A blog post highlighting the article written by D.C. Cardoso, M.P. Cristiano, C.B. da Costa-Milanez and  J. Heinze in Insectes Sociaux

Written by Aniek Ivens

Sometimes a chance encounter leads to a new scientific discovery. Let me tell you the story of four biologists in Brazil who were looking for fungus-growing ants and then discovered that these ants’ fungus gardens got stolen by other ants: thief ants. This discovery is more than just a fun fact; below you’ll find how it may contribute to a better understanding of the farming practices of ants, which are cases of mutualism and how these mutualisms persist despite the threat of parasites.

Our historical transition from a hunter-gatherer to a farming-based lifestyle contributed significantly to our success as a species.

We humans weren’t the only beneficiaries when we transitioned to farming. The crops and animals that we keep and farm also benefited from this interaction. For example, in some countries there are at the moment more pigs than humans. It is hard to imagine that such vast numbers of pigs could be maintained in the wild without human assistance⁴. These reciprocally beneficial cooperative relationships between the farmers and the farmed species are called ‘mutualisms.’

Given the mutual benefits to farmers and the species they farm, it is not surprising that we are not the only organisms that practice agriculture or husbandry. Nature provides many examples of such non-human farming: there are ants that farm aphids as we do cattle, damselfish that grow little gardens of algae in the sea, and even amoebae that farm bacteria. Perhaps the most frequently grown crop out there is fungus: we find ‘mushroom growers’ among termites, beetles, sloths, snails, and, of course, ants.

Figure 1: A worker of fungus-growing ant Trachymyrmex intermedius carries a leaf to the nest as substrate for its fungus. Photo: Alex Wild (www.alexanderwild.com)

Fungus-growing ants are sophisticated farmers. They build subterranean nests in which they grow gardens of fungi, for food. To grow the fungus they bring in substrate from outside the nest, often flowers or cut leaves (Fig. 1). They also maintain the garden by applying their excrement as manure and planting new tufts of fungus.

The ants and fungi together form thriving little communities from which they both profit. Unfortunately, their success also puts them at risk: any thriving mutualism will attract parasites that reap the benefits without paying the costs. Yet, many mutualisms persist and how they defend themselves against these parasites is a major question in biology. Studying the interactions between mutualists and their parasites can shed light on this question.

It is no surprise that the ants’ fungus-garden risks parasite invasion. We’ve long known that ants need to actively weed out and even apply pesticide to parasitic fungi, which try to profit from the ants’ care without providing food. In recent years, it has become clear that the fungus-gardens also risk ‘agro-predation’, in which other ants come in and steal the entire garden⁵. This is of course a major loss – imagine you have carefully planted a patch of strawberries and once they are ripe, somebody comes in and steals all of them!

In the study highlighted here, the biologists discovered by chance that this is exactly what happens to Mycetophylax (My) fungus-growing ants. The biologists set out to collect some colonies of My ants from sand dunes near Ilhéus, Brazil. However, in one case, they found that the fungus-garden was inhabited by a different ant, Megalomyrmex incisus (Me) (Fig. 2). No Mycetophylax ants were in sight. Knowing that other Me can be agro-predators⁵, or ‘thief ants’, they hypothesized that this nest indeed had been usurped by the Me ants and brought it to the lab to test this hypothesis.

Figure 2: Thief ant Megalomyrmex incises seen from the front (‘frontal view’, a) and its left side (‘lateral view’, b). Photo: Cardoso et al. 2016

The researchers first confirmed that the found Me ants were parasitic ants, by testing whether these ants were able to rear the fungus garden themselves. As it turns out, the Me ants could not. Although they ate the fungus, they did not provide the fungus with substrate and did not weed it. As a result, the fungus died within three weeks.

Next, the scientists gave the thief Me ants the opportunity to steal a fungus, by providing the colony with a piece of fungus garden including about 20 workers of its original farmers, the My ants. Turns out that raiding a fungus garden is indeed what the Me ants are very good at: within an hour, they had taken possession of the garden and expelled all My ants by employing an arsenal of aggressive weaponry. The thieves bite, sting and pull the My ants (see video below). Presumably in response to the venom the Me ants produce⁶, the My ants mostly play dead – and the thief ants just carry them off their garden.

Why didn’t the My ants, the mutualists, evolve to protect their garden better? The reason is probably the same as the reason why nobody observed this case of agro-predation before: the chance of these Me ants encountering a My colony is just extremely low. This is because Me ants are rare and the habitats of these two different types of ants hardly overlap. Evolution is only able to shape better defenses when an attack happens often enough.

Even though it only happens rarely, this case of agro-predation by Me ants can still be very valuable for science. Combined with other known cases of garden-stealing by Me ants^5,7,8, it will allow us to study the strategies of parasites – and their victims’ defenses against them – in more detail. Ultimately this will contribute to a better understanding of the fragile balance between mutualists and parasites and how best to protect mutualist crops (and maybe even our own) from being stolen by other species.

References

1. Cardoso, D. C., Cristiano, M. P., Costa-Milanez, C. B. da & Heinze, J. Agro-predation by Megalomyrmex ants on Mycetophylax fungus-growing ants. Insectes Sociaux 63, 483–486 (2016).
2. Larsen, C. S. Biological changes in human populations with agriculture. Annu. Rev. Anthropol. 24, 185–213 (1995).
3. Diamond, J. Evolution, consequences and future of plant and animal domestication. Nature 418, 700–707 (2002).
4. Aanen, D. K. As you weed, so shall you reap: on the origin of algaculture in damselfish. BMC Biol. 8, 81 (2010).
5. Adams, R. M. M., Norden, B., Mueller, U. G. & Schultz, T. R. Agro-predation: usurpation of attine fungus gardens by Megalomyrmex ants. Naturwissenschaften 87, 549–554 (2000).
6. Adams, R. M. M., Jones, T. H., Longino, J. T., Weatherford, R. G. & Mueller, U. G. Alkaloid venom weaponry of three Megalomyrmex thief ants and the behavioral response of Cyphomyrmex costatus host ants. J. Chem. Ecol. 41, 373–385 (2015).
7. Adams, R. M. M. et al. Chemically armed mercenary ants protect fungus-farming societies. Proc. Natl. Acad. Sci. 110, 15752–15757 (2013).
8. Adams, R. M. M., Shah, K., Antonov, L. D. & Mueller, U. G. Fitness consequences of nest infiltration by the mutualist-exploiter Megalomyrmex adamsae. Ecol. Entomol. 37, 453–462 (2012).