Large-bodied Frugivores Research Articles

Significance of seed dispersal by the largest frugivore for large-diaspore trees

How do large-bodied frugivores contribute to seed dispersal of large-diaspore plants? This study examined seed dispersal effectiveness for two large-diaspore tree species, Astrotrichilia asterotricha (AA) and Abrahamia deflexa (AD), in a Madagascan forest. I evaluated fruit removal rates through focal tree observations and factors affecting seedling recruitment up to the 2-year-old seedling stage. I confirmed brown lemur (Eulemur fulvus) as the sole disperser, removing 58.8% and 26.0% of fruits produced by AA and AD. Brown lemurs frequently visited large-crowned AA trees with high density of fallen fruits and more adjacent fruiting trees during seasons with low fruit diversity. Most AA seedlings were removed by predators, although canopy openness slightly improved seedling establishment. Although AD seeds were severely attacked by predators under mother trees, the seedlings survived under dispersal conditions distant from the mother trees, and with low density of diaspores. AD had a higher cumulative probability from fruit removal to seedling recruitment (6.5%) than AA (1.5%) in the first rainy season. This study clarifies the significance of seed dispersal to tree recruitment strategies, which vary among different combinations of tree species and large frugivores, i.e. quantitative dispersal to reach suitable microhabitats, and qualitative dispersal to escape from dangerous zones near mother trees.

Plant-frugivore network simplification under habitat fragmentation leaves a small core of interacting generalists

Habitat fragmentation impacts seed dispersal processes that are important in maintaining biodiversity and ecosystem functioning. However, it is still unclear how habitat fragmentation affects frugivorous interactions due to the lack of high-quality data on plant-frugivore networks. Here we recorded 10,117 plant-frugivore interactions from 22 reservoir islands and six nearby mainland sites using the technology of arboreal camera trapping to assess the effects of island area and isolation on the diversity, structure, and stability of plant-frugivore networks. We found that network simplification under habitat fragmentation reduces the number of interactions involving specialized species and large-bodied frugivores. Small islands had more connected, less modular, and more nested networks that consisted mainly of small-bodied birds and abundant plants, as well as showed evidence of interaction release (i.e., dietary expansion of frugivores). Our results reveal the importance of preserving large forest remnants to support plant-frugivore interaction diversity and forest functionality.

Response of avian and mammal seed dispersal networks to human-induced forest edges in a sub-humid tropical forest

AbstractSpecies-rich ecosystems as tropical forests are extremely vulnerable to anthropogenic destruction. Most tropical plant species rely on animals to disperse their seeds. However, patterns of mutualistic interactions have rarely been explored, and seed dispersal networks are still poorly studied in Africa. Here, we examine how forest edges’ (FE) seed dispersal networks differ from the mature forest (MF) at a West African sub-humid tropical forest within the National Park of Cantanhez (Guinea-Bissau). Additionally, we explore species’ roles within the network. MF had higher fruit availability, more frugivore visitors, and plant–frugivore interactions. Network structure was quite similar between habitats, showing signs of redundancy, and some robustness to species’ extinction. FE was more nested, modular, and specialized, whereas MF had higher connectance, interaction evenness, and robustness to extinction. Most species were generalists, but large-bodied frugivores prevailed at MF. FE showed a higher vulnerability, mostly to the loss of trees. Trees are key, keeping the structure of both networks. Large-bodied frugivores and fruiting-tree species that work as network connectors should thus be the focus of active conservation management in these forests. Only viable populations of these species will ensure a good performance of the seed dispersal network, promoting the natural regeneration of the ecosystem.

