Jumping in the night: an investigation of leaping activity of western tarsier (cephalopachus bancanus borneanus) using accelerometers

Accelerometers enable scientists to quantify the activity of free-living animals whose direct observation is difficult or demanding due to their elusive nature or nocturnal habits. However, the deployment of accelerometers on small-bodied animals and, in particular, on primates has been little explored. Here we show the first application of accelerometers on the western tarsier (Cephalopachus bancanus borneanus), a nocturnal, small-bodied primate endemic to the forests of Borneo. The fieldwork was carried out in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysian Borneo. We provide guidelines for the deployment of accelerometers on tarsiers that might also be applied to other primate species. Our collected data on 2 females show levels of leaping activity comparable to those previously described using direct observation of wild or captive individuals. The 2 females showed different patterns of leaping activity, which calls for work to explore individual differences further. Our work demonstrates that accelerometers can be deployed on small primates to acquire body motion data that would otherwise be demanding to collect using classic field observations. Future work will be focused on using accelerometer data to discriminate in more detail the different behaviours tarsiers can display and to address the causes and consequences of individual variations in activity

Habitat use and movement of proboscis monkeys (Nasalis larvatus) in a degraded and human-modified forest landscape

Proboscis monkeys (Nasalis larvatus) are endemic to Borneo and live in habitats threatened by land clearance for agriculture, aquaculture and timber. This thesis examines the roles of structural and landscape characteristics on both short- and long-term habitat use through the first application of GPS tags to proboscis monkeys. In a comparison of four home range estimators, biased random bridges provided the best home range estimates given the GPS-collar dataset and landscape characteristics (Chapter 3). Differences in long-term ranging patterns of 10 individuals across a range of forest-block sizes and disturbance levels were examined, as well as daily and seasonal variation in movement and sleeping site selection. Using Light Detection and Ranging (LiDAR) structural metrics of the forest, as well as landscape characteristics, forest with taller canopies, forests in close proximity to river edges were found to be of particular importance to proboscis monkeys, and plantation edges were avoided (Chapter 4). Changes in daily and monthly movements were associated with seasonal changes in rainfall and potential food availability. Movement patterns also changed near forest edges, with faster, more direct movements near agricultural boundaries. Less rainfall, higher temperatures and brighter moon phases correlated with selection of sleeping sites in the forest interior (Chapter 5). By understanding the ranging requirements of proboscis monkeys, drone and GPS collar data were combined to inform conservation policy (Chapter 6). This thesis provides the most in-depth examination of proboscis monkey ecology to date. They appeared more generalist in their home range use and structural habitat requirements than previously realised, suggesting a higher degree of versatility and resilience to habitat loss and degradation. This study provides increased understanding of potential consequences of human-mediated disturbances and can be used to assist in the protection of this charismatic species and the management of degraded landscapes

Combining drones and satellite tracking as an effective tool for informing policy change in riparian habitats: a proboscis monkey case study

Rapid reaction times to undesirable events are becoming increasingly important for the protection and conservation of habitats and species. This study demonstrates how Unmanned Aerial Vehicles, or drones, and satellite tracking of individual animals can be combined to identify important conservation issues (e.g. deforestation). When quickly disseminated, the information can lead to a rapid change in conservation policy. An adult male proboscis monkey, belonging to a one-male social group, was GPS tracked for 6 months in Sabah, Malaysian Borneo during 2012. Riparian habitats featured heavily (25.4% of total time, 88.6% of all sleeping sites) in the group’s home range. A fixed-wing drone was used in 2015 to map the habitat in high-resolution. These data revealed that 47.54 ha of forest had been cleared shortly before the drone flights. GPS tagging data revealed the importance of this area for a one-male proboscis monkey group. A total of 30.1% of the proboscis monkeys’ home range area had been cleared, as well as 11.4% of sleeping sites. Furthermore, drone images revealed that the felling extended to the river’s edge, disregarding water resources laws requiring riparian reserves of a minimum of 20 m. Following this discovery, a press release including drone imagery combined with GPS data, was published linking habitat destruction to a species that is economically important for the tourism industry in Sabah. The day following dissemination of the data, the Sabah State Government ordered an immediate cessation on further land clearing at sensitive riparian reserves along the river. We propose that this combination of satellite and aerial data provides potential for an effective conservation tool for endangered, iconic and economically important species. This visually compelling data, feasible over large spatial scales, can directly inform policy change in a quick and timely manner

