Frugivory and seed dispersal in the Cerrado: Network structure and defaunation effects

Seed dispersal is a fundamental process that is highly threatened by the rapid decline of large-bodied frugivores worldwide. The Brazilian Cerrado, the largest savanna in the world, represents an ideal site for investigating seed dispersal because of its biodiversity, environmental challenges, and knowledge shortfalls. We performed a systematic literature review to analyze the seed dispersal network in the Cerrado and the potential impacts of the defaunation of large-bodied frugivores on it. We considered network metrics, calculated the defaunation index of the frugivore assemblage, and compared traits among different fruit-sized plants and their respective dispersers in the network. We retrieved 1565 interactions involving 193 plant species and 270 animal species. Results show that the Cerrado seed dispersal network is slightly nested and considerably modular, dominated by small- to medium-sized generalist species, such as passerines, marsupials, and mesocarnivores. Nonetheless, large-bodied frugivores like the lowland tapir have a key role in the network due to their great foraging and network integration capacity. The Cerrado frugivore assemblage is moderately defaunated, with possible effects in its interactions with large-fruited plants. The Cerrado's defaunation and functional loss of large vertebrates deserve urgent attention to further understand the impacts on seed dispersal mechanisms and ecosystem functioning.     

Incorporating seed fate into plant–frugivore networks increases interaction diversity across plant regeneration stages

Plant–animal mutualistic interactions, such as pollination and seed dispersal, affect ecosystem functioning by driving plant population dynamics. However, little is known of how the diversity of interactions in these mutualistic networks determines plant regeneration dynamics. To fill this gap, interaction networks should not only account for the number of seeds dispersed by animals, but also for seed fate after dispersal. Here, we compare plant–animal networks at both the seed dispersal and seedling recruitment stage to evaluate how interaction diversity, represented by different network metrics, changes throughout the process of plant regeneration. We focused on a system with six species of frugivorous birds and three species of fleshy‐fruited trees in the temperate secondary forest of the Cantabrian Range (northern Iberian Peninsula). We considered two plant cohorts corresponding to two fruiting years showing strong differences in fruit and frugivore abundance. Seed dispersal interactions were estimated from a spatially‐explicit, field‐validated model predicting tree and bird species‐specific seed deposition in different microhabitats. These interactions were further transformed into interactions at the seedling recruitment stage by accounting for plant‐ and microhabitat‐specific seed fates estimated from field sampling. We found that network interaction diversity varied across plant regeneration stages and cohorts, both in terms of the evenness and the number of paired interactions. Tree–bird interactions were more evenly distributed across species pairs at the recruitment stage than at the seed deposition stage, although some interactions disappeared in the seed‐to‐seedling transition for one plant cohort. The variations in interaction diversity were explained by between‐plant differences in post‐dispersal seed fate and in inter‐annual fruit production, rather than by differences between frugivores in seed deposition patterns. These results highlight the need for integrating plant traits and disperser quality to predict the functional outcome of plant–animal mutualistic networks.     

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.     

Can network metrics predict vulnerability and species roles in bird‐dispersed plant communities? Not without behaviour

Network metrics are widely used to infer the roles of mutualistic animals in plant communities and to predict the effect of species' loss. However, their empirical validation is scarce. Here we parameterized a joint species model of frugivory and seed dispersal with bird movement and foraging data from tropical and temperate communities. With this model, we investigate the effect of frugivore loss on seed rain, and compare our predictions to those of standard coextinction models and network metrics. Topological coextinction models underestimated species loss after the removal of highly linked frugivores with unique foraging behaviours. Network metrics informed about changes in seed rain quantity after frugivore loss. However, changes in seed rain composition were only predicted by partner diversity. Nestedness, closeness, and d’ specialisation could not anticipate the effects of rearrangements in plant–frugivore communities following species loss. Accounting for behavioural differences among mutualists is critical to improve predictions from network models.     

