Macaques as Seed Dispersal Agents in Asian Forests: A Review

The role of primates in seed dispersal is well recognized. Macaques (Macaca spp.) are major primate seed dispersers in Asia, and recent studies have revealed their role as seed dispersal agents in this region. Here, we review present knowledge of the traits that define the role of macaques as seed dispersers. The size of seeds in fruit influences whether macaques swallow (0.5–17.1 mm; median: 3.0), spit (1–37 mm; median: 7.6), or drop (8.2–57.7 mm; median: 20.5) them. Dispersal distances via defecation are several hundreds of meters (median: 259 m, range: 0–1300 m), shorter than those achieved by some mammals and birds in tropical and temperate regions. However, macaques disperse seeds by defecation at comparable distances to omnivorous carnivores, and further than passerines. Seed dispersal distance by spitting is much shorter (median: 20 m, range: 0–405 m) than by defecation. Among Asian primates, seed dispersal distances resulting from macaque defecation are shorter than those for gibbons and longer than those for langurs. The effects of seed ingestion on the percentage and speed of germination vary among both plant and macaque species. The degree of frugivory, fruit/seed handling methods, seed dispersal distance, microhabitats of dispersed seeds, and effects of dispersal on seed germination vary seasonally and interannually, and long-term studies of the ecological role of macaques are needed. Researchers have begun to assess the effectiveness of seed dispersal by macaques, secondary dispersal of seeds originally dispersed by macaques, and the effects of provisioning on seed dispersal. Future studies should also test the effects of social factors (such as age and rank), which have received little attention in studies of seed dispersal.     

Mammalian seed dispersal in Cantabrian woodland pastures: Network structure and response to forest loss

We evaluated the role of wild large mammals as dispersers of fleshy-fruited woody plants in woodland pastures of the Cantabrian range (N Spain). By searching for seeds in mammal scats across four localities, we addressed how extensive seed dispersal was in relation to the fleshy-fruited plant community, and applied a network approach to identify the relative role of mammal species in the seed dispersal process. We also tested the response of mammalian dispersers to forest availability at increasing spatial scales. Five carnivores and three ungulates dispersed seeds of eight fleshy-fruited trees and shrubs. Mammalian seed dispersal did not mirror community-wide fruit availability, as abundant fruiting trees were scarce whereas thorny shrubs were over-represented among dispersed species. The dispersal network was dominated by bramble (Rubus ulmifolius/fruticosus), the remaining plants being rarer and showing more restricted disperser coteries. Fox (Vulpes vulpes), badger (Meles meles), and wild boar (Sus scrofa) dispersed mostly bramble, whereas martens (Martes sp.) dispersed mostly wild rose (Rosa sp.). Ungulates occasionally dispersed holly (Ilex aquifolium) and hawthorn (Crataegus monogyna). The empirical network reflected a skewed distribution of interactions and some functional complementarity (as judged from the low levels of connectance and nestedness), but also some degree of specialization. Mammals overused uncovered microsites for seed deposition, and increased their disperser activity in those landscape sectors devoid of forest. Combined with previous findings on avian seed dispersal, this study suggest a strong functional complementarity coming from the low overlap in the main plant types that mammals and birds disperse – thorny shrubs and trees, respectively – and the differential patterns of seed deposition, with mammals mostly dispersing into deforested areas, and birds into forest-rich landscapes.     

Seed Dispersal by Primates in Asian Habitats: From Species,to Communities,to Conservation

Primates are among the most important seed dispersers in the habitats they occupy. Understanding the extent of, and gaps in, our knowledge of seed dispersal by Asian primates is essential, because many of these primates are extremely vulnerable to anthropogenic disturbance. In this review, I show how initial studies focused on the role of individual species in seed dispersal have expanded more recently to consider their role in the wider frugivore community. There are five functional groups of primate seed dispersers in Asia; most of our information comes from the (usually) highly frugivorous macaques and gibbons, while our understanding of the roles played by orangutans and, especially, colobines and lorises remains rudimentary. Preliminary community-wide studies suggest a pivotal role for gibbons and macaques in frugivore communities, with higher dispersal overlap with other mammals than with birds. The gaps in our knowledge are plentiful, however, including understanding fruit selection in detail, determining how seed dispersal roles might change across different habitats, evaluating the balance between mutualisms and antagonisms in orangutans and macaques, describing postdispersal processes, and documenting how habitats are impacted by changes in primate abundance and behavior.     

