Hyperparasitoids exploit herbivore-induced plant volatiles during host location to assess host quality and non-host identity

Abstract

Although consumers often rely on chemical information to optimize their foraging strategies, it is poorly understood how top carnivores above the third trophic level find resources in heterogeneous environments. Hyperparasitoids are a common group of organisms in the fourth trophic level that lay their eggs in or on the body of other parasitoid hosts. Such top carnivores use herbivore-induced plant volatiles (HIPVs) to find caterpillars containing parasitoid host larvae. Hyperparasitoids forage in complex environments where hosts of different quality may be present alongside non-host parasitoid species, each of which can develop in multiple herbivore species. Because both the identity of the herbivore species and its parasitization status can affect the composition of HIPV emission, hyperparasitoids encounter considerable variation in HIPVs during host location. Here, we combined laboratory and field experiments to investigate the role of HIPVs in host selection of hyperparasitoids that search for hosts in a multi-parasitoid multi-herbivore context. In a wild Brassica oleracea-based food web, the hyperparasitoid Lysibia nana preferred HIPVs emitted in response to caterpillars parasitized by the gregarious host Cotesia glomerata over the non-host Hyposoter ebeninus. However, no plant-mediated discrimination occurred between the solitary host C. rubecula and the non-host H. ebeninus. Under both laboratory and field conditions, hyperparasitoid responses were not affected by the herbivore species (Pieris brassicae or P. rapae) in which the three primary parasitoid species developed. Our study shows that HIPVs are an important source of information within multitrophic interaction networks allowing hyperparasitoids to find their preferred hosts in heterogeneous environments.Electronic supplementary materialThe online version of this article (10.1007/s00442-019-04352-w) contains supplementary material, which is available to authorized users.

Volatiles of bacteria associated with parasitoid habitats elicit distinct olfactory responses in an aphid parasitoid and its hyperparasitoid

“…elicited a significant attractive response in the hyperparasitoid. Hence, this suggests that the olfactory response of primary and secondary parasitoids towards mVOCs is different, as has also been found for HIPVs (Cusumano et al, ; Poelman et al, ).…”

“…Furthermore, little is known about whether and how mVOCs mediate insect behaviour across trophic levels. Previous studies on plant–insect interactions have shown that herbivore‐induced plant volatiles (HIPVs) are an important source of information mediating multitrophic interactions (Dicke & Baldwin, ; van Oudenhove, Mailleret, & Fauvergue, ), not only attracting primary parasitoids but also mediating the behavioural response of secondary parasitoids (also referred to as ‘hyperparasitoids’ having primary parasitoids as their host; Cusumano, Harvey, Dicke, & Poelman, ; Poelman et al, ). Virtually nothing is known so far on the role of microbial volatiles in the chemical ecology of hyperparasitoids.…”

Short-term Thermal Changes Affect Parasitism on Asian Chestnut Gall Wasp

“…However, the higher presence of Eupelmus spp. could also be linked to variations in emissions of herbivore-induced plant volatiles in response to thermal stress [78].…”

Exploiting chemical ecology to manage hyperparasitoids in biological control of arthropod pests

“…The chemical composition of the HIPV blend changes according to the parasitism status of the attacking herbivore, allowing hyperparasitoids to locate their hosts. Interestingly, HIPV attraction of L. nana occurs regardless of the host caterpillars in which C. glomerata parasitoid larvae develop ( Pieris brassicae or P. rapae ), showing that the parasitoid signature overrules herbivore identity in this system . Lysibia nana and also Pteromalus semotus are attracted to HIPVs induced by parasitized caterpillars on different cabbage cultivars and both hyperparasitoids preferred cultivars that also are more attractive to their primary parasitoid host C. glomerata …”

“…More recently, increasing attention has been paid to life‐history traits of hyperparasitoids that affect hyperparasitoid reproduction and hence fitness, such as development and host‐feeding . Progress has also been made in understanding hyperparasitoid behavior, in particular host‐ and mate‐finding, which are mainly guided by chemical cues (infochemicals) . The idea of manipulating hyperparasitoids to enhance biological control was put forward more than two decades ago, but recent progress in chemical ecology makes it possible now to develop truly eco‐friendly pest control, including strategies for managing hyperparasitoids.…”