Sympatric primate seed dispersers and predators jointly contribute to plant diversity in a subtropical forest.

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.

Effectiveness of primate seed dispersers for an "oversized" fruit, Garcinia benthamii.

The largest fruits found in tropical forests may depend on complementary seed dispersal strategies. These fruits are dispersed most effectively by megafauna, but populations can persist where megafauna are absent or erratic visitors. Smaller animals often consume these large fruits, but their capacity to disperse these seeds effectively has rarely been assessed. We evaluated the contributions of gibbons (Hylobates lar) and other frugivores in the seed dispersal of the megafaunal fruit Garcinia benthamii, using the SDE (seed dispersal effectiveness) landscape. Gibbons preferentially consumed G. benthamii fruits and were the main seed disperser that we observed. However, gibbons became satiated when availability was high, with 57% of fruits falling to the ground unhandled. Recruitment of seedlings from gibbon-dispersed seeds was also very low. Elephants consumed G. benthamii fruit, but occurred at low density and were rare visitors to the trees. We suggest that gibbons might complement the seed dispersal role of elephants for G. benthamii, allowing limited recruitment in areas (such as the study site) where elephants occur at low density. Fruit availability varied between years; when availability was low, gibbons reliably consumed most of the crop and dispersed some seeds that established seedlings, albeit at low numbers (2.5 seedlings per crop). When fruit availability was high, the fruit supply overwhelmed the gibbons and other arboreal frugivores, ensuring a large abundance of fruit available to terrestrial seed dispersers. Although gibbons effectively dispersed more seeds at these times (20.7 seedlings per crop), there was the potential for elephants to move many more seeds. Complementary seed dispersal strategies may be important for megafaunal fruit, because they ensure that very large fruits are able to benefit from megafaunal dispersal but also persist where this dispersal becomes erratic. However, our data suggest that smaller seed dispersers might not be capable of replacing large dispersers, leading to potential changes in landscape-scale dispersal patterns where megafauna are absent.

Seed dispersal by rhesus macaques Macaca mulatta in Northern India.

Frugivorous primates are important seed dispersers and their absence from forest patches is predicted to be detrimental to tropical forest regeneration and recruitment. With the reduction of primate populations globally, ecologically resilient primate species, characterized by dietary flexibility and the ability to thrive in a variety of habitats, assume new importance as seed dispersers. The most widely distributed non-human primate, the rhesus macaque Macaca mulatta has been intensively studied but little is known about its role in maintaining ecosystem structure and functions. Due to their frugivorous diet, large group sizes, large home ranges and tolerance to disturbance, rhesus macaques may be effective seed dispersers. We studied seed dispersal by rhesus macaques at the Buxa Tiger Reserve, India, through a combination of behavioural observations and germination experiments. Rhesus macaques dispersed 84% of the 49 species they fed on either through spitting or defecation. Nearly 96% of the handled seeds were undamaged and 61% of the species for which germination tests were performed had enhanced germination. Almost 50% of the monitored seeds among those deposited in situ germinated and 22% established seedlings, suggesting that rhesus macaques are important seed dispersers in tropical forests. Due to their widespread distribution and large populations, rhesus macaques are perceived as common and are categorized as Least Concern on the IUCN Red List, effectively excluding them from any conservation plans. Based on the results of our study, we argue that rhesus macaques fulfill critical ecological functions in their habitat and that this parameter must be taken into consideration when they are reviewed for conservation priorities.

Scientific concept and practices of life community of mountains, rivers, forests, farmlands, lakes, grasslands, and deserts in China.

China prioritizes ecological civilization construction and embraces the concept of "lucid waters and lush mountains are invaluable assets." Great achievements have been made in ecological protection and restoration through implementing a series of policies and projects. This paper reviews the history of ecological restoration in China and the current development of the "integrated protection and restoration project of mountains, rivers, forests, farmlands, lakes, grasslands, and deserts (IPRP)." Furthermore, the characteristics of IPRP were systematically elaborated from the perspectives of the ecological civilization thought, the policy management, and the key scientific issues. Also, the current achievements were summarized in the fields of national ecological space management, biodiversity conservation, and ecological protection and restoration. Existing challenges in management policy, scientific issues, and engineering practices were highlighted. Future perspectives include ecological space control, nature-based Solutions, biodiversity big data platform, modern techniques, and value realization mechanisms of ecological products.

Nonredundancy in the dispersal network of a generalist tropical forest tree.

