Kings And Queens Of The Underworld

Kings and queens, the most commonly known forms of reproductive termites, produce highly complex underground societies.

Termites are among the most captivating of all insects because of their fascinating societies. Humans choose to build structures out of termite food, and we have a hard time viewing them as anything but disturbing pests when they dine on those structures. But beyond their diet and its interference with our own society, the intrigue of a termite society is remarkable. Understanding the organization and reproductive biology of termite colonies will give pest control professionals insights into control strategies and realities.

PRIMARY REPRODUCTIVES. The best known types of termite reproductives are the king and queen. These are the original founders of a colony, and were once winged swarmers, or alates. After flight from their natal colony, successful alates find a mate, drop their wings, and walk in tandem to locate a suitable nest site. The main portion of the wings break off along a line of weakness called a suture, but the upper articulation and base of the wing remain on the thorax of the insect. Presence of these wing stubs, or bracts, are diagnostic of a true king or queen, also known as primary or first form termite reproductives.

One of the major differences between a termite society and colonies of ants or social bees or wasps is that termites mate after they are cloistered within their nuptial chamber, and termite queens do not store a lifetime supply of sperm. Reproductive male ants, bees, and wasps die shortly after mating, but king termites remain as consorts to their queen. In species in which reproductive behavior has been studied, the king works as an egalitarian "Mr. Mom" in helping to rear early broods of offspring.

Although true kings and queens are the most commonly known types of termite reproductives, and are featured prominently in textbook accounts of termite colony organization, they are found rarely in field colonies of Reticulitermes, the prominent genus of subterranean termites in the United States. There are amusing accounts from the early 1900s recording the delight of entomologists who finally document a "true queen" of Reticulitermes. The scarcity of sightings may be due in part to the challenge of finding a royal "needle in a haystack" of seething termites as they scurry amidst disturbed chambers of rigid wood, but experienced PCOs and termite biologists will attest to the extreme rarity of finding a primary Reticulitermes queen in nature.

While alate-derived queens are an exceptional find in the field, other types of reproductive termites are found frequently in Reticulitermes colonies. As with many types of termites, the developmental pathways of Reticulitermes individuals are rather flexible, and under the right social circumstances, termites that are progressing towards becoming alates can differentiate into functional reproductives. In some cases even worker termites become reproductives within their colony.

OTHER REPRODUCTIVES. The most common of the alternate types of Reticulitermes reproductives are brachypterous neotenic or second form reproductives. Depending on the species and the circumstance, brachypterous neotenic reproductives differentiate in as little as six to eight weeks in Reticulitermes groups that are isolated from their king and queen. These reproductives develop from pre-alate nymphs within the nest, and have small wing buds (visible under a microscope) on the last two thoracic segments.

Brachypterous neotenic reproductives never disperse from their own colonymates, although they may travel within the colony's gallery network to move to a new location. Large numbers of fertile brachypterous neotenic reproductives from several hundred up to more than a thousand may be found within a single log, often clustered together in the same area and always with a sex ratio skewed heavily toward females.

The third type of Reticulitermes reproductives differentiate from secluded groups of workers, but generally only after months of isolation from other reproductives. These third form or apterous neo tenic reproductives have no wing buds. Like the brachypterous neotenic reproductives, a large number of them differentiate within a colony. Apterous neotenics are found much less frequently than brachypterous neotenic reproductives, and the two forms are not found together.

The circumstances and dynamics that induce differentiation of brachypterous versus apterous neotenic reproductives are not known. Developmental options likely depend on the age distribution and developmental status of the group at the time of death or separation from the primary reproductive(s).

All types of termite reproductives have compound eyes. These are well developed in primary reproductives, rudimentary in apterous neotenics, and of intermediate development in brachypterous neotenics. Primary kings and queens have a chitinized, pigmented exocuticle. The coloration and degree of sclerotization of second- and third-form reproductives is variable, even within a species.