Plant–frugivore networks are less specialized and more robust at forest–farmland edges than in the interior of a tropical forest

Forest fragmentation and local disturbance are prevailing threats to tropical forest ecosystems and affect frugivore communities and animal seed dispersal in different ways. However, very little is known about the effects of anthropogenic forest edges and of local disturbance on the structure and robustness of plant–frugivore networks. We carried out focal tree observations to record the frugivore species feeding on eight canopy tree species in the forest interior and at forest–farmland edges in a little and a highly disturbed part of a Kenyan rain forest. For each frugivore species, we recorded its body mass and its forest dependence. We examined how forest edge and local disturbance affected the abundance, the richness and the composition of the frugivore community and tested whether forest edge and local disturbance affected plant frugivore networks. Abundance and species richness of frugivores were higher at edges than in the forest interior. Forest visitors and small‐bodied frugivores increased, while forest specialists decreased in abundance at forest edges. The changes in frugivore community composition resulted in plant–frugivore networks that were more connected, more nested and more robust against species extinctions at forest–farmland edges than in the forest interior. Network specialization was lower at forest edges than in the forest interior because at the edges plant specialization on frugivores was very low in small‐fruited species. In contrast, small‐fruited plants were more specialized than large‐fruited plants in the forest interior. Our findings suggest that forest‐visiting birds may stabilize seed‐dispersal services for small‐fruited plant species at rain forest margins, while seed‐dispersal services for large‐fruited plant species may be disrupted at forest edges due to the decrease of large‐bodied frugviores. To assess the ultimate consequences of bird movements from farmland to forest edges for ecosystem functioning, future studies are required to investigate the seed‐dispersal qualities provided by forest‐visiting bird species in the tropics.     

Generalist Species Have a Central Role In a Highly Diverse Plant–Frugivore Network

Analysis of plant–frugivore interactions provides a quantitative framework for integrating community structure and ecosystem function in terms of how the roles and attributes of individual species contribute to network structure and resilience. In this study, we used centrality metrics to rank and detect the most important species in a mutualistic network of fruit‐eating birds and plants in a cloud forest in the Colombian Andes. We identified a central core of ten bird and seven plant species in a network of 135 species that perform dual roles as local hubs and connectors. The birds were mostly large forest frugivores, such as cracids, cotingas, and toucans, which consume fruits of all sizes. The plants were species of intermediate successional stages with small‐ to medium‐sized seeds that persist in mature forest or forest borders (e.g., Miconia, Cecropia, Ficus). We found the resilience of our network depends on super‐generalist species, because their elimination makes the network more prone to disassemble than random extinctions, potentially disrupting seed‐dispersal processes. At our study site, extirpation of large frugivores has already been documented, and if this continues, the network might collapse despite its high diversity. Our results suggest that generalist species play critical roles in ecosystem function and should be incorporated into conservation and monitoring programs.     

Reliability of macaques as seed dispersers

Seed dispersal is an ecological process crucial for forest regeneration and recruitment. To date, most studies on frugivore seed dispersal have used the seed dispersal effectiveness framework and have documented seed-handling mechanisms, dispersal distances and the effect of seed handling on germination. In contrast, there has been no exploration of “disperser reliability” which is essential to determine if a frugivore is an effective disperser only in particular regions/years/seasons or across a range of spatio-temporal scales. In this paper, we propose a practical framework to assess the spatial reliability of frugivores as seed dispersers. We suggest that a frugivore genus would be a reliable disperser of certain plant families/genera if: (a) fruits of these plant families/genera are represented in the diets of most of the species of that frugivore, (b) these are consumed by the frugivore genus across different kinds of habitats, and (c) these fruits feature among the yearly staples and preferred fruits in the diets of the frugivore genus. Using this framework, we reviewed frugivory by the genus Macaca across Asia to assess its spatial reliability as seed dispersers. We found that the macaques dispersed the seeds of 11 plant families and five plant genera including at least 82 species across habitats. Differences in fruit consumption/preference between different groups of macaques were driven by variation in plant community composition across habitats. We posit that it is essential to maintain viable populations of macaques across their range and keep human interventions at a minimum to ensure that they continue to reliably disperse the seeds of a broad range of plant species in the Anthropocene. We further suggest that this framework be used for assessing the spatial reliability of other taxonomic groups as seed dispersers.     

