Carbon and nitrogen stable isotopic offsets between diet and hair/feces in captive orangutans.

Estimating stable isotopic offset values is crucial for dietary reconstructions. Although research into stable isotope ecology of wild nonhuman primates is increasing overall, only a minority of studies involve laboratory experiments. This study is the first to report the carbon and nitrogen stable isotopic offset values in hair and feces of orangutans. During an experiment lasting 1 week, the weight of each consumed food item was recorded for each of six captive Bornean orangutan (Pongo pygmaeus) individuals. The food, hair, and fecal samples were collected for a few days, and their stable carbon and nitrogen isotope ratios were measured using an elemental analyzer/isotope ratio mass spectrometer. Subsamples of feces were treated with ethanol during the preservation process. Monte Carlo analyses showed that the 95% confidence intervals (CIs) of the carbon and nitrogen offset values between hair and diet were +0.9‰ to +3.9‰ and +2.3‰ to +4.5‰, respectively. The 95% CIs of the carbon and nitrogen offset values between feces and diet were -3.7‰ to -0.9‰ and +0.3‰ to +2.7‰, respectively. The effect of ethanol treatment on the stable isotope ratios of feces was unclear and inconclusive. The computed offset values of hair in captive orangutans are similar to those reported in other nonhuman primates, although those of feces showed greater interspecies variations. The offset values estimated in this study contribute to isotopic studies into the feeding ecology of free-ranging orangutans who are critically endangered in most wild settings.

Comparative analysis of sperm motility in liquid and seminal coagulum portions between Bornean orangutan (Pongo pygmaeus) and chimpanzee (Pan troglodytes).

Coagulum in the semen of some primates plays different roles, depending on the species. In the present study, we examined sperm motility in the coagulum and liquid portions of semen collected from captive individuals from two great ape species: two adult Bornean orangutans (Pongo pygmaeus) (n = 27) and three adult chimpanzees (Pan troglodytes) (n = 14). The results revealed that orangutan sperm remained motile for significantly longer in the coagulum than in the liquid portion (> 18 h). By contrast, chimpanzee sperm motility did not differ significantly over time between the two portions of the semen, although motility was slightly higher in the liquid portion than in the coagulum. The evolution of the seminal coagulum is thought to be related to postcopulatory sperm competition; however, functions of seminal coagulum have not been completely elucidated. Our data from the orangutan semen suggest that in this species, seminal coagulum may strengthen own-sperm survival. This report is the first to provide evidence for this distinctive function of the seminal coagulum. This unique property of orangutan seminal coagulum might be attributable to their reproductive traits, e.g., difficulty in predicting ovulation due to a lack of genital swelling during estrus. The orangutan is a Critically Endangered species, and captive breeding, including artificial insemination (AI), is expected. However, worldwide, only one case of orangutan AI has been successful. Our findings may contribute to an understanding of their basic semen characteristics and help improve the AI method.

Habitat use by a primate community in a lowland dipterocarp forest in Danum Valley, Borneo.

Knowledge of niche partitioning with respect to habitat is indispensable to understand the mechanism of coexistence of multiple species. Among primates, however, data are still deficient because repeated survey for a sufficiently long time, covering seasonal changes over a large area, is the only way to clarify habitat segregation within a seasonally fluctuating environment. Southeast Asia is particularly interesting because of the supra-annual, highly unpredictable seasonality in fruiting known as mast fruiting. We conducted repeated route census, habitat monitoring, and group tracking for 25 months in two study sites (ca. 10 km apart) in the largely primary lowland dipterocarp forest of the Danum Valley Conservation Area, eastern Sabah, northern Borneo, Malaysia. The five species of diurnal primates (Bornean orangutan Pongo pygmaeus, Müeller's gibbon Hylobates muelleri, red leaf monkey Presbytis rubicunda, long-tailed macaque Macaca fascicularis, and southern pig-tailed macaque M. nemestrina) did not show horizontal spatial segregation. Red leaf monkeys showed preferences for places with short tree height, but their distribution was not confined to such places. In response to the fruiting peak observed once during the study period, orangutans increased their numbers simultaneously in the two study sites. The average tree height used by the five species was different, but their range overlapped substantially. Compared with other primate communities, the lack of horizontal spatial segregation and the suggested long-distance movement of orangutans seem to be unique characteristics in Borneo, although the use of different forest strata is a widespread phenomenon among primate communities throughout the world.

Gynaecological diagnosis by ultrasound and the measurement of urinary sex steroid hormones in female orangutans.

