from April to June. After short dispersal flight, wings are broken off and pairs search for holes and crevices in which to form copularium. Mating does not occur until pair seal themselves in.

conservation status

Not threatened; expanding and prospering due to human activity.

significance to humans

Destructive pest of human-made wooden structures, particularly houses and historical buildings. Sometimes referred to as the furniture termite because of its unusual ability to form colonies in relatively small, moveable, wooden items and furnishings. Also known to attack books and archived documents.

Giant Sonoran drywood termite

Pterotermes occidentis

family

Kalotermitidae

taxonomy

Termes occidentis Walker, 1853, Baja California, Mexico.

other common names

None known.

physical characteristics

Large, alates 0.7–0.78 in (18–20 mm) from head to wing tips; antennae with 20 or 21 segments, reddish brown. Soldiers heavy bodied, 0.5–0.6 in (14–15 mm); toothed mandibles, round heads with black compound eyes, broad pronotum, thorax with wing pads, brilliant orange and yellow. Pseudergates large with large compound eyes.

distribution

Sonoran Desert, including Baja California and Sonora, Mexico, and southwestern Arizona, United States.

habitat

Dead standing branches of paloverde trees of the genus Cercidium.

behavior

Colonies pro-eusocial, rarely exceed 3,000 individuals; most mature colonies have standing population of 1,000 to 1,500. All individuals develop as nymphs. About 5% of nymphs have wing pad scars resulting in development as pseuder-gates, comprising about 10 to 15% of population. Pseuder-gates may molt to presoldiers and then to soldiers. Soldiers comprise about 2% of population, guard breaches of the galleries. Nymphs molt to alates in July, small numbers fly from nest at night over flight season from late July through September. Dispersal flights last at least four minutes but not more than one hour. Alates seek beetle emergence holes on dead paloverde trees, which male and female pairs enter and seal off copularium. Primary reproductives always bite off the distal halves of their antenna for reasons that remain unknown.

feeding ecology and diet

Xylophagous; colonies excavate wide, meandering galleries inside dead paloverde branches. Occasionally found in saguaro cactus skeletons.

reproductive biology

Most colonies headed by pair of primary reproductives. However, if one or both are removed, pseudergates start to molt within weeks to become replacement reproductives. When excess numbers molt following death of primaries, lethal fighting follows among neotenic replacements until one male and one female reproductive again become established and suppress, presumably by inhibitory pheromones, further neotenic molting.

conservation status

Not threatened. Critical habitat (dead standing branches of paloverde trees) not utilized by humans except sometimes as firewood. However, as the species is monophagous on one tree species and standing branches on tree are limited, could be subject to local extirpation if intensively collected near urban areas.

significance to humans

Excellent study organism because of large size and ease of maintenance; one of the most well-studied North American drywood termites. Not a pest; no known economic value.

Giant Australian termite

Mastotermes darwiniensis

family

Mastotermitidae

taxonomy

Mastotermes darwiniensis Froggatt, 1896, Port Darwin, West Australia.

other common names

None known.

physical characteristics

Large: alates up to 1.4 in (35 mm) with wings, 2 in (50 mm) wingspan; soldiers 0.45–0.5 in (11.5–13 mm); workers 0.4 in–0.45 in (10–11.5 mm). Only termite whose winged alates possess anal lobe in hind wing; tarsi have five segments, females have short blattoidlike ovipositor with ventral valves, long enough to overlap the dorsal valves; eggs laid in ootheca. Soldiers have round reddish heads with relatively stout short mandibles, long apical teeth; right mandible has two well-defined marginal teeth, but in left mandible only first marginal tooth is well defined, second and third are indistinct. Soldiers and workers have unique coxal armature, or flange, on front legs, and rows of small opposable teeth on femora and tibia, unique leg characters in this family.

distribution

Once cosmopolitan (as indicated by fossils), now confined to tropical northern Australia and nearby islands.

habitat

Xylophagous and subterranean, feeds on logs, dead standing trees, and surface wood. Also known to girdle live trees, including commercial tree plantings, then feed on killed trees.

behavior

Meso-eusocial. Little is known aside from feeding ecology and reproductive biology.

feeding ecology and diet

Independently evolved subterranean foraging habits and ability to build mud shelter tubes to access wood above ground level. Simple nest chambers of several tiers of thin-walled carton cells usually in bole of tree or stump, near or below ground level. Colonies may exceed 1 million individuals and forage over 328 ft (100 m).

reproductive biology

Workers frequently transform into ergatoid reproductives that replace primary reproductives when colonies are orphaned, but more typically develop as supplementary reproductives and form new colonies by budding off from parent colonies. Most reproduction probably by neotenic ergatoid reproductives.

conservation status

Not threatened.

significance to humans

Of phylogenetic interest because of status as a monotypic family, exhibits unique morphological characters that place it as most basal termite and possibly most basal extant species of Dictyopterid. Serious structural, forest, and agricultural pest; most destructive termite in tropical northern Australia; damaging timber in buildings, bridges, poles, fence posts, railway sleepers, living trees, and crops. Also feeds on many host tree species, including live trees, and attacks plantations and crops such as sugar cane. However, its large body, large colony size, and wide diet make it an excellent candidate for beneficial termiticulture on cellulosic wastes.

