Declining Orangutan Encounter Rates from Wallace to the Present Suggest the Species Was Once More Abundant

Background

Bornean orangutans (Pongo pygmaeus) currently occur at low densities and seeing a wild one is a rare event. Compared to present low encounter rates of orangutans, it is striking how many orangutan each day historic collectors like Alfred Russel Wallace were able to shoot continuously over weeks or even months. Does that indicate that some 150 years ago encounter rates with orangutans, or their densities, were higher than now?

Methodology/Principal Findings

We test this hypothesis by quantifying encounter rates obtained from hunting accounts, museum collections, and recent field studies, and analysing whether there is a declining trend over time. Logistic regression analyses of our data support such a decline on Borneo between the mid-19th century and the present. Even when controlled for variation in the size of survey and hunting teams and the durations of expeditions, mean daily encounter rates appear to have declined about 6-fold in areas with little or no forest disturbance.

Conclusions/Significance

This finding has potential consequences for our understanding of orangutans, because it suggests that Bornean orangutans once occurred at higher densities. We explore potential explanations—habitat loss and degradation, hunting, and disease—and conclude that hunting fits the observed patterns best. This suggests that hunting has been underestimated as a key causal factor of orangutan density and distribution, and that species population declines have been more severe than previously estimated based on habitat loss only. Our findings may require us to rethink the biology of orangutans, with much of our ecological understanding possibly being based on field studies of animals living at lower densities than they did historically. Our approach of quantifying species encounter rates from historic data demonstrates that this method can yield valuable information about the ecology and population density of species in the past, providing new insight into species'' conservation needs.     

Orangutan Nesting Behavior in Disturbed Forest of Sabah,Malaysia: Implications for Nest Census

High concentrations of orangutans remain in the multiple-use forests of the Lower Kinabatangan, Sabah, Malaysia. Compared to primary forest, the habitat is highly fragmented, characterized by a low tree density (332 stems/ha), small tree size (83.6% of trees are <20 m high), low basal area (18 m²/ha), abundance of canopy gaps and high level of soil disturbance. The forest structure and composition influence orangutan nesting patterns, and thus directly influence the results of nest surveys used to determine orangutan population size. In logged forests, tall and large trees are the preferred nesting sites of orangutans. The scarcity of suitable nesting sites in the logged-over forests of Kinabatangan, could partly explain the lower daily rate of nest construction (r = 1.00) versus those of other orangutan populations. The nest decay rate t recorded at the study site (average ± SD = 202 ± 151 days) strongly depends on the species of tree in which a nest is built. Our results illustrate that the nest-related parameters used for orangutan censuses fluctuate among habitat types and emphasize the need to determine specific values of r for specific orangutan populations and of t for different tree species in order to achieve accurate analysis of census data.     

Changes in Orangutan Caloric Intake,Energy Balance,and Ketones in Response to Fluctuating Fruit Availability

I used novel quantitative measures to assess the impact of fruit seasonality on changes in diet and energy balance during 4918 hours of observation on <60 orangutans in Gunung Palung National Park, West Kalimantan, Indonesia, from September 1994 through September 1995. During this period a mast fruiting occurred, resulting in large fluctuations in fruit availability, measured by monitoring of 558 orangutan fruit trees. Orangutan diet varied tremendously in accordance with these fluctuations. During the month of highest fruit production, 100% of the orangutan diet was composed of fruit. In contrast, during the fruit-poor period as little as 21% of the diet was fruit, while 37% was bark. Nutritional analyses of 78 of the foods most commonly eaten during this study show that mast foods were significantly higher in caloric content than were nonmast foods, which translates into substantial changes in caloric intake. During the month of highest fruit consumption (January), males consumed an estimated 8422 kcal/day and females consumed 7404 kcal/day. During the month of lowest fruit consumption (May), males consumed 3824 kcal/day and females consumed 1793 kcal/day. These differences were significantly different between the 2 months for both males and females. In May, males ate significantly more kcal/day than females did. Time spent feeding did not differ between the two periods for either males or females. I assessed the impact of these changes in diet and caloric intake on orangutan physiological functioning by measuring ketones in 257 urine samples collected from adult males and females. Ketones—products of fat metabolism—were present in urine only during the fruit-poor period. These data suggest that orangutans are highly efficient at storing fat during fruit-rich periods and utilizing the reserves during times of fruit shortfall. This response may have important implications for orangutan survivorship, reproduction, and behavior.     

Fur-Rubbing as a Form of Self-Medication in <Emphasis Type="Italic">Pongo pygmaeus</Emphasis>

Orangutans exhibit fur-rubbing possibly for medicinal use. I hypothesize that they use a species of Commelina, an uncommon herb in the peat-swamp forests of Central Kalimantan, Borneo, as either an antibacterial or anti-inflammatory agent. In Central Kalimantan, local indigenous people use the same species as an external medication to treat their arms after a stroke, for muscular pain, and for sore bones and swellings. Thus, the possible convergence of human and orangutan use of Commelina may indicate that orangutans are using it for a similar purpose.     

