Seed-dispersal Interactions Research Articles

Species-level drivers of avian centrality within seed-dispersal networks across different levels of organisation.

Bird-plant seed-dispersal networks are structural components of ecosystems. The role of bird species in seed-dispersal networks (from less [peripheral] to more connected [central]), determines the interaction patterns and their ecosystem services. These roles may be driven by morphological and functional traits as well as evolutionary, geographical and environmental properties acting at different spatial extents. It is still unknown if such drivers are equally important in determining species centrality at different network levels, from individual local networks to the global meta-network representing interactions across all local networks. Using 308 networks covering five continents and 11 biogeographical regions, we show that at the global meta-network level species' range size was the most important driver of species centrality, with more central species having larger range sizes, which would facilitate the interaction with a higher number of plants and thus the maintenance of seed-dispersal interactions. At the local network level, body mass was the only driver with a significant effect, implying that local factors related to resource availability are more important at this level of network organisation than those related to broad spatial factors such as range sizes. This could also be related to the mismatch between species-level traits, which do not consider intraspecific variation, and the local networks that can depend on such variation. Taken together, our results show that the drivers determining species centrality are relative to the levels of network organisation, suggesting that prediction of species functional roles in seed-dispersal interactions requires combined local and global approaches.

Seasonal variation in impact of non‐native species on tropical seed dispersal networks

Abstract Invasive non‐native species can alter animal‐mediated seed dispersal interactions and ultimately affect the stability of recipient communities. The degree of such disturbances, however, is highly variable and depends on several factors, two of which have received little attention: the relative timing of native and non‐native fruiting phenologies, and the associated variation in relative resource availability across the fruiting period. Both are likely to alter plant–seed disperser interactions threatened by biological invasions. Here we investigated the impact of plant invasions on the seasonal dynamics of frugivory and seed dispersal networks across a large‐scale experimental setup and a plant invasion gradient on a tropical island. We recorded fruit and frugivore abundances, and plant–frugivore interactions across eight inselbergs (i.e. rocky outcrops) with different levels of plant invasion during 10 months on the island of Mahé, Seychelles. By combining four sampling methods of plant–frugivore interactions we constructed quantitative seed dispersal networks at all sites across two 5‐month seasons: the on‐peak and off‐peak fruiting season. Our findings showed that, by fruiting mostly synchronously with natives, non‐native plants compete with natives for dispersal services, predominantly carried out by native frugivores. Variation in native seed dispersal was driven by plant invasion and seasonality. Specifically, native seed dispersal declined with the degree of invasion; dispersal frequency increased with fruit abundance more strongly during the off‐peak fruiting season; and networks became increasingly specialised during off‐peak. These results indicated that during the main fruiting peak seed dispersal services were saturated, which likely intensified the competition between native and non‐native fruits. When resources were scarce during off‐peak fruiting season, native and non‐native frugivores were more selective in their fruit choice at sites dominated by non‐native plants. We showed that native plant and frugivore populations and native seed dispersal interactions were more vulnerable in invaded plant communities, where non‐native plants compete with natives for dispersal services potentially reducing native recruitment. As invasive non‐native plants dominate many ecosystems world‐wide, particularly on islands, our findings showed that controlling plant invasions in vulnerable native communities can be critical to maintain native ecosystem functions and biodiversity. Read the free Plain Language Summary for this article on the Journal blog.

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 949seed-dispersal interactions between 46bird and 81plant species from 13woodland 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.

Accelerating homogenization of the global plant-frugivore meta-network.

Introductions of species by humans are causing the homogenization of species composition across biogeographic barriers1-3. The ecological and evolutionary consequences of introduced species derive from their effects on networks of species interactions4,5, but we lack a quantitative understanding of the impacts of introduced species on ecological networks and their biogeographic patterns globally. Here we address this data gap by analysing mutualistic seed-dispersal interactions from 410 local networks, encompassing 24,455 unique pairwise interactions between 1,631 animal and 3,208 plant species. We show that species introductions reduce biogeographic compartmentalization of the global meta-network, in which nodes are species and links are interactions observed within any local network. This homogenizing effect extends across spatial scales, decreasing beta diversity among local networks and modularity within networks. The prevalence of introduced interactions is directly related to human environmental modifications and is accelerating, having increased sevenfold over the past 75 years. These dynamics alter the coevolutionary environments that mutualists experience6, and we find that introduced species disproportionately interact with other introduced species. These processes are likely to amplify biotic homogenization in future ecosystems7 and may reduce the resilienceof ecosystems by allowing perturbations to propagate more quickly and exposing disparate ecosystems to similar drivers. Our results highlight the importance of managing the increasing homogenization of ecological complexity.

Estimating interaction credit for trophic rewilding in tropical forests.