Forest cover,hunting pressure,and fruit availability influence seed dispersal in a forest‐savanna mosaic in the Congo Basin

Forest fragmentation, reduced forest cover, and hunting pressure are the main threats affecting animal‐mediated seed dispersal. However, their combined effects on seed dispersal rates have been simultaneously investigated only rarely, and never in Africa. We aimed to disentangle the effects of forest cover, hunting pressure, frugivore abundance, and fruit availability at the local and landscape scales on the seed dispersal rates of Staudtia kamerunensis (Myristicaceae). To estimate the percentages of seed dispersal failure (undispersed seeds), we quantitated fruit remains below fruiting trees distributed across five contrasting sites in a semi‐natural forest‐savanna mosaic in the Democratic Republic of Congo. We used statistical analyses accounting for spatial autocorrelation and found that forest cover in the surrounding landscape, hunting level, the associated abundance of dispersers, and fruit availability all had significant effects on the percentage of seed dispersal failure. The combination of high fruit availability and reduced abundance of seed dispersers could accelerate seed disperser satiation, causing the seed dispersal system to be saturated. Our study highlights how two major factors associated with anthropogenic activities, forest cover and hunting, affect seed dispersal by animals. These findings could have far‐reaching implications for our understanding of tree‐frugivore interactions and the conservation of tropical communities.     

Conflicting selection pressures on seed size: evolutionary ecology of fruit size in a bird-dispersed tree, Olea europaea

Recent evidence indicates that fruit size has evolved according to dispersers' size. This is hypothesized to result from a balance between factors favouring large seeds and dispersers setting the maximum fruit size. This hypothesis assumes that (1) the size of fruits that can be consumed by dispersers is limited, (2) fruit and seed size are positively correlated, and (3) the result of multiple selection pressures on seed size is positive. Our studies on the seed dispersal mutualism of Olea europaea have supported the first and second assumptions, but valid tests of the third assumption are still lacking. Here we confirm the third assumption. Using multiplicative fitness components, we show that conflicting selection pressures on seed size during and after dispersal reverse the negative pattern of selection exerted by dispersers.     

Frugivory and spatial patterns of seed deposition by carnivorous mammals in anthropogenic landscapes: a multi-scale approach

Background

Knowledge about how frugivory and seed deposition are spatially distributed is valuable to understand the role of dispersers on the structure and dynamics of plant populations. This may be particularly important within anthropogenic areas, where either the patchy distribution of wild plants or the presence of cultivated fleshy-fruits may influence plant-disperser interactions.

Methodology/Principal Findings

We investigated frugivory and spatial patterns of seed deposition by carnivorous mammals in anthropogenic landscapes considering two spatial scales: ‘landscape’ (∼10 km²) and ‘habitat type’ (∼1–2 km²). We sampled carnivore faeces and plant abundance at three contrasting habitats (chestnut woods, mosaics and scrublands), each replicated within three different landscapes. Sixty-five percent of faeces collected (n = 1077) contained seeds, among which wild and cultivated seeds appeared in similar proportions (58% and 53%) despite that cultivated fruiting plants were much less abundant. Seed deposition was spatially structured among both spatial scales being different between fruit types. Whereas the most important source of spatial variation in deposition of wild seeds was the landscape scale, it was the habitat scale for cultivated seeds. At the habitat scale, seeds of wild species were mostly deposited within mosaics while seeds of cultivated species were within chestnut woods and scrublands. Spatial concordance between seed deposition and plant abundance was found only for wild species.