Integrating frugivory and animal movement: a review of the evidence and implications for scaling seed dispersal

General principles about the consequences of seed dispersal by animals for the structure and dynamics of plant populations and communities remain elusive. This is in part because seed deposition patterns emerge from interactions between frugivore behaviour and the distribution of food resources, both of which can vary over space and time. Here we advocate a frugivore‐centred, process‐based, synthetic approach to seed dispersal research that integrates seed dispersal ecology and animal movement across multiple spatio‐temporal scales. To guide this synthesis, we survey existing literature using paradigms from seed dispersal and animal movement. Specifically, studies are discussed with respect to five criteria: selection of focal organisms (animal or plant); measurement of animal movement; characterization of seed shadow; animal, plant and environmental factors included in the study; and scales of the study. Most studies focused on either frugivores or plants and characterized seed shadows directly by combining gut retention time with animal movement data or indirectly by conducting maternity analysis of seeds. Although organismal traits and environmental factors were often measured, they were seldom used to characterize seed shadows. Multi‐scale analyses were rare, with seed shadows mostly characterized at fine spatial scales, over single fruiting seasons, and for individual dispersers. Novel animal‐ and seed‐tracking technologies, remote environmental monitoring tools, and advances in analytical methods can enable effective implementation of a hierarchical mechanistic approach to the study of seed dispersal. This kind of mechanistic approach will provide novel insights regarding the complex interplay between the factors that modulate animal behaviour and subsequently influence seed dispersal patterns across spatial and temporal scales.     

Species richness matters for the quality of ecosystem services: a test using seed dispersal by frugivorous birds

The positive link between biodiversity and ecosystem functioning is a current paradigm in ecological science. However, little is known of how different attributes of species assemblages condition the quality of many services in real ecosystems affected by human impact. We explore the links between the attributes of a frugivore assemblage and the quantitative and qualitative components of its derived ecosystem service, seed dispersal, along a landscape-scale gradient of anthropogenic forest loss. Both the number and the richness of seeds being dispersed were positively related to frugivore abundance and richness. Seed dispersal quality, determined by the fine-scale spatial patterns of seed deposition, mostly depended on frugivore richness. In fact, richness was the only attribute of the frugivore assemblage affecting the probability of seed dispersal into deforested areas of the landscape. The positive relationships between frugivore richness per se (i.e. independent of frugivore abundance and composition) and all components of seed dispersal suggest the existence of functional complementarity and/or facilitation between frugivores. These links also point to the whole assemblage of frugivores as a conservation target, if we aim to preserve a complete seed dispersal service and, hence, the potential for vegetation regeneration and recovery, in human-impacted landscapes.     

Importance of animal and plant traits for fruit removal and seedling recruitment in a tropical forest

The traits of animals and plants influence their interaction networks, but the significance of species' traits for the resulting ecosystem functions is poorly understood. A crucial ecosystem function in the tropics is seed dispersal by animals. While the importance of species' traits for structuring plant–frugivore networks is supported by a number of studies, no study has so far identified the functional traits determining the subsequent processes of fruit removal and seedling recruitment. Here, we conducted a comprehensive field study on fruit removal by frugivorous birds and seedling recruitment along an elevational gradient in the Colombian Andes. We measured morphological traits of birds (body mass, bill width, Kipp's index) and plants (plant height, crop mass, fruit width and seed mass) which we expected to be related to fruit removal and seedling recruitment. We tested 1) which bird and plant traits influence fruit removal, and 2) whether network metrics at plant species level, functional identities of frugivores (community‐based mean trait values) and/or plant traits were the main determinants of seedling recruitment. We found that large‐bodied bird species contributed more to fruit removal than small‐bodied bird species and that small‐sized fruits were more frequently removed than large‐sized fruits. Small plant species and plants with heavy seeds recruited more seedlings than did large plants and plants with light seeds. Network metrics and functional identities of seed dispersers were unrelated to seedling recruitment. Our findings have two important implications. First, large birds are functionally more important than small birds in tropical seed‐removal networks. Second, the detected tradeoff between fruit size and seed mass in subsequent recruitment processes suggests that the adaptability of forest plant communities to a loss of large frugivores is limited by life‐history constraints. Hence, the protection of large‐bodied frugivores is of primary importance for the maintenance of diverse tropical plant communities.     

