CamTrapAsia: A dataset of tropical forest vertebrate communities from 239 camera trapping studies.

Information on tropical Asian vertebrates has traditionally been sparse, particularly when it comes to cryptic species inhabiting the dense forests of the region. Vertebrate populations are declining globally due to land-use change and hunting, the latter frequently referred as "defaunation." This is especially true in tropical Asia where there is extensive land-use change and high human densities. Robust monitoring requires that large volumes of vertebrate population data be made available for use by the scientific and applied communities. Camera traps have emerged as an effective, non-invasive, widespread, and common approach to surveying vertebrates in their natural habitats. However, camera-derived datasets remain scattered across a wide array of sources, including published scientific literature, gray literature, and unpublished works, making it challenging for researchers to harness the full potential of cameras for ecology, conservation, and management. In response, we collated and standardized observations from 239 camera trap studies conducted in tropical Asia. There were 278,260 independent records of 371 distinct species, comprising 232 mammals, 132 birds, and seven reptiles. The total trapping effort accumulated in this data paper consisted of 876,606 trap nights, distributed among Indonesia, Singapore, Malaysia, Bhutan, Thailand, Myanmar, Cambodia, Laos, Vietnam, Nepal, and far eastern India. The relatively standardized deployment methods in the region provide a consistent, reliable, and rich count data set relative to other large-scale pressence-only data sets, such as the Global Biodiversity Information Facility (GBIF) or citizen science repositories (e.g., iNaturalist), and is thus most similar to eBird. To facilitate the use of these data, we also provide mammalian species trait information and 13 environmental covariates calculated at three spatial scales around the camera survey centroids (within 10-, 20-, and 30-km buffers). We will update the dataset to include broader coverage of temperate Asia and add newer surveys and covariates as they become available. This dataset unlocks immense opportunities for single-species ecological or conservation studies as well as applied ecology, community ecology, and macroecology investigations. The data are fully available to the public for utilization and research. Please cite this data paper when utilizing the data.

Novel insight into the genetic diversity of strongylid nematodes infecting South-East and East Asian primates.

With many non-human primates (NHPs) showing continued population decline, there is an ongoing need to better understand their ecology and conservation threats. One such threat is the risk of disease, with various bacterial, viral and parasitic infections previously reported to have damaging consequences for NHP hosts. Strongylid nematodes are one of the most commonly reported parasitic infections in NHPs. Current knowledge of NHP strongylid infections is restricted by their typical occurrence as mixed infections of multiple genera, which are indistinguishable through traditional microscopic approaches. Here, modern metagenomics approaches were applied for insight into the genetic diversity of strongylid infections in South-East and East Asian NHPs. We hypothesized that strongylid nematodes occur in mixed communities of multiple taxa, dominated by Oesophagostomum, matching previous findings using single-specimen genetics. Utilizing the Illumina MiSeq platform, ITS-2 strongylid metabarcoding was applied to 90 samples from various wild NHPs occurring in Malaysian Borneo and Japan. A clear dominance of Oesophagostomum aculeatum was found, with almost all sequences assigned to this species. This study suggests that strongylid communities of Asian NHPs may be less species-rich than those in African NHPs, where multi-genera communities are reported. Such knowledge contributes baseline data, assisting with ongoing monitoring of health threats to NHPs.

The fast-food effect: costs of being a generalist in a human-dominated landscape.

Agricultural expansion in Southeast Asia has converted most natural landscapes into mosaics of forest interspersed with plantations, dominated by the presence of generalist species that benefit from resource predictability. Dietary shifts, however, can result in metabolic alterations and the exposure of new parasites that can impact animal fitness and population survival. Our study focuses on the Asian water monitor lizard (Varanus salvator), one of the largest predators in the Asian wetlands, as a model species to understand the health consequences of living in a human-dominated landscape in Sabah, Malaysian Borneo. We evaluated the effects of dietary diversity on the metabolism of monitor lizards and the impact on the composition of their parasite communities in an oil palm-dominated landscape. Our results showed that (1) rodent-dominated diets were associated with high levels of lipids, proteins and electrolytes, akin to a fast-food-based diet of little representativeness of the full nutritional requirements, but highly available, and (2) lizards feeding on diverse diets hosted more diverse parasite communities, however, at overall lower parasite prevalence. Furthermore, we observed that the effect of diet on lipid concentration differed depending on the size of individual home ranges, suggesting that sedentarism plays an important role in the accumulation of cholesterol and triglycerides. Parasite communities were also affected by a homogeneous dietary behaviour, as well as by habitat type. Dietary diversity had a negative effect on both parasite richness and prevalence in plantations, but not in forested areas. Our study indicates that human-dominated landscapes can pose a negative effect on generalist species and hints to the unforeseen health consequences for more vulnerable taxa using the same landscapes. Thus, it highlights the potential role of such a widely distributed generalist as model species to monitor physiological effects in the ecosystem in an oil palm-dominated landscape.

