Social tolerance and interactional opportunities as drivers of gestural redoings in orang-utans.

Communicative repair is a fundamental and universal element of interactive language use. It has been suggested that the persistence and elaboration after communicative breakdown in nonhuman primates constitute two evolutionary building blocks of this capacity, but the conditions favouring it are poorly understood. Because zoo-housed individuals of some species are more social and more terrestrial than in the wild, they should be more likely to show gestural redoings (i.e. both repetition and elaboration) after communicative failure in the coordination of their joint activities. Using a large comparative sample of wild and zoo-housed orang-utans of two different species, we could confirm this prediction for elaboration, the more flexible form of redoings. Specifically, results showed that gestural redoings in general were best predicted by the specific social action context (i.e. social play) and interaction dyad (i.e. beyond mother-offspring), although they were least frequent in captive Bornean orang-utans. For gestural elaboration, we found the expected differences between captive and wild research settings in Borneans, but not in Sumatrans (the more socially tolerant species). Moreover, we found that the effectiveness of elaboration in eliciting responses was higher in Sumatrans, especially the captive ones, whereas effectiveness of mere repetition was influenced by neither species nor setting. We conclude that the socio-ecological environment plays a central role in the emergence of communicative repair strategies in great apes. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

The role of great ape behavioral ecology in One Health: Implications for captive welfare and re-habilitation success.

Behavior is the interface through which animals interact with their environments, and therefore has potentially cascading impacts on the health of individuals, populations, their habitats, and the humans that share them. Evolution has shaped the interaction between species and their environments. Thus, alterations to the species-typical "wild-type" behavioral repertoire (and the ability of the individual to adapt flexibly which elements of the repertoire it employs) may disrupt the relationship between the organism and its environment, creating cascading One Health effects. A good example is rehabilitant orangutans where, for example, seemingly minor differences from wild conspecifics in the time spent traveling on the ground rather than in the forest canopy can affect an individual's musculoskeletal and nutritional health, as well as social integration. It can also increase two-way transmission of infectious diseases and/or pathogens with local human populations, or potentially with neighboring wild populations if there are no geographical barriers and rehabilitants travel far enough to leave their release area. Primates are well known ecosystem engineers, reshaping plant communities and maintaining biodiversity through seed dispersal, consuming plants, and creating canopy gaps and trails. From the habitat perspective, a rehabilitant orangutan which does not behave like a wild orangutan is unlikely to fulfill these same ecosystem services. Despite the importance of the diversity of an ape's behavioral repertoire, how it compares to that of wild conspecifics and how it alters in response to habitat variation, behavior is an often under-appreciated aspect of One Health. In this review, focusing on orangutans as an example of the kinds of problems faced by all captive great apes, we examine the ways in which understanding and facilitating the expression of wild-type behavior can improve their health, their ability to thrive, and the robustness of local One Health systems.

Wild Bornean orangutans experience muscle catabolism during episodes of fruit scarcity.

Pronounced temporal and spatial variation in the availability of food resources can produce energetic deficits in organisms. Fruit-dependent Bornean orangutans face extreme variation in fruit availability and experience negative energy and protein balance during episodes of fruit scarcity. We evaluate the possibility that orangutans of different sexes and ages catabolize muscle tissue when the availability of fruit is low. We assess variation in muscle mass by examining the relationship between urinary creatinine and specific gravity and use the residuals as a non-invasive measure of estimated lean body mass (ELBM). Despite orangutans having a suite of adaptations to buffer them from fruit scarcity and associated caloric deficits, ELBM was lower during low fruit periods in all age-sex classes. As predicted, adult male orangutans had higher ELBM than adult females and immatures. Contrary to expectation, flanged and unflanged males did not differ significantly in ELBM. These findings highlight the precarity of orangutan health in the face of rapid environmental change and add to a growing body of evidence that orangutans are characterized by unique metabolic traits shaped by their unpredictable forest environment.

Wild Bornean orangutan (Pongo pygmaeus wurmbii) feeding rates and the Marginal Value Theorem.

The Marginal Value Theorem (MVT) is an integral supplement to Optimal Foraging Theory (OFT) as it seeks to explain an animal's decision of when to leave a patch when food is still available. MVT predicts that a forager capable of depleting a patch, in a habitat where food is patchily distributed, will leave the patch when the intake rate within it decreases to the average intake rate for the habitat. MVT relies on the critical assumption that the feeding rate in the patch will decrease over time. We tested this assumption using feeding data from a population of wild Bornean orangutans (Pongo pygmaeus wurmbii) from Gunung Palung National Park. We hypothesized that the feeding rate within orangutan food patches would decrease over time. Data included feeding bouts from continuous focal follows between 2014 and 2016. We recorded the average feeding rate over each tertile of the bout, as well as the first, midpoint, and last feeding rates collected. We did not find evidence of a decrease between first and last feeding rates (Linear Mixed Effects Model, n = 63), between a mid-point and last rate (Linear Mixed Effects Model, n = 63), between the tertiles (Linear Mixed Effects Model, n = 63), nor a decrease in feeding rate overall (Linear Mixed Effects Model, n = 146). These findings, thus, do not support the MVT assumption of decreased patch feeding rates over time in this large generalist frugivore.