Eastern subterranean termite

Reticulitermes flavipes

family

Rhinotermitidae

taxonomy

Termes flavipes Kollar, 1837, Vienna, Austria (where it was introduced).

other common names

None known.

physical characteristics

Alates small, 0.4 in (10 mm) from head to wing tips; black except for yellow tibiae. Soldiers with elongate, parallel-sided, subrectangular, yellow heads, and stout, black, toothless mandibles, strongly curved inward at tips. Top of soldier head with minute opening of frontal gland, or fontanelle. Workers about 0.2 in (6 mm) long; creamy white.

distribution

Native to eastern forests of United States from Florida to Maine, and in the west from Texas to Minnesota; introduced into Canada in southern Ontario, including the Toronto area.

habitat

Deciduous hardwood forests.

behavior

Colonies are meso-eusocial and forage through shallow, narrow tunnels in soil that connect dead wood items, including stumps, logs, and roots. Also forages up trees on dead limbs and into rotten boles of trees with heart rot or butt rot. In urban environment, feeds on wood landscaping items such as fence posts, edging boards, firewood piles, wood-chip mulch, scrap lumber, and flower planter boxes. Once established in these items, explores foundation cracks and crevices and often finds access to structural wood framing, recruiting more workers and establishing numerous access points into the structure. Since feeding is from inside and most wood framing is concealed, may cause extensive damage over many years before being discovered.

feeding ecology and diet

Xylophagous, consumes hardwoods and softwoods, prefers sap-wood to heartwood. Preferentially feeds on more porous spring wood of annual rings, leaving harder summer wood, thus damaged wood may have laminated appearance. Consumes both sound wood and partially decayed wood. Galleries often have small parchmentlike partitions of fecal paste and light tan specks of fecal plastering. When working above ground, in structures, or when foraging up trees, builds protective shelter tubes of fine soil particles and saliva, lined with fecal plaster. Shelter tubes are the most conspicuous sign of presence and activity, as no fecal pellets are produced.

reproductive biology

No definitive nest, establishes reproductive chambers in logs, stumps, or other large moist wood items. Since structural wood is usually dry, reproduction rarely occurs in structural timbers. Moves deeper into ground in winter, staying beneath frost line, probably occupying roots of old stumps. Generates large number of nymphoid neotenics from nymphs, which serve as supplementary reproductives and allow seeding of all potential reproductive resources within foraging territory with reproductives; thus, colonies expand continuously as resources are colonized. Most reproduction is by supplementary reproductives. Older colonies have no central nest or foraging territory headed by single primary or replacement pair, but instead extensive, loosely connected gallery systems with an extended family structure. Foraging territories are discovered, exploited to exhaustion, then abandoned as new foraging areas are expanded. This foraging-reproductive strategy is appropriate and well adapted, matched to the pattern of wood production and dispersion in the temperate zone.

conservation status

Not threatened despite intensive control efforts.

significance to humans

Major subterranean termite pest in eastern North America. Responsible for hundreds of millions of dollars of damage and control annually; this damage and collateral expenses of inspection, control, and renovation make it one of the most destructive urban insect pests.

Black macrotermes

Macrotermes carbonarius

family

Termitidae

taxonomy

Termes carbonarius Hagen, 1858, Malay Peninsula.

other common names

None known.

physical characteristics

Very large (largest in Southeast Asia); alates about 1.2 in (30 mm) from head to wing tips, wing span at least 2 in (50 mm). As suggested by species name carbonarius, workers and soldiers very dark, nearly black, a feature often found in free-foraging termites exposed to sunlight. Workers dimorphic, males larger than females. Soldiers also dimorphic but all females; with fleshy lobe at end of labrum; subrectangular heads; razor sharp, saberlike mandibles.

distribution

Southeast Asia, including Thailand, Cambodia, Malaysia, and Borneo.

habitat

Occurs in flat lowlands, uncommon in hilly terrain. Found in plantations such as rubber, coconut, durian, and teak, especially common in coastal dipterocarp forests.

