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Hyperparasitoids Exploit Herbivore-Induced Plant Volatiles During Host Location to Assess Host Quality and Non-Host Identity

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Hyperparasitoids Exploit Herbivore-Induced Plant Volatiles During Host Location to Assess Host Quality and Non-Host Identity Oecologia (2019) 189:699–709 https://doi.org/10.1007/s00442-019-04352-w PLANT-MICROBE-ANIMAL INTERACTIONS – ORIGINAL RESEARCH Hyperparasitoids exploit herbivore‑induced plant volatiles during host location to assess host quality and non‑host identity Antonino Cusumano1 · Jefrey A. Harvey2,3 · Marcel Dicke1 · Erik H. Poelman1 Received: 12 November 2018 / Accepted: 30 January 2019 / Published online: 5 February 2019 © The Author(s) 2019 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 fnd 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 carni- vores use herbivore-induced plant volatiles (HIPVs) to fnd caterpillars containing parasitoid host larvae. Hyperparasitoids forage in complex environments where hosts of diferent 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 afect the composition of HIPV emission, hyperparasitoids encounter considerable variation in HIPVs during host location. Here, we combined laboratory and feld experiments to investigate the role of HIPVs in host selection of hyperpara- sitoids 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 feld conditions, hyperparasitoid responses were not afected 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 fnd their preferred hosts in heterogeneous environments. Keywords Hyperparasitoid foraging behavior · Non-host parasitoid species · Fourth trophic level organisms · Multitrophic interactions · Plant-based food web Introduction Consumers often forage in heterogeneous environments in Communicated by Richard Karban. which resources of diferent quality are interspersed among other resources that are nutritionally unsuitable. The ef- Electronic supplementary material The online version of this ciency in finding and exploiting nutritionally suitable article (https ://doi.org/10.1007/s0044 2-019-04352 -w) contains supplementary material, which is available to authorized users. resources is crucial for maximizing the consumers’ ftness (Charnov 1976; Pyke 1984). The problem of foraging in * Antonino Cusumano heterogeneous environments is widespread among consum- [email protected] ers structured within food webs; for example, herbivorous 1 Laboratory of Entomology, Department of Plant and carnivorous insects that are part of plant-based food Sciences, Wageningen University, Droevendaalsesteeg 1, webs have to fnd resources which are commonly embedded 6708 PB Wageningen, The Netherlands within larger patches of non-resources (Aartsma et al. 2017, 2 Department of Terrestrial Ecology, Netherlands Institute 2019). Herbivores need to fnd their food plants among a of Ecology (NIOO-KNAW), Droevendaalsesteeg 1, diverse array of non-food plants, whereas carnivores such 6708 PB Wageningen, The Netherlands as parasitoids have to fnd their herbivore hosts and dis- 3 Section Animal Ecology, Department of Ecological criminate between non-infested and infested plants (Bruce Sciences, VU University Amsterdam, De Boelelaan 1085, and Pickett 2011; De Rijk et al. 2013). To orient towards 1081 HV Amsterdam, The Netherlands Vol.:(0123456789)1 3 700 Oecologia (2019) 189:699–709 suitable resources in structurally complex vegetation, her- physiology of the caterpillar in such a way that each parasi- bivorous and carnivorous insects often rely on chemical toid species induces a specifc efect on herbivore oral secre- sources of information among which plant volatiles play a tions and plant responses to herbivory (Poelman et al. 2011; key role (Bruce et al. 2005; Clavijo McCormick et al. 2012; Zhu et al. 2015; Kaplan et al. 2016; Ode et al. 2016). As a Webster and Cardé 2017). Herbivores have been shown to consequence, HIPVs may convey valuable information that exploit specifc ratios of ubiquitous plant volatiles to locate hyperparasitoids can use to assess the identity of the para- host–plant species (Bruce et al. 2005; Webster et al. 2010) sitoid host and, possibly, even parasitoid host quality and whereas parasitoids use plant volatiles induced by herbi- suitability (Poelman and Kos 2016). Yet, how hyperparasi- vore attack (HIPVs) as cues for host location (Mumm and toids forage in complex environments containing hosts and Dicke 