Dr Thomas Chouvenc, Associate Professor at the Ft Lauderdale Research and Education Center of the University of Florida, explores the life cycle of a termite colony, which in some cases can span many decades.
Termites have a complicated life cycle, which departs from most other household pests. Cockroaches for example, have a simple egg-to-adult developmental scheme, where a female lays eggs, which hatch, develop through a series of moults, and later mature into individual fertile adults. In comparison, a termite colony overwhelmingly produces sterile individuals (workers and soldiers) and individuals with a potential for reproduction (winged individuals i.e. alates) are only produced seasonally, once the colony has reached maturity (Figure 1).
However, this concept of ‘colony maturity’ is rarely discussed. I wonder how many of us, during an inspection have said, “Well this is a baby colony that has not matured yet!” Let’s be honest: very few of us.
Why is that? Because a subterranean termite colony often infests a structure when it has the ability to forage extensive distances and recruit large numbers of workers, which is only possible when the colony has already reached a critical mass. The usual thought process upon discovery of an infestation during an inspection is that the colony has already caused damage and that damage will continue if no action is taken. There is no rationale to think “I wonder how old this colony is?” because it is often irrelevant on how to approach a termite management protocol. The point is: if you found the activity of a live termite colony, it implies that the colony was big enough to be noticed, and therefore has already reached a mature status, or is soon about to.
As you are preparing for the colony elimination process (after the customer has signed all the legally binding forms), you may want to keep in mind: this termite colony has a whole history and had a life of its own, with an origin story, growing pains, a phase through puberty (yes, sort of!), and finally, perennial reproductive success. You are therefore not only about to kill hundreds of thousands, maybe millions of termites, you are about to obliterate a biological entity (i.e. the colony) with a unique story to tell. Don’t get me wrong: this article is not about taking you on a guilt trip. I am not that malicious. Instead, I hope to raise awareness about the complexity of termite colony development, so you can have some appreciation of this fascinating organism, help you find the beauty in the beast, and make some money in the process (you, not me).
The colony as a ‘superorganism’
To understand the origin and success of a termite colony, we have to look at the colony as a family unit that represents a biological entity at a higher degree of organisation than individual organisms, where a termite colony is often referred to as a ‘superorganism’. The reproductive division of labour effectively results in within-colony reproduction often being restricted to the queen and king (i.e. mum and dad). The colony has to go through a series of phases analogous to the ones of a single organism: a colony is initiated by its ‘birth’, must then ‘grow’, to eventually reach ‘reproductive maturity’, and finally ‘die’. From birth to death, the colony must therefore go through a long series of events to successfully spread their genes to the next generations and perpetuate the species over evolutionary times (Chouvenc and Su 2014, Chouvenc et al. 2022). Let’s briefly go over these colony life phases.
The birth of a termite colony
The ‘birth’ of a colony usually occurs soon after a dispersal flight event, when established mature colonies synchronously produce alates, which fly into the air (Figure 2). Such flights have also been referred to as: swarms, nuptial flights, royal flights, and mating flights, among other used terms.
However, such events in termites have only one function: dispersal (hence the appropriate use of ‘dispersal flight’). Contrary to swarming events in social Hymenoptera such as ants and bees, where mating occurs during the flight (and where the males usually die in the process), termite alates fly out of their parental nest only to disperse away from it, in hope to find a potential partner. Termite alates often drop their wings rapidly (Figure 3) after a short flight period (becoming ‘dealates’).
This phase is critical for all dispersing individuals, as predation is strong during such events (Nutting, 1969). The sudden emergence of millions of alates is the equivalent of a massive nutritional dump of defenceless individuals in the environment, which any opportunistic predators can feast upon (Figure 4). Dealates have to rapidly find a suitable partner and hide before becoming someone else’s meal, in what can be seen as an ‘ultimate speed dating’ event, where the loser dies immediately (I really should get the rights for a potential reality TV show on this concept).
