Ant–aphid interactions on Asclepias syriaca are mediated by plant genotype and caterpillar damage

Abstract

The means by which plant genotypes influence species interactions and arthropod community structure remain poorly understood. One potential, but largely unstudied mechanism is that occurring through plant genetic variation in induced responses to herbivory. Here we test whether induced responses to leaf damage and genotypic variation for induction in Asclepias syriaca influence interactions among Formica podzolica ants, the ant‐tended aphid Aphis asclepiadis, and the untended aphid Myzocallis asclepiadis. In so doing, we assess genetic variation in plant‐mediated interactions among different herbivore guilds. We conducted a three‐way factorial field experiment manipulating plant genotype, leaf damage by specialist monarch caterpillars Danaus plexippus, and ant presence, and documented effects on aphid and ant abundances. Leaf damage increased Aphis abundance in both the presence and absence of ants and Myzocallis abundance under ant exclusion. In the presence of ants, leaf damage decreased Myzocallis abundance, likely due to effects on ant–Myzocallis interactions; ants showed a positive association with Myzocallis, leaf damage increased the strength of this association (425% more ants per aphid), and this in turn fed back to suppress Myzocallis abundance. Yet, these aggregate effects of leaf damage on Myzocallis and ants were underlain by substantial variation among milkweed geno types, with leaf damage inducing lower aphid and ant abundances on some genotypes, but higher abundances on others. As a consequence, a substantial fraction of the variation in leaf damage effects on ants (R2 =0.42) was explained by milkweed genetic variation in the strength and sign of leaf damage effects on Myzocallis. Although plant genetic variation influenced Aphis abundance, this did not translate into genetic variation in ant abundance, and leaf damage did not influence Aphis–ant interactions. Overall, we show that variation in induced responses to herbivory is a relevant condition by which plant genotype influences interactions in plant‐centered arthropod communities and provide novel results of effects on the third trophic level.

Trait plasticity is more important than genetic variation in determining species richness of associated communities

“…By measuring plant functional traits, we showed that trait plasticity was more important than genetic variation in determining species richness of associated communities in a coastal dune ecosystem. Despite the increasing number of genotype‐by‐environment studies in the past decade (Abdala‐Roberts et al, ; Busby, Newcombe, Dirzo, & Whitham, ; Johnson, ; Johnson & Agrawal, ; Mooney & Agrawal, ; Tack, Ovaskainen, Pulkkinen, & Roslin, ; Wagner et al, ), most studies neglect to measure functional traits, precluding an understanding of the relative importance of trait plasticity vs. genetic variation in structuring communities. The few studies that can give insight to the relative importance of trait plasticity vs. genetic variation have been limited to manipulations of soil nutrients within common gardens and focused on the response of plant growth traits and above‐ground arthropod communities (Abdala‐Roberts & Mooney, ; Barrios‐Garcia et al, ; Burkle et al, ; Orians & Fritz, ).…”

Elevational cline in herbivore abundance driven by a monotonic increase in trophic‐level sensitivity to aridity

“…In these interactions, myrmecophilous plants and insects (e.g., aphids) provide ants with carbohydrate‐rich resources in exchange for protection against herbivores (Chamberlain & Holland, ) or predators and parasitoids (Stadler & Dixon, ), respectively. By doing so, ants can alter the abundance, distribution and evolution of their mutualist partners (Abdala‐Roberts et al, ; Olmstead & Wood, ; Pellissier et al, ). Some evidence suggests that ant protection mutualisms are stronger at lower elevations and latitudes (Chamberlain & Holland, ; Koptur, ; Olmstead & Wood, ), and this pattern may be driven by changes in plant quality (first trophic level) or the traits, abundances and community composition of herbivores (second trophic level), natural enemies (third trophic level) or mutualist ants (fourth trophic level) (Chamberlain et al, ; Mooney et al, ; Petry et al, ; Staab.et al, ).…”

Bottom-up effects of host-plant species diversity and top-down effects of ants interactively increase plant performance

“…As a consequence, the factors that mediate ant-aphid interactions can have broad effects themselves. Although there are several studies showing that ant-aphid interactions vary across plant genotypes [26][27][28][29], the effects of plant diversity (both intra-and inter-specific) on this mutualistic interaction remain unstudied.…”