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 km2) and 'habitat type' (~1-2 km2). 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.Conselleria de Educacion Xunta de Galicia PGIDIT 05RFO 20001 P

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

Agricultural intensification erodes taxonomic and functional diversity in Mediterranean olive groves by filtering out rare species

Agri-Environmental Schemes (AES) have been proposed to mitigate the impact of agriculture on both taxonomic and functional biodiversity. However, a better knowledge of the mechanisms involved in the loss of agrobiodiversity is needed to implement efficient AES. An unbalanced effort on research towards arable lands compared to permanent crops, and on fauna relative to plants, is patent, which limits the generalization of AES effectiveness. We evaluated the effects of agricultural management and landscape simplification on taxonomic and functional diversity of the ground herb cover of 40 olive groves. We use a recently developed approach based on Hill numbers (rare, common and dominant species based) to analyse taxonomic and functional dissimilarity between farms with contrasting agricultural practices, and its potential attenuation by landscape complexity. We further explore the filtering effect of agricultural intensification on functional traits, and the relationship between functional and species richness across landscapes. We found that taxonomic and functional dissimilarity of herb assemblages between intensively and low-intensively managed fields was mainly due to rare species. Dissimilarity decreased as landscape complexity increased, evidencing that complex landscapes attenuate the impact of agriculture intensification on herb assemblage composition. Agricultural intensification favoured more functionally homogeneous assemblages and disfavoured the herbs pollinated by insects, while it did not seem to affect wind-pollinated species. Overall, functional richness increased exponentially with species richness across landscapes, but the latter was insufficient to drive any clear enhancement in functional richness in simple landscapes. In contrast, high species richness accelerated the enhancement in functional richness in intermediate and complex landscapes. These results highlight the functional filtering that intensive agriculture has generated for decades in homogeneous olive-dominated landscapes. Synthesis and applications. Herb cover is essential to support the fauna of permanent croplands and their sustainable production. Hence, Agri-Environmental Schemes (AES) in these croplands should promote management practices favouring the diversity and functionality of herb assemblages. Such AES should be particularly prioritized in homogeneous landscapes, where ground herb cover composition and function has long been homogenized to a great extent

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.This study was funded by grants (to P.J.) of the Spanish MINECO (CGL2013-47429P) and Junta de Andalucía Excellence Projects (RNM-5731), and 632 supported by a Severo Ochoa Award for Centres of Excellence in R+D+I (SEV-2012-0262). While writing this paper, J.P.G.V. was funded by an Individual Fellowship from the Marie 634 Sklodowska-Curie Actions (H2020-MSCA- IF-2014-656572: MobileLinks). C.C. received scholarships from the National Counsel of Technological and Scientific Development (CNPq, 636 401258/2012-2) and the São Paulo Research Foundation (FAPESP, 2014/01029-5)

Increasing efficiency and reducing bias in the sampling of seed-dispersal interactions based on mist-netted birds

Efficient and unbiased sampling of ecological interactions is essential to our understanding of the functions they mediate. Seed dispersal by frugivorous birds is a key mutualism for plant regeneration and community dynamics. Mist-netting is one of the most widely used methods to sample avian seed dispersal through the identification of seeds in droppings of captured birds kept inside cloth bags. However, birds may drop seeds on the ground before being extracted from the net, leading to a fraction of missing information due to ineffective sampling. Worryingly, this fraction could be unevenly distributed across bird and plant species, leading to sampling biases. Here, we assess the effectiveness of using a 1-m wide mesh below mist nets to sample seeds dropped by entangled birds. We used data from birds mist-netted during one-year-round. We sampled nearly 50% of interaction events and 75% of dispersed seeds on the mesh band below the mist nets (i.e. lost information without this optimization). The proportion of seeds sampled on the mesh bands was not evenly distributed among bird species but strongly related to bird size, ranging from 57–63% in warblers to 84–94% in thrushes. Moreover, the proportion of seeds sampled on the mesh was negatively related to seed size, although this relationship was weaker. We also evaluated accumulation curves of species and pairwise interactions with increasing sampling effort, both with and without using the mesh bands. The number of seed species sampled increased by 21% when using the mesh bands and the number of pairwise interactions by 36%. Our findings provide strong evidence on how inefficient and biased traditional mist-netting can be for sampling community-wide seed–dispersal interactions. We thus urge the use of mesh bands in future studies to increase sampling effectiveness and avoid biases, which will ultimately improve our understanding of the seed dispersal function

