Plant reproductive traits mediate tritrophic feedback effects within an obligate brood-site pollination mutualism

Abstract

Plants, herbivores and parasitoids affect each other directly and indirectly; however, feedback effects mediated by host plant traits have rarely been demonstrated in these tritrophic interactions. Brood-site pollination mutualisms (e.g. those involving figs and fig wasps) represent specialised tritrophic communities where the progeny of mutualistic pollinators and of non-mutualistic gallers (both herbivores) together with that of their parasitoids develop within enclosed inflorescences called syconia (hence termed brood-sites or microcosms). Plant reproductive phenology (which affects temporal brood-site availability) and inflorescence size (representing brood-site size) are plant traits that could affect reproductive resources, and hence relationships between trees, pollinators and non-pollinating wasps. Analysing wasp and seed contents of syconia, we examined direct, indirect, trophic and non-trophic relationships within the interaction web of the fig-fig wasp community of Ficus racemosa in the context of brood site size and availability. We demonstrate that in addition to direct resource competition and predator-prey (host-parasitoid) interactions, these communities display exploitative or apparent competition and trait-mediated indirect interactions. Inflorescence size and plant reproductive phenology impacted plant-herbivore and plant-parasitoid associations. These plant traits also influenced herbivore-herbivore and herbivore-parasitoid relationships via indirect effects. Most importantly, we found a reciprocal effect between within-tree reproductive asynchrony and fig wasp progeny abundances per syconium that drives a positive feedback cycle within the system. The impact of a multitrophic feedback cycle within a community built around a mutualistic core highlights the need for a holistic view of plant-herbivore-parasitoid interactions in the community ecology of mutualisms.

Life-history strategy, resource dispersion and phylogenetic associations shape dispersal of a fig wasp community

“…The fruiting phenology of the cluster fig Ficus racemosa shows little seasonality and trees exhibit high degrees of within-tree reproductive synchrony but population-level reproductive asynchrony throughout the year [ 46 , 47 ]. Syconia of Ficus racemosa progress through several developmental stages: a) the pre-receptive phase, which constitutes the primordial stages of syconium development and the stages before pollen receptivity; b) the pollen-receptive stage, when pollinators enter syconia to pollinate flowers; c) the post-pollination stage, or the developmental stage when wasps and seeds develop in the syconia; d) the emergence phase, when adult winged female wasps disperse in search of oviposition sites; e) the fruit ripening stage when seeds are dispersed; and f) a gap phase when no syconia are present on the host plant [ 37 ] (Additional file 1 : Figure S1).…”

Interactions Between Figs and Gall-Inducing Fig Wasps: Adaptations, Constraints, and Unanswered Questions

“…We know nothing about waste management within the syconial microcosm as in aphid galls (Kutsukake et al, 2019) or how waste in a syconial microcosm, where hundreds of wasps develop, may be recycled. We require data on interactions between plant traits and larval trophic levels (Krishnan et al, 2015;Segar et al, 2018) and mode of feeding, since unusual reports of early instar larvae suspended in acellular gall fluid and ingesting a liquid diet (Yadav and Borges, 2018b) need wider validation.…”

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

“…For parasitoids that need to seek out hidden hosts within galls ( Figure 2E ), the use of cues such as CO 2 that signal locations of actively respiring galler larvae/pupae are potentially extremely important in successful parasitism. Parasitoids in the fig system may be considered apparent mutualists if they target non-beneficial gallers or control the population of pollinating gallers within fig syconia ( Krishnan et al, 2015 ); therefore, the role of VOCs in maintaining such tritrophic interactions in order to stabilize the core mutualism is likely profound.…”