In most termite species, the female dealate produces a sex pheromone at the dorsal tip of the abdomen, which facilitates the encounter with prospective males (Chouvenc et al. 2020). Once a male detects a female and initiates contact with her abdomen using his mouthparts, they engage in a ‘tandem run’ (Figure 5), where the female leads to quickly find a suitable nesting site, while the job of the male following behind is to maintain contact with the female (Mizumoto et al. 2021).
In termites, mate choice is quasi non-existent, as it primarily follows a first-come-first-served ground rule. This implies that initiating a tandem run with a sibling is possible (but the probability is reduced with increasing dispersing distance). It appears that males and females do not have the ability to tell the origin of their partner, whether they are from the same colony of origin, from an unrelated colony, or from a completely different species (some sex pheromones in termites are shared among many taxa). As a result, termites are not picky during tandem run parings; as long as the male cues on the female’s sex pheromone and the female has ‘someone’ following her, they have a shot at getting things started.
So, what if the pairing involves siblings, different species or poor quality partners? Well, most of them (if not all) are doomed to fail the next step: colony foundation. The reality is, only a tiny fraction of all alates successfully reaches and completes the colony foundation phase. Termite dispersal flights use a ‘number’s game’ approach to successfully establish new colonies. It does not matter if most alates die or fail to find a suitable partner; as long as just a few of them succeed, a sufficient number of newly established colonies will maintain the gene pool within the population over generations. In a way, termite colonies rely on luck to be successful, by repeatedly playing the lottery with so many possible permutations, that it ensures colony foundation success. If alates only have a <0.1% establishment success rate from many millions of alates and haphazard partner combinations, it can still result in dozens or hundreds of newly established colonies.
If lucky, the female and male tandem run may find a place to hide within the immediate environment. If not, they would just join the statistics above. Too hot, too cold, too wet or too dry and the story is over before it even started for the couple. The two dealates spend the first day establishing a claustral chamber, as a way to seal themselves away from environmental and predatory threats. Depending on the species, they use saliva, masticated wood pulp and soil particles to create this seal. Finally, once they are alone and ‘safe’, the male and female engage in copulation (Figure 6), which occurs multiple times a day for several weeks. The female lays a dozen eggs within a few weeks, which are tended both by the male and the female to ensure their embryonic development toward hatching. Saliva is regularly deposited on the eggs to prevent their desiccation or to remove potential parasites. As the first few larvae emerge, the colony is officially ‘born’ as small family unit: mum, dad and the few first babies.
Growing pains
Once the first offspring have emerged, the incipient colony is far from being guaranteed to succeed, as many events can result in colony establishment failures. For example: genetic incompatibilities between the male and the female could result in an unviable brood; both partners could bring insufficient microbial symbiont inoculum, which would prevent the establishment of inadequate digestive capabilities within the family unit; or one of the partners could be incompetent in brood care duties (Chouvenc 2022, Velenovsky et al. 2023). Alternatively, ants could find their hiding place and that would be the end of it, as the colony does not yet have the capability to defend itself. The first five months after colony foundation are critical, as the two founding parents only have a single shot to establish a successful brood. They both come with limited internal resources and if their combined contribution is insufficient to kickstart a first cohort of offspring, colony foundation will fail. If successful, both the male and female display extensive biparental care to their brood, which results in the emergence of a dozen larvae (Figure 7).
Within five months, the first few workers and soldiers are produced, after several larval moults. At this point, a fundamental change occurs within the colony, as workers acquire the ability to chew and digest wood, and also to provide care to subsequently laid eggs and developing larvae. Parental care duties progressively shift away from mum and dad, to be entirely taken over by workers. This shift toward alloparental care (i.e. older siblings taking care of younger siblings) is irreversible (Chouvenc and Su 2017) as the two parents solely focus their time and energy toward colony growth by laying more and more eggs. At this point in the development of the young colony, reproductive division of labour is fully established, and the female and the males are no longer just ‘mum and dad’; they are now functionally ‘queen and king’ of their colony, taking over a single function: colony reproductive output, which involves a lot more sex.
