Frugivorous vertebrates such as primates are important dispersal agents in tropical forests, although the role of folivorous colobines is generally not considered. However, recent studies reported seed dispersal by endo- and epizoochory in colobine primates, including the proboscis monkey (Nasalis larvatus), suggesting that the role colobines play in seed dispersal might have been underestimated. In the Lower Kinabatangan Floodplain in Sabah, Malaysian Borneo, we investigated whether seeds were still able to germinate after being ingested by proboscis monkeys. Faecal samples (n = 201) from proboscis monkeys were collected between 2015 and 2017. Intact seeds belonging to eight plant species were found in 77% of the faecal samples. Nauclea spp. were the most abundant plant species, accounting for 98% of all intact seeds. This study is the first to conduct germination trials on seeds defecated by proboscis monkeys. Higher germination success was recorded in ingested Nauclea spp. seeds than in control seeds, from both ripe and unripe Nauclea orientalis fruits (P seed dispersal by enhancing the germination success of defecated seeds for at least some plant species. Similar to other colobines, although proboscis monkeys may provide a lower contribution to seed dispersal (low seed diversity over short distances) than other sympatric frugivores, this study emphasises that proboscis monkeys do contribute to the dispersal of intact seeds, such as Nauclea spp., in potentially suitable riverine habitats.
Seed dispersals deal with complex systems through which the data collected using advanced seed tracking facilities pose challenges to conventional approaches, such as empirical and deterministic models. The use of stochastic models in current seed dispersal studies is encouraged. This review describes three existing stochastic models: the birth-death process (BDP), a 2 dimensional ( 2
D
) symmetric random walks and a 2
D
intermittent walks. The three models possess Markovian property, which make them flexible for studying natural phenomena. Only a few of applications in ecology are found in seed dispersals. The review illustrates how the models are to be used in seed dispersals context. Using the nonlinear BDP, we formulate the individual-based models for two competing plant species while the cover time model is formulated by the symmetric and intermittent random walks. We also show that these three stochastic models can be formulated using the Gillespie algorithm. The full cover time obtained by the symmetric random walks can approximate the Gumbel distribution pattern as the other searching strategies do. We suggest that the applications of these models in seed dispersals may lead to understanding of many complex systems, such as the seed removal experiments and behaviour of foraging agents, among others.
The loss of large animals due to overhunting and habitat loss potentially affects tropical tree populations and carbon cycling. Trees reliant on large-bodied seed dispersers are thought to be particularly negatively affected by defaunation. But besides seed dispersal, defaunation can also increase or decrease seed predation. It remains unclear how these different defaunation effects on early life stages ultimately affect tree population dynamics. We reviewed the literature on how tropical animal loss affects different plant life stages, and we conducted a meta-analysis of how defaunation affects seed predation. We used this information to parameterize models that altered matrix projection models from a suite of tree species to simulate defaunation-caused changes in seed dispersal and predation. We assessed how applying these defaunation effects affected population growth rates. On average, population-level effects of defaunation were negligible, suggesting that defaunation may not cause the massive reductions in forest carbon storage that have been predicted. In contrast to previous hypotheses, we did not detect an effect of seed size on changes in seed predation rates. The change in seed predation did not differ significantly between exclosure experiments and observational studies, although the results of observational studies were far more variable. Although defaunation surely affects certain tree taxa, species that benefit or are harmed by it and net changes in forest carbon storage cannot currently be predicted based on available data. Further research on how factors such as seed predation vary across tree species and defaunation scenarios is necessary for understanding cascading changes in species composition and diversity.
Mutualistic and antagonistic plant-animal interactions differentially contribute to the maintenance of species diversity in ecological communities. Although both seed dispersal and predation by fruit-eating animals are recognized as important drivers of plant population dynamics, the mechanisms underlying how seed dispersers and predators jointly affect plant diversity remain largely unexplored. Based on mediating roles of seed size and species abundance, we investigated the effects of seed dispersal and predation by two sympatric primates (Nomascus concolor and Trachypithecus crepusculus) on local plant recruitment in a subtropical forest of China. Over a 26 month period, we confirmed that these primates were functionally distinct: gibbons were legitimate seed dispersers who dispersed seeds of 44 plant species, while langurs were primarily seed predators who destroyed seeds of 48 plant species. Gibbons dispersed medium-seeded species more effectively than small- and large-seeded species, and dispersed more seeds of rare species than common and dominant species. Langurs showed a similar predation rate across different sizes of seeds, but destroyed a large number of seeds from common species. Due to gut passage effects, gibbons significantly shortened the duration of seed germination for 58% of the dispersed species; however, for 54% of species, seed germination rates were reduced significantly. Our study underlined the contrasting contributions of two primate species to local plant recruitment processes. By dispersing rare species and destroying the seeds of common species, both primates might jointly maintain plant species diversity. To maintain healthy ecosystems, the conservation of mammals that play critical functional roles needs to receive further attention.