Simplified Communities of Seed-Dispersers Limit the Composition and Flow of Seeds in Edge Habitats

Edge effects, driven by human modification of landscapes, can have critical impacts on ecological processes such as species interactions, with cascading impacts on biodiversity as a whole. Characterizing how edges affect vital biotic interactions such as seed dispersal by frugivores is important for better understanding potential mechanisms that drive species coexistence and diversity within a plant community. Here, we investigated how differences between frugivore communities at the forest edge and interior habitats of a diverse tropical rainforest relate to patterns of animal-mediated seed dispersal and early seedling recruitment. We found that the lemur communities across the forest edge-interior gradient in this system showed the highest species richness and variability in body sizes at intermediate distances; the community of birds showed the opposite pattern for species richness. Three large-bodied frugivores, known to be effective dispersers of large seeds, tended to avoid the forest edge. As result, the forest edges received a lower rate of animal-mediated seed dispersal compared to the interior habitats. In addition, we also found that the seeds that were actively dispersed by animals in forest edge habitats were smaller in size than seeds dispersed in the forest interior. This pattern was found despite a similarity in seed size of seasonally fruiting adult trees and shrubs between the two habitats. Despite these differences in dispersal patterns, we did not observe any differences in the rates of seedling recruitment or seed-size distribution of successful recruit species. Our results suggest that a small number of frugivores may act as a potential biotic filter, acting on seed size, for the arrival of certain plant species to edge habitats, but other factors may be more important for driving recruitment patterns, at least in the short term. Further research is needed to better understand the potential long-term impacts of altered dispersal regimes relative to other environmental factors on the successional dynamics of edge communities. Our findings are important for understanding potential ecological drivers of tree community changes in forest edges and have implications for conservation management and restoration of large-seeded tree species in disturbed habitats.

Sowing forests: a synthesis of seed dispersal and predation by agoutis and their influence on plant communities.

Granivorous rodents have been traditionally regarded as antagonistic seed predators. Agoutis (Dasyprocta spp.), however, have also been recognized as mutualistic dispersers of plants because of their role as scatter-hoarders of seeds, especially for large-seeded species. A closer look shows that such definitions are too simplistic for these Neotropical animals because agoutis can influence plant communities not only through seed dispersal of large seeds but also through predation of small seeds and seedlings, evidencing their dual role. Herein, we summarize the literature on plant-agouti interactions, decompose agouti seed dispersal into its quantitative and qualitative components, and discuss how environmental factors and plant traits determine whether these interactions result in mutualisms or antagonisms. We also look at the role of agoutis in a community context, assessing their effectiveness as substitutes for extinct megafaunal frugivores and comparing their ecological functions to those of other extant dispersers of large seeds. We also discuss how our conclusions can be extended to the single other genus in the Dasyproctidae family (Myoprocta). Finally, we examine agoutis' contribution to carbon stocks and summarize current conservation threats and efforts. We recorded 164 interactions between agoutis and plants, which were widespread across the plant phylogeny, confirming that agoutis are generalist frugivores. Seed mass was a main factor determining seed hoarding probability of plant species and agoutis were found to disperse larger seeds than other large-bodied frugivores. Agoutis positively contributed to carbon storage by preying upon seeds of plants with lower carbon biomass and by dispersing species with higher biomass. This synthesis of plant-agouti interactions shows that ecological services provided by agoutis to plant populations and communities go beyond seed dispersal and predation, and we identify still unanswered questions. We hope to emphasise the importance of agoutis in Neotropical forests.

Fruit and seed traits of native and invasive plant species in Hawai‘i: implications for seed dispersal by non-native birds

For alien invasive plant species dependent on frugivores for seed dispersal, traits that influence consumption can be important determinants of invasion and spread. However, trait comparisons between native and invasive species have documented mixed results. In Hawai‘i, one of the most invaded systems in the world, nearly all frugivory, and thus seed dispersal, is dependent on non-native birds. Moreover, the majority of dispersal events also involve invasive plants, suggesting the potential for an “invasional meltdown”. Here we compare fruit and seed traits between native and invasive plants and evaluate how those traits influence consumption by non-native avian frugivores. Although we found that most traits examined were similar between native and invasive fruiting species, invasive species tended to have higher fruit protein content, longer fruiting duration, were less likely to have orange fruits, and have less variable seed length. Longer fruiting duration and smaller seed size were important predictors for avian frugivore consumption. In combination, these results suggest that traits that increase probability of encounter (fruiting duration) and ability to be consumed (seed size) are more important for dispersal by frugivores than traits associated with fruit preferences and, thus, are driving the spread of invasive species and limiting dispersal of some native species. Further, we document an apparent seed size threshold for avian consumption (~ 7.0 mm), supporting previous work suggesting that large seeded species, particularly native plant species adapted for extinct large-bodied frugivores, are likely dispersal limited based on gape size limitation of the current non-native frugivore community.