behavior

Colonies are ultra-eusocial. Builds large mounds up to 13 ft (4m) high and 16 ft (5 m) wide at base. Fungus combs usually in large chambers around periphery of mound. Minor workers specialized for nest work, including tending king and queen, feeding larvae and nymphs, and nest repair. Major workers mainly forage.

feeding ecology and diet

Gramivorous, eating mainly dead grass, twigs, and surface debris cut into short pieces. Only species of subfamily Macrotermitinae to forage above ground; usually at night. Foraging parties involve major and minor soldiers and major workers, but not minor workers. Foraging area changes daily. After opening foraging hole, major workers build pavement track-ways to foraging area. More workers then join, fanning out to collect dead grass and twigs; continuous cordon of major and minor soldiers guards outskirts of foraging area. Collected forage is carried below ground and passed to minor workers, who chew it and pass it rapidly through their digestive tract as "primary" feces, then deposit it on fungus comb upon which species of basidiomycete fungus (genus Termitomyces) grow.

reproductive biology

Colonies usually headed by royal pair in thick-walled royal cell. Queen's abdomen unfolds and expands to gross dimensions (physogastry). Subfamily cannot produce neotenic reproductives; when primary reproductives die, colony may also die unless alates are there as replacements.

conservation status

Not threatened.

significance to humans

Plantation pest. Alates sometimes harvested and eaten or used as chicken feed.

Black-headed nasute termite

Nasutitermes nigriceps

family

Termitidae

taxonomy

Termes nigriceps Haldeman, 1858, western Mexico.

other common names

English: Haldeman's black nasute

physical characteristics

Queen physogastric; rusty yellow except for costal margins of wing scales which are dark brown, 0.7 in (18.5 mm) without wings. Soldiers with very dark heads; nasus wide and dark reddish; dense erect setae over head capsule. Workers dimorphic, rectangular heads; darkly pigmented.

distribution

Widely distributed from western Mexico as far north as Mazatlan, south to Panama and northern South America.

habitat

Coastal plains from sea level to about 3,280 ft (1,000 m).

behavior

Colonies are meta-eusocial. Builds large conspicuous arboreal carton nests in trees, on fence posts and poles. May have more than one nest per colony.

feeding ecology and diet

Xylophagous; feeds mainly above ground via an extensive network of wide shelter tubes attached usually to the lower sides of tree branches.

reproductive biology

Colonies headed by primary reproductives.

conservation status

Not threatened.

significance to humans

Occasional structural pest.

Linnaeus's snapping termite

Termes fatalis

family

Termitidae

taxonomy

Termes fatalis Linnaeus, 1758, Para-Maribo, Suriname.

other common names

None known.

physical characteristics

Small, alate about 0.3 in (8.5 mm) with wings; brown, with large apical teeth. Soldiers monomorphic, with pale yellow, elongate, parallel-sided heads with hornlike tubercle projecting forward. Mandibles slender, elongate and rodlike; apices cupped together. Soldier labrum is narrow and rectangular with short points on anterior corners.

distribution

Northeastern South America, in Guyana, Suriname, Trinidad, and Amazonia, Brazil.

habitat

Rainforest.

behavior

Colonies are meta-eusocial. Soldiers capable of violently snapping their mandibles, forcing them to cross downward, pushing the pointed head upward into ceiling of tunnel or nest chamber opening. Presumed function of snapping behavior is to lock soldiers' head into tunnel to block the advance of predators such as ants or other termites. Species of the subfamily Termitinae often build short, turretlike nests of hard dark fecal material. Nests composed of numerous interconnected cells. Little known about nesting behavior, but some species in the subfamily build nests inside mounds and nests of other termites.

feeding ecology and diet

Humivorous. Large apical teeth and molar without grinding ridges suggest diet of very soft decayed wood or humus.

reproductive biology

Nothing known.

conservation status

Nothing known.

significance to humans

First species of termite formally named by Linnaeus in 1758, thus has taxonomic significance as ordinal type.

