Sensorimotor cognition in young feral orangutans (Pongo pygmaeus)

The goal of this study was to describe object manipulation in wild orangutan infants and juveniles. Object manipulation is an important subsistence activity that also reflects cognitive functioning. Orangutans were studied in the field, at the Tanjung Puting Reserve, Kalimantan Tengah, Indonesia. Fourteen orangutans, grouped by age (infants 2.5 to 4.6 years; juveniles 5 to 8.5 years), were observed over a total of 555 hr and for an average of three full dawn-to-dusk “follows” each. Young orangutan’s manipulations were categorized along a hierarchy of complexity. The least complex manipulations were single sensorimotor actions such as grasping, mouthing, and waving. The most complex manipulations were combinations and coordinations of actions, such as experimentation with objects, tool use, and planning. Manipulative behavior occurred mainly when foraging, i.e. when obtaining and processing food items. Interestingly, complex behavior occurred most often when locomoting. The most complex object manipulations, however, occurred rarely. Infants and juveniles exhibited equivalent levels of complexity. Several aspects of this study point to the importance of social assistance provided by competent mothers for the development of young orangutans’ ability to locomote and to locate, obtain, and process food items. This study also highlights the cognitive abilities of young wild orangutans regarding tool use.     

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.     

Wild orangutan birth at tanjung puting reserve

During ten years (1971–1981) of research on wild orangutans at the Orangutan Research and Conservation Project study area in the Tanjung Puting Reserve, Central Indonesian Borneo, parturition was observed twice. Observations centered on parturition totalled 1,206 hr and included 95 whole days of observation (when the target individual was followed from nest to nest). The two females who gave birth are mother and daughter, one multiparous, the other primiparous. The 1977 birth to the daughter made the older female who subsequently gave birth in 1979 the first known wild orangutan grandmother. In 1977 the entire birth process was observed while in 1979 only the emergence of the fetal membranes was seen. The females' behavior during parturition as well as prepartum and postpartum was quite different and is described. Parity may account for some of these differences.     

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.     

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.     

Reproductive parameters of female orangutans (Pongo pygmaeus wurmbii) 1971–2011, a 40-year study at Tanjung Puting National Park, Central Kalimantan, Indonesia

This study presents reproductive parameter data gathered by direct observation over a 40-year period (1971–2011) of the provisioned free-ranging population of orangutans at Camp Leakey in Tanjung Puting National Park, Central Kalimantan, Indonesia. Age at first reproduction, interbirth interval (IBI), sex ratio at birth, and infant mortality for 19 female orangutans (11 first-generation wild-born ex-captive mothers and 8 second-generation mothers) are included in this analysis. Age at first reproduction among the first-generation mothers was similar to that among wild orangutans, while second-generation mothers had a significantly earlier age at first reproduction. IBIs were similar among first- and second-generation mothers and were significantly shorter than those recorded in studies of wild orangutan populations. There was an expected male-biased sex ratio at birth and a slightly higher than expected rate of infant mortality when compared to wild populations. Infant mortality was primarily seen among second-generation mothers who gave birth before the age of 12, and among first births of some first-generation mothers. These results lend support to the ecological energetics hypothesis, which predicts that increased diet quality leads to a faster rate of reproduction.     

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.     

Modeling dietary selectivity by Bornean orangutans: Evidence for integration of multiple criteria in fruit selection

Food patch visitation was compared to the availability of fruit patches of different species during 2 years in a Bornean lowland forest to examine orangutan (Pongo pygmaeus) diet selectivity. Feeding on both the pulp and the seeds of nonfig fruit varied directly with fruit patch availability, demonstrating preference for these foods over fig fruit or other plant parts (bark or leaves). Factors determining fruit selectivity rank were examined through multiple regression analysis. Modeling selectivity for 52 chemically unprotected primate-fruit pulp species revealed strong preferences for species of (i) large crop size (numbers of fruits ripening in an individual patch), (ii) high pulp weight/fruit, and (iii) high pulp mass per swallowed unit of pulp + seed, demonstrating orangutan sensitivity especially to patch size (g of pulp or total energy/patch) and perhaps to fruit handling time. Modeling selectivity for 18 fig species showed that 4 factors significantly influenced fig species rank: crop size, pulp weight/fruit, and 2 chemical variables, percentage digestible carbohydrate and percentage phenolic compounds in the fig fruit pulp. The selectivity rank based on the overall nutrient gain from feeding in the fruit patch (the product of the first 3 variables) is proportionally depressed by the percentage tannin content, demonstrating that orangutans integrate values for these variables in selecting fig patches. The conclusions from these results and from analysis of selectivity for seeds and for other fruit types are that orangutan foraging decisions are strongly influenced by the meal size expected from a feeding visit (i.e., by patch size), that tannins and other toxins deter feeding, and that the energy content, rather than the protein content, of foods is important in diet selection. The foraging strategy of orangutans is interpreted relative to these results and to Bornean fruiting phenology. By integrating spatial, morphometric, and chemical variables in analysis, this study is the first to demonstrate the application of foraging theory to separate out the key variables that determine diet selection in a primate. Multivariate analysis should routinely be applied to such data to distinguish among the many covarying attributes of food items and patches; inferences drawn in previous studies of primate diet selection, which ignore key spatial and morphological variables and rely on univariate correlations, are therefore suspect.     

