Lowland tapirs facilitate seed dispersal in degraded Amazonian forests

The forests of southeastern Amazonia are highly threatened by disturbances such as fragmentation, understory fires, and extreme climatic events. Large‐bodied frugivores such as the lowland tapir (Tapirus terrestris) have the potential to offset this process, supporting natural forest regeneration by dispersing a variety of seeds over long distances to disturbed forests. However, we know little about their effectiveness as seed dispersers in degraded forest landscapes. Here, we investigate the seed dispersal function of lowland tapirs in Amazonian forests subject to a range of human (fire and fragmentation) and natural (extreme droughts and windstorms) disturbances, using a combination of field observations, camera traps, and light detection and ranging (LiDAR) data. Tapirs travel and defecate more often in degraded forests, dispersing much more seeds in these areas [9,822 seeds per ha/year (CI_95% = 9,106; 11,838)] than in undisturbed forests [2,950 seeds per ha/year (CI_95% = 2,961; 3,771)]. By effectively dispersing seeds across disturbed forests, tapirs may contribute to natural forest regeneration—the cheapest and usually the most feasible way to achieve large‐scale restoration of tropical forests. Through the dispersal of large‐seeded species that eventually become large trees, such frugivores also contribute indirectly to maintaining forest carbon stocks. These functions may be critical in helping tropical countries to achieve their goals to maintain and restore biodiversity and its ecosystem services. Ultimately, preserving these animals along with their habitats may help in the process of natural recovery of degraded forests throughout the tropics. Abstract in Portuguese is available with online material.     

Can remnant frugivore species effectively disperse tree seeds in secondary tropical rain forests?

Seed dispersal by frugivores in tropical rain forests is important for maintaining viable tree populations. Over the years, vertebrate assemblages in tropical forests have been altered by anthropogenic disturbances, leading to concerns about the ability of remnant vertebrates to substitute for the lost or declining vertebrate populations. We compared vertebrate composition and frugivore visitation rates as an indirect measure of rate of seed dispersal in three tropical rain forests in Uganda, namely Mabira, Budongo and Kibale Forests. Mabira is highly disturbed, Kibale is little and Budongo is intermediate. The aim was to determine whether vertebrate assemblages in differentially disturbed forests had comparable abilities to disperse seeds and whether tree species were equally vulnerable to loss of seed dispersers. Assemblages of forest generalist species were similar in all forests, but specialists were less abundant in the heavily disturbed forest. Remnant frugivores in the heavily disturbed forest were mainly small-bodied species that spat seeds beneath fruiting trees compared to large-bodied species observed in the less disturbed forests that ingested and carried away the seeds. We postulate that the quantity of seeds dispersed in heavily disturbed forests is much reduced due to low visitation rates of frugivores and the absence of large frugivores that consume large quantities of fruit. The quality of seed dispersal is affected as well by the distance over which seeds are moved. Assessment of vulnerability of trees shows no evidence for disperser substitution for trees producing large fruits. Fruit trees with low nutritional contents and digestibility were least visited in frugivore-impoverished forests. The loss of large specialist frugivores is likely to affect recruitment of many trees, especially of species that cannot establish beneath adult conspecifics.     

Survival and Scatterhoarding of Frugivores-Dispersed Seeds as a Function of Forest Disturbance

The effect of forest disturbance on survival and secondary dispersal of an artificial seed shadow (N= 800) was studied at Brownsberg Natural Park, Suriname, South America. We scattered single seeds of the frugivore‐dispersed tree Virola kwatae (Myristicaceae), simulating loose dispersal by frugivores, in undisturbed and disturbed secondary forest habitats. Seed survival rate aboveground was high (69%) within 2 wk and was negatively correlated with scatterhoarding rate by rodents, the latter being significantly lower in the undisturbed forest (9%) than in the disturbed forest (20%). Postdispersal seed predation by vertebrates was low (3%) and infestation of seeds by invertebrates was almost zero in all instances. Therefore, secondary seed dispersal by rodents in forest is not as critical for recruitment as observed among other bruchid‐infested large‐seeded species. Secondary seed dispersal by rodents may, however, facilitate seedling recruitment whether cached seeds experience greater survival than seeds remaining above ground surface.     

