Orangutan pantomime: elaborating the message

We present an exploratory study of forest-living orangutan pantomiming, i.e. gesturing in which they act out their meaning, focusing on its occurrence, communicative functions, and complexities. Studies show that captive great apes may elaborate messages if communication fails, and isolated reports suggest that great apes occasionally pantomime. We predicted forest-living orangutans would pantomime spontaneously to communicate, especially to elaborate after communication failures. Mining existing databases on free-ranging rehabilitant orangutans'' behaviour identified 18 salient pantomimes. These pantomimes most often functioned as elaborations of failed requests, but also as deceptions and declaratives. Complexities identified include multimodality, re-enactments of past events and several features of language (productivity, compositionality, systematicity). These findings confirm that free-ranging rehabilitant orangutans pantomime and use pantomime to elaborate on their messages. Further, they use pantomime for multiple functions and create complex pantomimes that can express propositionally structured content. Thus, orangutan pantomime serves as a medium for communication, not a particular function. Mining cases of complex great ape communication originally reported in functional terms may then yield more evidence of pantomime.     

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.     

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.     

Return of the Native: Cognition and Site-Specific Expertise in Orangutan Rehabilitation

Ex-captive orangutans that have returned to free forest life in Bornean forests offer exceptional opportunities to assess the cognitive challenges facing feral great apes. They also provide opportunities to track readaptation, which requires building expertise to survive in tropical rain forests and to integrate into orangutan communities. I outline some of the foraging problems that ex-captive orangutans encounter, the cognitive processes used in their solutions, and acquisition patterns. Evidence derives primarily from observational studies of feeding behavior in free-ranging ex-captives. Discussion focuses on implications for conservation initiatives.     

A Noninvasive Method for Estimating Nitrogen Balance in Free-Ranging Primates

The vital role of body protein as an energy reserve has received little focus in studies of wild primates. Owing to the relatively low protein content of fruit, some frugivorous primates could face a protein deficit if body protein is catabolized for energy during periods of low fruit availability. Such an imbalance can be detected if fatty acids, amino acids, and nitrogen (N) catabolites are reincorporated or recycled back to tissues. Here we describe a method to quantify protein recycling by measuring standardized urea concentration and N isotope signatures from urine samples collected from wild Bornean orangutans (Pongo pygmaeus wurmbii). Our overall goal was to explore if concentrations of urea and ??¹⁵N values could be used as indicators of the amount of protein consumed and the degree of protein recycling, respectively, in wild, free-ranging primates. We examine the relationships between urea concentration, ??¹⁵N values, protein intake, and fruit availability. Urea concentration increased with fruit availability, reflecting a slight increase in protein consumption when fruit was abundant. However, we found no relationship between ??¹⁵N values and fruit availability, suggesting that orangutans avert a negative protein balance during periods of low fruit availability. These noninvasive methods complement recent advances in primate energy balance research and will contribute to our understanding of adaptations of primates during periods of fruit shortage.     

Behavioral differences as predictors of breeding status in captive cheetahs

Individual behavioral variation of 44 adult captive‐born cheetahs, Acinonyx jubatus, was assessed using observer and keeper ratings on a variety of behavioral attributes. Inter‐rater consensus was high for most questionnaire items, several of which were significantly correlated with direct behavioral measures recorded in a mirror‐image experiment. Principal component analysis was applied to identify patterns of individual variation as measured by observer and keeper ratings. Three major components, labeled as tense‐fearful, excitable‐vocal, and aggressive, accounted for 69% of the observed variation. Females showed significantly higher scores on the component tense‐fearful than males. Non‐breeders of both sexes scored significantly higher on the component tense‐fearful than breeders. Assessment of individual behavioral variation through questionnaire ratings may therefore provide a simple and non‐invasive tool for predicting an individual's ability to adjust to the constraints of certain husbandry regimens and to reproduce in captivity. Simple measures of behavioral attributes may offer new insights for solving breeding problems and improving conservation management of endangered species in captivity. Zoo Biol 18:335–349, 1999. © 1999 Wiley‐Liss, Inc.     

