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

Lurking in the dark: cryptic Strongyloides in a Bornean slow loris

Within host communities, related species are more likely to share common parasitic agents, and as a result, morphological similarities have led researchers to conclude that parasites infecting closely related hosts within a community represent a single species. However, genetic diversity within parasite genera and host range remain poorly investigated in most systems. Strongyloides is a genus of soil-transmitted nematode that has been reported from several primate species in Africa and Asia, and has been estimated to infect hundreds of millions of people worldwide, although no precise estimates are available. Here we describe a case of infection with a cryptic species of Strongyloides in a Bornean (Philippine) slow loris (Nycticebus menagensis) living within a diverse community of several primate species in the Lower Kinabatangan Wildlife Sanctuary, Malaysian Borneo. Fresh fecal samples were collected from five primate species and nematode larvae cultured from these samples were selected for phylogenetic analyses. Sequences obtained for most larvae were identified as S. fuelleborni, grouping into three different clusters and showing no aggregation within specific hosts or geographic location. In contrast, a set of parasite sequences obtained from a slow loris clustered closely with S. stercoralis into a different group, being genetically distinct to sequences reported from other primate hosts, humans included. Our results suggest that although S. fuelleborni infects all haplorrhines sampled in this primate community, a different species might be infecting the slow loris, the only strepsirrhine in Borneo and one of the least studied primates in the region. Although more data are needed to support this conclusion, we propose that Strongyloides species in primates might be more diverse than previously thought, with potential implications for ecological and evolutionary host-parasite associations, as well as epidemiological dynamics

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

Faecal particle size in free-ranging proboscis monkeys, Nasalis larvatus: variation between seasons

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

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

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

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

A pinworm's tale: The evolutionary history of Lemuricola (Protenterobius) nycticebi

Lemuricola (Protenterobius) nycticebi is the only pinworm species known to infect strepsirrhine primates outside Africa, and the only pinworm species yet described in slow lorises. Here, we provided a detailed morphological comparison of female and male worms, and a first description of fourth-stage larvae collected from free-living slow lorises (Nycticebus menagensis) in Sabah, Malaysian Borneo. Using mitochondrial and nuclear markers, we also reconstructed the species' phylogenetic relationship with other pinworms infecting primates. Both morphological and molecular results indicated a distinct association between L. (P.) nycticebi and its host. However, while taxonomy identified this species as a member of the Lemuricola clade and grouped pinworms infecting lemurs and slow lorises together, phylogenetic reconstruction split them, placing L. (P.) nycticebi within the Enterobius clade. Our results suggest that L. (P.) nycticebi may represent a different taxon altogether, and that it is more closely related to pinworm species infecting Old World primates outside Madagascar. Pongobius pongoi (Foitová et al., 2008) n. comb. is also proposed