The Brood Thief

brood (/bru:d/)- noun: the first three stages of life cycle (eggs, larvae, and pupae) in social insects like ants

Manabi Paul stared into the plexiglass arena where she ran her experiments. She was supposed to join the adjoining Dog Lab for her PhD but had decided to spend a month of her mandatory lab rotation course in the Ant Lab to gain experience and because she enjoyed the work. The set-up she had put up to test the outcome of competition between two colonies for a scarce resource, was simple enough- two artificial nests occupied by two distinct colonies, under bright lights to induce stress and placed in two corners of the arena. In the centre was the reward- a new, inviting nest. A part of this nest had already been occupied by one of the colonies while some of the scouts, called leaders, of the other colony had only just discovered it. Some of the ants of this second colony had taken shelter on one side of the arena to escape the immediate stress conditions of their home. Out of the corner of her eyes, Manabi noticed a leader of the first colony stealthily crawling towards this area, unnoticed by the beleaguered members. This intruder extended its antennae this way and that, testing the waters, feeling for danger, for enemies, alerted no doubt by the foreign scent of the second colony. In a corner, she (for all worker ants are female) spotted, through a combination of tactile and visual sensation, an unguarded treasure, a black cylindrical structure. She smelled it too, a scent quite unlike its own colony scent and knew she had hit paydirt. This was the pupa, the enclosure containing a sleeping juvenile ant. In its tiny mind the ant may have felt elation or the thrill of a hunt going well. We can never know but Manabi certainly felt a tinge of excitement run up her spine as the thief picked up the pupa and dashed towards her own nest.

Thievery in animal kingdom is nothing new. This behaviour is so widespread that some animals have developed this way of exploitation into an art form. Take, for example, the fork-tailed drongo that normally acts as a lookout against predators for meerkats and babblers. They produce an alarm call, sort of a “heads up”, on spotting a predator. But on occasions when they are hungry or their naïve charges find a particularly large food item, these apparently “good Samaritans” mimic a false alarm call, that is when no predators are present in the vicinity causing the meerkats and babblers to skedaddle leaving the food behind which the drongo then makes its own. In case the target species is able to see through this tactic, the drongo has a repertoire of 51 different alarm calls to choose from, some of them mimicking the target species’ own alarm calls.

Nowhere is the behaviour of stealing more ubiquitous than in insects (although opinions differ). Honey bees steal food, bumblebees steal nests from birds no less, and wax moths live as a free-loading parasite in honeybee combs. And ants. They steal brood and make slaves. And it is as despotic as it sounds (though there are exceptions as we will soon see). The technical term for such behaviour is “dulosis”, from the Greek word, “doulōsis”, meaning slavery or enslavement and the ants are known as dulotic or slave-making ants. These ants are specialised social parasites, so much so that some of them, like the European Amazon ants are unable to feed themselves or rear their young without the help of their slaves. Almost all of these slave makers will raid interspecific colonies to kidnap the brood – the egg, larvae, and pupae – of the target ant species. These slaves are “indoctrinated” from their larvae-hood (so to speak) through an early chemo-olfaction learning process to recognise the enslaver’s colony as their own and to work for its benefit. In fact, on subsequent raids, these slaves will battle for their dulotic masters against their own conspecifics. A typical raid, although variations exist, begin with scouts, units of solitary ants or in groups of two or three scuttling about on forest floors or grassy knolls in search of an ant colony to invade and prey on. On locating the entrance of a prey nest, these scouts return to their own nests. There they recruit hundreds and thousands of their own nest-mates through a pheromone signal. This raiding party, nay, a behemoth war-machine functioning as one cohesive unit, whipped up into a frenzy by glandular secretions from the scouts or a signaller ant, makes its way to the unfortunate prey nest. Resistance, if any, is futile and the whole prey colony is overwhelmed through sheer number and superior mandibles. Such is the savagery of attacks in some cases that 75% of the adult prey colony is killed immediately post attack and their entire brood stolen. As if to further drive the point of how close it mirrors reality, some of these dulotic ants like the European Amazon ants release a “propaganda” chemical in the prey nest which causes the nest defenders to panic and run away while the workers drop the brood they were carrying to safety only a moment before.