Trophic rewilding has been suggested as a restoration tool to restore ecological interactions and reverse defaunation and its cascading effects on ecosystem functioning. One of the ecological processes that has been jeopardized by defaunation is animal-mediated seed dispersal. Here, we propose an approach that combines joint species distribution models with occurrence data and species interaction records to quantify the potential to restore seed-dispersal interactions through rewilding and apply it to the Atlantic Forest, a global biodiversity hotspot. Using this approach, we identify areas that should benefit the most from trophic rewilding and candidate species that could contribute to cash the credit of seed-dispersal interactions in a given site. We found that sites within large fragments bearing a great diversity of trees may have about 20 times as many interactions to be cashed through rewilding as small fragments in regions where deforestation has been pervasive. We also ranked mammal and bird species according to their potential to restore seed-dispersal interactions if reintroduced while considering the biome as a whole and at finer scales. The suggested approach can aid future conservation efforts in rewilding projects in defaunated tropical rainforests.This article is part of the theme issue 'Trophic rewilding: consequences for ecosystems under global change'.

Multilayer networks reveal the spatial structure of seed-dispersal interactions across the Great Rift landscapes

Species interaction networks are traditionally explored as discrete entities with well-defined spatial borders, an oversimplification likely impairing their applicability. Using a multilayer network approach, explicitly accounting for inter-habitat connectivity, we investigate the spatial structure of seed–dispersal networks across the Gorongosa National Park, Mozambique. We show that the overall seed–dispersal network is composed by spatially explicit communities of dispersers spanning across habitats, functionally linking the landscape mosaic. Inter-habitat connectivity determines spatial structure, which cannot be accurately described with standard monolayer approaches either splitting or merging habitats. Multilayer modularity cannot be predicted by null models randomizing either interactions within each habitat or those linking habitats; however, as habitat connectivity increases, random processes become more important for overall structure. The importance of dispersers for the overall network structure is captured by multilayer versatility but not by standard metrics. Highly versatile species disperse many plant species across multiple habitats, being critical to landscape functional cohesion.

Disclosing the double mutualist role of birds on Gal\xe1pagos

Life on oceanic islands deviate in many ways from that on the mainland. Their biodiversity is relatively poor and some groups are well-represented, others not, especially not insects. A scarcity of insects forces birds to explore alternative food, such as nectar and fruit. In this way, island birds may pollinate and disperse seed to an extent unseen on any mainland; they may even first consume floral resources of a plant species and then later harvest the fruit of the same species. Through this biotic reuse, they may act as double mutualists. The latter have never been studied at the level of the network, because they are traditionally considered rare. We sampled pollination and seed-dispersal interactions on Galápagos and constructed a plant-bird mutualism network of 108 plant (12% being double mutualists) and 21 bird species (48% being double mutualists), and their 479 interactions, being either single (95%) or double mutualisms (5%). Double mutualists constitute the core in the pollination-dispersal network, coupling the two link types together. They may also initiate positive feedbacks (more pollination leading to more dispersal), which theoretically are known to be unstable. Thus, double mutualisms may be a necessary, but risky prerequisite to the survival of island biodiversity.

Phylogenetic and Functional Diversity of Fleshy-Fruited Plants Are Positively Associated with Seedling Diversity in a Tropical Montane Forest

Mutualistic interactions between plants and animals can affect both plant and animal communities, and potentially leave imprints on plant demography. Yet, no study has simultaneously tested how trait variation in plant resources shapes the diversity of animal consumers, and how these interactions influence seedling recruitment. Here, we analyzed whether i) phylogenetic diversity and functional diversity of fruiting plants were correlated with the corresponding diversity of frugivorous birds, and ii) whether phylogenetic diversity and functional identity of plant and bird communities influenced the corresponding diversity and identity of seedling communities. We recorded mutualistic interactions between fleshy-fruited plants and frugivorous birds and seedling communities in ten plots along an elevational gradient in the Colombian Andes. We built a phylogeny for plants/seedlings and birds and measured relevant morphological plant and bird traits that influence plant-bird interactions and seedling recruitment. We found that phylogenetic diversity and functional diversity of frugivorous birds were positively associated with the corresponding diversities of fruiting plants, consistent with a bottom-up effect of plants on birds. Moreover, the phylogenetic diversity of seedlings was related to the phylogenetic diversity of plants, but was unrelated to the phylogenetic diversity of frugivorous birds, suggesting that top-down effects of animals on seedlings were weak. Mean seed mass of seedling communities was positively associated with the mean fruit mass of plants, but was not associated with the mean avian body mass in the frugivore communities. Our study shows that variation in the traits of fleshy-fruited plants was associated with the diversity of frugivorous birds and affected the future trajectory of seedling recruitment, whereas the morphological traits of animal seed dispersers were unrelated to the phylogenetic and functional structure of seedling communities. These findings suggest that bottom-up effects are more important than top-down effects for seed-dispersal interactions and seedling recruitment in diverse tropical communities.

