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.
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.
The Bornean orangutan is critically endangered and monitoring its population is needed to inform effective conservation management. In this paper, we present results of 2014-17 aerial nest surveys of the major orangutan populations in Sabah and compare them with baseline data produced during surveys conducted in 2002-03 using similar methods. Our results show three important points: a) by increasing the survey effort (estimated at 15-25% cover), sparsely scattered orangutan sub-populations not recorded in the previous aerial surveys were located and the accuracy of the nest count estimates is expected to improve; b) large populations in the interior forests of Sabah, occupying sustainably managed logged and unlogged forests, have been stable over 15 years and are of vital importance for the species' conservation; c) fragmented populations located in eastern Sabah, that are surrounded by extensive oil palm plantations, have declined at varying rates.
One Health is increasingly being used as a tool in ecosystem protection. The Orangutan Veterinary Advisory Group (OVAG) is working to address One Health concerns in Pongo spp. (orangutan) welfare and conservation. Orangutans are vital contributors to the ecosystem health of their range areas. Strengthening national capacity is crucial to make a lasting difference in the currently bleak outlook for orangutan species survival. OVAG is a capacity strengthening and expertise network that brings together all those working with orangutans, in- and ex-situ, to share knowledge, skills, and to collectively learn. Using the One Health paradigm embedded to enhance professional development, the OVAG network is successfully supporting conservation outcomes and impact. As part of our adaptive management approach, and to assess individual and organizational change attributable to the capacity strengthening work of OVAG, we evaluated technical skill test data, program satisfaction data, and asked participants to complete a self-reflective survey. This pilot study of our work demonstrates statistically significant improvements in conservation medicine (t = 5.481, p
The Sumatran orangutan is currently listed by the IUCN as critically endangered and the Bornean species as endangered. Unless effective conservation measures are enacted quickly, most orangutan populations without adequate protection face a dire future. Two main strategies are being pursued to conserve orangutans: (i) rehabilitation and reintroduction of ex-captive or displaced individuals; and (ii) protection of their forest habitat to abate threats like deforestation and hunting. These strategies are often mirrored in similar programs to save other valued and endangered mega-fauna. Through GIS analysis, collating data from across the literature, and combining this information within a modelling and decision analysis framework, we analysed which strategy or combination of strategies is the most cost-effective at maintaining wild orangutan populations, and under what conditions. We discovered that neither strategy was optimal under all circumstances but was dependent on the relative cost per orangutan, the timescale of management concern, and the rate of deforestation. Reintroduction, which costs twelve times as much per animal as compared to protection of forest, was only a cost-effective strategy at very short timescales. For time scales longer than 10-20 years, forest protection is the more cost-efficient strategy for maintaining wild orangutan populations. Our analyses showed that a third, rarely utilised strategy is intermediate: introducing sustainable logging practices and protection from hunting in timber production forest. Maximum long-term cost-efficiency is achieved by working in conservation forest. However, habitat protection involves addressing complex conservation issues and conflicting needs at the landscape level. We find a potential resolution in that well-managed production forests could achieve intermediate conservation outcomes. This has broad implications for sustaining biodiversity more generally within an economically productive landscape. Insights from this analysis should provide a better framework to prioritize financial investments, and facilitate improved integration between the organizations that implement these strategies.
We analysed the reproductive parameters of free-ranging female orangutans at Sepilok Orangutan Rehabilitation Centre (SORC) on Borneo Island, Sabah, Malaysia. Fourteen adult females produced 28 offspring in total between 1967 and 2004. The average censored interbirth interval (IBI) (i.e. offspring was still alive when mother produced a next offspring) was 6 years. This was shorter than censored IBIs reported in the wild but similar to IBIs reported for those in captivity. The nonparametric survival analysis (Kaplan-Meier method) revealed a significantly shorter IBI at SORC compared with wild orangutans in Tanjung Putting. The infant (0-3 years) mortality rate at SORC of 57% was much higher than rates reported both in the wild and captivity. The birth sex-ratio was significantly biassed toward females: 24 of the 27 sex-identified infants were females. The average age at first reproduction was 11.6 years, which is younger than the age in the wild and in captivity. The high infant mortality rate might be caused by human rearing and increased transmission of disease due to frequent proximal encounters with conspecifics around the feeding platforms (FPs). This young age of first reproduction could be because of the uncertainty regarding estimated ages of the female orangutans at SORC. It may also be affected by association with other conspecifics around FPs, which increased the number of encounters of the females with males compared with the number of encounters that would take place in the wild. Provision of FPs, which improves the nutritional condition of the females, caused the shorter IBI. The female-biassed birth sex-ratio can be explained by the Trivers and Willard hypothesis. The female-biassed sex ratio could be caused by the mothers being in poor health, parasite prevalence and/or high social stress (but not food scarcity) due to the frequent encounters with conspecifics around FPs.
