Arbuscular mycorrhizal fungi mediate herbivore‐induction of plant defenses differently above and belowground

Abstract

Plants are exposed to herbivores and symbionts above and below ground. Herbivores above ground alter plant defenses in both leaves and roots, affecting plant–herbivore interactions above and below ground. Root symbionts, such as arbuscular mycorrhizal fungi (AMF), also influence the defenses of leaves and roots, and alter plant responses to herbivory. However, we lack an understanding of how AMF mediate plant responses to herbivores simultaneously in above and belowground plant tissues, despite the ubiquity of such interactions and their consequences for ecological communities. In a full factorial experiment, we subjected plants of four milkweed (Asclepias) species under three levels of AMF inoculum availability to damage by aphids Aphis nerii, caterpillars Danaus plexippus, or no herbivores. We then measured foliar and root cardenolides (chemical defenses), leaf toughness, latex exudation (physical defenses), foliar carbon, nitrogen, and phosphorous concentrations, plant biomass, and levels of AMF colonization of roots.Plants inoculated with AMF generally produced tougher leaves with higher cardenolide concentrations than did plants without AMF. In contrast, root cardenolides were altered by AMF inoculum availability in a plant species‐specific manner. The relative induction or suppression of foliar cardenolides and leaf toughness by herbivores was altered strongly by the level of AMF inoculum available to plants. However, AMF did not influence caterpillar‐induction or aphid‐suppression of root cardenolides. In addition, herbivore feeding induced substantial changes in levels of AMF colonization of roots in a plant species‐specific manner. We demonstrate that the availability of AMF in soil alters herbivore induction and suppression of plant defenses strongly, and does so differently in above and belowground plant tissues. Furthermore, we show that herbivore feeding alters levels of AMF colonization substantially, completing a feedback loop between above‐ and belowground organisms. Our study suggests that indirect interactions between AMF and herbivores may have community‐wide consequences by altering plant phenotype above and below ground.