Changes in tree community structure in defaunated forests are not driven only by dispersal limitation.

Bushmeat hunting has reduced population sizes of large frugivorous vertebrates throughout the tropics, thereby reducing the dispersal of seeds. This is believed to affect tree population dynamics, and therefore community composition, because the seed dispersal of large‐seeded trees depends upon large‐bodied vertebrates.We report on a long‐running study of the effect of defaunation on a tropical tree community. In three censuses over 11 years, we compared sapling recruitment between a hunted and a nonhunted site, which are nearby and comparable to one another, to determine the extent to which species composition has changed through time following defaunation. We expected to find a reduced abundance of tree species that rely on large frugivores for dispersal at the hunted site and altered community structure as a consequence.Although community composition at the hunted site diverged from that at the nonhunted site, the changes were independent of dispersal syndrome, with no trend toward a decline in species that are dispersed by large, hunted vertebrates. Moreover, the loss of large‐bodied dispersers did not generate the changes in tree community composition that we hypothesized. Some species presumed to rely on large‐bodied frugivores for dispersal are effectively recruiting despite the absence of their dispersers.Synthesis: The presumption that forests depleted of large‐bodied dispersers will experience rapid, directional compositional change is not fully supported by our results. Altered species composition in the sapling layer at the hunted site, however, indicates that defaunation may be connected with changes to the tree community, but that the nature of these changes is not unidirectional as previously assumed. It remains difficult to predict how defaunation will affect tree community composition without a deeper understanding of the driving mechanisms at play.

Defaunation of large-bodied frugivores reduces carbon storage in a tropical forest of Southeast Asia

Recent studies have suggested that defaunation of large-bodied frugivores reduces above-ground carbon storage in tropical forests of South America and Africa, but not, or less so, in Southeast Asian tropical forests. Here we analyze the issue using the seed dispersal network (data of interaction between trees and animal seed dispersers) and forest composition of a 30-ha forest dynamics plot in central Thailand, where an intact fauna of primates, ungulates, bears and birds of all sizes still exists. We simulate the effect of two defaunation scenarios on forest biomass: 1) only primates extirpated (a realistic possibility in near future), and 2) extirpation of all large-bodied frugivores (LBF) including gibbons, macaques, hornbills and terrestrial mammals, the main targets of poachers in this region. For each scenario, we varied the population size reduction of the LBF dispersed tree species from 20% to 100%. We find that tree species dependent on seed dispersal by large-bodied frugivores (LBF) account for nearly one-third of the total carbon biomass on the plot, and that the community turnover following a complete defaunation would result in a carbon reduction of 2.4% to 3.0%, depending on the defaunation scenario and the model assumptions. The reduction was always greater than 1% when the defaunation intensity was at least 40%. These effect sizes are comparable to values reported for Neotropical forests, suggesting that the impact of defaunation on carbon deficit is not necessarily lower in Southeast Asian forests. The problem of defaunation in Asia, and the mutual benefits between biodiversity conservation and climate change mitigation, should therefore not be neglected by global policies to reduce carbon emissions.

How complementary are large frugivores for tree seedling recruitment? A case study in the Congo Basin

AbstractLarge frugivores provide critical seed dispersal services for many plant species and their extirpation from forested ecosystems can cause compositional shifts in regenerating plant cohorts. Yet, we still poorly understand whether large seed-dispersers have complementary or redundant roles for forest regeneration. Here, to assess the functional complementarity of large-bodied frugivores in forest regeneration, we quantified the effects of varying abundance of hornbills, primates and the forest elephant on the density, species richness and the mean weighted seed length of animal-dispersed tree species among seedlings in five sites in a forest–savanna mosaic in D. R. Congo, while accounting for percentage forest cover and the local presence of fruiting trees. We found that the abundance of primates was positively associated with species richness of seedlings, while percentage forest cover was negatively associated (R2 = 0.19). The abundance of hornbills, the presence of elephants and percentage forest cover were positively associated with mean seed length of the regenerating cohort (R2 = 0.13). Spatially explicit analysis indicated that some additional processes have an important influence on these response indices. Primates would seem to have a preponderant role for maintaining relatively high species richness, while hornbills and elephant would seem to be predominantly responsible for the recruitment of large-seeded trees. Our results could indicate that these taxa of frugivores play complementary functional roles for forest regeneration. This suggests that the extirpation of one or more of these dispersers would likely not be functionally compensated for by the remaining taxa, hence possibly cascading into compositional shifts.