When Manabi reported her observations to her supervisor, Prof. Annagiri was cautious about the findings. After all most of the dulotic ants had been documented predominantly in two subfamilies found in temperate regions – Myrmicinae and Formicinae, where harsh conditions and a lack of resources give rise to such parasitic behaviour. But Dr. Annagiri worked in India, a tropical country and the ant she worked with, Diacamma indicum belonged to neither subfamily.

Diacamma indicum is a eusocial ant, i.e. it has a high level of social organisation, belonging to the family Ponerinae found in northern and southern India, Sri Lanka, and Japan. It is primitively eusocial unlike its more highly eusocial cousins in that it does not have physically distinct reproductive and non-reproductive castes. Furthermore, it does not use chemical trail laying for foraging or relocation, an evolutionary upgrade available to dulotic ants among others. Combined with the fact that the workers of the D. indicum colony are perfectly capable of sustaining it by themselves, the stealing of a conspecific pupa by the ant-thief made Prof. Annagiri and her team realise that they were observing something other than “slave-making”.

By then, Manabi Paul had already left the lab and the experiments passed onto a new recruit, Biswarup Paul (no relation to Manabi). But before he could get down to the experiments, he first had to collect ant-colonies from the field. Biswarup along with Basudeb Ghosh, the field assistant spent days under the sun, hours on end at a time, sitting on haunches, peering through grass and dry leaves and soil looking for nests. They followed stray foraging ants to their nests under the soil, in coconut husks, in tree and tarmac crevices and flushed out the colony with water. These colony members were then collected and brought to the lab where they were color-coded with a combination of enamel paint colors for easier recognition.

Next came the experiment. The experiment Biswarup designed with his supervisor, Prof. Annagiri was simple but ingenious. The day before the experiment, he placed an ant colony housed in an artificial nest in a corner of a sand arena and let the colony familiarise itself to its new surroundings. This became the resident colony. After a gap of twelve hours, they introduced another colony in another random corner of the arena, away from the resident colony. Each such set-up was called a replicate and eight replicates were carried out. The cover of the artificial nest of the new colony was removed. A bright light was placed directly over the new nest causing its residents great discomfort. And so, their scouts dispersed looking for a new haven. Some of the scouts made their way to the center of the arena where Paul had placed an empty artificial nest at the start of the experiment. The scouts elated at having discovered a safer abode started bringing in their other members, one at a time. And some of these members brought their colony’s most precious treasure with them- the brood. Unknown to them, they had been set up for an ambush. But even the would-be attackers did not know about it yet. Ants don’t have great vision so the resident colony was not immediately aware that they were sharing space. Neither was the new colony. It would not be until a resident scout, out and about to find food would randomly stumble upon one of the other nests. Unlike the dulotic ants, this scout would not go back to its own nest to recruit more members but would wait patiently for an opportunity to steal. In transition between two nests, the new colony was spread thin without proper guard over the brood and the opportunistic indicum scouts took full advantage of that by looting whatever they could. The new colonies fought back whenever they detected an intruder presence. They boxed her and chased her and bit her and did whatever they could to protect their brood. Some of the new colony scouts even made incursions into enemy territory occasionally although their attack and success rate were much lower.

“We wants it, we needs it. Must have the precious. MY PRECIOUS!”

An inventory check of the colonies informed the ethologists that pupa had been the predominantly stolen item with a larva being stolen in one single instance. It made sense too. The pupa ecloses as an adult ant. Thus, the colony gains a new worker without any additional effort on their part. The D.indicum ants might have been primitive on the evolutionary scale but they were not primitive in their thieving ways. In a follow-up experiment to ascertain the fate of these kidnapped pupa it was discovered that they were not treated any differently than the colonies’ own pupa and were assimilated into the colony when they eclosed thus further cementing Biswarup’s and Prof. Annagiri’s hypothesis that the ways of the D.indicum were indeed different from those of other slave-making ants and brood stealing in the context of relocation as observed might even be the precursor of organized nest raiding.