Isolation of Bacteria from Freeze-Dried Samples and the Functional Characterization of Species-Specific Lactic Acid Bacteria with a Comparison of Wild and Captive Proboscis Monkeys.

Previously, we isolated a novel lactic acid bacteria species (Lactobacillus nasalidis) from the fresh forestomach contents of a captive proboscis monkey (Nasalis larvatus) in a Japanese zoo. In this study, we isolated two strains of L. nasalidis from the freeze-dried forestomach contents of a wild proboscis monkey inhabiting a riverine forest in Malaysia. The samples had been stored for more than six years. Phenotypic analysis showed that strains isolated from the wild individual had more diverse sugar utilization and lower salt tolerance than strains previously isolated from the captive counterpart. These phenotypic differences are most likely induced by feeding conditions; wild individuals consume a wide variety of natural food, unlike their zoo-raised counterparts that consume formula feed with sodium sufficiency. Since 16s rRNA sequences of L. nasalidis were detected in the previously created 16S rRNA libraries of wild, provisioned, and captive proboscis monkeys in Malaysia and Japan, L. nasalidis may be an essential bacterium of the foregut microbial community of the proboscis monkey. The currently established method for the isolation of gut bacteria from freeze-dried samples under storage will be applicable to many already-stored precious samples.

Modifying the diets of captive proboscis monkeys in a temperate zoo to reduce weight loss and renal disease.

In animal husbandry, diets should help in maintaining a healthy body condition, support reproduction, and promote species-specific longevity. It is recommended to feed folivorous primates kept in zoos a high-fiber diet, i.e., leaves, although satisfying such a requirement is challenging in temperate regions because it is difficult to obtain fresh leaves, especially in autumn and winter. As equally important for their appropriate treatment, it is valuable to provide details of clinical reports of medical problems and pathological findings, although such clinical reports are rather limited. Therefore, in foregut-fermenting proboscis monkeys (Nasalis larvatus), we (1) described the individual clinical reports of renal disease and weight loss at the Yokohama Zoological Gardens in Japan, (2) determined the nutritional profile of the diets supplied to these animals because other potential triggers for their renal disease and weight loss could be excluded, (3) modified the diet regimen to minimize weight loss and the development of hypercalcemia and hypophosphatemia, and (4) assessed the effects of such dietary modification by comparing the body weight and the Ca and P concentrations and the Ca/P ratios in the blood before and after diet modification with a comparison of these measurements between zoo and free-ranging individuals. Based on the nutritional profile of the diets, we concluded that the reported cases of renal failure might be caused by consumption of leaves with a Ca/P ratio far above the appropriate level in autumn and winter. Additionally, the dietary modification of minerals and metabolizable energy achieved certain beneficial effects on zoo-kept proboscis monkeys.

External environmental conditions impact nocturnal activity levels in proboscis monkeys (Nasalis larvatus) living in Sabah, Malaysia.