Male and female western gorilla diet: Preferred foods,use of fallback resources,and implications for ape versus old world monkey foraging strategies

Most of what is currently known about western gorilla (Gorilla gorilla) diet is based on indirect studies using fecal samples and trail signs rather than measures based on direct observations. Here we report results on adult male and female western gorilla foraging behavior, based on systematic focal observations and nutritional analyses of foods. We found that western gorillas, like other apes, are highly selective ripe fruit specialists, seeking fruit high in energy, low in antifeedants, and rare in the environment. During seasonal fruiting peaks, fruit accounted for up to 70% of feeding time. When ripe fruit was scarce, gorillas increased time spent feeding on leaves and nonpreferred fruits and herbs. Leaves were the major fallback food, accounting for up to 70% of feeding time in males and 50% in females during periods of fruit scarcity. In spite of large differences in body size, the sexes were remarkably similar in their overall diet, not differing in time spent feeding on fruit or preferred herbs. However, the male consistently fed more often and on a greater variety of leaves than did females, whereas females fed more often on fallback herbs and termites. Our findings, when considered in light of previous findings on sympatric mangabeys, indicate that the foraging strategy of western gorillas is broadly similar to that of chimpanzees and orangutans, and distinct from that of old world monkeys. Am J Phys Anthropol 140:727–738, 2009. © 2009 Wiley-Liss, Inc.     

Dietary and Energetic Responses of Pongo abelii to Fruit Availability Fluctuations

Like many primates, orangutans face fluctuations in fruit availability. We show that in Ketambe (Sumatra), fruit availability fluctuations have very little influence on orangutan diet. Most importantly, the percentages of fruits including figs, fruits excluding figs, and figs in their diet do not differ significantly between periods of varying fruit availability. In addition, there is no trace of ketones in orangutan urine samples during periods of varying fruit availability. Unlike 1 orangutan population in Borneo, orangutans in Sumatra experience no prolonged negative energy budget because of fluctuations in fruit availability. Dietary data from other Sumatran and Bornean orangutan populations indicate that the pattern might be representative for a more general difference between Sumatra and Borneo, and we discuss how this might have affected orangutan reproduction and life history for the 2 species.     

Feeding ecology of the long-tailed macaque(Macaca fascicularis) in Kalimantan Tengah,Indonesia

I studied long- tailed macaque (Macaca fascicularis)feeding behavior and ecology as part of a larger behavioral ecological study at the Natai Lengkuas Station, Tanjung Puting National Park, Kalimantan Tengah, Indonesia. I collected data on feeding behavior via scan sampling of all visible individuals in the focal group (approximately 800 observation hours). I established vegetational plots and monitored them monthly to determine food availability and abundance. I found long- tailed macaques to be primarily frugivorous;leaves, flowers, insects and bark provided the remainder of the diet. They used at least 33 plant species as food sources, but >60% of the diet was provided by only 5 species. Based on previous vegetational analyses, these tree species were among the highest in relative density. However, selection ratios for 19 food species indicate that 13 of them were selected more often than expected. Long- tailed macaques appear to be selective feeders but can exploit a variety of food sources during periods of food scarcity.     

Seasonal variation in the feeding behavior and diet of Japanese macaques (Macaca fuscata yakui) in lowland forest of Yakushima

The feeding behavior of the southern subspecies of Japanese macaque (Macaca fuscata yakui) was studied over a period of 18 months in warm temperate broad-leaved forest on the island of Yakushima, Japan. Focal animal data were collected for the eight adults in the troop. Over a full annual cycle, 35.0% of foraging on identified foods was on leaves and shoots, 30.2% on fleshy fruit, 13.2% on seeds, and 5.5% on flowers. Invertebrates and other animal matter accounted for 10.3% of foraging and fungi for 4.6%. There was marked seasonal variation in the use of different food categories, and seeds, leaves, fleshy fruit, and animal matter were each predominant at different times of year. There was also evidence of annual cyclicity in patterns of foraging on all major food types. The monkeys spent less time moving and ate a greater variety of foods when feeding on leaves than when feeding on fruit and seeds, or on insects. Time spent foraging was positively correlated with diversity of the diet, but there was no simple relationship between time spent foraging and the predominant food type. This suggests that a wide variety of foods takes longer to harvest and process, irrespective of the food type. The diet of the study troop was flexible and could not be assigned to a simple dietary category, such as frugivorous or folivorous. If these data are representative of the subspecies, the Yakushima macaque is much more of a dietary generalist than most primates for which there are adequate data. Am. J. Primatol. 43:305–322, 1997. © 1997 Wiley-Liss, Inc.     

