Great apes are threatened with extinction, but precise information about the distribution and size of most populations is currently lacking. We conducted orangutan nest counts in the Malaysian state of Sabah (North Borneo), using a combination of ground and helicopter surveys, and provided a way to estimate the current distribution and size of the populations living throughout the entire state. We show that the number of nests detected during aerial surveys is directly related to the estimated true animal density and that a helicopter is an efficient tool to provide robust estimates of orangutan numbers. Our results reveal that with a total estimated population size of about 11,000 individuals, Sabah is one of the main strongholds for orangutans in North Borneo. More than 60% of orangutans living in the state occur outside protected areas, in production forests that have been through several rounds of logging extraction and are still exploited for timber. The role of exploited forests clearly merits further investigation for orangutan conservation in Sabah.
We investigated the genetic structure within and among Bornean orang-utans (Pongo pygmaeus) in forest fragments of the Lower Kinabatangan flood plain in Sabah, Malaysia. DNA was extracted from hair and faecal samples for 200 wild individuals collected during boat surveys on the Kinabatangan River. Fourteen microsatellite loci were used to characterize patterns of genetic diversity. We found that genetic diversity was high in the set of samples (mean H(E) = 0.74) and that genetic differentiation was significant between the samples (average F(ST) = 0.04, P < 0.001) with F(ST) values ranging from low (0.01) to moderately large (0.12) values. Pairwise F(ST) values were significantly higher across the Kinabatangan River than between samples from the same river side, thereby confirming the role of the river as a natural barrier to gene flow. The correlation between genetic and geographical distance was tested by means of a series of Mantel tests based on different measures of geographical distance. We used a Bayesian method to estimate immigration rates. The results indicate that migration is unlikely across the river but cannot be completely ruled out because of the limited F(ST) values. Assignment tests confirm the overall picture that gene flow is limited across the river. We found that migration between samples from the same side of the river had a high probability indicating that orang-utans used to move relatively freely between neighbouring areas. This strongly suggests that there is a need to maintain migration between isolated forest fragments. This could be done by restoring forest corridors alongside the river banks and between patches.
Behavioural observations suggest that orang-utans are semi-solitary animals with females being philopatric and males roaming more widely in search of receptive partners, leading to the prediction that females are more closely related than males at any given site. In contrast, our study presents evidence for male and female philopatry in the orang-utan. We examined patterns of relatedness and parentage in a wild orang-utan population in Borneo using noninvasively collected DNA samples from animals observed to defecate, and microsatellite markers to assess dispersal and mating strategies. Surprisingly, resident females were equally as related to other resident females (mean r(xy) = 0.303) as resident males were to other resident males (mean r(xy) = 0.305). Moreover, resident females were more related to each other and to the resident males than they were to nonresident females, and resident males were more related to each other (and resident females) than they were to nonresident males. We assigned genetic mothers to 12 individuals in the population, while sires could be identified for eight. Both flanged males and unflanged males achieved paternity, similar to findings reported for Sumatran orang-utans.
We examined mitochondrial DNA control region sequences of 73 Kinabatangan orangutans to test the hypothesis that the phylogeographical structure of the Bornean orangutan is influenced by riverine barriers. The Lower Kinabatangan Wildlife Sanctuary contains one of the most northern populations of orangutans (Pongo pygmaeus) on Borneo and is bisected by the Kinabatangan River, the longest river in Sabah. Orang-utan samples on either side of the river were strongly differentiated with a high Phi(ST) value of 0.404 (P < 0.001). Results also suggest an east-west gradient of genetic diversity and evidence for population expansion along the river, possibly reflecting a postglacial colonization of the Kinabatangan floodplain. We compared our data with previously published sequences of Bornean orangutans in the context of river catchment structure on the island and evaluated the general relevance of rivers as barriers to gene flow in this long-lived, solitary arboreal ape.
The approximately 300 (298, 95% CI: 152-581) elephants in the Lower Kinabatangan Managed Elephant Range in Sabah, Malaysian Borneo are a priority sub-population for Borneo's total elephant population (2,040, 95% CI: 1,184-3,652). Habitat loss and human-elephant conflict are recognized as the major threats to Bornean elephant survival. In the Kinabatangan region, human settlements and agricultural development for oil palm drive an intense fragmentation process. Electric fences guard against elephant crop raiding but also remove access to suitable habitat patches. We conducted expert opinion-based least-cost analyses, to model the quantity and configuration of available suitable elephant habitat in the Lower Kinabatangan, and called this the Elephant Habitat Linkage. At 184 km(2), our estimate of available habitat is 54% smaller than the estimate used in the State's Elephant Action Plan for the Lower Kinabatangan Managed Elephant Range (400 km(2)). During high flood levels, available habitat is reduced to only 61 km(2). As a consequence, short-term elephant densities are likely to surge during floods to 4.83 km(-2) (95% CI: 2.46-9.41), among the highest estimated for forest-dwelling elephants in Asia or Africa. During severe floods, the configuration of remaining elephant habitat and the surge in elephant density may put two villages at elevated risk of human-elephant conflict. Lower Kinabatangan elephants are vulnerable to the natural disturbance regime of the river due to their limited dispersal options. Twenty bottlenecks less than one km wide throughout the Elephant Habitat Linkage, have the potential to further reduce access to suitable habitat. Rebuilding landscape connectivity to isolated habitat patches and to the North Kinabatangan Managed Elephant Range (less than 35 km inland) are conservation priorities that would increase the quantity of available habitat, and may work as a mechanism to allow population release, lower elephant density, reduce human-elephant conflict, and enable genetic mixing.