Use and selection of sleeping sites by proboscis monkeys, Nasalislarvatus, along the Kinabatangan River, Sabah, Malaysia

The choice of a sleeping site is crucial for primates and may influence their survival. In this study, we investigated several tree characteristics influencing the sleeping site selection by proboscis monkeys (Nasalis larvatus) along Kinabatangan River, in Sabah, Malaysia. We identified 81 sleeping trees used by one-male and all-male social groups from November 2011 to January 2012. We recorded 15 variables for each tree. Within sleeping sites, sleeping trees were taller, had a larger trunk, with larger and higher first branches than surrounding trees. The crown contained more mature leaves, ripe and unripe fruits but had vines less often than surrounding trees. In addition, in this study, we also focused on a larger scale, considering sleeping and non-sleeping sites. Multivariate analyses highlighted a combination of 6 variables that revealed the significance of sleeping trees as well as surrounding trees in the selection process. During our boat surveys, we observed that adult females and young individuals stayed higher in the canopy than adult males. This pattern may be driven by their increased vulnerability to predation. Finally, we suggest that the selection of particular sleeping tree features (i.e. tall, high first branch) by proboscis monkeys is mostly influenced by antipredation strategies

A comparative evaluation of thermal camera and visual counting methods for primate census in a riparian forest at the Lower Kinabatangan Wildlife Sanctuary (LKWS), Malaysian Borneo.

A number of primate census techniques have been developed over the past half-century, each of which have advantages and disadvantages in terms of resources required by researchers (e.g., time and costs), availability of technologies, and effectiveness in different habitat types. This study aims to explore the effectiveness of a thermal imaging technique to estimate the group size of different primate species populations in a degraded riparian forest in the Lower Kinabatangan Wildlife Sanctuary (LKWS), Sabah. We compared this survey technique to the conventional visual counting method along the riverbank. For 38 days, a total of 138 primate groups were observed by thermal camera and visually throughout the study. Optimal conditions for the thermal camera were clear weather, not more than 100 m distance from the observer to the targeted area, boat speed ranging between 5 and 12 km/h, and early morning between 04:30 and 05:30 am. The limitations of the thermal cameras include the inability to identify individual species, sexes, age classes, and also to discern between animals closely aggregated (i.e., mothers with attached infants). Despite these limitations with the thermal camera technique, 1.78 times more primates were detected than counting by eye (p < 0.001), showing the potential benefit of using thermal cameras as an important tool in primate surveys. Nevertheless, ground truthing must be conducted immediately after, or simultaneously during, the thermal survey to verify the species of animals observed on the thermal imagery

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

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

Coming down from the trees: is terrestrial activity in Bornean orangutans natural or disturbance driven?

The orangutan is the world's largest arboreal mammal, and images of the red ape moving through the tropical forest canopy symbolise its typical arboreal behaviour. Records of terrestrial behaviour are scarce and often associated with habitat disturbance. We conducted a large-scale species-level analysis of ground-based camera-trapping data to evaluate the extent to which Bornean orangutans Pongo pygmaeus come down from the trees to travel terrestrially, and whether they are indeed forced to the ground primarily by anthropogenic forest disturbances. Although the degree of forest disturbance and canopy gap size influenced terrestriality, orangutans were recorded on the ground as frequently in heavily degraded habitats as in primary forests. Furthermore, all age-sex classes were recorded on the ground (flanged males more often). This suggests that terrestrial locomotion is part of the Bornean orangutan's natural behavioural repertoire to a much greater extent than previously thought, and is only modified by habitat disturbance. The capacity of orangutans to come down from the trees may increase their ability to cope with at least smaller-scale forest fragmentation, and to cross moderately open spaces in mosaic landscapes, although the extent of this versatility remains to be investigated

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