The seed dispersal syndrome hypothesis in ungulate-dominated landscapes.

The Seed Dispersal Syndrome Hypothesis (SDSH) posits that fruit traits predict the main dispersers interacting with plant species. Mammalian dispersers, relying heavily on olfactory cues, are expected to select dull-colored, scented, and larger fruits compared to birds. However, challenges like overabundant seed predators and context-dependency of frugivore-plant interactions complicate SDSH expectations. We studied the Iberian pear, Pyrus bourgaeana, an expected mammal-dispersed tree based on its fruit traits. Extensive camera-trapping data (over 35,000 records) from several tree populations and years revealed visits from seven frugivore groups, with ungulate fruit predators (59-97%) and carnivore seed dispersers (1-20%) most frequent, while birds, lagomorphs, and rodents were infrequent (0-10%). Red deer and wild boar were also the main fruit removers in all sites and years but acted as fruit and seed predators, and thus likely exert conflicting selection pressures to those exerted by seed dispersers. Although, as predicted by the SDSH, most Iberian pear fruits were consumed by large and medium-sized mammals, the traits of Iberian pear fruits likely reflect selection pressures from dispersal vectors in past times. Our results do not challenge the SDHS but do reveal the importance of considering frugivore functional roles for its adequate evaluation.

Unmasking the perching effect of the pioneer Mediterranean dwarf palm Chamaerops humilis L.

Although farmlands are the most extensive terrestrial biomes, the abandonment of traditional agriculture in many parts of the world has brought opportunities and challenges for the restoration of such human-disturbed habitats. Seed arrival is a crucial necessary ecological process during plant recolonization that can be enhanced by the use of the so-called "perch plants". Little is known, however, about whether the seed arrival via frugivorous birds is affected by the spatial distribution of the perch plants in disturbed habitats. To evaluate several spatial aspects of "perching" effect, we used a spatially explicit approach in two disturbed plots within the Doñana National Park (SW Spain). Specifically, we chose as study system the pioneer Mediterranean dwarf palm Chamaerops humilis L., which is often used as a perch by a variety of frugivorous bird species. A total of 289 C. humilis individuals were sampled in search of bird feces (N = 2998) and dispersed seeds (N = 529). Recorded seeds belonged to six different woody species from five different families. Nine bird species from six different families were recorded using C. humilis as perches. GLMs analyses indicated that taller C. humilis males with higher numbers of spatially associated woody species received more dispersed seeds. We detected a random spatial structure of bird feces and dispersed seeds in one study plot, while a nonrandom spatial structure was found in the other one, where isolated C. humilis received a higher number of bird feces and dispersed seeds than expected under spatial null models. The difference in spatial patterns between both study plots could relate, among other factors, to their different state of development in the ecological succession. Most of dispersed seeds were concentrated in a small number of C. humilis individuals, usually male and large ones, that acted as "hotspots" of seed arrival. The fact that frugivorous birds in one study site visited most often isolated C. humilis questions the aggregated spatial structure of revegetation designs typically used in restoration projects. This study reveals novel spatial aspects of the "perching" effect which could be helpful in the restoration of human-disturbed habitats worldwide.

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

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.

Genetic rescue by distant trees mitigates qualitative pollen limitation imposed by fine-scale spatial genetic structure.

