The sub-terrainian undertaker…A new movie, wrestler or the funeral job of a social insect?

This may seem like a strange subject to write about, but it was prompted by a question a guest asked me on game drive one day, 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 termatorium? Do predators outside the mound just eat all dead termites? Bearing in mind that a single colony can support hundreds upon thousands of individuals with a short life span, the death rate must be pretty high.

Colony of fungus growing termites

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 by 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 “move over, I am the undertaker”. I laughed out loud, but actually, that is exactly what happens.

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.¹ Any nestmates that die inside the nest represent a high risk for insect societies, especially those that have died due to some infectious agent². 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 lead 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 nests¹. Bees, wasps, ants and termites are the only animals apart from humans that harbor complex behavioral strategies for disposing of dead belonging to their same species.

Termite caste system

So what does happen to social insects when they die? Honeybees, ants, and termites each show species-specific undertaking responses toward corpses (see Figure 1).

Figure 1.

Studies of undertaking behavior in bees have traditionally focused on the honey bee³. Honeybees dispose of nestmate corpses in a straightforward manner, i.e, corpse removal⁴. An “undertaker” bee typically antennae’s 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 rapidly³.

 

The behavioral 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 behaviors as corpses are transported more rapidly and over greater distances than inanimate objects⁵. Cannibalism of dead individuals was observed in some species, and the Matabele ant, for example, eat their defeated enemies after intercolony battle⁶, which has been considered to be adaptive as they practice cannibalism behavior more frequently during period of food shortage⁷. Besides cannibalism, ants are reported to perform burial behaviors using soil and nest material in response to corpses⁸ but it is less common probably because the energy input of burial activity is higher than corpse removal⁹.

The undertaker ant...removing a dead nestmate

Termites too have evolved complex systems of corpse management dealing with corpses of different ages, origins, and infection status.1 They include burial, avoidance, and cannibalism. Cannibalism of the dead in termites is considered to be a mechanism of recycling nitrogenous nutrients¹⁰, which is, in part, due to their nutritionally poor cellulosic diet¹¹. In comparison to ants and bees, termites preference for tunnel building plays an important role in their burial behavior¹². In fungus-growing species, the existence of corpses induces building behavior to separate the dead from the rest of the colony. The use of fecal material, chewed material or soil coated with saliva for building (and burial) provides antifungal components that act as further protection against fungal growth and spreadable diseases.

Termite workers and soldiers

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 nestmate 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”¹³. 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 activities¹⁴.

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 nestmate 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 cannibalised¹⁵. Soldiers were also involved with guarding corpses as the burial response was underway. In honeybees, 1h old corpses were observed to be removed more quickly than freshly killed individuals³, and dead ants of the species “Red wood Ant” were consumed for food, but infectious ants were avoided¹⁶. In another species, workers discriminated old corpses from freshly killed individuals, with new corpses buried while old ones are transported outside¹⁷.

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

Ant caste system

Reference List

1. The funeral ways of social insects
http://www.academia.edu/6390866/The_funeral_ways_of_social_insects._Social_strategies_for_corpse_disposal
2. Corpse Management in social insects http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3619097/
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;23:273–28Wilson EO, Durlach NI, Roth LM. Chemical releaser of necrophoric behavior in ants. Psyche. 1958;65(4):108–114
5. Marikovsky P. On some features of behavior of the ants Formica rufa L. infected with fungous disease. Insect Soc. 1962;9(2):173–179
6. Driessen GJJ, Raalte ATV, Bruyn GJD. Cannibalism in the red wood ant, Formica polyctena (Hymenoptera: Formicidae) Oecol. 1984;63(1):13–22
7. Hölldobler B, Wilson EO. The Ants. Cambridge: Harvard University Press; 1990.
8. 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.
9. 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
10. 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.
11. 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.
12. Wilson EO, Durlach NI, Roth LM. Chemical releaser of necrophoric behavior in ants. Psyche. 1958;65(4):108–114.)
13. 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.
14. 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.
15. Marikovsky P. On some features of behavior of the ants Formica rufa L. infected with fungous disease. Insect Soc. 1962;9(2):173–179.
16. 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.