Methods for Studying the Ecological Physiology of Feeding in Free-Ranging Howlers (Alouatta palliata) at La Pacifica, Costa Rica

We lack a general understanding of how primates perform physiologically during feeding to cope with the challenges of their natural environments. We here discuss several methods for studying the ecological physiology of feeding in mantled howlers (Alouatta palliata) at La Pacifica, Costa Rica. Our initial physiological effort focuses on recording electromyographic activity (EMG) from the jaw muscles in free-ranging howlers while they feed in their natural forest habitat. We integrate these EMG data with measurements of food material properties, dental wear rates, as well as spatial analyses of resource use and food distribution. Future work will focus on incorporating physiological measures of bone deformation, i.e., bone strain; temperatures; food nutritional data; and hormonal analyses. Collectively, these efforts will help us to better understand the challenges that howlers face in their environment and the physiological mechanisms they employ during feeding. Our initial efforts provide a proof of concept demonstrating the methodological feasibility of studying the physiology of feeding in free-ranging primates. Although howlers offer certain advantages to in vivo field research, many of the approaches described here can be applied to other primates in natural habitats. By collecting physiological data simultaneously with ecological and behavioral data, we will promote a more synthetic understanding of primate feeding and its evolutionary history.     

Intestinal Parasites of Free-ranging,Semicaptive,and Captive <Emphasis Type="Italic">Pongo abelii</Emphasis> in Sumatra,Indonesia

We collected fecal samples from 32 free-ranging, 19 semicaptive, and 54 captive Sumatran orangutans on Sumatra from 1998 until 2004 and screened them for gastrointestinal parasites. Our objectives were to compare the intestinal parasites of free-ranging, semicaptive, and captive orangutans and to evaluate the risk of parasite transmission in orangutan reintroduction programs. We identified 4 genera of Protozoa, 7 genera of nematodes, 1 trematode sp., and 1 cestode sp. The prevalence of Balantidium coli in free-ranging orangutans was significantly higher than in captive individuals. However, the prevalence of Strongyloides sp. was higher in captive than in free-ranging orangutans. Free-ranging female orangutans had a significantly higher total prevalence of intestinal parasites than that of males. We found no significant difference between parasite prevalences in different age groups. Compared to gorillas and chimpanzees, orangutans carry a smaller variety of protozoan and nematode species. Strongyloides sp. infections form the highest risk in reintroduction programs as crowding, ground-dwelling, and poor hygiene in captive and semicaptive orangutans may cause a constant reinfection.     

Determining Sensitive Parameters for the Population Viability of Reintroduced Sumatran Orangutans (Pongo abelii)

Although reintroduction has been a widely implemented conservation tool, in many cases it is unclear whether the released animals can successfully establish a viable and self-sustaining population. We constructed a population model for reintroduced Sumatran orangutans (Pongo abelii) and conducted a population viability analysis to evaluate the probability of persistence. We based our study on a reintroduced orangutan population at Bukit Tigapuluh, Jambi, Central Sumatra, Indonesia. We used various scenarios to assess the effects of adaptation time, number of released individuals, duration of release period, variation in infant survival, and carrying capacity on population extinction probability over time. We found that behavioral adaptation of individuals to living in the wild within <6 yrs after release enhanced population persistence, and that initial losses may be compensated by additional releases. Our analyses indicated that a lack of information about released orangutans prevented accurate evaluation of the effectiveness of reintroduction procedures. Consequently, we recommend that reintroduction projects improve data quality on the fates of released individuals in order to provide a reliable basis for a population viability analysis. The use of population viability analyses would allow proactive management and a better evaluation of reintroduction progress.     

Forest Structure and Support Availability Influence Orangutan Locomotion in Sumatra and Borneo

