Competition Mediating the Outcome of a Mutualism: Protective Services of Ants as a Limiting Resource for Membracids

Although competition for mutualists is known to be an influential force in plant-animal interactions, its importance in animal-animal associations is largely unexplored. Here, we demonstrate that phloem-feeding membracids (Publilia modesta) compete intraspecifically for the protective services of an ant mutualist (Formica altipetens). By experimentally increasing membracid densities in the field, we observed three negative effects due to competition for ants: (1) a 45%-59% reduction in the number of ants tending membracid aggregations, (2) a 63% increase in the abundance of a predatory salticid spider (Pellenes sp.), and (3) a 59% reduction in the mean number of membracid nymphs per plant. In total, the loss of protective services due to competition for mutualists translated into a 92% decrease in the production of newly eclosed membracid adults. These findings provide the first experimental demonstration that animal species compete for mutualists. In addition, our work indicates that mutualisms can be strongly influenced by the local biotic neighborhoods in which they occur and thus may be far more variable than previously thought.