Observational learning in orangutan cultural transmission chains

Field reports suggest that orangutans acquire local traditions by observing neighbouring conspecifics. However, there is little direct evidence of social learning to support this conclusion. The present study investigated whether orangutans would learn a novel foraging method through observation of a conspecific in a diffusion-chain paradigm testing for the spread of the behaviour. A foraging box with two possible methods for extracting food was used to investigate the transmission of a foraging tradition among zoo-living subjects. In a socially housed group of five orangutans, the dominant male was trained to use one technique exclusively to retrieve food. He then performed this technique in the presence of another group member, who was then allowed to forage. After several trials, the observer became the model for the next individual. A second experimental group of six individuals was introduced to the alternative method. The model-seeded technique was successfully transmitted along both experimental chains, with significant preferences for the model method. These results are consistent with claims for social transmission of foraging methods in wild orangutans.     

The fourth dimension of tool use: temporally enduring artefacts aid primates learning to use tools

All investigated cases of habitual tool use in wild chimpanzees and capuchin monkeys include youngsters encountering durable artefacts, most often in a supportive social context. We propose that enduring artefacts associated with tool use, such as previously used tools, partly processed food items and residual material from previous activity, aid non-human primates to learn to use tools, and to develop expertise in their use, thus contributing to traditional technologies in non-humans. Therefore, social contributions to tool use can be considered as situated in the three dimensions of Euclidean space, and in the fourth dimension of time. This notion expands the contribution of social context to learning a skill beyond the immediate presence of a model nearby. We provide examples supporting this hypothesis from wild bearded capuchin monkeys and chimpanzees, and suggest avenues for future research.     

In-Group Conformity Sustains Different Foraging Traditions in Capuchin Monkeys (Cebus apella)

Background

Decades of research have revealed rich cultural repertoires encompassing multiple traditions in wild great apes, a picture crucially complemented by experimental simulations with captive apes. Studies with wild capuchin monkeys, the most encephalized simian species, have indicated a New World convergence on these cultural phenomena, involving multiple traditions and tool use. However, experimental studies to date are in conflict with such findings in concluding that capuchins, like other monkeys, show minimal capacities for social learning.

Methodology/Principal Findings

Here we report a new experimental approach in which the alpha male of each of two groups of capuchins was trained to open an artificial foraging device in a quite different way, using either a slide or lift action, then reunited with his group. In each group a majority of monkeys, 8 of 11 and 13 of 14, subsequently mastered the task. Seventeen of the successful 21 monkeys discovered the alternative action to that seeded in the group, performing it a median of 4 times. Nevertheless, all 21 primarily adopted the technique seeded by their group''s alpha male. Median proportions of slide versus lift were 0.96 for the group seeded with slide versus 0. 01 for the group seeded with lift.

Conclusions/Significance

These results suggest a striking effect of social conformity in learned behavioral techniques, consistent with field reports of capuchin traditions and convergent on the only other species in which such cultural phenomena have been reported, chimpanzees and humans.     

Tolerance for inequity may increase with social closeness in chimpanzees

Economic decision-making depends on our social environment. Humans tend to respond differently to inequity in close relationships, yet we know little about the potential for such variation in other species. We examine responses to inequity in several groups of chimpanzees (Pan troglodytes) in a paradigm similar to that used previously in capuchin monkeys (Cebus apella). We demonstrate that, like capuchin monkeys, chimpanzees show a response to inequity of rewards that is based upon the partner receiving the reward rather than the presence of the reward alone. However, we also found a great amount of variation between groups tested, indicating that chimpanzees, like people, respond to inequity in a variable manner, which we speculate could be caused by such variables as group size, the social closeness of the group (as reflected in length of time that the group has been together) and group-specific traditions.     

