Insect herbivory induces plant volatile emissions to a greater extent aboveground than belowground, but both depend on plant-herbivore coexistence history

Following insect herbivory, plants emit a blend of chemical compounds known as herbivore-induced plant volatiles (HIPVs). HIPVs provide direct protection to plants by repelling subsequent herbivores and indirectly defend plants by recruiting predatory insects to kill herbivores. Plants emit ecologically important HIPVs from both aboveground leaves and belowground roots, but whether closely related plants species differ in their aboveground or belowground HIPV emission remains uncharacterized. Here, we examined how foliar and root HIPVs differ within and among closely related plant species and tested the relevance of shared coexistence histories with herbivores in shaping interspecific patterns of HIPV emissions. We predicted greater differences in foliar and root HIPVs would be observed between plant species than within species. To explore this question, we selected six plant species in the gourd family (Cucurbitaceae) that differed in their coexistence histories with specialist insect herbivores. For each of the cucurbit species, we collected and characterized foliar volatiles from non-damaged controls and plants damaged by squash bugs (Anasa tristis). In separate experiments for each cucurbit species, we collected and characterized root volatiles from non-damaged controls and plants damaged by striped cucumber beetle larvae (Acalymma vittatum). We confirmed herbivory induced quantitative and qualitative changes in volatiles both aboveground and belowground, and we discovered that foliar and root volatile diversity varied with coexistence histories with herbivores. Overall, this work advances our understanding on the diversity of HIPVs produced by specific plant tissues aboveground and belowground and also sheds light on evolutionary forces shaping HIPVs.