In each of the three types of Reticulitermes reproductives, the female's abdomen distends as its ovarioles develop and its egg-laying capacity increases (termed physogastry). The number of eggs that a female termite can produce is correlated with its developmental origin. Mature primary queens have the greatest individual egg-laying potential. It is impossible to state exactly how many eggs this will be per day or per lifetime, but we do know that, within a species, relative egg productivity of a female termite is correlated with its size. A typical R. flavipes primary queen is approximately 14.5 millimeters in length. Brachypterous neotenic females have the next highest potential egg productivity; when mature they are about 12 millimeters long in R. flavipes. Fully developed apterous neotenic female reproductives are about 7 to 9 millimeters in length in R. flavipes, and regardless of the species, these females will be the least fecund type of reproductive (Snyder 1920, 1934).

Surprisingly, all types of Reticulitermes reproductives, even as mature, physogastric females, remain highly mobile. Large and seemingly cumbersome primary queens can move unassisted up nearly vertical inclines. Reproductives are capable of moving within a piece of wood, they can travel underground to reach a cooler and moister habitat, or they can walk from one resource to another used by the colony.

COLONY GROWTH RATES. Unfortunately there is no way to accurately estimate the age or rate of growth of subterranean termite colonies in the field. Therefore, in collaboration with Drs. Nancy Breisch (University of Maryland) and James Traniello (Boston University), I studied growth rates of young R. flavipes colonies headed by primary reproductives in the laboratory at the University of Maryland. We set up alate pairs in containers with everything that a young termite couple could possibly need: good and plentiful food, constant temperatures, adequate moisture, and protection from competitors and enemies.

We left the young termites undisturbed (except for adding food and water) for two years, and then we did a complete census of each colony. In the 55 colonies that had a surviving king and queen, we saw remarkable growth rates compared to those reported previously. The average colony population size (sum of all individuals, including immatures but excluding eggs) was 387 termites. The median colony size was 382; the range was 51 to 984 termites. Interestingly, the percentage of soldiers in these young colonies averaged about 2%, the same as that found in mature field colonies.

The colony growth rates seen in our laboratory study represent "best-case scenario" results, almost certainly higher than the growth rates of all but exceptional colonies in the field. The growth rates we witnessed are high compared to previous lab results, but they do not explain field sizes of termite colonies.

Even if we assume that a colony had the highest growth rate observed in the lab (approximately 1,000 termites in two years), and if we further assume that the growth rate doubles in each successive two-year period (as the queen grows and matures), the projected colony population size at 10 years would be 16,000 termites. (Assume that individual worker and soldier termites live for less than two years.)

Therefore, even using liberal projections of best-case colony growth rates, it would probably take a primary king and queen a very long time to build a colony up to a size approaching what is considered common in the field - which is well over 20,000 for most species (R. flavipes averages about 244,000, according to excavation counts conducted by Howard et al. 1982).

The queen's lifespan is unknown, but it is unlikely that an average Reticulitermes queen in the field has many more than seven to ten years of high fecundity even under the most favorable circumstances. Thus the question is raised: How do natural Reticulitermes colonies reach the immense population sizes of several hundred thousand to more than a million termites that we know exist? Furthermore, how are these large colonies organized?

MULTIPLE REPRODUCTIVES. The very large colony sizes that we know exist in the field, the apparent rarity of primary queens in these colonies, and the relatively slow growth rates of young colonies combine as lines of evidence to suggest the following scenario of Reticulitermes colony development.

Alates are dispersers that attempt to initiate new colonies. Colonies that survive have relatively low growth rates during their early years, almost certainly lower on average than the "best case" figures found in our laboratory study. Colony growth rates likely escalate over time in healthy colonies because the expanding number of workers can support higher egg production by the increasingly physogastric queen. Upon senescence of the founding queen or upon isolation of a group of individuals from that queen, multiple female neotenic reproductives differentiate. (A parallel process occurs with males in the absence of a king.)

Even though a mature primary queen can lay more eggs than a mature brachypterous or apterous neotenic reproductive, the cumulative egg production in Reticulitermes colonies headed by multiple neotenic reproductives is boosted substantially over that of colonies containing a single primary queen. It is at this point that the huge numbers of tens and hundreds of thousands, possibly up to millions of individuals, begin to build in these subterranean termite colonies.