The influence of habitat structure and support availability on support use is an important aspect of understanding locomotor behavior in arboreal primates. We compared habitat structure and support availability in three orangutan study sites—two on Sumatra (Pongo abelii) in the dry‐lowland forest of Ketambe and peat swamp forest of Suaq Balimbing, and one on Borneo (Pongo pygmaeus wurmbii) in the disturbed peat swamp forest of Sabangau—to better understand orangutan habitat use. Our analysis revealed vast differences in tree and liana density between the three sites. Sabangau had a much higher overall tree density, although both Sumatran sites had a higher density of larger trees. The two peat swamp forests were more similar to each other than to Ketambe, particularly with regard to support availability. Ketambe had a wider variety of supports of different sizes and types, and a higher density of larger lianas than the two peat swamps. Orangutans in all three sites did not differ substantially in terms of their preferred supports, although Sumatran orangutans had a strong tendency to use lianas, not observed in Sabangau. Differences in observed frequencies of locomotor behavior suggest the homogeneous structure of Sabangau limits the locomotor repertoire of orangutans, with high frequencies of fewer behaviors, whereas the wider range of supports in Ketambe appears to have facilitated a more varied locomotor repertoire. There were no differences among age‐sex classes in the use of arboreal pathways in Suaq Balimbing, where orangutans selected larger trees than were typically available. This was less apparent in Sabangau, where orangutans generally used trees in relation to their environmental abundance, reflecting the homogeneous nature of disturbed peat swamp forest. These results demonstrate that forest architecture has an important influence on orangutan locomotion, which may become increasingly important as the structure of orangutan habitat continues to be altered through human disturbance. Am. J. Primatol. 74:1128‐1142, 2012. © 2012 Wiley Periodicals, Inc.     

Health evaluation of free-ranging and semi-captive orangutans (Pongo pygmaeus pygmaeus) in Sabah,Malaysia

Baseline data on health of free-ranging wildlife is essential to evaluate impacts of habitat transformation and wildlife translocation, rehabilitation, and reintroduction programs. Health information on many species, especially great apes, is extremely limited. Between 1996 and 1998, 84 free-ranging orangutans captured for translocation, underwent a complete health evaluation. Analogous data were gathered from 60 semi-captive orangutans in Malaysia. Baseline hematology and serology; vitamin, mineral and pesticide levels; and results of health evaluations, including physical examination, provide a baseline for future monitoring. Free-ranging and semi-captive orangutans shared exposure to 11 of 47 viruses. The semi-captive orangutans had significantly higher prevalence of antibodies to adenovirus (P < 0.0005) and rota (SA 11) virus (P < 0.008). More free-ranging than semi-captive animals had antibodies to Japanese encephalitis virus (P < 0.08) and foamy virus (P = 0.05). Exposure to parainfluenza and langat viruses was detected exclusively in semi-captive animals and exposure to sinbis virus was only found in free-ranging orangutans. There was evidence of exposure to respiratory syncytial virus, coxsackie virus, dengue virus, and zika virus in both groups. Ebstein-Barr virus was ubiquitous in both groups. Prevalence of antibodies against mumps virus changed from 0% in 1996 to 45% in 1998. No antibodies were detected to many important zoonotic viral pathogens, including herpesvirus and hepatitis virus. Prevalence of Balantidium coli and Plasmodium pitheci infections and exposure to mycobacterium was higher in the semi-captive animals. Differences in exposure to pathogens between the groups may be due to environmental factors including differences in exposures to other species, habitat quality, nutritional status, and other potential stressors. Differences in health parameters between captive and free-ranging orangutans need to be considered when planning conservation areas, translocation procedures, and rehabilitation protocols. Because survival of the orangutan is linked to animal and ecosystem health, results of this study will assist wildlife conservation programs by providing baseline health information.     

Morningness–eveningness and amplitude – development and validation of an improved composite scale to measure circadian preference and stability (MESSi)

Measuring morningness–eveningness is an important aspect of individual differences because it is associated with many aspects of personality and health. The present study outlines recent advancements in the field of measurement and proposes an improved assessment of morningness–eveningness, such as the measurement of circadian amplitude, updating and reflecting new item developments, addressing the clock time based measures, the morning-biased items and the aspect of uni versus multidimensionality. Four studies have been carried out in Germany to present a novel development (with a total sample of N = 1181). In study I, the exploratory factor analysis (EFA) revealed three dimensions, one of morningness, one of eveningness and one of amplitude/stability. Then, items were reduced to present a clearer factor structure by removing ambiguous items. In the second study, a shortened questionnaire was applied, with 15 items (5 per construct), but Confirmatory Factor Analysis (CFA) did not provide acceptable fit indices. Refining items were made in study III, which again showed a clearer factor structure in EFA, and subsequently, in study IV, the refined set of 15 items provided a good fit of a CFA. The final questionnaire was tested for validity by applying clock times, personality questions and alertness ratings. Thus, this newly developed questionnaire contains three distinct dimensions. To reflect the new content, the scale is labelled morningness–eveningness-stability-scale improved (MESSi).     