Can Traditions Emerge from the Interaction of Stimulus Enhancement and Reinforcement Learning? An Experimental Model

The study of social learning in captivity and behavioral traditions in the wild are two burgeoning areas of research, but few empirical studies have tested how learning mechanisms produce emergent patterns of tradition. Studies have examined how social learning mechanisms that are cognitively complex and possessed by few species, such as imitation, result in traditional patterns, yet traditional patterns are also exhibited by species that may not possess such mechanisms. We propose an explicit model of how stimulus enhancement and reinforcement learning could interact to produce traditions. We tested the model experimentally with tufted capuchin monkeys (Cebus apella), which exhibit traditions in the wild but have rarely demonstrated imitative abilities in captive experiments. Monkeys showed both stimulus enhancement learning and a habitual bias to perform whichever behavior first obtained them a reward. These results support our model that simple social learning mechanisms combined with reinforcement can result in traditional patterns of behavior.     

Social traditions and social learning in capuchin monkeys (Cebus)

Capuchin monkeys (genus Cebus) have evolutionarily converged with humans and chimpanzees in a number of ways, including large brain size, omnivory and extractive foraging, extensive cooperation and coalitionary behaviour and a reliance on social learning. Recent research has documented a richer repertoire of group-specific social conventions in the coalition-prone Cebus capucinus than in any other non-human primate species; these social rituals appear designed to test the strength of social bonds. Such diverse social conventions have not yet been noted in Cebus apella, despite extensive observation at multiple sites. The more robust and widely distributed C. apella is notable for the diversity of its tool-use repertoire, particularly in marginal habitats. Although C. capucinus does not often use tools, white-faced capuchins do specialize in foods requiring multi-step processing, and there are often multiple techniques used by different individuals within the same social group. Immatures preferentially observe foragers who are eating rare foods and hard-to-process foods. Young foragers, especially females, tend to adopt the same foraging techniques as their close associates.     

Similarity in food cleaning techniques within matrilines in wild vervet monkeys

Social learning and the formation of traditions rely on the ability and willingness to copy one another. A central question is under which conditions individuals adapt behaviour to social influences. Here, we demonstrate that similarities in food processing techniques emerge on the level of matrilines (mother-offspring) but not on the group level in an experiment on six groups of wild vervet monkeys that involved grapes covered with sand. Monkeys regularly ate unclean grapes but also used four cleaning techniques more similarly within matrilines: rubbing in hands, rubbing on substrate, open with mouth, and open with hands. Individual cleaning techniques evolved over time as they converged within matrilines, stabilised at the end and remained stable in a follow-up session more than one year later. The similarity within matrilines persisted when we analyzed only foraging events of individuals in the absence of other matriline members and matriline members used more similar methods than adult full sisters. Thus, momentary conversion or purely genetic causation are unlikely explanations, favouring social learning as mechanism for within matriline similarities. The restriction of traditions to matriline membership rather than to the group level may restrict the development of culture in monkeys relative to apes or humans.     

Social influences on the acquisition of sex-typical foraging patterns by juveniles in a group of wild tufted capuchin monkeys (Cebus nigritus)

Foraging traditions in primates are becoming the subject of increasing debate. Recent evidence for such a phenomenon was recently provided for wild Cebus capucinus [Fragaszy & Perry, 2003]. To better understand the bases of animal traditions, one should examine intrapopulation behavioral variability and the influence of social context on within-group transmission of specific foraging patterns. We studied the variability of foraging patterns across age and sex classes, and the proximity patterns of juveniles to adults of both sexes in a group of wild tufted capuchin monkeys (Cebus nigritus) living in the Iguazu National Park, Argentina. Foraging activity was examined for a period of 9 months in terms of proportions of focal samples devoted to foraging on certain food targets, microhabitats, and supports, and using specific foraging patterns. Proximity analyses were performed to reveal patterns of association between juveniles and adults. Sex differences in foraging behavior were present and overrode age differences. Overall, males ate more animal foods, foraged more for invertebrates on woody microhabitats (especially large branches), palms, and epiphytes, and used lower and larger supports than females. Females ate more fruits, foraged more on leaves and bamboo microhabitats, and used smaller supports than males. Juveniles were similar to adults of the same sex in terms of food targets, foraging substrates, and choice of supports, but were less efficient than adults. Proximity patterns indicated that juvenile males stayed in close spatial association with adult males and preferentially focused their "food interest" on them. This phenomenon was less evident in juvenile females. The degree to which juveniles, especially males, showed some of the sex-typical foraging patterns correlated positively with their proximity to adults of the same sex. These findings suggest that the acquisition of foraging behaviors by juvenile males is socially biased by their closeness to adults of the same sex.     