The Interplay of Habitat and Seed Type on Scatterhoarding Behavior in a Fragmented Afromontane Forest Landscape

Scatterhoarding by rodents, whereby seeds are collected and stored for later consumption, can result in seed dispersal. Seeds may be covered in litter on the forest floor (cached) or buried. This is particularly so in the Neotropics for large, nutritious seeds, and where primary dispersers are rare or missing. In African forests, contemporary anthropogenic pressures such as hunting, forest degradation, and fragmentation are contributing toward major declines in large frugivores, yet the potential for scatterhoarding to mitigate this loss is largely unknown. In this study, we used thread‐marked seed to explore the balance between seed predation and dispersal by rodents in Afromontane forest. We studied two tree species in three habitats: (1) continuous forest; (2) continuous forest edge, and (3) small, degraded riparian forest patches. We found that seed removal rates were high and almost the same in all three habitats for both tree species, but that the predation/dispersal balance differed among habitats. In continuous forest, more seeds of each species were scatterhoarded than depredated, and rates of scatterhoarding differed between the two species. In all habitats, burying seeds up to 2 cm belowground was more common than caching. Distances seeds were moved was approximately five times greater in continuous forest than in forest edge or riparian patches. We found strong evidence to suggest that the African pouched rat, Cricetomys sp. nov was responsible for the scatterhoarding.     

Toucans (Ramphastos ambiguus) facilitate resilience against seed dispersal limitation to a large‐seeded tree (Virola surinamensis) in a human‐modified landscape

Large‐seeded plants may suffer seed dispersal limitation in human‐modified landscapes if seed dispersers are absent or unable to disperse their seeds. We investigated dispersal limitation for the large‐seeded tree Virola surinamensis in a human‐modified landscape in southern Costa Rica. During two fruiting seasons, we monitored crop size, seed removal rates, the number of fruiting conspecifics within 100 m, and feeding visitation rates by frugivores at trees located in high and low forest disturbance conditions. Seed removal rates and the total number of seeds removed were high regardless of the disturbance level, but these parameters increased with tree crop size and decreased with the number of fruiting V. surinamensis trees within a 100 m radius. Trees at low disturbance levels were more likely to be visited by seed dispersers. Black mandibled toucans (Ramphastos ambiguus) and spider monkeys (Ateles geoffroyi) were the most important seed dispersers, based on visitation patterns and seed removal rates. Spider monkey feeding visits were more frequent at high disturbance levels, but the monkeys preferentially visited isolated trees with large yields and surrounded by a low number of fruiting Virola trees within 100 m. Toucan visitation patterns were not constrained by any of the predictors and they visited trees equally across the landscape. We suggest that isolated and highly fecund Virola trees are an important food resource for spider monkeys in human‐modified landscapes and that toucans can provide resilience against seed dispersal limitations for large‐seeded plants in human‐modified landscapes in the absence of hunting.     

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.     

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.     

Response of ants to human‐altered habitats with reference to seed dispersal of the myrmecochore Corydalis giraldii Fedde (Papaveraceae)

Anthropogenic habitat disturbance has potential consequences for ant communities. However, there is limited information on the effects of ant responses on associated ecological processes such as seed dispersal. We investigated the effect of disturbance on the abundance, richness, and composition of ant communities and the resulting seed‐dispersal services for a herbaceous myrmecochore, Corydalis giraldii (Papaveraceae), in an undisturbed habitat (forest understory), moderately disturbed habitat (abandoned arable field), and highly disturbed habitat (road verge) on Qinling Mountains, China. In total, we recorded 13 ant species, and five out of these were observed to transport seeds. The community composition of dispersers was significantly different amongst habitats. The richness of the dispersers did not differ among the habitats, but their total abundance varied significantly across habitats and was 21% lower in the road verge than in the abandoned arable fields. The major seed‐dispersing ant species in both the forest understory and the abandoned arable field were large‐bodied (Myrmica sp. and Formica fusca, respectively), whereas the major seed‐dispersing ants found in the road verge were the small‐bodied Lasius alienus. This difference resulted in lower seed removal rates and dispersal distances in the road verge than in the other two habitats. The different dispersal patterns were attributed primarily to differences in dispersing ant abundance and identity, most likely in response to habitats with different degree of anthropogenic disturbance. The possible influence of disturbance on the ecological specialization of ant‐seed dispersal interaction is also discussed.     

