Condo-style living helps keep the peace inside these ant plants

Odd plants from a remote Pacific island reveal new insights into an important ecological question: how unrelated and antagonistic partners can form long-term mutualistic relationships with the same host.

Scientists studying ant plants in Fiji have discovered one way that a host plant can keep the peace among residents that might otherwise kill each other. By providing separate chambers inside a gradually enlarging tuber -- each chamber with an entry hole from the outside but no connection to any adjacent chamber -- the Squamellaria plant prevents conflicts between the multiple ant species that feed it and call it home. The new research from Washington University in St. Louis and Durham University in the United Kingdom is reported July 10 in Science.

“Our study shows that compartmentalization is one solution,” said Guillaume Chomicki, of Durham, first author of the study. “The importance of compartmentalization is clear from the deadly conflicts sparked when the partition between distinct ant species living in adjacent compartments is removed.

“But it’s not for the good of the ants that these plants have evolved those compartments — no, it’s for their own good. Because the more ants that live inside a tuber, the more nutrients for the plant,” he said.

“Dried Squamellaria tubers — and similar tubers, many of which have been sitting in herbaria or natural history collections since at least the 1880s — never yielded the insights Guillaume was able to gain in the field,” said Susanne S. Renner, a biologist in Arts & Sciences at WashU, senior author of the study. “One needs two things: Seeing and identifying the ants, and then understanding that the tubers contain entirely separate compartments with separate entrances to the outside, just like a condo building.”

In biology, a symbiotic relationship, or symbiosis, is a close and long-term interaction between two different species. When this relationship is mutually beneficial, it is called a mutualism. Many symbioses involve one host species having several mutualist partners. Yet theory predicts that unrelated partners can lead to destabilizing conflict through competition for host resources.

In the case of Squamellaria, Chomicki and Renner previously had reported on how certain specialized ants actively farm Squamellaria — by planting its seeds and fertilizing the seedlings with their feces — and then nesting in the domatia (hollow chambers) that form on each plant shortly after the unfolding of its cotyledons. Only after the ants insert a seed into a crevice in bark can Squamellaria begin to germinate.

The farming activity is essential to the plant’s survival, as it is an epiphyte that grows on the branches of rainforest trees and has no other way get established in the rainforest canopy. Back in 2014, during a field excursion high in the treetops of Waisali Rainforest Reserve, Chomicki pulled down a Squamellaria that revealed an even more complex set of interactions.  

“When I dissected this plant (Squamellaria wilkinsonii), which had a domatium that was about 8 inches in diameter, I was very surprised to see two ant colonies living inside it,” he said. “My immediate thought was parabiosis, a specific type of symbiotic association where two species of ants nest together. But the nests were completely separate, which was puzzling.” 

That observation was the impetus for his new study with Renner. Together, they describe a series of experiments designed to investigate how the plant enables more than one species of ants to live inside its hollow chambers — starting by observing what happens when the interior walls come down.

“Removing the partition walls between two ‘apartments’ using a dissecting knife — thereby placing in direct physical contact different ant colonies — led to an immediate conflict in which workers fight to the death,” Chomicki said.  

The scientists quantified the number of conflicts between ant workers of the relevant ant species during a 25-minute window following the removal of the partition walls. They documented high worker mortality in both ant colonies that were previously living in separate compartments.

The new study included feeding experiments that documented that the plants were getting nutritional benefits from the multiple ant species living inside their compartments. The study also made use of computed-tomography scanning, a method that only rarely has been applied to plants. “The scanning was key in the discovery of compartmentalization of the domatia,” Renner said. “Simply by dissecting domatia, it is impossible to work out which chambers are connected to which and which is isolated. This discovery came when building 3D models from the CT scanning data.”

The results reveal a conflict-reduction mechanism that allows the hosts to take advantage of multiple, unrelated symbionts, Renner and Chomicki said.

“What is unique in Squamellaria is that we can visualize directly what theory has long predicted — that unrelated partners would conflict by competing for host resources,” Renner said.  “But here we also have a simple, highly effective evolutionary strategy to mitigate these conflicts: compartmentalization. So, despite being unique, these Squamellaria-ant symbioses illuminate an old, general problem in the ecology and evolution of species interactions.”