We observed the diet and activity of Bornean orangutans (Pongo pygmaeus morio) in the primary lowland dipterocarp forests of Danum Valley, Sabah, Malaysia, during 2005-2007, including two mast fruitings. We collected 1,785 hr of focal data on 26 orangutans. We identified 1,466 samples of their food plants and conducted a fallen fruit census to monitor fruit availability in the study area. Their activity budget was 47.2% feeding, 34.4% resting, and 16.9% traveling. Fruits accounted for the largest part (60.9%) of feeding time, especially during mast fruiting periods (64.0-100%), although the percentages of leaves (22.2%) and bark (12.3%) were higher than those reported for P. abelii and P. pygmaeus wurmbii. Although 119 genera and 160 plant species were consumed by focal animals, only 9 genera accounted for more than 3% of feeding time (total: 67.8% for 9 genera). In particular, the focal orangutans fed intensively on Ficus and Spatholobus during most of the study period, especially in periods of fruit shortage. The percentage of fruit feeding changed markedly from 11.7 to 100% across different months of the year, and was positively correlated with the amount of fallen fruit. When fruit feeding and availability decreased, orangutans fed primarily on leaves of Spatholobus and Ficus, and the bark of Spatholobus and dipterocarp. The percentage of time devoted to feeding during mast fruitings, when the orangutans foraged almost exclusively on fruits, was lower than during seasons when the orangutan diet included leaves and bark as well as fruits. Resting increased as feeding decreased in the late stage of each fruiting season, suggesting that the orangutans adopted an energy-minimizing strategy to survive the periods of fruit shortage by using energy stored during the fruit season.
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.
Orangutans have a long period of immaturity and the longest inter-birth interval (IBI) of all mammals, which can be explained by their solitary life style, preventing the mother from rearing two offspring simultaneously (solitary life hypothesis) [corrected]. We collected data on mother-offspring dyads living in a primary lowland forest in Danum Valley, East Borneo in an effort to examine the developmental and behavioral patterns of the subspecies Pongo pygmaeus morio. We analyzed developmental changes in mother-offspring distance, contact, and activity budgets in orangutans ranging from 1 to 7 years of age. The results indicated decreased resting and playing with increasing age, whereas feeding, traveling and social play all increased significantly. Mothers' feeding and traveling time were good predictors of their offspring's feeding and traveling activities. Mother-offspring contact lasted longer in resting contexts; contact during traveling was almost non-existent after 4 years of age. Comparisons with previously published data on the Sumatran species Pongo abelli revealed no fundamental differences in these behavioral measures. However, a shorter association time with the mother after behavioral independence is documented for this East Bornean population in comparison to Sumatran populations. These results are best explained by the solitary life hypothesis, in agreement with previous studies. We suggest that environmental constraints in Bornean forests, as well as a lower population density, should be considered when interpreting the differences between Sumatran and Bornean orangutans in both the period of association with mother and the IBI.
Orangutans display remarkable developmental changes and sexual differences in facial morphology, such as the flanges or cheek-pads that develop only on the face of dominant adult males. These changes suggest that facial morphology is an important factor in visual communication. However, developmental changes in facial morphology have not been examined in detail. We studied developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus) by observing 79 individuals of various ages living in the Sepilok Orangutan Rehabilitation Centre (SORC) in Malaysia and in Japanese zoos. We also analyzed photographs of one captive male that were taken over a period of more than 16 years. There were clear morphological changes that occurred with growth, and we identified previously unreported sexual and developmental differences in facial morphology. Light-colored skin around the eyes and mouth is most prominent in animals younger than 3 years, and rapidly decreases in area through the age of approximately 7 years. At the same time, the scattered, erect hairs on the head (infant hair) become thick, dense hairs lying on the head (adult hair) in both sexes. The results suggest that these features are infant signals, and that adult signals may include darkened face color, adult hair, whiskers, and a beard, which begin to develop after the age of approximately 7 years in both sexes. In females, the eyelids remain white even after 10 years, and turn black at around the age of 20; in males, the eyelids turn black before the age of 10. The whiskers and beards of adults are thicker in males than in females, and are fully developed before the age of 10 in males, while they begin to develop in females only after approximately 20 years. White eyelids and undeveloped whiskers and beards may be visual signals that are indicative of young adult females. Our results also show that the facial morphology of the unflanged male is similar to that of the adult female, although it has also been pointed out that unflanged males resemble younger individuals.
