Plant‐mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage

Abstract

ABSTRACT• Plants are part of biodiverse communities and frequently suffer from attack by multiple herbivorous insects. Plant responses to these herbivores are specific for insect feeding guilds: aphids and caterpillars induce different plant phenotypes. Moreover, plants respond differentially to single or dual herbivory, which may cascade into a chain of interactions in terms of resistance to other community members. Whether differential responses to single or dual herbivory have consequences for plant resistance to yet a third herbivore is unknown.• We assessed the effects of single or dual herbivory by Brevicoryne brassicae aphids and/ or Plutella xylostella caterpillars on resistance of plants from three natural populations of wild cabbage to feeding by caterpillars of Mamestra brassicae. We measured plant gene expression and phytohormone concentrations to illustrate mechanisms involved in induced responses.• Performance of both B. brassicae and P. xylostella was reduced when feeding simultaneously with the other herbivore, compared to feeding alone. Gene expression and phytohormone concentrations in plants exposed to dual herbivory were different from those found in plants exposed to herbivory by either insect alone. Plants previously induced by both P. xylostella and B. brassicae negatively affected growth of the subsequently arriving M. brassicae. Furthermore, induced responses varied between wild cabbage populations.• Feeding by multiple herbivores differentially activates plant defences, which has plantmediated negative consequences for a subsequently arriving herbivore. Plant population-specific responses suggest that plant populations adapt to the specific communities of insect herbivores. Our study contributes to the understanding of plant defence plasticity in response to multiple insect attacks.

The timing of leaf damage affects future herbivory in mountain sagebrush (Artemisia tridentata)

“…Changes in plant defensive traits in response to herbivory can affect subsequently arriving herbivores (Kroes et al. , Li et al. ).…”

“…A simple statement of the timing of manipulations or data collection when appropriate could facilitate future meta-analyses or reviews investigating the importance of daily timing in ecological fieldwork. Changes in plant defensive traits in response to herbivory can affect subsequently arriving herbivores (Kroes et al 2016, Li et al 2016. In addition to seasonal timing of herbivory affecting plant-mediated interactions, these results suggest that the daily timing of herbivory may also affect the characteristics of plant response.…”

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

“…This interactive effect may be due to variation in inducibility of traits that mediate indirect insect interactions between the populations of wild B. oleracea plants, such as the foliar concentration of glucosinolates (Gols et al 2008, Newton et al 2009) and the effect size of induced traits on insect community members (Li et al 2014). We speculate that Kimmeridge and Winspit plants differ in SA-JA crosstalk (Kroes et al 2016), which may result from selection by insect communities that differ in the order of herbivore arrival, or presence/absence of keystone species that subsequently affect a cascade of plantmediated interactions (Keith et al 2010, Utsumi et al 2013, Stam et al 2014, Poelman and Kessler 2016. When priority effects on individual plants are consistent across seasons, they may form an important selective regime on plant plasticity in defence as well as induced responses to herbivory (Poelman and Kessler 2016).…”

“…Caterpillar feeding on the plants may have altered the quality of the aphids and affected parasitoid populations through trait mediated effects (Ohgushi 2005). 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).…”

Aboveground herbivory induced jasmonates disproportionately reduce plant reproductive potential by facilitating root nematode infestation

“…Another open question in the field of plant‐mediated interactions between herbivores is how plant‐mediated effects translate into changes in plant fitness (Arce et al, ; Kroes et al, ; X. Li, Li, & Meng, ; Luo et al, ; Pineda, Soler, Pastor, Li, & Dicke, ; Rasmann et al, ; Rodriguez‐Saona, Chalmers, Raj, & Thaler, ; Schöning & Wurst, ). In coyote tobacco, for instance, mirids decrease caterpillar growth, and the fitness penalties of caterpillar attack are reduced when plants are co‐colonized by mirids (Kessler & Baldwin, ).…”