Acute toxicity of the plant volatile indole depends on herbivore specialization

Abstract

Herbivore-induced plant volatiles (HIPVs) provide direct benefits to plants as antimicrobials and herbivore repellents, but their potential as direct toxins to herbivores is unclear. Here we assayed the larvicidal activity of six common HIPVs from three different biochemical pathways and tested the hypothesis that the larvicidal activity of HIPVs is related to the host specialization of the insect pest. We first assessed {beta}-caryophyllene, linalool, z-3-hexenyl acetate, z-3-hexenol, e-2-hexenol, and indole against the beet armyworm (Spodoptera exigua), and found that indole was 7-fold more toxic compared to the other volatiles when incorporated into diet. Then, we tested the larvicidal activity of indole against six common, destructive pest caterpillars with varying host ranges. Consistent with our hypothesis, indole toxicity varied with caterpillar host range: indole toxicity was seven-fold higher in more specialized insect species relative to generalist insect species. That said, the LC50 of indole was comparable to other reported anti-herbivore agents even against the generalist caterpillars. Yet, indole in headspace had neither larvicidal nor ovicidal activity on any caterpillar species tested. These results support a key ecological precept regarding tradeoffs between host specialization and chemical detoxification, and also indicate that indole functions as a direct defense against herbivores that could be potentially useful in integrated pest management strategies.\n\nKey messageO_LIWe measured the direct toxicity of six common HIPVs against the beet armyworm.\nC_LIO_LIIndole was the most toxic HIPV against the beet armyworm.\nC_LIO_LIWe determined the toxicity of indole against six different pest caterpillar species.\nC_LIO_LIToxicity of indole was associated with the host preference of the insect species.\nC_LIO_LIIndole exposure in headspace had no effect on egg hatching or caterpillar survival.\nC_LIO_LIIndole has the potential to be developed as an insecticide against crop pests.\nC_LI\n\nAuthor Contribution StatementCJF and AKM designed research. AKM and RCP conducted experiments. AKM and CJF analyzed data and wrote the manuscript. All authors read and approved the manuscript.