Non-invasive measures of stress are crucial for captive and conservation management programs. The adrenal hormone dehydroepiandrosterone-sulfate (DHEAS) has recently been adopted as a stress marker, but there is little investigation of its relationship to glucocorticoids (GC), well-known indicators of stress. This study examined the influence of age, reproductive state and environment on GC and DHEAS levels in orangutans, to test whether the GC/DHEAS ratio can provide an index of stress response in primates. We measured fecal GC (fGC) and fecal DHEAS (fDHEAS) concentrations in 7 captive orangutans from zoological parks in Japan and 22 wild orangutans from Danum Valley Conservation Area, Malaysia. We found that in a stressful condition (transportation), fDHEAS levels increased 2 days after the fGC response, which occurred 1 day after the stressor. One pregnant female had elevated levels of both hormones, and a higher fGC/fDHEAS ratio than baseline. Females in the first year of lactation had fGC levels and the fGC/fDHEAS ratio significantly higher than both baseline and females in the second and subsequent years of lactation. There was no effect of age on fGC levels, but the fGC/fDHEAS ratio was higher in infants than adults and adolescents. fDHEAS concentrations were lower in infants than juveniles, adolescents and adults, a phenomenon known as adrenarche, shared with humans and other great apes. We suggest that changes in DHEAS during orangutan life history are associated with changes in the dynamics of maintaining homeostasis that vary with age and reproductive state. The GC/DHEAS ratio index is useful to evaluate age-related abilities of responding to stressful challenges.
Nature-based tourism can generate important revenue to support conservation of biodiversity. However, constant exposure to tourists and subsequent chronic activation of stress responses can produce pathological effects, including impaired cognition, growth, reproduction, and immunity in the same animals we are interested in protecting. Utilizing fecal samples (N = 53) from 2 wild habituated orangutans (Pongo pygmaeus morio) (in addition to 26 fecal samples from 4 wild unhabituated orangutans) in the Lower Kinabatangan Wildlife Sanctuary of Sabah, Malaysian Borneo, we predicted that i) fecal glucocorticoid metabolite concentrations would be elevated on the day after tourist visitation (indicative of normal stress response to exposure to tourists on the previous day) compared to samples taken before or during tourist visitation in wild, habituated orangutans, and ii) that samples collected from habituated animals would have lower fecal glucocorticoid metabolites than unhabituated animals not used for tourism. Among the habituated animals used for tourism, fecal glucocorticoid metabolite levels were significantly elevated in samples collected the day after tourist visitation (indicative of elevated cortisol production on the previous day during tourist visitation). Fecal glucocorticoid metabolite levels were also lower in the habituated animals compared to their age-matched unhabituated counterparts. We conclude that the habituated animals used for this singular ecotourism project are not chronically stressed, unlike other species/populations with documented permanent alterations in stress responses. Animal temperament, species, the presence of coping/escape mechanisms, social confounders, and variation in amount of tourism may explain differences among previous experiments. Acute alterations in glucocorticoid measures in wildlife exposed to tourism must be interpreted conservatively. While permanently altered stress responses can be detrimental, preliminary results in these wild habituated orangutans suggest that low levels of predictable disturbance can likely result in low physiological impact on these animals.
Taste perception is an essential function that provides valuable dietary and sensory information, which is crucial for the survival of animals. Studies into the evolution of the sweet taste receptor gene (TAS1R2) are scarce, especially for Bornean endemic primates such as Nasalis larvatus (proboscis monkey), Pongo pygmaeus (Bornean orangutan), and Hylobates muelleri (Muller's Bornean gibbon). Primates are the perfect taxa to study as they are diverse dietary feeders, comprising specialist folivores, frugivores, gummivores, herbivores, and omnivores. We constructed phylogenetic trees of the TAS1R2 gene for 20 species of anthropoid primates using four different methods (neighbor-joining, maximum parsimony, maximum-likelihood, and Bayesian) and also established the time divergence of the phylogeny. The phylogeny successfully separated the primates into their taxonomic groups as well as by their dietary preferences. Of note, the reviewed time of divergence estimation for the primate speciation pattern in this study was more recent than the previously published estimates. It is believed that this difference may be due to environmental changes, such as food scarcity and climate change, during the late Miocene epoch, which forced primates to change their dietary preferences. These findings provide a starting point for further investigation.
