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.     

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.     

The nature and evolution of intelligence in orangutans (Pongo pygmaeus)

Orangutans share many intellectual qualities with African great apes and humans, likely because of their recent common ancestry. They may also show unique intellectual adaptations because of their long evolutionary divergence from the African lineage. This paper assesses orangutan intelligence in light of this evolutionary history. Evidence derives from observations of juvenile ex-captive orangutans reintroduced to free forest life by the Wanariset Orangutan Reintroduction Project, East Kalimantan, Indonesia. The intellectual qualities shared by great apes and humans point to a distinct “great ape” intelligence with hierarchization as a pivotal cognitive mechanism. Evolutionary reconstructions jibe with this view and suggest that technically difficult foods may have been key selection pressures. Orangutans should then show hierarchical intelligence when obtaining difficult foods. Evidence on ex-captive orangutans' techniques for processing difficult foods concurs. Intellectual qualities distinct to orangutans may owe to arboreal travel pressures; in particular arboreality may aggravate foraging problems. Evidence confirms that ex-captive orangutans' techniques for accessing difficult foods located arboreally are intellectually complex—i.e. they show hierarchization. These findings suggest other factors probably important to understanding great ape and orangutan forms of intelligence and their evolutionary origins.     

Treatment of disseminated Strongyloides spp. infection in an infant Sumatran orangutan (Pongo abelii)

Strongyloides nematodes have been reported in all species of great apes with orangutans ≤5 years old most susceptible to severe clinical disease. This brief communication describes the first published case of antemortem diagnosis and treatment of disseminated strongyloidiasis in a clinically affected 5‐month‐old Sumatran orangutan (Pongo abelii).     

Population history, biogeography, and taxonomy of orangutans (Genus: Pongo) based on a population genetic meta-analysis of multiple loci

This paper examines orangutan population history and evolution through a meta-analysis of seven loci collected from both Sumatran and Bornean orangutans. Within orangutans, most loci show that the Sumatran population is about twice as diverse as the Bornean population. Orangutans are more diverse than African apes and humans. Sumatran and Bornean populations show significant genetic differentiation from one another and their history does not differ significantly from an 'island model' (population splitting without gene flow). Two different methods support a divergence of Bornean and Sumatran orangutans at 2.7-5 million years ago. This suggests that Pleistocene events, such as the cyclical exposure of the Sunda shelf and the Toba volcanic eruption, did not have a major impact on the divergence of Bornean and Sumatran orangutans. Pairwise mismatch analyses, however, suggest that Bornean orangutans have undergone a recent population expansion (beginning 39,000-64,000 years ago), while Sumatran orangutan populations were stable. Pleistocene events may have contributed to these aspects of orangutan population history. These conclusions are applied to the debate on orangutan taxonomy.     

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.     

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.     

Behavioral, Ecological, and Evolutionary Aspects of Meat-Eating by Sumatran Orangutans (Pongo abelii)

Meat-eating is an important aspect of human evolution, but how meat became a substantial component of the human diet is still poorly understood. Meat-eating in our closest relatives, the great apes, may provide insight into the emergence of this trait, but most existing data are for chimpanzees. We report 3 rare cases of meat-eating of slow lorises, Nycticebus coucang, by 1 Sumatran orangutan mother–infant dyad in Ketambe, Indonesia, to examine how orangutans find slow lorises and share meat. We combine these 3 cases with 2 previous ones to test the hypothesis that slow loris captures by orangutans are seasonal and dependent on fruit availability. We also provide the first (to our knowledge) quantitative data and high-definition video recordings of meat chewing rates by great apes, which we use to estimate the minimum time necessary for a female Australopithecus africanus to reach its daily energy requirements when feeding partially on raw meat. Captures seemed to be opportunistic but orangutans may have used olfactory cues to detect the prey. The mother often rejected meat sharing requests and only the infant initiated meat sharing. Slow loris captures occurred only during low ripe fruit availability, suggesting that meat may represent a filler fallback food for orangutans. Orangutans ate meat more than twice as slowly as chimpanzees (Pan troglodytes), suggesting that group living may function as a meat intake accelerator in hominoids. Using orangutan data as a model, time spent chewing per day would not require an excessive amount of time for our social ancestors (australopithecines and hominids), as long as meat represented no more than a quarter of their diet.     