In the next few years, the colony slowly grows from two individuals, to potentially millions of individuals (species dependent). This colony growth follows a logistical function, which means that early on, it may take a year to produce 200 workers owing to the initial limited nurturing capacity of the young colony (numbers used here are relative and vary greatly among species and conditions). However, with the accumulation of caregivers and foragers from the first year’s growth, resources within the colony become more accessible, which allows for additional oviposition by the queen, in a positive feedback loop. Within two years, the colony could reach 2000 termites, 20,000 within three years, and 200,000 within four years. In Coptotermes, the colony may reach one million individuals within five years of growth (Chouvenc and Su 2014). This initial exponential growth then slows down, as the queen may reach maximum oviposition capacity (Figure 8) where the population can maintain degrees of stability owing to the natality rate and mortality rate being somewhat equivalent.
Again, several adverse events may terminate development and result in colony failure during such ongoing growth. Competition with other termite colonies (intra and interspecies) can lead to a loss of access to resources required for colony maintenance. As the colony grows and expands its foraging territory, the rate of encounter with competitors and predators increases, and optimal defensive strategies involving nest architecture and soldier production can contribute to the self-preservation of the colony. Finally, for the few lucky ones that survived up to this phase, the colony can reach a critical capacity, which allows it to venture toward colony maturity. Colony size and time required for a colony to reach maturity can be highly variable depending on species and conditions, so estimations to determine what it takes for a colony to become mature can be rather speculative.
Colony maturity and reproductive shift
Colony maturity is determined by its ability to produce nymphs, which then moult into alates, which in turn can disperse to establish new colonies. This means that the first time a colony produces nymphs, it engages in a fundamental reproductive shift, and is analogous to the superorganism undergoing ‘puberty’. Until now, all eggs laid by the queen were aimed at within-colony growth, which means that all sterile individuals were produced with the aim of upholding colony functions. Similarly, a human baby grows through childhood by developing cells and organs that are aimed at growth and body function (soma line). When the individual goes through puberty, body functions change toward becoming reproductively active (germ line), by reallocating resources toward reproduction (e.g. oocytes in females, sperm in males). In termites, colony maturation implies that resource allocation partially shifts away from colony growth and maintenance (production of workers and soldiers) toward reproductively capable individuals (alates) that can make new colonies through dispersal flight events (external reproduction).
The shift of resource investment from the equivalent of the soma line (workers) toward the germ line (alates) is then repeated annually, through the seasonal production of nymphs, which then leads the mature colony to enter perennial reproductive output. Each year, the established mature colony allocates a portion of its resource budget toward nymph production, which may take up to a whole year to mature into alates (Figure 9), and then participate in synchronous dispersal flight events with other mature colonies within the proximate environment. Not only does the mature colony complete its life cycle as soon as one of the produced alates successfully establishes a new colony, it continues to do so by repeating the process every year, potentially for decades. As a result, cumulated over the years, a single mature colony can be the source of hundreds of newly established colonies throughout its lifetime, where each colony can complete its own reproductive success through unique demographic trajectories (Chouvenc et al. 2022).
Senescence and death of a termite colony
Finally, within-colony reproduction may end, as the queen or king eventually dies. Some species can produce replacement reproductives (secondary queens and kings), leading to potential cycles of inbreeding, which can be temporarily tolerated in many termite species. However, colony functions and reproductive output eventually decline, resulting in the accumulation of old individuals in the absence of population renewal. During this time, the colony goes through a senescent phase, with a notable absence of larvae, young workers, and nymphs. Within three years of the loss of reproduction, the colony eventually collapses and dies. In all reality, a majority of termite colonies in the environment that were reproductively successful eventually succumb to their natural death. Such ‘natural’ death may become artificially accelerated if a series of factors align:
- if the termite species has a pest status;
- if the colony is currently infesting a man-made structure;
- if the homeowner has access to a sufficient discretionary income; and
- if the services of a locally competent pest control company are affordable. This is where you step in.