Bornean orangutan is a critically endangered non-human primate; however, the threat of extinction is not merely from poaching and habitat loss. Orangutan survival is also threatened by the genetic loss and genetic bottleneck due to the low effective population, prompting the dire need for an immediate genetic preservation program through systematic biobanking and assisted reproductive technology (ART). This study aims to provide integral data to the semen characteristics, extension, and cryopreservation of the Bornean orangutan and the potential relationship to male traits. Five captive orangutans from Sepilok Orangutan Rehabilitation Centre (SORC) with a mean body weight of 52.81 ± 7.00 kg were used for this study. Semen collection was performed using electroejaculation (EE) under complete general anesthesia. Semen was subjected to macroscopic and microscopic evaluation while testicular measurement was obtained using digital calipers. The semen characteristics of the orangutans are volume (778 ± 250.21 µl), pH (7.80 ± 0.25), concentration (32.38 ± 17.40 × 106 sperm/ml), total motility (61.00 ± 12.88%), adjusted motility index (48.76 ± 11.32%), live spermatozoa (77.75 ± 6.94%) and normal spermatozoa (11.48 ± 11.34%). Analysis of variance statistical analysis test was used to compare the significant difference between means, at (p
Unsustainable exploitation of natural resources is increasingly affecting the highly biodiverse tropics [1, 2]. Although rapid developments in remote sensing technology have permitted more precise estimates of land-cover change over large spatial scales [3-5], our knowledge about the effects of these changes on wildlife is much more sparse [6, 7]. Here we use field survey data, predictive density distribution modeling, and remote sensing to investigate the impact of resource use and land-use changes on the density distribution of Bornean orangutans (Pongo pygmaeus). Our models indicate that between 1999 and 2015, half of the orangutan population was affected by logging, deforestation, or industrialized plantations. Although land clearance caused the most dramatic rates of decline, it accounted for only a small proportion of the total loss. A much larger number of orangutans were lost in selectively logged and primary forests, where rates of decline were less precipitous, but where far more orangutans are found. This suggests that further drivers, independent of land-use change, contribute to orangutan loss. This finding is consistent with studies reporting hunting as a major cause in orangutan decline [8-10]. Our predictions of orangutan abundance loss across Borneo suggest that the population decreased by more than 100,000 individuals, corroborating recent estimates of decline [11]. Practical solutions to prevent future orangutan decline can only be realized by addressing its complex causes in a holistic manner across political and societal sectors, such as in land-use planning, resource exploitation, infrastructure development, and education, and by increasing long-term sustainability [12]. VIDEO ABSTRACT.
Reports of wild great ape fatalities have been very limited, and only two have described wild orangutan deaths. We found a wounded juvenile female Bornean orangutan on 7 October 2006 in the Danum Valley, Sabah, Malaysia, and observed the individual's behavior for 7 days until her death on 13 October 2006. The 5-6-year-old orangutan, which we had observed since 2004, was wounded in the left brachium, back, and right hand. The individual's behavior changed after injury; the mean nest-nest active time became significantly shorter than before injury (from 12 h 3 min to 9 h 33 min), the mean waking time became significantly later (0552-0629 hours) and the mean bedtime became significantly earlier (from 1747 to 1603 hours). In the activity budget, resting increased significantly from 28.0 to 53.3%. Traveling and feeding decreased significantly from 23.5 to 12.7% and from 45.6 to 32.8%, respectively. The rate of brachiation during traveling and nest making decreased, whereas ground activity increased from 0 to 9%. We observed one vomiting incident and four occurrences of watery diarrhea during the 7 days before the individual died. The results of an autopsy performed by a local veterinarian suggested that the cause of death was septicemia because of Pseudomonas aeruginosa infection of the severely contaminated wounds. The morphology and distribution of the wounds suggested they had been incurred during an attack by a large animal with fangs and/or claws. This juvenile female became independent of its mother at ~4-5 years of age, slightly earlier than average. This individual might have been vulnerable to predatory attack because of her small body size (~5 kg at death) and lack of the mother's protection.
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.
Ecotourism can function as a powerful tool for species conservation. However, a significant proportion of travelers at wildlife sanctuaries may be ill and potentially infectious, creating unnecessary risk of pathogen transmission to wildlife.
The Bukit Merah Orang Utan Island (OUI) Foundation has been conducting behavioral and veterinary research on orangutans as an attempt at ex situ conservation. Since 2010, the Primate Research Institute, Kyoto University has been collaborating with OUI to promote environmental enrichment and infant rearing by biological mothers in addition to the continuous efforts of refining the veterinary management of the endangered species. In 2011, three Bornean orangutans (Pongo pygmaeus pygmaeus) were released on an island, called BJ Island, adjacent to OUI. This island is approximately 5.6 ha in size, and 635 trees belonging to 102 plant species were identified prior to their release. Behavioral monitoring of the released individuals has been conducted to evaluate their behavioral adaptation to the new environment. Two of the three released orangutans were born in the wild, whereas the youngest individual was born on OUI and expected to learn forest survival strategies from the two older individuals. One of the orangutans was pregnant at the time of release and subsequently gave birth to two male infants on BJ Island. The behavioral monitoring indicated that these orangutans traveled more and spent more time on trees following their release onto BJ Island. However, resting was longer for two females both on OUI and BJ Island when compared to other populations. The orangutans consumed some natural food resources on BJ Island. The release into a more naturalistic environment may help the orangutans to develop more naturalistic behavioral patterns that resemble their wild counterparts.