An invasive tree alters the structure of seed dispersal networks between birds and plants in French Polynesia

Aim We studied how the abundance of the highly invasive fruit‐bearing tree Miconia calvescens DC. influences seed dispersal networks and the foraging patterns of three avian frugivores. Location Tahiti and Moorea, French Polynesia. Methods Our study was conducted at six sites which vary in the abundance of M. calvescens. We used dietary data from three frugivores (two introduced, one endemic) to determine whether patterns of fruit consumption are related to invasive tree abundance. We constructed seed dispersal networks for each island to evaluate how patterns of interaction between frugivores and plants shift at highly invaded sites. Results Two frugivores increased consumption of M. calvescens fruit at highly invaded sites and decreased consumption of other dietary items. The endemic fruit dove, Ptilinopus purpuratus, consumed more native fruit than either of the two introduced frugivores (the red‐vented bulbul, Pycnonotus cafer, and the silvereye, Zosterops lateralis), and introduced frugivores showed a low potential to act as dispersers of native plants. Network patterns on the highly invaded island of Tahiti were dominated by introduced plants and birds, which were responsible for the majority of plant–frugivore interactions. Main conclusions Shifts in the diet of introduced birds, coupled with reduced populations of endemic frugivores, caused differences in properties of the seed dispersal network on the island of Tahiti compared to the less invaded island of Moorea. These results demonstrate that the presence of invasive fruit‐bearing plants and introduced frugivores can alter seed dispersal networks, and that the patterns of alteration depend both on the frugivore community and on the relative abundance of available fruit.     

Frugivore loss limits recruitment of large-seeded trees

Although global declines in frugivores may disrupt seed dispersal mutualisms and inhibit plant recruitment, quantifying the likely reduction in plant regeneration has been difficult and rarely attempted. We use a manipulative factorial experiment to quantify dependence of recruitment on dispersal (i.e. fruit pulp removal and movement of seed away from parental area) in two large-seeded New Zealand tree species. Complete dispersal failure would cause a 66 to 81 per cent reduction in recruitment to the 2-year-old seedling stage, and synergistic interactions with introduced mammalian seed and seedling predators increase the reduction to 92 to 94 per cent. Dispersal failure reduced regeneration through effects on seed predation, germination and (especially) seedling survival, including distance- and density-dependent (Janzen-Connell) effects. Dispersal of both species is currently largely dependent on a single frugivore, and many fruits today remain uneaten. Present-day levels of frugivore loss and mammal seed and seedling predators result in 57 to 84 per cent fewer seedlings after 2 years. Our study demonstrates the importance of seed dispersal for local plant population persistence, and validates concerns about the community consequences of frugivore declines.     