Stone banging by wild capuchin monkeys: an unusual auditory display

Primates often react to possible predators by using intimidation displays, although the occurrence of these displays is dependent on the risk of predation. Functional explanations for these kinds of displays range from sexual selection to predator deterrence. The ability to respond to different predators can be socially acquired, and social traditions could explain population differences in response to the same potential predator. Here I report wild groups of Cebus apella libidinosus banging stones to produce sound in a remarkable aggressive display. I observed this display in 6 wild groups and I suggest its primary function is a predator-deterrent behaviour. Although banging objects is an innate behaviour in capuchin monkeys, in all wild groups observed so far it has been observed only in a foraging context. Stone banging is a novel behavioural variant that is most likely learned socially. The absence of this display in other populations of capuchins, which have access to stones, suggests that stone banging could be a social tradition in the population studied.     

Interaction Between Capuchins and Coatis: Nonagonistic Behaviors and Lack of Predation

We compare the nature of capuchin-coati interactions by Cebus apella in 2 populations under semifree-ranging and wild conditions. We report a similar pattern of interaction at both sites, in spite of their ecological differences. Most frequent capuchin behaviors toward coatis were agonistic, but we noted no predation. Contrarily, the monkeys also exhibited nonagonistic behaviors, such as play and grooming. As tufted capuchins predate other mammalian species, and as the subjects were aggressive towards competitor species, showing their belligerent temperament, we believe the lack of predation can be attributed to 2 different ecological contigencies – the absence of coati pups in a period of food shortage, and the cost of dealing with a dangerous adult coati where other rich resources were available–and also, perhaps, to different traditions in capuchin behavior towards coatis, established via intraspecific social learning.     

Identification of learning mechanisms in a wild meerkat population

Vigorous debates as to the evolutionary origins of culture remain unresolved due to an absence of methods for identifying learning mechanisms in natural populations. While laboratory experiments on captive animals have revealed evidence for a number of mechanisms, these may not necessarily reflect the processes typically operating in nature. We developed a novel method that allows social and asocial learning mechanisms to be determined in animal groups from the patterns of interaction with, and solving of, a task. We deployed it to analyse learning in groups of wild meerkats (Suricata suricatta) presented with a novel foraging apparatus. We identify nine separate learning processes underlying the meerkats' foraging behaviour, in each case precisely quantifying their strength and duration, including local enhancement, emulation, and a hitherto unrecognized form of social learning, which we term 'observational perseverance'. Our analysis suggests a key factor underlying the stability of behavioural traditions is a high ratio of specific to generalized social learning effects. The approach has widespread potential as an ecologically valid tool to investigate learning mechanisms in natural groups of animals, including humans.     

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.     

Evidence of social learning in black-and-white ruffed lemurs (Varecia variegata)

Although many studies have examined social learning capabilities in apes and monkeys, experiments involving prosimians remain largely absent. We investigated the potential for social learning in black-and-white ruffed lemurs using a two-action foraging task. Eight individuals were divided into two experimental groups and exposed to conspecifics using one of two techniques to access food. Subjects were then given access to the apparatus and their retrieval techniques were recorded and compared. All subjects made their first retrieval using the technique they observed being demonstrated, and there were significant differences between the two groups in their overall response patterns. These results suggest that prosimians are capable of social learning and that additional long-term field studies may reveal the presence of behavioural traditions similar to those found in other primates.     

