Ants Learn Aphid Species as Mutualistic Partners: Is the Learning Behavior Species-Specific?

In ant-aphid associations, many aphid species provide ants with honeydew and are tended by ants, whereas others are never tended and are frequently preyed upon by ants. In these relationships, ants must have the ability to discriminate among aphid species, with mutualistic aphids being accepted as partners rather than prey. Although ants reportedly use cuticular hydrocarbons (CHCs) of aphids to differentiate between mutualistic and non-mutualistic species, it is unclear whether the ability to recognize mutualistic aphid species as partners is innate or involves learning. Therefore, we tested whether aphid recognition by ants depends on learning, and whether the learning behavior is species-specific. When workers of the ant Tetramorium tsushimae had previously tended the cowpea aphid, Aphis craccivora, they were less aggressive toward this species. In addition, ants also reduced their aggressiveness toward another mutualistic aphid species, Aphis fabae, after tending A. craccivora, whereas ants remained aggressive toward the non-mutualistic aphid, Acyrthosiphon pisum, regardless of whether or not they had previous experience in tending A. craccivora. When ants were offered glass dummies treated with CHCs of these aphid species, ants that had tended A. craccivora displayed reduced aggression toward CHCs of A. craccivora and A. fabae. Chemical analyses showed the similarity of the CHC profiles between A. craccivora and A. fabae but not with A. pisum. These results suggest that aphid recognition of ants involves learning, and that the learning behavior may not be species-specific because of the similarity of CHCs between different aphid species with which they form mutualisms.