Volatile-mediated foraging behaviour of three parasitoid species under conditions of dual insect herbivore attack

Ponzio, Camille; Cascone, Pasquale; Cusumano, Antonino; Weldegergis, Berhane T.; Fatouros, Nina E.; Guerrieri, Emilio; Dicke, Marcel; Gols, Rieta

doi:10.1016/j.anbehav.2015.10.024

Cited by 60 publications

(75 citation statements)

References 51 publications

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“…Aphid performance on caterpillar-induced plants may be poorer than on plants where aphids feed alone (Kroes et al 2016, but see Soler et al 2012) and may have resulted in smaller aphids that are less frequently parasitized by parasitoids (Bukovinszky et al 2008). Moreover, caterpillar presence may hamper host location by aphid parasitoids (Ponzio et al 2016). The outcome of herbivore-herbivore interactions as well as interactions with higher trophic levels may be herbivore density dependent (Ponzio et al 2016, Pineda et al 2017).…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, caterpillar presence may hamper host location by aphid parasitoids (Ponzio et al 2016). The outcome of herbivore-herbivore interactions as well as interactions with higher trophic levels may be herbivore density dependent (Ponzio et al 2016, Pineda et al 2017). In the second year, when plants flowered, infestation of the leaves with herbivores had consequences for the flower-associated community, but were weak and short term for the leaf-associated community.…”

Section: Discussionmentioning

confidence: 99%

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Order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development

Stam

Dicke

Poelman

2018

Oikos

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In plant–arthropod associations, the first herbivores to colonise a plant may directly or indirectly affect community assembly on that particular plant. Whether the order of arrival of different arthropod species further modulates community assembly and affects plant fitness remains unclear. Using wild Brassica oleracea plants in the field, we manipulated the order of arrival of early‐season herbivores that belong to different feeding guilds, namely the aphid Brevicoryne brassicae and caterpillars of Plutella xylostella. We investigated the effect of herbivore identity and order of arrival on community assembly on two B. oleracea plant populations during two growth seasons. For this perennial plant, we evaluated whether foliar herbivory also affected herbivore communities on the flowers and if these interactions affected plant seed production. Aphid infestation caused an increase in parasitoid abundance, but caterpillars modulated these effects, depending on the order of herbivore infestation and plant population. In the second growth season, when plants flowered, the order of infestation of leaves with aphids and caterpillars more strongly affected abundance of herbivores feeding on the flowers than those feeding on leaves. Infestation with caterpillars followed by aphids caused an increase in flower‐feeding herbivores compared to the reversed order of infestation in one plant population, whereas the opposite effects were observed for the other plant population. The impact on plant seed set in the first reproductive year was limited. Our work shows that the identity and arrival order of early season herbivores may have long‐term consequences for community composition on individual plants and that these patterns may vary among plant populations. We discuss how these community processes may affect plant fitness and speculate on the implications for evolution of plant defences.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development

Stam

Dicke

Poelman

2018

Oikos

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“…When we manipulated single and dual-guild herbivory in our open-field experiments, we found that foliar concentrations of gluconapin were reduced by 30% in B. oleracea plants fed upon by both caterpillars and aphids rather than aphids alone (Fig. Indeed, recent greenhouse work in this system has shown that both the glucosinolate profile (Ponzio et al 2017), and the volatile chemical profile (Ponzio et al 2016) are distinct in single and dual infestations of aphids and caterpillars. A hydrolyzed volatile product of gluconapin, 3-butenyl isothiocyanate, is innately attractive to dominant aphid parasitoid species at our sites, D. rapae (Blande et al 2007, Pope et al 2008.…”