Spontaneous tool use by wild capuchin monkeys (Cebus libidinosus) in the Cerrado

Among primates, only chimpanzees and orang-utans are credited with customary tool use in nature. Among monkeys, capuchins stand out with respect to the number of accounts of tool use. However, the majority of capuchin tool use observations reported in nature is anecdotal or idiosyncratic. In this report, we documented the stone pounding of dry fruits (Hymenea courbaril and Acrocomia aculeata) in two wild free-ranging groups of Cebus libidinosus in the Brasilia National Park, a preserved area representative of the Cerradobiome of Central Brazil. In 2004, we noted 2 episodes at which 4 monkeys used stones to crack open nuts. In 2005, we recorded 5 pounding episodes involving 2 different monkeys. Observations of tool use over the course of 2 consecutive years by some individuals, as well as other indirect evidence, indicate that this behaviour could be habitual in the studied groups. We propose that the probability of the emergence of the use of pounding stones as tools may be dependent on the ecological variables that influence the degree of terrestriality and extractive foraging and the complex interaction of these factors.     

The enhanced tool‐kit of two groups of wild bearded capuchin monkeys in the Caatinga: tool making,associative use,and secondary tools

The use of stones to crack open encapsulated fruit is widespread among wild bearded capuchin monkeys (Cebus libidinosus) inhabiting savanna‐like environments. Some populations in Serra da Capivara National Park (Piauí, Brazil), though, exhibit a seemingly broader toolkit, using wooden sticks as probes, and employing stone tools for a variety of purposes. Over the course of 701.5 hr of visual contact of two wild capuchin groups we recorded 677 tool use episodes. Five hundred and seventeen of these involved the use of stones, and 160 involved the use of sticks (or other plant parts) as probes to access water, arthropods, or the contents of insects' nests. Stones were mostly used as “hammers”—not only to open fruit or seeds, or smash other food items, but also to break dead wood, conglomerate rock, or cement in search of arthropods, to dislodge bigger stones, and to pulverize embedded quartz pebbles (licking, sniffing, or rubbing the body with the powder produced). Stones also were used in a “hammer‐like” fashion to loosen the soil for digging out roots and arthropods, and sometimes as “hoes” to pull the loosened soil. In a few cases, we observed the re‐utilization of stone tools for different purposes (N=3), or the combined use of two tools—stones and sticks (N=4) or two stones (N=5), as sequential or associative tools. On three occasions, the monkeys used smaller stones to loosen bigger quartz pebbles embedded in conglomerate rock, which were subsequently used as tools. These could be considered the first reports of secondary tool use by wild capuchin monkeys. Am. J. Primatol. 71:242–251, 2009. © 2008 Wiley‐Liss, Inc.     

Physical properties of palm fruits processed with tools by wild bearded capuchins (Cebus libidinosus)

Habitually, capuchin monkeys access encased hard foods by using their canines and premolars and/or by pounding the food on hard surfaces. Instead, the wild bearded capuchins (Cebus libidinosus) of Boa Vista (Brazil) routinely crack palm fruits with tools. We measured size, weight, structure, and peak-force-at-failure of the four palm fruit species most frequently processed with tools by wild capuchin monkeys living in Boa Vista. Moreover, for each nut species we identify whether peak-force-at-failure was consistently associated with greater weight/volume, endocarp thickness, and structural complexity. The goals of this study were (a) to investigate whether these palm fruits are difficult, or impossible, to access other than with tools and (b) to collect data on the physical properties of palm fruits that are comparable to those available for the nuts cracked open with tools by wild chimpanzees. Results showed that the four nut species differ in terms of peak-force-at-failure and that peak-force-at-failure is positively associated with greater weight (and consequently volume) and apparently with structural complexity (i.e. more kernels and thus more partitions); finally for three out of four nut species shell thickness is also positively associated with greater volume. The finding that the nuts exploited by capuchins with tools have very high resistance values support the idea that tool use is indeed mandatory to crack them open. Finally, the peak-force-at-failure of the piassava nuts is similar to that reported for the very tough panda nuts cracked open by wild chimpanzees; this highlights the ecological importance of tool use for exploiting high resistance foods in this capuchin species.     