Populations of forest trees exhibit large temporal fluctuations, but little is known about the synchrony of these fluctuations across space, including their sign, magnitude, causes and characteristic scales. These have important implications for metapopulation persistence and theoretical community ecology. Using data from permanent forest plots spanning local, regional and global spatial scales, we measured spatial synchrony in tree population growth rates over sub-decadal and decadal timescales and explored the relationship of synchrony to geographical distance. Synchrony was high at local scales of less than 1 km, with estimated Pearson correlations of approximately 0.6-0.8 between species' population growth rates across pairs of quadrats. Synchrony decayed by approximately 17-44% with each order of magnitude increase in distance but was still detectably positive at distances of 100 km and beyond. Dispersal cannot explain observed large-scale synchrony because typical seed dispersal distances (<100 m) are far too short to couple the dynamics of distant forests on decadal timescales. We attribute the observed synchrony in forest dynamics primarily to the effect of spatially synchronous environmental drivers (the Moran effect), in particular climate, although pests, pathogens and anthropogenic drivers may play a role for some species.
Although the role of primates in seed dispersal is generally well recognized, this is not the case for colobines, which are widely distributed in Asian and African tropical forests. Colobines consume leaves, seeds and fruits, usually unripe. A group of proboscis monkeys (Colobinae, Nasalis larvatus) consisting of 1 alpha-male, 6 adult females and several immatures, was observed from May 2005 to May 2006. A total of 400 fecal samples from focal group members covering 13 months were examined, with over 3500 h of focal observation data on the group members in a forest along the Menanggul River, Sabah, Malaysia. Intact small seeds were only found in 23 of 71 samples in Nov 2005, 15 of 38 in Dec 2005 and 5 of 21 in Mar 2006. Seeds of Ficus (all <1.5 mm in length) were found in all 3 months and seeds from Antidesma thwaitesianum (all <3 mm) and Nauclea subdita (all <2 mm) only in Nov and Dec, which was consistent with members of the study group consuming fruits of these species mostly at these times. To our knowledge, these are the first records of seeds in the fecal samples of colobines. Even if colobines pass relatively few seeds intact, their high abundance and biomass could make them quantitatively significant in seed dispersal. The potential role of colobines as seed dispersers should be considered by colobine researchers.
Many carnivorous mammals consume fruits and disperse the intact seeds to specific sites. Few studies have attempted to quantify this seed dispersal or evaluate its effectiveness, despite its potential importance and functional uniqueness. In the study reported here, we found that a frugivorous carnivore, the common palm civet (Paradoxurus hermaphroditus), generated seed shadows that are distinct from those of the sympatric frugivore, the pig-tailed macaque (Macaca nemestrina), and played a unique and important role in the regeneration of Leea aculeata (Leeaceae). We found that macaques dispersed the seeds randomly, while civets dispersed them non-randomly to sites such as the banks of small rivers, rain-flow paths, abandoned trails, and treefall gaps, which are characterized by low stem density and canopy cover. Seeds of L. aculeata that were dispersed by civets to the banks of rivers and gaps had significantly higher survival and growth rates than those dispersed to rain-flow paths or abandoned trails. Seeds dispersed by macaques or to random locations also had low survival. Although the effects of the civets on seed fate were not straightforward, compared with macaques and random dispersal, civets significantly enhanced the survival and growth of L. aculeata seeds after 1 year. These results indicate that non-random dispersal by civets is important for the persistence of L. aculeata. Civets may disperse other plant species and thus could have profound effects on forest dynamics.
A frequent observation in plant-animal mutualistic networks is that abundant species tend to be more generalised, interacting with a broader range of interaction partners than rare species. Uncovering the causal relationship between abundance and generalisation has been hindered by a chicken-and-egg dilemma: is generalisation a by-product of being abundant, or does high abundance result from generalisation? Here, we analyse a database of plant-pollinator and plant-seed disperser networks, and provide strong evidence that the causal link between abundance and generalisation is uni-directional. Specifically, species appear to be generalists because they are more abundant, but the converse, that is that species become more abundant because they are generalists, is not supported by our analysis. Furthermore, null model analyses suggest that abundant species interact with many other species simply because they are more likely to encounter potential interaction partners.
