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.

The Cheetah: A bright future or no future?

Cheetah…the worlds fastest land mammal, boasting an impressive 0-60km/hour in 3 seconds or less, able to leave any regular automobile in the dust (and regularly us, too). I am often asked during safari why we see comparatively fewer cheetahs  than other predators, especially lions and leopards. The are a number of general answers, ranging from territory size, competition, topography and  other factors, but I’d like to explore which of the reasons most affect the cheetah population at Singita Sabi Sand, and,  if at all, we will see changes in the coming few months and years.

Ten years ago, there were reports of some 35 different individual cheetahs that were regularly seen in this area. Today, numbers are significantly less, certainly fewer than 10 at any one time, for the sake of argument. And we are not alone in reporting such a dramatic decrease; according to the Wildlife Conservation Society, cheetah numbers have dwindled globally from 100,000 in 1990 to less than 15,00 today…a mere 7,000 if you prefer the Africa Geographic figures. This makes the cheetah one of the most endangered big cats in the world.

For a species that has been around for 2.2 million years, what has been the catalyst for such a sudden drop in numbers? Many will say the threats are primarily human ones, responsible for encroaching on their territory, dispersing both cheetahs and their prey, not to mention direct human conflict, especially over cattle and goats (it is worth noting that over 90% of cheetahs live outside conservation areas). No doubt these are huge contributing factors. Luke Hunter, executive of Panthera, makes an interesting point though. With the addition of a new cheetah fossil found in 2008, that brings the tally of cheetah and cheetah-like specimens known to have existed to 5/6…only one of which is still alive today. Hunter quotes “It suggests that the 'sprinting cat' specialization is a fragile one, prone to extinction even under natural circumstances."¹ It is an interesting analogy, and fragile they certainly seem to be. But fragile to what, and to whom?

Competition & predation

Predators, namely lions, leopards and hyenas, affect Cheetahs in a variety of ways; restricting access to high resource areas and thus limiting their food intake, stealing their kills (e.g. 10–12% of kills are kleptoparasitized (stolen) in Serengeti National Park (SNP))² and predating on their cubs, reducing population sizes via increased cub mortality (e.g. 73% of cub mortality was due to predation in the SNP).²

At Singita Sabi Sands, whilst we have witnessed a drop in cheetah numbers, the lion population  particularly has done quite the opposite, and expanded tremendously. Is this see-saw effect a coincidence, or is it proof that lions have outcompeted the cheetah? Research carried out in the Serengeti indeed found that “cheetah numbers decreased when lion densities were high.”³ It is worthwhile noting that an increase in the lion population has a two-fold effect, not just in there physically being more lions, but that hyenas, as scavengers, are drawn to areas with more lions due to the larger number kills, and it is them too who play a significant role in this competition scenario.

To confirm the fact that lions and hyenas, particularly, have a negative affect on cheetahs, a study on avoidance tactics to these animals by cheetahs found that;

“cheetahs actively moved away from lion and hyena playback experiments…(they) showed no differences in their responses to playbacks dependent on their sex or reproductive status, suggesting they were responding principally to a competition rather than a predation threat. However, cheetahs were much less likely to hunt after competitor playbacks than after dummy playbacks, and this resulted in a lower kill rate after competitor playbacks, demonstrating that the perceived presence of competitors had a noticeable impact on the foraging rate of cheetahs. Furthermore, while cheetahs moved just as far following lion playbacks as after hyena playbacks, they spent significantly more time looking at the loudspeaker and were less likely to make a kill after lion playbacks, suggesting that cheetahs perceive lions to be a greater threat than hyenas.”⁴

Avoiding the competition and having kills stolen is one thing, but a key problem facing the cheetah population is high cub mortality. Cubs are most vulnerable when at a carcass, which attracts other predators, often ending in disaster for the youngsters if they can’t keep up with their mother as she runs for safety.  Recent research into cub mortality notes;

“Generally, recruitment (cub survival) declined with increasing lion numbers, regardless of other factors such as whether rainfall was high or low or whether gazelle numbers were high or low. The only exception to this pattern occurred when the number of female cheetahs in the population was high, when there was an increase in numbers with lion numbers”³.