Food Neophobia and Social Learning Opportunities in Great Apes

Finding food resources and maintaining a balanced diet are major concerns for all animals. A compromise between neophobia and neophilia is hypothesised to enable animals to enlarge their diet while limiting the risk of poisoning. However, little is known about how primates respond to novel food items and whether their use is socially transmitted. By comparing how four different species of great apes respond to novel food items, we investigated how differences in physiology (digestive tract size and microbial content), habitats (predictability of food availability), and social systems (group size and composition) affect their response toward novelty. We presented two familiar foods, one novel fruit, four novel aromatic plants from herbal medicine, and kaolin to captive chimpanzees (Pan troglodytes), western gorillas (Gorilla gorilla), Bornean orangutans (Pongo pygmaeus) and Sumatran orangutans (Pongo abelii). We recorded smelling, approach-taste delays, ingestion, interindividual observations, and food transfers with continuous sampling. We found that behaviors differed between the apes: chimpanzees were the most cautious species and observed their conspecifics handling the items more frequently than the other apes. Close observations and food transfers were extremely rare in gorillas in comparison to orangutans and chimpanzees. We suggest that a low neophobia level reflects an adaptive response to digestive physiological features in gorillas and to unpredictable food availability in orangutans. Social interactions appeared to be predominant in chimpanzees and in both orangutan species to overcome food neophobia. They reflect higher social tolerance and more opportunities for social learning and cultural transmission in a feeding context.     

Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output

There is growing evidence that behavioral tendencies, or “personalities,” in animals are an important aspect of their biology, yet their evolutionary basis is poorly understood. Specifically, how individual variation in personality arises and is subsequently maintained by selection remains unclear. To address this gap, studies of personality require explicit incorporation of genetic information. Here, we explored the genetic basis of personality in rhesus macaques by determining the heritability of personality components and by examining the fitness consequences of those components. We collected observational data for 108 adult females living in three social groups in a free-ranging population via focal animal sampling. We applied principal component analysis to nine spontaneously occurring behaviors and identified six putative personality components, which we named Meek, Bold, Aggressive, Passive, Loner, and Nervous. All components were repeatable and heritable, with heritability estimates ranging from 0.14 to 0.35. We found no evidence of an association with reproductive output, measured either by infant survival or by interbirth interval, for any of the personality components. This finding suggests either that personality does not have fitness-related consequences in this population or that selection has acted to reduce fitness-associated variation in personality.     

Habitat use of Bornean Orangutans (<Emphasis Type="Italic">Pongo pygmaeus morio</Emphasis>) in an Industrial Forestry Plantation in East Kalimantan,Indonesia

Many primates now live in anthropogenic landscapes dominated by human activity such as agriculture. Conserving primates in such contexts requires detailed information about habitat use, including landscape features that may influence population viability. We studied Northeast Bornean orangutan (Pongo pygmaeus morio) habitat use in a forestry plantation in East Kalimantan, Indonesia. We conducted camera trapping and nest surveys at 13 locations across three habitat types in the plantation (planted acacia stands, planted eucalyptus stands, and secondary forest patches left uncut or allowed to regenerate) September 2012–March 2013, and calculated four measures of orangutan abundance for each location (independent photo captures/100 camera trap days, or RAI₂; nest encounter rate; nest density; and orangutan density). Orangutans are relatively common in the plantation; they used all three habitat types and exhibited a higher RAI₂ than 70% of other mammal species detected. A logistic regression found that proximity to natural forest areas best predicted orangutan abundance calculated using camera trap data (RAI₂) but that habitat type combined with distance to natural forest best predicted orangutan abundance calculated using nest counts. This suggests that orangutans use planted areas for movement and feeding, but rely on patches of natural forest for resting and access to key resources. Our study and others indicate that orangutans can coexist with some human activities if provided with sufficient access to natural forest. However, we must conduct further research to facilitate effective conservation planning, including gathering additional details about habitat and resource use and possible long-term population impacts.     