Seasonal patterns of diet and ranging in two species of tamarin monkeys: Stability versus variability

From June through December, data were collected on the diet and ranging patterns of moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarin monkeys in the Amazon Basin of northeastern Peru. During this 7-month period, insects and nonleguminous fruits accounted for 83% of tamarin feeding and foraging time. Despite marked seasonal variation in rainfall and forest productivity, patterns of habitat utilization, day range, dietary diversity, resource exploitation, and activity budget remained relatively stable throughout the year. Moustached and saddle-back tamarins appear to solve problems of food acquisition and exploit patchily distributed feeding sites using a relatively limited set of foraging patterns. In general, these primates concentrate their daily feeding efforts on several trees from a small number of target plant species. These feeding sites are uncommon, produce only a small amount of ripe fruit each day, and are characterized by a high degree of intraspecific fruiting and flowering synchrony. Trees of the same species are frequently visited in succession, and individual feeding sites are revisited several times over the course of 1–2 weeks. This type of foraging pattern occurred during both dry and wet seasons and when exploiting fruit, nectar, legume, and exudate resources. Seasonal variation in the percentage of feeding and foraging time devoted to insectivory was also limited. In this investigation, there was no consistent evidence that temporal changes in overall forest fruit production had a major impact on the feeding, foraging, or ranging behavior of either tamarin species.     

Apes in space: saving an imperilled orangutan population in Sumatra

Deforestation rates in Sumatra are amongst the highest in the tropics. Lowland forests, which support the highest densities of orangutans, are particularly vulnerable to clearance and fragmentation because they are highly accessible. Consequently, many orangutans will, in the future, live in strictly or partially isolated populations. Whilst orangutans have been extensively studied in primary forests, their response to living in human-dominated landscapes remains poorly known, despite it being essential for their future management. Here, we focus on an isolated group of critically endangered Sumatran orangutans (Pongo abelii) that co-exist with farmers in a mixed agroforest system consisting of degraded natural forest, smallholder (predominantly rubber) farms and oil palm plantations. Over 24 months we conducted the first ever spatial assessment of orangutan habitat use in the human-transformed landscape of Batang Serangan, North Sumatra. From 1,204 independent crop-raiding incidents recorded, orangutans showed strong foraging preference for mixed farmland/degraded forest habitat over oil palm patches. The core home range areas of the eight adult orangutans encompassed only 14% of the available study area. Monthly home range sizes averaged 423 ha (±139, SD) for males, and 131 ± 46 ha for females, and were positively influenced by wild and cultivated fruit presence, and by crop consumption. The average daily distance travelled was similar for both adult males (868 m ± 350, SD) and females (866 m ± 195), but increased when orangutans raided crops. These findings show that orangutans can survive, demographically, in certain types of degraded landscapes, foraging on a mixture of crops and wild fruits. However, the poor quality habitat offered to orangutans by oil palm plantations, in terms of low food availability and as a barrier to female movements, is cause for concern since this is the land use type that is most rapidly replacing the preferred forest habitat across both Sumatran and Bornean orangutan ranges.     

Foraging habits of Alouatta palliata mexicana in three forest fragments

The activity patterns and diet of howler monkeys (Alouatta palliata mexicana) were studied in 3 forest fragments in south-eastern Mexico: Playa Escondida (PLA), Agaltepec Island (AGA) and Arroyo Liza (LIZ). Intersite differences offered the opportunity to investigate the foraging adaptations of howler monkeys in response to population and habitat size. In the largest fragment (PLA), the howlers' diet was based on high-quality items (fruit and young leaves). In AGA, where the density of howlers was the highest, their diet was mostly folivorous with a marked exploitation of uncommon food items such as vines, lianas, shrubs and herbs. The dietary differences in AGA were accompanied by more time spent travelling and less time spent resting. Although LIZ was the smallest fragment and had a high howler density, the small group size and the use of energy-minimizing strategies (less time spent travelling and more time spent resting) probably allowed howlers to maintain a frugivorous diet.     