Quantitative and functional studies on the hands of the anthropoidea. I. The Hominoidea

The hands of the Hominoidea evidence four adaptive modes which distinguish the lesse apes (Hylobatidae), the orangutan (Pongo), the African apes (Pan), and man (Homo) from one another. The hands of the apes consist of compromises between manipulatory and locomotor functions because selection has operated for precision of grip as well as for special locomotor mechanisms. The human hand is almost totally devoted to manipulation. The hands of gibbons, orangutans and the African apes differ in many features that may be correlated with locomotion. The gibbons and siamang are specially adapted for ricochetal arm-swinging. The great apes possess morphological adaptations for arboreal foraging and climbing distinct from those of the hylobatids. In addition, the African apes have become secondarily adapted for terrestrial quadrupedal locomotion. Many features that distinguish the hands of chimpanzees and gorillas may be associated with the development of efficient knuckele-walking propulsive and support mechanisms.     

Immature wild orangutans acquire relevant ecological knowledge through sex-specific attentional biases during social learning

As a part of growing up, immature orangutans must acquire vast repertoires of skills and knowledge, a process that takes several years of observational social learning and subsequent practice. Adult female and male orangutans show behavioral differences including sex-specific foraging patterns and male-biased dispersal. We investigated how these differing life trajectories affect social interest and emerging ecological knowledge in immatures. We analyzed 15 years of detailed observational data on social learning, associations, and diet repertoires of 50 immatures (16 females and 34 males), from 2 orangutan populations. Specific to the feeding context, we found sex differences in the development of social interest: Throughout the dependency period, immature females direct most of their social attention at their mothers, whereas immature males show an increasing attentional preference for individuals other than their mothers. When attending to non-mother individuals, males show a significant bias toward immigrant individuals and a trend for a bias toward adult males. In contrast, females preferentially attend to neighboring residents. Accordingly, by the end of the dependency period, immature females show a larger dietary overlap with their mothers than do immature males. These results suggest that immature orangutans show attentional biases through which they learn from individuals with the most relevant ecological knowledge. Diversifying their skills and knowledge likely helps males when they move to a new area. In sum, our findings underline the importance of fine-grained social inputs for the acquisition of ecological knowledge and skills in orangutans and likely in other apes as well.

To understand the development and evolution of cognition of our closest relatives, we need to investigate their learning behavior during every-day life. This study finds that wild orangutan males and females differ in their social learning strategies and subsequent learning outcomes from an early age, underlining the general importance of, and the effects of sex on, social learning in non-human great apes.     

Comparative and functional morphology of hominoid fingers.

Comparisons of hominoid metacarpals and phalanges reveal differences, many of which are closely linked to locomotor hand postures. The African apes display features of the metacarpals and phalanges which distinguish them from the other Hominoidea. These features are most evident in digits III and IV. The orangutan hand is demonstrably less well adapted to knuckle-walking and is distinctive in its adaptation to power and hook grasping of vertical and horizontal supports, respectively. Orangutan fingers possess a "double-locking" mechanism (Napier, '60), and a slight ulnad shift in the axis of the hand which results in lengthened phalanges of ray IV. Hylobatid apes are more like orangutans in their finger morphology than any of the other Hominoidea, but exhibit unique features of their own. These include elongate phalanges of fingers II-V. Human metacarpals II-V form two sets composed of II-III, and IV-V. The heads of both metacarpals II and III are characterized by axial torsion. This reflects the enhanced manipulatory role of the third finger in humans. Human distal phalanges are unique in the development of pronounced apical tufts. Multivariate analysis of metacarpal III and proximal III yields variables that array the extant apes along an arboreal-terrestrial axis, from hylobatid apes to male gorillas. The positions of taxa on this discriminant concur with observations on the locomotion of free-ranging apes.     

