Frugivore-mediated seed dispersal in fragmented landscapes: Compositional and functional turnover from forest to matrix.

Seed dispersal by frugivores is a fundamental function for plant community dynamics in fragmented landscapes, where forest remnants are typically embedded in a matrix of anthropogenic habitats. Frugivores can mediate both connectivity among forest remnants and plant colonization of the matrix. However, it remains poorly understood how frugivore communities change from forest to matrix due to the loss or replacement of species with traits that are less advantageous in open habitats and whether such changes ultimately influence the composition and traits of dispersed plants via species interactions. Here, we close this gap by using a unique dataset of seed-dispersal networks that were sampled in forest patches and adjacent matrix habitats of seven fragmented landscapes across Europe. We found a similar diversity of frugivores, plants, and interactions contributing to seed dispersal in forest and matrix, but a high turnover (replacement) in all these components. The turnover of dispersed seeds was smaller than that of frugivore communities because different frugivore species provided complementary seed dispersal in forest and matrix. Importantly, the turnover involved functional changes toward larger and more mobile frugivores in the matrix, which dispersed taller, larger-seeded plants with later fruiting periods. Our study provides a trait-based understanding of frugivore-mediated seed dispersal through fragmented landscapes, uncovering nonrandom shifts that can have cascading consequences for the composition of regenerating plant communities. Our findings also highlight the importance of forest remnants and frugivore faunas for ecosystem resilience, demonstrating a high potential for passive forest restoration of unmanaged lands in the matrix.

Limited potential for bird migration to disperse plants to cooler latitudes.

Climate change is forcing the redistribution of life on Earth at an unprecedented velocity1,2. Migratory birds are thought to help plants to track climate change through long-distance seed dispersal3,4. However, seeds may be consistently dispersed towards cooler or warmer latitudes depending on whether the fruiting period of a plant species coincides with northward or southward migrations. Here we assess the potential of plant communities to keep pace with climate change through long-distance seed dispersal by migratory birds. To do so, we combine phenological and migration information with data on 949 seed-dispersal interactions between 46 bird and 81 plant species from 13 woodland communities across Europe. Most of the plant species (86%) in these communities are dispersed by birds migrating south, whereas only 35% are dispersed by birds migrating north; the latter subset is phylogenetically clustered in lineages that have fruiting periods that overlap with the spring migration. Moreover, the majority of this critical dispersal service northwards is provided by only a few Palaearctic migrant species. The potential of migratory birds to assist a small, non-random sample of plants to track climate change latitudinally is expected to strongly influence the formation of novel plant communities, and thus affect their ecosystem functions and community assembly at higher trophic levels.

Seed dispersal by dispersing juvenile animals: a source of functional connectivity in fragmented landscapes.

Juvenile animals generally disperse from their birthplace to their future breeding territories. In fragmented landscapes, habitat-specialist species must disperse through the anthropogenic matrix where remnant habitats are embedded. Here, we test the hypothesis that dispersing juvenile frugivores leave a footprint in the form of seed deposition through the matrix of fragmented landscapes. We focused on the Sardinian warbler ( Sylvia melanocephala), a resident frugivorous passerine. We used data from field sampling of bird-dispersed seeds in the forest and matrix of a fragmented landscape, subsequent disperser identification through DNA-barcoding analysis, and data from a national bird-ringing programme. Seed dispersal by Sardinian warblers was confined to the forest most of the year, but warblers contributed a peak of seed-dispersal events in the matrix between July and October, mainly attributable to dispersing juveniles. Our study uniquely connects animal and plant dispersal, demonstrating that juveniles of habitat-specialist frugivores can provide mobile-link functions transiently, but in a seasonally predictable way.

Interspecific competition for frugivores: population-level seed dispersal in contrasting fruiting communities.

Indirect interactions among plant species mediated by frugivorous animals can be central to population and community dynamics, since the successful seed dispersal of species may depend on facilitative or competitive interactions with heterospecific plants. Yet, empirical evidence on these interactions is very scarce and mostly available at small spatial scales, within populations. Because lipid-rich fruits are known to be preferred by migratory birds, here we test our prediction of competitive inferiority of a carbohydrate-rich fruited species (the hawthorn Crataegus monogyna) compared to lipid-rich co-fruiting species in a Mediterranean region where the bulk of seed dispersal relies on migratory birds. We assessed avian seed dispersal in both relative (fruit removal rate) and absolute terms (seed dispersal magnitude) in seven hawthorn populations distributed across an altitudinal gradient encompassing three contrasting fruiting contexts: hawthorn is scarce in the lowlands, common in the midlands, and the dominant fruit species in the highlands. We found evidence of seed dispersal reduction due to interspecific competition in the lowland populations, where lipid-rich fruits dominate. Besides, DNA barcoding analysis of bird-dispersed seeds revealed that only a small subset of the local frugivore assemblages consumed hawthorn fruits in the lowland communities. Instead, the consumers of hawthorn fruits resembled the local frugivore assemblages where hawthorn fruits were more dominant and frugivore choices more limited. Our study suggests mechanisms by which the rarity or dominance of plant species might be jointly influenced by environmental constraints (here, precipitation along the altitudinal gradient) and frugivore-mediated indirect interactions among plants hindering or facilitating seed dispersal.