Large frugivores matter: Insights from network and seed dispersal effectiveness approaches.

While large avian frugivores are known to be key dispersers for large-seeded tree species, their role in community-wide plant-disperser networks is still poorly known. Large avian frugivores are also among the most threatened due to anthropogenic impacts. We evaluated the role of large avian frugivores in a plant-disperser community by (a) determining whether the plant-disperser community was modular, with a distinct community of large frugivores (thereby highlighting their importance), (b) determining relative qualitative and quantitative roles played by large-bodied frugivores vis-à-vis other frugivores and (c) determining impacts of large-bodied frugivore loss on the plant-disperser community. The study was carried out at a tropical forest site in north-east India, which is part of the Eastern Himalaya Biodiversity Hotspot. We collected tree watch data (20:55hr) from 46 tree species, which represented 85% of tree species that are predominantly bird-dispersed in the area. We found that the plant-disperser community was modular, with a distinct module of large-seeded tree species and large frugivores. Intermediate-sized frugivores such as barbets and bulbuls were the most connected, while large-sized frugivores, such as hornbills and imperial pigeons, were moderately well connected. Qualitative and quantitative roles played by different dispersers varied across the gradient of frugivore body size. Hornbills, the largest avian frugivores, consumed a significantly greater number of fruits and swallowed larger proportions of fruits compared with other avian groups. In comparison with similar-sized frugivores, imperial pigeons fed on larger-sized fruits, highlighting their importance for dispersal of large-seeded plants. Under simulated extinction scenarios, larger extinction cascades were not necessarily caused by larger frugivores; however, extinctions of certain large-bodied frugivores (hornbills, imperial pigeons) caused extinction cascades. Integrating information from networks and seed dispersal effectiveness approaches enabled a better understanding of large frugivore role in a plant-disperser community. While large-bodied frugivores may not be playing a central role in plant-disperser communities, they are crucial as seed dispersal service providers for large-seeded plants. In conjunction with the reported local extinctions of large frugivores like hornbills from the south Asian region, this study's findings highlight the irreplaceable quantitative and qualitative impacts that tropical plant communities are likely to experience in the future.

High microhabitat heterogeneity drives high functional traits in forest birds in five protected forest areas in the urban mosaic of Durban, South Africa

Anthropogenic forest disturbance poses a significant threat to the persistence of wildlife. Generally, disturbance of forest environments alters vegetation structure, affecting specialised niche-dependent avian species. We investigated the influence of a comprehensive suite of vegetation structures on the taxonomic and functional diversity of avian forest species in five protected forest areas in the urban mosaic of eThekwini Municipality, Durban, South Africa during the austral breeding season of 2016. We conducted 135 fixed-radius point-count surveys between the vegetation classes of Indigenous Forest (IF) and Coastal Thicket/Dense Bush (TDB; a secondary wooded-habitat that represents regenerating Indigenous Forest), and recorded microhabitat structure covariates at each survey site. We conducted RLQ analyses to examine the association between avian functional traits and microhabitat structures present at each survey site. There was no significant difference in vegetation structure nor species richness between IF and TDB. Species with specialised ecological niches (e.g. large-bodied frugivores; small-bodied insectivores, cavity-nesters) were present in both IF and TDB, indicating that TDB in Durban represents an advanced stage of forest regeneration. We highlight the importance of both IF and TDB for providing critical habitat for both avian generalised and specialised functional traits in the forest patches in the urban mosaic. Crucially, we show that forested areas under conservation management in urbanised areas successfully provide species with a wide variety of functional traits critical to ecosystem functioning and human health.

