Does Aphid Infestation Interfere with Indirect Plant Defense against Lepidopteran Caterpillars in Wild Cabbage?

J Chem Ecol DOI 10.1007/s10886-017-0842-z Does Aphid Infestation Interfere with Indirect Plant Defense against Lepidopteran Caterpillars in Wild Cabbage? Yehua Li 1 & Berhane T. Weldegergis 1 & Surachet Chamontri 1 & Marcel Dicke 1 & Rieta Gols 1 Received: 18 January 2017 / Revised: 9 March 2017 / Accepted: 3 April 2017 # The Author(s) 2017. This article is published with open access at Springerlink.com Abstract Attraction of parasitoids to plant volatiles induced by multiple herbivory depends on the specific combinations of attacking herbivore species, especially when their feeding modes activate different defense signalling pathways as has been reported for phloem feeding aphids and tissue feeding caterpillars. We studied the effects of pre-infestation with nonhost aphids (Brevicoryne brassicae) for two different time periods on the ability of two parasitoid species to discriminate between volatiles emitted by plants infested by host caterpillars alone and those emitted by plants infested with host caterpillars plus aphids. Using plants originating from three chemically distinct wild cabbage (Brassica oleracea) populations, Diadegma semiclausum switched preference for dually infested plants to preference for plants infested with Plutella xylostella hosts alone when the duration of pre-aphid infestation doubled from 7 to 14 days. Microplitis mediator, a parasitoid of Mamestra brassicae caterpillars, preferred duallyinfested plants irrespective of aphid-infestation duration. Separation of the volatile blends emitted by plants infested with hosts plus aphids or with hosts only was poor, based on multivariate statistics. However, emission rates of individual compounds were often reduced in plants infested with aphids plus hosts compared to those emitted by plants infested with hosts alone. This effect depended on host caterpillar species and plant population and was little affected by aphid infestation duration. Thus, the interactive effect of aphids and hosts Electronic supplementary material The online version of this article (doi:10.1007/s10886-017-0842-z) contains supplementary material, which is available to authorized users. * Rieta Gols 1 Laboratory of Entomology, Wageningen University, P.O. Box 16, 6700 AA Wageningen, The Netherlands on plant volatile production and parasitoid attraction can be dynamic and parasitoid specific. The characteristics of the multi-component volatile blends that determine parasitoid attraction are too complex to be deduced from simple correlative statistical analyses. Keywords Brassica oleracea . Diadegma semiclausum . Indirect defense . Mamestra brassicae . Microplitis mediator . Multiple herbivory . Natural enemies . Parasitoid behavior . Plutella xylostella . Plant volatiles Introduction Natural enemies of herbivorous insects must find their hosts or prey in habitats that are often structurally and chemically heterogeneous (Meiners 2015; Schoonhoven et al. 2005). Plant volatiles are particularly important during foraging behavior of natural enemies of insect herbivores (Dicke and Baldwin 2010; Hare 2011; Heil 2008). Plant volatiles that are produced in response to herbivory, also referred to as herbivore-induced plant volatiles (HIPVs), can be reliable cues in host-location behaviour by parasitoids of insect herbivores (Mumm and Dicke 2010). Moreover, HIPVs may play an important role in structuring plant-associated insect communities as they mediate multitrophic interactions between plants, herbivores and their carnivorous natural enemies (Dicke and Baldwin 2010; Hare 2011; Poelman et al. 2012; Vet and Dicke 1992). Herbivory by multiple species is the norm in nature. This may affect the induction of HIPVs and as a result the attraction of natural enemies of insect herbivores (De Rijk et al. 2013; Dicke et al. 2009; Ponzio et al. 2013). Reviewing the existing literature, De Rijk et al. (2013) found that when given the choice between volatiles emitted by plants infested with hosts plus non-hosts vs. plants infested with hosts alone, roughly J Chem Ecol 50% of the insect carnivores investigated did not discriminate between the two sources of volatiles, 25% preferred volatiles emitted by plants infested with hosts alone and an equal percentage preferred dually-infested plants. Plant volatile biosynthesis in response to insect herbivory is initiated by a combination of mechanical damage and elicitors from oral secretions of the herbivores (Bonaventure et al. 2011; Dicke 2009; Mumm and Dicke 2010; Turlings et al. 1990). The composition of the HIPV blend depends on the identity of the attacking herbivore and is also highly plant-species specific (Agbogba and Powell 2007; Dicke et al. 2003; Turlings et al. 1998). However, many of the blend components are produced by a wide range of plant species (Mumm and Dicke 2010). Different herbivore species attacking the same host plant may induce subtle differences in volatile profiles, even when the herbivores belong to the same feeding guild (De Moraes et al. 1998; Delphia et al. 2007; Dicke et al. 2003; Turlings et al. 1998). Thus, the effect of multiple herbivory on the behavioral response of parasitoids to HIPVs depends on the specific combination of host and non-host herbivores (De Rijk et al. 2013; Dicke 2009; Erb et al. 2010; RodriguezSaona et al. 2003; Takabayashi et al. 2006; Zhang et al. 2013; Zhang et al. 2009). The production of HIPVs is controlled by different plant signal-transduction pathways regulated by the key phytohormones jasmonic acid (JA) and salicylic acid (SA) (Arimura et al. 2009; Erb et al. 2012; Heil and Ton 2008). Different types of attack often trigger different signalling pathways in the plant (Dicke et al. 2009). Phloem-feeding insect herbivores, such as aphids, mainly activate SA-dependent responses, whereas leaf-chewing herbivores, such as lepidopteran caterpillars, predominantly trigger JA-dependent responses (Moran and Thompson 2001; Thaler et al. 2012; Zarate et al. 2007). When two herbivore species attack the same plant, these two signalling pathways interact through crosstalk (Koornneef and Pieterse 2008; Thaler et al. 2012). The effect of JA-SA crosstalk on HIPV production and parasitoid attraction to plants infested with two different herbivore species has been shown to be variable (De Rijk et al. 2013; Dicke et al. 2009; Engelberth et al. 2001; Howe and Jander 2008; Ponzio et al. 2013). For example, infestation with phloem-feeding whiteflies (Bemisia tabaci) was shown to perturb the JAmediated plant volatile emission and parasitoid attraction in response to leaf-chewing herbivory (Rodriguez-Saona et al. 2003; Zhang et al. 2013). Contrastingly, the parasitoid Cotesia marginiventris showed enhanced attraction to plants simultaneously infested with aphids (Macrosiphum euphorbiae) and caterpillars (Spodoptera exigua), compared to plants only infested with caterpillars (Rodriguez-Saona et al. 2005). The temporal dynamics of induction of the signaltransdu (...truncated)