Indirect plant–parasitoid interactions mediated by changes in herbivore physiology

Kaplan, Ian; Carrillo, Juli; Garvey, Michael; Ode, Paul J.

doi:10.1016/j.cois.2016.03.004

Cited by 56 publications

(49 citation statements)

References 79 publications

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“…We have shown previously that there can be species‐specific effects of below‐ground soil microbes on plant associated pests mediated by interference with plant hormonal signalling, resulting in trade‐offs in defence against different types of pests (phloem feeders vs. leaf chewers) or among bacterial pathogens and insect herbivores (Haney et al, ). Others have shown that plant‐associated microbes, both above‐ and belowground, can induce or inhibit direct plant defences (Pieterse et al, ; Simon, Wellham, Aradottir, & Gange, ; Vannette, Hunter, & Rasmann, ), and change plant nutritional quality (Shikano, Rosa, Tan, & Felton, ), with potential cascades to herbivores and parasitoids foraging on these plants (Kaplan, Carrillo, Garvey, & Ode, ). These cascades can occur independent of changes to plant nutritional status (Hempel et al, ), but multiple mechanisms acting in concert likely are at play.…”

Section: Discussionmentioning

confidence: 99%

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

Carrillo

Ingwell

et al. 2019

Journal of Ecology

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Domesticated plants can differ from their wild counterparts in the strength and outcome of species interactions, both above‐ and belowground. Plant–soil feedbacks influence plant success, and plant‐associated soil microbial communities can influence plant interactions with herbivores and their natural enemies, yet, it remains unclear if domestication has changed these relationships. To determine the effects of domestication on plant–soil interactions, we characterized soil microbial communities associated with various cultivars of domesticated tomato and some of its wild relatives. We measured the strength and direction of plant–soil feedbacks for domesticated and wild tomatoes, and the effects of soil on plant resistance to specialist herbivory by Manduca sexta, and the attraction of a parasitoid wasp, Cotesia congregata. Domesticated tomatoes and their wild relatives had negative plant–soil feedbacks, as conspecifics cultivated soil that negatively impacted performance of subsequent plants (longer germination time, lower biomass) than if they grew in non‐tomato soils. Significant variation existed among domesticated and wild tomato varieties in the strength of these feedbacks, ranging from neutral to strongly negative. For above‐ground plant biomass, tomato wild relatives were unaffected by growing in tomato‐conditioned soil, whereas domesticated tomatoes grew smaller in tomato soil, indicating effects of plant domestication. Overall, increased microbial biomass within the rhizosphere resulted in progressively less‐negative plant–soil feedbacks. Plant cultivars had different levels of resistance to herbivory by M. sexta, but this did not depend on plant domestication or soil type. The parasitoid C. congregata was primarily attracted to herbivore damaged plants, independent of plant domestication status, and for these damaged plants, wasps preferred some cultivars over others, and wild plants grown in tomato soil over wild plants grown in non‐tomato soil. Synthesis. These results indicate that crop tomatoes are more likely to show negative plant–soil feedbacks than wild progenitors, which could partially explain their sensitivity to monocultures in agricultural soils. Furthermore, cultivar‐specific variation in the ability to generate soil microbial biomass, independent of domestication status, appears to buffer the negative consequences of sharing the same soil. Last, soil legacies were relatively absent for herbivores, but not for parasitoid wasps, suggesting trophic level specificity in soil feedbacks on plant–insect interactions.

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Section: Discussionmentioning

confidence: 99%

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

Carrillo

Ingwell

et al. 2019

Journal of Ecology

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“…It is known that koinobiont endoparasitoids (such as C. glomerata, C. rubecula and H. ebeninus ) affect physiology and metabolism of their herbivore hosts in ways that benefit the parasitoid offspring (Pennacchio and Strand 2006). Evidence is accumulating that host regulation not only affects the caterpillar host but also extends to the herbivore food plant via alterations of the oral secretions of parasitized caterpillars (Poelman et al 2011; Kaplan et al 2016; Shikano et al 2017; Mason et al 2018). As a conclusion, parasitism can override herbivore identity in terms of plant defense responses and HIPV emission.…”

Section: Discussionmentioning

confidence: 99%

“…The changes in HIPV composition that allow hyperparasitoids to find their hosts are mainly driven by an alteration in the composition of oral secretions of caterpillar hosts as a result of being parasitized (Poelman et al 2011; Shikano et al 2017; Tan et al 2018; Zhu et al 2018), which in turn play a key role in herbivore recognition and plant defense signaling (Bonaventure et al 2011; Bonaventure 2012; Rivera-Vega et al 2017). Interestingly, the specificity of the parasitoid signature is reflected in the physiology of the caterpillar in such a way that each parasitoid species induces a specific effect on herbivore oral secretions and plant responses to herbivory (Poelman et al 2011; Zhu et al 2015; Kaplan et al 2016; Ode et al 2016). As a consequence, HIPVs may convey valuable information that hyperparasitoids can use to assess the identity of the parasitoid host and, possibly, even parasitoid host quality and suitability (Poelman and Kos 2016).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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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.

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“…Understanding the mechanisms involved in plant-herbivore-parasitoid tritrophic interactions (see Kaplan et al, 2016 for a review), and how global warming could impact them is particularly relevant for predicting herbivore pest outbreaks in agricultural systems. Understanding the mechanisms involved in plant-herbivore-parasitoid tritrophic interactions (see Kaplan et al, 2016 for a review), and how global warming could impact them is particularly relevant for predicting herbivore pest outbreaks in agricultural systems.…”

Section: Introductionmentioning

confidence: 99%

Mechanisms structuring host–parasitoid networks in a global warming context: a review

Thierry

Hrček

Lewis

2019

Ecological Entomology

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1. In natural communities, multiple host and parasitoid species are linked to form complex networks of trophic and non-trophic interactions. Understanding how these networks will respond to global warming is of wide relevance for agriculture and conservation.2. This study synthesises the emerging evidence surrounding host-parasitoid networks in the context of global warming. The suite of direct and indirect interaction types within host-parasitoid networks is summarised, as well as their sensitivity to temperature changes. The study also compiles and reviews studies investigating the responses of whole host-parasitoid networks to increasing temperatures or proxy variables. The findings reveal there is limited evidence overall for the prediction that parasitism will be reduced under global warming: approximately equal numbers of studies show elevated and reduced parasitism.3. Increasingly, endosymbiotic bacteria are recognised as influential mediators of host-parasitoid interactions. These endosymbionts can change how individual species respond to global warming, and their effects can cascade to affect whole host-parasitoid networks. The evidence that symbiotic bacteria are likely to affect the response of host-parasitoid networks to global warming is reviewed. Symbionts can protect hosts from their parasitoids or influence thermal tolerance of their host species. Furthermore, the symbionts themselves can be impacted by global warming.4. Finally, the study considers the most promising avenues for future research into the mechanisms structuring host-parasitoid networks in the context of global warming. Alongside the increasing availability of modern molecular methods to document the structure of real, species-rich host-parasitoid networks, the study highlights the utility of manipulative experiments and mathematical models.

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Indirect plant–parasitoid interactions mediated by changes in herbivore physiology

Cited by 56 publications

References 79 publications

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

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

Mechanisms structuring host–parasitoid networks in a global warming context: a review

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