Predicting the Long-Term Effects of Hunting on Plant Species Composition and Diversity in Tropical Forests

Hunting can change abundances of vertebrate seed predators and seed dispersers, causing species‐specific changes in seed dispersal and seed predation and altering seedling communities. What are the consequences of these changes for the adult plant community in the next generation and beyond? Here, I derive equations showing how reduced seed dispersal reduces plant reproduction by intensifying kin competition, increasing vulnerability to natural enemies, and reducing the proportion of seeds passing through disperser guts. I parameterize these equations with available empirical data to estimate the likely effects on next‐generation abundances. I then consider the indirect effects and longer‐term feedbacks of changed seed or adult abundances on reproductive rates due to density‐dependent interactions with natural enemies and mutualists, as well as niche differentiation with competitors, and discuss their likely qualitative effects. The factors limiting seed disperser and seed predator populations in natural and hunted forests emerge as critical for determining the long‐term effects of hunting on rates of seed dispersal and seed predation. For example, where seed dispersers are held to a constant abundance by hunters, decreases in the availability of their preferred food plants are expected to lead to increased per‐seed dispersal probabilities, potentially to the point of compensating for the initial disperser decline. I close by discussing the likely reversibility of hunting‐induced changes in tropical forests and key questions and directions for future research.     

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

1. 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.
2. 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.
3. 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.
4. 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.

     

Consequences of Lemur Loss for Above-Ground Carbon Stocks in a Malagasy Rainforest

Anthropogenic disturbances have resulted in declines of seed-dispersing primate frugivores in tropical forests. Previous work has suggested that loss of seed dispersal by large frugivores may have a negative impact on ecosystem carbon storage by reducing tree biomass. However, we know little about the potential impacts of losing frugivores in Madagascar’s diverse rainforest ecosystem. Understanding the effects of frugivore extinction on carbon loss is relevant in Madagascar, where threatened lemur taxa are the only dispersers of many large-seeded plant species. Using a dataset of tree species composition and traits from the southeastern rainforests of Ranomafana National Park, we examined whether seed size and lemur-dependent dispersal are positively associated with above-ground tree biomass. We then simulated different scenarios of population declines of large-seeded trees (>10 mm seed length) dependent on lemur-mediated seed dispersal, to examine potential directional changes in carbon storage capacity of Malagasy forests under lemur loss. Lemur-dispersed tree species, which have large seeds, had higher above-ground biomass than other species. Our simulations showed that the loss of large frugivorous primates in Madagascar may decrease the forest’s potential to store carbon. These results demonstrate the importance of primate conservation for maintaining functioning ecosystems and forest carbon stocks in one of the world’s hottest hotspots of biodiversity.     

The Role of Arboreal Seed Dispersal Groups on the Seed Rain of a Lowland Tropical Forest1

Most tropical plants produce fleshy fruits that are dispersed primarily by vertebrate frugivores. Behavioral disparities among vertebrate seed dispersers could influence patterns of seed distribution and thus forest structure. This study investigated the relative importance of arboreal seed dispersers and seed predators on the initial stage of forest organization–seed deposition. We asked the following questions: (1) To what degree do arboreal seed dispersers influence the species richness and abundance of the seed rain? and (2) Based on the plant species and strata of the forest for which they provide dispersal services, do arboreal seed dispersers represent similar or distinct functional groups? To answer these questions, seed rain was sampled for 12 months in the Dja Reserve, Cameroon. Seed traps representing five percent of the crown area were erected below the canopies of 90 trees belonging to nine focal tree species: 3 dispersed by monkeys, 3 dispersed by large frugivorous birds, and 3 wind‐dispersed species. Seeds disseminated by arboreal seed dispersers accounted for ca 12 percent of the seeds and 68 percent of the seed species identified in seed traps. Monkeys dispersed more than twice the number of seed species than large frugivorous birds, but birds dispersed more individual seeds. We identified two distinct functional dispersal groups, one composed of large frugivorous birds and one composed of monkeys, drop dispersers, and seed predators. These groups dispersed plants found in different canopy strata and exhibited low overlap in the seed species they disseminated. We conclude it is unlikely that seed dispersal services provided by monkeys could be compensated for by frugivorous birds in the event of their extirpation from Afrotropical forests.     

