Eavesdropping on gall–plant interactions: the importance of the signaling function of induced volatiles

Abstract

The galling insect manipulates the host plant tissue to its own benefit, building the gall structure where it spends during most of its life cycle. These specialist herbivore insects can induce and manipulate plant structure and metabolism throughout gall development and may affect plant volatile emission. Consequently, volatile emission from altered metabolism contribute to eavesdropping cueing. Eavesdropping can be part of adaptive strategies used by evolution for both galling insects and the entire-associated community in order to cue some interaction response. This is in contrast to some herbivores associated with delayed induced responses, altering plant metabolites during the short time while they feed. Due to the different lifestyles of the galling organism, which are associated with different plant tissues and organs (e.g leaves, flowers or fruits), a distinct diversity of organisms may eavesdrop on induced volatiles interacting with the galls. Furthermore, the eavesdropping cues may be defined according to the phenological coupling between galling organism and host plant, which results from the development of a gall structure. For instance, when plants release volatile-induced defenses after galling insects' activity, another interactor may perceive these volatiles and change its behavior and interactions with host plants and galls. Thus, natural enemies could be attracted by different volatiles emitted by the gall tissues. Considering the duration of the life cycle of the galling organism and the gall, the temporal extent of gall-induced volatiles may include more persistent volatile cues and eavesdropping effects than the volatiles induced by non-galling herbivores. Accordingly, from chemical ecology perspective we expect that galling herbivore-induced volatiles may exhibit robust effects on neighboring-plant interactions including those ones during different plant developmental or phenological periods. Information about multitrophic interactions between insects and plants supports the additional understanding of direct and indirect effects, and allows insight into new hypotheses.

Infestation of Anthonomus grandis grandis (Coleoptera: Curculionidae) contributes to forming shelter structures in cotton plants

“…The greater diameter and mass per dry boll in plants infested with boll weevils indicate changes in these structures resulting from infestation, as observed with other herbivorous arthropods (Barônio & Oliveira, 2019;de Lillo et al, 2018;Giron et al, 2016).…”

“…Herbivorous arthropods can induce their host to form structures, such as galls and erinoses, which they use for protection and feeding, increasing their survival (Barônio & Oliveira, 2019; de Lillo et al., 2018; Eitle et al., 2019). Such structures may increase the development and survival of eriophyid mites and other galling arthropods (de Lillo et al., 2018; Giron et al., 2016; Ronquist et al., 2015) and reduce the impact action of natural enemies (Barônio & Oliveira, 2019; Borges, 2018; Giron et al., 2016).…”

The Potential of Visual and Olfactory Signals in Gall Defence

“…Gall signalling (colouration, shape, and scent) may be part of their defensive arsenal. Insects can manipulate the chemical production and accumulation of defensive substances in the galls (Martinson et al, 2022;Davidovich-Rikanati, 2022), alter volatile emission from the galls to reduce the level of parasitism or deter enemies (Tooker et al, 2008;Rostás et al, 2013;Barônio and Oliveira, 2019), and manipulate gall phenotypes including pigmentation (Korgaonkar et al, 2021; see also Maderspacher, 2021). Considering the selective evolutionary forces on the gall systems, and having the ecological, behavioural, biochemical and molecular tools available, the adaptive significance (or not) of gall signalling could be readily addressed, and many new and exiting discoveries are expected.…”

Bottom‐up and top‐down forces in plant‐gall relationships: testing the hypotheses of resource concentration, associational resistance, and host fitness reduction

“…A more diverse plant community surrounding the host plant can lead to background complexity that masks the specific host volatiles the insects use in host localisation (Barbosa et al, 2009). Although the use of plant volatiles as cues to predict galling insect distribution is still unknown (Barônio & Oliveira, 2019), these volatile cues are mainly used when the insects are close enough to the resource (as in our study area), where the airflow causes little dilution (Finch, 1980). Since volatile preferences are highly site-adapted, and differ among insects (Doddala et al, 2016), shifts in species composition may confound the galling insect orientation when searching for a host.…”