Recently, several diurnal nonhuman anthropoids have been identified displaying varying degrees of nocturnal activity, which can be influenced by activity "masking effects"-external events or conditions that suppress or trigger activity, temporarily altering normal activity patterns. Environmental masking characteristics include nocturnal temperature, rainfall, cloud cover, and moon brightness. Similarly, other ecological characteristics, including proximity to humans and predators and daytime activity, may also trigger or suppress nocturnal activity. Understanding the effects of external conditions on activity patterns is pertinent to effective species conservation. We investigated the presence of nocturnal activity and the influence of masking effects on the level of nocturnal activity displayed by wild proboscis monkeys (Nasalis larvatus) in Sabah, Malaysian Borneo. Dual-axis accelerometers were attached by collar to six male proboscis monkeys from different one-male, multi-female groups to record activity continuously (165-401 days each). We measured the monkeys' nocturnal and diurnal activity levels and investigated the effects of seven potential masking effects. Nocturnal activity was much lower than diurnal activity. Still, proboscis monkeys did display varying levels of nocturnal activity. Generalized linear mixed models identified higher nocturnal activity in the study individuals during nights with cooler temperatures, higher rainfall, and after higher diurnal activity. These three masking effects affected nocturnal activity levels during the observation period that informed our model, although they did not predict nocturnal activity outside of this period. While the generalizability of these results remains uncertain, this study highlights the utility of accelerometers in identifying activity patterns and masking effects that create variability in these patterns.

Serological evidence of exposure of Bornean wild carnivores to feline-related viruses at the domestic animal-wildlife interface.

We conducted an exploratory serological survey to evaluate the exposure of Bornean wild carnivores to several viruses common to domestic felids, at interface areas between protected forest and industrial agriculture in the Kinabatangan floodplain (Sabah, Malaysia). Blood samples, collected from wild carnivores (n = 21) and domestic cats (n = 27), were tested for antibodies against feline coronavirus (FCoV), feline panleukopenia virus (FPLV), feline herpesvirus (FHV) and feline calicivirus (FCV), using commercial enzyme-linked immunosorbent assay (ELISA) test kits. Anti-FCoV antibodies were detected in most species, including one flat-headed cat (Prionailurus planiceps, [1/2]), leopard cats (Prionailurus bengalensis, [2/5]), Malay civets (Viverra tangalunga, [2/11]) and domestic cats (Felis catus, [2/27]). Anti-FCV antibodies were present in all domestic cats and one flat-headed cat, while anti-FPLV antibodies were identified in Sunda clouded leopards (Neofelis diardi, [2/2]), domestic cats [12/27] and Malay civets [2/11]. Anti-FHV antibodies were only detected in domestic cats [2/27]. Our findings indicate pathogen transmission risk between domestic and wild carnivore populations at the domestic animal-wildlife interface, emphasizing the concern for wildlife conservation for several endangered wild carnivores living in the area. Special consideration should be given to species that benefit from their association with humans and have the potential to carry pathogens between forest and plantations (e.g., Malay civets and leopard cats). Risk reduction strategies should be incorporated and supported as part of conservation actions in human-dominated landscapes.

Effectiveness of 20 years of conservation investments in protecting orangutans.

Conservation strategies are rarely systematically evaluated, which reduces transparency, hinders the cost-effective deployment of resources, and hides what works best in different contexts. Using data on the iconic and critically endangered orangutan (Pongo spp.), we developed a novel spatiotemporal framework for evaluating conservation investments. We show that around USD 1 billion was invested between 2000 and 2019 into orangutan conservation by governments, nongovernmental organizations, companies, and communities. Broken down by allocation to different conservation strategies, we find that habitat protection, patrolling, and public outreach had the greatest return on investment for maintaining orangutan populations. Given the variability in threats, land-use opportunity costs, and baseline remunerations in different regions, there were differential benefits per dollar invested across conservation activities and regions. We show that although challenging from a data and analysis perspective, it is possible to fully understand the relationships between conservation investments and outcomes and the external factors that influence these outcomes. Such analyses can provide improved guidance toward a more effective biodiversity conservation. Insights into the spatiotemporal interplays between the costs and benefits driving effectiveness can inform decisions about the most suitable orangutan conservation strategies for halting population declines. Although our study focuses on the three extant orangutan species of Sumatra and Borneo, our findings have broad application for evidence-based conservation science and practice worldwide.

The effect of oil palm-dominated landscapes on the home range and distribution of a generalist species, the Asian water monitor.