Pleistocene megafaunal extinctions and the functional loss of long‐distance seed‐dispersal services

Pleistocene extinctions affected mainly large‐bodied animals, determining the loss or changes in numerous ecological functions. Evidence points to a central role of many extinct megafauna herbivores as seed dispersers. An important step in understanding the legacy of extinct mutualistic interactions is to evaluate the roles and effectiveness of megafauna herbivores in seed dispersal. Here we use morphological and ecophysiological allometries to estimate both quantitative and qualitative aspects of seed‐dispersal services likely provided by extinct megafauna. We developed a mechanistic model that encompasses four stages of seed dispersal – seed ingestion, gut retention, animal movement, and seed deposition. We estimate seed‐dispersal kernels through simulations to infer the role of Pleistocene megafauna in promoting long‐distance dispersal and examine how seed dispersal was affected by extinctions. Simulations suggest extinct large‐bodied frugivores would frequently disperse large seeds over a thousand meters, whereas smaller‐bodied frugivores are more likely to deposit the seeds over a few hundred meters. Moreover, events of long‐distance seed dispersal by the extinct megafauna would be up to ten times longer than long‐distance dispersal by smaller‐sized extant mammals. By estimating the combined distribution of seed dispersal distances considering all large‐bodied mammalian frugivores in specific South American Pleistocene assemblages we found that long‐distance dispersal contracted by at least two thirds after the megafauna died out. The disruption of long‐distance dispersal is expected to have consequences for recruitment, spatial and genetic structure of plant populations, population persistence and community composition. Promoting long‐distance seed dispersal was one among other salient features of extinct Pleistocene megafauna that reveal their influence on natural ecosystems. Modeling the consequences of megafaunal extinctions can offer quantitative predictions on the consequences of ongoing defaunation to plant populations and ecological communities.     

Arborescent palm seed morphology and seedling distribution.

This study examines how the seed morphology of two large arborescent palms, Attalea maripa (Aubl.) Mart. and Astrocaryum aculeatum G. Mey, may affect their seed shadow in a seasonally dry Amazonian forest. In addition to being smaller and produced in larger numbers than those of A. aculeatum, A. maripa seeds also presented a substantially lower amount of nutritional reserves available for the embryo. However, A. maripa seedlings were found in much higher numbers than those of A. aculeatum. The results suggest that, within the spatial scale considered, the seed rain of A. maripa is more restricted to the area surrounding around reproductive conspecifics than that of A. aculeatum. Furthermore, in comparison with those of A. aculeatum, the smaller seeds of A. maripa might be less attractive to scatterhoarding rodents (e.g. Dasyprocta aguti). The pattern observed emphasizes the importance of scatterhoarding rodents as dispersers of large-seeded plant species in Neotropical forests.     

Primate seed dispersal: Coevolution and conservation implications

Early studies of primates have demonstrated that many species rely heavily on fruit, and that primates constitute a large component of the frugivore biomass in tropical forests. Consequently, primates have long been thought to be important seed dispersers. It is only recently that studies have been conducted that have illustrated the complex nature of the interactions between fruit-eating primates and their food trees. Such studies have raised questions as to the causes and conse-quences of the intriguing differences between primate communities, the importance of other animals in the interactions (such as dung beetles and rodents that secon-darily disperse seeds), how primate-plant interactions evolve, and the significance of primates in forest regeneration and conservation. Since subsistence and com-mercial hunting of primates has heavily impacted frugivore communities, but left the physical structure of the forest relatively unaltered, studies of primate seed dispersal have important implications for the future of forests where seed dispersers have declined or disappeared.     

