Wild Orangutans Research Articles

Observational learning in orangutan cultural transmission chains

Field reports suggest that orangutans acquire local traditions by observing neighbouring conspecifics. However, there is little direct evidence of social learning to support this conclusion. The present study investigated whether orangutans would learn a novel foraging method through observation of a conspecific in a diffusion-chain paradigm testing for the spread of the behaviour. A foraging box with two possible methods for extracting food was used to investigate the transmission of a foraging tradition among zoo-living subjects. In a socially housed group of five orangutans, the dominant male was trained to use one technique exclusively to retrieve food. He then performed this technique in the presence of another group member, who was then allowed to forage. After several trials, the observer became the model for the next individual. A second experimental group of six individuals was introduced to the alternative method. The model-seeded technique was successfully transmitted along both experimental chains, with significant preferences for the model method. These results are consistent with claims for social transmission of foraging methods in wild orangutans.

Diet traditions in wild orangutans

This study explores diet differences between two populations of wild Bornean orangutans (Pongo pygmaeus wurmbii) to assess whether a signal of social learning can be detected in the observed patterns. The populations live in close proximity and in similar habitats but are separated by a river barrier that is impassable to orangutans in the study region. We found a 60% between-site difference in diet at the level of plant food items (plant species-organ combinations). We also found that individuals at the same site were more likely to eat the same food items than expected by chance. These results suggest the presence of diet (food selection) traditions. Detailed tests of three predictions of three models of diet acquisition allowed us to reject a model based on exclusive social learning but could not clearly distinguish between the remaining two models: one positing individual exploration and learning of food item selection and the other one positing preferential social learning followed by individual fine tuning. We know that maturing orangutans acquire their initial diet through social learning and then supplement it by years of low-level, individual sampling. We, therefore, conclude that the preferential social learning model produces the best fit to the geographic patterns observed in this study. However, the very same taxa that socially acquire their diets as infants and show evidence for innovation-based traditions in the wild paradoxically may have diets that are not easily distinguished from those acquired exclusively through individual learning.

A possible case of hantavirus infection in a Borneo orangutan and its conservation implication

Natural infection of hantavirus in orangutans has never been reported. Enzyme-linked immunosorbent assays (ELISA), Indirect immunofluorescence assay (IFA), and RT-PCR were used to diagnosis a suspected case in a pet orangutan in southern Taiwan. Although the RT-PCR result was negative, the high IgG titer in the beginning and its dramatic drop after treatments suggested a recent Seoul-type hantavirus infection. Hantavirus transmission and its potential damage to wild orangutans should not be overlooked.

Adaptation to Forest Life During the Reintroduction Process of Immature Pongo abelii

Reintroduction of Sumatran orangutans can be an important tool to conserve the species in the face of the current decline of wild populations. Monitoring ex-captive orangutans during the reintroduction process provides insight into their adaptation to forest life and is important for evaluating the success of such programs. We investigated activity patterns, food choice, height use, and nest-building abilities of 8 immature orangutans at a reintroduction station in Sumatra. All focal individuals spent most of their time in the forest feeding, but at a lower proportion than wild conspecifics. Among the focal individuals, the behavior of orangutans that avoided human contact differed in several aspects from those that were human bonded. Their diet was composed mainly of fruits, similar to the food choice of wild orangutans, and their ground-avoidance and superior nest-building abilities indicated more effective predation-avoidance behavior vs. that of human-bonded animals. Finally, these immatures showed regular social contact with more experienced conspecifics, which ultimately may facilitate the social learning of local feral expertise. Human-bonded individuals, in contrast, preferentially stayed on the ground and at low heights and rarely built nests, thereby increasing predation risk. Their choice of leaves over fruits as foods indicated a less effective foraging strategy. Nevertheless, this group exhibited individual learning trends toward an adult-like foraging pattern and height use. We conclude that social interactions with conspecifics and humans, especially during an early developmental period, can affect adaptation to forest life and probably also influence the success of orangutan reintroduction processes.