Our experience here in the Sabi Sands seems aligned with these theories. The maps below illustrate the overlapping home ranges between lions, leopards, hyenas and cheetahs and demonstrate clearly that competition, in its multiple formats, is a very real problem facing cheetahs in the Sabi Sands. We witness it too on game drive; the nervous behavior of cheetahs, not just when they are on a kill but as they move from place to place. Furthermore, just last year, we witnessed an entire litter of 5 cubs disappear in less than a month, predated upon lions, hyenas and even another male cheetah.

 

It’s thus clear that cheetahs don’t do as well in areas where they have to compete with larger predators for herd animals. This is major problem for reserves however, which despite succeeding to conserve and protect the animals from negative human affects, fence all of the animals in together,  forcing cheetahs to compete with these larger predators.

Habitat, territory…and weather??

No animal got through evolution without adapting and changing to new environments however, so surely there is something these cheetahs can do to improve their situation? Recent research² from Hunter and colleagues on cheetah kill site selection found evidence that perhaps cheetahs are doing just that – adapting to survive.

“Due to the cheetah’s high-speed hunting strategy, it was long assumed that the species relied on open habitats such as grasslands. However, research showed that woodland vegetation, often assumed to be sub-optimal for cheetahs, increased cub survival, and therefore was suggested to be key in the ultimate survival of the species. Although cheetahs preferred open over closed habitats in previous studies, they used denser habitat for hunting or to reduce kleptoparasitism. Retention of kills was longer and kleptoparasitism rates were lower in thicket vegetation for cheetahs in areas of South Africa under study”²

Based on our sightings capture, we certainly have viewed cheetah on a more regular basis in thicker vegetation then you otherwise would have expected, suggesting compliance with Hunter & Co’s theory.  Saying that, the majority of sightings continue to be in the southern sections of the reserve where it remains a more grassland environment. Don’t discount the cheetah yet though – have another look at the sightings graphs. Although there are presences of predators in the south, it is certainly not a regular hangout for them. Rather, a majority of the predators are found in the middle of the reserve where the perennial Sand River runs though, attracting many a water dependent animal…cue the lions. It seems that the cheetahs share this understanding and that their habitat as a result is determined both by an abundance of prey and lack of other big predators, as opposed to strictly terrain and vegetation.

There is a further positive to this story though and here it is. According to Durant, 2000b³;

“It is possible that low rainfall may benefit cheetahs indirectly because it forces lions, which are water dependent, to remain near water sources, thus restricting their range. Cheetah mothers may therefore be able to avoid lions more easily in years of low rainfall”³

Why point this out, you may ask. Have a look at this next graph, showing average rainfall for our rainfall season (September-April) over the last 10 years:

Rainfall this season has been significantly below that of other years and some say that we are at the beginning of a six-year “dry spell”. Should this be the case, the lions will be further limited on their movements, leaving cheetahs to roam the south in peace, and give the species valuable time to recover their numbers (which at an average litter size of 4, can change quickly!). An added bonus would be an increase in adult females, potentially illuminating the lion vs. cheetah problem all together, as earlier discussed that, “when the number of female cheetahs in the population was high…there was an increase in (cheetah) numbers with lion number”³. So despite our worries for the dry season and its implications many the animals, it may well turn out to be a positive for our cheetah population. Watch this space and our Wildlife Report statistics to see if indeed our cheetahs manage to stage a come back.

Interesting & cited articles

1.     Ancient fossil suggests origin of Cheetahs 

2.     “To Kill, Stay or Flee: The Effects of Lions and Landscape Factors on Habitat and Kill Site Selection of Cheetahs in South Africa” by Susana Rostro-García1, Jan F. Kamler1, Luke T. B. Hunter2. Plos One, April 2014

3.     “Factors affecting life and death in Serengeti cheetahs: environment, age, and sociality” by Sarah Durant, Marcella Kelly and Tim Caro, Oxford Journals, December 2002. 

4.     “Living with the enemy: avoidance of lions and hyenas by cheetahs in the Serengeti” by Sarah Durant, Behavioral Ecology (2000) 11 (6): 624-632.

5.     Cheetah Information pack: http://www.cheetah.co.za/pdf/CheetahInformation.pdf