The timing of frugivore-mediated seed dispersal effectiveness.

The seed dispersal effectiveness framework allows assessing mutualistic services from frugivorous animals in terms of quantity and quality. Quantity accounts for the number of seeds dispersed and quality for the probability of recruitment of dispersed seeds. Research on this topic has largely focused on the spatial patterns of seed deposition because seed fates often vary between microhabitats due to differences in biotic and abiotic factors. However, the temporal dimension has remained completely overlooked despite these factors-and even local disperser assemblages-can change dramatically during long fruiting periods. Here, we test timing effects on seed dispersal effectiveness, using as study case a keystone shrub species dispersed by frugivorous birds and with a fruiting period of 9 months. We evaluated quantity and quality in different microhabitats of a Mediterranean forest and different periods of the fruiting phenophase. We identified the bird species responsible for seed deposition through DNA barcoding and evaluated the probability of seedling recruitment through a series of field experiments on sequential demographic processes. We found that timing matters: The disperser assemblage was temporally structured, seed viability decreased markedly during the plant's fruiting phenophase, and germination was lower for viable seeds dispersed in the fruiting peak. We show how small contributions to seed deposition by transient migratory species can result in a relevant effectiveness if they disperse seeds in a high-quality period for seedling recruitment. This study expands our understanding of seed dispersal effectiveness, highlighting the importance of timing and infrequent interactions for population and community dynamics.

Moving from frugivory to seed dispersal: Incorporating the functional outcomes of interactions in plant-frugivore networks.

There is growing interest in understanding the functional outcomes of species interactions in ecological networks. For many mutualistic networks, including pollination and seed dispersal networks, interactions are generally sampled by recording animal foraging visits to plants. However, these visits may not reflect actual pollination or seed dispersal events, despite these typically being the ecological processes of interest. Frugivorous animals can act as seed dispersers, by swallowing entire fruits and dispersing their seeds, or as pulp peckers or seed predators, by pecking fruits to consume pieces of pulp or seeds. These processes have opposing consequences for plant reproductive success. Therefore, equating visitation with seed dispersal could lead to biased inferences about the ecology, evolution and conservation of seed dispersal mutualisms. Here, we use natural history information on the functional outcomes of pairwise bird-plant interactions to examine changes in the structure of seven European plant-frugivore visitation networks after non-mutualistic interactions (pulp pecking and seed predation) have been removed. Following existing knowledge of the contrasting structures of mutualistic and antagonistic networks, we hypothesized a number of changes following interaction removal, such as increased nestedness and lower specialization. Non-mutualistic interactions with pulp peckers and seed predators occurred in all seven networks, accounting for 21%-48% of all interactions and 6%-24% of total interaction frequency. When non-mutualistic interactions were removed, there were significant increases in network-level metrics such as connectance and nestedness, while robustness decreased. These changes were generally small, homogenous and driven by decreases in network size. Conversely, changes in species-level metrics were more variable and sometimes large, with significant decreases in plant degree, interaction frequency, specialization and resilience to animal extinctions and significant increases in frugivore species strength. Visitation data can overestimate the actual frequency of seed dispersal services in plant-frugivore networks. We show here that incorporating natural history information on the functions of species interactions can bring us closer to understanding the processes and functions operating in ecological communities. Our categorical approach lays the foundation for future work quantifying functional interaction outcomes along a mutualism-antagonism continuum, as documented in other frugivore faunas.

The major barriers to evidence-informed conservation policy and possible solutions.