Drivers of species' role in avian seed-dispersal mutualistic networks.

The mutualistic interaction between frugivore birds and the fruiting plants they disperse presents an asymmetric interaction pattern, with some species having a more important role (i.e. being essential) for maintaining the structure and functioning of the interaction network. The identification of the biological characteristics of these species is of major importance for the understanding and conservation of seed-dispersal interactions. In this study, I use a network approach and avian seed-dispersal networks from 23 different geographical areas to test five hypotheses about species characteristics determining the structure of the assemblage. I expected (i) large birds to forage on a large number of fruits and (ii) large fruits to be dispersed by few bird species (because of morphological constraints), and (iii) highly energetic fruits to be dispersed by more bird species (in accordance with optimal foraging theory). Besides the number of interacting partners, I also expected (iv) large birds and (v) small energetic fruits to be important for the maintenance of the structure of the interactions in seed-dispersal networks. As species that are closely related are more likely to be similar to each other, I performed phylogenetically corrected analyses to account for this data dependence. Although bird size was not associated to species important in the maintenance of the structure of the seed-dispersal community, I identified that bird species whose diet was strongly dependent on fruits were important for the structure of the network. Regarding the plants, I found that large fruits were dispersed by fewer species, but the most important attribute to predict the role of a fruit was its energy content (higher energy, more bird species dispersing the plant, but low-energy fruits being of conservation concern because they are dispersed by specific species). The results of this study suggest that the role of the species in seed-dispersal assemblages seems to be determined by the role of the species as consumers (frugivory degree for animals) or by their nutritional inputs (energy content for fruits) rather than by morphological constrains.

The geographic distribution of seed-dispersal mutualisms in North America

It is often difficult to determine the relative importance of different sorts of species interactions in shaping community structure or how communities function because we lack basic information on patterns of occurrence of biotic interactions. Here we determine the geographic distribution of seed-dispersal mutualisms across North America, and then test the hypotheses that those patterns are correlated with mean annual precipitation and latitude. We analyze the floras of 197 sites across North America to identify which species of native seed plants are dispersed by animals in one of three types of plant-animal mutualisms: frugivory, scatter hoarding, and ants. We identified 1655 plant species that are involved in these seed-dispersal mutualisms. 16.5 ± 6.5% of all seed plants across North America are dispersed by animals; 10.0 ± 4.2% by frugivores, 3.7 ± 1.7% by scatter hoarders, and 3.9 ± 2.2% by ants. Secondary dispersal by a different mode and vector (e.g., wind dispersal followed by scatter hoarding, or ballistic dispersal followed by myrmecochory) occurred in 16.8% of all plant mutualist records. Although each mode of dispersal showed a different pattern, the prevalence of seed-dispersal mutualisms increased with mean annual precipitation. The prevalence of seed dispersal by frugivory and scatter-hoarding decreased with increasing latitude. The prevalence of seed-dispersal interactions varies dramatically across North America. The center of greatest diversity for all three types of seed-dispersal mutualisms is the eastern United States, roughly coincident with the eastern deciduous forest. Knowing the distribution of species interactions improves our understanding of how the structure and functioning of communities varies across environmental gradients.

Ecology of Plant-Animal Interactions: Pollination, Seed Dispersal and Tritrophic Interactions

Ecology of Plant-Animal Interactions: Pollination, Seed Dispersal and Tritrophic Interactions

Patterns of seed-dispersal interactions across temperate North America

Patterns of seed-dispersal interactions across temperate North America

Reconstructing past ecological networks: the reconfiguration of seed-dispersal interactions after megafaunal extinction.

The late Quaternary megafaunal extinction impacted ecological communities worldwide, and affected key ecological processes such as seed dispersal. The traits of several species of large-seeded plants are thought to have evolved in response to interactions with extinct megafauna, but how these extinctions affected the organization of interactions in seed-dispersal systems is poorly understood. Here, we combined ecological and paleontological data and network analyses to investigate how the structure of a species-rich seed-dispersal network could have changed from the Pleistocene to the present and examine the possible consequences of such changes. Our results indicate that the seed-dispersal network was organized into modules across the different time periods but has been reconfigured in different ways over time. The episode of megafaunal extinction and the arrival of humans changed how seed dispersers were distributed among network modules. However, the recent introduction of livestock into the seed-dispersal system partially restored the original network organization by strengthening the modular configuration. Moreover, after megafaunal extinctions, introduced species and some smaller native mammals became key components for the structure of the seed-dispersal network. We hypothesize that such changes in network structure affected both animal and plant assemblages, potentially contributing to the shaping of modern ecological communities. The ongoing extinction of key large vertebrates will lead to a variety of context-dependent rearranged ecological networks, most certainly affecting ecological and evolutionary processes.