Large, fruit-eating vertebrates have been lost from many of the world's ecosystems. The ecological consequences of this defaunation can be severe, but the evolutionary consequences are nearly unknown because it remains unclear whether frugivores exert strong selection on fruit traits. I assessed the macroevolution of fruit traits in response to variation in the diversity and size of seed-dispersing vertebrates. Across the Indo-Malay Archipelago, many of the same plant lineages have been exposed to very different assemblages of seed-dispersing vertebrates. Phylogenetic analysis of >400 plant species in 41 genera and five families revealed that average fruit size tracks the taxonomic and functional diversity of frugivorous birds and mammals. Fruit size was 40.2-46.5% smaller in the Moluccas and Sulawesi (respectively), with relatively depauperate assemblages of mostly small-bodied animals, than in the Sunda Region (Borneo, Sumatra, and Peninsular Malaysia), with a highly diverse suite of large and small animals. Fruit color, however, was unrelated to vertebrate diversity or to the representation of birds versus mammals in the frugivore assemblage. Overhunting of large animals, nearly ubiquitous in tropical forests, could strongly alter selection pressures on plants, resulting in widespread, although trait-specific, morphologic changes.
We use individual-based information on the behavior of wild female Japanese macaques in two consecutive years with different food availability (nut-rich vs. nut-poor) to test effects of dominance rank and nut fruiting on seed dispersal parameters. We predicted that social rank would affect dispersal (1) quantity, (2) quality, (3) species richness, and (4) percentage of berries in the diet in the nut-poor year, while these differences would disappear in the nut-rich year. We found seeds of nine fleshy-fruited plant species in the feces of the monkeys. The frequency of seed occurrence for two plant species (Viburnum dilatatum and Rosa multiflora) showed an interaction between dominance ranks and years; in the nut-poor year V. dilatatum seeds were more abundant among dominant females and R. multiflora among subordinates, while such inter-rank differences disappeared in the nut-rich year. Similarly, the intact ratio of V. dilatatum seeds was lower for dominants in the nut-poor year, while inter-rank variations disappeared in the nut-rich year. Finally, percentage of berries in diet and seed richness showed no inter-annual nor inter-rank variations. Our study highlights that differences in individuals' social rank lead to within-group variation in seed dispersal services and that these differences are dependent on nut availability.
Homoplastic evolution of 'unique' morphological characteristics in the Schismatoglottideae - many previously used to define genera - prompted this study to compare morphology and function in connection with pollination biology for Aridarum nicolsonii, Phymatarum borneense and Schottarum sarikeense. Aridarum nicolsonii and P. borneense extrude pollen through a pair of horned thecae while S. sarikeense sheds pollen through a pair of pores on the thecae. Floral traits of spathe constriction, presence and movement of sterile structures on the spadix, the comparable role of horned thecae and thecae pores, the presence of stamen-associated calcium oxalate packages, and the timing of odour emission are discussed in the context of their roles in pollinator management. Pollinators for all investigated species were determined to be species of Colocasiomyia (Diptera: Drosophilidae).
Defaunation is causing declines of large-seeded animal-dispersed trees in tropical forests worldwide, but whether and how these declines will affect carbon storage across this biome is unclear. Here we show, using a pan-tropical data set, that simulated declines of large-seeded animal-dispersed trees have contrasting effects on aboveground carbon stocks across Earth's tropical forests. In our simulations, African, American and South Asian forests, which have high proportions of animal-dispersed species, consistently show carbon losses (2-12%), but Southeast Asian and Australian forests, where there are more abiotically dispersed species, show little to no carbon losses or marginal gains (±1%). These patterns result primarily from changes in wood volume, and are underlain by consistent relationships in our empirical data (∼2,100 species), wherein, large-seeded animal-dispersed species are larger as adults than small-seeded animal-dispersed species, but are smaller than abiotically dispersed species. Thus, floristic differences and distinct dispersal mode-seed size-adult size combinations can drive contrasting regional responses to defaunation.
