An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars

Herbivore-induced plant volatiles (HIPVs) can mediate tritrophic interactions by attracting natural enemies of insect herbivores such as predators and parasitoids. Whether HIPVs can also mediate tritrophic interactions by influencing the attractiveness of the herbivores themselves remains unknown. We explored this question by studying the role of indole, a common HIPV in the plant kingdom. We found that herbivory-induced indole increases the recruitment of the solitary endoparasitoid Microplitis rufiventris to maize plants that are induced by Spodoptera littoralis caterpillars. Surprisingly, however, indole reduces parasitoid recruitment when the caterpillars themselves are present on the plants. Further experiments revealed that indole exposure renders S. littoralis caterpillars unattractive to M. rufiventris, leading to an overall reduction in attractiveness of plant-herbivore complexes. Furthermore, indole increases S. littoralis resistance and decreases M. rufiventris parasitization success. S. littoralis caterpillars are repelled by indole in the absence of M. rufiventris but specifically stop avoiding the volatile in the presence of the parasitoid. Our study shows how an HIPV can undermine tritrophic interactions by reducing the suitability and attractiveness of caterpillars to parasitoids.