Pisos bioclimáticos para la Cuenca Mediterránea como capas SIG de acceso abierto

Entender cómo se distribuye la biodiversidad terrestre y los tipos de vegetación en relación con el clima es fundamental en ecología. Se han desarrollado diversos sistemas bioclimáticos para clasificar las zonas de vida del planeta. Entre ellos, el sistema de clasificación bioclimática global de Rivas-Martínez permite categorizar el territorio en pisos bioclimáticos a partir de variables climáticas. De este modo, los continuos climáticos se expresan como categorías discretas que resultan útiles para hacer inferencias sobre las comunidades ecológicas y el funcionamiento de los ecosistemas. Sin embargo, la distribución de los pisos bioclimáticos no está disponible ni completamente ni de forma unificada para el conjunto de la Cuenca Mediterránea, un punto caliente de biodiversidad con gran amplitud bioclimática. En el presente trabajo, hemos solventado este vacío de información siguiendo las reglas del sistema de clasificación bioclimática global de Rivas-Martínez para generar un mapa de pisos bioclimáticos de toda la Cuenca Mediterránea, a una resolución de 30 segundos (~ 1 km). Para ello, hemos utilizado las bases de datos de temperatura de WorldClim y el software R como Sistema de Información Geográfica (SIG) para operar con las capas ráster de interés (índices de temperatura positiva, de continentalidad, de termicidad, y de termicidad compensado). El código R y las capas bioclimáticas resultantes están disponibles tanto en formato vectorial como ráster en un repositorio de acceso abierto.Understanding how the distribution of terrestrial biodiversity and vegetation types relate to climate is a fundamental goal in ecology. Several bioclimatic systems have been developed to classify the life zones of the world. Among them, the global bioclimatic classification system by Rivas-Martínez allows to categorize the territory into bioclimatic belts according to climatic variables. This way, climatic continua are expressed as discrete categories that prove useful for inference about ecological communities and ecosystem functioning. However, the distribution of bioclimatic belts is not available either fully or in an unified way for the whole Mediterranean Basin, a biodiversity hotspot including a large bioclimatic breadth. To fill this information gap, we followed the rules of the global bioclimatic classification system of Rivas-Martínez and generated a bioclimatic belt map of the whole Mediterranean Basin at a resolution of 30 seconds (~1 km). We used the WorldClim temperature database and the R software as a Geographic Information System (GIS) to operate with the raster layers of interest (indices of positive temperature, continentality, thermicity, and compensated thermicity). The R code and resulting bioclimatic layers in vector and raster formats are available in an open access repository

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

1. 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. 2. 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. 3. 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 hypothesised a number of changes following interaction removal, such as increased nestedness and lower specialisation. 4. 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, specialisation and resilience to animal extinctions, and significant increases in frugivore species strength. 5. 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.B.I.S. was supported by the Natural Environment Research Council as part of the Cambridge Earth System Science NERC DTP (NE/L002507/1). J.P.G.‐V. was funded by an Individual Fellowship from the Marie Sklodowska‐Curie Actions (H2020‐MSCA‐IF‐2014‐656572: MobileLinks). D.G. was funded by a grant from the Spanish MinECo (CGL2017‐82847‐P). W.J.S. is funded by Arcadia. N.F. thanks the administration of the Białowieża National Park, the forestry administrations of Białowieża, Hajnówka and Browsk and Polish authorities (Ministry of Environment, GDOS and RDOS) for the permissions to work in Białowieża Forest. J.A. was supported by the German Federal Foundation for Environment (DBU) and by the German Academic Exchange Service in the framework of a post‐doctorate fellowship grant (DAAD, No 91568794). L.V.D. was supported by the Natural Environment Research Council (grants NE/K015419/1 and NE/N014472/1)

Who dispersed the seeds? The use of DNA barcoding in frugivory and seed dispersal studies

Assessing dispersal events in plants faces important challenges and limitations. A methodological issue that limits advances in our understanding of seed dissemination by frugivorous animals is identifying 'which species dispersed the seeds'. This is essential for assessing how multiple frugivore species contribute distinctly to critical dispersal events such as seed delivery to safe sites, long-distance dispersal and the colonization of non-occupied habitats. Here, we describe DNA-barcoding protocols successfully applied to bird-dispersed seeds sampled in the field. Avian DNA was extracted from the surface of defecated or regurgitated seeds, allowing the identification of the frugivore species that contributed each dispersal event. Disperser species identification was based on a 464-bp mitochondrial DNA region (COI: cytochrome c oxidase subunit I). We illustrate the possible applications of this method with bird-dispersed seeds sampled in the field. DNA-barcoding provides a non-invasive technique that allows quantifying frugivory and seed dispersal interaction networks, assessing the contribution of each frugivore species to seed rain in different microhabitats, and testing whether different frugivore species select different fruit/seed sizes. DNA barcoding of animal-dispersed seeds can resolve the distribution of dispersal services provided by diverse frugivore assemblages, allowing a robust and precise estimation of the different components of seed dispersal effectiveness, previously unattainable to traditional field studies at individual seed level. Given that seeds are sampled at the end of the dispersal process, this technique enables us to link the identity of the disperser species responsible for each dispersal event to plant traits and environmental features, thereby building a bridge between frugivory and seed deposition patterns. © 2014 British Ecological Society.Peer Reviewe

DatasetBarcodingSeedDispersal_GonzalezVaro_Arroyo_Jordano

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Data from: Who dispersed the seeds? The use of DNA barcoding in frugivory and seed dispersal studies

1. Assessing dispersal events in plants faces important challenges and limitations. A methodological issue that limits advances in our understanding of seed dissemination by frugivorous animals is identifying ‘which species dispersed the seeds’. This is essential for assessing how multiple frugivore species contribute distinctly to critical dispersal events such as seed delivery to safe sites, long-distance dispersal, and the colonization of non-occupied habitats. 2. Here we describe DNA barcoding protocols successfully applied to bird-dispersed seeds sampled in the field. Avian DNA was extracted from the surface of defecated or regurgitated seeds, allowing the identification of the frugivore species that contributed each dispersal event. Disperser species identification was based on a 464-bp mitochondrial DNA region (COI: cytochrome c oxidase subunit I). 3. We illustrate the possible applications of this method with bird-dispersed seeds sampled in the field. DNA barcoding provides a non-invasive technique that allows quantifying frugivory and seed dispersal interaction networks, assessing the contribution of each frugivore species to seed rain in different microhabitats, and testing whether different frugivore species select different fruit/seed sizes. 4. DNA barcoding of animal-dispersed seeds can resolve the distribution of dispersal services provided by diverse frugivore assemblages, allowing a robust and precise estimation of the different components of seed dispersal effectiveness, previously unattainable to traditional field studies at individual seed level. Given that seeds are sampled at the end of the dispersal process, this technique enables us to link the identity of the disperser species responsible for each dispersal event to plant traits and environmental features, thereby building a bridge between frugivory and seed deposition patterns