The Asian water monitor lizard, Varanus salvator, is one of the largest predators in Southeast Asia which persists in human-dominated landscapes and, as such, is a suitable model to understand the behavioral plasticity of generalists in anthropogenic landscapes. We used Local Convex Hull with adaptive algorithm to estimate the home range size of 14 GPS-tagged individuals, followed by a MAXENT approach and community prey composition to understand the habitat preferences within the landscape. We estimated larger home ranges in forest than in oil palm plantations, as well as a larger diversity and abundance of mammals. Core home ranges were always linked to water bodies. However, the use of underproductive oil palm, freshwater swamp forest, and degraded forest by monitor lizards were higher than other kind of vegetation. This suitable habitat is proportionally larger in forest (73.7%) than in oil palm plantations (39.6%). Generalized estimation equation models showed that, while full home range size was negatively associated with the abundance of mammals, core areas depicted a positive association with mammal abundance, as well as with the proportion of suitable habitat within the home range. Besides having smaller home ranges in oil palm plantations, our findings suggest that limited suitable habitat availability forces the Asian water monitor lizard's population to establish only one or very few core areas. Contrastingly, under the protection of forest, they have more core areas, widely dispersed within larger home ranges. We conclude that regardless the plasticity of the species, human-dominated landscapes are altering natural patterns of home range establishment in the monitor lizard's population, creating a potential ecological trap where conditions may not remain favorable for them in the long run. A deeper understanding of the ecological implications on the species and the prey community is advisable.

Whole genome analysis of clouded leopard species reveals an ancient divergence and distinct demographic histories.

Similar to other apex predator species, populations of mainland (Neofelis nebulosa) and Sunda (Neofelis diardi) clouded leopards are declining. Understanding their patterns of genetic variation can provide critical insights on past genetic erosion and a baseline for understanding their long-term conservation needs. As a step toward this goal, we present draft genome assemblies for the two clouded leopard species to quantify their phylogenetic divergence, genome-wide diversity, and historical population trends. We estimate that the two species diverged 5.1 Mya, much earlier than previous estimates of 1.41 Mya and 2.86 Mya, suggesting they separated when Sundaland was becoming increasingly isolated from mainland Southeast Asia. The Sunda clouded leopard displays a distinct and reduced effective population size trajectory, consistent with a lower genome-wide heterozygosity and SNP density, relative to the mainland clouded leopard. Our results provide new insights into the evolutionary history and genetic health of this unique lineage of felids.

The price of persistence: Assessing the drivers and health implications of metal levels in indicator carnivores inhabiting an agriculturally fragmented landscape.

Patterns and practices of agricultural expansion threaten the persistence of global biodiversity. Wildlife species surviving large-scale land use changes can be exposed to a suite of contaminants that may deleteriously impact their health. There is a paucity of data concerning the ecotoxicological impacts associated with the global palm oil (Elaeis guineensis) industry. We sampled wild Malay civets (Viverra tangalunga) across a patchwork landscape degraded by oil palm agriculture in Sabah, Malaysian Borneo. Using a non-lethal methodology, we quantified the levels of 13 essential and non-essential metals within the hair of this adaptable small carnivore. We robustly assessed the biological and environmental drivers of intrapopulation variation in measured levels. Metal concentrations were associated with civet age, weight, proximity to a tributary, and access to oxbow lakes. In a targeted case study, the hair metal profiles of 16 GPS-collared male civets with differing space use patterns were contrasted. Civets that entered oil palm plantations expressed elevated aluminium, cadmium, and lead, and lower mercury hair concentrations compared to civets that remained exclusively within the forest. Finally, we paired hair metal concentrations with 34 blood-based health markers to evaluate the possible sub-lethal physiological effects associated with varied hair metal levels. Our multi-facetted approach establishes these adaptable carnivores as indicator species within an extensively altered ecosystem, and provides critical and timely evidence for future studies.

The critical role of natural forest as refugium for generalist species in oil palm-dominated landscapes.