It’s Not Just Conflict That Motivates Killing of Orangutans

We investigated why orangutans are being killed in Kalimantan, Indonesia, and the role of conflict in these killings. Based on an analysis of interview data from over 5,000 respondents in over 450 villages, we also assessed the socio-ecological factors associated with conflict and non-conflict killings. Most respondents never kill orangutans. Those who reported having personally killed an orangutan primarily did so for non-conflict reasons; for example, 56% of these respondents said that the reason they had killed an orangutan was to eat it. Of the conflict-related reasons for killing, the most common reasons orangutans were killed was fear of orangutans or in self-defence. A similar pattern was evident among reports of orangutan killing by other people in the villages. Regression analyses indicated that religion and the percentage of intact forest around villages were the strongest socio-ecological predictors of whether orangutans were killed for conflict or non-conflict related reasons. Our data indicate that between 44,170 and 66,570 orangutans were killed in Kalimantan within the respondents’ active hunting lifetimes: between 12,690 and 29,024 for conflict reasons (95%CI) and between 26,361 and 41,688 for non-conflict reasons (95% CI). These findings confirm that habitat protection alone will not ensure the survival of orangutans in Indonesian Borneo, and that effective reduction of orangutan killings is urgently needed.     

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.     

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. Am. J. Primatol. 71:680–686, 2009. © 2009 Wiley‐Liss, Inc.     

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.     

Social behavior of captive,group-living Orangutans

The behavior of orang-utans (Pongo pygmaeus)was observed in two captive groups (one adult group, one juvenile group). Activity profiles,animal interactions, and compartmental spatial use for both adult-group and juvenile-group individuals were recorded over a 9-month period. Behavioral repertoires for both groups included large amounts of social activity. Equivalent amounts of social activity were found for each group. The social behavior of juvenile animals involved more active behavior such as play. The social behavior of the adult animals was more subtle, involving social monitoring and allogrooming. These results indicate that orangutans, at least when group-living in captivity, exhibit the potential to display social behavior which is apparently of greater frequency and complexity than that which has been observed in the wild. These findings suggest that the solitary behavior of wild orangutans is not a necessary characteristic of orangutan behavior. Under different environmental conditions orangutans appear to readily adapt socially, and, like other nonhuman primates,they have the capacity to exhibit complex and subtle social behavior. This report is based on part of a senior thesis submitted by Sara D. Edwards     

Orangutan diet,range, and activity at Tanjung Puting,Central Borneo

Previously, wild orangutan feeding and ranging behaviors have been described only from populations in hilly or mountainous regions. The Tanjung Puting study focuses on an orangutan population in a swampy lowland area near sea level. Tanjung Puting also differs from other areas in the virtual absence of large figs, which are significant orangutan food sources elsewhere. During a 4-year period and 6804 hr of observation, focal orangutans were recorded in 11,338 foraging bouts accounting for 3805 hr. Composition and phenology of the forest habitat were documented. The orangutans were predominantly frugivorous, with fruit-eating accounting for 61% of the foraging time. However, the overall variety in their diet was remarkable; 317 different food types have been identified, including fungus, insects, and honey. Orang-utans were strongly opportunistic foragers, with the composition of their diet varying markedly from month to month. During most months orangutans fed on a complex mix of fruit, leaves, bark, insects, and small vines. During some months fruit was not the major component of the diet. All orangutans foraged in both the dry-ground mixed dipterocarp forest and the peatswamp forest habitats found in their ranges. Adult males and females utilized different proportions of certain resources in their diets. Prime adult males also ranged further per day and spent more time on the ground than prime adult females. At Tanjung Puting contact with other orangutans usually increased a focal orangutan’s day length, day range, and amount of time spent moving. This suggests that foraging alone maximized each orangutan’s foraging returns by minimizing the day range traveled. Orangutan solitariness is the result of a large body size and of a predominantly frugivorous and opportunistic diet.     

The development of wild immature Sumatran orangutans (Pongo abelii) at Ketambe

Orangutans have the longest immature period and inter-birth interval of all ape species. This may be explained by a slow life history, the need to develop skills or by their relatively solitary lifestyle, which prevents a mother from associating with two offspring. This study of wild immature orangutans at the Ketambe Research Station, Indonesia, describes, with partly cross-sectional, partly longitudinal data, their development to independence. The study subjects ranged from 1 to 11 years of age. Data on their activity budget, diet, mother–offspring proximity and maintenance of proximity, association with conspecifics and play behavior were collected. The results indicate that immature orangutans can provide for their own food and transport, and therefore were independent of direct maternal care, at an age of possibly 3 but more clearly 6 years. This is similar to chimpanzees, and refutes the slow life history hypothesis. Immature orangutans remain within their mother’s vicinity until the age of 8 years, indicating a dependence on indirect maternal care, and this coincides with the period during which the mother does not produce another offspring. A female orangutan seems unable to associate with an older immature while caring for a new infant. This is consistent with the solitary-lifestyle hypothesis and corroborates the results obtained with the Sumatran orangutan population at Suaq Balimbing. However, why an immature depends indirectly on its mother for such a long period remains unclear. It is possible that it needs to develop ecological or social skills or needs the protection of its mother. Unfortunately, no data were available to distinguish between these possibilities.     

