Sofia I. F. Forss

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.

Contrasting responses to novelty by wild and captive orangutans

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. Am. J. Primatol. 77:1109–1121, 2015.

Observational social learning and socially induced practice of routine skills in immature wild orang-utans

Experiments have shown that captive great apes are capable of observational learning, and patterns of cultural variation between 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 orang-utans, Pongo spp. We found, first, that peering was most frequent in contexts in which 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 items frequency in the mothers 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 this 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.

Cognitive differences between orang-utan species: a test of the cultural intelligence hypothesis.

Cultural species can - or even prefer to - learn their skills from conspecifics. According to the cultural intelligence hypothesis, selection on underlying mechanisms not only improves this social learning ability but also the asocial (individual) learning ability. Thus, species with systematically richer opportunities to socially acquire knowledge and skills should over time evolve to become more intelligent. We experimentally compared the problem-solving ability of Sumatran orang-utans (Pongo abelii), which are sociable in the wild, with that of the closely related, but more solitary Bornean orang-utans (P. pygmaeus), under the homogeneous environmental conditions provided by zoos. Our results revealed that Sumatrans showed superior innate problem-solving skills to Borneans, and also showed greater inhibition and a more cautious and less rough exploration style. This pattern is consistent with the cultural intelligence hypothesis, which predicts that the more sociable of two sister species experienced stronger selection on cognitive mechanisms underlying learning.

Development of foraging skills in two orangutan populations: needing to learn or needing to grow?

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.

Orientation toward humans predicts cognitive performance in orang-utans

Non-human animals sometimes show marked intraspecific variation in their cognitive abilities that may reflect variation in external inputs and experience during the developmental period. We examined variation in exploration and cognitive performance on a problem-solving task in a large sample of captive orang-utans (Pongo abelii & P. pygmaeus, N = 103) that had experienced different rearing and housing conditions during ontogeny, including human exposure. In addition to measuring exploration and cognitive performance, we also conducted a set of assays of the subjects’ psychological orientation, including reactions towards an unfamiliar human, summarized in the human orientation index (HOI), and towards novel food and objects. Using generalized linear mixed models we found that the HOI, rather than rearing background, best predicted both exploration and problem-solving success. Our results suggest a cascade of processes: human orientation was accompanied by a change in motivation towards problem-solving, expressed in reduced neophobia and increased exploration variety, which led to greater experience, and thus eventually to higher performance in the task. We propose that different experiences with humans caused individuals to vary in curiosity and understanding of the physical problem-solving task. We discuss the implications of these findings for comparative studies of cognitive ability.

Explaining the Paradox of Neophobic Explorers: The Social Information Hypothesis

How animals react to novel food and objects is commonly thought of as a crucial step toward innovations. One would therefore expect innovative species to be attracted to novelty and benefit from a combination of low neophobia and a high motivation to explore. Here we draw attention to the innovation paradox: the most innovative species tend to show neophobic reactions when confronted with novel objects or food, but can use social cues to overcome their initial neophobia. Work on novelty response has highlighted the role of ecological factors as determinants of neophobia and exploration tendency. We examine social influences on novelty response and present the idea that social factors enable some species to maintain the paradoxical combination of high neophobia and high exploration tendency. We compare primates with other species, to assess the extent to which primates are unusual. We review empirical studies that show how intrinsic neophobia is generally overcome by social facilitation and social information, i.e., the presence of experts, especially in species with slow life history, probably because social information reduces risk. We also briefly discuss the role of environmental risk in reducing intrinsic neophobia, in particular its absence in captivity. We draw attention to a strong neophobia-reducing effect of being in captivity, due to humans acting as sources of social information. We propose that species showing the paradoxical combination of strong neophobia and strong exploration tendency use social information to select aspects of the environment worth exploring. The social information hypothesis thus offers an explanation for the paradox of neophobic explorers.

The effects of sociability on exploratory tendency and innovation repertoires in wild Sumatran and Bornean orangutans

It has been hypothesized that opportunities for social learning affect the size and complexity of the adult skill set of birds and mammals, their learning ability, and thus ultimately also their innovation frequency. To test these predictions we compared rates of social learning, rates of independent exploration (independent learning) and innovation repertoires between individuals of a highly sociable population of Pongo abelii at Suaq Balimbing and a less sociable population of Pongo pygmaeus wurmbii at Tuanan. Suaq immatures showed significantly higher rates of peering, even after controlling for differences in association time and diet complexity, implying that they make disproportionally greater use of their increased opportunities for social learning. As predicted, we found that immatures and adults at Suaq also showed significantly higher rates of exploratory behaviour. The difference between the individuals of the two popuations remained when controlling for association time, suggesting persistent developmental effects, intrinsic differences, or both. Accordingly, Suaq animals had a larger set of learned skills and a higher mean dietary complexity. Our findings show that population level sociability, individual rates of exploration and population-wide repertoires of innovations are positively linked, as predicted.