Low relationship quality predicts scratch contagion during tense situations in orangutans (Pongo pygmaeus).

Primates show various forms of behavioral contagion that are stronger between kin and friends. As a result, behavioral contagion is thought to promote group coordination, social cohesion, and possibly state matching. Aside from contagious yawning, little is known about the contagious effect of other behaviors. Scratching is commonly observed during arousal and as such may play a role within group dynamics. While the Bornean orangutan (Pongo pygmaeus) is commonly considered the least social great ape, orangutans do engage in social interactions. Therefore, their social organization makes them a suitable case for studying the social function of behavioral contagion. Through behavioral observations of captive orangutans, we recorded all yawn and scratch events together with the corresponding behavior of all bystander group-members. As yawning was rarely observed, no conclusions could be drawn regarding this behavior. Scratching was contagious and occurred within 90 s after the triggering scratch. Specifically, orangutans showed increased scratch contagion when they had seen a weakly bonded individual scratch during tense contexts. When the orangutan had not seen the triggering scratch, the contagiousness of scratching was not affected by context or relationship quality. Our results indicate that behavioral contagion is not simply higher between individuals with stronger social relationships, but that the contagiousness of behaviors may vary based on the context and on social factors. We discuss these findings in light of an adaptive function that may reduce aggression.

Sociosexual behavioral patterns involving nulliparous female orangutans (Pongo sp.) reflect unique challenges during the adolescent period.

The primate adolescent period is characterized by a series of changes in physiology, behavior, and social relationships. Orangutans have the slowest life history and the longest period of dependency of all primates. As members of a semisolitary species with high levels of sexual coercion, adolescent female orangutans face a unique combination of challenges when achieving independence from their mother. This study examined the mating behavior of adolescent female orangutans and compared it with that of adult females to assess whether mating behavior reflects distinct strategies at these different points in the life cycle. Data were collected in Gunung Palung National Park on the island of Borneo over 20 years. Mating events from adolescent (n = 19) and adult females (n = 26) were scored and compared. Adolescent female mating events had significantly higher mating scores (indicating more proceptivity) than those of adult females (ß = 1.948, p = .001). Adolescent females also engaged in elaborate sociosexual interactions with different flanged males, behaviors that were never observed during mating events of adult females. These interactions involved characteristic behavior on the part of both the adolescent females and the flanged males. Given these findings and the documentation of similar accounts of adolescent female-flanged male mating from the island of Sumatra, we propose that adolescent female orangutans display distinctive behavioral repertoires throughout the genus Pongo which serves to overcome male ambivalence toward nulliparous females, establish familiarity, and evaluate coercive tendencies in flanged males. We suggest that these behavioral patterns are an integral part of female social development in a female philopatric, but highly dispersed species where consistent social support is absent after ranging independence is achieved.

Developmental changes in the endocrine stress response in orangutans (Pongo pygmaeus).

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.

Changes to Sabah's orangutan population in recent times: 2002-2017.

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.

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.

Population estimates of Bornean orang-utans using Bayesian analysis at the greater Batang Ai-Lanjak-Entimau landscape in Sarawak, Malaysia.

The integration of Bayesian analysis into existing great ape survey methods could be used to generate precise and reliable population estimates of Bornean orang-utans. We used the Marked Nest Count (MNC) method to count new orang-utan nests at seven previously undocumented study sites in Sarawak, Malaysia. Our survey teams marked new nests on the first survey and revisited the plots on two more occasions; after about 21 and 42 days respectively. We used the N-mixture models to integrate suitability, abundance and detection models which account for zero inflation and imperfect detection for the analysis. The result was a combined estimate of 355 orang-utans with the 95% highest density interval (HDI) of 135 to 602 individuals. We visually inspected the posterior distributions of our parameters and compared precisions between study sites. We subsequently assess the strength or reliability of the generated estimates using identifiability tests. Only three out of the seven estimates had <35% overlap to indicate strong reliability. We discussed the limitations and advantages of our study design, and made recommendations to improve the sampling scheme. Over the course of this research, two of the study sites were gazetted as extensions to the Lanjak-Entimau Wildlife Sanctuary for orang-utan conservation.

Stillbirth rates across three ape species in accredited American zoos.

