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Primate ecotourism is a fast-growing tourism sector that may have a negative effect on wildlife. In riparian areas, tourists can conveniently reach primates via motor boats, but no study has directly examined whether such boats cause stress in primates. Our goal was to test whether the approach of a motor boat induces stress-related and other behaviors in proboscis monkeys (Nasalis larvatus), an Endangered species. We studied six one-male, multifemale groups living in a remote riparian area in Sabah, Malaysia, and conducted an experiment by approaching the monkeys in a motor boat by using three conditions with different speeds and travel distances (fast-close, slow-close, and slow-far conditions; 7-8 subjects per condition). For each condition, we compared stress-related behaviors before the boat approach with after the boat started approaching. Feeding, allogrooming and aggression were similarly examined, respectively. We also observed the monkeys’ behaviors at other times to examine age-sex classes differences in vigilance, social proximity, allogrooming, aggression and play (87 subjects). In the experiment, subjects displayed stress-related behaviors for longer in the fast-close and slow-close conditions once the boat started approaching than before the boat approach. The subjects also reduced feeding in the fast-close condition after the boat started approaching. In our observational study, males were more vigilant than females—a behavior that is likely to relate to male-male competition and group protection. This study provides evidence that even a single motor boat moving slowly, with humans behaving calmly, may negatively affect primate behavior and induce stress—an impact that is likely to be larger with tourist boats. Our study also shows that using conditions comparable to the slow-far condition (speed of 3.6 km/hr; no closer than 60 m), where no impact was observed, may help with to develop guidelines for primate tourism in riparian areas. Future research that examines the impact of boats on other primates is needed.

Vocal intervention is a triadic social interaction, where a third party responds vocally to a conflict between group members, minimizing the costs of aggression in response to the intervention. Because there is little information on vocal third-party intervention in nonhuman mammals, we investigated whether adult male proboscis monkeys use the bray vocalization as a vocal third-party intervention signal to intervene in intragroup conflicts. First, we audio-recorded 1,811 vocalizations from 17 free-ranging proboscis monkey groups in the Lower Kinabatangan Wildlife Sanctuary, analyzing 378 vocal responses of the adult male to agonistic vocal exchanges (shrieks) of group members. Second, we video- and audio-recorded five habituated groups in the Labuk Bay Proboscis Monkey Sanctuary investigating the context of these vocalizations and the conflict dyads evoking vocal support. We found that adult males of one-male/multifemale groups mainly uttered bray vocalizations, whereas females, immatures, and infants uttered shrieks in intragroup conflicts or in response to other animal species. The adult male uttered significantly more often brays after agonistic shrieks than expected based on the overall occurrence of brays. Brays ended 65% of agonistic conflicts, which were accompanied by vocalizations of the conflict partners and occurred more often after conflicts between females than between offspring. This suggests that the bray functions as a vocal third-party intervention signal for intragroup conflict resolution. We suggest that living in the high canopies of the tropical rainforest might restrict direct access to conflict partners and prevent physical intervention, favoring the evolution of the bray as a third-party vocal intervention signal.

Strongyles are commonly reported parasites in studies of primate parasite biodiversity. Among them, nodule worm species are often overlooked as a serious concern despite having been observed to cause serious disease in nonhuman primates and humans. In this study, we investigated whether strongyles found in Bornean primates are the nodule worm Oesophagostomum spp., and to what extent these parasites are shared among members of the community. To test this, we propose two hypotheses that use the parasite genetic structure to infer transmission processes within the community. In the first scenario, the absence of parasite genetic substructuring would reflect high levels of parasite transmission among primate hosts, as primates’ home ranges overlap in the study area. In the second scenario, the presence of parasite substructuring would suggest cryptic diversity within the parasite genus and the existence of phylogenetic barriers to cross‐species transmission. By using molecular markers, we identify strongyles infecting this primate community as O. aculeatum, the only species of nodule worm currently known to infect Asian nonhuman primates. Furthermore, the little to no genetic substructuring supports a scenario with no phylogenetic barriers to transmission and where host movements across the landscape would enable gene flow between host populations. This work shows that the parasite's high adaptability could act as a buffer against local parasite extinctions. Surveys targeting human populations living in close proximity to nonhuman primates could help clarify whether this species of nodule worm presents the zoonotic potential found in the other two species infecting African nonhuman primates.

