Effects of arbuscular mycorrhizal fungi on above‐ground tri‐trophic interactions are contingent upon plant genetic effects of cross type in the perennial herb Ruellia nudiflora

Abstract

Abstract Recent work has improved our understanding of the linkages between above‐ and below‐ground interactions mediated by plants. However, relatively few of the studies conducted thus far have focused on multi‐trophic interactions (i.e. beyond two trophic levels) and the influence of plant genetic intraspecific variation on these dynamics has rarely been addressed. We tested the effect of arbuscular mycorrhizal fungi (AMF) on above‐ground tri‐trophic interactions associated with the canopy of the perennial herb Ruellia nudiflora, and further determined whether genetic effects due to cross type (i.e. whether a plant originated from self‐ or cross‐pollination) influenced these interactions. We propagated plants originating from self‐ or cross‐pollination, and within each category inoculated half of the plants with AMF. We subsequently established a common garden where plants were exposed to naturally occurring seed‐eating caterpillars and their parasitoids. We measured plant growth, fruit output, calculated the proportion of attacked fruits by the caterpillar and the proportion of parasitized caterpillars, and also estimated the proportion of “rescued” seeds by parasitoids representing an indirect positive effect of the third trophic level on the plant by reducing caterpillar consumption. Arbuscular mycorrhizal fungi drove 18% and 15% increases in plant growth and fruit output respectively, and drove a 25% reduction in caterpillar fruit attack, but did not influence parasitism or parasitoid seed “rescue.” In contrast, cross type did not influence growth, fruit number, herbivore attack, parasitism or seed rescue. More importantly, however, we found a significant AMF by cross type interaction on caterpillar attack, where AMF significantly reduced fruit attack (by 30%) in progeny from cross‐pollination but did not influence herbivory in progeny from self‐pollination. Synthesis. Results indicate that effects of arbuscular mycorrhizal fungi on above‐ground interactions are contingent upon plant intraspecific variation originating from cross type, which is likely a common source of variation in associated interactions for plants with mixed mating systems. Further studies examining plant‐mediated below‐ and above‐ground interactions should consider the influence of specific sources of plant genetic variation, as well as address the consequences of such dynamics for interactions beyond two trophic levels.