The Subterranean Undertaker

THE SUBTERRANEAN UNDERTAKER

This may seem like a strange subject to write about, but it was prompted by a question a guest once asked me on a game drive, and that was, “What happens to termites when they die?” I recall pulling my, “Hmmm good question!” face… and I thought to myself, what DOES happen to termites when they die? Do they only die outside the termatarium? Do predators outside the mound just eat all dead termites? Bearing in mind that a single colony can support hundreds of thousands of individuals with a short life span, the death rate must be pretty high.

Completely intrigued, I did some research, and was most surprised by the results. Scientific papers dating back to 1958, entitled the likes of “The undertaking activities of social insects”, “Corpse management of social insects”, “Differential undertaking responses of a lower termite to corpses.”…The list was endless. I read through a number of these papers and sat back in my chair at the end to mull results over. I played out a scenario in my head of a termite dying, a second individual finding it, and a third termite rushing up and stating aloud “Step aside, I am the undertaker”. I laughed out loud, but actually, that is exactly what happens.

STEP ASIDE, I AM THE UNDERTAKER

To maintain healthy colonies, social insects, i.e. bees, wasps, ants and termites have evolved sophisticated ways to counter the threat of disease at both the individual and colony level. Any nest-mates that die inside the nest represent a high risk for insect societies, especially those that have died due to some infectious agent. All possible measures are thus taken to prevent potential sources of diseases from spreading to other members of the society, especially the queen and the brood. The nature of these insects allows for the specific division of labour in their social structures, in the sense that different individuals engage in very specialised tasks. This has led to the development of an “undertaker worker” that exists for the purpose of engaging in corpse management and must quickly remove all the dead members of the colony inside the nests. Bees, wasps, ants and termites are the only animals apart from humans that harbour complex behavioural strategies for disposing of dead belonging to their same species.

So what does happen to social insects when they die? Honeybees, ants, and termites each show species – specific undertaking responses toward corpses:

Studies of undertaking behaviour in bees have traditionally focused on the honeybee. Honeybees dispose of nest-mate corpses in a straightforward manner, i.e. corpse removal. An “undertaker” bee typically uses its antennae to touch the dead bee briefly, grasps its appendages with mandibles, transports it outside, and drops it from the hive. Noteworthy is that other debris in honey bee colonies have been observed to be removed less rapidly.

The behavioural patterns of ants are extremely diverse, but they are known to keep the interior of their nest meticulously clean. Corpse removal is common in various ant species, and is distinguished from other nest cleaning behaviours as corpses are transported more rapidly and over greater distances than inanimate objects. Cannibalism of dead individuals was observed in some species, and the Matabele ant, for example, eat their defeated enemies after inter-colony battle, which has been considered to be adaptive as they practice cannibalism behaviour more frequently during period of food shortage. Besides cannibalism, ants are reported to perform burial behaviours using soil and nest material in response to corpses but it is less common probably because the energy input of burial activity is higher than corpse removal.

Termites too have evolved complex systems of corpse management dealing with corpses of different ages, origins, and infection status. They include burial, avoidance, and cannibalism. Cannibalism of the dead in termites is considered to be a mechanism of recycling nitrogenous nutrients, which is, in part, due to their nutritionally poor cellulosic diet. In comparison to ants and bees, termites’ preference for tunnel building plays an important role in their burial behaviour. In fungus-growing species, the existence of corpses induces building behaviour to separate the dead from the rest of the colony. The use of faecal material, chewed material or soil coated with saliva for building (and burial) provides anti-fungal components that act as further protection against fungal growth and spreadable diseases.

It is one thing accepting undertaking activities, but how do these insects, some who don’t even have a brain (only a central nervous system), even know that their nest mate is dead? Research suggests that death recognition is a combination of factors, but in particular can be explained by two hypotheses: a “fatty acid death cue” and a “chemical vital sign”. Fatty acids are released upon death for decomposition, but where corpses are found and removed within one hour (which is too short a time period to allow for decomposition), it has been suggested that the absence of a chemical associated with life may prompt undertaking activities.

