Abstract

1. Aboveground plant tissues produce characteristic blends of volatile compounds in response to insect herbivory. These herbivore-induced plant volatiles (HIPVs) function in plant defence and mediate foraging decisions by herbivores and their natural enemies. The ecological roles of HIPVs as foraging cues for different trophic levels highlight an important conflict for herbivores that need to locate suitable host plants while avoiding competition and predation. 

2. Plant roots also emit HIPVs following herbivory, but our understanding of root-produced volatiles and their ecological functions in soil environments remains limited. Moreover, recent studies have documented the effects of temporal dynamics of plant volatile production on ecological interactions, but little is known about how root HIPVs change throughout herbivory or the resulting ecological implications from such changes.  

3. In this study, we examined the roles of HIPVs from roots of cucumber plants (Cucumis sativus) as foraging cues for a specialist herbivore, striped cucumber beetle (Acalymma vittatum) and its natural enemies, entomopathogenic nematodes (EPNs). We predicted HIPVs from A. vittatum-damaged roots would attract EPNs, while repelling conspecific larvae that avoid competition, induced plant defences, and increased risk of predation by EPNs. To capture the temporal dynamics of root HIPVs, we determined how HIPV-mediated interactions change over time with sustained herbivory.  

4. Initially (after 24 h), A. vittatum herbivory on C. sativus, or mechanical wounding, induced greater production of root volatiles. These root HIPVs recruited EPNs and repelled foraging A. vittatum larvae, although larval performance was not affected by prior damage. Sustained (7-day) herbivory by larvae reduced HIPVs to levels indistinguishable from undamaged control roots, while mechanically damaged roots continued to produce higher levels of volatiles. Attenuation of HIPVs impaired indirect defence responses of C. sativus by reducing recruitment of EPNs and deterrence of A. vittatum larvae.  

5. These results suggest that root HIPVs function as honest signals that indicate the presence of herbivores, induction of indirect plant defences, and increased risk of predation by natural enemies. However, some herbivores may overcome this line of plant defence by attenuating production of HIPVs and thus altering the outcomes of subsequent interactions among plants, herbivores, and natural enemies.