A root-feeding herbivore suppresses indirect plant defenses to avoid elevated predation risk.
It has been well documented that herbivore feeding damage triggers the production of herbivore-induced plant volatiles (HIPVs), which can protect plants directly by repelling herbivores or indirectly by recruiting natural enemies that kill herbivores. However, our understanding of root-produced HIPVs and their ecological functions in soil environments remains limited. We investigated the role of HIPVs from roots of cucumber plants (Cucumis sativus) in mediating foraging decisions of entomopathogenic nematodes (Heterorhabditis bacteriophora; EPNs) and how these volatiles change over the course of herbivory. We found that feeding damage by cucumber beetle larvae (Acalymma vittatum) and mechanical wounding induced similar blends volatiles in C. sativus roots after 24 hr, compared to undamaged control plants. However, after 7 days of continuous damage, A. vittatum herbivory suppressed root volatile production, while mechanical wounding continued to induce higher production of volatiles. Furthermore, we found that EPNs were attracted to cucumber root HIPVs after 24 hr of damage, but after 7 days of herbivory EPNs did not differentiate between herbivore-damaged and control plants. Taken together our results indicate that HIPVs from C. sativus roots serve as indirect defenses against A. vittatum larvae by recruiting EPNs, and that A. vittatum larvae can overcome these defenses by suppressing HIPVs.