Modelling ranging behaviour of female orang-utans: a case study in Tuanan, Central Kalimantan, Indonesia

Quantification of the spatial needs of individuals and populations is vitally important for management and conservation. Geographic information systems (GIS) have recently become important analytical tools in wildlife biology, improving our ability to understand animal movement patterns, especially when very large data sets are collected. This study aims at combining the field of GIS with primatology to model and analyse space-use patterns of wild orang-utans. Home ranges of female orang-utans in the Tuanan Mawas forest reserve in Central Kalimantan, Indonesia were modelled with kernel density estimation methods. Kernel results were compared with minimum convex polygon estimates, and were found to perform better, because they were less sensitive to sample size and produced more reliable estimates. Furthermore, daily travel paths were calculated from 970 complete follow days. Annual ranges for the resident females were approximately 200 ha and remained stable over several years; total home range size was estimated to be 275 ha. On average, each female shared a third of her home range with each neighbouring female. Orang-utan females in Tuanan built their night nest on average 414 m away from the morning nest, whereas average daily travel path length was 777 m. A significant effect of fruit availability on day path length was found. Sexually active females covered longer distances per day and may also temporarily expand their ranges.

An evaluation of the geographic method for recognizing innovations in nature, using zoo orangutans

Innovation and social learning are the raw materials for traditions and culture. Of these two, innovation has received far less scrutiny, largely because of difficulties assessing the innovation status of behaviors. A recent attempt proposes recognition of innovations in natural populations based on assessment of the behavior's properties and its geographic and local prevalence. Here we examine the validity of this approach and the list of 43 potential innovations it generated for wild orangutans by extending the comparison to zoo orangutans. First, we created an inventory of the behavioral repertoire in the zoo population. Four of ten putative innovations recognized in the field and potentially present in captivity did not occur despite appropriate conditions, suggesting they are indeed innovations. Second, we experimentally produced relevant conditions to evaluate whether another five potential innovations could be elicited. Based on their continued absence or on their latencies relative to known behaviors, four of the potential innovations could be assessed as innovations and one as a modification. Because 53% of relevant innovations recognized in the field could be confirmed in this analysis, and another 27% assigned possible innovation status, we conclude that the geographic method for detecting innovation in the wild is valid. However, the experiments also yielded up to 13 additional innovations, suggesting that zoo orangutans are far more innovative than wild ones. We discuss the implications of this latter finding with regard to limiting factors for the expansion of cultural repertoires in wild orangutans.

Orangutans

Orangutans

Female reproductive strategies in orangutans, evidence for female choice and counterstrategies to infanticide in a species with frequent sexual coercion.

Intersexual conflicts over mating can engender antagonistic coevolution of strategies, such as coercion by males and selective resistance by females. Orangutans are exceptional among mammals for their high levels of forced copulation. This has typically been viewed as an alternative mating tactic used by the competitively disadvantaged unflanged male morph, with little understanding of how female strategies may have shaped and responded to this behaviour. Here, we show that male morph is not by itself a good predictor of mating dynamics in wild Bornean orangutans but that female conception risk mediated the occurrence and quality of male-female interactions. Near ovulation, females mated cooperatively only with prime flanged males who they encountered at higher rates. When conception risk was low, willingness to associate and mate with non-prime males increased. Our results support the hypothesis that, together with concealed ovulation, facultative association is a mechanism of female choice in a species in which females can rarely avoid coercive mating attempts. Female resistance, which reduced copulation time, may provide an additional mechanism for mate selection. However, coercive factors were also important as prime males were frequently aggressive to females and females used mating strategies consistent with infanticide avoidance.

Social learning of diet and foraging skills by wild immature Bornean orangutans: implications for culture

Studies of social learning in the wild are important to complement findings from experiments in captivity. In this field study, immature Bornean orangutans rarely foraged independently but consistently followed their mothers' choices. Their diets were essentially identical to their mothers' even though not all mothers had the same diet. This suggests vertical transmission of diet by enhancement. Also, immatures selectively observed their mothers during extractive foraging, which increased goal-directed practice but not general manipulation of similar objects, suggesting observational forms of learning of complex skills. Teaching was not observed. These results are consistent with the reported presence of food traditions and skill cultures in wild orangutans. We suggest that food traditions can develop wherever association commonly allows for social learning. However, the capacity for observational learning, and thus more complex culture, is more likely to evolve among extractive foragers with prolonged association between adults and immatures.