It was determined in Coptotermes that the use of chitin synthesis inhibitors in bait formulations can result in colony elimination within three months after initial feeding (Chouvenc 2018, Gordon et al. 2022). The colony collapse from baiting (previously described in Termite Professional 2022 edition) inherently terminates within-colony reproduction as the queen(s) stop laying viable eggs (Chouvenc and Lee 2021), larvae rapidly die, and the colony accumulates old workers. Essentially, the baiting process recapitulates the natural colony senescence process, but accelerates it from three years down to three months (Chouvenc et al. 2022). So, next time you achieve customer satisfaction on a subterranean termite job, please keep in mind that you just put an end to a biological entity that had a remarkable life, until it met you.
Additional reading
This article is a simplified overview of a termite colony life cycle that is reviewed in depth in an upcoming book chapter: Chouvenc T. 2023. A primer to termite biology: Coptotermes colony life cycle, development and demographics (Chapter 4). In: Biology and Management of the Formosan Subterranean Termite and Related Species (Su N-Y and Lee C-Y, Eds). CABI, in press.
More information on termites
Dr Thomas ChouvencAssociate Professor in Urban Entomology at the Ft Lauderdale Research and Education Center of the University of Florida Institute of Food and Agricultural Sciences, Florida, USA
[email protected]
Among some of his recent work, Dr Chouvenc investigated the impact of chitin synthesis inhibitor baits on subterranean termites at the colony level, documented the important role of access to dietary nitrogen from soils in Coptotermes, and characterised the complex demographic dynamics of termite colonies over several decades. Dr Chouvenc is also the coordinator of the University of Florida School of Structural Fumigation, and the organiser of the International Termite Course for Academics and the Termite Course for Professionals.
All images courtesy of Thomas Chouvenc/UF-IFAS.
References
Chouvenc, T., 2018. Comparative impact of chitin synthesis inhibitor baits and non-repellent liquid termiticides on subterranean termite colonies over foraging distances: colony elimination versus localized termite exclusion. Journal of Economic Entomology, 111: 2317-2328.
Chouvenc, T., 2022. Eusociality and the transition from biparental to alloparental care in termites. Functional Ecology, 36: 3049-3059.
Chouvenc, T., 2022. The Global impact of Coptotermes and the rise of CSI bait formulation as a solution. Termite Professional, 2022 Australian Edition, 1: 6-11.
Chouvenc, T. and Lee, S.B., 2021. Queen egg laying and egg hatching abilities are hindered in subterranean termite colonies when exposed to a chitin synthesis inhibitor bait formulation. Journal of Economic Entomology, 114: 2466-2472.
Chouvenc, T. and Su, N.Y., 2014. Colony age-dependent pathway in caste development of Coptotermes formosanus Shiraki. Insectes Sociaux, 61: 171-182.
Chouvenc, T. and Su, N.Y., 2017. Irreversible transfer of brood care duties and insights into the burden of caregiving in incipient subterranean termite colonies. Ecological entomology, 42: 777-784.
Chouvenc, T., Sillam-Dussès, D. and Robert, A., 2020. Courtship behavior confusion in two subterranean termite species that evolved in allopatry (Blattodea, Rhinotermitidae, Coptotermes). Journal of Chemical Ecology, 46: 461-474.
Chouvenc, T., Ban, P.M. and Su, N.Y., 2022. Life and death of termite colonies, a decades-long age demography perspective. Frontiers in Ecology and Evolution, 10.911042.
Gordon, J.M., Velenovsky IV, J.F. and Chouvenc, T., 2022. Subterranean termite colony elimination can be achieved even when only a small proportion of foragers feed upon a CSI bait. Journal of Pest Science, 95, 1207-1216.
Mizumoto, N., Rizo, A., Pratt, S.C. and Chouvenc, T., 2020. Termite males enhance mating encounters by changing speed according to density. Journal of Animal Ecology, 89: 2542-2552.
Nutting, W.L., 1969. Flight and colony foundation. In: The biology of termites, Vol. 1 (Krishna, K. and Weesner, F.M. Eds) Academic Press, New York. pp.233-282.
Velenovsky, J.F., De Martini, F., Hileman, J.T., Gordon, J.M., Su, N.Y., Gile, G.H. and Chouvenc, T., 2023. Vertical transmission of cellulolytic protists in termites is imperfect, but sufficient, due to biparental transmission. Symbiosis, 90: 25-38.