The Javan rhinoceros (Rhinoceros sondaicus) is one of five extant rhinoceros species and among the rarest large mammals on Earth. Once widespread across Southeast Asia, it is now on the verge of extinction, with only one wild population remaining (estimated at ~60 individuals) on the island of Java, Indonesia. To assess the past genetic diversity of the female lineage of R. sondaicus, we generated mitochondrial genome data from eight museum specimens dating back to the 19th century, before the range of the Javan rhinoceros was dramatically reduced, for comparison against mitochondrial DNA (mtDNA) sequences of current R. sondaicus and other rhinoceros species. We succeeded in reconstructing five full and three partial ancient mitogenomes from the eight samples. We used BEAST to assess the phylogenetic relationship of the five extant rhinoceros species and the historical samples. The results show that the oldest and most diverse mtDNA lineages of R. sondaicus are found in historical samples, indicating a significant reduction of mtDNA diversity in modern Javan rhinos. We anticipate that the newly sequenced data will represent a useful resource for improving our understanding of evolutionary history of this species, should future studies be able to increase the available dataset. We hope this information may help in conservation efforts for this species.

Largely as a result of the expansion of oil palm Elaeis guineensis, forest fragmentation has occurred on a large scale in Borneo. There is much concern about how forest-dependent species, such as the Vulnerable sun bear Helarctos malayanus, can persist in this landscape. The absence of sufficient natural food in forest fragments could drive sun bears into oil palm plantations, where they risk coming into conflict with people. We interviewed oil palm plantation workers and farmers in the Lower Kinabatangan region of Sabah, Malaysian Borneo, to ascertain if sun bears were utilizing plantations, if they were causing damage to the crop, and how the bears were perceived by people. To obtain a comparative baseline we extended these questions to include other species as well. We found that bears were rarely encountered in plantations and were not considered to be destructive to the oil palm crop, although they were generally feared. Other species, such as macaques Macaca spp., bearded pigs Sus barbatus, and elephants Elephas maximus, had more destructive feeding habits. Sun bears could use this readily available food resource without being targeted for retribution, although incidental human-related mortality remains a risk. Although bears could gain some nutritional benefit from oil palm, plantations do not provide the diversity of food and cover available in a natural forest.

Changes in land use/cover are the main drivers of global biodiversity loss, and thus tools to evaluate effects of landscape change on biodiversity are crucial. In this study we integrated several methods from landscape ecology and landscape genetics into a GIS-based analytical framework, and evaluated the impacts of development and forest restoration scenarios on landscape connectivity, population dynamics and genetic diversity of Sunda clouded leopard in the Malaysian state of Sabah. We also investigated the separate and interactive effects of changing mortality risk and connectivity. Our study suggested that the current clouded leopard population size is larger (+26%) than the current carrying capacity of the landscape due to time lag effects and extinction debt. Additionally, we predicted that proposed developments in Sabah may decrease landscape connectivity by 23% and, when including the increased mortality risk associated with these developments, result in a 40–63% decrease in population size and substantial reduction in genetic diversity. These negative impacts could be mitigated only to a very limited degree through extensive and targeted forest restoration. Our results suggest that realignment of roads and railways based on resistance to movement, without including mortality risk, might be misleading and may in some cases lead to decrease in population size. We therefore recommend that efforts to optimally plan road and railway locations base the optimization on effects of development on population size, density and distribution rather than solely on population connectivity.

As large areas of forest are lost throughout the tropics, prime habitat of many species decline and become fragmented. The island of Borneo is a prime example, with accelerated clearing of forests primarily for oil palm expansion. Borneo is recognized as an important stronghold for the conservation of the sun bear (Helarctos malayanus), but it is unclear how habitat reduction and fragmentation is affecting this frugivore. We used camera traps and sign surveys to understand patterns of sun bear habitat use in a matrix of fragmented forests and extensive oil palm development, which has existed as such for > 15 years: the Lower Kinabatangan floodplain in Sabah, Malaysian Borneo. Within these small forest fragments, squeezed between a major river and oil palm plantations, bears exhibited selection for areas farther from human activity (plantations, river boat traffic, and buildings), and were rarely active during the day, demonstrating both spatial and temporal avoidance of potential human-related threats. They selected large trees to feed and rest, and also exploited adjacent plantations to feed on oil palm fruits. We conclude that even relatively small forest fragments (~ 2000 ha) within large agricultural landscapes can be important for sun bears. Our research highlights the remarkable adaptations this species has employed to persist in a drastically modified landscape.

Foregut fermentation is well known to occur in a wide range of mammalian species and in a single bird species. Yet, the foregut microbial community of free-ranging, foregut-fermenting monkeys, that is, colobines, has not been investigated so far. We analysed the foregut microbiomes in four free-ranging proboscis monkeys (Nasalis larvatus) from two different tropical habitats with varying plant diversity (mangrove and riverine forests), in an individual from a semi-free-ranging setting with supplemental feeding, and in an individual from captivity, using high-throughput sequencing based on 16S ribosomal RNA genes. We found a decrease in foregut microbial diversity from a diverse natural habitat (riverine forest) to a low diverse natural habitat (mangrove forest), to human-related environments. Of a total of 2700 bacterial operational taxonomic units (OTUs) detected in all environments, only 153 OTUs were shared across all individuals, suggesting that they were not influenced by diet or habitat. These OTUs were dominated by Firmicutes and Proteobacteria. The relative abundance of the habitat-specific microbial communities showed a wide range of differences among living environments, although such bacterial communities appeared to be dominated by Firmicutes and Bacteroidetes, suggesting that those phyla are key to understanding the adaptive strategy in proboscis monkeys living in different habitats.

