Ants primarily use chemical communication to identify themselves as members of the colony and to indicate their reproductive status. This system can be exploited by parasites, which imitate the chemicals produced by the ants and thereby gain access to the nest. In the case of the caterpillar of the Maculinea rebeli butterfly (the Mountain Alcon blue), the mimicry is so precise that Myrmica schencki ants that come across a caterpillar will pick it up and bring it back to the nest, as though it was an ant larva. However, Italian and British researchers, led by Francesca Barbero, noticed that once in the ant nest, the caterpillar was no longer treated simply as a larva. The ant queen acted as though the caterpillar was another, rival queen,while the workers behaved as though the intruder was a high-ranking ant. The scientists could find no chemical explanation for this phenomenon, so they looked for other ways the caterpillar might be imitating a queen.
Knowing that Myrmica ants use sound as an alarm signal, the team wondered whether acoustic signals might also account for the way the caterpillars were treated. First they tested whether the caterpillars were also capable of making sound and found that distressed M. rebelicaterpillars make a hissing noise, similar to the sound made by alarmed Myrmica workers. As ants make this hissing sound by rubbing together two parts of their bodies – one part carrying a `plectrum' and the other a `file' – the team suspect that the M. rebeli caterpillars may have similar structures.
Next Barbero and her colleagues decided to find out how the worker and queen ants produce their respective sounds. The scientists used an electron microscope to compare the `plectrum' and the `file' on M. schenckiworkers and queens. These structures – each about half a millimetre long– were substantially different in the two kinds of ant, and when a tiny microphone was introduced into the nest, the sounds made by the queens and the workers were quite distinct, and different from alarm `hissing'. The differences were entirely due to the shapes of the `plectrum' and the `file'. When these sounds were played back to ants in the nest, the noises made by the queen prompted the workers to take up a guard behaviour, whereas the noises made by a worker did not, suggesting that the sounds enable the ants to identify the social status of the insect that produced them.
The next step was to see whether the caterpillars could imitate this sound. The team used the tiny microphones again, this time to record the noises made by M. rebeli caterpillars and pupae. The caterpillars and pupae made similar sounds which the scientists' computers could distinguish from both queen and worker noises, but which were more similar to the sounds made by the queens. So the caterpillars could make sounds, but would they provoke the workers to behave defensively?
Playing back the M. rebeli noises to the worker ants, the noises made by the pupae had the same effect as the queen noises; the workers switched to their guarding behaviour. The caterpillars were able mimic key aspects of M. rebeli communication to successfully parasitize the ants' nest.
It seems likely that this fascinating story is simply the tip of the iceberg. Many other Myrmica ant species are parasitized by other butterfly species. The authors suggest that acoustic communication may be widespread in these ants and that the caterpillars may be taking advantage of this. In a single study, Barbero and her colleagues made two important discoveries: they showed that ants use acoustic signals to communicate social status, and that a social parasite can imitate these signals in order to camouflage itself more effectively. In Darwin's bicentenary year, this study of host–parasite relations is a tremendous example of the power of natural selection, and of the exquisite adaptations shown by parasites in their continuous combat with their hosts.