Intestinal parasites of endangered orangutans(Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia

Faecal samples from 163 captive and semi-captive individuals, 61 samples from wild individuals and 38 samples from captive groups of Bornean orangutans (Pongo pygmaeus) in Kalimantan, Indonesia, were collected during one rainy season (November 2005-May 2006) and screened for intestinal parasites using sodium acetate-acetic acid-formalin-concentration (SAFC), sedimentation, flotation, McMaster- and Baermann techniques. We aimed to identify factors influencing infection risk for specific intestinal parasites in wild orangutans and individuals living in captivity. Various genera of Protozoa (including Entamoeba, Endolimax, Iodamoeba, Balantidium, Giardia and Blastocystis), nematodes (such as Strongyloides, Trichuris, Ascaris, Enterobius, Trichostrongylus and hookworms) and one trematode (a dicrocoeliid) were identified. For the first time, the cestode Hymenolepis was detected in orangutans. Highest prevalences were found for Strongyloides (individuals 37%; groups 58%), hookworms (41%; 58%), Balantidium (40%; 61%), Entamoeba coli (29%; 53%) and a trichostrongylid (13%; 32%). In re-introduction centres, infants were at higher risk of infection with Strongyloides than adults. Infection risk for hookworms was significantly higher in wild males compared with females. In groups, the centres themselves had a significant influence on the infection risk for Balantidium. Ranging patterns of wild orangutans, overcrowding in captivity and a shift of age composition in favour of immatures seemed to be the most likely factors leading to these results.

Tool use in wild orang-utans modifies sound production: a functionally deceptive innovation?

Culture has long been assumed to be uniquely human but recent studies, in particular on great apes, have suggested that cultures also occur in non-human primates. The most apparent cultural behaviours in great apes involve tools in the subsistence context where they are clearly functional to obtain valued food. On the other hand, tool-use to modify acoustic communication has been reported only once and its function has not been investigated. Thus, the question whether this is an adaptive behaviour remains open, even though evidence indicates that it is socially transmitted (i.e. cultural). Here we report on wild orang-utans using tools to modulate the maximum frequency of one of their sounds, the kiss squeak, emitted in distress. In this variant, orang-utans strip leaves off a twig and hold them to their mouth while producing a kiss squeak. Using leaves as a tool lowers the frequency of the call compared to a kiss squeak without leaves or with only a hand to the mouth. If the lowering of the maximum frequency functions in orang-utans as it does in other animals, two predictions follow: (i) kiss squeak frequency is related to body size and (ii) the use of leaves will occur in situations of most acute danger. Supporting these predictions, kiss squeaks without tools decreased with body size and kiss squeaks with leaves were only emitted by highly distressed individuals. Moreover, we found indications that the calls were under volitional control. This finding is significant for at least two reasons. First, although few animal species are known to deceptively lower the maximum frequency of their calls to exaggerate their perceived size to the listener (e.g. vocal tract elongation in male deer) it has never been reported that animals may use tools to achieve this, or that they are primates. Second, it shows that the orang-utan culture extends into the communicative domain, thus challenging the traditional assumption that primate calling behaviour is overall purely emotional.

Why male orangutans do not kill infants.

Infanticide is widespread among mammals, is particularly common in primates, and has been shown to be an adaptive male strategy under certain conditions. Although no infanticides in wild orangutans have been reported to date, several authors have suggested that infanticide has been an important selection pressure influencing orangutan behavior and the evolution of orangutan social systems. In this paper, we critically assess this suggestion. We begin by investigating whether wild orangutans have been studied for a sufficiently long period that we might reasonably expect to have detected infanticide if it occurs. We consider whether orangutan females exhibit counterstrategies typically employed by other mammalian females. We also assess the hypothesis that orangutan females form special bonds with particular “protector males” to guard against infanticide. Lastly, we discuss socioecological reasons why orangutan males may not benefit from infanticide. We conclude that there is limited evidence for female counterstrategies and little support for the protector male hypothesis. Aspects of orangutan paternity certainty, lactational amenorrhea, and ranging behavior may explain why infanticide is not a strategy regularly employed by orangutan males on Sumatra or Borneo.