In Borneo, oil palm plantations have replaced much of natural resources, where generalist species tend to be the principal beneficiaries, due to the abundant food provided by oil palm plantations. Here, we analyse the distribution of the Asian water monitor lizard (Varanus salvator) population within an oil palm-dominated landscape in the Kinabatangan floodplain, Malaysian Borneo. By using mark-recapture methods we estimated its population size, survival, and growth in forest and plantation habitats. We compared body measurements (i.e. body weight and body length) of individuals living in forest and oil palm habitats as proxy for the population's health status, and used general least squares estimation models to evaluate its response to highly fragmented landscapes in the absence of intensive hunting pressures. Contrary to previous studies, the abundance of lizards was higher in the forest than in oil palm plantations. Recruitment rates were also higher in the forest, suggesting that these areas may function as a source of new individuals into the landscape. While there were no morphometric differences among plantation sites, we found significant differences among forested areas, where larger lizards were found inhabiting forest adjacent to oil palm plantations. Although abundant in food resources, the limited availability of refugia in oil palm plantations may intensify intra-specific encounters and competition, altering the body size distribution in plantation populations, contrary to what happens in the forest. We conclude that large patches of forest, around and within oil palm plantations, are essential for the dynamics of the monitor lizard population in the Kinabatangan floodplain, as well as a potential source of individuals to the landscape. We recommend assessing this effect in other generalist species, as well as the impact on the prey communities, especially to reinforce the establishment of buffer zones and corridors as a conservation strategy within plantations.

Genomic insights into the conservation status of the world's last remaining Sumatran rhinoceros populations.

Small populations are often exposed to high inbreeding and mutational load that can increase the risk of extinction. The Sumatran rhinoceros was widespread in Southeast Asia, but is now restricted to small and isolated populations on Sumatra and Borneo, and most likely extinct on the Malay Peninsula. Here, we analyse 5 historical and 16 modern genomes from these populations to investigate the genomic consequences of the recent decline, such as increased inbreeding and mutational load. We find that the Malay Peninsula population experienced increased inbreeding shortly before extirpation, which possibly was accompanied by purging. The populations on Sumatra and Borneo instead show low inbreeding, but high mutational load. The currently small population sizes may thus in the near future lead to inbreeding depression. Moreover, we find little evidence for differences in local adaptation among populations, suggesting that future inbreeding depression could potentially be mitigated by assisted gene flow among populations.

Parasite community structure in sympatric Bornean primates.

Parasites are important components of ecosystems, influencing trophic networks, competitive interactions and biodiversity patterns. Nonetheless, we are not nearly close to disentangling their complex roles in natural systems. Southeast Asia falls within global areas targeted as most likely to source parasites with zoonotic potential, where high rates of land conversion and fragmentation have altered the circulation of wildlife species and their parasites, potentially resulting in altered host-parasite systems. Although the overall biodiversity in the region predicts equally high, or even higher, parasite diversity, we know surprisingly little about wild primate parasites, even though this constitutes the first step towards a more comprehensive understanding of parasite transmission processes. Here, we characterise the gastrointestinal helminth parasite assemblages of a community of Bornean primates living along the Kinabatangan floodplain in Sabah (Malaysian Borneo), including two species endemic to the island. Through parasitological analyses, and by using several measures of parasite infection as proxies for parasite diversity and distribution, we show that (i) most parasite taxonomic groups are not limited to a single host, suggesting a greater flexibility for habitat disturbance, (ii) parasite infracommunities of nocturnal primates differ from their diurnal counterparts, reflecting both phylogenetic and ecological constraints, and (iii) soil-transmitted helminths such as whipworm, threadworm and nodule worm are widespread across the primate community. This study also provides new parasite records for southern pig-tailed macaques (Macaca nemestrina), silvered langurs (Trachypithecus cristatus) and Western tarsiers (Cephalopachus bancanus) in the wild, while adding to the limited records for the other primate species in the community. Given the information gap regarding primate-parasite associations in the region, the information presented here should prove relevant for future studies of parasite biodiversity and infectious disease ecology in Asia and elsewhere.

Large male proboscis monkeys have larger noses but smaller canines.

The uniquely enlarged noses of male proboscis monkeys are prominent adornments, and a sexually selected male trait. A recent study showed significant correlations among nose, body, and testis sizes and clear associations between nose size and the number of females in a male's harem. However, to date, the analyses of other common male traits, i.e., canines, are lacking. Whereas male nose size had a positive correlation with body size, we unexpectedly found a negative correlation between body and canine sizes. We explain this by an interaction between sexual and natural selection. Larger noses in males may interfere with the use of canines, thereby reducing their effectiveness as weapons. Additionally, longer canines are opposed by natural selection because the larger gape it imposes upon its bearer reduces foraging efficiency, particularly in folivores. This unique case of decoupling of body and canine size reveals that large canines carry an ecological cost.