Southeast Asian deforestation rates are among the world's highest and threaten to drive many forest-dependent species to extinction. Climate change is expected to interact with deforestation to amplify this risk. Here we examine whether regional incentives for sustainable forest management will be effective in improving threatened mammal conservation, in isolation and when combined with global climate change mitigation.
Home range is defined as the extent and location of the area covered annually by a wild animal in its natural habitat. Studies of African and Indian elephants in landscapes of largely open habitats have indicated that the sizes of the home range are determined not only by the food supplies and seasonal changes, but also by numerous other factors including availability of water sources, habitat loss and the existence of man-made barriers. The home range size for the Bornean elephant had never been investigated before.
Wild chimpanzee populations are still declining due to logging, disease transmission and hunting. The bushmeat trade frequently leads to an increase in the number of orphaned primates. HELP Congo was the first project to successfully release wild-born orphan chimpanzees into an existing chimpanzee habitat. A collection of post monitoring data over 16 years now offers the unique opportunity to investigate possible behavioural adaptations in these chimpanzees. We investigated the feeding and activity patterns in eight individuals via focal observation techniques from 1997-1999 and 2001-2005. Our results revealed a decline in the number of fruit and insect species in the diet of released chimpanzees over the years, whereas within the same period of time, the number of consumed seed species increased. Furthermore, we found a decline in time spent travelling, but an increase in time spent on social activities, such as grooming, as individuals matured. In conclusion, the observed changes in feeding and activity patterns seem to reflect important long-term behavioural and ecological adaptations in wild-born orphan released chimpanzees, demonstrating that the release of chimpanzees can be successful, even if it takes time for full adaptation.
The endangered proboscis monkey (Nasalis larvatus) is a sexually highly dimorphic Old World primate endemic to the island of Borneo. Previous studies focused mainly on its ecology and behavior, but knowledge of its vocalizations is limited. The present study provides quantified information on vocal rate and on the vocal acoustics of the prominent calls of this species. We audio-recorded vocal behavior of 10 groups over two 4-month periods at the Lower Kinabatangan Wildlife Sanctuary in Sabah, Borneo. We observed monkeys and recorded calls in evening and morning sessions at sleeping trees along riverbanks. We found no differences in the vocal rate between evening and morning observation sessions. Based on multiparametric analysis, we identified acoustic features of the four common call-types "shrieks," "honks," "roars," and "brays." "Chorus" events were also noted in which multiple callers produced a mix of vocalizations. The four call-types were distinguishable based on a combination of fundamental frequency variation, call duration, and degree of voicing. Three of the call-types can be considered as "loud calls" and are therefore deemed promising candidates for non-invasive, vocalization-based monitoring of proboscis monkeys for conservation purposes.
Lowland tropical forests are increasingly threatened with conversion to oil palm as global demand and high profit drives crop expansion throughout the world's tropical regions. Yet, landscapes are not homogeneous and regional constraints dictate land suitability for this crop. We conducted a regional study to investigate spatial and economic components of forest conversion to oil palm within a tropical floodplain in the Lower Kinabatangan, Sabah, Malaysian Borneo. The Kinabatangan ecosystem harbours significant biodiversity with globally threatened species but has suffered forest loss and fragmentation. We mapped the oil palm and forested landscapes (using object-based-image analysis, classification and regression tree analysis and on-screen digitising of high-resolution imagery) and undertook economic modelling. Within the study region (520,269 ha), 250,617 ha is cultivated with oil palm with 77% having high Net-Present-Value (NPV) estimates ($413/ha-yr-$637/ha-yr); but 20.5% is under-producing. In fact 6.3% (15,810 ha) of oil palm is commercially redundant (with negative NPV of $-299/ha-yr-$-65/ha-yr) due to palm mortality from flood inundation. These areas would have been important riparian or flooded forest types. Moreover, 30,173 ha of unprotected forest remain and despite its value for connectivity and biodiversity 64% is allocated for future oil palm. However, we estimate that at minimum 54% of these forests are unsuitable for this crop due to inundation events. If conversion to oil palm occurs, we predict a further 16,207 ha will become commercially redundant. This means that over 32,000 ha of forest within the floodplain would have been converted for little or no financial gain yet with significant cost to the ecosystem. Our findings have globally relevant implications for similar floodplain landscapes undergoing forest transformation to agriculture such as oil palm. Understanding landscape level constraints to this crop, and transferring these into policy and practice, may provide conservation and economic opportunities within these seemingly high opportunity cost landscapes.