Stillbirths, or births of infants that died in the womb, represent a failure of the materno-feto-placental unit to maintain a suitable fetal environment. Typical studies of nonhuman primate (NHP) stillbirth patterns are primarily descriptive and focus on macaques (genus Macaca). Thus, less is known about other NHP species and rarer still are studies that examine possible biological factors that influence stillbirth rates across taxa. To examine possible contributors to stillbirths in great apes, we analyzed 36 years (1980-2016) of historical data documenting births of zoo-housed chimpanzees (Pan troglodytes, N = 391), western lowland gorillas (Gorilla gorilla gorilla, N = 491), and orangutans (Pongo spp, N = 307) in accredited zoological parks in the United States. The average number of births for each of the 446 mothers was 2.7, resulting in a total of 1,189 births with 143 stillbirths (12%). Stillbirths represented 12% of chimpanzee births, 13% of gorilla births, and 10% of orangutan births. We used generalized linear mixed-effects models to assess possible relationships between stillbirth likelihood and mother origin (wild- versus captive-born), age, and genus. Across taxa, older mothers were more likely to have a stillbirth (p = 0.004). While these results are likely influenced by both biological and management-related factors (e.g., selective captive breeding), they may be useful to population managers in evaluating pregnancy risks for great apes. Captive settings and archival studbook data such as these may provide a unique opportunity to further explore this topic.

Wildfire smoke impacts activity and energetics of wild Bornean orangutans.

Indonesia's peatlands experience frequent and intense wildfires, producing hazardous smoke with consequences for human health, yet there is a lack of research into adverse effects on wildlife. We evaluated the effects of smoke on the activity and energy balance of Bornean orangutans (Pongo pygmaeus wurmbii) in a peat swamp forest at the Tuanan Research Station, Central Kalimantan. We collected behavioural data and urine samples from four adult flanged males before, during, and after wildfires between March 2015 and January 2016. During fires, particulate matter (PM10) concentrations were hazardous. Orangutans increased rest time during and after the smoke period, and decreased travel time and distance and increased fat catabolism post-smoke. The increase in post-smoke ketones was not related to changes in caloric intake and was likely due to an increase in energy expenditure, possibly related to immune response. Results show that wildfire smoke negatively affects orangutan condition, and sustained research is needed to assess the magnitude of the threat to the long-term viability of this Critically Endangered species.

Reproductive success of two male morphs in a free-ranging population of Bornean orangutans.

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.

Behavioral studies and veterinary management of orangutans at Bukit Merah Orang Utan Island, Perak, Malaysia.

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.

Global Demand for Natural Resources Eliminated More Than 100,000 Bornean Orangutans.

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.

Cyclical nursing patterns in wild orangutans.

Nursing behavior is notoriously difficult to study in arboreal primates, particularly when offspring suckle inconspicuously in nests. Orangutans have the most prolonged nursing period of any mammal, with the cessation of suckling (weaning) estimated to occur at 6 to 8 years of age in the wild. Milk consumption is hypothesized to be relatively constant over this period, but direct evidence is limited. We previously demonstrated that trace element analysis of bioavailable elements from milk, such as barium, provides accurate estimates of early-life diet transitions and developmental stress when coupled with growth lines in the teeth of humans and nonhuman primates. We provide the first detailed nursing histories of wild, unprovisioned orangutans (Pongo abelii and Pongo pygmaeus) using chemical and histological analyses. Laser ablation inductively coupled plasma mass spectrometry was used to determine barium distributions across the teeth of four wild-shot individuals aged from postnatal biological rhythms. Barium levels rose during the first year of life in all individuals and began to decline shortly after, consistent with behavioral observations of intensive nursing followed by solid food supplementation. Subsequent barium levels show large sustained fluctuations on an approximately annual basis. These patterns appear to be due to cycles of varying milk consumption, continuing until death in an 8.8-year-old Sumatran individual. A female Bornean orangutan ceased suckling at 8.1 years of age. These individuals exceed the maximum weaning age reported for any nonhuman primate. Orangutan nursing may reflect cycles of infant demand that relate to fluctuating resource availability.

Orientation toward humans predicts cognitive performance in orang-utans.

Non-human animals sometimes show marked intraspecific variation in their cognitive abilities that may reflect variation in external inputs and experience during the developmental period. We examined variation in exploration and cognitive performance on a problem-solving task in a large sample of captive orang-utans (Pongo abelii &P. pygmaeus, N = 103) that had experienced different rearing and housing conditions during ontogeny, including human exposure. In addition to measuring exploration and cognitive performance, we also conducted a set of assays of the subjects' psychological orientation, including reactions towards an unfamiliar human, summarized in the human orientation index (HOI), and towards novel food and objects. Using generalized linear mixed models we found that the HOI, rather than rearing background, best predicted both exploration and problem-solving success. Our results suggest a cascade of processes: human orientation was accompanied by a change in motivation towards problem-solving, expressed in reduced neophobia and increased exploration variety, which led to greater experience, and thus eventually to higher performance in the task. We propose that different experiences with humans caused individuals to vary in curiosity and understanding of the physical problem-solving task. We discuss the implications of these findings for comparative studies of cognitive ability.

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.