Indirect interactions in communities occur when ecological interactions between two species depend upon the presence of a third, mediating species. When the third species undergoes phenotypic changes brought about by the first species, the outcome of indirect effects can change. This can be seen in the facultative mutualism between aphids and ants within a host-parasitoid community. In ant-aphid mutualisms, aphids provide a honeydew food source for ants, and ants provide protection of aphids from predators and parasitoids. This mutualism creates an indirect interaction between ant-tended aphids and parasitoids by reducing rates of parasitism on susceptible aphid species in the community. The mutualism, however, can switch to exploitation in which ants eat aphids; this can occur when ants have an excess supply of sugar relative to protein food sources (e.g. when aphid densities are very high). Using a model for an ant species, two aphid species – one tended and one not – and a parasitoid wasp, I investigated how the role of ants along the continuum between mutualists and exploiters affects the aphid-parasitoid interaction, and the ultimate role of ants for the dynamics of this four-species system.
As the ant species switches from mutualist to exploiter of aphids, its interaction with the parasitoid remains one of competition: as mutualists they can remove non-tended aphids from vulnerability to parasitoid attack, and as exploiters they are direct competitors of the parasitoid. Nonetheless, the consequences for aphids are large, with exploitation leading to much lower densities of aphids than mutualism, as aphids are subjected to both predation by ants and parasitism. This combined effect of ant predation and unprotected parasitism can lead to rapid aphid population collapse if aphid densities become high enough to change ants into exploiters. Most of the literature on indirect effects has focused strictly on predator-prey interactions. The results from this study illustrate how indirect effects can act through mutualisms as well.