Patterns and mechanisms of the exploitation of mutualisms

Abstract

Mutualisms are reciprocally exploitative interactions providing net benefits to both partners. These interactions can be exploited, in turn, by individuals that take advantage of benefits offered by one or both partners in a mutualism, while offering no benefits in return. For many mutualist-exploiter interactions the mechanisms allowing exploitation, and the maintenance of mutualisms in the face of exploitation, are still poorly understood. Here I describe manipulative field and laboratory experiments to investigate the mechanisms used by an exploiter to invade an ant-plant mutualism. I tested two non-mutually exclusive hypotheses for how a coreid (Mozena sp., Hemiptera: Coreidae) feeds on mymecophytic acacia trees (Vachellia spp.) while avoiding attack by resident ants: chemical defense and chemical mimicry. I found that chemical compounds produced by Mozena sp. in both the metathoracic gland and the cuticle reduced the number of ant attacks and cuticular compounds appeared to be essential in escaping recognition on ant-occupied Vachellia spp. trees. The compounds were effective on multiple colonies and for multiple ant species, thus they are not strictly host- or species-specific. In addition, gas chromatography and mass spectrometry analyses of cuticular compounds revealed a close match between chemical profiles of Mozena sp. and Pseudomyrmex spinicola ants, suggesting chemical mimicry is the primary mechanism by which Mozena sp. exploits the ant-acacia mutualism. To examine the prevalence of a cost of exploitation for plant partners in exploited mutualisms, I conducted a meta-analysis of studies from the published literature. I found that exploitation has a weak, negative, but insignificant impact on the reproductive success of mutualistic plants. Collectively, these analyses illuminated methods by which exploiters may succeed in infiltrating mutualisms and suggested that the relatively low costs of exploitation may account for the lack of destabilization and degradation by exploiters of some mutualistic interactions.