广西化石猩猩牙尖釉质的日分泌率

作为现仅存于亚洲大陆的现生大猿,更新世时期猩猩曾广泛分布于东南亚大陆及华南地区,但其保留下来的化石材料主要为单颗牙齿。从牙齿形态、尺寸等外部特征的研究得出的关于猩猩的分类及演化问题的结论并未得到广泛一致的认同,而研究表明牙齿生长发育特征可作为系统分类研究的一个潜在工具。本研究选取了一批来自于中国广西更新世时期的猩猩牙齿化石,制作牙齿组织学切片,测量计算了其牙釉质日分泌率,结果显示广西化石猩猩牙尖釉质日分泌率在2.32-6.88μm/d之间,平均值约为4.61μm/d,从牙尖内部到表面,釉质日分泌率有增加趋势。此外,还将广西化石猩猩与其他现生大猿和现代人进行比较,以期从牙齿生长发育的角度为猩猩的演化和分类问题提供一点线索和证据。     

Orangutan Energetics and the Influence of Fruit Availability in the Nonmasting Peat-swamp Forest of Sabangau,Indonesian Borneo

Data on energy intake and the effects of fluctuations in fruit availability on energy intake for African apes, and orangutans in mast-fruiting habitats, indicate that orangutans may face greater energetic challenges than do their African counterparts. Comparable data on orangutans in nonmasting forests, which experience lower fluctuations in fruit availability, have been lacking, however, complicating interpretations. We conducted a 46-mo study of orangutan energetics in the nonmasting Sabangau peat-swamp forest, Indonesian Borneo. Sabangau orangutans experienced periods of negative energy balance apparently even longer than in mast-fruiting habitats, as indicated by comparisons of observed energy intake with theoretical requirements and analysis of urinary ketones. Daily energy intake was positively related to fruit availability in flanged males, but not in adult females or unflanged males. This may represent different foraging strategies between age-sex classes and suggests that fruit availability is not always an accurate indicator of ape energy intake/balance. Urinary ketone levels were not generally related to fruit availability, daily energy intake, day range, or party size. This is probably due to low energy intake, and consequently high ketone production, throughout much of the study period. Comparisons with published results on African apes support the hypothesis that orangutans are unique among hominoids in regularly experiencing prolonged periods of negative energy balance. This has important effects on orangutan behavior and socioecology, and has likely been a key factor driving the evolutionary divergence of orangutans and African apes.     

Rotator cuff muscle function and its relation to scapular morphology in apes

It is widely held that many differences among primate species in scapular morphology can be functionally related to differing demands on the shoulder associated with particular locomotor habits. This perspective is largely based on broad scale studies, while more narrow comparisons of scapular form often fail to follow predictions based on inferred differences in shoulder function. For example, the ratio of supraspinous fossa/infraspinous fossa size in apes is commonly viewed as an indicator of the importance of overhead use of the forelimb, yet paradoxically, the African apes, the most terrestrial of the great apes, have higher scapular fossa ratios than the more suspensory orangutan. The recent discovery of several nearly complete early hominin scapular specimens, and their apparent morphological affinities to scapulae of orangutans and gorillas rather than chimpanzees, has led to renewed interest in the comparative analysis of human and extant ape scapular form. To facilitate the functional interpretation of differences in ape scapulae, particularly in regard to relative scapular fossa size, we used electromyography (EMG) to document the activity patterns in all four rotator cuff muscles in orangutans and gibbons, comparing the results with previously published data for chimpanzees.     

