In response to herbivory, plants emit volatile compounds that play important roles in plant defense. Herbivore-induced plant volatiles (HIPVs) can deter herbivores, recruit natural enemies, and warn other plants of possible herbivore attack. Following HIPV detection, neighboring plants often respond by enhancing their anti-herbivore defenses, but a recent study found that herbivores can manipulate HIPV-interplant communication for their own benefit and suppress defenses in neighboring plants. Herbivores induce species-specific blends of HIPVs and how these different blends affect the specificity of plant defense responses remains unclear. Here we assessed how HIPVs from zucchini plants (Cucurbita pepo) challenged with different herbivore species affect resistance in neighboring plants. Volatile “emitter” plants were damaged by one of three herbivore species: saltmarsh caterpillars (Estigmene acrea), squash bugs (Anasa tristis), or striped cucumber beetles (Acalymma vittatum), or were left as undamaged controls. Neighboring “receiver” plants were exposed to HIPVs or control volatiles and then challenged by the associated herbivore species. As measures of plant resistance, we quantified herbivore feeding damage and defense-related phytohormones in receivers. We found that the three herbivore species induced different HIPV blends from squash plants. HIPVs induced by saltmarsh caterpillars suppressed defenses in receivers, leading to greater herbivory and lower defense induction compared to controls. In contrast, HIPVs induced by cucumber beetles and squash bugs did not affect plant resistance to subsequent herbivory in receivers. Our study shows that herbivore species identity affects volatile-mediated interplant communication in zucchini, revealing a new example of herbivore defense suppression through volatile cues.

Plants attacked by insects may induce defenses locally in attacked plant tissues and/or systemically in non-attacked tissues, such as aboveground herbivory affecting belowground roots or belowground herbivory modifying aboveground tissues (i.e., cross-compartment systemic defense). Through induced systemic plant defenses, above-and belowground insect herbivores indirectly interact when feeding on a shared host plant. However, determining the systemic effects of herbivory on cross-compartment plant tissues and cascading consequences for herbivore communities remains underexplored. The goal of this study was to determine how belowground striped cucumber beetle (Acalymma vittatum) larval herbivory alters aboveground zucchini squash (Cucurbita pepo subsp. pepo) defenses and interactions with herbivores, including adult cucumber beetles and squash bugs (Anasa tristis). To explore this question, field and laboratory experiments were conducted to compare responses of aboveground herbivores to belowground larvae-damaged plants and non-damaged control plants. We also characterized changes in defensive chemicals and nutritional content of aboveground plant structures following belowground herbivory. We discovered belowground herbivory enhanced aboveground plant resistance and deterred aboveground foraging herbivores. We also found that larvae-damaged plants emitted higher amounts of a key volatile compound, (E)-β-ocimene, compared to non-damaged controls. Further investigation suggests that other mechanisms, such as plant nutrient content, may additionally contribute to aboveground herbivore foraging decisions. Collectively, our findings underscore connections between above-and belowground herbivore communities as mediated through induced systemic defenses of a shared host plant. Specifically, these findings indicate that belowground larval herbivory systemically enhances plant defenses and deters a suite of aboveground herbivores, suggesting larvae may manipulate aboveground plant defenses for their own benefit, while plants may benefit from enhanced systemic defenses against multi-herbivore attack.