Intra-specific downsizing of frugivores affects seed germination of fleshy-fruited plant species

The loss of largest-bodied individuals within species of frugivorous animals is one of the major consequences of defaunation. The gradual disappearance of large-bodied frugivores is expected to entail a parallel deterioration in seed dispersal functionality if the remaining smaller-sized individuals are not so effective as seed dispersers. While the multiple impacts of the extinction of large bodied species have been relatively well studied, the impact of intraspecific downsizing (i.e. the extinction of large individuals within species) on seed dispersal has rarely been evaluated. Here we experimentally assessed the impact of body-size reduction in the frugivorous lizard Gallotia galloti (Lacertidae), an endemic species of the Canary Islands, on the seed germination patterns of two fleshy-fruited plant species (Rubia fruticosa and Withania aristata). Seed germination curves and the proportions of germinated seeds were compared for both plant species after being defecated by large-sized individuals and small-sized individuals. The data show that seeds of W. aristata defecated by larger-sized lizards germinated faster and in a higher percentage than those defecated by small-sized lizards, while no differences were found for R. fruticosa seeds. Our results suggest that disappearance of the largest individuals of frugivorous species may impair recruitment of some plant species by worsening seed germination. They also warn us of a potential cryptic loss of seed dispersal functionality on defaunated ecosystems, even when frugivorous species remain abundant.

Persisting in defaunated landscapes: Reduced plant population connectivity after seed dispersal collapse

Abstract Defaunation of large‐bodied frugivores could be causing severe losses of crucial ecosystem functions such as seed dispersal. The immediate ecological consequences may include alteration or even collapse of seed‐mediated gene flow affecting plant population connectivity, with impacts on the regional scale distribution of genetic variation. Yet, these far‐reaching consequences of defaunation remain understudied. Here, we tested whether human‐induced defaunation of the Canarian frugivorous lizards (Gallotia, Lacertidae) altered within‐island population connectivity and the amount and large‐scale distribution of genetic variation of Neochamaelea pulverulenta (Rutaceae), which relies exclusively on these lizards for seed dispersal. Our study system defines a lizard downsizing gradient with three contrasted ecological scenarios (islands) with relatively optimal (Gran Canaria; large‐sized lizards), suboptimal (Tenerife; medium) and collapsed seed dispersal processes (La Gomera; small). We extensively sampled individual plant genotypes from 80 populations spanning the full geographical range of the plant to examine their genetic diversity, population‐genetic network topologies, and the patterns of isolation both by distance (IBD) and resistance (IBR) across these three ecological scenarios. Plant genetic diversity appeared unaffected by defaunation‐mediated downsizing of frugivorous lizards. However, we found a reduced overall plant population connectivity together with an increased isolation by distance within the most defaunated islands (La Gomera and, to a lesser extent, Tenerife) when compared with the scenario preserving the functionality of lizard‐mediated seed dispersal (Gran Canaria). The results, with a significant effect of lizard downsizing, were robust when controlling for biotic/abiotic differences among the three islands by means of isolation by resistance models (IBR). Synthesis. Our results provide valuable insights into the far‐reaching consequences of the deterioration of mutualisms on plant population dynamics over very large spatial scales. Conservation of large‐bodied frugivores is, thus, essential because their irreplaceable mutualistic dispersal services maintain an extensive movement of seeds across the landscape, crucial for maintaining the genetic cohesiveness of metapopulations and the adaptive potential of plant species across their entire geographical range.

Water availability not fruitfall modulates the dry season distribution of frugivorous terrestrial vertebrates in a lowland Amazon forest.

