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.
Orangutans (Pongo spp.) are reported to have extremely slow life histories, including the longest average interbirth intervals of all mammals. Such slow life history can be viable only when unavoidable mortality is kept low. Thus, orangutans' survivorship under natural conditions is expected to be extremely high. Previous estimates of orangutan life history were based on captive individuals living under very different circumstances or on small samples from wild populations. Here, we combine birth data from seven field sites, each with demographic data collection for at least 10 years (range 12-43 years) on wild orangutans to better document their life history. Using strict criteria for data inclusion, we calculated infant survival, interbirth intervals and female age at first reproduction, across species, subspecies and islands. We found an average closed interbirth interval of 7.6 years, as well as consistently very high pre-weaning survival for males and females. Female survival of 94% until age at first birth (at around age 15 years) was higher than reported for any other mammal species under natural conditions. Similarly, annual survival among parous females is very high, but longevity remains to be estimated. Current data suggest no major life history differences between Sumatran and Bornean orangutans. The high offspring survival is remarkable, noting that modern human populations seem to have reached the same level of survival only in the 20th century. The orangutans' slow life history illustrates what can be achieved if a hominoid bauplan is exposed to low unavoidable mortality. Their high survival is likely due to their arboreal and non-gregarious lifestyle, and has allowed them to maintain viable populations, despite living in low-productivity habitats. However, their slow life history also implies that orangutans are highly vulnerable to a catastrophic population crash in the face of drastic habitat change.
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.
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.
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.
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.
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.
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.
The reproductive success of male primates is not always associated with dominance status. For example, even though male orangutans exhibit intra-sexual dimorphism and clear dominance relationships exist among males, previous studies have reported that both morphs are able to sire offspring. The present study aimed to compare the reproductive success of two male morphs, and to determine whether unflanged males sired offspring in a free-ranging population of Bornean orangutans, using 12 microsatellite loci to determine the paternity of eight infants. A single flanged male sired most of the offspring from parous females, and an unflanged male sired a firstborn. This is consistent with our observation that the dominant flanged male showed little interest in nulliparous females, whereas the unflanged males frequently mated with them. This suggests that the dominant flanged male monopolizes the fertilization of parous females and that unflanged males take advantage of any mating opportunities that arise in the absence of the flanged male, even though the conception probability of nulliparous females is relatively low.
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.
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.
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.
Medetomidine (0.02-0.06 mg/kg) in combination with zolazepam-tiletamine (0.8-2.3 mg/kg) were evaluated for reversible anesthesia in four species of Southeast Asian primates: Bornean orangutan (Pongo pygmaeus pygmaeus), Bornean gibbon (Hylobates muelleri), long-tailed macaque (Macaca fascicularis), and pig-tailed macaque (Macaca nemestrina). Twenty-three anesthetic procedures of captive-held and free-ranging primates were studied in Sabah, Malaysia. The induction was smooth and rapid. Respiratory and heart rates were stable throughout anesthesia, whereas body temperature and systolic arterial blood pressure decreased significantly. Atipamezole at five times the medetomidine dose effectively reversed anesthesia, with first signs of recovery within 3-27 min.