The reluctant innovator: orangutans and the phylogeny of creativity

Young orangutans are highly neophobic, avoid independent exploration and show a preference for social learning. Accordingly, they acquire virtually all their learned skills through exploration that is socially induced. Adult exploration rates are also low. Comparisons strongly suggest that major innovations, i.e. behaviours that have originally been brought into the population through individual invention, are made where ecological opportunities to do so are propitious. Most populations nonetheless have large innovation repertoires, because innovations, once made, are retained well through social transmission. Wild orangutans are therefore not innovative. In striking contrast, zoo-living orangutans actively seek novelty and are highly exploratory and innovative, probably because of positive reinforcement, active encouragement by human role models, increased sociality and an expectation of safety. The explanation for this contrast most relevant to hominin evolution is that captive apes generally have a highly reduced cognitive load, in particular owing to the absence of predation risk, which strongly reduces the costs of exploration. If the orangutan results generalize to other great apes, this suggests that our ancestors could have become more curious once they had achieved near-immunity to predation on the eve of the explosive increase in creativity characterizing the Upper Palaeolithic Revolution.     

Assessments made easier: examining the use of a rating-based questionnaire to capture behavioral data in rehabilitant orangutans (Pongo pygmaeus morio)

Rehabilitation and release are commonly used for confiscated, surrendered, and rescued primates. To improve release efficacy it is important to generate accurate behavioral profiles of release candidates. Research on primates traditionally uses observer ratings to measure individual differences. This method is easily implemented, but its validity has been questioned. We evaluated whether observer ratings reflect behavioral data indicating forest adaptation in 18 free-ranging rehabilitant orangutans (Pongo pygmaeus morio). In 2017, we used a species-specific questionnaire to measure how often orangutans engaged in behaviors linked to living successfully in the wild (e.g., nest building) and the extent to which they express personality traits that may influence forest adaptation. We collected 11 months of observational data on 17 of the orangutans concurrently to validate the questionnaire items, and collected further questionnaire data for 16 of the individuals in 2019. We used regularized exploratory factor analysis (REFA) and parallel analysis to condense the ratings and determine that two factors could be reliably extracted. We conducted another REFA using the observational data, and calculated factor congruence coefficients following procrustean rotation. The first of the two factors represented forest skills and human aversion, and was congruent with observational data. The second factor reflected boldness, sociability, and exploration, and was not congruent with observational data. Ratings correlated significantly with observations for all five questionnaire items reflecting adaptation to forest life, and for three of seven items reflecting personality traits. We conclude that ratings can be a valid approach to obtain individual-based behavioral information reflecting forest adaptation in free-ranging rehabilitant orangutans, and may be particularly useful in summarizing behaviors relevant to forest adaptation that are otherwise challenging to gather in primates.

     

The cross-sectional geometry of the hand and foot bones of the hominoidea and its relationship to locomotor behavior

Cheiridia are valuable indicators of positional behavior, as they directly contact the substrate, but systematic comparison of the structural properties of both metacarpals and metatarsals has never been carried out. Differences in locomotor behavior among the great apes (knuckle-walking vs. quadrumanous climbing) can produce biomechanical differences that may be elucidated by the parallel study of cross-sectional characteristics of metacarpals and metatarsals. The aim of this work is to study the cross-sectional geometric properties of these bones and their correlation with locomotor behavior in large-bodied hominoids. The comparisons between bending moments of metacarpals and metatarsals of the same ray furnished interesting results. Metacarpals III and especially IV of the knuckle-walking African apes were relatively stronger than those of humans and orangutans, and metatarsal V of humans was relatively stronger than those of the great apes. Interestingly, the relative robusticity of the metacarpal IV of the quadrumanous orangutan was between that of the African apes and that of humans. The main conclusions of the study are: 1) cross-sectional dimensions of metacarpals and metatarsals are influenced by locomotor modes in great apes and humans; 2) interlimb comparisons of cross-sectional properties of metacarpals and metatarsals are good indicators of locomotor modes in great apes and humans; and 3) the results of this study are in accord with those of previous analyses of plantar pressure and morphofunctional traits of the same bones, and with behavioral studies. These results provide a data base from which it will be possible to compare the morphology of the fossils in order to gain insight into the locomotor repertoires of extinct taxa.     

