Whose Phenotype is it Anyway? The Complex Role of Species Interactions and Resource Availability in Determining Plant Defense Phenotype and Community Consequences.

Abstract

The expression of plant defense is influenced by resource availability and biotic interactions, with consequences for herbivores and plant fitness. While the majority of plants associate with mycorrhizal fungi, which dramatically affect plant resource status, the role of these belowground interactions in shaping the expression of plant defense is poorly understood. In addition, plant-herbivore interactions affect plant growth and defense, but their effects on mycorrhizal interactions can vary dramatically. I hypothesized that changes in plant resource status and subsequent defense expression may mediate the interactions between mycorrhizal fungi and aboveground herbivores. Drawing from current knowledge of resource mutualisms, I hypothesized that the carbon costs and nutrient benefits of hosting mycorrhizal fungi would predict a nonlinear effect of mycorrhizae on the expression of plant defense. An experimental manipulation of the abundance and identity of mycorrhizal fungi associating with Asclepias syriaca revealed mycorrhizal colonization nonlinearly affected the expression of plant defense, although the shape of the response to increasing fungal colonization depended on the plant trait examined. In particular, traits (eg. trichomes, plant biomass) that increased with the concentration of phosphorus responded unimodally to mycorrhizal colonization as predicted, while those traits that were putatively carbon-limited (eg. latex and toughness) declined with fungal colonization. I also manipulated carbon available to plants and examined changes in plant defense and the effects of herbivores on mycorrhizal fungi. Growth under elevated CO2 increased plant biomass by 15% and toughness by 40%, but decreased cardenolide concentration by 20% and had little effect on trichome density. Herbivory by either aphids or caterpillars had no effect on mycorrhizal colonization when plants were grown in ambient CO2, but herbivory dramatically increased mycorrhizal colonization under elevated CO2. Taken together, these results indicate that fungi and aboveground herbivores interact through changes in plant resource status and defense phenotype and exert strong influence on the expression of plant defense phenotype. In addition, these experiments revealed substantial genetic variation within a single population of A. syriaca in the expression of plant defense and in response to mycorrhizal colonization and carbon addition, indicating the potential for evolutionary adaptation to changing environmental conditions.