2010; Clavijo McCormick et al. 2012; Turlings and non-hosts has not been explored. Erb 2018). In this study, we used a food web based on wild Brassica Plant-based food webs usually go beyond the third trophic oleracea to investigate the foraging behavior of hyperpara- level (Bukovinszky et al. 2008; Harvey et al. 2009; Frago sitoids in a scenario in which hosts of diferent quality and 2016; Sanders et al. 2016; Seibold et al. 2018). Obligate non-host parasitoid species develop in diferent herbivore hyperparasitoids are a common group of insects in the fourth species feeding on neighboring plants (Fig. 1). As focal trophic level which lay their eggs in or on the body of other hyperparasitoid species we used L. nana which is a special- parasitoid hosts. Primary hyperparasitoids develop on para- ist attacking pupae of parasitoids in the genus Cotesia. In sitoid host larvae whereas secondary hyperparasitoids attack cabbage felds of The Netherlands, L. nana mainly attacks parasitoid prepupae or pupae (Sullivan 1987; Sullivan and the gregarious parasitoid Cotesia glomerata and the solitary Volkl 1999). The foraging behavior of hyperparasitoids has parasitoid C. rubecula; both parasitoid species parasitize the received little attention compared to insects in lower trophic co-occurring herbivorous caterpillars Pieris brassicae and levels, such as herbivores and primary parasitoids. Despite P. rapae (Geervliet et al. 1998, 2000). However, the solitary this paucity of information, hyperparasitoids clearly must parasitoid Hyposoter ebeninus can also attack both P. brassi- also deal with several constraints when foraging. For one cae and P. rapae and is locally sympatric with C. glomerata thing, their primary parasitoid hosts are more scarce (and and C. rubecula (Feltwell 1982; Poelman et al. 2014). As thus presumably harder to fnd) than herbivore hosts of pri- H. ebeninus is not a suitable resource for L. nana ofspring mary parasitoids. Moreover, parasitoid host larvae do not development, it can potentially disrupt HIPV exploitation feed on plants and, therefore, they are inconspicuous and and limit the hyperparasitoid’s foraging efciency if no often concealed within the body of their herbivore hosts discrimination between hosts and non-host parasitoids is (Sullivan and Volkl 1999; Brodeur 2000). Additional chal- displayed. Furthermore, the two Cotesia species represent lenges faced by hyperparasitoids include the fact that the hosts of diferent quality for L. nana in terms of maternal same herbivore species may be attacked by several parasitoid ftness investments. In fact, the gregarious C. glomerata is species which difer in host quality and some of them may a high-quality resource because a L. nana female will often not even be suitable for hyperparasitoid ofspring develop- parasitize most of the gregarious brood in sequence during ment (Harvey 2005). Furthermore, the same parasitoid host a single foraging bout. By contrast, the solitary C. rubecula may develop on/in diferent herbivore species. Because of represents a host of lower quality as it allows only a sin- all these challenges, hyperparasitoids clearly need to make gle reproductive opportunity with the consequence that an the best use of all available information when searching for L. nana female has to disperse after attacking a parasitized hosts to optimize their foraging efciency. caterpillar. Previous studies show that the hyperparasitoid Lysibia Plant-mediated discrimination between hosts of diferent nana can use plant volatiles emitted in response to feeding quality and non-host parasitoid species may also be afected by parasitized caterpillars to locate their parasitoid hosts by the herbivore in which parasitoid larvae are developing: and discriminate HIPVs according to the parasitization sta- because the two Pieris species display diferent feeding tus of the caterpillar feeding on the plant (Poelman et al. behavior (P. brassicae caterpillars feed gregariously on the 2012; Zhu et al. 2015). The changes in HIPV composition plants whereas P. rapae caterpillars feed individually), the that allow hyperparasitoids to fnd their hosts are mainly way the parasitized herbivore species interact with the plant driven by an alteration in the composition of oral secretions may difer with consequences for variation in HIPV blends of caterpillar hosts as a result of being parasitized (Poelman and hyperparasitoid foraging behavior (Poelman
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