Comparing the Dispersal of Large-seeded Tree Species by Frugivore Assemblagesin Tropical Montane Forest in Africa

We examined frugivore visitation and seed dispersal of five large-seeded (≥ 5 mm) tree species in tropical montane forest based on their occurrence in frugivorous primate diets: Ekebergia capensis, Olea capensis, Parinari excelsa, Prunus africana , and Syzygium guineense. A total of 21 frugivores in five assemblages ( i.e. , chimpanzees, cercopithecines, large-bodied birds, small-bodied birds, and squirrels) were observed over the study period (August 2006 and October–April 2007). We observed seed dispersal in four of five tree species studied; no dispersal was observed for P. excelsa . Frugivore assemblages did not visit tree species equally. Primates spent the most time in trees and had the largest group size. Large-bodied birds (LB) and chimpanzees dispersed the highest number of seeds per minute. LB and cercopithecines potentially dispersed the greatest number of seeds for E. capensis , and chimpanzees for S. guineense . Our analyses indicated that the mean fruiting duration of the focal tree, time in the tree, and number of species present are important predictor variables for seed dispersal by small- and large-bodied birds, and cercopithecines. The number of fruiting trees in the immediate vicinity of the focal tree further predicted seed dispersal for small-bodied birds (SB). Large-bodied birdseed dispersal also was predicted by time in tree by SB, and the number of individuals for SB and cercopithecines. Cercopithecines (CS) were further explained by the time in tree and number of species (SB & LB), and number of individuals for CS. Our study highlights the complexity of describing the relative importance of a frugivore assemblage to the dispersal of a tree species seeds.     

Can Functional Traits Predict Ecological Interactions? A Case Study Using Rain forest Frugivores and Plants in Australia

In rain forest, the large numbers of species of fleshy-fruited plants and frugivorous animals result in a large number of potential fruit–frugivore interactions, which are challenging to survey in the field. Yet, knowledge of these relationships is needed to predict consequences of changes in the frugivore assemblage for seed dispersal. In the absence of comprehensive dietary information, it may be possible to delineate between frugivores that disperse different plants using ‘functional traits,’ or morphological and behavioral attributes of frugivores that interact with differences in salient characteristics of plant species. Here we use data on the consumption of 244 Australian rain forest plant species by 38 bird species to test for associations between patterns of frugivory and birds': (1) degree of frugivory, (2) gape width, and (3) seed treatment (seed crushing or seed dispersing). Degree of frugivory and gape width explain 74 percent of the variation in the sizes of fruits consumed by frugivorous birds. Among birds that consume a substantial dietary proportion of fruit, birds with wider gapes consume larger fruits. In contrast, this relationship was not shown by birds for which fruit is only a minor dietary component. Degree of frugivory and gape width, together with seed treatment, also strongly predict the overall taxonomic composition and diversity of plants consumed by bird species. Functional classifications of frugivore species may prove useful in developing a predictive understanding of fruit–frugivore interactions in other rain forest regions where detailed dietary information is not available for most frugivores.     

Microsites of seed arrival: spatio–temporal variations in complex seed‐disperser networks

Microsites where seeds arrive during the dispersal process determine plant reproductive success, affecting the quality of dispersal. Despite their crucial role for plant recruitment, very few studies have addressed spatio–temporal variations in microsites of seed arrival in complex seed‐disperser networks. Using an endozoochorous dispersal system, we characterized the microsites of seed arrival of eight fleshy‐fruited plant species dispersed by five mammal species during two consecutive seasons across three sites in a Mediterranean environment (n = 383 feces with seeds; 261 453 seeds). We evaluated spatial and temporal variations in the probability of a seed to arrive at open microsites or at microsites with varying plant cover, considering selection by frugivores and assessing the extent to which seeds of particular species arrived under conspecifics or heterospecifics. We found strong spatio–temporal variations in the amounts of seeds of the eight target species arriving at different microsites. These variations were strongly driven by frugivores’ selection of different landscape elements (i.e. open areas and microsites dominated by different plant species), which differed from expectations based on their local availability. In general, more seeds than expected arrived at vacant (open) microsites. Using bipartite network graphs to connect seeds with their arrival microsites, we found that the proportion of seeds of fleshy‐fruited species arriving near conspecifics or heterospecifics, or at vacant microsites, varied depending on the target plant species, but also on the frugivore species dispersing it, on the study site and on the dispersal season. Our study revealed marked spatio–temporal variations in the microsites of seed arrival, which will potentially have implications for the quality of dispersal effectiveness, ultimately affecting plant population dynamics and community structure. Such a strong context‐dependence in the microsites of seed arrival is likely to confer resilience against unpredictable environmental conditions, like those typical of Mediterranean ecosystems.     