Ficus species are keystone plants in tropical rainforests, and hemi-epiphytic figs play a notably important role in forest ecosystems. Because hemi-epiphytic figs have strict germination requirements, germination and establishment stages regulate their populations. Despite the ecological importance of hemi-epiphytic figs in the rainforests, seed dispersal systems by fig-eating animals under natural conditions remain unknown because of the difficulty in tracing the destiny of dispersed seeds in the canopy. Therefore, seed dispersal effectiveness (SDE) has never been evaluated for hemi-epiphytic figs. We evaluated the SDE of hemi-epiphytic figs using qualitative and quantitative components by three relatively large-sized (> 3 kg) arboreal and volant animals in Bornean rainforests that largely depend on fig fruits in their diets: binturongs Arctictis binturong, Mueller's gibbons Hylobates muelleri, and helmeted hornbills Rhinoplax vigil. The SDE values of binturongs was by far the highest among the three study animals. Meanwhile, successful seed dispersal of hemi-epiphytic figs by gibbons and helmeted hornbills is aleatory and rare. Given that seed deposition determines the fate of hemi-epiphytic figs, the defecatory habits of binturongs, depositing feces on specific microsites in the canopy, is the most reliable dispersal method, compared to scattering feces from the air or upper canopy. We showed that reliable directed dispersal of hemi-epiphytic figs occurs in high and uneven canopy of Bornean rainforests. This type of dispersal is limited to specific animal species, and therefore it may become one of the main factors regulating low-success hemi-epiphytic fig recruitment in Bornean rainforests.
There is an urgent need to identify and understand the ecosystem services of pollination and seed dispersal provided by threatened mammals such as flying foxes. The first step towards this is to obtain comprehensive data on their diet. However, the volant and nocturnal nature of bats presents a particularly challenging situation, and conventional microhistological approaches to studying their diet can be laborious and time-consuming, and provide incomplete information. We used Illumina Next-Generation Sequencing (NGS) as a novel, non-invasive method for analysing the diet of the island flying fox (Pteropus hypomelanus) on Tioman Island, Peninsular Malaysia. Through DNA metabarcoding of plants in flying fox droppings, using primers targeting the rbcL gene, we identified at least 29 Operationally Taxonomic Units (OTUs) comprising the diet of this giant pteropodid. OTU sequences matched at least four genera and 14 plant families from online reference databases based on a conservative Least Common Ancestor approach, and eight species from our site-specific plant reference collection. NGS was just as successful as conventional microhistological analysis in detecting plant taxa from droppings, but also uncovered six additional plant taxa. The island flying fox's diet appeared to be dominated by figs (Ficus sp.), which was the most abundant plant taxon detected in the droppings every single month. Our study has shown that NGS can add value to the conventional microhistological approach in identifying food plant species from flying fox droppings. At this point in time, more accurate genus- and species-level identification of OTUs not only requires support from databases with more representative sequences of relevant plant DNA, but probably necessitates in situ collection of plant specimens to create a reference collection. Although this method cannot be used to quantify true abundance or proportion of plant species, nor plant parts consumed, it ultimately provides a very important first step towards identifying plant taxa and spatio-temporal patterns in flying fox diets.
The world's largest terrestrial animals (megafauna) can play profound roles in seed dispersal. Yet, the term 'megafauna' is often used to encompass a diverse range of body sizes and physiologies of, primarily, herbivorous animals. To determine the extent to which these animals varied in their seed dispersal effectiveness (SDE), we compared the contribution of different megafauna for the large-fruited Platymitra macrocarpa (Annonaceae), in a tropical evergreen forest in Thailand. We quantified 'seed dispersal effectiveness' by measuring the quantity and quality contributions of all consumers of P. macrocarpa fruit. Seed dispersal quantity was the proportion of the crop consumed by each species. Quality was defined as the proportion of seeds handled by each animal taxon that survived to produce a 2-month seedling. Megafauna (elephants, sambar deer, bears) dispersed 78% of seeds that produced seedlings, with 21% dispersed by gibbons (a medium-sized frugivore). The main megafaunal consumers displayed different dispersal strategies. Elephants were the most effective dispersers (37% of seedlings) and they achieved this by being high-quality and low-quantity dispersers. Bears displayed a similar strategy but were especially rare visitors to the trees (24% of the total seedlings produced). Sambar were high-quantity dispersers, but most seeds they handled did not survive and they were responsible for only 17% of seedlings. Gibbons displayed a high SDE relative to their body size, but they probably cannot match the role of elephants despite being more regular consumers of the fruit. The low density and poor regeneration of P. macrocarpa in the study site suggest that current dispersal rates by megafauna are insufficient, possibly reflecting reduced or missing megafauna populations. We show that different megafaunal species disperse seeds in different ways and may make unique contributions to the reproductive success of the plant species.