Conservation policy decisions can suffer from a lack of evidence, hindering effective decision-making. In nature conservation, studies investigating why policy is often not evidence-informed have tended to focus on Western democracies, with relatively small samples. To understand global variation and challenges better, we established a global survey aimed at identifying top barriers and solutions to the use of conservation science in policy. This obtained the views of 758 people in policy, practice, and research positions from 68 countries across six languages. Here we show that, contrary to popular belief, there is agreement between groups about how to incorporate conservation science into policy, and there is thus room for optimism. Barriers related to the low priority of conservation were considered to be important, while mainstreaming conservation was proposed as a key solution. Therefore, priorities should focus on convincing the public of the importance of conservation as an issue, which will then influence policy-makers to adopt pro-environmental long-term policies.

Honeybee spillover reshuffles pollinator diets and affects plant reproductive success.

During the past decades, managed honeybee stocks have increased globally. Managed honeybees are particularly used within mass-flowering crops and often spill over to adjacent natural habitats after crop blooming. Here, we uniquely show the simultaneous impact that honeybee spillover has on wild plant and animal communities in flower-rich woodlands via changes in plant-pollinator network structure that translate into a direct negative effect on the reproductive success of a dominant wild plant. Honeybee spillover leads to a re-assembly of plant-pollinator interactions through increased competition with other pollinator species. Moreover, honeybee preference for the most abundant plant species reduces its seed set, driven by high honeybee visitation rates that prevent pollen tube growth. Our study therefore calls for an adequate understanding of the trade-offs between providing pollination services to crops and the effects that managed pollinators might have on wild plants and pollinators.

Unravelling seed dispersal through fragmented landscapes: Frugivore species operate unevenly as mobile links.

Seed dispersal constitutes a pivotal process in an increasingly fragmented world, promoting population connectivity, colonization and range shifts in plants. Unveiling how multiple frugivore species disperse seeds through fragmented landscapes, operating as mobile links, has remained elusive owing to methodological constraints for monitoring seed dispersal events. We combine for the first time DNA barcoding and DNA microsatellites to identify, respectively, the frugivore species and the source trees of animal-dispersed seeds in forest and matrix of a fragmented landscape. We found a high functional complementarity among frugivores in terms of seed deposition at different habitats (forest vs. matrix), perches (isolated trees vs. electricity pylons) and matrix sectors (close vs. far from the forest edge), cross-habitat seed fluxes, dispersal distances and canopy-cover dependency. Seed rain at the landscape-scale, from forest to distant matrix sectors, was characterized by turnovers in the contribution of frugivores and source-tree habitats: open-habitat frugivores replaced forest-dependent frugivores, whereas matrix trees replaced forest trees. As a result of such turnovers, the magnitude of seed rain was evenly distributed between habitats and landscape sectors. We thus uncover key mechanisms behind "biodiversity-ecosystem function" relationships, in this case, the relationship between frugivore diversity and landscape-scale seed dispersal. Our results reveal the importance of open-habitat frugivores, isolated fruiting trees and anthropogenic perching sites (infrastructures) in generating seed dispersal events far from the remnant forest, highlighting their potential to drive regeneration dynamics through the matrix. This study helps to broaden the "mobile-link" concept in seed dispersal studies by providing a comprehensive and integrative view of the way in which multiple frugivore species disseminate seeds through real-world landscapes.

Languages Are Still a Major Barrier to Global Science.

While it is recognized that language can pose a barrier to the transfer of scientific knowledge, the convergence on English as the global language of science may suggest that this problem has been resolved. However, our survey searching Google Scholar in 16 languages revealed that 35.6% of 75,513 scientific documents on biodiversity conservation published in 2014 were not in English. Ignoring such non-English knowledge can cause biases in our understanding of study systems. Furthermore, as publication in English has become prevalent, scientific knowledge is often unavailable in local languages. This hinders its use by field practitioners and policy makers for local environmental issues; 54% of protected area directors in Spain identified languages as a barrier. We urge scientific communities to make a more concerted effort to tackle this problem and propose potential approaches both for compiling non-English scientific knowledge effectively and for enhancing the multilingualization of new and existing knowledge available only in English for the users of such knowledge.

Total Bee Dependence on One Flower Species Despite Available Congeners of Similar Floral Shape.