Over the years, more research on brood theft has thrown up some interesting observations such as ants who steal, on some level, might be aware of what they are doing. If not by intention, then by action, evidenced by the unnatural speed with which they trundle away after snatching an unguarded brood, about three times faster than their normal speed. The fastest recorded speed during the experiment was about 24 cm/s (23.7, if you want to be exact). Consider the fact that the body length of a D. indicum ant is 1 cm and thus it was running away at a speed of 24 bodylengths per second which makes it faster than a cheetah (which can only manage 16 bodylengths per second)! This behaviour is of course motivated by the presence of foreign ants and the potential chance of being the victim of aggression, if discovered. What’s interesting about this whole phenomenon in D. indicum is the fact that they don’t need to steal. Their tropical habitat has enough resources to feed everyone and nurture larvae in their small colonies, unlike the slave making ants. So, what then is the reason to purloin? Why take the chance of being kicked to Kingdom Come? Are these ants real life counterparts to Gollum, chasing after their Precious, their brood? “They are definitely attracted to brood”, both Biswarup and Prof. Annagiri agree.

Looking back fondly on the initial experiments, Prof. Annagiri considers it to be the fortunate intersection of serendipity and curiosity driven science. But there is so much more to know, so much more to be curious about. Biswarup, who earned his PhD based on his work on brood theft is now back in the lab for a second stint as a postdoc. He wondered if there was something different about the thieves that make them successful. After all, the ant Ectatoma ruidum has members specialised for thieving in nests, characterised by their chemical composition on their cuticles which confuses the nestmate recognition system of foreign nest members. Prof. Annagiri, on her part is more interested in tracing the evolutionary development of the brood stealing behaviour and whether or not their hypothesis of this being a precursor to slave raiding holds water. “The more I know about these ants, the more they amaze me,” she signs off.

References

Brood Theft papers

  1. Paul, B., Paul, M., & Annagiri, S. (2016). Opportunistic brood theft in the context of colony relocation in an Indian queenless ant. Scientific reports, 6(1), 1-10
  2. Paul, B., & Annagiri, S. (2018). Tricks of the trade: Mechanism of brood theft in an ant. Plos one, 13(2), e0192144.
  3. Paul, B., & Annagiri, S. (2019). Caught red-handed: behaviour of brood thieves in an Indian ant. Journal of Experimental Biology, 222(2), jeb193755.

Other relevant papers

4. LaPolla, J. S., Mueller, U. G., Seid, M., & Cover, S. P. (2002). Predation by the army ant Neivamyrmex rugulosus on the fungus-growing ant Trachymyrmex arizonensis. Insectes Sociaux, 49(3), 251-256.

5. Visicchio, R., Mori, A., Grasso, D. A., Castracani, C., & Le Moli, F. (2001). Glandular sources of recruitment, trail, and propaganda semiochemicals in the slave-making ant Polyergus rufescens. Ethology Ecology & Evolution, 13(4), 361-372.

6. Breed, M. D., Cook, C., & Krasnec, M. O. (2012). Cleptobiosis in social insects. Psyche, 2012.

7. Flower, T. (2011). Fork-tailed drongos use deceptive mimicked alarm calls to steal food. Proceedings of the Royal Society B: Biological Sciences, 278(1711), 1548-1555.

8. Flower, T. P., Gribble, M., & Ridley, A. R. (2014). Deception by flexible alarm mimicry in an African bird. Science, 344(6183), 513-516.

9. Jablonski, P. G., Cho, H. J., Song, S. R., Kang, C. K., & Lee, S. I. (2013). Warning signals confer advantage to prey in competition with predators: bumblebees steal nests from insectivorous birds. Behavioral Ecology and Sociobiology, 67(8), 1259-1267

10. Alloway, T. M. (1979). Raiding behaviour of two species of slave-making ants, Harpagoxenus americanus (Emery) and Leptothorax duloticus Wesson (Hymenoptera: Formicidae). Animal Behaviour, 27, 202-210.

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