Restricted seed dispersal frequently leads to fine-scale spatial genetic structure (i.e., FSGS) within plant populations. Depending on its spatial extent and the mobility of pollinators, this inflated kinship at the immediate neighbourhood can critically impoverish pollen quality. Despite the common occurrence of positive FSGS within plant populations, our knowledge regarding the role of long-distance pollination preventing reproductive failure is still limited. Using microsatellite markers, we examined the existence of positive FSGS in two low-density populations of the tree Pyrus bourgaeana. We also designed controlled crosses among trees differing in their kinship to investigate the effects of increased local kinship on plant reproduction. We used six pollination treatments and fully monitored fruit production, fruit and seed weight, proportion of mature seeds per fruit, and seed germination. Our results revealed positive FSGS in both study populations and lower fruit initiation in flowers pollinated with pollen from highly-genetically related individuals within the neighbourhood, with this trend intensifying as the fruit development progressed. Besides, open-pollinated flowers exhibited lower performance compared to those pollinated by distant pollen donors, suggesting intense qualitative pollen limitation in natural populations. We found positive fine-scale spatial genetic structure is translated into impoverished pollen quality from nearby pollen donors which negatively impacts the reproductive success of trees in low-density populations. Under this scenario of intrapopulation genetic rescue by distant pollen donors, the relevance of highly-mobile pollinators for connecting spatially and genetically distant patches of trees may be crucial to safeguarding population recruitment.

The endemic Mediterranean dwarf palm boosts the recolonization of old-fields: Implications for restoration.

Understanding the mechanisms underlying the recolonization of old-fields is critical to promote the recovery of the ecosystem functioning, particularly in regions where agricultural abandonment has increased in the last 60 years. Given that seed arrival and seedling survival often limit the recolonization process by woody species in many Mediterranean habitats, the 'perching' and 'nursing' effects exerted by some pioneer species could be crucial for the restoration of such abandoned lands. We examined the role of an endemic Mediterranean palm (Chamaerops humilis) on the recolonization of old-fields by woody species in southern Iberian Peninsula. We chose three independent old-fields differing in their shrub encroachment levels. To identify potential facilitation by C. humilis, we used a spatially-explicit approach and analyzed its spatial associations with ten common woody species (e.g. Asparagus spp., Daphne gnidium, Olea europaea var. sylvestris, Pyrus bourgaeana). We detected positive spatial associations between C. humilis and woody species at small-scale (1-5 m) in the three plots. Most of such small-scale associations were linked to the bird-dispersal of woody species. Nonetheless, there were marked differences among plots in spatial associations between C. humilis and woody plants, being Asparagus spp. the only species positively associated with C. humilis within the three studied old-fields. These species-specific differences were likely related to variations among old-fields in encroachment level and the legacy of human management. Such small-scales spatial associations between C. humilis and woody species across Iberian old-fields were linked to the perching and nursing effects exerted by the palm. We emphasize the strong potential of this pioneer Mediterranean palm for the restoration of native ecosystems and the recovery of ecosystems services.

Strong among population variation in frugivory strength by functional diverse frugivores: a 'reciprocal translocation' experiment.

Fruit-frugivore interactions are critical for the dynamics and evolution of many plant communities. The strength of the interactions between a given plant species and different frugivore guilds (e.g., seed dispersers, seed predators) often vary in space due to changes in plant extrinsic factors (e.g., frugivore abundances) and plant traits (e.g., fruit size and reward). By reciprocally translocating Pyrus bourgaeana ripe fruits representative of five Mediterranean localities during 2 consecutive years, we experimentally quantified guild-specific variations among populations in frugivory strength, while accounted for plant-intrinsic and- extrinsic factors. Though overall fruit removal did not differ among localities, there were strong guild-specific differences in fruit removal strength. Fruit removal by pulp feeders, seed dispersers, and fruit predators varied among populations up to 8.5-, 5.6-, and 4.0-folds, respectively. These strong variations seemed mediated by changes in frugivore relative abundances rather than on availability of alternative fruits. As expected, all fruit traits considered (e.g., fruit size, pulp amount) markedly varied among tree populations. However, no frugivore guild showed preference for fruits from any locality, suggesting that fruit traits did not contribute much to differences in frugivory strength among populations. Since the functional diverse frugivore guilds played contrasting roles in P. bourgaeana dynamics (e.g., seed dispersal vs. seed predation), our study highlights the importance of accounting for functional diversity in frugivore guilds when estimating spatial variations in the strenght of seed dispersal. This investigation also illustrates a neglected but widely applicable experimental approach to identify the relative importance of extrinsic factors and fruit traits in mediating fruit-frugivore interactions.