Conclusions/Significance

Spatial patterns of seed deposition by carnivores differed between fruit types and seemed to be modulated by the fleshy-fruited plant assemblages and the behaviour of dispersers. Our results suggest that a strong preference for cultivated fruits by carnivores may influence their spatial foraging behaviour and lower their dispersal services to wild species. However, the high amount of seeds removed within and between habitats suggests that carnivores must play an important role – often overlooked – as ‘restorers’ and ‘habitat shapers’ in anthropogenic areas.     

Did fleshy fruit pulp evolve as a defence against seed loss rather than as a dispersal mechanism?

Relatively few studies have examined the evolution of the mutualism between endozoochorous plants and seed dispersers. Most seed dispersal studies are ecological and examine the role of fruit pulp in promoting seed dispersal. This interaction is often assumed to have originated due to selection stemming from seed dispersers. Here I suggest a "defence scenario" wherein fleshy fruits originated as mechanisms to defend seeds and secondarily became structures to promote seed dispersal. I suggest that frugivory followed from herbivores that specialized on consuming seed defensive tissues and that enhanced seed dispersal was initially a consequence of seed defence. The proposed defence scenario is not posited as an explanation for the sequence that led to all modern frugivores. However, it is suggested that seed predation was the initial source of selection that led to fleshy fruits; the necessary precursor to frugivory. Support is described from the fossil record and from modern structures and interactions. Testable predictions are made in hope that greater interest will be focused on the defensive role of fleshy fruit pulp both in modern interactions and historically.     

Intraspecific directed deterrence by the mustard oil bomb in a desert plant

Plant secondary metabolites (SMs) acting as defensive chemicals in reproductive organs such as fruit tissues play roles in both mutualistic and antagonistic interactions between plants and seed dispersers/predators. The directed-deterrence hypothesis states that SMs in ripe fruits deter seed predators but have little or no effect on seed dispersers. Indeed, studies have demonstrated that birds are able to cope with fruit SMs whereas rodents are deterred by them. However, this mechanism was only demonstrated at the class level, i.e., between birds and mammals, based on differences in the vanilloid receptors. Here we present experimental and behavioral data demonstrating the use of the broad-range, class-independent "mustard oil bomb" mechanism in Ochradenus baccatus fruits to force a behavioral change at an ecological timescale, converting rodents from seed predators to seed dispersers. This is achieved by a unique compartmentalization of the mustard oil bomb, causing activation of the system only upon seed and pulp coconsumption, encouraging seed dispersal via seed spitting by rodents. Our findings demonstrate the power of SMs to shift the animal-plant relationship from predation to mutualism and provide support for the directed-deterrence hypothesis at the intraspecific level, in addition to the interspecific level.     

Selection on fruit traits is mediated by the interplay between frugivorous birds,fruit flies,parasitoid wasps and seed‐dispersing ants

Every organism on Earth must cope with a multitude of species interactions both directly and indirectly throughout its life cycle. However, how selection from multiple species occupying different trophic levels affects diffuse mutualisms has received little attention. As a result, how a given species amalgamates the combined effects of selection from multiple mutualists and antagonists to enhance its own fitness remains little understood. We investigated how multispecies interactions (frugivorous birds, ants, fruit flies and parasitoid wasps) generate selection on fruit traits in a seed dispersal mutualism. We used structural equation models to assess whether seed dispersers (frugivorous birds and ants) exerted phenotypic selection on fruit and seed traits in the spiny hackberry (Celtis ehrenbergiana), a fleshy‐fruited tree, and how these selection regimes were influenced by fruit fly infestation and wasp parasitoidism levels. Birds exerted negative correlational selection on the combination of fruit crop size and mean seed weight, favouring either large crops with small seeds or small crops with large seeds. Parasitoids selected plants with higher fruit fly infestation levels, and fruit flies exerted positive directional selection on fruit size, which was positively correlated with seed weight. Therefore, higher parasitoidism indirectly correlated with higher plant fitness through increased bird fruit removal. In addition, ants exerted negative directional selection on mean seed weight. Our results show that strong selection on phenotypic traits may still arise in perceived diffuse species interactions. Overall, we emphasize the need to consider diverse direct and indirect partners to achieve a better understanding of the mechanisms driving phenotypic trait evolution in multispecies interactions.     

