Belowground symbioses with plants, such as arbuscular mycorrhizal fungi (AMF), can have far-reaching effects on aboveground species interactions. By altering plant nutrient uptake and interacting with plant signaling pathways, AMF can alter both the nutritive quality of plants and plant defensive traits, thus affecting herbivore performance. We investigated how root colonization by a community of ubiquitous AMF species influences plant constitutive and herbivore-induced defensive traits and herbivore performance in four North American milkweed species (Asclepias incarnata, A. curassavica, A. latifolia, A. syriaca). In a fully factorial manipulation of plant species, level of AMF colonization, and herbivore species, we subjected plants to feeding by aphids (Aphis nerii), monarch caterpillars (Danaus plexippus), or no herbivores. We assessed herbivore performance and concurrently measured defensive traits of herbivore-damaged and control plants. We hypothesized that a) AMF increase constitutive and herbivore-induced plant defenses, but the magnitude of the effect varies among plant species and extent of AMF colonization. b) AMF-mediated changes in plant phenotype influence differentially the performance of herbivores from different feeding guilds.
Plant defensive traits are influenced, but not always increased, by AMF colonization. The manner in which AMF affect these traits is context-dependent, varying among plant species, extent of AMF colonization of roots, and herbivore feeding guilds. Specifically, AMF colonization increased constitutive cardenolide concentrations (primary chemical defense) across plant species. However, level of AMF colonization differentially affected the amount of latex exuded by plants (physical defense) among plant species. In response to aphid feeding, but not caterpillar damage, cardenolide concentrations were induced or reduced only in highly AMF colonized plants and varied in a plant species-specific manner. Both aphid and caterpillar feeding induced similar changes in latex exudation, but the pattern of induction of latex exudation with increasing AMF colonization varied among plant species. Across all plant species, aphids had the highest per capita growth rates and masses on highly AMF colonized plants and lowest on plants colonized by low amounts of AMF. In contrast, caterpillar growth rates were unaffected by level of AMF colonization. Our findings demonstrate that AMF colonization can have substantial effects on plant defenses and herbivore performance and highlight the context-dependent nature of the impacts of AMF on plant-herbivore interactions.