Interspecific interactions among functionally diverse frugivores and their outcomes for plant reproduction: A new approach based on camera-trap data and tailored null models

Abstract

The study of plant-frugivore interactions is essential to understand the ecology and evolution of many plant communities. However, very little is known about how interactions among frugivores indirectly affect plant reproductive success. In this study, we examined direct interactions among vertebrate frugivores sharing the same fruit resources. Then, we inferred how the revealed direct interspecific interactions could lead to indirect (positive or negative) effects on reproductive success of fleshy fruited plants. To do so, we developed a new analytical approach that combines camera trap data (spatial location, visitor species, date and time, activity) and tailored null models that allowed us to infer spatial-temporal interactions (attraction, avoidance or indifference) between pairs of frugivore species. To illustrate our approach, we chose to study the system composed by the Mediterranean dwarf palm, Chamaerops humilis, the Iberian pear tree, Pyrus bourgaeana, and their shared functionally diverse assemblages of vertebrate frugivores in a Mediterranean area of SW Spain. We first assessed the extent to which different pairs of frugivore species tend to visit the same or different fruiting individual plants. Then, for pairs of species that used the same individual plants, we evaluated their spatial-temporal relationship. Our first step showed, for instance, that some prey frugivore species (e.g. lagomorphs) tend to avoid those C. humilis individuals that were most visited by their predators (e.g. red foxes). Also, the second step revealed temporal attraction between large wild and domestic frugivore ungulates (e.g. red deer, cows) and medium-sized frugivores (e.g. red foxes) suggesting that large mammals could facilitate the C. humilis and P. bourgaeana exploitation to other smaller frugivores by making fruits more easily accessible. Finally, our results allowed us to identify direct interaction pathways, that revealed how the mutualistic and antagonistic relations between animal associates derived into indirect effects on both plants seed dispersal success. For instance, we found that large-sized seed predators (e.g. ungulates) had a direct positive effect on the likelihood of visits by legitimate seed dispersers (e.g. red foxes) to both fleshy fruited plants. Then, seed predators showed an indirect positive effect on the plants’ reproductive success. Our new analytical approach provides a widely applicable framework for further studies on multispecies interactions in different systems beyond plant-frugivore interactions, including plant-pollinator interactions, the exploitation of plants by herbivores, and the use of carcasses by vertebrate scavengers.