Plant species with generalized dispersal mutualisms are considered to be robust to local frugivore extinctions because of redundancy between dispersal agents. However, real redundancy can only occur if frugivores have similar foraging and ranging patterns and if fruit is a limiting resource. We evaluated the quantitative and qualitative contributions of seed dispersers for an endochorus mast-fruiting species, Prunus javanica (Rosaceae) in Khao Yai National Park, Thailand, to evaluate the potential redundancy of dispersers. Data were collected from tree watches, seed/fruit traps, and seed transects under and away from fruiting trees, feeding and seed deposition by gibbons (Hylobates lar), and evaluations of seed and first-year seedling survival. We identified three clusters of dispersers within the network. Most (>80%) frugivore species observed were small birds and squirrels that were not functional dispersers, dropping most seeds under or very near the tree crown, where seedling survival was ultimately nil. Monkeys (Macaca leonina) were low-quality, short-range dispersers, but they dispersed large numbers of seeds and were responsible for 67% of surviving first-year seedlings. Gibbons and Oriental Pied Hornbills (Anthracoceros albirostris) handled few fruits, but they provided the highest quality service by carrying most seeds away from the canopy to medium and long distances, respectively. Although there was overlap in the deposition patterns of the functional dispersers, they displayed complementary, rather than redundant, roles in seed dispersal. Satiation of all functional dispersers further limited their capacity to "replace" one another. Redundancy must be evaluated at the community level because each type of disperser may shift to different species in the non-masting years of P. javanica. Our results underscore the need for research on broader spatial and temporal scales, which combines studies of dispersal and plant recruitment, to better understand mechanisms that maintain network stability.

Intraspecific differences in seed dispersal caused by differences in social rank and mediated by food availability.

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.

Crypticity in Biological Invasions.

Ecological effects of alien species can be dramatic, but management and prevention of negative impacts are often hindered by crypticity of the species or their ecological functions. Ecological functions can change dramatically over time, or manifest after long periods of an innocuous presence. Such cryptic processes may lead to an underestimation of long-term impacts and constrain management effectiveness. Here, we present a conceptual framework of crypticity in biological invasions. We identify the underlying mechanisms, provide evidence of their importance, and illustrate this phenomenon with case studies. This framework has potential to improve the recognition of the full risks and impacts of invasive species.

Different megafauna vary in their seed dispersal effectiveness of the megafaunal fruit Platymitra macrocarpa (Annonaceae).

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.

Elucidating the diet of the island flying fox (Pteropus hypomelanus) in Peninsular Malaysia through Illumina Next-Generation Sequencing.

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.

Pollination by the locally endangered island flying fox (Pteropus hypomelanus) enhances fruit production of the economically important durian (Durio zibethinus).

Fruit bats provide valuable pollination services to humans through a unique coevolutionary relationship with chiropterophilous plants. However, chiropterophily in the Old World and the pollination roles of large bats, such as flying foxes (Pteropus spp., Acerodon spp., Desmalopex spp.), are still poorly understood and require further elucidation. Efforts to protect these bats have been hampered by a lack of basic quantitative information on their role as ecosystem service providers. Here, we investigate the role of the locally endangered island flying fox Pteropus hypomelanus in the pollination ecology of durian (Durio zibethinus), an economically important crop in Southeast Asia. On Tioman Island, Peninsular Malaysia, we deployed 19 stations of paired infrared camera and video traps across varying heights at four individual flowering trees in a durian orchard. We detected at least nine species of animal visitors, but only bats had mutualistic interactions with durian flowers. There was a clear vertical stratification in the feeding niches of flying foxes and nectar bats, with flying foxes feeding at greater heights in the trees. Flying foxes had a positive effect on mature fruit set and therefore serve as important pollinators for durian trees. As such, semi-wild durian trees-particularly tall ones-may be dependent on flying foxes for enhancing reproductive success. Our study is the first to quantify the role of flying foxes in durian pollination, demonstrating that these giant fruit bats may have far more important ecological, evolutionary, and economic roles than previously thought. This has important implications and can aid efforts to promote flying fox conservation, especially in Southeast Asian countries.

Flying foxes cease to function as seed dispersers long before they become rare.

Rare species play limited ecological roles, but particular behavioral traits may predispose species to become functionally extinct before becoming rare. Flying foxes (Pteropodid fruit bats) are important dispersers of large seeds, but their effectiveness is hypothesized to depend on high population density that induces aggressive interactions. In a Pacific archipelago, we quantified the proportion of seeds that flying foxes dispersed beyond the fruiting canopy, across a range of sites that differed in flying fox abundance. We found the relationship between ecological function (seed dispersal) and flying fox abundance was nonlinear and consistent with the hypothesis. For most trees in sites below a threshold abundance of flying foxes, flying foxes dispersed < 1% of the seeds they handled. Above the threshold, dispersal away from trees increased to 58% as animal abundance approximately doubled. Hence, flying foxes may cease to be effective seed dispersers long before becoming rare. As many species' populations decline worldwide, identifying those with threshold relationships is an important precursor to preservation of ecologically effective densities.