Specialized Seed Dispersal in Epiphytic Cacti and Convergence with Mistletoes

Mistletoes represent the best example of specialization in seed dispersal, with a reduced assemblage of dispersal agents. Specific dispersal requirements mediated by the specificity of seed deposition site have apparently led to the evolution of such close relationships between mistletoes and certain frugivores. Here, we provide evidences for another case of specialization involving epiphytic cacti in the genus Rhipsalis, and small Neotropical passerines Euphonia spp., which also act as the main seed dispersers of mistletoes in the family Viscaceae. With field observations, literature search, and observations on captive birds, we demonstrated that Rhipsalis have specific establishment requirements, and euphonias are the most effective dispersers of Rhipsalis seeds in both quantitative and qualitative aspects, potentially depositing seeds onto branches of host plants. We interpret the similar dispersal systems of Rhipsalis and Viscaceae mistletoes, which involve the same dispersal agents, similar fruit morphologies, and fruit chemistry as convergent adaptive strategies that enable seeds of both groups to reach adequate microsites for establishment in host branches.     

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.     

Spanish juniper gain expansion opportunities by counting on a functionally diverse dispersal assemblage community

Seed dispersal is typically performed by a diverse array of species assemblages with different behavioral and morphological traits which determine dispersal quality (DQ, defined as the probability of recruitment of a dispersed seed). Fate of ecosystems to ongoing environmental changes is critically dependent on dispersal and mainly on DQ in novel scenarios. We assess here the DQ, thus the multiplicative effect of germination and survival probability to the first 3 years of life, for seeds dispersed by several bird species (Turdus spp.) and carnivores (Vulpes vulpes, Martes foina) in mature woodland remnants of Spanish juniper (Juniperus thurifera) and old fields which are being colonized by this species. Results showed that DQ was similar in mature woodlands and old fields. Germination rate for seeds dispersed by carnivores (11.5%) and thrushes (9.12%) was similar, however, interacted with microhabitat suitability. Seeds dispersed by carnivores reach the maximum germination rate on shrubs (16%), whereas seeds dispersed by thrushes did on female juniper canopies (15.5) indicating that each group of dispersers performed a directed dispersal. This directional effect was diluted when survival probability was considered: thrushes selected smaller seeds which had higher mortality in the seedling stage (70%) in relation to seedlings dispersed by carnivores (40%). Overall, thrushes resulted low‐quality dispersers which provided a probability or recruitment of 2.5%, while a seed dispersed by carnivores had a probability of recruitment of 6.5%. Our findings show that generalist dispersers (i.e., carnivores) can provide a higher probability of recruitment than specialized dispersers (i.e., Turdus spp.). However, generalist species are usually opportunistic dispersers as their role as seed dispersers is dependent on the availability of trophic resources and species feeding preferences. As a result, J. thurifera dispersal community is composed by two functional groups of dispersers: specialized low‐quality but trustworthy dispersers and generalist high‐quality but opportunistic dispersers. The maintenance of both, generalist and specialist dispersers, in the dispersal assemblage community assures the dispersal services and increases the opportunities for regeneration and colonization of degraded areas under a land‐use change scenario.     