Crassignathadanaugirangensis sp. n. (Araneae: Symphytognathidae) was discovered during a tropical ecology field course held at the Danau Girang Field Centre in Sabah, Malaysia. A taxonomic description and accompanying ecological study were completed as course activities. To assess the ecology of this species, which belongs to the ground-web-building spider community, three habitat types were surveyed: riparian forest, recently inundated riverine forest, and oil palm plantation. Crassignathadanaugirangensis sp. n. is the most abundant ground-web-building spider species in riparian forest; it is rare or absent from the recently inundated forest and was not found in a nearby oil palm plantation. The availability of this taxonomic description may help facilitate the accumulation of data about this species and the role of inundated riverine forest in shaping invertebrate communities.
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.
Plant recovery rates after herbivory are thought to be a key factor driving recursion by herbivores to sites and plants to optimise resource-use but have not been investigated as an explanation for recursion in large herbivores. We investigated the relationship between plant recovery and recursion by elephants (Elephas maximus borneensis) in the Lower Kinabatangan Wildlife Sanctuary, Sabah. We identified 182 recently eaten food plants, from 30 species, along 14 × 50 m transects and measured their recovery growth each month over nine months or until they were re-browsed by elephants. The monthly growth in leaf and branch or shoot length for each plant was used to calculate the time required (months) for each species to recover to its pre-eaten length. Elephant returned to all but two transects with 10 eaten plants, a further 26 plants died leaving 146 plants that could be re-eaten. Recursion occurred to 58% of all plants and 12 of the 30 species. Seventy-seven percent of the re-eaten plants were grasses. Recovery times to all plants varied from two to twenty months depending on the species. Recursion to all grasses coincided with plant recovery whereas recursion to most browsed plants occurred four to twelve months before they had recovered to their previous length. The small sample size of many browsed plants that received recursion and uneven plant species distribution across transects limits our ability to generalise for most browsed species but a prominent pattern in plant-scale recursion did emerge. Plant recovery time was a good predictor of time to recursion but varied as a function of growth form (grass, ginger, palm, liana and woody) and differences between sites. Time to plant recursion coincided with plant recovery time for the elephant's preferred food, grasses, and perhaps also gingers, but not the other browsed species. Elephants are bulk feeders so it is likely that they time their returns to bulk feed on these grass species when quantities have recovered sufficiently to meet their intake requirements. The implications for habitat and elephant management are discussed.
Reducing Emissions from Deforestation and forest Degradation (REDD+) aims to avoid forest conversion to alternative land-uses through financial incentives. Oil-palm has high opportunity costs, which according to current literature questions the financial competitiveness of REDD+ in tropical lowlands. To understand this more, we undertook regional fine-scale and coarse-scale analyses (through carbon mapping and economic modelling) to assess the financial viability of REDD+ in safeguarding unprotected forest (30,173 ha) in the Lower Kinabatangan floodplain in Malaysian Borneo. Results estimate 4.7 million metric tons of carbon (MgC) in unprotected forest, with 64% allocated for oil-palm cultivations. Through fine-scale mapping and carbon accounting, we demonstrated that REDD+ can outcompete oil-palm in regions with low suitability, with low carbon prices and low carbon stock. In areas with medium oil-palm suitability, REDD+ could outcompete oil palm in areas with: very high carbon and lower carbon price; medium carbon price and average carbon stock; or, low carbon stock and high carbon price. Areas with high oil palm suitability, REDD+ could only outcompete with higher carbon price and higher carbon stock. In the coarse-scale model, oil-palm outcompeted REDD+ in all cases. For the fine-scale models at the landscape level, low carbon offset prices (US $3 MgCO2e) would enable REDD+ to outcompete oil-palm in 55% of the unprotected forests requiring US $27 million to secure these areas for 25 years. Higher carbon offset price (US $30 MgCO2e) would increase the competitiveness of REDD+ within the landscape but would still only capture between 69%-74% of the unprotected forest, requiring US $380-416 million in carbon financing. REDD+ has been identified as a strategy to mitigate climate change by many countries (including Malaysia). Although REDD+ in certain scenarios cannot outcompete oil palm, this research contributes to the global REDD+ debate by: highlighting REDD+ competitiveness in tropical floodplain landscapes; and, providing a robust approach for identifying and targeting limited REDD+ funds.