Cryptic function loss in animal populations.

The essential functional roles performed by animal species are lost when they become locally extinct, and ecosystems are critically threatened by this decline in functional diversity. Theory that links function, diversity, and ecosystem stability exists but fails to assess function loss that occurs in species with persistent populations. The entire functional role of a species, or a critical component of it, can be lost following large population declines (functional extinction), following population increase, or after behavioural adaptations to changes in the population, community, habitat, or climate. Here, we provide a framework that identifies the scenarios under which 'cryptic' function loss can occur in persistent populations. Cryptic function loss is potentially widespread and critically threatens ecosystem stability across the globe.

Low redundancy in seed dispersal within an island frugivore community.

The low species diversity that often characterizes island ecosystems could result in low functional redundancy within communities. Flying foxes (large fruit bats) are important seed dispersers of large-seeded species, but their redundancy within island communities has never been explicitly tested. In a Pacific archipelago, we found that flying foxes were the sole effective disperser of 57 % of the plant species whose fruits they consume. They were essential for the dispersal of these species either because they handled >90 % of consumed fruit, or were the only animal depositing seeds away from the parent canopy, or both. Flying foxes were especially important for larger-seeded fruit (>13 mm wide), with 76 % of consumed species dependent on them for dispersal, compared with 31 % of small-seeded species. As flying foxes decrease in abundance, they cease to function as dispersers long before they become rare. We compared the seed dispersal effectiveness (measured as the proportion of diaspores dispersed beyond parent crowns) of all frugivores for four plant species in sites where flying foxes were, and were not, functionally extinct. At both low and high abundance, flying foxes consumed most available fruit of these species, but the proportion of handled diaspores dispersed away from parent crowns (quality) was significantly reduced at low abundance. Since alternative consumers (birds, rodents and land crabs) were unable to compensate as dispersers when flying foxes were functionally extinct, we conclude that there is almost no redundancy in the seed dispersal function of flying foxes in this island system, and potentially on other islands where they occur. Given that oceanic island communities are often simpler than continental communities, evaluating the extent of redundancy across different ecological functions on islands is extremely important.

Primates, Provisioning and Plants: Impacts of Human Cultural Behaviours on Primate Ecological Functions.

Human provisioning of wildlife with food is a widespread global practice that occurs in multiple socio-cultural circumstances. Provisioning may indirectly alter ecosystem functioning through changes in the eco-ethology of animals, but few studies have quantified this aspect. Provisioning of primates by humans is known to impact their activity budgets, diets and ranging patterns. Primates are also keystone species in tropical forests through their role as seed dispersers; yet there is no information on how provisioning might affect primate ecological functions. The rhesus macaque is a major human-commensal species but is also an important seed disperser in the wild. In this study, we investigated the potential impacts of provisioning on the role of rhesus macaques as seed dispersers in the Buxa Tiger Reserve, India. We studied a troop of macaques which were provisioned for a part of the year and were dependent on natural resources for the rest. We observed feeding behaviour, seed handling techniques and ranging patterns of the macaques and monitored availability of wild fruits. Irrespective of fruit availability, frugivory and seed dispersal activities decreased when the macaques were provisioned. Provisioned macaques also had shortened daily ranges implying shorter dispersal distances. Finally, during provisioning periods, seeds were deposited on tarmac roads that were unconducive for germination. Provisioning promotes human-primate conflict, as commensal primates are often involved in aggressive encounters with humans over resources, leading to negative consequences for both parties involved. Preventing or curbing provisioning is not an easy task as feeding wild animals is a socio-cultural tradition across much of South and South-East Asia, including India. We recommend the initiation of literacy programmes that educate lay citizens about the ill-effects of provisioning and strongly caution them against the practice.

The capuchin, the howler, and the Caatinga: seed dispersal by monkeys in a threatened Brazilian forest.

Regeneration of the Brazilian Caatinga forest may be restricted by the naturally low diversity and density of fruit-eating animals, which has been aggravated by local faunal extinction induced by human activities. We made a preliminary evaluation of the potential seed-dispersal role of capuchin (Cebus apella libidinosus) and howler monkeys (Alouatta caraya) in Serra da Capivara National Park. The monkeys dispersed at least 26 species. Alouatta dispersed larger seeds than Cebus, and the two species apparently dispersed seeds in different local habitats. Seed dispersal by monkeys potentially makes a significant contribution to Caatinga regeneration.