Wide-headed rottenwood termite

Zootermopsis laticeps

family

Termopsidae

taxonomy

Termopsis laticeps Banks, 1906, Florence and Douglas, Arizona, United States.

other common names

None known.

physical characteristics

Largest and most primitive North American termite. Winged alates 1–1.2 in (26–30 mm) from head to wing tips with wing span 1.8–1.9 in (46–48 mm); antennae with 26 segments; cerci with 5 segments; tarsi with 5 segments; reniform compound eyes, simple eyes or ocelli absent; body dark yellowish. Soldiers up to 0.6–0.9 in (16–23 mm) long with spectacularly long and jaggedly toothed mandibles; flattened heads; widest posteriorly; pronotum with anterior corners pointed; large spines on tibiae. Pseuder-gates develop from nymphs after wing-pad abscission or wing-pad biting. Pseudergates develop different pattern of hair over body and may molt several times, enlarging in size each time and developing large, wide head. Functionally reproductive replacement soldiers sometimes develop in orphaned colonies.

distribution

Central and southeastern Arizona to southern New Mexico, West Texas, United States, and Chihuahua and Sonora, Mexico; within altitudinal range 1,500–5,500 ft (457–1,676 m) above sea level.

habitat

Occurs in canyons and river valleys in rotten cores of boles and large branches of living riparian trees such as willow, cottonwood, sycamore, oak, alder, ash, walnut, hackberry, and other hardwoods. Not recorded from conifers or dead, rotten logs. In the relatively arid region it inhabits, only live trees can provide the moist conditions it requires.

behavior

Colonies are pro-eusocial. Gallery excavations extend several feet (meters) with concentric, wandering, open chambers in rotten wood. Excavated central area becomes filled with caked mass of fecal pellets. Galleries typically originate from knot hole plugged with a mass of hard fecal pellets; galleries often damp or wet inside. Soldiers agile, defend openings against ants or other predatory intruders.

feeding ecology and diet

Mycetoxylophagous, feeding only on rotten hardwoods. Feeding probably helps advance development of heart rot in infested trees.

reproductive biology

Alates fly in middle of night from late June through early August. Colonies initiated by alate pairs in tree scars, knot holes, or small rot pockets where tree previously damaged by wind or beetles. Most field colonies headed by primary reproductive pairs, but replacement reproductives may develop from pseudergates or nymphs. Functional reproductive soldiers with heads smaller than typical soldiers have also been found as replacement reproductives in field colonies. Colonies rarely exceed 1,000 individuals.

conservation status

Not threatened, but could be affected by agricultural or urban development in riparian habitats.

significance to humans

Attacks live trees and extends rot from dead to live portions of trees, hastening collapse or breakage of trees. However, most attacked tree species are not of economic importance, so not considered a pest. Could be pest in mature orchard crops such as pecan and pistachio, but this has not been reported. Could be used for physiological studies of termites because of large size, but collecting colonies difficult, requiring bucksaws or chainsaws, wedges, and sledgehammers.

Resources

Books

Abe, T., D. E. Bignell and M. Higashi, eds. Termites: Evolution, Sociality, Symbiosis, Ecology. Dordrecht, The Netherlands: Kluwer Academic, 2000.

Choe, J. C., and B. J. Crespi, eds. The Evolution of Social Behavior in Insects and Arachnids. Cambridge, U.K.: Cambridge University Press, 1997.

Grassé, P.-P. Termitologia, 3 vols. Paris: Masson, 1982–1986.

Kofoid, C. A., et al., eds. Termites and Termite Control. Berkeley: University of California Press, 1934.

Krishna, K., and F. M. Weesner, eds. Biology of Termites, 2 vols. New York: Academic Press, 1969–1970.

Myles, T. G. "Resource Inheritance in Social Evolution from Termites to Man." In The Ecology of Social Behavior, edited by C. N. Slobodchikoff. New York: Academic Press, 1988.

Sands, W. A. The Identification of Worker Castes of Termite Genera from Soils of Africa and the Middle East. London: CAB International, 1988.

Uys, V. A Guide to the Termite Genera of Southern Africa. Plant Protection Research Handbook No. 15. Pretoria, South Africa: Agricultural Research Council, 2002.

Wilson, E. O. The Insect Societies. Cambridge: Belknap Press of Harvard University Press, 1971.

——. Sociobiology: The Abridged Edition. Cambridge: Belknap Press of Harvard University Press, 1980.

Periodicals

Myles, T. G. "Evidence of Parental and/or Sibling Manipulation in Three Species of Termites in Hawaii." Proceedings of the Hawaiian Entomological Society 27 (1986): 129–136.

——. "Reproductive Soldiers in the Termopsidae (Isoptera)." Pan-Pacific Entomologist 62, no. 4 (1986): 293–299.

——. "Review of Secondary Reproduction in Termites (Insecta: Isoptera) with Comments on Its Role in Termite Ecology and Social Evolution." Sociobiology 33 (1999): 1–91.

——. "Termite Eusocial Evolution: A Re-Examination of Bartz's Hypothesis and Assumptions." The Quarterly Review of Biology 63 (1988): 1–23.

Timothy George Myles, PhD