The structure of a bottlenose dolphin society is coupled to a unique foraging cooperation with artisanal fishermen

Diverse and localized foraging behaviours have been reported in isolated populations of many animal species around the world. In Laguna, southern Brazil, a subset of resident bottlenose dolphins (Tursiops truncatus) uses a foraging tactic involving cooperative interactions with local, beach-casting fishermen. We used individual photo-identification data to assess whether cooperative and non-cooperative dolphins were socially segregated. The social structure of the population was found to be a fission-fusion system with few non-random associations, typical for this species. However, association values were greater among cooperative dolphins than among non-cooperative dolphins or between dolphins from different foraging classes. Furthermore, the dolphin social network was divided into three modules, clustering individuals that shared or lacked the cooperative foraging tactic. Space-use patterns were not sufficient to explain this partitioning, indicating a behavioural factor. The segregation of dolphins using different foraging tactics could result from foraging behaviour driving social structure, while the closer association between dolphins engaged in the cooperation could facilitate the transmission and learning of this behavioural trait from conspecifics. This unique case of a dolphin-human interaction represents a valuable opportunity to explore hypotheses on the role of social learning in wild cetaceans.     

Stone Throwing as a Sexual Display in Wild Female Bearded Capuchin Monkeys,Sapajus libidinosus

Capuchin monkeys (Sapajus spp.) in captive settings frequently manipulate and throw objects. In the wild, they may push or drop stones and sticks toward targets during inter- or intraspecific threat displays. In addition, female capuchin monkeys exhibit a broad repertoire of behaviors during their proceptive period, including facial expressions, vocalizations, stereotyped body postures, and touch-and-run behavior. This study reports stone throwing as a newly-described communicative behavior during the proceptive display of females in a group of bearded capuchin monkeys (S. libidinosus) in Serra da Capivara National Park, Brazil. During a two-year study, three females from one group were seen throwing stones at males during their proceptive phase. After this period, three other females in the same group exhibited the same behavior. Although it may be possible that this pattern is the result of several independent innovations by each female, the apparent absence of this behavior in other groups leads us to suggest that we have documented the diffusion of a new behavioral trait or tradition within this capuchin social group.     

Conceptual thresholds for same and different in old-(Macaca mulatta) and new-world (Cebus apella) monkeys

Learning of the relational same/different (S/D) concept has been demonstrated to be largely dependent upon stimulus sets containing more than two items for pigeons and old-world monkeys. Stimulus arrays containing several images for use in same/different discrimination procures (e.g. 16 identical images vs. 16 nonidentical images) have been shown to facilitate and even be necessary for learning of relational concepts ( [Flemming et al., 2007], [Wasserman et al., 2001] and [Young et al., 1997]). In the present study, we investigate the threshold at which a new world primate, the capuchin (Cebus apella) may be able to make such a discrimination. Utilizing a method of increasing entropy, rather than conventional procedures of decreasing entropy, we demonstrate unique evidence that capuchin monkeys are readily capable of making 2-item relational S/D conditional discriminations. In another experiment, we examine the supposed level of difficulty in making S/D discriminations by rhesus monkeys (Macaca mulatta). Whereas pigeons (Columba livia) and baboons (Papio papio) have shown marked difficulty simultaneously discriminating same from different arrays at all when composed of fewer than 8 items each, rhesus monkeys seem to understand that pairs of stimuli connote sameness and difference just the same (Flemming et al., 2007). With sustained accurate performance of 2-item S/D discriminations, both experienced and task-naïve rhesus monkeys appear quite certain in their conceptual knowledge of same and different. We conclude that learning of the same/different relational concept may be less dependent upon high levels of entropy contrast than originally hypothesized for nonhuman primates.