Ecological Constraints on the Foraging Effort of Western Gorillas (Gorilla gorilla gorilla) at Bai Hoköu, Central African Republic

Recent studies demonstrate that western lowland gorillas incorporate much more fruit into their diet than Virunga mountain gorillas do. Very little is known, however, about how the frugivorous behavior of western gorillas influences their daily ranging behavior, which may ultimately affect social factors such as group size and structure. I examined the influence of diet and the spatiotemporal availability of plant foods on the foraging effort of nonhabituated western lowland gorilla groups during 17 months at Bai Hoköu in the Dzanga-Ndoki National Park, Central African Republic. I determined diet from indirect methods and gorilla plant food availability and spatial distribution from phenology and line transects. Daily path length gives an estimate of foraging effort and was the distance paced, following fresh gorilla trails, from morning to evening nest sites. The availability and distribution of fruit and its consumption by gorillas varied seasonally. When concentrating on fruits, gorillas traveled significantly farther (mean = 3.1 km/day) than when their diet consisted mostly of nonfruit vegetation, such as leaves and woody pith, stems, and bark (mean = 2.1 km/day). The amount of herbaceous vegetation in the diet did not vary seasonally and did not influence daily path length. The best environmental predictor of foraging effort was fruit density, or a measure combining both density and spatial pattern: coefficient of dispersion. In addition, when fruit patches were small, path length tended to increase but not significantly. Compared with results of other studies, gorillas at Bai Hoköu travel farther (mean = 2.6 km/day) than gorillas in Gabon (mean = 1.7 km/day) and five times farther than mountain gorillas in the Virungas (mean = 0.5 km/day). Increased foraging effort of gorillas in this region, especially during the fruiting season, may have profound effects on group size and structure.     

A Case Study of Orangutan and Siamang Behavior Within a Mixed-Species Zoo Exhibit

This empirical case study assessed the behavior and welfare of 2 orangutans (Pongo abelii) and 2 siamangs (Symphalangus syndactylus) within a mixed-species zoo exhibit. The study used instantaneous scan-sampling to record behavior, location, and interspecies proximity over 174 hr and all-occurrences data for any interactions between species. Results revealed frequent affiliative interactions between the female orangutan and siamang pair and an absence of agonistic or aggressive encounters. All individuals used the majority of the exhibit without segregation by species. Both orangutans spent most of their time on the ground (above 70% of all scans), and low levels of foraging were identified (1–4% of scans for all individuals). Overall, the findings support the notion that mixed-species exhibits may be enriching to the species involved through increased stimulation and opportunities for interaction. A poststudy incident also highlights the need for careful and continual monitoring of mixed-species exhibits over time.     

The orangutan long call and snag crashing at Tanjung Puting Reserve

The long call, which is only given by adult males, is the most frequently uttered orangutan vocalization and the only one which can be heard over long distances. At the Orangutan Research and Conservation Project study area in the Tanjung Puting Reserve, Central Indonesian Borneo, adult males were calling more regularly and frequently than reported from other areas in Borneo. Adult males also exhibited a behavior, not reported elsewhere, sometimes associated with the vocalization of long calls: the pushing over of large snags (branchless dead trees) to the ground. At Tanjung Puting long calls functioned primarily to mediate dominance relationships among adult males who rarely came into direct contact with one another. In addition, long calls may have been helping sexually receptive females locate males.     

Time Allocation Patterns of Lowland Woolly Monkeys (Lagothrix lagotricha poeppigii) in a Neotropical Terra Firma Forest

We investigated the time allocation decisions of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a terra firma forest in eastern Ecuador where they occur sympatrically with 9 other primate species. Woolly monkeys spent considerable amounts of time searching for and attempting to procure animal prey—roughly as much time as they spent consuming plant material: ripe fruits, leaves, and flowers. The amount of time spent foraging for animal prey is positively related to the habitat-wide availability of ripe fruits (the predominant component of the woolly monkey diet), and negatively related to both ambient temperature and the abundance of potential prey items in the habitat. Time spent resting showed exactly the opposite pattern with respect to these ecological variables. These results suggest that woolly monkeys follow an energy-maximizing strategy of food acquisition during times of fruit abundance—focusing on animal foods and perhaps laying down fat reserves to utilize when ecological conditions worsen—and follow an energy-minimizing strategy when fruit resources are scarce. Such a strong and seasonal commitment to animal prey foraging is unique among the ateline primates and is not ubiquitous even among lowland woolly monkeys. We suggest that this foraging strategy, and the greater intragroup cohesion that characterizes some populations of Lagothrix, are both opportunistic responses to regional differences in habitat quality. Identifying and accounting for such intraspecific variation should be a goal of any analysis of comparative socioecology.     

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.