ORGANIZATION & EXPANSION. How are large Reticulitermes colonies organized, and what are their modes of expansion?

A large Reticulitermes colony can be viewed as a network of population centers of various sizes (normally located in and around food resources) connected to other such centers by a system of roads (termite trails) of varying activity levels. Some of the connections between the hubs are heavily traveled highways, some are rarely traveled paths, and others may be obsolete passageways that are now out of use.

The distribution of termites among resources will change over time; new food sources will be occupied, and some resources will be abandoned. Individual termites may center their activity around certain food sources, moving only occasionally to other portions of the colony. At least one of these population centers, and possibly several of them, will contain reproductives.

As this termite community grows it undergoes transitions, probably including occasional divisions. Observations and experimental data suggest that an important reproductive pattern for Reticulitermes is colony splitting or budding. Colonies of many other types of termites are known to divide or bud, and evidence suggests that species of Reticulitermes should be included among those groups.

The first scientist to present a compelling case for colony budding in Reticuli termes was the renowned termitologist Dr. T.E. Snyder. He reported (1920, 1934) that extra brachypterous, or more rarely apterous, neotenic reproductives are found in R. flavipes colonies at the same time as the alates mature, but that before the alate flight they "disappear." He also witnessed two "pseudo flights" of R. virginicus, in which brachypterous neotenics emerged from stumps at the same time as the alate flight but "could only run about" because they had no wings (Snyder 1920, 1934). Based on these observations, Snyder proposed that neotenics may leave their parent log and migrate through subterranean passages to a new nesting site, accompanied by workers and soldiers because the neotenics must be fed.

Ralph Howard and Mike Haverty (1980) conducted a field experiment in Mississippi that suggests a similar dynamic. They located 100 "source" colonies of Reticulitermes in fallen logs and stumps, and put sampling baits (large weathered pine bolts) at intervals around the periphery of 89 of the source locations. Periodically over the next two years they collected and dissected three baits around each colony.

They found reproductives in at least one bait from 26 of the 89 colonies. Three of the baits contained primary reproductives, confirming that mature, physogastric queens can and do move among resource sites. All of the other reproductives found in the baits were neotenics. When reproductives were found, they were usually located in only one of the three sampled baits. It is not known whether these neotenic reproductives dispersed from the source colony into the baits, or whether they differentiated within the baits, but either way the study demonstrates a movement of the location of reproductives in a colony.

Esenther (1969) reported that he never saw a normal alate flight, nor did he ever find a field colony headed by primary reproductives during several years of working with Reticulitermes in Wisconsin. He concluded that, at least in that region, local spreading of colonies of infestations occurs largely through new colony formation associated with splitting of mature colonies.

ON THE MOVE. The pattern that emerges is that Reticulitermes colonies are mobile. Foragers explore, occupy, and leave resources within a "home range" that can span a linear distance of at least 79 meters (Grace et al. 1989). The "colony headquarters" is not a permanent, central position. The entire colony, including reproductives, may move between logs or soil as temperature, moisture, and resource conditions vary.

In laboratory cultures of nest boxes connected by 5-meter lengths of Tygon tubing, R. flavipes carry eggs and immatures from one box to another. Reticulitermes colonies are dynamic and appear to have a number of reproductive options depending on circumstances.

Reticulitermes colonies that attain large population sizes probably contain multiple neotenic reproductives. In some cases a portion of the neotenics may migrate from the colony "headquarters" to a satellite reproductive unit. A satellite nursery may also form if neotenics differentiate within a group of termites living within a resource that is distant from the original colony center. It is not known whether either of these possibilities can occur if a healthy primary pair remains within the colony.

