Modification of plant‐induced responses by an insect ecosystem engineer influences the colonization behaviour of subsequent shelter‐users

Abstract

Summary 1.Herbivores that modify plant morphology, such as gall-forming insects, can disproportionately impact arthropod community on their host plants by providing novel habitats and shelters from biotic and abiotic stresses. These ecosystem engineers could also modify plant chemical properties, but how such changes in plant quality affect the behaviour of subsequent colonizers has rarely been investigated. 2. We explored how an initial infestation of the tall goldenrod (Solidago altissima) by an ecosystem engineer, the rosette gall-midge (Rhopalomyia solidaginis), affects colonization behaviour of a shelter-using beetle (Microrhopala vittata) through plant-induced responses in the field. 3. Beetles preferentially colonized plants with galls and exhibited a clumped distribution on those plants, which suggested a possible advantage for aggregating on galled plants. Accordingly, we found that beetles remained longer on galled plants with previous beetle damage than those without beetle damage. No such effect of beetle damage was found on plants without a gall. Similar interactions between galler infestation and beetle damage were found in beetle's feeding choice, leaf diterpene and serine protease inhibitor production, and volatile organic compound (VOC) emission. These plant metabolic induction and herbivore response patterns indicated that the gall-midge can alter how plants respond to the beetle damage and that gall presence coupled with beetle damage improves leaf palatability for the beetle. Finally, we found reciprocal effects of beetles on gall-midge performance to be neutral to slightly positive, suggesting that the observed field association of the two herbivores could be formed by plant-mediated facilitation. 4. Synthesis. Our study suggests that an ecosystem engineer could have significant impact on herbivore community not only by changing plant morphology, but also by altering host quality and modifying plant-induced responses to subsequent herbivory. As such, R. solidaginis also functions as a keystone herbivore that has disproportionate effects on community dynamics and composition meditated by induced plant growth and metabolic responses.

Insect community structure covaries with host plant chemistry but is not affected by prior herbivory

“…), and have been shown to occur in both herbaceous and woody species (Gonzalez‐Megias and Gomez , Ohgushi , Uesugi et al. ). The indirect plant‐mediated interactions can have unexpected consequences for plant fitness, if they result in increased or decreased resistance toward more harmful herbivores (Kessler and Baldwin , McArt et al.…”

“…The changes in plant physiology caused by one herbivore species can influence the quality and quantity of the plant as a food source for other species. Such plantmediated indirect interactions can occur between herbivore species that are temporally separated (Van Zandt and Agrawal 2004, Poelman et al 2008, Hernandez-Cumplido et al 2016, or attack different parts of the same host plant (McArt et al 2013, Arce et al 2017, and have been shown to occur in both herbaceous and woody species (Gonzalez-Megias and Gomez 2003, Ohgushi 2005, Uesugi et al 2016. The indirect plantmediated interactions can have unexpected consequences for plant fitness, if they result in increased or decreased resistance toward more harmful herbivores (Kessler and Baldwin 2004, McArt et al 2013, Machado et al 2018, or disruption of important mutualistic interactions (Kessler et al 2011).…”

The Galling Truth: Limited Knowledge of Gall-Associated Volatiles in Multitrophic Interactions

“…(2) Mirroring research on externally feeding herbivores, where HIPVs have been investigated from the egg-laying stage ( Hilker and Fatouros, 2015 ), comparable information is needed in galler–plant–parasitoid/inquiline interactions including stages such as tissue damage by ovipositor probing, egg laying, damage by larval mandibles, and finally gall induction. (3) Metabolic plasticity can occur in host-plant–galler interactions vis-a-vis different gallers and plant genotypes ( Uesugi et al, 2013 , 2016 ), resulting in varied responses that must, therefore, be interpreted within the context of the specific interactants. (4) We need to understand correlation networks of VOCs produced by plants under a variety of circumstances.…”

“…In S. altissima attacked by the rosette gall-midge Rhopalomyia solidaginis , emissions of terpenes such as copaene and β-pinene increased post-galling ( Uesugi et al, 2016 ); these attracted herbivorous beetles whose presence facilitated galler performance, suggesting that VOC emission patterns must be viewed in an integrated manner.…”

Why do entomologists and plant pathologists approach trophic relationships so differently? Identifying biological distinctions to foster synthesis

“…A consequence of directed behavior is that individual insects can actively choose not only particular plant genotypes, but also plants experiencing a particular physiological circumstance, age or habitat (Janz et al, 2005;Knolhoff & Heckel, 2014). For example, individuals of various insect species specifically search for individuals within the host species range that are under drought stress or are well hydrated (Carr et al, 1998;Kolb et al, 2016), are previously damaged by abiotic or biotic agents, or, conversely, host individuals that are undamaged (Roininen et al, 1997;Powell et al, 2012;Uesugi et al, 2016), or are of a particular age category (Kearsley & Whitham, 1989). Furthermore, insects may prefer plants that, by chance, are located on a site that provides higher nutritional quality or, conversely, may avoid plants that harbor predators (Stamp & Bowers, 2000) or are near other plant species that emit volatile repellents (Barbosa et al, 2009).…”