How do primates affect seed germination? A meta‐analysis of gut passage effects on neotropical plants

Biotic seed dispersal is a key process maintaining biodiversity in tropical forests where most trees produce vertebrate‐dispersed seeds. Existing meta‐analyses suggest an overall positive effect of vertebrate gut passage on seed germination, but no significant effects for non‐flying mammals. However, previous meta‐analyses combined rodents (seed predators) and primates (seed dispersers) into the non‐flying mammals category, which may confound specific effects of each group on seed germination. However positive effects of monkeys on germination had previously been found in some studies. Here we disentangle the role of Neotropical primates as contributors to seed dispersal in tropical forests by running a meta‐analysis to determine the overall magnitude of gut passage effects on seed germination percentage and mean time to germination. We also compare effect sizes as a function of different feeding guilds, gut complexities, and seed size. Our results show a strong, positive effect of primates on seed germination percentage and on the number of days to first germination. Strictly frugivorous monkeys, the group most threatened by extinction, showed the highest dispersal quality, increasing germination percentage by 75%. Primates that include insects in their diets had no average effect on germination percentage or time. Gut passage had different outcomes on seeds with different sizes; both large and small seeds showed similar increases in germination percentages after gut passage, but only large seeds germinated faster than control seeds after gut passage. Our results show a relevant role for primates in providing high seed dispersal quality and as drivers of forest regeneration. The combined effects of defaunation and forest fragmentation may result in decreased regeneration of trees, which has the potential to affect negatively both forest structure and ecosystem processes. Finally, we provide general guidelines for standardizing research on seed dispersal by primates. Synthesis Consuming fleshy fruits and dispersing seeds is the main ecological service provided by vertebrates to plants. Vertebrate increases seed germination due to treatment given during digestive system passage. Previous meta‐analyses suggest an overall positive effect of vertebrate gut passage on germination, but no insights are available on its variation among different functional groups of mammals. Our analyses indicated that gut passage by Neotropical primates increased seed germination. Strict frugivores, the ones most threatened by extinction, were the most efficient. Our results show a relevant role for primates in providing high seed dispersal quality and as drivers of forest regeneration, which can be meaningful for conservation in a community scale.     

Fishing‐down within populations harms seed dispersal mutualism

Large fish are often the most effective seed dispersers, but they are also the preferred target for fisheries. We recently started to comprehend the detrimental impacts of the extirpation of large frugivorous fish species on natural forest regeneration, but we lack a general understanding of how intraspecific size‐selective harvest affects fish–fruit mutualism. Our literature review demonstrated that large individuals within populations positively affect diverse aspects of seed dispersal, from consuming a higher diversity of seeds to enhancing germination. Furthermore, we filled a research gap by studying how individual size variations within two small frugivorous fish species (<16 cm) affect seed dispersal in flooded savannas. Even within small‐bodied species, large individuals swallow a higher number of intact seeds, but not necessarily a higher proportion. Overall, our results demonstrate the disproportional role of large‐bodied individuals as key seed dispersers in flooded habitats. Consequently, fishing‐down within both large‐ and small‐bodied species can negatively affect seed dispersal and natural regeneration in overfished wetlands.     

Dung Beetle Communities and Seed Dispersal in Primary Forest and Disturbed Land in Amazonia1