Gynaecological diagnoses were carried in three adult female orangutans (Pongo spp.) using ultrasound, and their estrous states were estimated by measuring urinary sex steroid hormone concentrations using enzyme immunoassay. Ultrasound diagnosis revealed that the endometrial thickness and follicle size were correlated with the oestrogen-3-glucuronide concentrations in the follicular phase. In addition, administration of the ovulation inducer human chorionic gonadotropin (hCG) had the strongest effect on the pregnanediol-3-glucuronide (PdG) concentration when the follicle size was 22.3 mm, suggesting that the follicle reaches this size before ovulation. The similarity between this and the maximum ovarian follicle size in humans (approximately 20 mm) indicates that the ancestral reproductive characteristics may have been retained in these species.

The slow ape: High infant survival and long interbirth intervals in wild orangutans.

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.

Development and behavior of wild infant-juvenile East Bornean orangutans (Pongo pygmaeus morio) in Danum Valley.

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.

Urinary sex steroid hormone and placental leucine aminopeptidase concentration differences between live births and stillbirth of Bornean orangutans (Pongo pygmaeus).

BACKGROUND: Under the environment of pregnancy, the placenta assumes an important steroidogenic role in the maintenance of pregnancy. METHODS: Urinary placental leucine aminopeptidase (PLAP), estrone-3-glucuronide (E1 G), and pregnanediol-3-glucuronide (PdG) concentrations were compared among five pregnancies (four live births and one stillbirth) in four orangutans. RESULTS: The gestation period of the stillbirth (223 days) was shorter than that of the live births (239-254 days). In females who gave a live birth, average PLAP and E1 G concentrations increased until the delivery. Conversely, in the female who gave a stillbirth, PLAP concentration failed to increase, and E1 G concentration was significantly low in late pregnancy period. Regarding PdG concentrations, there was no significant difference among all pregnancies. CONCLUSIONS: This is the first study reporting a change in urinary PLAP, E1 G, and PdG concentrations during orangutan stillbirth and live birth pregnancies. The findings will assist in developing pregnancy screening tests.

Fluctuations of population density in Bornean orangutans (Pongo pygmaeus morio) related to fruit availability in the Danum Valley, Sabah, Malaysia: a 10-year record including two mast fruitings and three other peak fruitings.

We investigated the population density of Bornean orangutans (Pongo pygmaeus morio) and fruit availability for 10 years (2005-2014), in primary lowland dipterocarp forests in the Danum Valley, Sabah, Malaysia. During the research period, two mast fruitings and three other peak fruiting events of different scales occurred in the study area. The orangutan population density, estimated every 2 months by the marked nest count method, changed between 0.3 and 4.4 ind/km2 and the mean population density was 1.3 ind/km2 ± SE 0.1 (n = 56). The population density increased markedly during mast and peak fruiting periods. A significant positive correlation was observed between the population density and fruit availability in the study period (Spearman, R = 0.3, P < 0.01, n = 56). During non-fruiting periods, however, no significant correlation was observed between them. These results suggest that the spatial difference in fruit availability during mast and peak fruiting periods was larger than during non-fruiting periods, and many orangutans temporarily moved to the study site from the surrounding areas seeking fruit.

Detection of urinary estrogen conjugates and creatinine using near infrared spectroscopy in Bornean orangutans (Pongo Pygmaeus).

For promoting in situ conservation, it is important to estimate the density distribution of fertile individuals, and there is a need for developing an easy monitoring method to discriminate between physiological states. To date, physiological state has generally been determined by measuring hormone concentration using radioimmunoassay or enzyme immunoassay (EIA) methods. However, these methods have rarely been applied in situ because of the requirements for a large amount of reagent, instruments, and a radioactive isotope. In addition, the proper storage of the sample (including urine and feces) on site until analysis is difficult. On the other hand, near infrared (NIR) spectroscopy requires no reagent and enables rapid measurement. In the present study, we attempted urinary NIR spectroscopy to determine the estrogen levels of orangutans in Japanese zoos and in the Danum Valley Conservation Area, Sabah, Malaysia. Reflectance NIR spectra were obtained from urine stored using a filter paper. Filter paper is easy to use to store dried urine, even in the wild. Urinary estrogen and creatinine concentrations measured by EIA were used as the reference data of partial least square (PLS) regression of urinary NIR spectra. High accuracies (R(2) > 0.68) were obtained in both estrogen and creatinine regression models. In addition, the PLS regressions in both standards showed higher accuracies (R(2) > 0.70). Therefore, the present study demonstrates that urinary NIR spectra have the potential to estimate the estrogen and creatinine concentrations.

Fatality of a wild Bornean orangutan (Pongo pygmaeus morio): behavior and death of a wounded juvenile in Danum Valley, North Borneo.