Positive relationship between fruit removal by animals and seedling recruitment in a tropical forest

Fleshy-fruited plants rely on animal frugivores to disperse their seeds, and seed removal by frugivores may leave an imprint on seedling recruitment. However, to what extent plant–frugivore interactions are related to seedling recruitment has rarely been quantified at the community level, especially in species-rich tropical forests. In this study, we tested the effect of different plant traits on fruit removal by frugivores and tested the relative importance of fruit removal, plant traits and abiotic factors for seedling recruitment. We quantified plant–frugivore interactions of 22 fleshy-fruited plant species consumed by 56 diurnal frugivore species, and counted the number of seedlings that emerged along an elevational gradient in the Colombian Andes. We measured a set of plant traits (i.e., crop size; fruit size; seed load and mass; fruit nutritional contents), estimated the density of adult plants and recorded relevant abiotic factors (light, temperature and humidity). We found that fruit removal by frugivores was positively associated with crop size, but negatively associated with fruit length and unrelated to seed load and fruit nutritional content. Seedling densities were positively related to the density of adult plants, seed mass and fruit removal by animals. We found no relationship between abiotic factors and seedling recruitment. Our results indicate that fruit abundance and morphology are important determinants of fruit removal and that fruit removal is positively associated with seedling recruitment accounting for effects of species abundance and plant traits. We conclude that plant traits shape fruit removal and seedling recruitment at the community level, while these two crucial processes of forest regeneration are directly linked by seed dispersal of animals.     

Bird Assemblage and Visitation Pattern at Fruiting Elmerrillia tsiampaca (Magnoliaceae) Trees in Papua New Guinea

Most tropical trees produce fleshy fruits that attract frugivores that disperse their seeds. Early demography and distribution for these tree species depend on the effects of frugivores and their behavior. Anthropogenic changes that affect frugivore communities could ultimately result in changes in tree distribution and population demography. We studied the frugivore assemblage at 38 fruiting Elmerrillia tsiampaca, a rain forest canopy tree species in Papua New Guinea. Elmerrillia tsiampaca is an important resource for frugivorous birds at our study site because it produces abundant lipid-rich fruits at a time of low fruit availability. We classified avian frugivores into functional disperser groups and quantified visitation rates and behavior at trees during 56 canopy and 35 ground observation periods. We tested predictions derived from other studies of plant–frugivore interactions with this little-studied frugivore assemblage in an undisturbed rain forest. Elmerrillia tsiampaca fruits were consumed by 26 bird species, but most seeds were removed by eight species. The most important visitors (Columbidae, Paradisaeidae and Rhyticeros plicatus) were of a larger size than predicted based on diaspore size. Columbidae efficiently exploited the structurally protected fruit, which was inconsistent with other studies in New Guinea where structurally protected fruits were predominantly consumed by Paradisaeidae. Birds vulnerable to predation foraged for short time periods, consistent with the hypothesis that predator avoidance enhances seed dispersal. We identified seven functional disperser groups, indicating there is little redundancy in disperser groups among the regular and frequent visitors to this tropical rain forest tree species.     