Forest disturbance and seasonal food availability influence a conditional seed dispersal mutualism

The interaction between granivorous scatterhoarding mammals and plants is a conditional mutualism: scatterhoarders consume seeds (acting as predators), but the movement of seed by scatterhoarders may contribute to dispersal (acting as mutualists). Understanding the ecological factors that shape this relationship is highly relevant in anthropogenically disturbed tropical forests where large‐bodied frugivores are extirpated. In such forests, large‐seeded trees that once depended on these frugivores for dispersal may now only have scatterhoarders as prospective dispersers. We studied Carapa oreophila (Meliaceae) in an Afromontane forest, to test the hypotheses that the proportion of seeds immediately consumed or hoarded (dispersed) would vary over a disturbance gradient. Temporal replication also afforded exploration of how habitat effects might vary with food availability. Using a Bayesian framework, we demonstrate that seeds were more likely to be hoarded in less disturbed forest, irrespective of temporal variation in food abundance. In contrast, forest disturbance only appeared to increase seed predation in temporal replicates that coincided with sustained food availability. These results highlight the potential variability in the dynamics between plants and scatterhoarders over fine temporal scales, elucidating possible ecological scenarios where scatterhoarders might act as mutualists (contributing positively to plant recruitment). Our study also fills important knowledge gaps about the importance of scatterhoarders as dispersers in tropical forests depleted of large‐bodied frugivores, particularly in Africa where scatterhoarding mutualisms have not been extensively studied.     

Context‐dependent fruit–frugivore interactions: partner identities and spatio‐temporal variations

Fruit–frugivore interactions are crucial for the dynamics and regeneration of most forested ecosystems. Still, we lack an understanding of the potential variation in the sign and strength of such interactions in relation to variations in the spatial and temporal ecological context. Here, we evaluated spatial (three sites) and temporal (two fruiting seasons) local variation in the sign (seed predation versus dispersal) and strength (frequency and quantity) of the interactions among six frugivorous mammals and a community of Mediterranean fleshy‐fruited shrubs. We examined mammal faecal samples and quantified frequency of seed occurrence, number of seeds per faecal sample, seed species diversity and quality of seed treatment (i.e. percentage of undamaged seeds). The frequency of seed occurrence and number of seeds per faecal sample strongly varied among dispersers, sites, seasons and fruit species. For instance, fox Vulpes vulpes faeces showed between 6 and 40 times more seeds than wild boar Sus scrofa faeces in seasons or sites in which Rubus and Juniperus seeds were dominant. However, in seasons or sites dominated by Corema seeds, wild boar faeces contained up to seven times more seeds than fox faeces. Mammalian carnivores (fox and badger, Meles meles) treated seeds gently, acting mostly as dispersers, whereas deer (Cervus elaphus and Dama dama) acted mainly as seed predators. Interestingly, rabbit Oryctolagus cuniculus acted as either mostly seed disperser or seed predator depending on the plant species. Our results indicated that the sign of fruit–frugivore interactions depended mainly on the identity of the partners. For a particular fruit–frugivore pair, however, our surrogate of interaction strength largely varied with the spatio‐temporal context (year and habitat), leading to a low specificity across the seed–frugivore network. The high spatio‐temporal variability of seed dispersal (in quantity, quality and seed diversity) by different frugivores would confer resilience against unpredictable environmental conditions, such as those typical of Mediterranean ecosystems.     

Interspecific and annual variation in pre-dispersal seed predation by a granivorous bird in two East Asian hackberries, Celtis biondii and Celtis sinensis

Pre-dispersal seed predation by granivorous birds has potential to limit fruit removal and subsequent seed dispersal by legitimate avian seed dispersers in bird-dispersed plants, especially when the birds form flocks. We monitored pre-dispersal seed predation by the Japanese grosbeak, Eophona personata, of two bird-dispersed hackberry species (Cannabaceae), Celtis biondii (four trees) and Celtis sinensis (10 trees), for 3 years (2005, 2007 and 2008) in a fragmented forest in temperate Japan. Throughout the 3 years, predation was more intense on C. biondii, which, as a consequence, lost a larger part of its fruit crop. Grosbeaks preferred C. biondii seeds that had a comparatively lower energy content and lower hardness than C. sinensis, suggesting an association between seed hardness and selective foraging by grosbeaks. In C. biondii, intensive predation markedly reduced fruit duration and strongly limited fruit removal by seed dispersers, especially in 2007 and 2008. In C. sinensis, seed dispersers consumed fruits throughout the fruiting seasons in all 3 years. In C. biondii, variation in the timing of grosbeak migration among years was associated with annual variation in this bird's effects on fruit removal. Our results demonstrate that seed predation by flocks of granivorous birds can dramatically disrupt seed dispersal in fleshy-fruited plants and suggest the importance of understanding their flocking behaviour.     

