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.     

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.     

Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella)

It has been reported that wild capuchin monkeys exhibit several group-specific behavioural traditions. By contrast, experiments have found little evidence for the social learning assumed necessary to support such traditions. The present study used a diffusion chain paradigm to investigate whether a novel foraging task could be observationally learned by capuchins (Cebus apella) and then transmitted along a chain of individuals. We used a two-action paradigm to control for independent learning. Either of two methods (lift or slide) could be used to open the door of a foraging apparatus to retrieve food. Two chains were tested (N1=4; N2=5), each beginning with an experimenter-trained model who demonstrated to a partner its group-specific method for opening the foraging apparatus. After the demonstration, if the observer was able to open the apparatus 20 times by either method, then it became the demonstrator for a new subject, thus simulating the spread of a foraging tradition among 'generations' of group members. Each method was transmitted along these respective chains with high fidelity, echoing similar results presently available only for chimpanzees and children. These results provide the first clear evidence for faithful diffusion of alternative foraging methods in monkeys, consistent with claims for capuchin traditions in the wild.     

Social networks predict patch discovery in a wild population of songbirds

Animals use social information in a wide variety of contexts. Its extensive use by individuals to locate food patches has been documented in a number of species, and various mechanisms of discovery have been identified. However, less is known about whether individuals differ in their access to, and use of, social information to find food. We measured the social network of a wild population of three sympatric tit species (family Paridae) and then recorded individual discovery of novel food patches. By using recently developed methods for network-based diffusion analysis, we show that order of arrival at new food patches was predicted by social associations. Models based only on group searching did not explain this relationship. Furthermore, network position was correlated with likelihood of patch discovery, with central individuals more likely to locate and use novel foraging patches than those with limited social connections. These results demonstrate the utility of social network analysis as a method to investigate social information use, and suggest that the greater probability of receiving social information about new foraging patches confers a benefit on more socially connected individuals.     

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.     

Use of Social and Ecological Information in Tamarin Foraging Decisions

A major consequence of group living is that foragers may rely on social information in addition to ecological information to locate feeding sites. Although conspecifics can provide cues as to the spatial location of food patches, individual foraging decisions also must include some assessment of the likelihood of obtaining access to a resource other group members seek. This likelihood differs in the 2 models generally proposed to explain intragroup social foraging: the information-sharing model and the producer-scrounger model. We conducted an experimental field study on wild groups of emperor (Saguinus imperator) and saddleback (S. fuscicollis) tamarins to determine the foraging strategies adopted by individual group members and their relationship to social rank, food intake, and the ability to use ecological and social information in making intra-patch foraging decisions. Individual tamarins applied different behavioral strategies compatible with a finder-joiner paradigm to solve foraging problems. About half of the individuals in each study group initiated 74%–90% of all food searches and acted as finders. Most alpha individuals adopted a joiner strategy by monitoring the activities of others' to obtain a reward. The individual arriving first at a reward platform enjoyed a finder's advantage. Despite differences in search effort, both finders and joiners presented similar abilities in learning to associate ecological cues with the presence of food rewards at our experimental feeding stations. We conclude that within a group foraging context, tamarins integrate social and ecological information in decision-making.     

Fragility of Traditions: The Disturbance Hypothesis for the Loss of Local Traditions in Orangutans

Chimpanzees and orangutans have increasingly well documented local traditions involving learned skillful behaviors, often involving tools, which vary from place to place and are maintained by social transmission. These local traditions are most likely the antecedents of human culture. The complexity of local traditions is thought largely to be a function of the cumulative frequency of opportunities for social learning, and hence of the extent of tolerant gregarious foraging. Data on orangutans and chimpanzees are consistent with this hypothesis. This reliance on continued social transmission makes local traditions vulnerable to interruptions of transmission. I examine the disturbance hypothesis, which suggests that local extinction, hunting pressure, selective logging, and habitat loss in general affect the key parameters of the transmission process—innovation, diffusion, horizontal transmission—and hence will significantly impoverish the repertoire of complex skills for subsistence. Given current trends in orangutan habitats, serious erosion of local traditions is taking place. I also speculate that disturbance in the past has led to a significant loss of orangutan traditions.     