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.

Factors affecting reproduction in rehabilitant female orangutans: young age at first birth and short inter-birth interval.

This study investigated the reproductive parameters of free-ranging rehabilitant female orangutans. We aimed to assess the factors that influence these parameters and provide information that could assist with the management of orangutan reintroduction programs. We analyzed the birth records of free-ranging female rehabilitants at Bukit Lawang, Bukit Tigapuluh, Sepilok, Camp Leakey, Kaja Island, Sungai Wain, and Meratus and compared them with reproductive parameters reported in wild and zoo populations. Females' ages at first birth were 10.6-14.7 years, significantly earlier than those of wild and zoo orangutans. Computed inter-birth intervals (IBIs) calculated by the Kaplan-Meier method were 65.1-90.1 months; the values for Camp Leakey and Bukit Lawang rehabilitants were significantly shorter than those reported for wild Sumatran orangutans. Infant mortality rates were 18-61%; the values for Bukit Lawang and Sepilok were significantly higher than those reported for wild Sumatran and zoo orangutans. In rehabilitants, young ages at first birth and shorter IBIs may result from the high energy intake enabled by provisioning, although the possibility exists that they reflect underestimations of age on arrival at rehabilitation centers. The observed high infant mortality rate may reflect poor mothering skills due to human rearing and/or increased disease transmission. This study demonstrates that accelerated reproductive rates (younger age at first birth and shorter IBI) are common in provisioned rehabilitant females on both Sumatra and Borneo.

Effects of Pleistocene glaciations and rivers on the population structure of Bornean orangutans (Pongo pygmaeus).

Sundaland, a tropical hotspot of biodiversity comprising Borneo and Sumatra among other islands, the Malay Peninsula, and a shallow sea, has been subject to dramatic environmental processes. Thus, it presents an ideal opportunity to investigate the role of environmental mechanisms in shaping species distribution and diversity. We investigated the population structure and underlying mechanisms of an insular endemic, the Bornean orangutan (Pongo pygmaeus). Phylogenetic reconstructions based on mtDNA sequences from 211 wild orangutans covering the entire range of the species indicate an unexpectedly recent common ancestor of Bornean orangutans 176 ka (95% highest posterior density, 72-322 ka), pointing to a Pleistocene refugium. High mtDNA differentiation among populations and rare haplotype sharing is consistent with a pattern of strong female philopatry. This is corroborated by isolation by distance tests, which show a significant correlation between mtDNA divergence and distance and a strong effect of rivers as barriers for female movement. Both frequency-based and Bayesian clustering analyses using as many as 25 nuclear microsatellite loci revealed a significant separation among all populations, as well as a small degree of male-mediated gene flow. This study highlights the unique effects of environmental and biological features on the evolutionary history of Bornean orangutans, a highly endangered species particularly vulnerable to future climate and anthropogenic change as an insular endemic.

Parasites found from the feces of Bornean orangutans in Danum Valley, Sabah, Malaysia, with a redescription of Pongobius hugoti and the description of a new species of Pongobius (Nematoda: Oxyuridae).

In order to obtain basic data on parasitic infections of Bornean orangutans, Pongo pygmaeus morio (Owen, 1837), in Danum Valley, Sabah, Malaysia, fecal examinations were conducted. Based on a total of 73 fecal samples from 25 individuals, cysts of Entamoeba coli, Entamoeba spp., and Chilomastix mesnili, cysts and trophozoites of Balantidium coli, and eggs of Trichuris sp. or spp., unknown strongylid(s), Strongyloides fuelleborni, and an unknown oxyurid, plus a rhabditoid larva of Strongyloides sp., were found. Mature and immature worms of Pongobius hugoti Barus et al., 2007 and Pongobius foitovae n. sp. (Oxyuridae: Enterobiinae) were recovered from fecal debris and described. Pongobius foitovae is readily distinguished from P. hugoti by having a much longer esophageal corpus, a longer and distally hooked spicule in males, and a more posteriorly positioned vulva in female. Presence of plural species of non- Enterobius pinworms is a remarkable feature of the orangutan-pinworm relationship, which may reflect speciation process of the orangutans, host switching, and coevolution by pinworms.

Feeding ecology of Bornean orangutans (Pongo pygmaeus morio) in Danum Valley, Sabah, Malaysia: a 3-year record including two mast fruitings.

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.

Reproductive parameters over a 37-year period of free-ranging female Borneo orangutans at Sepilok Orangutan Rehabilitation Centre.

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.

Developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus): possible signals in visual communication.

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.