Forest fragmentation and edge effects on the genetic structure ofClusia sphaerocarpaandC. lechleri(Clusiaceae) in tropical montane forests

Abstract:Fragmentation of tropical forests influences abiotic and biotic processes that affect the genetic structure of plant populations. In forest fragments, edge effects, i.e. changes of abiotic and biotic factors at forest edges, may be prevalent. In two forest fragments (c. 200 ha atc. 2450 m asl) of tropical montane forest in Bolivia, sympatric populations of the dioecious tree speciesClusia sphaerocarpaandC. lechleriwere used as case study species to compare genetic diversity and small-scale genetic structure (SGS) between edge and interior habitats. Eight microsatellite markers were employed to genotype 343 individuals including adults, juveniles and seedlings ofC. sphaerocarpaand 196 ofC. lechleri. Genetic differentiation was found between habitats in both species (ΦRT= 0.071 forC. sphaerocarpaand ΦRT= 0.028 forC. lechleri) and among ages inC. sphaerocarpa(ΦRT= 0.016). Overall, SGS was weak but significant with more pronounced SGS inC. lechleri(Sp= 0.0128) than inC. sphaerocarpa(Sp= 0.0073). However, positive spatial genetic autocorrelation extended only up to 10 m. ForC. sphaerocarpa, SGS was stronger in seedling and juvenile stages than in adults and in the forest interior than at forest edges. Our results show that edge effects can extend to the genetic level by breaking-up local genetic structures, probably due to increased gene flow and enhanced pollination and seed-dispersal interactions at forest edges.

The conservation physiology of seed dispersal.

At a time when plant species are experiencing increasing challenges from climate change, land-use change, harvesting and invasive species, dispersal has become a very important aspect of plant conservation. Seed dispersal by animals is particularly important because some animals disperse seeds to suitable sites in a directed fashion. Our review has two aims: (i) to highlight the various ways plant dispersal by animals can be affected by current anthropogenic change and (ii) to show the important role of plant and (particularly) animal physiology in shaping seed-dispersal interactions. We argue that large-bodied seed dispersers may be particularly important for plant conservation because seed dispersal of large-seeded plants is often more specialized and because large-bodied animals are targeted by human exploitation and have smaller population sizes. We further argue that more specialized seed-dispersal systems on island ecosystems might be particularly at risk from climate change both owing to small population sizes involved but also owing to the likely thermal specialization, particularly on tropical islands. More generally, the inherent vulnerability of seed-dispersal mutualisms to disruption driven by environmental change (as well as their ubiquity) demands that we continue to improve our understanding of their conservation physiology.

Influence of habitat complexity and landscape configuration on pollination and seed-dispersal interactions of wild cherry trees

Land-use intensification is a major cause for the decline in species diversity in human-modified landscapes. The loss of functionally important species can reduce a variety of ecosystem functions, such as pollination and seed dispersal, but the intricate relationships between land-use intensity, biodiversity and ecosystem functioning are still contentious. Along a gradient from forest to intensively used farmland, we quantified bee species richness, visitation rates of bees and pollination success of wild cherry trees (Prunus avium). We analysed the effects of structural habitat diversity at a local scale and of the proportion of suitable habitat around each tree at a landscape scale. We compared these findings with those from previous studies of seed-dispersing birds and mammals in the same model system and along the same land-use gradient. Bee species richness and visitation rates were found to be highest in structurally simple habitats, whereas bird species richness--but not their visitation rates--were highest in structurally complex habitats. Mammal visitation rates were only influenced at the landscape scale. These results show that different functional groups of animals respond idiosyncratically to gradients in habitat and landscape structure. Despite strong effects on bees and birds, pollination success and bird seed removal did not differ along the land-use gradient at both spatial scales. These results suggest that mobile organisms, such as bees and birds, move over long distances in intensively used landscapes and thereby buffer pollination and seed-dispersal interactions. We conclude that measures of species richness and interaction frequencies are not sufficient on their own to understand the ultimate consequences of land-use intensification on ecosystem functioning.

The evolutionary ecology of nut dispersal

A variety of nut-producing plants have mutualistic seed-dispersal interactions with animals (rodents and corvids) that scatter hoard their nuts in the soil. The goals of this review are to summarize the widespread horticultural, botanical, and ecological literature pertaining to nut dispersal inJuglans, Carya, Quercus, Fagus, Castanae, Castanopsis, Lithocarpus, Corylus, Aesculus, andPrunus; to examine the evolutionary histories of these mutualistic interactions; and to identify the traits of nut-bearing plants and nut-dispersing rodents and jays that influence the success of the mutualism. These interactions appear to have originated as early as the Paleocene, about 60 million years ago. Most nuts appear to have evolved from ancestors with wind-dispersed seeds, but the ancestral form of dispersal in almonds (Prunus spp.) was by frugivorous animals that ingested fruit.