The role that oil palm plays in the Lower Kinabatangan region of Eastern Sabah is of considerable scientific and conservation interest, providing a model habitat for many tropical regions as they become increasingly fragmented. Crocodilians, as apex predators, widely distributed throughout the tropics, are ideal indicator species for ecosystem health. Drones (or unmanned aerial vehicles (UAVs)) were used to identify crocodile nests in a fragmented landscape. Flights were targeted through the use of fuzzy overlay models and nests located primarily in areas indicated as suitable habitat. Nests displayed a number of similarities in terms of habitat characteristics allowing for refined modelling of survey locations. As well as being more cost-effective compared to traditional methods of nesting survey, the use of drones also enabled a larger survey area to be completed albeit with a limited number of flights. The study provides a methodology for targeted nest surveying, as well as a low-cost repeatable flight methodology. This approach has potential for widespread applicability across a range of species and for a variety of study designs.
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.
For many threatened species the rate and drivers of population decline are difficult to assess accurately: species' surveys are typically restricted to small geographic areas, are conducted over short time periods, and employ a wide range of survey protocols. We addressed methodological challenges for assessing change in the abundance of an endangered species. We applied novel methods for integrating field and interview survey data for the critically endangered Bornean orangutan (Pongo pygmaeus), allowing a deeper understanding of the species' persistence through time. Our analysis revealed that Bornean orangutan populations have declined at a rate of 25% over the last 10 years. Survival rates of the species are lowest in areas with intermediate rainfall, where complex interrelations between soil fertility, agricultural productivity, and human settlement patterns influence persistence. These areas also have highest threats from human-wildlife conflict. Survival rates are further positively associated with forest extent, but are lower in areas where surrounding forest has been recently converted to industrial agriculture. Our study highlights the urgency of determining specific management interventions needed in different locations to counter the trend of decline and its associated drivers.
There is currently no available information regarding the veterinary management of Sunda clouded leopards (Neofelis diardi), either in captivity or in the wild. In this study, 12 Sunda clouded leopards were anesthetized between January 2008 and February 2014 for medical exams, and/or GPS-collaring. Seven wild-caught individuals were kept in captivity and 5 free-ranging animals were captured by cage traps. Two anesthesia combinations were used: medetomidine-ketamine (M-K) or tiletamine-zolazepam (T-Z). Atipamezole (0.2 mg/kg im) was used as an antagonist for medetomidine. Medetomidine (range: 0.039-0.054 mg/kg) and ketamine (range: 3-4.39 mg/kg) were administered during 5 immobilizations, resulting in median induction times of 7 min. After a median anesthesia time of 56 min, atipamezole was injected, observing effects of antagonism at a median time of 12 min. T-Z (range: 6.8-10.8 mg/kg) was administered on 7 occasions. Median induction times observed with this combination were shorter than with M-K (4 min vs 7 min; P=0.04), and anesthesia and recovery times were significantly longer (244 and 35 min vs 56 and 16 min, respectively; P=0.02). Lower heart rates were measured in the M-K group, while lower rectal temperatures were found in the T-Z group. Both combinations resulted in safe and reliable immobilizations, although given the favorable anesthesia and recovery times of M-K, we recommend this approach over T-Z for the veterinary handling of Sunda clouded leopards.
Six extant species of non-human great apes are currently recognized: Sumatran and Bornean orangutans, eastern and western gorillas, and chimpanzees and bonobos [1]. However, large gaps remain in our knowledge of fine-scale variation in hominoid morphology, behavior, and genetics, and aspects of great ape taxonomy remain in flux. This is particularly true for orangutans (genus: Pongo), the only Asian great apes and phylogenetically our most distant relatives among extant hominids [1]. Designation of Bornean and Sumatran orangutans, P. pygmaeus (Linnaeus 1760) and P. abelii (Lesson 1827), as distinct species occurred in 2001 [1, 2]. Here, we show that an isolated population from Batang Toru, at the southernmost range limit of extant Sumatran orangutans south of Lake Toba, is distinct from other northern Sumatran and Bornean populations. By comparing cranio-mandibular and dental characters of an orangutan killed in a human-animal conflict to those of 33 adult male orangutans of a similar developmental stage, we found consistent differences between the Batang Toru individual and other extant Ponginae. Our analyses of 37 orangutan genomes provided a second line of evidence. Model-based approaches revealed that the deepest split in the evolutionary history of extant orangutans occurred ∼3.38 mya between the Batang Toru population and those to the north of Lake Toba, whereas both currently recognized species separated much later, about 674 kya. Our combined analyses support a new classification of orangutans into three extant species. The new species, Pongo tapanuliensis, encompasses the Batang Toru population, of which fewer than 800 individuals survive. VIDEO ABSTRACT.