Experiments have shown that captive great apes are capable of observational learning, and patterns of cultural variation among populations suggest that they use this capacity in the wild. So far, the contexts and extent of observational forms of social learning in the wild remain unclear. Social learning is expected to be most pronounced during the skill acquisition of immature individuals. We therefore examined peering (attentive close range watching) by immatures in two populations of wild orangutans (Pongo spp.). A total of 1537 peering events collected during 2571 observation hours were analysed. We found, first, that peering was most frequent in contexts where learning is expected, namely feeding and nest building. Second, peering in the feeding context was significantly positively correlated with complexity of food processing and negatively with an item's frequency in the mother's diet. Food peering was also followed by significantly increased rates of exploratory behaviours targeting the same food items, indicating that it leads to selective practice. Food peering also decreased with age and increasing feeding competence of the immatures. Third, the age of peak peering in the nesting context coincided with the onset of nest-practice behaviour, and peering events were followed by significantly increased rates of nest-practice behaviour. Fourth, the proportion of peering directed at other individuals rather than the mother increased with age. These findings are consistent with the prediction that immature orang-utans learn by observing others in a variety of contexts and that peering is followed by selective practice of the observed behaviour. We conclude that observational social learning in combination with socially induced practice over a period of several years is a critical component of the acquisition of learned subsistence skills in orang-utans.

Abstract

Several studies have suggested that wild primates tend to behave with caution toward novelty, whereas captive primates are thought to be less neophobic, more exploratory, and more innovative. However, few studies have systematically compared captive and wild individuals of the same species to document this "captivity effect" in greater detail. Here we report the responses of both wild and captive orangutans to the same novel items. Novel objects were presented to wild orangutans on multiple platforms placed in the canopy and equipped with motion-triggered video cameras. The same and different novel objects were also presented to orangutans in two different zoos. The results demonstrate extreme conservatism in both Bornean and Sumatran wild orangutans, who gradually approached the novel objects more closely as they became familiar, but avoided contact with them over many encounters spanning several months. Their zoo-living conspecifics, in contrast, showed an immediate neophilic response. Our results thus confirm the "captivity effect." To the various ecological explanations proposed before (reduced risk and increased time and energy balance for captive individuals relative to wild ones), we add the social information hypothesis, which claims that individuals confronted with novel items preferentially rely on social cues whenever possible. This caution toward novelty disappears when human caretakers become additional role models and can also be eroded when all experience with novelty is positive.

Orangutans (Pongo spp.) are reported to have extremely slow life histories, including the longest average interbirth intervals of all mammals. Such slow life history can be viable only when unavoidable mortality is kept low. Thus, orangutans' survivorship under natural conditions is expected to be extremely high. Previous estimates of orangutan life history were based on captive individuals living under very different circumstances or on small samples from wild populations. Here, we combine birth data from seven field sites, each with demographic data collection for at least 10 years (range 12-43 years) on wild orangutans to better document their life history. Using strict criteria for data inclusion, we calculated infant survival, interbirth intervals and female age at first reproduction, across species, subspecies and islands. We found an average closed interbirth interval of 7.6 years, as well as consistently very high pre-weaning survival for males and females. Female survival of 94% until age at first birth (at around age 15 years) was higher than reported for any other mammal species under natural conditions. Similarly, annual survival among parous females is very high, but longevity remains to be estimated. Current data suggest no major life history differences between Sumatran and Bornean orangutans. The high offspring survival is remarkable, noting that modern human populations seem to have reached the same level of survival only in the 20th century. The orangutans' slow life history illustrates what can be achieved if a hominoid bauplan is exposed to low unavoidable mortality. Their high survival is likely due to their arboreal and non-gregarious lifestyle, and has allowed them to maintain viable populations, despite living in low-productivity habitats. However, their slow life history also implies that orangutans are highly vulnerable to a catastrophic population crash in the face of drastic habitat change. ABSTRACT 28 Orangutans (Pongo spp.) are reported to have extremely slow life histories, including the 29 longest average interbirth intervals of all mammals. Such slow life history can be viable only 30 when unavoidable mortality is kept low. Thus, orangutans' survivorship under natural 31 conditions is expected to be extremely high. Previous estimates of orangutan life history were 32 based on captive individuals living under very different circumstances or on small samples from 33 wild populations. Here, we combine birth data from seven field sites, each with demographic 34 data collection for at least 10 years (range 12-43 years) on wild orangutans to better document 35their life history. Using strict criteria for data inclusion, we calculated infant survival, interbirth 36 intervals and female age at first reproduction, across species, subspecies and islands. We found 37 an average closed interbirth interval of 7.6 years, as well as consistently very high pre-weaning 38 survival for males and females. Female survival of 94% until age at first birth (at around age 15 39 years) was higher than rep...

