Interaction engineering: Non‐trophic effects modify interactions in an insect galler community

Abstract

Theory suggests that non‐trophic interactions can be a major mechanism behind community stability and persistence, but community‐level empirical data are scarce, particularly for effects on species interactions mediated through changes in the physical environment. Here, we explored how ecosystem engineering effects can feed back to the engineer, not only modulating the engineer’s population density (node modulation) but also affecting its interactions with other species (link modulation). Gall induction can be viewed as ecosystem engineering since galls serve as habitat for other species. In a community‐level field experiment, we generated treatments with reduced or elevated ecosystem engineering by removing or adding post‐emergence galls to different plots of their host plant in the Brazilian Cerrado. We tested the effect of post‐emergence galls on the galler, as well as on the galler–parasitoid and galler—aphid interactions. The manipulation of post‐emergence galls had little effect on the galler—abundance and survivorship were not affected, and gall volume changed only slightly—but modified interactions involving the galler, parasitoid wasps and inquiline aphids. Aphid inquilines negatively affected density‐dependent parasitism rates (interaction modification) likely by killing parasitised galling larvae. Post‐emergence galls interfered with aphid inquilinism—likely by the provision of alternative habitat for aphids—and thus interfered with the negative effect of aphids on parasitism (modification of an interaction modification). This work is one of the few studies to demonstrate experimentally the role played by environment‐mediated interaction modification at a community level in the field. Moreover, by manipulating a species’ ecosystem engineering effect (post‐emergence galls) instead of the species itself, we demonstrate the novel result that populations can be regulated by non‐trophic effects initiated by their own activities that alter their interaction with other species. This reveals that indirect interactions mediated via the environment offer new pathways of feedback loops for population regulation. Our results indicate that interaction modification has the potential to be a key regulatory mechanism underlying interaction variation in nature, and play a major role in community structure, dynamics and stability.

Gallers as leaf rollers: ecosystem engineering in a tropical system and its effects on arthropod biodiversity

“…The presence of galls and their effects on host plant morphology, architecture, and performance have been previously investigated in the literature , but no study has shown that galls might facilitate ecosystem engineering when galled leaves are rolled and act as shelters for secondary colonization. After experimental manipulation of leaf galls in the shrub Baccharis dracunculifolia, Barbosa et al (2017) have shown increased parasitism in the gall Baccharopelma dracunculifoliae and reduced connectance, evenness, and robustness of arthropod food webs, indicating the central role gallers have in interaction engineering (Barbosa et al, 2019). Our study reinforces and highlights this important role, as gall presence facilitated ecosystem engineering, changing community composition, richness, and biomass.…”

“…Results were even stronger when shelters created by galls were unoccupied. Arthropod communities associated to galls are not discrete ecological communities and interactions with other members might occur via habitat availability (Barbosa et al, 2017(Barbosa et al, , 2019. Leaf rolling by gallers and changes in leaf morphology and plant architecture are frequent, but facilitation of shelter creation by gallers has been rarely studied, although many galls curl leaves during development (Harris & Pitzschke, 2019).…”

“…After experimental manipulation of leaf galls in the shrub Baccharis dracunculifolia , Barbosa et al . (2017) have shown increased parasitism in the gall Baccharopelma dracunculifoliae and reduced connectance, evenness, and robustness of arthropod food webs, indicating the central role gallers have in interaction engineering (Barbosa et al ., 2019). Our study reinforces and highlights this important role, as gall presence facilitated ecosystem engineering, changing community composition, richness, and biomass.…”

“…These structures can be secondarily occupied by other arthropods, that sometimes co‐occur with the EE (Cornelissen et al ., 2016). Gallers are seldom suggested as EE, representing only 4.3% of EE records for invertebrates in a global meta‐analytic review (Romero et al ., 2014), but they are important allogeneic engineers because by inducing cell differentiation – by hyperplasia and/or hypertrophy – in their host plants (Price et al ., 1986; Fernandes et al ., 2014), they create a variety of structures that can provide shelter for several arthropods, such as ants who use galls as nests (e.g., Fernandes et al ., 1988; Fukui, 2001; Shorthouse et al ., 2005; Maruyama et al ., 2012; Barbosa et al ., 2019; Novais et al ., 2020).…”

“…These structures can increase the diversity of associated organisms, changing for example arthropod community richness and/or composition (Crawford et al ., 2007; Maruyama et al ., 2012; Vieira & Romero, 2013; Novais et al ., 2020). These changes might, in turn, change the functional structure of these communities when functional groups such as herbivores and predators become more or less frequent in plants, changing ecosystem processes such as herbivory and decomposition at different spatial – leaves, plants, or patches – and temporal scales (i.e., over seasons) (see Vieira & Romero, 2013; Barbosa et al ., 2019).…”