Determinants of variation in orangutans' cognitive performance: I. effects of background and housing conditions

Classic ecological models of social groups suggest that increasing group size typically leads to a decrease in both individual predation risk and net food intake, with optimal group size being a compromise between these benefits and costs. Among rainforest primates, the main antipreda-tor benefits of sociality are thought to result from the dilution effect and collective detection of predators. However, recent research suggests that vegetation density in rainforest habitats limits the benefits of collective detection against ambush predators such as raptors, felids and snakes. Further, while larger groups are acknowledged to be more conspicuous to predators, it is widely assumed that this cost is unlikely to outweigh dilution benefits. Here we show in a simple model that per-individual rates of both encounters with predators and successful ambush attacks per encounter can increase with group size, under conditions likely to hold for many primate groups (when increases in group size lead to increases in group spread, conspicuousness and daily trav-el distance). Consequently, individual risk against ambush predators that employ a sit-and-wait strategy to search for prey, such as many snakes and some raptors, is lowest in small to medium-sized groups. In contrast, individuals in relatively large groups are favoured against ambush pred-ators like felids that employ a cruising strategy to search for prey, although even in this case in-creasing group size above some threshold increases individual risk. These results suggest that maximum group size among primates can be limited by increasing predation risk. Research fo-cused on primate predators is needed to determine the extent to which the model accurately re-flects their behaviour.Bushmeat hunting contributes to the decline of primate species across Africa; however, few studies have explored how such practises change over time in specific localities and how changes in land-use patterns and economic drivers may enhance threats to primates in Muslim dominated areas where, traditionally, primates are spared from such trade. The Haut Niger National Park (HNNP) is one of only two national parks in the Republic of Guinea. The park is one of the last remaining important formations of dry forest-savannah mosaics in West Africa and is a site of high conservation priority for ungulates and the western subspecies of chimpanzee. This study aimed to: (1) estimate the diversity and abundance of animal species sold for consumption across several markets in and around the HNNP, (2) analyse the evolution of the bushmeat trade since the mid-1990s, and (3) identify the players and drivers of the commercial bushmeat trade in the area. Local market assessments were conducted across four village markets and in Faranah, one of the closest urban areas abutting the HNNP. We successfully identified 5,807 wildlife carcasses of 46 species and 22 families on markets surveyed over a 7 month period spanning both the dry and wet seasons. In addition, semi-structured interviews with hunters, farmers and people involved in the bushmeat trade helped identify more recent drivers of the bushmeat trade in the HNNP. Our results indicated an increase in diversity of species targeted and the influence of crop-foraging and local microcredit systems in exacerbating the presence of primate species sold at bushmeat stalls in urban areas. Finally, whilst identifying key recommendations and gaps for future research, this study emphasises the growing risks facing primates as targets for bushmeat where people depend on agriculture and natural resource extraction for subsistence. This study complied with the International Primatological Society (IPS) Guidelines for the Use of Nonhuman Primates in Research.Comparative studies of primate grasping and manipulative behaviours in captivity have highlighted, among others, two human abilities that are generally considered unique compared with other primates: (1) the use of forceful precision and power squeeze grips involving the use of the thumb, and (2) a species-wide dominant use of one hand (usually the right hand), known as laterality. However, recent research has highlighted a diversity of precision and power grips in general among many non-human primates, and there is much debate around the potential for population-level or species-wide laterality in non-human primates. The majority of this research to date has been done on captive primates performing specific manipulative tasks, which may bias or confound these species comparisons. Comparatively little research has been done on hand use in wild primates, especially during natural, non-manipulative activities, including locomotion. Here, we investigate hand use during locomotor and non-locomotor behaviours in wild mountain gorillas ( Gorilla beringei beringei , Bwindi Impenetrable National Park, Uganda), wild chimpanzees ( Pan troglodytes verus , Tai National Park, Cote d’Ivoire) and chimpanzees kept under semi-natural conditions ( Pan troglodytes ssp., Chimfunshi Wildlife Trust, Zambia). Preliminary results propose that hand grips are similar between gorillas and chimpanzees during the manipulation of common object types. Bwindi gorillas show various hand use strategies during the processing of several plant foods. Chimfunshi chimpanzees also use forceful precision grips during daily manipulative tasks, suggesting that this is not a uniquely human ability.