Extreme specialization is a common phenomenon in antagonistic biotic interactions but it is quite rare in mutualistic ones. Indeed, bee specialization on a single flower species (monolecty) is a questioned fact. Here, we provide multiple lines of evidence on true monolecty in a solitary bee (Flavipanurgus venustus, Andrenidae), which is consistent across space (18 sites in SW Iberian Peninsula) and time (three years) despite the presence of closely related congeneric plant species whose flowers are morphologically similar. The host flower (Cistus crispus, Cistaceae) is in turn a supergeneralist, visited by at least 85 insect species. We uncover ultraviolet light reflectance as a distinctive visual cue of the host flower, which can be a key mechanism because bee specialization has an innate basis to recognize specific signals. Moreover, we hypothesized that a total dependence on an ephemeral resource (i.e. one flower species) must lead to spatiotemporal matching with it. Accordingly, we prove that the bee's flight phenology is synchronized with the blooming period of the host flower, and that the densities of bee populations mirror the local densities of the host flower. This case supports the 'predictable plethora' hypothesis, that is, that host-specialization in bees is fostered by plant species providing predictably abundant floral resources. Our findings, along with available phylogenetic information on the genus Cistus, suggest the importance of historical processes and cognitive constraints as drivers of specialization in bee-plant interactions.

Mass-flowering crops dilute pollinator abundance in agricultural landscapes across Europe.

Mass-flowering crops (MFCs) are increasingly cultivated and might influence pollinator communities in MFC fields and nearby semi-natural habitats (SNHs). Across six European regions and 2 years, we assessed how landscape-scale cover of MFCs affected pollinator densities in 408 MFC fields and adjacent SNHs. In MFC fields, densities of bumblebees, solitary bees, managed honeybees and hoverflies were negatively related to the cover of MFCs in the landscape. In SNHs, densities of bumblebees declined with increasing cover of MFCs but densities of honeybees increased. The densities of all pollinators were generally unrelated to the cover of SNHs in the landscape. Although MFC fields apparently attracted pollinators from SNHs, in landscapes with large areas of MFCs they became diluted. The resulting lower densities might negatively affect yields of pollinator-dependent crops and the reproductive success of wild plants. An expansion of MFCs needs to be accompanied by pollinator-supporting practices in agricultural landscapes.

The Labile Limits of Forbidden Interactions.

Forbidden links are defined as pairwise interactions that are prevented by the biological traits of the species. We focus here on the neglected importance of intraspecific trait variation in the forbidden link concept. We show how intraspecific trait variability at different spatiotemporal scales, and through ontogeny, reduces the expected prevalence of forbidden interactions. We also highlight how behavior can foster interactions that, from traits, would be predicted to be forbidden. We therefore discuss the drawbacks of frameworks recently developed to infer biotic interactions using available trait data (mean values). Mispredictions can have disproportionate effects on inferences about community dynamics. Thus, we suggest including intraspecific variability in trait-based models and using them to guide the sampling of real interactions in the field for validation.

Combined effects of global change pressures on animal-mediated pollination.

Pollination is an essential process in the sexual reproduction of seed plants and a key ecosystem service to human welfare. Animal pollinators decline as a consequence of five major global change pressures: climate change, landscape alteration, agricultural intensification, non-native species, and spread of pathogens. These pressures, which differ in their biotic or abiotic nature and their spatiotemporal scales, can interact in nonadditive ways (synergistically or antagonistically), but are rarely considered together in studies of pollinator and/or pollination decline. Management actions aimed at buffering the impacts of a particular pressure could thereby prove ineffective if another pressure is present. Here, we focus on empirical evidence of the combined effects of global change pressures on pollination, highlighting gaps in current knowledge and future research needs.

Functional diversity among seed dispersal kernels generated by carnivorous mammals.

1. Knowledge of the spatial scale of the dispersal service provided by important seed dispersers (i.e. common and/or keystone species) is essential to our understanding of their role on plant ecology, ecosystem functioning and, ultimately, biodiversity conservation. 2. Carnivores are the main mammalian frugivores and seed dispersers in temperate climate regions. However, information on the seed dispersal distances they generate is still very limited. We focused on two common temperate carnivores differing in body size and spatial ecology - red fox (Vulpes vulpes) and European pine marten (Martes martes) - for evaluating possible functional diversity in their seed dispersal kernels. 3. We measured dispersal distances using colour-coded seed mimics embedded in experimental fruits that were offered to the carnivores in feeding stations (simulating source trees). The exclusive colour code of each simulated tree allowed us to assign the exact origin of seed mimics found later in carnivore faeces. We further designed an explicit sampling strategy aiming to detect the longest dispersal events; as far we know, the most robust sampling scheme followed for tracking carnivore-dispersed seeds. 4. We found a marked functional heterogeneity among both species in their seed dispersal kernels according to their home range size: multimodality and long-distance dispersal in the case of the fox and unimodality and short-distance dispersal in the case of the marten (maximum distances = 2846 and 1233 m, respectively). As a consequence, emergent kernels at the guild level (overall and in two different years) were highly dependent on the relative contribution of each carnivore species. 5. Our results provide the first empirical evidence of functional diversity among seed dispersal kernels generated by carnivorous mammals. Moreover, they illustrate for the first time how seed dispersal kernels strongly depend on the relative contribution of different disperser species, thus on the composition of local disperser assemblages. These findings provide a key starting point for understanding and modelling plant population processes that include mammal-mediated seed dispersal, such as connectivity, range expansion and colonization.