Duality of interaction outcomes in a plant–frugivore multilayer network

In plant–animal interactions, species are commonly labeled as either mutualists or antagonists, based on the most common, most studied, or most easily observed outcome. Nevertheless, evidence from simple systems comprising 2–4 species suggests that those labels are an oversimplification: individual species often function in both roles, either simultaneously or at different places or times. We include both mutualistic and antagonistic interactions between mammals and seeds in a multilayer network, to explore for the first time the community‐level consequences of the dual roles played by some species. We tested whether negative and positive interactions within a plant–frugivore network are separated into different modules, or whether they overlap due to the presence of frugivores that both kill and disperse seeds. The frugivorous diets of nonvolant small mammals were studied at one dry tropical forest site in southeastern Brazil by analyzing fecal samples from individuals captured in live traps. Seed viability was assessed with a tetrazolium test to determine the outcome of those interactions, as estimated by whether or not seeds survived gut passage. Interactions were analyzed as a weighted multilayer network, subdivided into one potentially mutualistic (live seeds deposited) and one antagonistic (dead seeds deposited) layer. The two layers had similar structure with high overlap between them. Some mammal species exhibited highly central, dual roles, acting both as antagonists and mutualists, in many cases of the same plant species. Dispersal service by most of these small mammals is accompanied by seed destruction, suggesting that the selective pressures exerted by those animals on the plants is much more complex than often assumed. Our results demonstrate that the complexity of plant–frugivore networks can not be fully understood without proper incorporating measures of seed fate following gut passage.     

Exploring the interaction of avian frugivory and plant spatial heterogeneity and its effect on seed dispersal kernels using a simulation model

Seed dispersal by avian frugivores is one of the key processes influencing plant spatial patterns, but may fail if there is disruption of plant–frugivore mutualisms, such as decline in abundance of dispersers, fragmentation of habitat, or isolation of individual trees. We used simulation model experiments to examine the interaction between frugivore density and behaviour and the spatial arrangement of fruiting plants and its effect on seed dispersal kernels. We focussed on two New Zealand canopy tree species that produce large fruits and are dispersed predominantly by one avian frugivore (Hemiphaga novaeseelandiae). Although the mean seed dispersal distance decreased when trees became more aggregated, there were more frugivore flights between tree clusters, consequently stretching the tails of the dispersal kernels. Conversely, when trees were less aggregated in the landscape, mean dispersal distances increased because seeds were deposited over larger areas, but the kernels had shorter tails. While there were no statistically meaningful changes in kernel parameters when frugivore density changed, decreases in density did cause a proportional reduction in the total number of dispersed seeds. However, birds were forced to move further when fruit availability and fruit ripening were low. Sensitivity analysis showed that dispersal kernels were primarily influenced by the model parameters relating to disperser behaviour, especially those determining attractiveness based on distance to candidate fruiting trees. Our results suggest that the spatial arrangement of plants plays an important role in seed dispersal processes – although tree aggregation curbed the mean seed dispersal distance, it was accompanied by occasional long distance events, and tree dispersion caused an increase in mean dispersal distance, both potentially increasing the probability of seeds finding suitable habitats for germination and growth. Even though low frugivore densities did not cause dispersal failure, there were negative effects on the quantity of seed dispersal because fewer seeds were dispersed.     

A simple null model predicts fruit-frugivore interactions in a temperate rainforest

Studies of seed dispersal mutualisms typically test for adaptive relationships between fruits and frugivores. Here, I take the opposite approach, and ask what relationships would be expected based on chance encounters between mutualists. I derived a simple null model to predict pair-wise relationships between fruit and frugivore species. I assumed that all frugivores had identical fruit preferences, but allowed for interspecific variation in plant abundances, frugivore abundances and fruit phenologies. Under these conditions, the number of visits each frugivore species makes to each plant species results from the product of plant abundances and frugivore abundances when each plant species produces fruit. I then tested null model predictions with observations in a temperate rainforest in British Columbia, Canada. I measured the abundance and phenology of seven bird-dispersed plant species, seasonal changes in the abundances of six avian frugivore species and 212 interactions between them. Empirical results were generally consistent with predictions, suggesting that relationships between birds and fruits are structured randomly. However, some variation in relationships between observations and predictions was observed, suggesting deterministic processes may also be important. Overall results illustrate that predictable relationships between fruit and frugivore species can result from random encounters between mutualists.