Intra- and interspecific plant quality effects on an ant-aphid mutualism
Variation in plant traits has important consequences for herbivore performance. While plant quality can directly affect the distribution and occurrence of herbivores, traits can also interact with higher trophic levels to indirectly modify these effects. Aphids live in close association with plants and are susceptible to small differences in plant quality, while also being exposed to a diversity of threats such as predators, parasitoids, and fungal pathogens. To maximize their survival, a considerable fraction of aphid species have independently evolved mutualisms with ants that provide colony defense and health maintenance in exchange for honeydew excretions. Tended and untended aphid species differ in their honeydew composition, indicating that tending behavior of ants is mediated by specific honeydew characteristics and quality. Furthermore, within a tended aphid species the net effect of ant-aphid interactions is dependent on host plant genotype, varying from mutualistic to antagonistic. Here, we tested the effect of inter- and intraspecific host plant variation on the milkweed aphid Aphis asclepiadis and its interaction with the ant Formica podzolica in a field experiment. Using ten genotypes each of two natural hosts of the aphid, common milkweed Asclepias syriaca and dogbane Apocynum cannabinum, we manipulated ant access and measured aphid performance.
Ant tending in the field had no overall effect on aphid population densities, but varied according to genotype. On milkweed, aphids on five genotypes benefited from ant tending, while aphids on the remaining genotypes performed better in the absence of ants. On dogbane, aphids reached smaller population sizes and plant effects were less pronounced, but ant tending effects still varied from positive to negative on different genotypes. Ant recruitment to aphid populations was driven by aphid number, but recruitment was stronger to dogbane than to milkweed, resulting in equal ant visitation at lower aphid densities. While there was no genotype effect on recruitment to dogbane, recruitment of ants to milkweed differed according to genotypes, ranging from positive to negative association between aphid number and ant visitation. Importantly, none of these effects were driven by the per-capita amount of exuded honeydew, thus we will next measure qualitative differences in honeydew composition. In conclusion, plant genotypes are important factors in establishing mutualistic interactions between aphids and ants, most likely by directly determining the quality of honeydew that is exuded by aphids.