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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.

Climate change is forcing the redistribution of life on Earth at an unprecedented velocity 1,2 . Migratory birds are thought to help plants to track climate change through long-distance seed dispersal 3,4 . 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.

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.

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 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., (© 2018 John Wiley & Sons Ltd.)

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., (© 2017 John Wiley & Sons Ltd.)

Ecologists have long recognized that seed dispersal mutualisms trigger natural regeneration and range expansion of animal‐dispersed trees. Yet we lack empirical studies addressing whether frugivore activity influences founder effects, which reduce genetic diversity at the colonization front of expanding populations.Here, we evaluate the contribution, from both demographic and genetic perspectives, of animal frugivores dispersing seeds across an expansion gradient. We used DNA barcoding for frugivores identification and highly polymorphic genetic markers (SSRs) for maternal analysis of juniper seeds to investigate how (1) stand maturity, (2) microhabitat types and (3) foraging patterns shape the distribution of the maternal progenies along this gradient.We expect both reduced seed rain density and low numbers of source trees contributing to the seed rain at the colonization front, with limited availability of local fruiting trees. We also anticipated that large‐sized frugivore species would promote maternally rich seed rain due to their ability to mix seed progenies during digestive processing and move further distances across the landscape.Contrary to our expectations, we found that all identified frugivores produced dense and genetically diverse seed rains across the expansion gradient, even at the colonization front, characterized by scarce fruiting trees.Synthesis: Our findings shed light on the fundamental and applied implications of plant–frugivore interactions in shaping highly diverse second‐growth forests. These results emphasize the necessity of preserving plant–animal mutualistic interactions to ensure the persistence and expansion of natural tree populations, particularly in formerly fragmented landscapes [ABSTRACT FROM AUTHOR]

The consequences of plant–animal interactions often transcend the mere encounter stage, as those encounters are followed by a chain of subsequent stages on the plant's reproductive cycle that ultimately determine fitness. Yet, the dissemination and recruitment stages of animal‐mediated seed dispersal are seldom analysed jointly, hindering a full understanding of the ecology of seed dispersal.We analyse the dispersal and recruitment of a fleshy‐fruited plant (Pistacia lentiscus), from fruit production to seedling survival up to their second year. We link early reproductive investment of individual plants to seedling recruitment and explore the role played by seed viability, the coterie of frugivores and microhabitat seed deposition.The proportion of viable seeds was generally low (mean = 34%) but highly variable among individual plants (range: 0%–95%). Seed viability did not seem to have a direct effect on individual plant's recruitment.We recorded 28 bird species feeding on P. lentiscus fruits or seeds. Their contribution to plant recruitment was mainly determined by their intensity of fruit consumption and probability to disperse viable seeds. Most frugivores presented non‐random microhabitat preferences, delivering uneven seed contributions to different sites.Post‐dispersal seed predation by rodents was the most limiting phase in P. lentiscus recruitment. Yet, microhabitats showing the lowest predation rates received the lowest seed rain. Hence, we found a decoupling of the dissemination and recruitment stages: most seeds do not arrive at the most suitable microhabitats.We estimate P. lentiscus plants need to produce c. 5 × 105 fruits to recruit a single seedling that survives to its second summer in our study site. Its success as a prevalent species in Mediterranean lowland landscapes relies on its high fecundity and thorough fruit removal and dispersal by a diversified frugivore assemblage, which compensates for the high seed unviability characteristic of this genus.Synthesis: Measuring the delayed, post‐dispersal outcomes of animal frugivory interactions may overturn inferences based on consumption observations only. Seed rain patterns are often decoupled from microhabitats' suitability for seedling recruitment. Hence, more integrative studies that encompass the entire plant reproductive cycle (from fruit production to seedling recruitment) are needed to fully understand frugivores' lasting contribution to plant regeneration in natural populations. [ABSTRACT FROM AUTHOR]

Plant–animal mutualisms such as seed dispersal are key interactions for sustaining plant range shifts. It remains elusive whether the organization of interactions with seed dispersers is reconfigured along the expansion landscape template and, if so, whether its effects accelerate or slow colonization. Here we analyse plant–frugivore interactions in a scenario of rapid population expansion of a Mediterranean juniper. We combined network analyses with field surveys, sampling interactions between individual plants and frugivores by DNA-barcoding and phototrapping over two seasons. We assess the role of intrinsic and extrinsic intraspecific variability in shaping interactions and we estimate the individual plant contributions to the seed rain. The whole interaction network was highly structured, with a distinct set of modules including individual plants and frugivore species arranged concordantly along the expansion gradient. The modular configuration was partially shaped by individual neighbourhood context (density and fecundity) and phenotypic traits (cone size). Interaction reconfiguration resulted in a higher and more uneven propagule contribution, with most effective dispersers having a prominent role at the colonization front stand, where a distinct subset of early arriving plants dominated the seed rain. Our study offers new insights into the key role of mutualistic interactions in colonization scenarios by promoting fast plant expansion processes. [ABSTRACT FROM AUTHOR]

We report 13 polymorphic nuclear microsatellite loci for Neochamaelea pulverulenta (Cneoraceae) using an enriched-library approach. Although this plant species is tetraploid, expected patterns for tetrasomic segregation were completely absent, and all loci analysed showed a diploid pattern of inheritance. We detected a total of 102 alleles in 57 individuals genotyped (mean number of alleles per locus was 7.85). The values of observed and expected heterozygosities ranged from 0.193 to 0.737 and 0.425 to 0.812 respectively. Disomic segregation, levels of polymorphism and the exclusionary power of the developed markers render them readily applicable for parentage assignment of dispersed seeds, and for analyses of spatial genetic structure and population connectivity. [ABSTRACT FROM AUTHOR]

Studies the demographic structure, seed set and initial recruitment in relict populations of the endangered tree Frangula alnus in the southern part of the Iberian Peninsula to evaluate its regeneration potential under present environmental conditions. Seed production; Seed dispersal; Seed recruitment; Population demographic structure.