We are ready to do your bidding, all-powerful caterpillar (Image: Masaru Hojo)

Kill, Fido! Docile ants become aggressive guard dogs after a secret signal from their caterpillar overlord. The idea turns on its head the assumption that the two species exchange favours in an even-handed relationship.

The caterpillars of the Japanese oakblue butterfly (Narathura japonica) grow up wrapped inside leaves on oak trees. To protect themselves against predators like spiders and wasps, they attract ant bodyguards, Pristomyrmex punctatus, with an offering of sugar droplets.


The relationships was thought to be a fair exchange of services in which both parties benefit. But Masaru Hojo from Kobe University in Japan noticed something peculiar: the caterpillars were always attended by the same ant individuals.

“It also seemed that the ants never moved away or returned to their nests,” he says. They seemed to abandon searching for food, and were just standing around guarding the caterpillar.

Flipping the tentacle

Intrigued, Hojo and his colleagues conducted lab experiments in which they allowed some ants to interact with the caterpillars and feed on the secretions, and kept others separate.

Ants that ate the caterpillar’s secretions remained close to the caterpillar. They didn’t return to their nest.

And whenever the caterpillar everted its tentacles – flipped them so they turned inside out – the ants moved around rapidly, acting aggressively.

In the field, Hojo saw the ants attack predatory spiders and wasps, so he thinks the caterpillar responds to predators by ordering ant servants to attack them.

“There are glandular cells near the tentacles that could be secreting chemical signals,” says Hojo. “It is possible that both visual and chemical signals are stimulating the ant aggression.”

Doped up

Back in the lab, ants that had not eaten caterpillar secretions did not react when the tentacles flipped.

So it seems that caterpillars can directly dictate the behaviour of ants, and it’s something in their sugary secretions that makes the ants such obedient servants.

The team found that doped up ants had lower levels of dopamine, a compound shown to affect movement and aggression in insects, than ants that had not eaten the secretions.

To investigate further, the team treated the ants with a drug called reserpine that blocks the transport of dopamine.

Ants that previously reacted to the tentacle eversion by becoming more aggressive, stopped doing so, suggesting that dopamine does indeed play a role.

The chemical cocktail in the caterpillar secretion that affects dopamine levels in the ants is yet to be identified.

Unequal partners?

These findings hint that the ant-caterpillar mutualism, which is similar to relationships found between many other species, could actually be a manipulative parasitic behaviour.

“This is really perspective-changing”, says John Mathew from the Indian Institute of Science Education and Research in Pune. “I’d like to see how it may work across other species hitherto believed to be mutualistic.”

The situation isn’t so clear cut, says Martin Heil of the Center for Research and Advanced Studies of the National Polytechnic Institute in Irapuato, Mexico.

“The benefit for the caterpillar is obvious, but we do not know whether the benefit for the ants is as minimal as the authors argue,” he says. “If the liquid that the caterpillars secrete is sufficiently nutritious, then it might well be that the overall balance for the ants also is positive.”

Journal reference: Current Biology, DOI: 10.1016/j.cub.2015.07.016