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.
Highlights
A major long-established goal in community ecology and evolutionary biology is to understand how interspecific interactions influence population density, distribution, phenotypes, and genotypes [1], crucial to the selection and evolution of life-history traits
Most of these studies have focused on a single type of interaction at a time, usually studying either mutualistic or antagonistic interactions among species of particular taxonomic groups [9]. Examples of such interspecific interactions that have been most often investigated separately are competitive interactions among vertebrates [e.g., 10, 11] facilitative interactions among plants [e.g., 12, 13] and mutualistic/antagonistic plant-animal interactions [e.g., 8, 14]. Many of these interaction types take place within the same habitats [15,16,17] and species involved in one interaction type can participate in other interactions
To illustrate the usefulness of our approach, we evaluate whether interspecific interactions among vertebrate frugivores alter the likelihood of their subsequent interactions with fleshy-fruited plants
Summary
A major long-established goal in community ecology and evolutionary biology is to understand how interspecific interactions influence population density, distribution, phenotypes, and genotypes [1], crucial to the selection and evolution of life-history traits. During the few last decades, the study of interspecific interactions has experienced an outstanding progress [2] such as, for example, moving from a traditional pair-wise perspective [3,4,5,6] to a more realistic and complex multispecific approach, where multiple species interact with each other [2, 7, 8] Most of these studies have focused on a single type of interaction at a time, usually studying either mutualistic or antagonistic interactions among species of particular taxonomic groups [9]. To our knowledge, studies integrating these interaction types are still scarce [but see 18]
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