Determinants of variation in orangutans' cognitive performance: II. influences of rearing conditions and human exposure

Classic ecological models of social groups suggest that increasing group size typically leads to a decrease in both individual predation risk and net food intake, with optimal group size being a compromise between these benefits and costs. Among rainforest primates, the main antipreda-tor benefits of sociality are thought to result from the dilution effect and collective detection of predators. However, recent research suggests that vegetation density in rainforest habitats limits the benefits of collective detection against ambush predators such as raptors, felids and snakes. Further, while larger groups are acknowledged to be more conspicuous to predators, it is widely assumed that this cost is unlikely to outweigh dilution benefits. Here we show in a simple model that per-individual rates of both encounters with predators and successful ambush attacks per encounter can increase with group size, under conditions likely to hold for many primate groups (when increases in group size lead to increases in group spread, conspicuousness and daily trav-el distance). Consequently, individual risk against ambush predators that employ a sit-and-wait strategy to search for prey, such as many snakes and some raptors, is lowest in small to medium-sized groups. In contrast, individuals in relatively large groups are favoured against ambush pred-ators like felids that employ a cruising strategy to search for prey, although even in this case in-creasing group size above some threshold increases individual risk. These results suggest that maximum group size among primates can be limited by increasing predation risk. Research fo-cused on primate predators is needed to determine the extent to which the model accurately re-flects their behaviour.Bushmeat hunting contributes to the decline of primate species across Africa; however, few studies have explored how such practises change over time in specific localities and how changes in land-use patterns and economic drivers may enhance threats to primates in Muslim dominated areas where, traditionally, primates are spared from such trade. The Haut Niger National Park (HNNP) is one of only two national parks in the Republic of Guinea. The park is one of the last remaining important formations of dry forest-savannah mosaics in West Africa and is a site of high conservation priority for ungulates and the western subspecies of chimpanzee. This study aimed to: (1) estimate the diversity and abundance of animal species sold for consumption across several markets in and around the HNNP, (2) analyse the evolution of the bushmeat trade since the mid-1990s, and (3) identify the players and drivers of the commercial bushmeat trade in the area. Local market assessments were conducted across four village markets and in Faranah, one of the closest urban areas abutting the HNNP. We successfully identified 5,807 wildlife carcasses of 46 species and 22 families on markets surveyed over a 7 month period spanning both the dry and wet seasons. In addition, semi-structured interviews with hunters, farmers and people involved in the bushmeat trade helped identify more recent drivers of the bushmeat trade in the HNNP. Our results indicated an increase in diversity of species targeted and the influence of crop-foraging and local microcredit systems in exacerbating the presence of primate species sold at bushmeat stalls in urban areas. Finally, whilst identifying key recommendations and gaps for future research, this study emphasises the growing risks facing primates as targets for bushmeat where people depend on agriculture and natural resource extraction for subsistence. This study complied with the International Primatological Society (IPS) Guidelines for the Use of Nonhuman Primates in Research.Comparative studies of primate grasping and manipulative behaviours in captivity have highlighted, among others, two human abilities that are generally considered unique compared with other primates: (1) the use of forceful precision and power squeeze grips involving the use of the thumb, and (2) a species-wide dominant use of one hand (usually the right hand), known as laterality. However, recent research has highlighted a diversity of precision and power grips in general among many non-human primates, and there is much debate around the potential for population-level or species-wide laterality in non-human primates. The majority of this research to date has been done on captive primates performing specific manipulative tasks, which may bias or confound these species comparisons. Comparatively little research has been done on hand use in wild primates, especially during natural, non-manipulative activities, including locomotion. Here, we investigate hand use during locomotor and non-locomotor behaviours in wild mountain gorillas ( Gorilla beringei beringei , Bwindi Impenetrable National Park, Uganda), wild chimpanzees ( Pan troglodytes verus , Tai National Park, Cote d’Ivoire) and chimpanzees kept under semi-natural conditions ( Pan troglodytes ssp., Chimfunshi Wildlife Trust, Zambia). Preliminary results propose that hand grips are similar between gorillas and chimpanzees during the manipulation of common object types. Bwindi gorillas show various hand use strategies during the processing of several plant foods. Chimfunshi chimpanzees also use forceful precision grips during daily manipulative tasks, suggesting that this is not a uniquely human ability.