Terrestrial vertebrate frugivores constitute one of the major guilds in tropical forests. Previous studies show that the meso-scale distribution of this group is only weakly explained by variables such as altitude and tree basal area in lowland Amazon forests. For the first time we test whether seasonally limiting resources (water and fallen fruit) affect the dry season distribution in 25 species of terrestrial vertebrates. To examine the effects of the spatial availability of fruit and water on terrestrial vertebrates we used a standardized, regularly spaced arrangement of camera-traps within 25km2 of lowland Amazon forest. Generalized linear models (GLMs) were then used to examine the influence of four variables (altitude, distance to large rivers, distance to nearest water, and presence vs absence of fruits) on the number of photos on five functional groups (all frugivores, small, medium, large and very large frugivores) and on seven of the most abundant frugivore species (Cuniculus paca, Dasyprocta leporina, Mazama americana, Mazama nemorivaga, Myoprocta acouchy, Pecari tajacu and Psophia crepitans). A total of 279 independent photos of 25 species were obtained from 900 camera-trap days. For most species and three functional groups, the variation in the number of photos per camera was significantly but weakly explained by the GLMs (deviance explained ranging from 6.2 to 48.8%). Generally, we found that the presence of water availability was more important than the presence of fallen fruit for the groups and species studied. Medium frugivores, large-bodied frugivores, and two of the more abundant species (C. paca and P. crepitans) were recorded more frequently closer to water bodies; while none of the functional groups nor the most abundant species showed any significant relationship with the presence of fallen fruit. Two functional groups and two of the seven most common frugivore species assessed in the GLMs showed significant results with species-specific responses to altitude. Our findings provide a more detailed understanding of how frugivorous vertebrates cope with periods of water and fruit scarcity in lowland Amazon forests.

Defaunation leads to microevolutionary changes in a tropical palm.

Many large species have declined worldwide due to habitat fragmentation and poaching. The defaunation of large frugivores and the consequent reductions of seed dispersal services may have immediate effects on plant demography. Yet, the lasting effects of frugivore defaunation on microevolutionary processes of the plants they disperse remain understudied. We tested if the loss of large seed dispersers can lead to microevolutionary changes of a tropical palm. We show that frugivore defaunation is the main driver of changes in allelic frequency among populations. Turnover of alleles accounted for 100% of dissimilarity in allelic frequencies of individuals between defaunated and non-defaunated forests; and individuals from defaunated sites are 1.5 times more similar genetically than those found in pristine sites. Given that sizeable fractions of the palm fruit crops remain undispersed in defaunated sites due to lack of large-bodied frugivores, this distinct pattern of gene pool composition of early recruits may reveal strong dispersal limitation for specific genotypes, or collapses of gene flow between fragmented areas, or both. Because most of tropical tree species rely on seed dispersal by vertebrates, our results show that defaunation has a lasting effect on microevolutionary processes, with potential consequences for persistence under scenarios of environmental change.

Isolation and characterization of microsatellite loci for the large-seeded tree Protorhus deflexa (Anacardiaceae).

• Premise of the study: Protorhus deflexa is an endemic large-seeded tree in Madagascar that depends heavily on insects for cross-pollination and on large-bodied frugivores for seed dispersal. Because such mutualistic relationships are vulnerable to human disturbance, the development of microsatellite markers will enhance analyses of gene flow in this tree species in degraded forests.• Methods and Results: Nineteen microsatellite markers were developed for P. deflexa using 454 pyrosequencing. The number of alleles ranged from two to nine, and the ranges of observed and expected heterozygosities were 0.200–0.800 and 0.303–0.821, respectively. The parentage exclusion probability by the 19 loci reached 0.98583 for the first parent and 0.99971 for the second parent.• Conclusions: These markers will be useful for studying gene flow via pollination and seed dispersal by animals and the genetic structure of P. deflexa in protected and degraded forests in Madagascar.

The Role of Frugivores in Determining Seed Removal and Dispersal in the Neotropical Nutmeg

At the Nouragues field station (French Guiana), we studied the seed dispersal system of two sympatric tropical tree species that differ in seed size, Virola kwatae and V. michelii (Myristicaceae), to evaluate the degree of interaction between Virola species and their dispersers, and consistency in the fruit traits affecting seed removal rate. Only the spider monkey ( Ateles paniscus) and three species of ramphastid toucan dispersed the large (4.8g) V. kwatae seeds. These four animal species, as well as three smaller-bodied bird species, also dispersed the small V. michelii seeds (2.1g). Annual fecundity of both Virola species did not affect seed removal rate. However, variation in V. kwatae seed size within tree populations, and increased seed removal rate due to fruit selection on seed size, suggest a potential for an evolutionary response of seed size to selection by large-bodied frugivores in this species. In contrast, seed size did not affect V. michelii seed removal rate, and the interactions between V. michelii and its dispersers are interpreted to be too diffuse to result in strong selection on plant traits affecting seed removal rate. Because hunting pressure is greater on larger than on smaller frugivores, extinction of A. paniscus (the main large-bodied seed disperser of the study Virola) is likely to affect the long tail of dispersal kernel, thus decreasing recruitment away from fruiting adult trees.