Unexpected Ecological Resilience in Bornean Orangutans and Implications for Pulp and Paper Plantation Management

Ecological studies of orangutans have almost exclusively focused on populations living in primary or selectively logged rainforest. The response of orangutans to severe habitat degradation remains therefore poorly understood. Most experts assume that viable populations cannot survive outside undisturbed or slightly disturbed forests. This is a concern because nearly 75% of all orangutans live outside protected areas, where degradation of natural forests is likely to occur, or where these are replaced by planted forests. To improve our understanding of orangutan survival in highly altered forest habitats, we conducted population density surveys in two pulp and paper plantation concessions in East Kalimantan, Indonesia. These plantations consist of areas planted with fast-growing exotics intermixed with stands of highly degraded forests and scrublands. Our rapid surveys indicate unexpectedly high orangutan densities in plantation landscapes dominated by Acacia spp., although it remains unclear whether such landscapes can maintain long-term viable populations. These findings indicate the need to better understand how plantation-dominated landscapes can potentially be incorporated into orangutan conservation planning. Although we emphasize that plantations have less value for overall biodiversity conservation than natural forests, they could potentially boost the chances of orangutan survival. Our findings are based on a relatively short study and various methodological issues need to be addressed, but they suggest that orangutans may be more ecologically flexible than previously thought.     

Feeding behavior, diet, and the functional consequences of jaw form in orangutans, with implications for the evolution of Pongo

Orangutans are amongst the most craniometrically variable of the extant great apes, yet there has been no attempt to explicitly link this morphological variation with observed differences in behavioral ecology. This study explores the relationship between feeding behavior, diet, and mandibular morphology in orangutans. All orangutans prefer ripe, pulpy fruit when available. However, some populations of Bornean orangutans (Pongo pygmaeus morio and P. p. wurmbii) rely more heavily on bark and relatively tough vegetation during periods of low fruit yield than do Sumatran orangutans (Pongo abelii). I tested the hypothesis that Bornean orangutans exhibit structural features of the mandible that provide greater load resistance abilities to masticatory and incisal forces. Compared to P. abelii, P. p. morio exhibits greater load resistance abilities as reflected in a relatively deeper mandibular corpus, deeper and wider mandibular symphysis, and relatively greater condylar area. P. p. wurmbii exhibits most of these same morphologies, and in all comparisons is either comparable in jaw proportions to P. p. morio, or intermediate between P. p. morio and P. abelii. These data indicate that P. p. morio and P. p. wurmbii are better suited to resisting large and/or frequent jaw loads than P. abelii. Using these results, I evaluated mandibular morphology in P. p. pygmaeus, a Bornean orangutan population whose behavioral ecology is poorly known. Pongo p. pygmaeus generally exhibits relatively greater load resistance capabilities than P. abelii, but less than P. p. morio. These results suggest that P. p. pygmaeus may consume greater amounts of tougher and/or more obdurate foods than P. abelii, and that consumption of such foods may intensify amongst Bornean orangutan populations. Finally, data from this study are used to evaluate variation in craniomandibular morphology in Khoratpithecus piriyai, possibly the earliest relative of Pongo from the late Miocene of Thailand, and the late Pleistocene Hoa Binh subfossil orangutan recovered from Vietnam. With the exception of a relatively thicker M(3) mandibular corpus, K. piriyai has jaw proportions that would be expected for an extant orangutan of comparable jaw size. Likewise, the Hoa Binh subfossil does not differ in skull proportions from extant Pongo, independent of the effects of increase in jaw size. These results indicate that differences in skull and mandibular proportions between these fossil and subfossil orangutans and extant Pongo are allometric. Furthermore, the ability of K. piriyai to resist jaw loads appears to have been comparable to that of extant orangutans. However, the similarity in jaw proportions between P. abelii and K. piriyai suggest the latter may have been dietarily more similar to Sumatran orangutans.     

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. Am. J. Primatol. 72:62–71, 2010. © 2009 Wiley‐Liss, Inc.     

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.     

The phylogeography of orangutan foamy viruses supports the theory of ancient repopulation of Sumatra

Phylogenetic analysis of foamy virus sequences obtained from Bornean and Sumatran orangutans showed a distinct clustering pattern. One subcluster was represented by both Bornean and Sumatran orangutan simian foamy viruses (SFV). Combined analysis of host mitochondrial DNA and SFV phylogeny provided evidence for the hypothesis of the repopulation of Sumatra by orangutans from Borneo.     

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.     

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.     

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.