As a result, these social insects exhibit specific responses to the nature of the corpses, including their postmortem time, infection status (whether harmful fungi are present), and origin (whether or not the corpse is a nest-mate or of the same species). Responses then vary from removal, burial or cannibalism. Fungus growing termites, for example, were found to isolate fungal infected individuals by burying the dead onsite, while the healthy corpses were cannibalised. Soldiers were also involved with guarding corpses as the burial response was underway. In honeybees, 1-hour old corpses were observed to be removed more quickly than freshly killed individuals, and dead ants of the species “Red wood ant” were consumed for food, but infectious ants were avoided. In another species, workers discriminated old corpses from freshly killed individuals, with new corpses buried while old ones are transported outside.

So next time you see one of these social insects, or drive past their colonies, keep an eye open for this intriguing behaviour, and you never know, one day you may even meet “The Undertaker”.

References for further reading

1. The funeral ways of social insects http://www.academia.edu/6390866/The_funeral_ ways_of_social_insects._Social_strategies_for_c orpse_disposal
2. Corpse Management in social insects http://www.ncbi.nlm.nih.gov/pmc/articles/PMC361 9097/
3. Visscher PK. The honey bee way of death: Necrophoric behaviour in Apis mellifera colonies. Anim Behav. 1983;31(4):1070–1076
4. Suzuki K, Yoshihama T, Shigematsu Y. Sweeping behaviours of honey bees at the hive entrance. Bull Fac Edu, Chiba Univ. 1974;23:273–281
5. Wilson EO, Durlach NI, Roth LM. Chemical releaser of necrophoric behavior in ants. Psyche. 1958;65(4):108–114
6. Marikovsky P. On some features of behavior of the ants Formica rufa L. infected with fungous disease. Insect Soc. 1962;9(2):173–179
7. Driessen GJJ, Raalte ATV, Bruyn GJD. Cannibalism in the red wood ant, Formica polyctena (Hymenoptera: Formicidae) Oecol. 1984;63(1):13–22
8. Hölldobler B, Wilson EO. The Ants. Cambridge: Harvard University Press; 1990.
9. Renucci M, Tirard A, Provost E. Complex undertaking behavior in Temnothorax lichtensteini ant colonies: from corpse-burying behavior to necrophoric behavior. Insect Soc. 2010;58(1):9–16
10. Kramm KR, West DF, Rockenbach PG. Termite pathogens: Transfer of the entomopathogen Metarhizium anisopliae between Reticulitermes sp. termites. J Invertebr Pathol. 1982;40(1):1–6
11. Rosengaus RB, Traniello JFA, Bulmer MS. Ecology, behavior and evolution of disease resistance in termites. In: Bignell ED, Roisin Y, Lo N, editors. Biology of termites: A modern synthesis. New York: Springer; 2011. pp. 165–191.
12. Apparent synergy among defense mechanisms in subterranean termites (Rhinotermitidae) against epizootic events: limits and potential for biological control.Chouvenc T, Su NYJ Econ Entomol. 2010 Aug; 103(4):1327- 37.1
13. Wilson EO, Durlach NI, Roth LM. Chemical releaser of necrophoric behavior in ants. Psyche. 1958;65(4):108–114.)
14. Choe DH, Millar JG, Rust MK. Chemical signals associated with life inhibit necrophoresis in Argentine ants. Proc Natl Acad Sci U S A. 2009;106(20):8251–8255.
15. Kramm KR, West DF, Rockenbach PG. Termite pathogens: Transfer of the entomopathogen Metarhizium anisopliae between Reticulitermes sp. termites. J Invertebr Pathol. 1982;40(1):1–6
16. Marikovsky P. On some features of behavior of the ants Formica rufa L. infected with fungous disease. Insect Soc. 1962;9(2):173–179.
17. Renucci M, Tirard A, Provost E. Complex undertaking behavior in Temnothorax lichtensteini ant colonies: from corpse-burying behavior to necrophoric behavior. Insect Soc. 2010;58(1):9–16.