Morphometric analysis of hominoid lower molars from Yuanmou of Yunnan Province, China

Shape analyses of cross-sectional mandibular molar morphology, using Euclidean Distance Matrix Analysis, were performed on 79 late Miocene hominoid lower molars from Yuanmou of Yunnan Province, China. These molars were compared to samples of chimpanzee, gorilla, orangutan,Lufengpithecus lufengensis, Sivapithecus, Australopithecus afarensis, and human mandibular molars. Our results indicate that the cross-sectional shape of Yuanmou hominoid lower molars is more similar to the great apes that to humans. There are few differences between the Yuanmou,L. lufengensis, andSivapithecus molars in cross-sectional morphology, demonstrating strong affinities between these three late Miocene hominoids. All three of the fossil samples show strong similarities to orangutans. From this, we conclude that these late Miocene hominoids are more closely related to orangutants than to either the African great apes or humans.     

广西化石猩猩牙齿釉质厚度研究

华南和东南亚发现大量更新世的猩猩牙齿化石。本研究应用CT扫描三维重建的技术方法研究了广西更新世化石猩猩牙齿釉质厚度,并与现生类人猿、现代人、化石类人猿以及早期人类进行比较分析。结果显示:广西猩猩同类牙齿的釉质厚度与牙齿大小相关性很小;臼齿和前臼齿釉质厚度在上下颌之间不存在显著性差异;来自广西不同地区的猩猩化石牙釉质厚度无显著差异。与早期人科成员相比,广西猩猩的牙釉质相对较薄,平均与相对釉质厚度值都明显小于南方古猿、傍人。与早期人属相比,小于直立人、尼人以及非洲和欧洲的早期人属化石。与现代人和现生灵长类相比,广西化石猩猩釉质厚度明显大于大部分猴类和非洲大猿;平均釉质厚度稍大于现生猩猩,而与现代人更为接近;相对釉质厚度小于现代人,而与现生猩猩差异不大,都属于偏厚型釉质。本文讨论了釉质厚度与系统分类演化、食性适应的相关问题,作者推测釉质厚度可能是物种的特征属性,与牙齿功能适应有密切关联。     

华南化石猩猩前部牙齿釉面横纹与牙冠形成时间研究

釉面横纹的分布与数目可以反映牙齿生长发育的时间和速率变化, 在化石研究中能为复原个体生活史提供重要依据。本研究运用扫描电子显微镜观察华南化石猩猩门齿、犬齿釉面横纹分布与数目, 并估算门齿和犬齿牙冠形成时间, 结果如下: 牙冠从牙尖至牙颈方向釉面横纹分布密度有疏密变化, 牙尖釉面横纹密度小于10条/mm, 中间至牙颈釉面横纹密度较尖部增大, 大约10-15条/mm; 犬齿釉面横纹数目多于门齿, 雄性犬齿釉面横纹数目多于雌性; 根据釉面横纹计数及其生长周期的组织切片观察结果, 估算门齿牙冠形成时间大约为2.97-6.66年, 犬齿雄性长于雌性, 分别为6.25-11.31年和4.28-7.29年。与一些古猿、早期人类、现代人以及现生大猿比较, 华南化石猩猩釉面横纹整体密度稍大于南方古猿和傍人, 小于黑猩猩、大猩猩、现代人和禄丰古猿; 除侧门齿外, 华南化石猩猩釉面横纹数目明显多于南方古猿、傍人和现代人, 与大猩猩接近; 华南猩猩前部牙齿牙冠形成时间与现生大猿、禄丰古猿差别不大, 与现生猩猩最相近, 长于南方古猿和傍人。