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

Research ArticleThe 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 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 scavengersinfo:eu-repo/semantics/publishedVersio

Thieves or mutualists? Pulp feeders enhance endozoochore local recruitment

Abstract. The persistence of mutualisms despite the strong incidence of exploiters could be explained if exploiters deny one or more services (i.e., cheat) while eventually supplying some subtler but critical services. Pulp feeders usually ingest fruit reward without dispersing seeds and thus are considered to be mainly cheaters or thieves of seed-disperser mutualisms. By consuming the fruit pulp, however, they could release seeds from pulp inhibitory effect, enhancing germination and, potentially, subsequent seedling emergence, growth, survival, and thus local recruitment. We evaluated such a largely neglected hypothesis by considering the interaction between Pyrus bourgaeana and its pulp feeders. We experimentally showed that pericarp removal had a consistent strong positive effect on seed performance (e.g., lower rotting and higher germination percentages) and seedling fate (greater emergence, growth, and survival to two years old). Interestingly, these relatively large positive effects of depulpation on plant fitness persisted for a surprisingly long time. Though seedlings experienced higher mortality under fruiting conspecifics, the benefits of depulpation were not overridden by high propagule mortality beneath fruiting trees or in adverse microhabitats after two years of monitoring. Specifically, the cumulative probability of establishment for depulped seeds was 4-25 times higher than for seeds in whole ripe fruits. Thus, under some circumstances, pulp feeders can provide essential services to endozoochorous plants. Our study contributes to clarifying the apparent paradox of plant-frugivore mutualisms that persist in the face of exploitation by pulp feeders. Because ''thieves'' and ''mutualists'' refer to the extremes of a complex continuum, and because organisms displaying concurrent cheating and honest behaviors during different host stages are likely prevalent, the persistent language of mutualists vs. thieves, cheaters, or exploiters might be misleading

Thieves or mutualists? Pulp feeders enhance endozoochore local recruitment

Abstract. The persistence of mutualisms despite the strong incidence of exploiters could be explained if exploiters deny one or more services (i.e., cheat) while eventually supplying some subtler but critical services. Pulp feeders usually ingest fruit reward without dispersing seeds and thus are considered to be mainly cheaters or thieves of seed-disperser mutualisms. By consuming the fruit pulp, however, they could release seeds from pulp inhibitory effect, enhancing germination and, potentially, subsequent seedling emergence, growth, survival, and thus local recruitment. We evaluated such a largely neglected hypothesis by considering the interaction between Pyrus bourgaeana and its pulp feeders. We experimentally showed that pericarp removal had a consistent strong positive effect on seed performance (e.g., lower rotting and higher germination percentages) and seedling fate (greater emergence, growth, and survival to two years old). Interestingly, these relatively large positive effects of depulpation on plant fitness persisted for a surprisingly long time. Though seedlings experienced higher mortality under fruiting conspecifics, the benefits of depulpation were not overridden by high propagule mortality beneath fruiting trees or in adverse microhabitats after two years of monitoring. Specifically, the cumulative probability of establishment for depulped seeds was 4-25 times higher than for seeds in whole ripe fruits. Thus, under some circumstances, pulp feeders can provide essential services to endozoochorous plants. Our study contributes to clarifying the apparent paradox of plant-frugivore mutualisms that persist in the face of exploitation by pulp feeders. Because ''thieves'' and ''mutualists'' refer to the extremes of a complex continuum, and because organisms displaying concurrent cheating and honest behaviors during different host stages are likely prevalent, the persistent language of mutualists vs. thieves, cheaters, or exploiters might be misleading

Subtle Gardeners : Inland Predators Enrich Local Topsoils and Enhance Plant Growth

Inland vertebrate predators could enrich of nutrients the local top soils in the area surrounding their nests and dens by depositing faeces, urine, and prey remains and, thus, alter the dynamics of plant populations. Surprisingly, and in contrast with convincing evidence from coastal habitats, whether and how this phenomenon occurs in inland habitats is largely uncertain even though these habitats represent a major fraction of the earth's surface. We investigated during two consecutive breeding seasons the potential enrichment of the top-soils associated with inland ground-nesting eagle owls Bubo bubo, as well as its possible consequences in the growth of two common annual grasses in southern Spain. Top-soils associated with owl nests differed strongly and significantly from control top-soils in chemical parameters, mainly fertility-related properties. Specifically, levels of available phosphorus, total nitrogen, organic matter, and available potassium were 49.1, 5.6, 3.1, and 2.7 times higher, respectively, in top-soils associated with owl nests as compared to control top-soils. Germination experiments in chambers indicated that nutrient enrichment by nesting owls enhanced seedling growth in both annual grasses (Phalaris canariensis and Avena sativa), with seedling size being 1.4-1.3 times higher in owl nest top-soils than in control top-soils. Our experimental study revealed that pervasive inland, predatory birds can profoundly enrich the topsoil around their nests and, thus, potentially enhance local vegetation growth. Because diverse inland vertebrate predators are widespread in most habitats they have a strong potential to enhance spatial heterogeneity, impinge on plant communities, and exert an overlooked effect on primary productivity worldwide.Peer reviewe