Long-term demographic consequences of a seed dispersal disruption.

The loss or decline of vertebrate frugivores can limit the regeneration of plants that depend on them. However, empirical evidence is showing that this is still very scarce, as functionally equivalent species may contribute to maintain the mutualistic interaction. Here, we investigated the long-term consequences of the extinction of frugivorous lizards on the population persistence of a Mediterranean relict shrub Cneorum tricoccon (Cneoraceae). We examined the demographic parameters among 26 insular and mainland populations, which encompass the entire plant distributional range, comparing populations with lizards with those in which these are extinct, but in which alien mammals currently act as seed dispersers. Plant recruitment was found to be higher on island populations with lizards than on those with mammals, and the long-term effects of the native disperser's loss were found in all vital phases of plant regeneration. The study thus gives evidence of the cascading effects of human-induced changes in ecosystems, showing how the disruption of native ecological processes can lead to species regression and, in the long term, even to local extinctions.

Contrasting heterozygosity-fitness correlations between populations of a self-compatible shrub in a fragmented landscape.

The mechanisms underlying heterozygosity-fitness correlations (HFCs) are subject of intense debates, especially about how important population features such as size or degree of isolation influence HFCs. Here, we report variation in HFCs between Large and Small populations of a self-compatible shrub (Myrtus communis) occurring within an extremely fragmented landscape. In each of the five study populations, we obtained data on both heterozygosity and fitness for 9-12 maternal families (i.e. offspring from the same mother plant). Whereas heterozygosity explained most of the variance (60-86 %) in growth rate of seedling families within Large populations, this relationship was absent within Small populations. Our results suggest that inbreeding may explain the observed HFCs within Large populations, and that different genetic processes (such as genetic drift and/or selection) could have overridden HFCs within Small populations. While it is difficult to draw general conclusions from five populations, we think our results open new research perspectives on how different genetic processes underlie variation in HFCs under different population contexts. Our study also points to a need for further attention on the complex relationships between heterozygosity in self-compatible plants and their progeny in relation to mating system variation. Finally, our results provide interesting new insights into how population genetic diversity is maintained or lost in a highly fragmented landscape.

Frugivory and spatial patterns of seed deposition by carnivorous mammals in anthropogenic landscapes: a multi-scale approach.

BACKGROUND: Knowledge about how frugivory and seed deposition are spatially distributed is valuable to understand the role of dispersers on the structure and dynamics of plant populations. This may be particularly important within anthropogenic areas, where either the patchy distribution of wild plants or the presence of cultivated fleshy-fruits may influence plant-disperser interactions. METHODOLOGY/PRINCIPAL FINDINGS: We investigated frugivory and spatial patterns of seed deposition by carnivorous mammals in anthropogenic landscapes considering two spatial scales: 'landscape' (∼10 km(2)) and 'habitat type' (∼1-2 km(2)). We sampled carnivore faeces and plant abundance at three contrasting habitats (chestnut woods, mosaics and scrublands), each replicated within three different landscapes. Sixty-five percent of faeces collected (n = 1077) contained seeds, among which wild and cultivated seeds appeared in similar proportions (58% and 53%) despite that cultivated fruiting plants were much less abundant. Seed deposition was spatially structured among both spatial scales being different between fruit types. Whereas the most important source of spatial variation in deposition of wild seeds was the landscape scale, it was the habitat scale for cultivated seeds. At the habitat scale, seeds of wild species were mostly deposited within mosaics while seeds of cultivated species were within chestnut woods and scrublands. Spatial concordance between seed deposition and plant abundance was found only for wild species. CONCLUSIONS/SIGNIFICANCE: Spatial patterns of seed deposition by carnivores differed between fruit types and seemed to be modulated by the fleshy-fruited plant assemblages and the behaviour of dispersers. Our results suggest that a strong preference for cultivated fruits by carnivores may influence their spatial foraging behaviour and lower their dispersal services to wild species. However, the high amount of seeds removed within and between habitats suggests that carnivores must play an important role--often overlooked--as 'restorers' and 'habitat shapers' in anthropogenic areas.