Serum Nutritional Profiles of Free-Ranging <Emphasis Type="Italic">Alouatta Caraya</Emphasis> in Northern Argentina: Lipoproteins; Amino Acids; Vitamins A,D, and E; Carotenoids; and Minerals

Quantifying circulating nutrient concentrations in sera of free-ranging subjects will help to establish a basis from which we can evaluate the nutritional status and needs of the captive population. We collected serum samples from 26 free-ranging black-and-gold howlers (Alouatta caraya) in San Cayetano forest in northern Argentina. We analyzed them for concentrations of lipoproteins; amino acids; vitamins A, D, and E; carotenoids; and minerals. There are a few significant differences between sexes in concentrations of high-density lipoprotein cholesterol, certain amino acids, vitamin E, lutein + zeaxanthin, and copper. Most nutritional parameters are similar to the ones measured in free-ranging Mexican mantled howlers (Alouatta palliata mexicana) and in captive New World primates (NWPs). Carotenoid, vitamin D, and phosphorus concentrations are the exceptions. Carotenoid concentrations are higher in free-ranging Alouatta caraya than reported for other free-ranging and captive species. Vitamin D concentrations are 14 times greater in the free-ranging black-and-gold howlers than in captive NWPs. Phosphorus concentrations are also higher than expected and higher than typically occur in captive primates, leading to a 1:1.6 calcium:phosphorus ratio. Because we based our study on a small number of free-ranging howlers, additional samples from different regions and throughout the year would better define desirable nutritional parameters for captive howlers.     

Adaptation to Forest Life During the Reintroduction Process of Immature <Emphasis Type="Italic">Pongo abelii</Emphasis>

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.     

The evolution of large body size in orangutans: A model for hominoid divergence

Recent Miocene fossil discoveries of large hominoids resemble orangutans. Since the evolution of large body size was functionally related to a powerful masticatory system in Miocene ape radiations, a better understanding of adaptations in extant orangutans will be informative of hominoid evolution. It is suggested here, based on the behavioral ecology of extant orangutans, that foraging energetics and large body size are tied to a dietary shift that provided access to and utilization of resources not generally available to other primates.     

Systematic Investigation of the Stability of Food Preferences in Captive Orangutans: Implications for Positive Reinforcement Training

Using preference-assessment tests with humans in conjunction with behavioral modification sessions has been a regular component of almost all operant conditioning programs with mentally challenged humans. This has been very effective in improving the efficiency of behavioral training in these settings and could be similarly effective in zoological and research environments. This study investigated the preferences of 9 captive orangutans for different food items. The study used a pairwise presentation to record each nonhuman animal's preferences for 5 different foods on 6 different occasions over the course of 6 months. Results of a Friedman's 2-way ANOVA indicated that the orangutans showed a clear overall preference for apple. However, there was significant variability among different orangutans in preference ranking for the 5 foods, as shown by a Kendall's tau. In addition, there was variability in preference rankings across time for each orangutan. Because the orangutans' preferences change over time and vary according to individual, regular assessments should identify items to be used as rewards in behavioral husbandry training or as part of feeding enrichment strategies.     

Gaze Duration Biases for Colours in Combination with Dissonant and Consonant Sounds: A Comparative Eye-Tracking Study with Orangutans

Research on colour preferences in humans and non-human primates suggests similar patterns of biases for and avoidance of specific colours, indicating that these colours are connected to a psychological reaction. Similarly, in the acoustic domain, approach reactions to consonant sounds (considered as positive) and avoidance reactions to dissonant sounds (considered as negative) have been found in human adults and children, and it has been demonstrated that non-human primates are able to discriminate between consonant and dissonant sounds. Yet it remains unclear whether the visual and acoustic approach–avoidance patterns remain consistent when both types of stimuli are combined, how they relate to and influence each other, and whether these are similar for humans and other primates. Therefore, to investigate whether gaze duration biases for colours are similar across primates and whether reactions to consonant and dissonant sounds cumulate with reactions to specific colours, we conducted an eye-tracking study in which we compared humans with one species of great apes, the orangutans. We presented four different colours either in isolation or in combination with consonant and dissonant sounds. We hypothesised that the viewing time for specific colours should be influenced by dissonant sounds and that previously existing avoidance behaviours with regard to colours should be intensified, reflecting their association with negative acoustic information. The results showed that the humans had constant gaze durations which were independent of the auditory stimulus, with a clear avoidance of yellow. In contrast, the orangutans did not show any clear gaze duration bias or avoidance of colours, and they were also not influenced by the auditory stimuli. In conclusion, our findings only partially support the previously identified pattern of biases for and avoidance of specific colours in humans and do not confirm such a pattern for orangutans.