Large vertebrates as the missing components of seed-dispersal networks

Large-bodied frugivores may play a key role in the networks of plants and their seed dispersers. These species, however, are often threatened by human impacts that lead to defaunation. In this paper, we discuss the potential implications of the loss of large frugivores for seed-dispersal networks. First, we review the role of large vertebrates as seed dispersers in different tropical ecosystems to show that these species are likely to be important components of seed-dispersal networks. Second, we showed that, despite their importance, large vertebrates are absent from most of the seed-dispersal networks described in the available literature. We identified three main reasons for this absence: (1) large vertebrates have already died out in the studied areas; (2) studies focus on particular taxonomic groups that consist mostly of small birds; and (3) it is inherently difficult to describe the interactions of naturally rare and secretive species such as large vertebrates. We argue that a proper evaluation of the importance of large frugivores within seed-dispersal networks would benefit from considering aspects other than the frequency of interactions. We suggest weighting pairwise interactions by their ecological consequences to quantify the contribution of large frugivores to outcomes of seed dispersal, such as landscape connectivity.

Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree

Unregulated hunting of large-bodied frugivores is ubiquitous in tropical forests. Due to their low fecundity and complex social organization, large primates are often the first tropical forest vertebrates to be extirpated by hunting. Large primates are important seed dispersers and the only dispersal vectors of many large-seeded plants, leading to concerns that primate-dispersed trees will succumb to large-scale recruitment failure wherever they co-occur with overhunting. We used a field experiment in a remote, nonhunted region of the western Brazilian Amazon to test how the seedling recruitment success of a primate-dispersed Sapotaceae tree (Manilkara bidentata) is affected by distance from parent trees, protection from vertebrate seed predators, and gastro-intestinal seed cleaning associated with passage through frugivorous vertebrates. Only seed cleaning significantly increased the rate of seedling recruitment. Janzen–Connell effects have been widely purported as the central mechanism for recruitment failure, but our results suggest that for many tropical forest plant species Janzen–Connell effects are a second-order effect that acts once seeds have been successfully cleaned of fruit pulp by gut treatment. As an illustration of the relative importance of the sheer quantity of seeds ingested by woolly monkeys (Lagothrix cana), we further estimate the density and dispersal services provided by a complete primate assemblage to show that L. cana cleans and disperses nearly one million seeds per km2 per 24-day Manilkara fruiting season, amounting to over 71% of the seed dispersal services provided by the entire primate assemblage. The disperser vacuum in the absence of L. cana greatly reduces the quantity of cleaned seeds deposited on the forest floor. For similar fleshy-fruited species where gut passage greatly increases survival, a simple lack of redundancy in seed consumption may be the primary driver of recruitment failure resulting from large-primate extirpation due to overhunting, with Janzen–Connell effects secondarily influencing recruitment success as a function of either dispersal distance or seed density.

Shifts in community structure of tropical trees and avian frugivores in forests recovering from past logging

Logging is one of the most pervasive threats to biodiversity in tropical forests. In this study, we concurrently examined the responses of the avian frugivore community and the community of fruiting trees to past logging in a tropical forest in northeastern India. We predicted that the abundance of, and visitation by large-bodied frugivores would be lower in logged forests, resulting in reduced seed dispersal and recruitment of biotically dispersed species (especially large-seeded species). Data were collected from two logged and unlogged sites using (a) belt transects for estimating avian frugivore abundance (b) fruiting tree watches to quantify frugivore visitation and (c) vegetation plots to characterize recruitment. Our results show that differences in the abundance of bird species between logged and unlogged sites was correlated with body mass, with larger species being scarcer and smaller species more abundant in logged areas. Correspondingly, visitation rates by large avian frugivores was lower in logged compared with unlogged sites. Finally, biotically dispersed tree species, especially large-seeded species, had lower recruitment in logged forests, potentially due to lowered visitation rates and decreased fruit removal by large bodied avian frugivores. In the long term, these differences in recruitment may result in a tree community shift towards small-seeded biotically dispersed species and abiotically dispersed species in logged areas.