Food Competition Between Wild Orangutans in Large Fig Trees

Orangutans are usually solitary. However, occasionally aggregations are formed, especially in large fruiting fig trees. Individuals in these aggregations may experience scramble or contest competition for food. We investigated the type and strength of food competition in large figs among wild Sumatran orangutans. Adult males foraged more efficiently than adult females and subadult males did. The availability of ripe fruit is positively related to the number of orangutans visiting a fig tree and their foraging efficiency. The number of orangutans in a fig tree did not affect patch residence time and foraging behavior, though orangutans spent more time feeding when aggregation size increased in a fig tree. Dominance relationships could be measured in a number of dyads. Differences in dominance did not affect foraging behavior. The patch residence time of subordinate individuals was reduced on days that a dominant individual also visited the fig. In conclusion, orangutans seem to adjust aggregation size to the number of available ripe fruits in a fig tree in such a way that scramble competition was absent. Contest competition determined access to large fig trees.     

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 conditions for tool use in primates: implications for the evolution of material culture

In order to identify the conditions that favored the flourishing of primate tool use into hominid technology, we examine inter- and intraspecific variation in manufacture and use of tools in extant nonhuman primates, and develop a model to account for their distribution. We focus on tools used in acquiring food, usually by extraction. Any model for the evolution of the use of feeding tools must explain why tool use is found in only a small subset of primate species, why many of these species use tools much more readily in captivity, why routine reliance on feeding tools is found in only two species of ape, and why there is strong geographic variation within these two species. Because ecological factors alone cannot explain the distribution of tool use in the wild, we develop a model that focuses on social and cognitive factors affecting the invention and transmission of tool-using skills. The model posits that tool use in the wild depends on suitable ecological niches (especially extractive foraging) and the manipulative skills that go with them, a measure of intelligence that enables rapid acquisition of complex skills (through both invention and, more importantly, observational learning), and social tolerance in a gregarious setting (which facilitates both invention and transmission). The manipulative skills component explains the distribution across species of the use of feeding tools, intelligence explains why in the wild only apes are known to make and use feeding tools routinely, and social tolerance explains variation across populations of chimpanzees and orangutans. We conclude that strong mutual tolerance was a key factor in the explosive increase in technology among hominids, probably intricately tied to a lifestyle involving food sharing and tool-based processing or the acquisition of large, shareable food packages.     

Intra-and interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: implications for the invention of tool use

Tool manufacture and use have been described for wild orangutans (Pongo pygmaeus), with appreciable interpopulational differences in tool complexes. The ecological factors that contribute to these differences require investigation. Significant interpopulational differences in diet suggest that ecological factors contribute to variation in tool-based insect foraging. Using 4 years of behavioral data from the Suaq Balimbing Research Station (Sumatra, Indonesia), we tested predictions of two ecological hypotheses for the invention of tool use for insect foraging. We found limited evidence for inter- and intrasexual differences, as well as temporal variation, in activity budget and diet. However, differences did not correspond to variation in either rate of tool use or specialization on tool-based insectivory. Compared to other populations, orangutans at Suaq Balimbing ate significantly more insects. Low temporal variation in insectivory and an abundance of social insects at Suaq Balimbing suggest that insects formed a staple in the diet rather than a fallback food. Our findings do not support the hypothesis that tool use is a response to the low availability of primary food sources. Rather, greater opportunities for invention likely contributed to insect-extraction tool use at Suaq Balimbing.     

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.     

Cross-site differences in foraging behavior of white-faced capuchins (Cebus capucinus)

Researchers have identified a variety of cross-site differences in the foraging behavior of free-ranging great apes, most notably among chimpanzees (Pan troglodytes) and more recently orangutans (Pongo pygmaeus), that are not due to obvious genetic or ecological differences. These differences are often referred to as "traditions." What is not known is whether this high level of interpopulation variation in behavior is limited to hominoids. In this study, we use long-term data from three Costa Rican field sites that are geographically close and similar ecologically to identify potential foraging traditions in white-faced capuchins (Cebus capucinus). Foraging traditions are predicted in Cebus because of many behavioral and morphological convergences between this genus and the great apes. The processing techniques used for the same food species were compared across sites, and all differences found were classified as present, habitual, or customary. Proximity data were also analyzed to determine if social learning mechanisms could explain variation in foraging behavior. Of the 61 foods compared, we found that 20 of them are processed differently by capuchins across sites. The differences involve pound, rub, tap, "fulcrum," "leaf-wrap," and "army ant following." For most of the differences with enough data to analyze, the average proximity score of the "matched" dyads (two individuals within a group who shared a "different" processing technique) was statistically higher than the average proximity score of the remaining "unmatched" dyads.     