Crop size is more important than neighborhood fruit availability for fruit removal of <Emphasis Type="Italic">Eugenia uniflora</Emphasis> (Myrtaceae) by bird seed dispersers

For a plant with bird-dispersed seeds, the effectiveness of seed dispersal can change with fruit availability at scales ranging from individual plants to neighborhoods, and the scale at which frugivory patterns emerge may be specific for frugivorous species differing in their life-history and behavior. The authors explore the influence of multispecies fruit availability at two local spatial scales on fruit consumption of Eugenia uniflora trees for two functional groups of birds. The authors related visitation and fruit removal by fruit gulpers and pulp mashers to crop size and conspecific and heterospecific fruit abundance to assess the potential roles that facilitative or competitive interactions play on seed dispersal. The same fruiting scenario influenced fruit gulpers (legitimate seed dispersers) and pulp mashers (inefficient dispersers) in different ways. Visits and fruit removal by legitimate seed dispersers were positively related to crop size and slightly related to conspecific, but not to heterospecific fruit neighborhoods. Visits and fruit consumption by pulp mashers was not related to crop size and decreased with heterospecific fruit availability in neighborhoods; however, this might not result in competition for dispersers. The weak evidence for facilitative or competitive processes suggest that interaction of E. uniflora with seed dispersers may depend primarily on crop size or other plant’s attributes susceptible to selection. The results give limited support to the hypothesis that spatial patterns of fruit availability influence fruit consumption by birds, and highlight the importance of considering separately legitimate and inefficient dispersers to explain the mechanisms that lie behind spatial patterns of seed dispersal.     

Frugivory by the fish Brycon hilarii (Characidae) in western Brazil

Frugivory and seed dispersal have been poorly studied in Neotropical freshwater fishes. We studied frugivory and seed dispersal by the piraputanga fish (Brycon hilarii, Characidae) in the Formoso River, Bonito, western Brazil. We examined the stomach contents of 87 fish and found the diet of piraputanga consisted of 24% animal prey (arthropods, snails, and vertebrates), 31% seeds/fruits and 45% other plant material (algae/macrophytes/leaves/flowers). The piraputangas fed on 12 fruit species, and were considered as seed dispersers of eight species. Fruits with soft seeds larger than 10 mm were triturated, but all species with small seeds (e.g. Ficus, Psidium) and one species with large hard seed (Chrysophyllum gonocarpum) were dispersed. Piraputangas eat more fruits in the dry season just before the migration, but not during the spawning season. Fish length had a positive relation with the presence of fruits in their guts. The gallery forest of the Formoso River apparently does not have any plant species that depend exclusively on B. hilarii for seed dispersal because all fruit species are also dispersed by birds and mammals. Based on seed size and husk hardness of the riparian plant community of Formoso River, however, the piraputangas may potentially disperse at least 50% of the riparian fleshy fruit species and may be particularly important for long-distance dispersal. Therefore, overfishing or other anthropogenic disturbances to the populations of piraputanga may have negative consequences for the riparian forests in this region.     

Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate

Background

Some neotropical, fleshy-fruited plants have fruits structurally similar to paleotropical fruits dispersed by megafauna (mammals >10³ kg), yet these dispersers were extinct in South America 10–15 Kyr BP. Anachronic dispersal systems are best explained by interactions with extinct animals and show impaired dispersal resulting in altered seed dispersal dynamics.