Section: Discussionmentioning

confidence: 81%

Dual‐guild herbivory disrupts predator‐prey interactions in the field

Blubaugh

Asplund

Eigenbrode

et al. 2018

Ecology

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Plant defenses often mediate whether competing chewing and sucking herbivores indirectly benefit or harm one another. Dual-guild herbivory also can muddle plant signals used by specialist natural enemies to locate prey, further complicating the net impact of herbivore-herbivore interactions in naturally diverse settings. While dual-guild herbivore communities are common in nature, consequences for top-down processes are unclear, as chemically mediated tri-trophic interactions are rarely evaluated in field environments. Combining observational and experimental approaches in the open field, we test a prediction that chewing herbivores interfere with top-down suppression of phloem feeders on Brassica oleracea across broad landscapes. In a two-year survey of 52 working farm sites, we found that parasitoid and aphid densities on broccoli plants positively correlated at farms where aphids and caterpillars rarely co-occurred, but this relationship disappeared at farms where caterpillars commonly co-occurred. In a follow-up experiment, we compared single and dual-guild herbivore communities at four local farm sites and found that caterpillars (P. rapae) caused a 30% reduction in aphid parasitism (primarily by Diaeretiella rapae), and increased aphid colony (Brevicoryne brassicae) growth at some sites. Notably, in the absence of predators, caterpillars indirectly suppressed, rather than enhanced, aphid growth. Amid considerable ecological noise, our study reveals a pattern of apparent commensalism: herbivore-herbivore facilitation via relaxed top-down suppression. This work suggests that enemy-mediated apparent commensalism may override constraints to growth induced by competing herbivores in field environments, and emphasizes the value of placing chemically mediated interactions within their broader environmental and community contexts.

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“…For instance, interference by B. brassicae aphids with induced defenses against caterpillars depends on the density of the attacking aphids (Kroes et al 2015; Ponzio et al 2016). As a next step in the study of density-dependent interference of aphids with caterpillar-induced defenses, we studied the effect of different aphid densities on whole-genome transcriptional responses of A. thaliana to feeding by P. xylostella caterpillars.…”

Section: Discussionmentioning

confidence: 99%

Brevicoryne brassicae aphids interfere with transcriptome responses of Arabidopsis thaliana to feeding by Plutella xylostella caterpillars in a density-dependent manner

et al. 2016

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Plants are commonly attacked by multiple herbivorous species. Yet, little is known about transcriptional patterns underlying plant responses to multiple insect attackers feeding simultaneously. Here, we assessed transcriptomic responses of Arabidopsis thaliana plants to simultaneous feeding by Plutella xylostella caterpillars and Brevicoryne brassicae aphids in comparison to plants infested by P. xylostella caterpillars alone, using microarray analysis. We particularly investigated how aphid feeding interferes with the transcriptomic response to P. xylostella caterpillars and whether this interference is dependent on aphid density and time since aphid attack. Various JA-responsive genes were up-regulated in response to feeding by P. xylostella caterpillars. The additional presence of aphids, both at low and high densities, clearly affected the transcriptional plant response to caterpillars. Interestingly, some important modulators of plant defense signalling, including WRKY transcription factor genes and ABA-dependent genes, were differentially induced in response to simultaneous aphid feeding at low or high density compared with responses to P. xylostella caterpillars feeding alone. Furthermore, aphids affected the P. xylostella-induced transcriptomic response in a density-dependent manner, which caused an acceleration in plant response against dual insect attack at high aphid density compared to dual insect attack at low aphid density. In conclusion, our study provides evidence that aphids influence the caterpillar-induced transcriptional response of A. thaliana in a density-dependent manner. It highlights the importance of addressing insect density to understand how plant responses to single attackers interfere with responses to other attackers and thus underlines the importance of the dynamics of transcriptional plant responses to multiple herbivory.Electronic supplementary materialThe online version of this article (doi:10.1007/s00442-016-3758-3) contains supplementary material, which is available to authorized users.

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Volatile-mediated foraging behaviour of three parasitoid species under conditions of dual insect herbivore attack

Cited by 60 publications

References 51 publications

Order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development

Order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development

Dual‐guild herbivory disrupts predator‐prey interactions in the field

Brevicoryne brassicae aphids interfere with transcriptome responses of Arabidopsis thaliana to feeding by Plutella xylostella caterpillars in a density-dependent manner

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