Pre-extinction Demographic Stability and Genomic Signatures of Adaptation in the Woolly Rhinoceros.

Ancient DNA has significantly improved our understanding of the evolution and population history of extinct megafauna. However, few studies have used complete ancient genomes to examine species responses to climate change prior to extinction. The woolly rhinoceros (Coelodonta antiquitatis) was a cold-adapted megaherbivore widely distributed across northern Eurasia during the Late Pleistocene and became extinct approximately 14 thousand years before present (ka BP). While humans and climate change have been proposed as potential causes of extinction [1-3], knowledge is limited on how the woolly rhinoceros was impacted by human arrival and climatic fluctuations [2]. Here, we use one complete nuclear genome and 14 mitogenomes to investigate the demographic history of woolly rhinoceros leading up to its extinction. Unlike other northern megafauna, the effective population size of woolly rhinoceros likely increased at 29.7 ka BP and subsequently remained stable until close to the species' extinction. Analysis of the nuclear genome from a ∼18.5-ka-old specimen did not indicate any increased inbreeding or reduced genetic diversity, suggesting that the population size remained steady for more than 13 ka following the arrival of humans [4]. The population contraction leading to extinction of the woolly rhinoceros may have thus been sudden and mostly driven by rapid warming in the Bølling-Allerød interstadial. Furthermore, we identify woolly rhinoceros-specific adaptations to arctic climate, similar to those of the woolly mammoth. This study highlights how species respond differently to climatic fluctuations and further illustrates the potential of palaeogenomics to study the evolutionary history of extinct species.

Dispersal and genetic structure in a tropical small mammal, the Bornean tree shrew (Tupaia longipes), in a fragmented landscape along the Kinabatangan River, Sabah, Malaysia.

BACKGROUND: Constraints in migratory capabilities, such as the disruption of gene flow and genetic connectivity caused by habitat fragmentation, are known to affect genetic diversity and the long-term persistence of populations. Although negative population trends due to ongoing forest loss are widespread, the consequence of habitat fragmentation on genetic diversity, gene flow and genetic structure has rarely been investigated in Bornean small mammals. To fill this gap in knowledge, we used nuclear and mitochondrial DNA markers to assess genetic diversity, gene flow and the genetic structure in the Bornean tree shrew, Tupaia longipes, that inhabits forest fragments of the Lower Kinabatangan Wildlife Sanctuary, Sabah. Furthermore, we used these markers to assess dispersal regimes in male and female T. longipes. RESULTS: In addition to the Kinabatangan River, a known barrier for dispersal in tree shrews, the heterogeneous landscape along the riverbanks affected the genetic structure in this species. Specifically, while in larger connected forest fragments along the northern riverbank genetic connectivity was relatively undisturbed, patterns of genetic differentiation and the distribution of mitochondrial haplotypes in a local scale indicated reduced migration on the strongly fragmented southern riverside. Especially, oil palm plantations seem to negatively affect dispersal in T. longipes. Clear sex-biased dispersal was not detected based on relatedness, assignment tests, and haplotype diversity. CONCLUSION: This study revealed the importance of landscape connectivity to maintain migration and gene flow between fragmented populations, and to ensure the long-term persistence of species in anthropogenically disturbed landscapes.

First description of male worms of Enterobius (Colobenterobius) serratus (Nematoda: Oxyuridae), the pinworm parasite of proboscis monkeys.

Males of Enterobius (Colobenterobius) serratus Hasegawa et al., 2003 (Nematoda: Oxyuridae) are described for the first time based on six individuals collected from the feces of proboscis monkeys, Nasalis larvatus, in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysian Borneo. The males show identical cephalic morphology to females, being readily distinguishable from their congeners by the serrated inner margins of the lips. The bicolored esophageal corpus, long thin spicule and developed spicular pouch with paired muscular bands are also remarkable characteristics, presumably shared by other Asian members of the subgenus.