Reducing the size of food particles is crucial for herbivores. Seasonal dietary changes are known to influence animals’ chewing efficiency. Proboscis monkeys (Nasalis larvatus) are foregut fermenters, with a high chewing efficiency allowing them to achieve very fine faecal particles. In this study, we investigated how proboscis monkeys’ chewing efficiency varies between wet and dry seasons, hypothesising differences possibly related to diet change. Faecal particle size analysis is an established approach to estimate chewing efficiency in mammalian herbivores. We analysed 113 proboscis monkey faecal samples collected in the Lower Kinabatangan Wildlife Sanctuary, between 2015 and 2017. By following standard sieve analysis protocols, we measured a mean particle size MPS0.025–8 of 0.45 ± 0.14 mm, and confirmed a previous result that proboscis monkeys have a very low faecal MPS. This study highlights a seasonal influence on proboscis monkeys’ chewing efficiency, with smaller MPS (better chewing efficiency) during the wet season. During that time of the year, individuals may potentially change their diet, as all faecal samples contained intact seeds. Whether the seasonal MPS difference in proboscis monkeys is smaller than in other colobines due to their “rumination” strategy remains to be investigated.

Despite the implications for the development of life-history traits, endocrine–immune trade-offs in apes are not well studied. This is due, in part, to difficulty in sampling wild primates, and lack of methods available for immune measures using samples collected noninvasively. Evidence for androgenmediated immune trade-offs in orangutans is virtually absent, and very little is known regarding their pattern of adrenal development and production of adrenal androgens. To remedy both of these deficiencies, sera were collected from orangutans (Pongo pygmaeus morio) (N¼ 38) at the Sepilok Orangutan Rehabilitation Centre, Sabah, Malaysia, during routine health screenings. Testosterone, dehydroepiandrosterone (DHEA), and dehydroepiandrosterone-sulfate (DHEA-S) were assayed, along with two measures of functional innate immunity. DHEA-S concentrations, but not DHEA, increased with age in this sample of 1–18 year old animals. DHEA concentrations were higher in animals with higher levels of serum bacteria killing ability, while DHEA-S and testosterone concentrations were higher in animals with reduced complement protein activity. Patterns of DHEA-S concentration in this sample are consistent with patterns of adrenarche observed in other apes. Results from this study suggest that in addition to testosterone, DHEA and DHEA-S may have potent effects on immunological activity in this species. Am. J. Primatol. 9999:1–9, 2015. © 2015 Wiley Periodicals, Inc.

Although parasitic organisms are found worldwide, the relative importance of host specificity and geographic isolation for parasite speciation has been explored in only a few systems. Here, we study Plasmodium parasites known to infect Asian nonhuman primates, a monophyletic group that includes the lineage leading to the human parasite Plasmodium vivax and several species used as laboratory models in malaria research. We analyze the available data together with new samples from three sympatric primate species from Borneo: The Bornean orangutan and the long-tailed and the pig-tailed macaques. We find several species of malaria parasites, including three putatively new species in this biodiversity hotspot. Among those newly discovered lineages, we report two sympatric parasites in orangutans. We find no differences in the sets of malaria species infecting each macaque species indicating that these species show no host specificity. Finally, phylogenetic analysis of these data suggests that the malaria parasites infecting Southeast Asian macaques and their relatives are speciating three to four times more rapidly than those with other mammalian hosts such as lemurs and African apes. We estimate that these events took place in approximately a 3-4-Ma period. Based on the genetic and phenotypic diversity of the macaque malarias, we hypothesize that the diversification of this group of parasites has been facilitated by the diversity, geographic distributions, and demographic histories of their primate hosts.

The Sumatran rhinoceros Dicerorhinus sumatrensis is on the brink of extinction. Although habitat loss and poaching were the reasons of the decline, today's reproductive isolation is the main threat to the survival of the species. Genetic studies have played an important role in identifying conservation priorities, including for rhinoceroses. However, for a species such as the Sumatran rhinoceros, where time is of the essence in preventing extinction, to what extent should genetic and geographical distances be taken into account in deciding the most urgently needed conservation interventions? We propose that the populations of Sumatra and Borneo be considered as a single management unit.