Risky roots and careful herbivores: Sustained herbivory by a root-feeding herbivore attenuates indirect plant defences uri icon

abstract

  • Abstract Aboveground plant tissues produce characteristic blends of volatile compounds in response to insect herbivory. These herbivoreinduced 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. Plant roots also emit HIPVs following herbivory, but our understanding of rootproduced 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. 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. vittatumdamaged 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 HIPVmediated interactions change over time with sustained herbivory. Initially (after 24hr), 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 (7days) 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. 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. A free Plain Language Summary can be found within the Supporting Information of this article.

altmetric score

  • 7.7

author list (cited authors)

  • Grunseich, J. M., Thompson, M. N., Hay, A. A., Gorman, Z., Kolomiets, M. V., Eubanks, M. D., & Helms, A. M.

citation count

  • 23

complete list of authors

  • Grunseich, John M||Thompson, Morgan N||Hay, Allison A||Gorman, Zachary||Kolomiets, Michael V||Eubanks, Micky D||Helms, Anjel M

editor list (cited editors)

  • Holeski, L.

publisher