Diet traditions in wild orangutans

This study explores diet differences between two populations of wild Bornean orangutans (Pongo pygmaeus wurmbii) to assess whether a signal of social learning can be detected in the observed patterns. The populations live in close proximity and in similar habitats but are separated by a river barrier that is impassable to orangutans in the study region. We found a 60% between‐site difference in diet at the level of plant food items (plant species–organ combinations). We also found that individuals at the same site were more likely to eat the same food items than expected by chance. These results suggest the presence of diet (food selection) traditions. Detailed tests of three predictions of three models of diet acquisition allowed us to reject a model based on exclusive social learning but could not clearly distinguish between the remaining two models: one positing individual exploration and learning of food item selection and the other one positing preferential social learning followed by individual fine tuning. We know that maturing orangutans acquire their initial diet through social learning and then supplement it by years of low‐level, individual sampling. We, therefore, conclude that the preferential social learning model produces the best fit to the geographic patterns observed in this study. However, the very same taxa that socially acquire their diets as infants and show evidence for innovation‐based traditions in the wild paradoxically may have diets that are not easily distinguished from those acquired exclusively through individual learning. Am J Phys Anthropol 143:175–187, 2010. © 2010 Wiley‐Liss, Inc.     

Neophobia and learning mechanisms: how captive orangutans discover medicinal plants

Great apes sometimes feed on items of low nutritional value with bioactive secondary compounds. These molecules may be toxic and neophobia is presumed to be an essential factor in avoiding the ingestion of noxious items. The aim of this study is to investigate, in captive orangutans, individual and social learning involved in the discovery and ingestion of new items. We presented novel aromatic plants - 11 fresh plants and 4 infused plants - to 4 captive weaned Bornean orangutans, both under isolated and group conditions, and recorded their behaviour and interactions between group members. All animals tasted by nibbling or ingested most of the plants presented. Regardless of the experimental condition, individual responses did not vary visibly across the sessions, despite numerous close observations, and food transfers between individuals were observed. Our results suggest that a low level of neophobia and a strong propensity to look to conspecifics for information allow Bornean orangutans to expand their diet after weaning. Our results also provide some evidence that olfaction is a key sense in determining food edibility based on previous experience.     

Observer choices during experimental foraging tasks in brown capuchin monkeys (Cebus apella)

We investigated whether capuchin monkeys (Cebus apella) would choose to observe a high- or low-status adult female from their group during experimental foraging tests. The subject was located in the center of a test chamber, with a low- and high-ranking demonstrator on either side of two partitions. A peephole allowed the subject to observe the models by looking through either respective partition. Each model was trained on one of the two different methods, lift or pull, for retrieving food from a foraging apparatus. There were 22 subjects and four models. During the 40-trial test sessions, subjects could choose which model they would watch in each trial. It was predicted that subjects would prefer observing the model with whom it was closer in rank, and therefore share greater affiliation with. Results showed that only half the subjects showed a preference and that preference was not linked to status. Relatedness played a larger role in determining if a subject showed a preference for a model, and a correlation was found for relatedness and observer preference. After the observer preference tests, subjects were presented with the foraging apparatus to determine if they displayed a preference for one of the two tasks. The majority of subjects (17/22) showed a preference for the pull method, suggesting that this method may have been more salient to the monkeys in this study.     

Location effects of social partner on experimental foraging in the squirrel monkey

The effect of social context on experimental foraging in squirrel monkeys (Saimiri sciureus) was investigated. The 12 subjects comprised six pairs in which strong social preference and attraction had been demonstrated during observations of a stable group. Individuals were first trained to discriminate spatially separated rich and poor foraging bins containing 75% and 25% of the food items, respectively, with their partners restrained equidistant from the two bins. The monkeys invested an average of 75.5% of their foraging time in the rich bin. Each individual was then tested with its partner restrained in different locations relative to the bins to determine the effect of partner proximity on foraging patterns. Foraging efficiency at the start of a session was enhanced when the partner was restrained adjacent to the rich bin compared to restraint away from this bin. Over an entire foraging session, however, all conditions providing partner accessibility were similar in yielding enhanced foraging efficiency compared to partner absence. Little time was spent in close physical proximity to the partner under any condition. It is suggested that accessibility of the social partner, rather than close physical proximity, has an important influence on the foraging squirrel monkey. © 1995 Wiley-Liss, Inc.     