Methodology/Principal Findings

We introduce an operational definition of megafaunal fruits and perform a comparative analysis of 103 Neotropical fruit species fitting this dispersal mode. We define two megafaunal fruit types based on previous analyses of elephant fruits: fruits 4–10 cm in diameter with up to five large seeds, and fruits >10 cm diameter with numerous small seeds. Megafaunal fruits are well represented in unrelated families such as Sapotaceae, Fabaceae, Solanaceae, Apocynaceae, Malvaceae, Caryocaraceae, and Arecaceae and combine an overbuilt design (large fruit mass and size) with either a single or few (<3 seeds) extremely large seeds or many small seeds (usually >100 seeds). Within-family and within-genus contrasts between megafaunal and non-megafaunal groups of species indicate a marked difference in fruit diameter and fruit mass but less so for individual seed mass, with a significant trend for megafaunal fruits to have larger seeds and seediness.

Conclusions/Significance

Megafaunal fruits allow plants to circumvent the trade-off between seed size and dispersal by relying on frugivores able to disperse enormous seed loads over long-distances. Present-day seed dispersal by scatter-hoarding rodents, introduced livestock, runoff, flooding, gravity, and human-mediated dispersal allowed survival of megafauna-dependent fruit species after extinction of the major seed dispersers. Megafauna extinction had several potential consequences, such as a scale shift reducing the seed dispersal distances, increasingly clumped spatial patterns, reduced geographic ranges and limited genetic variation and increased among-population structuring. These effects could be extended to other plant species dispersed by large vertebrates in present-day, defaunated communities.     

Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) Region

Current knowledge of frugivory and seed dispersal by vertebrates in the Oriental Region is summarized. Some degree of frugivory has been reported for many fish and reptile species, almost half the genera of non-marine mammals and more than 40% of bird genera in the region. Highly frugivorous species, for which fruit dominates the diet for at least part of the year, occur in at least two families of reptiles, 12 families of mammals and 17 families of birds. Predation on seeds in fleshy fruits is much less widespread taxonomically: the major seed predators are colobine monkeys and rodents among the mammals, and parrots, some pigeons, and finches among the birds. Most seeds in the Oriental Region, except near its northern margins, are dispersed by vertebrate families which are endemic to the region or to the Old World. Small fruits and large, soft fruits with many small seeds are consumed by a wide range of potential seed dispersal agents, including species which thrive in small forest fragments and degraded landscapes. Larger, bigger-seeded fruits are consumed by progressively fewer dispersers, and the largest depend on a few species of mammals and birds which are highly vulnerable to hunting, fragmentation and habitat loss.     

Impact of habitat structure and fruit abundance on avian seed dispersal and fruit predation

So far, it is poorly understood how differential responses of avian seed dispersers and fruit predators to changes in habitat structure and fruit abundance along land-use gradients may translate into consequences for the seed dispersal of associated plants. We selected a gradient of habitat modification (forest, semi-natural, and rural habitat) characterized by decreasing tree cover and a high variation in local fruit availability. Along this gradient we quantified fruit removal by avian seed dispersers and fruit predators from 18 Sorbus aucuparia trees. We analyzed the relative importance of tree cover and fruit abundance in explaining species richness, abundance and fruit removal rates of both guilds from S. aucuparia trees. Species richness and abundance of seed dispersers decreased with decreasing tree cover, whereas fruit removal by seed dispersers decreased with decreasing fruit abundance independent of tree cover. Both variables had no effect on species richness, abundance and fruit removal by fruit predators. Consequently, seed dispersers dominated relative fruit removal in fruit-rich sites but the dispersal/predation ratio shifted in favor of predation in fruit-poor habitat patches. Our study demonstrates that variation in local habitat structure and fruit abundance can cause guild-specific responses. Such responses may result in a shift in fruit removal regimes and might affect the dispersal ability of dependent fruiting plants. Future studies should aim at possible consequences for plant recruitment and guild-specific responses of frugivores to disturbance gradients on the level of entire plant–frugivore associations.