The Role of Nursery Size and Plant Phenology on the Reproduction of and Relationships within a Fig-fig Wasp Nursery Pollination System

Abstract

Obligate nursery pollination mutualisms such as the fig–fig wasp system, with their central plant–pollinator mutualism associated with non-pollinating satellite wasp species, can function as closed system microcosms representative of tritrophic communities. In this system, enclosed inflorescences (syconia) function as sites of seed production, as well as brood-sites for the progeny of herbivorous mutualistic pollinators, non-pollinating gallers and parasitoids of the two. Plant reproductive traits such as inflorescence size (syconium volume) and within-plant phenology (within-tree asynchrony) as can affect inter-species relationships among the three trophic levels in such plant–herbivore–parasitoid systems. Induced or natural variations in such plant traits could influence various direct and indirect effects among the organisms in the community and could even lead to the formation of feedback cycles. Furthermore, changes in the abiotic environment could have major impacts on the biotic associations in the system either by affecting the community members directly, or through their effects on plant reproductive traits. Ficus racemosa with its fig wasp community comprised of a single herbivorous pollinator mutualist, three non-pollinating parasitic gallers and three non-pollinating parasitoids was used as a model to investigate: (1) the role of mutualistic and parasitic fig wasps in affecting within-tree phenology; (2) direct and indirect biotic associations between various groups of fig wasps (pollinators, gallers and parasitoids) and the influence of inflorescence size and within-tree phenology on them; and (3) variations in the reproduction of and the biotic associations between the organisms of the community under variable abiotic climatic conditions. Patterns of plant reproductive phenology are usually considered evolved responses directed at optimizing resource use, pollen receipt/donation schedules and seed dispersal for plant individuals. Within-plant reproductive synchrony or asynchrony can arise due to variation in floral initiation patterns, as well as from localised proximate mechanistic responses to interactants such as pollinators, parasites and herbivores which could affect floral longevity or fruit development time. The investigation was begun by exploring the role of a mutualistic pollinator, and for the first time in a brood-site mutualism, that of parasitic herbivores (gallers) and parasitoids in influencing within-plant reproductive phenology. Since a syconium functions as an inflorescence which develops into a fruit after pollination, investigations were carried out on the impact on syconium synchrony of fig wasps that began their development within the brood site syconium at pre-pollination, pollination, and post-pollination stages via their effects on the development time of individual syconia in Ficus racemosa. We found that syconium initiation patterns were not the only proximate mechanism for within-tree reproductive asynchrony, and that individual syconia (even within a tree) had highly plastic development times dependent on their sizes, pollination time and the species of wasp progeny developing within them. Syconium volume, pollination early in the pollen-receptive phase and presence of early-ovipositing galler progeny reduced syconium development time, whereas the presence of late-ovipositing parasitoid progeny or pollination late in the pollen-receptive phase increased syconium development time. These results suggest an ongoing tug-of-war between syconium inhabitants to modify syconium development times. Parasitic fig wasps pull in different directions to suit their own needs, such that final syconium development times are likely to be a compromise between conflicting demands from developing seeds and from different wasp species. Inter-species relationships among the three trophic levels in plant–herbivore–parasitoid systems can potentially include various direct and indirect effects possibly mediated by induced or natural variations in plant traits. Analysing the seed and fig wasp compositions of microcosm replicates, i.e. individual syconia, shows that besides direct competition for resources and predator–prey interactions, the F. racemosa community also displays exploitative or apparent competition and trait-mediated indirect interactions. Syconium volume and within-tree asynchrony were reproductive plant traits that not only affected plant–herbivore and plant–parasitoid associations, but also possibly modified herbivore–herbivore and herbivore–parasitoid interactions. Our results also indicated that the reciprocal effects of higher trophic level fauna on plant traits (and vice versa) within this system drive a positive feedback cycle between syconium inhabitants and within-tree reproductive asynchrony. In the F. racemosa system, abiotic environmental factors could affect the reproduction of mutualistic pollinators, non-mutualistic parasites and seed production via seasonal changes in plant reproductive traits such as syconium volume within-tree asynchrony. Temperature, relative humidity and rainfall defined four seasons: winter; hot days, cold nights; summer and wet seasons. Syconium volumes were highest in winter and lowest in summer, and affected syconium contents positively across all seasons. Greater transpiration from the nurseries was possibly responsible for smaller syconia in summer. The 3–5°C increase in mean temperatures between the cooler seasons and summer reduced fig wasp reproduction and increased seed production nearly two-fold. Yet, seed and pollinator progeny production were never negatively related in any season confirming the mutualistic fig–pollinator association across seasons. Parasites affected seed production negatively in some seasons, but had a surprisingly positive relationship with pollinators in most seasons. While within-tree reproductive phenology did not vary across seasons, its effect on syconium inhabitants varied with season. In all seasons, within-tree reproductive asynchrony affected parasite reproduction negatively, whereas it had a positive effect on pollinator reproduction in winter and a negative effect in summer. Seasonally variable syconium volumes probably caused the differential effect of within-tree reproductive phenology on pollinator reproduction. Within-tree reproductive asynchrony itself was positively affected by intra-tree variation in syconium contents and volume, creating a unique feedback loop which varied across seasons. Therefore, nursery size affected fig wasp reproduction, seed production and within-tree reproductive phenology via the feedback cycle in this system. Climatic factors affecting plant reproductive traits can cause biotic relationships between plants, mutualists and parasites to vary seasonally and must be accorded greater attention, especially in the context of climate change.