Interspecific social networks promote information transmission in wild songbirds

Understanding the functional links between social structure and population processes is a central aim of evolutionary ecology. Multiple types of interactions can be represented by networks drawn for the same population, such as kinship, dominance or affiliative networks, but the relative importance of alternative networks in modulating population processes may not be clear. We illustrate this problem, and a solution, by developing a framework for testing the importance of different types of association in facilitating the transmission of information. We apply this framework to experimental data from wild songbirds that form mixed-species flocks, recording the arrival (patch discovery) of individuals to novel foraging sites. We tested whether intraspecific and interspecific social networks predicted the spread of information about novel food sites, and found that both contributed to transmission. The likelihood of acquiring information per unit of connection to knowledgeable individuals increased 22-fold for conspecifics, and 12-fold for heterospecifics. We also found that species varied in how much information they produced, suggesting that some species play a keystone role in winter foraging flocks. More generally, these analyses demonstrate that this method provides a powerful approach, using social networks to quantify the relative transmission rates across different social relationships.     

Raiders of the lost bark: orangutan foraging strategies in a degraded landscape

Deforestation is rapidly transforming primary forests across the tropics into human-dominated landscapes. Consequently, conservationists need to understand how different taxa respond and adapt to these changes in order to develop appropriate management strategies. Our two year study seeks to determine how wild Sumatran orangutans (Pongo abelii) adapt to living in an isolated agroforest landscape by investigating the sex of crop-raiders related to population demographics, and their temporal variations in feeding behaviour and dietary composition. From focal animal sampling we found that nine identified females raided cultivated fruits more than the four males. Seasonal adaptations were shown through orangutan feeding habits that shifted from being predominantly fruit-based (56% of the total feeding time, then 22% on bark) to the fallback food of bark (44%, then 35% on fruits), when key cultivated resources such as jackfruit (Artocarpus integer), were unavailable. Cultivated fruits were mostly consumed in the afternoon and evening, when farmers had returned home. The finding that females take greater crop-raiding risks than males differs from previous human-primate conflict studies, probably because of the low risks associated (as farmers rarely retaliated) and low intraspecific competition between males. Thus, the behavioral ecology of orangutans living in this human-dominated landscape differs markedly from that in primary forest, where orangutans have a strictly wild food diet, even where primary rainforests directly borders farmland. The importance of wild food availability was clearly illustrated in this study with 21% of the total orangutan feeding time being allocated to feeding on cultivated fruits. As forests are increasingly converted to cultivation, humans and orangutans are predicted to come into conflict more frequently. This study reveals orangutan adaptations for coexisting with humans, e.g. changes in temporal foraging patterns, which should be used for guiding the development of specific human-wildlife conflict mitigation strategies to lessen future crop-raiding and conflicts.     

Social effects on foraging behavior and success depend on local environmental conditions

In social groups, individuals' dominance rank, social bonds, and kinship with other group members have been shown to influence their foraging behavior. However, there is growing evidence that the particular effects of these social traits may also depend on local environmental conditions. We investigated this by comparing the foraging behavior of wild chacma baboons, Papio ursinus, under natural conditions and in a field experiment where food was spatially clumped. Data were collected from 55 animals across two troops over a 5‐month period, including over 900 agonistic foraging interactions and over 600 food patch visits in each condition. In both conditions, low‐ranked individuals received more agonism, but this only translated into reduced foraging performances for low‐ranked individuals in the high‐competition experimental conditions. Our results suggest one possible reason for this pattern may be low‐ranked individuals strategically investing social effort to negotiate foraging tolerance, but the rank‐offsetting effect of this investment being overwhelmed in the higher‐competition experimental environment. Our results also suggest that individuals may use imbalances in their social bonds to negotiate tolerance from others under a wider range of environmental conditions, but utilize the overall strength of their social bonds in more extreme environments where feeding competition is more intense. These findings highlight that behavioral tactics such as the strategic investment of social effort may allow foragers to mitigate the costs of low rank, but that the effectiveness of these tactics is likely to be limited in certain environments.