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.

Predation risk can modify the foraging behaviour of frugivorous carnivores: Implications of rewilding apex predators for plant–animal mutualisms

“…However, we found the opposite relationship when carnivores did not coexist with lynx. In this scenario, carnivores invested foraging efforts to areas where food is easier to find, in accordance with other similar studies (Garcia et al, 2011;Selwyn et al, 2020;Virgós et al, 2010). We found that while badger visits were positively related to forest cover around pear trees in both the presence and absence of lynx, foxes only demonstrated this pattern in the predation risk scenario.…”

“…Frugivorous mesocarnivores actively search for Iberian pear fruits because these are a predictable and valuable resource in Mediterranean ecosystems (Fedriani & Delibes, 2009a). Therefore, less frequent visits to pear trees under predation risk could be due to lower population abundances, a behavioural avoidance of agonistic encounters or a combination of both (Carreira et al, 2020; Ripple & Beschta, 2004; Selwyn et al, 2020). We identified far fewer fox individuals and recorded fewer visits in a predation risk scenario, which supports previous work by Garrote et al (2018), who proposed that in the Doñana National Park, a low frequency of fox visitation to pear fruits was likely related to a high lynx density.…”

“…In lynx presence scenario, foxes consumed less fruit per unit of time (i.e. lower efficiency) and their visits to pear trees were shorter, behaviour likely linked to an anti‐predatory response (Carreira et al, 2020; Haswell et al, 2018; Selwyn et al, 2020). The combination of a lower fruit consumption and the alteration in the feeding behaviour can cause a cascading effect that disrupts a plant‐disperser mutualism (de Paula Mateus et al, 2018; Kurten, 2013).…”

Observing frugivores or collecting scats: a method comparison to construct quantitative seed dispersal networks

“…Additionally, the microhabitat properties of deposition sites may vary between birds and mammals, with potential consequences for plant populations and communities (Jordano et al 2007). Finding more mammalian species with DNA barcoding of deposited seeds compared to focal observations is not surprising, since most mammals are nocturnal (Selwyn et al 2020). However, given that mammals can be frequent dispersers and their dispersal service complements those of avian frugivores (Jordano et al 2007, Martínez et al 2008, Tsunamoto et al 2020), the inclusion of seed sampling in mammal scats is useful to assess the influence of the whole disperser community as well as the relative contribution of mammals and birds on the regeneration process of their fleshy‐fruited plant partners.…”

“…Seed dispersal networks, for instance, have traditionally been constructed by either direct observation of frugivore visits on fruiting focal plants or by the capture of frugivores in mist‐nets and subsequent analysis of seeds and pulp remains in their scats (Olesen et al 2011, Jordano 2016). In recent years also (infra‐red) camera‐ and video‐camera traps have been used to sample seed removal interactions, which help to capture interactions by nocturnal frugivores like mammals (Schipper 2007, Zakaria and Rajpar 2010, Selwyn et al 2020). Focal plant observations by direct observations or camera trapping focus on the plant perspective and yield information on the quantitative contribution each frugivore species has on the plant species.…”