Seeds from tropical fruiting trees ingested and defecated on the soil surface by primary dispersers (such as primates) are vulnerable to destruction from rodents, insects, and fungi. Burial by dung beedes as an incidental result of their feeding and nesting activities often provides these seeds with refugia from attack. To examine the effect of habitat disturbance on the dung beetle communities involved in this process, I surveyed dung beedes at three sites in the Amazon basin, in die states of Parí, Amazonas, and Rondónia, Brazil. Through principal component analysis on measurements of size and behavioral characters of beedes, I determined the relative quality of beetle species as seed dispersers (dispersal defined as horizontal or vertical movement of seeds) and ranked them into seed dispersal guilds. I used correspondence analysis to examine in what habitats (primary forest or varying degrees of disturbed habitat) these guilds were abundant. Most guilds decreased with increasing habitat disturbance, but one guild made up of large nocturnal burrowers (primarily Dichotomius) became more abundant with increasing disturbance (up to the level of highest disturbance surveyed), at which point all dung beede species became scarce. Clear–cuts had lower species richness, lower abundance, and lower biomass dian forested areas. These results imply that clear–cutting is detrimental to all seed dispersal dynamics in tropical rain forests, but that some levels of disturbance allow enough disperser activity to preserve this ecosystem function.     

Functional Redundancy and Complementarities of Seed Dispersal by the Last Neotropical Megafrugivores

Background

Functional redundancy has been debated largely in ecology and conservation, yet we lack detailed empirical studies on the roles of functionally similar species in ecosystem function. Large bodied frugivores may disperse similar plant species and have strong impact on plant recruitment in tropical forests. The two largest frugivores in the neotropics, tapirs (Tapirus terrestris) and muriquis (Brachyteles arachnoides) are potential candidates for functional redundancy on seed dispersal effectiveness. Here we provide a comparison of the quantitative, qualitative and spatial effects on seed dispersal by these megafrugivores in a continuous Brazilian Atlantic forest.

Methodology/Principal Findings

We found a low overlap of plant species dispersed by both muriquis and tapirs. A group of 35 muriquis occupied an area of 850 ha and dispersed 5 times more plant species, and 13 times more seeds than 22 tapirs living in the same area. Muriquis dispersed 2.4 times more seeds in any random position than tapirs. This can be explained mainly because seed deposition by muriquis leaves less empty space than tapirs. However, tapirs are able to disperse larger seeds than muriquis and move them into sites not reached by primates, such as large forest gaps, open areas and fragments nearby. Based on published information we found 302 plant species that are dispersed by at least one of these megafrugivores in the Brazilian Atlantic forest.

Conclusions/Significance

Our study showed that both megafrugivores play complementary rather than redundant roles as seed dispersers. Although tapirs disperse fewer seeds and species than muriquis, they disperse larger-seeded species and in places not used by primates. The selective extinction of these megafrugivores will change the spatial seed rain they generate and may have negative effects on the recruitment of several plant species, particularly those with large seeds that have muriquis and tapirs as the last living seed dispersers.     

Gibbons (Nomascus gabriellae) provide key seed dispersal for the Pacific walnut (Dracontomelon dao), in Asia's lowland tropical forest

Understanding the mutualisms between frugivores and plants is essential for developing successful forest management and conservation strategies, especially in tropical rainforests where the majority of plants are dispersed by animals. Gibbons are among the most effective seed dispersers in South East Asia's tropical forests, but are also one of the highly threatened arboreal mammals in the region. Here we studied the seed dispersal of the Pacific walnut (Dracontomelon dao), a canopy tree which produces fruit that are common in the diet of the endangered southern yellow-cheeked crested gibbon (Nomascus gabriellae). We found that gibbons were the most effective disperser for this species; they consumed approximately 45% of the fruit crop, which was four times more than that consumed by macaques – the only other legitimate disperser. Gibbons tracked the temporal (but not spatial) abundance of ripe fruits, indicating this fruit was a preferred species for the gibbon. Both gibbons and macaques dispersed the majority (>90%) of the seeds at least 20 m away from parent crowns, with mean dispersal distances by gibbons measuring 179.3 ± 98.0 m (range: 4–425 m). Seeds defecated by gibbons germinated quicker and at greater rates than seeds spat by macaques, or in undispersed fruits. Gibbon-dispersed seeds were also more likely to be removed by unknown seed predators or unknown secondary dispersers. Overall, gibbons play a key role in the regeneration of the Pacific walnut. Our findings have significant implications both for the management of the Pacific walnut tree dominating tropical rainforest as well as the reintroduction program of the Southern yellow-cheeked crested gibbon.