THE STRAWBERRY ANALOGY. It may sound like an odd comparison, but in many ways the life history of a Reticulitermes colony is analogous to that of a strawberry plant. A parent strawberry plant grows from a seed, as the termite colony begins with the king and queen. When the strawberry plant attains sufficient size and strength it produces fruit. The tiny seeds on a strawberry are comparable to the alates produced seasonally by a mature termite colony. Strawberry plants make lots of seeds; termite colonies may produce loads of alates. These propagules are able to disperse far from their parent, but very few succeed in establishing a new plant or new termite colony.

In addition to seeds, strawberry plants can produce vegetatively through runners that trail from the parent and then root to initiate a new plant in the same neighborhood. Over time the runner connection to the parent plant may be severed, and the budded plant functions as an independent unit. A satellite group of foragers in a subterranean termite colony is similar to a strawberry runner. It occupies a separate resource, but remains connected to the main colony by trails. Over time satellite groups may develop or acquire neotenic reproductives.

In such circumstances we do not know how long the termites remain in contact with other portions of the colony. The network may continue to function as a large and intermingling, but decentralized, society. Alternatively, some or all of the satellite units may eventually become isolated, separate groups, as when the strawberry runner severs from the parent plant.

Termites in separated pieces of wood or in other locations are always at some risk of being physically cut off from the main colony. Floods or droughts could temporarily or permanently disrupt connections between resources used by a colony. It would thus be an advantage for Reticulitermes to have reproductives dispersed among satellite groups, or to have the ability for reproductives to differentiate from nymphs or workers stranded in a separated arm of a colony. This spreading of colonies by active or passive splitting is also an effective method of local growth, expansion, and possible colony division. Sequential budding would ultimately create a neighborhood of closely related Reticulitermes colonies.

WHAT IS A `COLONY'? So what exactly is a Reticulitermes colony? The definition is not controversial when there is a simple organization of one "headquarters" containing primary, or neotenic, reproductives, with this base connected by active trails to satellite groups of foragers.

The concept of a colony is still straightforward even if reproductives are distributed among more than one satellite of a dispersed network that remains linked by operative trails. But if a portion of an expansive, spatially diffuse colony loses connection and contact with its parent colony, and then functions as an independent unit, is that fragment a new colony?

Semantics aside, the biological result is the same. Whole residential neighborhoods, or even larger areas, may contain a single termite "colony" either broadly expanded but still connected, or fragmented into related clones or buds from a single original colony.

Reticulitermes are notoriously difficult to study in the field. Many aspects of their natural history are still poorly known. These termites live in a matrix of hidden, subterranean galleries in large colonies that can be observed and sampled only through the hazy "windows" of monitors and opportunistic discoveries.

It is almost certainly inaccurate to lump all species of Reticulitermes as a group having a single life history pattern, yet at this point not enough is known about each species to discriminate among their characteristics. As the research community continues to make progress in unraveling the biology of these insects, we will more fully understand the most complex aspects of their societies, such as their reproductive dynamics and the organization of their colonies.

REFERENCES

Esenther, G.R. 1969. Termites in Wisconsin. Annals of the Entomological Society of America 62: 1274-1284.

Grace, J.K., Abdallay, A. & Farr, K.R. 1989. Eastern subterranean termite (Isoptera: Rhinotermitidae) foraging territories and populations in Toronto. Canadian Entomologist, 121, 551-556.

Howard, R.W. & Haverty, M.I. 1980. Reproductives in mature colonies of Reticulitermes flavipes: abundance, sex ratio, and association with soldiers. Environmental Entomology, 9, 458-460.

Howard, R.W., S.C. Jones, J.K. Mauldin and R.H. Beal. 1982. Abundance, distribution, and colony size estimates for Reticulitermes spp. (Isoptera: Rhinotermitidae) in southern Mississippi. Environmental Entomology 11: 1290-1293.

Snyder, T.E. 1920. The colonizing reproductive adults of termites. Proceedings of the Entomological Society of Washington 22: 109-150.

Snyder, T.E. 1934. American subterreanean termites other than those on the Pacific Coast. In: Kofoid, C.A. (ed.) Termites and Termite Control, 2nd Edition. University of California Press, Berkeley, pp. 187-195.