BackgroundOrangutans have one of the slowest-paced life histories of all mammals. Whereas life-history theory suggests that the time to reach adulthood is constrained by the time needed to reach adult body size, the needing-to-learn hypothesis instead suggests that it is limited by the time needed to acquire adult-level skills.To test between these two hypotheses, we compared the development of foraging skills and growth trajectories of immature wild orangutans in two populations: at Tuanan (Pongo pygmaeus wurmbii), Borneo, and Suaq Balimbing (Pongo abelii), Sumatra. We collected behavioral data on diet repertoire, feeding rates and ranging competence during focal follows, and estimated growth through non-invasive laser photogrammetry.ResultsWe found that adult-like diet repertoires are attained around the age of weaning and that female immatures increase their repertoire size faster than their male peers. Adult-level feeding rates of easy techniques are reached just after weaning, but several years later for more difficult techniques, albeit always before adulthood (i.e. age at first reproduction). Independent immatures had faster feeding rates for easy to process items than their mothers, with male immatures achieving faster feeding rates earlier in development relative to females. Sumatran immatures reach adult-level feeding rates 2–3 years later than their Bornean peers, in line with their higher dietary complexity and later weaning. The range-use competence of independently ranging and weaned immatures is similar to that of adult females. Body size measurements showed, immatures grow until female age of first reproduction.ConclusionsIn conclusion, unlike in humans, orangutan foraging skills are in place prior to reproduction. Growth trajectories suggest that energetic constraints, rather than skills, best explain the length of immaturity. However, skill competence for dietary independence is reached later where the adult niche is more complex, which is consistent with the relatively later weaning age with increasing brain size found generally in primates, and apes in particular.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-016-0178-5) contains supplementary material, which is available to authorized users.

One contribution of 15 to a theme issue 'Innovation in animals and humans: understanding the origins and development of novel and creative behaviour'. 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.

Humans stand out among primates and other mammals in reaching adult-level foraging skills very late in development, well after the onset of reproduction. The aim of this paper is to place this unusual human skill development into a broader comparative context. Among birds and mammals in general, duration of immaturity, indexed by age at first reproduction (AFR), and adult brain size have undergone correlated evolution. This pattern is consistent with two causal processes: AFR is either limited by the time needed to learn adult-level skills (needing to learn) or by the energy needed to grow brain and body to full size (energetic constraints). We tested predictions arising from these two hypotheses with data retrieved from the published literature for 57 mammal and bird species. First, most mammals reach adult-level foraging skills well before the developmental period is completed, implying that energy constraints determine the age at first reproduction, whereas most birds reach adult-level foraging skills around the time of maturity, suggesting time needed for skill acquisition determines the onset of reproduction. Second, within mammals we found that with increasing niche complexity, the age of adult-level skill competence moves closer to the age at first reproduction. Third, when looking at how adult-level skills can be reached later, we found that gregariousness, slow conservative development and post-weaning provisioning allow mammals to reach their skills later. Finally, in species with intense sharing of resources (such as cooperative hunters) competence in foraging skills may even reach peak values after age of first reproduction. We conclude that the human pattern of skill acquisition could arise because our hominin ancestors added cooperative breeding and hunting to the slow development they had as great apes with increasingly complex niches. This result provides a broad biological foundation for the embodied capital model.

In recent decades, researchers have increasingly documented the impact of anthropogenic activities on wild animals, particularly in relation to changes in behaviour. However, whether human-induced behavioural changes in wildlife may be considered evidence of cultural evolution remains an open question. We explored whether behavioural responses to different types of human activities in species already known to display behaviour transmitted through social learning, particularly non-human primates (NHPs), are suggestive of cultural evolution in the wild. Results indicate that human influence on NHP cultural repertoires includes the modification and disappearance of existing cultural traits, as well as the invention of novel traditions with the potential to become cultural. These examples are found mostly in the domain of food acquisition, where animals modify their diet to include new resources, and adopt novel foraging strategies to avoid humans. In summary, this paper suggests that human activities can act as a catalyst for cultural change in animals, both in terms of threatening existing traditions and fostering new ones. The current situation may echo environmental changes thought to have triggered major behavioural adaptations in our own evolutionary history and thus be useful for research on human cultural evolution. As wildlife is increasingly exposed to humans and their activities, understanding how animal behaviour patterns and cultures are impacted and change in response to anthropogenic factors is of growing conservation importance.