Captive and wild orangutan (Pongo sp.) survivorship: a comparison and the influence of management

For managers of captive populations it is important to know whether their management provides a species with the physical and social environment that maximizes its survivorship. To determine this, survivorship comparisons with wild populations and long-term evaluations of captive populations are important. Here we provide both for orangutans. We show that survivorship has increased during the past 60 years for captive orangutan populations in zoos. In addition, we show that survivorship of captive orangutans in the past used to be lower than for wild orangutans, but that for recently born (1986-2005) orangutans survivorship is not significantly different from the wild. This indicates that captive management in the past was suboptimal for orangutan survivorship, but that modern management of captive orangutans has increased their survivorship. We discuss the possible factors of modern management that could have influenced this.

Circadian long call distribution in wild orangutans

We present first data on circadian long call distribution of wild orangutans in Northwest Borneo. Data were collected during two months in Batang Ai National Park. A total of 151 male long calls were heard, exhibiting a bimodal distribution pattern with peaks at 05:00-06:00 hours and 18:00-19:00 hours. An earlier study found pronounced differences between the calling rates of Bornean orangutans, which showed an almost unimodal call distribution with its peak at mid-morning, and those of Sumatran orangutans, which showed a bimodal call distribution with a distinct calling peak at predawn and a more moderate peak near dusk (MacKinnon 1974). Our findings from Batang Ai resemble more closely the pattern reported for Sumatra than those reported for other Bornean localities and, therefore, contradict earlier reports suggesting a Sumatra-Borneo dichotomy in orangutan call distribution. In addition, orangutans in Batang Ai were heard to regularly emit long calls throughout the night. This behaviour is unusual for a diurnal species.

Interactions between zoo‐housed great apes and local wildlife

Although there are published reports of wild chimpanzees, bonobos, and orangutans hunting and consuming vertebrate prey, data pertaining to captive apes remain sparse. In this survey-based study, we evaluate the prevalence and nature of interactions between captive great apes and various indigenous wildlife species that range into their enclosures in North America. Our hypotheses were threefold: (a) facilities housing chimpanzees will report the most frequent and most aggressive interactions with local wildlife; (b) facilities housing orangutans and bonobos will report intermediate frequencies of these interactions with low levels of aggression and killing; and (c) facilities housing gorillas will report the lowest frequency of interactions and no reports of killing local wildlife. Chimpanzees and bonobos demonstrated the most aggressive behavior toward wildlife, which matched our predictions for chimpanzees, but not bonobos. This fits well with expectations for chimpanzees based on their natural history of hunting and consuming prey in wild settings, and also supports new field data on bonobos. Captive gorillas and orangutans were reported to be much less likely to chase, catch and kill wildlife than chimpanzees and bonobos. Gorillas were the least likely to engage in aggressive interactions with local wildlife, matching our predictions based on natural history. However unlike wild gorillas, captive gorillas were reported to kill (and in one case, eat) local wildlife. These results suggest that some behavioral patterns seen in captive groups of apes may be useful for modeling corresponding activities in the wild that may not be as easily observed and quantified. Furthermore, the data highlight the potential for disease transmission in some captive settings, and we outline the associated implications for ape health and safety.

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.

Begging for information: mother–offspring food sharing among wild Bornean orangutans

Transfer of solid food from mothers or other adults to dependent offspring is commonly observed in various primate species and both nutritional and informational benefits have been proposed to explain the function of such food sharing. Predictions from these hypotheses are tested using observational data on wild orangutans (Pongo pygmaeus wurmbii) at Tuanan, Central Borneo, Indonesia. In 1,145 hr of focal observation and 458 recorded food interactions between four pairs of females with offspring it was found that virtually all transfers were initiated by the offspring and that younger infants solicited food more often and did so for a greater variety of items than older offspring. All offspring primarily solicited food that was difficult to process, i.e., inaccessible to them. Furthermore, the amount of food solicitation was negatively correlated with ecological competence. Hence food sharing seemed to be related to an offspring's skill level, as suggested by the informational hypothesis. In contrast, offspring did not solicit high-quality items more than low-quality items and food sharing did not peak around the age of weaning, as predicted by the nutritional hypothesis. Mothers were usually passively tolerant, allowing offspring to take food but hardly ever provisioned. Parent-offspring conflict concerning food sharing was only observed well after weaning. Thus, by taking food directly from the mother, young orangutans were able to obtain information about the affordances and nutritional value of food items that were otherwise out of their reach and could familiarize themselves with the mother's diet. In species such as orangutans or other apes, characterized by a broad diet that requires extractive foraging, informational food transfer may be vital for an immature to acquire complex feeding skills and adult diet.

Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans

Assessment of energetic condition is a critical tool for behavioral and reproductive ecologists. However, accurate quantification of energy intake and expenditure is labor-intensive, and it can be problematic for field scientists to obtain regular data on individual animals. C-peptide, a polypeptide segment of the proinsulin molecule that is secreted along with insulin in an equimolar relationship, can be measured in urine, and thus offers a potential means for the non-invasive assessment of energy balance in wild animals. Here, we validate C-peptide for the quantification of energetic condition, with specific application to wild orangutans ( Pongo pygmaeus). We determined that application of urine to filter paper results in significantly lower C-peptide recoveries versus fresh samples. However, concentrations in filter paper samples were significantly correlated with fresh urine and were stable over various storage conditions and durations. We compared the C-peptide concentrations from wild orangutan urine samples with three independent measures of energetic condition: ketone bodies (urinalysis), caloric intake (nutritional biochemistry), and food availability (phenology). As expected, C-peptide concentrations were significantly lower in samples that tested positive for ketones in the field. Monthly average C-peptide concentrations of both male and female orangutans were significantly correlated with monthly determinations of energy intake and food availability. Therefore, we conclude that the collection and preservation of urine samples for C-peptide analysis are feasible under most field conditions and, in this species, presents a useful tool for assessing changes in energy balance.

Limb use and preferences in wild orang‐utans during feeding and locomotor behavior

Limited data are available on hemispheric lateralization in wild orang-utans. There has been only one previous investigation of limb preferences in wild orang-utans [Yeager, 1991]. We examined the lateralization of limb use in wild Bornean orang-utans (Pongo pygmaeus pygmaeus) with the aim of providing more insight into possible hemispheric specialization in wild nonhuman primates. Here, we report in detail on limb use and preference during arboreal locomotion between trees (N=6) and on feeding involving one limb (N=8) and two limbs (N=6). We distinguished between locomotion between overlapping trees (Type I) and locomotion involving gap crossing (Types II and III). For locomotion Type I, the six orang-utans showed no leading hand preference, however for locomotion Types II and III, all six showed significant right-hand preferences. All eight orang-utans showed individual hand preferences for reaching for food, but no significant group bias was found. Limb preferences for feeding involving two limbs (hand-hand or hand-foot) differed between juveniles (right hand-right foot), adult females (left hand-right hand) and adult males (right hand-left hand). Although not present for all tasks, the results indicate that orang-utans do show evidence of hemispheric specialization, but the use of the hands is not under a strong lateralized hemispheric control and is adaptable.

Potential applications of urinary C‐peptide of insulin for comparative energetics research

The study of comparative energetics offers a valuable way to identify broad ecological principles and assess the functional significance of energetic adaptations during the course of evolution. Yet, the quantification of energetic status for nonhuman primates under natural conditions remains one of the most challenging aspects of comparative energetics research. Here, we report on the development of a noninvasive field method for measuring energetic status in great apes, humans, and possibly other nonhuman primates. Specifically, we have explored measurement of a urinary metabolite of insulin (C-peptide) as a physiological marker of energetic condition in chimpanzees and orangutans. We performed three validation studies and successfully measured C-peptide in urine samples from captive chimpanzees, wild chimpanzees, and wild orangutans. Urinary C-peptide measures gave indications of being a reliable signal of energetic status in both species. For chimpanzees and orangutans in the wild, baseline urinary C-peptide levels were higher during periods of fruit abundance than periods of low fruit availability. Urinary C-peptide levels were also higher for well-fed captive chimpanzees compared with wild chimpanzees. Although sample size was small, top-ranking male chimpanzees showed higher C-peptide levels in the wild than low-ranking males only during the period of fruit abundance. These preliminary results indicate that further development of the urinary C-peptide method could expand opportunities to quantify energetic condition for great apes in the wild and generate new data for comparative research. We highlight specific applications for studying great ape reproduction as well as the nutritional ecology of human foragers.