Farmer termites bury invaders alive to protect fungus farms

Termites are often perceived as nightmares in human habitats, devouring wooden structures and ravaging crops and trees. But within their own homes, some of these farmer termites have sneaky tricks up their sleeves for pest control. The pests in question here are an unwelcome variety of fungi that infiltrate the termite nest mounds.

Seemingly innocuous and tiny, termites that farm beneficial fungus (Odontotermes obesus) in their nest mounds, have a pretty disquieting practice to defending their fungal farms from invasion of weedy, parasitic fungi (Pseudoxylaria). Researchers at Indian Institute of Science, Bengaluru, have documented that these blind insects sniff out the infiltrant in their mounds and selectively bury them alive.

This behaviour reported by Renee Borges’s lab at the institute also has implications for agricultural practices.

“Fungus-farming termites grow a fungus, Termitomyces, in carbon dioxide-rich environments of their nest mounds. In order to maintain a sustainable supply of cultivated fungi, termites must control weedy parasitic fungi and make sure that such fungi do not grow inside their nests,” Borges told Mongabay-India.

The live burial creates an oxygen deficient environment locally (hypoxia) in the vicinity of the parasitic fungus which affects survival of the parasitic fungus. “The burying behaviour, directed primarily at the parasitic weed, is coupled with antifungal activity which, in part, appears to be due to the effect of local hypoxic conditions,” the study said.

Several fungus-growing termite species build mounds, or termitaria, that are conspicuous features of African and Asian landscapes. Odontotermes obesus, belonging to the Macrotermitinae subfamily, is a major mound building termite found across the India subcontinent.

Odontotermes obesus build castle-shaped, buttressed mounds that are up to several metres in height.

Mound-building Macrotermitinae termites are major ecosystem engineers in the tropics and subtropics and maintain fungal gardens of Termitomyces, in controlled temperature and humidity conditions in their massive nest mounds, which are like organised greenhouses.

 These farming systems (also seen in farming ants) have evolved over millions of years and they are sustainable monocultures. The fungus is farmed on termite faecal matter, deposited in the form of a fungus comb inside their nest mounds.

The termites offer a protected environment for the Termitomyces fungus to thrive while in turn, the fungus is an important food resource for the insects. Essentially, the wood-eating termites “outsource” lignin (component of wood) breakdown to the farmed fungus.

Interestingly, healthy fungal gardens of farmer termites are devoid of the weedy fungus Pseudoxylaria.

“It is amazing how natural colonies of fungus-growing termites seem to be able to control Pseudoxylaria: we have done many experiments with fungus gardens. In the absence of termites, very quickly those are completely overgrown with Pseudoxylaria, just in a few days,” observed Duur Aanen, evolutionary geneticist at the Netherlands’ Wageningen University

Aanen, who was not associated with the study said: “From the number of combs that get infected, we infer that there is a very high frequency of those fungi present, probably as spores of tiny mycelia. Nevertheless, in the presence of the termites, those fungi are never seen, so apparently the termites suppress them.”

When the weedy fungus invades termite mounds, they take advantage of the same carbon sources and grow faster than the crop fungi, thereby competing with Termitomyces (crop fungi) for nutrition, said Borges. Therefore, as soon as the termites sniff out the presence of the weedy fungus, they act to nip the problem in the bud.

“In our previous study we had shown that worker termites can smell fungi and solely based on fungal scents, they can differentiate between the crop and weedy fungi. They are very sensitive to the fungus so even a few strands of Pseudoxylaria is enough to spur them to act and bury the fungus alive,” Borges explained.

In a matter of minutes, it is game over for the weedy parasitic fungus.

“The termites make a ball of soil, carry it in their mandible and round it up with saliva and dump the ball on the parasitic mass. This behaviour of termites to bury live fungi is in contrast to humans who bury dead bodies,” Borges said.

This also explains why Pseudoxylaria grows within the termite mound environment only in the absence of contact with termites. For example, in mounds abandoned by termites or when incubated within termite-proof enclosures within active mounds that allow circulation of mound air, said Borges.

“These studies very clearly show that like human farmers, fungus-farming termites have developed methods to control crop weeds and to protect their crops from parasitic attack. They do so both by targeted application of weed control treatments such as weed burial and fungicide application,” she said.

Aanen observed that the present study explores if selective burial can be a factor contributing to this suppression and demonstrates that it can. 

“Of course, those are in vitro experiments, so it remains to be seen how significant this is. Anyone who has worked with fungi and who had a contamination in a strain will be able to testify how difficult it is to control, let alone to get rid of a contamination. So it is not easy to see how termites would do this by selective burial. However, of course, they are many and they are small, so it could work,” Aanen said.

Dumping soil to deal with invaders

While chemical antifungal compounds have been reported in termite farms, live burial per se as an antifungal activity has never been investigated. To probe this dimension, the researchers carried out laboratory experiments using a locally prevalent fungus-farming termite, Odontotermes obesus, as their model system.

They offered farmer termites miniscule amounts of fungi in small petri-dishes filled with garden soil. When the researchers arrived in their laboratory next morning, they found that worker termites had buried the weedy fungus with soil completely. “We also noticed that the weedy fungus had been buried to a greater extent than the crop fungus,” Borges said.

However, what surprised the researchers the most, were the results of their next investigation. “We found that this live burial of fungi by worker termites led to greater decrease in the survival of the weedy fungus compared to the crop fungus, even after controlling for the varying amount of soil deposition,” Borges observed.

But was this decline in weed survival due to localised lack of oxygen (hypoxia) generated by the burial process?

To answer this, the researchers designed an artificial burial experiment. They mimicked the termite behaviour of burying the fungi by covering the fungi in small enclosures. This enabled the researchers to look at the effect of hypoxia alone on the fungal survival.

Their experiments with artificial burial revealed that, in the absence of chemical factors such as fungicides, weed survival is indeed negatively affected by the resulting hypoxia alone.

“Our results show that fungus-growing termites bury the weedy Pseudoxylaria to a significantly greater extent than the Termitomyces crop which results in relatively lowered survival of the former compared to the latter,” the study said.

In fact, any Pseudoxylaria sprouting inside a termite mound will experience hypoxia not only due to burying but also because of the hypoxic surroundings, since mounds are known to have high (but variable) ambient carbon dioxide levels.

Aanen said it remains to be demonstrated if selective burial is sufficient. It seems likely that, in addition, there are additional mechanisms, such as chemical control.

“We cannot rule out the additional presence of antifungal chemicals in the burial materials. It is also possible that antibiotic-producing bacteria and their products are deposited along with soil on the weedy fungi. Thus, further studies using soil deposited by termite workers to isolate antifungal compounds are warranted and are underway,” Borges said.

CITATION:
Katariya, L., Ramesh, P. B., & Borges, R. M. (2018). Dynamic environments of fungus‐farming termite mounds exert growth‐modulating effects on fungal crop parasites. Environmental microbiology, 20(3), 971-979.

Katariya, L., Ramesh, P. B., Gopalappa, T., Desireddy, S., Bessière, J. M., & Borges, R. M. (2017). Fungus-farming termites selectively bury weedy fungi that smell different from crop fungi. Journal of chemical ecology, 43(10), 986-995.

Banner image: Agar bolus (rounded mass) deposition by worker termites in lab assays. Photo by Renee M. Borges et al.