April 13, 2023

Rickia wasmannii

Rickia wasmannii is a fungus that lives on ants, and when it comes to ants and fungi most people usually think of Ophiocordyceps, i.e. the zombie ant fungus - which was the inspiration for The Last of Us series of video games and TV series. But R. wasmannii is not a killer - instead of zombifying its host and digesting the corpse, this fungus seems to reduce animosity and aggression between ants. First of all, let's take a look at what R. wasmannii actually does on ants. 

Left: Illustration of a Rickia wasmannii thallus, Right top: Uninfected ant, Right bottom: ant infected with R. wasmannii
Pictures from Figure 1 of this paper

Rickia wasmannii belongs to a group of fungi called Laboulbeniales, also known more colloquially as "labouls". These fungi have little holdfasts called haustoria that allows them to cling to the ant's cuticle. They are ectoparasites of insects that attach to their host's external surface and suck their hemolymph (insect's equivalent of blood). So in a way they are rather like ticks or lice (and yes, there are labouls that live on ectoparasitic insects, which one might consider as a bit of poetic justice).

But this fungus seems to do more than just suck the ant's blood, as it causes the infected ants and other ants around them to behave differently. Rickia wasmannii changes the host ant's cuticular hydrocarbon or CHC profile. CHC is essentially an ant's ID profile - they use it to recognise nestmates, tell each other apart, and be alerted to strangers from other nests. But R. wasmannii messes with that, scrambling the infected ants' CHC profile, and making them "smell" differently to uninfected ants.

Scientists wanted to find out how the presence of this fungus affects the way ants interact with each other. The challenge with studying ant behaviour is that when you put two ants together, it is difficult to tell apart whether the ant you are observing is responding to the other ant's chemical profile, or if it is responding to the way the other ant is reacting to them. The only way to get a clear observation is to present the ant with something that it would recognise as a fellow ant, but would not muddle the outcome by reacting to the ant that you are trying to observed

The solution turns out to be freeze-killed ants. Ants that are killed in this manner retain their CHC profile, so other ants would treat them just as another live ant, but obviously a dead ant wouldn't react to a live ant's presence and confound the outcome. In addition to those freeze-killed test subjects, scientists also made ant "dummies" which are essentially blank slates in ant forms that they can imbue with whatever chemical signature they were testing. These "dummies" were made by washing ant corpses in hexane to remove their chemical signature. To ants, these specially treated ant corpses are like faceless mannequin, with no identity - until the scientist imbues them with one, by anointing them with a droplet of cuticular extract from another ant.

When ants were presented with dummies that were smeared with the cuticular extract of ants from a different nest, the ants started biting, dragging, or stinging the dummies, much like how they would respond to a live ant from another nest. But when they were presented with either the corpse of a Rickia-infected ant, or dummies that "smell" like a Rickia-infected ant, they were more relaxed and less likely to get aggro. Furthermore, it's not just that the fungus made other ants act differently, the infected ant itself also starts behaving differently. Infected ants are generally less likely to pick a fight with another ant, but especially when facing other infected ants.

As mentioned previously, R. wasmannii seems to change the ant's CHC profile, but one would think scrambling the host ant's profile would make other ants react more aggressively towards them since ants usually have a "stranger danger" response to ants that "smell" different to their nestmates. But the way that R. wasmannii changes how an ant "smell" seems to have a calming effect, and this comes down to a molecule called n-C23 which is present in higher concentration on the cuticle of all infected ants. When the scientist presented ants with dummies that have been smeared with n-C23 and nothing else, almost all hints of aggressive behaviour ceased.

So by increasing n-C23 concentration in its host's cuticle, R. wasmannii has unlocked a life hack that allows it to not just access all areas in an ant colony, but to spread to other nests as well. In the scientists' study population, about half the colonies they studied had the fungus present, and in some nests, all the ants were infected with R. wasmannii. A testament to the fungus' successful manipulation of ant behaviour.

Furthermore the fungus' presence also affects another, very different parasite which also lives with ants - the caterpillar of blue butterflies. These caterpillars are social parasites that convince worker ants into adopting them into their nest. Once they are settled in, they start demanding food from the worker ants and even feed on the ant's developing broods. But the caterpillars don't seem to survive as long in nests which are already hosting R. wasmannii, and in the field, these two parasites co-occur less commonly than expected based on their respective prevalence, which indicates the caterpillar and the fungus are in competition over ant real estate.

By messing with their identity and making them more chilled out, R. wasmannii can turn an ant colony into a fungus party. But the consequences of that ripple out to other ant colonies too, along with the organisms that regularly take up residency in the homes of ants.

Reference:
Csata, E., Casacci, L. P., Ruther, J., Bernadou, A., Heinze, J., & Markó, B. (2023). Non-lethal fungal infection could reduce aggression towards strangers in ants. Communications Biology, 6: 183.