Third-party vocal intervention in the proboscis monkey (Nasalis larvatus)

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

Does the Vulnerable sun bear Helarctos malayanus damage crops and threaten people in oil palm plantations?

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

An approaching motor boat induces stress-related behaviors in Proboscis Monkeys (Nasalis larvatus) living in a riparian area

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

Nasalization by Nasalis larvatus: larger noses audiovisually advertise conspecifics in proboscis monkeys

Male proboscis monkeys have uniquely enlarged noses that are prominent adornments, which may have evolved through their sexually competitive harem group social system. Nevertheless, the ecological roles of the signals encoded by enlarged noses remain unclear. We found significant correlations among nose, body, and testis sizes and a clear link between nose size and number of harem females. Therefore, there is evidence supporting both male-male competition and female choice as causal factors in the evolution of enlarged male noses. We also observed that nasal enlargement systematically modifies the resonance properties of male vocalizations, which probably encode male quality. Our results indicate that the audiovisual contributions of enlarged male noses serve as advertisements to females in their mate selection. This is the first primate research to evaluate the evolutionary processes involved in linking morphology, acoustics, and socioecology with unique masculine characteristics

Seed dispersal by proboscis monkeys: the case of Nauclea spp.

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 < 0.001). Therefore, we suggest that proboscis monkeys play a role in 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

Integrating Sunda clouded leopard (Neofelis diardi) conservation into development and restoration planning in Sabah (Borneo)

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

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

Genetics and the last stand of the Sumatran rhinoceros Dicerorhinus sumatrensis

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

First report of foregut microbial community in proboscis monkeys: are diverse forests a reservoir for diverse microbiomes?

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

Survival strategies of a frugivore, the sun bear, in a forest-oil palm landscape

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