Soil characteristics, seedling size, and number of seedlings emerged per pot.

<p>The first file contains data on soil parameters and principal components for each owl nest and its corresponding control sample. The second file contains data on seedling size and number of  emerged seedlingsper pot</p

NCO ICV x # of nests

This file contains data concerning ICV of non centenarian oaks as well as the overall number of nests they hosted

Pre- and postdispersal seed predation by rodents: balance of food and safety

Seed presentation and availability for seed predators change during every plant reproductive cycle. We know very little about how those changes impinge on both the ability of seed predators to impact plant populations and the foraging costs associated with seed consumption. Therefore, we conducted several field experiments to evaluate whether wood mice Apodemus sylvaticus balance food and safety while foraging on Helleborus foetidus seeds during both the pre- and early postdispersal phases of the plant reproductive cycle. Both food and safety were key determinants of mouse foraging on H. foetidus seeds, though their roles were not consistent along the plant reproductive cycle. Thus, augmenting ambient food reduced fruit removal by mice during the predispersal phase. During the postdispersal phase, seeds in sheltered microsites experienced higher removal rates than those located in nonsheltered microsites; however, no effect of food augmentation was detected. This apparent reversed role of food and safety on decision making by mice seemed closely linked to both the dramatic changes in accessibility and presentation of H. foetidus seeds and the coupled changing foraging costs faced by mice at different phases of the plant reproductive cycle. For instance, because the cost of foraging for predispersal seeds was higher than for postdispersal seeds, the effect of food augmentation on foraging by wood mice was greater during the predispersal phase. Thus, our study illustrates the need of considering differences between pre- and postdispersal seed predation in the study of granivore rodents and their impact on plant populations. Copyright 2005.behavioural trade-offs; foraging; granivory; Helleborus foetidus; mice; pre- and postdispersal seed predation; predation risk

Data from: Non-trophic plant-animal interactions mediate positive density dependence among conspecific saplings

Trophic plant-animal interactions (e.g. browsing by ungulates, insect attack) are an important and well-studied source of mortality in many tree populations. Non-trophic tree-animal interactions (e.g. deer antler rubbing) also frequently lead to tree death, and thus have significant effects on forest ecosystem functioning, but they are much less well studied than trophic interactions are. As deer populations have increased in recent decades in the Northern Hemisphere, their impact on tree populations via browsing and antler rubbing will increase. The aim of the study was to illustrate the potential ability of non-trophic plant-animal interactions to regulate the dynamics of a natural forest. Specifically, we wanted to determine whether and how density and distance-dependent processes affect sapling mortality caused by an antler rubbing by red deer (Cervus elaphus). We used a spatially explicit approach to examine density and distance-dependent mortality effects in almost two thousand Picea abies saplings over 20 years, based on a fully mapped permanent 14.4 ha plot in a natural subalpine old-growth spruce forest. Antler rubbing by deer was the main identified cause of sapling mortality, and it showed a strong spatial pattern: positive density dependence of survival among spruce saplings. Deer selectively killed spruce saplings that were isolated from conspecifics. In consequence, non-trophic plant-deer interactions were a major driver of the spatial pattern of P. abies sapling survival. The other mortality causes (e.g. breaking, overturning) did not show density-dependent patterns or their effects were much weaker. In the medium and long term, the density-dependent pattern of sapling mortality due to antler rubbing can alter the tree stand structure. Our results highlight the ecological relevance of non-trophic plant-animal interactions for forest ecosystem functioning

SPPA of Picea abies mortality

The file consists of four sheets which present SPPA of mortality (p11{r}; p12{r} and g1,1+2 - g2,1+2 {r}) in years 1993-2013, 1993-2003 and 2003-2013:(1) overall mortality; (2) deer-caused mortality; (3) mortality due to mechanical causes and (4) mortality of unknown causes