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.     

社群学习对植食性鸟类和哺乳动物觅食行为的作用

社群学习是动物的一种可塑性行为表现型式。综述了社群学习对植食性鸟类和哺乳动物觅食行为的作用,并述评了其学习机制。社群同伴对动物个体觅食地点、时间和取食方式均有影响,母体摄食的食物信息可通过胎盘和乳汁显著影响幼体的食物选择。动物通过观察学习、嗅闻学习以及味觉厌恶学习,不仅能更快找到食物资源,提高觅食效率,而且能有效降低中毒与被捕食的风险,从而提高其适合度。     

Social learning and life skills training for hatchery reared fish

With the stress placed on our natural resources, many fisheries increasingly rely on restocking from hatchery-reared sources in an attempt to maintain commercially viable populations. However, the mortality rates of hatchery-reared fishes during the period directly following release are very high. The successful development of restocking programs is consequently dependent upon production and release strategies that lead to improved migratory, antipredator and feeding behaviour in hatchery fish. While relevant individual experience prior to release might improve performance, social learning potentially provides a process whereby fish can acquire locally adaptive behaviour rapidly and efficiently. It is now well over a decade since Suboski & Templeton (1989) raised the possibility of using social learning processes to improve the post-release survival of hatchery-reared fishes. This period has witnessed considerable progress in the understanding of how social learning operates in fish populations. We review new methods and recent findings that suggest how social learning protocols could realistically be applied on a large scale to enhance the viability of hatchery fish prior to their release into the wild. We also suggest a practical pre-release training protocol that may be applied at the hatchery level.     

Social foraging: individual learning and cultural transmission of innovations

We present two stochastic models of individual and social learningthat count the number of individuals exhibiting a learned, resource-producingtrait in a group of social foragers. The novelty of our modelingresults from incorporating the empirically based assumptionthat rates of both individual and social learning should dependon the frequency of the learned trait within the group. Whenresources occur as clumps shared by group members, a naive individual'sacquisition of the skill required for clump discovery/productionshould involve opposing processes of frequency dependence. Theopportunity to learn via cultural transmission should increasewith the trait's frequency, but the opportunity for learningindividually should decrease as the trait's frequency increases.The results of the model suggest that the evolution of the capacityfor cultural transmission may be promoted in environments wherescrounging at resource clumps inhibits rates of individual learning.     

‘Ghost’ experiments and the dissection of social learning in humans and animals

The focus of this review is the experimental techniques used to identify forms of social learning shown by humans and nonhuman animals. Specifically, the ‘ghost display’ and ‘end‐state’ conditions, which have been used to tease apart imitative and emulative learning are evaluated. In a ghost display, the movements of an apparatus are demonstrated, often through the discrete use of fishing‐line or hidden mechanisms, without a live model acting directly upon the apparatus so that the apparatus appears to be operated as if by a ‘ghostly’ agent. In an end‐state condition, an observing individual is shown the initial state of the test apparatus, the apparatus is then manipulated out‐of‐sight and then represented to the individual in its final state. The aim of the ghost display condition is to determine whether individuals are able to emulate by replicating the movements of an apparatus, or perform a task, without requiring information about the bodily movements required to do so (imitation). The end‐state condition is used to identify goal‐emulation by assessing whether the observer can replicate the steps required to solve the task without having been shown the required body actions or task movements. The responses of individuals tested with either the ghost display and/or end‐state conditions are compared to those of further individuals who have observed a full demonstration by either a human experimenter or a conspecific. The responses of a control group, to whom no information has been provided about the test apparatus or required actions, are also compared and evaluated. The efficacy of these experimental techniques employed with humans, nonhuman primates, dogs, rats and birds are discussed and evaluated. The experiments reviewed herein emphasise the need to provide ghost displays and end‐state conditions in combination, along with full live demonstrations and a no‐information control. Future research directions are proposed.     

Selective attention to philopatric models causes directed social learning in wild vervet monkeys

Human behaviour is often based on social learning, a mechanism that has been documented also in a variety of other vertebrates. However, social learning as a means of problem-solving may be optimal only under specific conditions, and both theoretical work and laboratory experiments highlight the importance of a potential model''s identity. Here we present the results from a social learning experiment on six wild vervet monkey groups, where models were either a dominant female or a dominant male. We presented ‘artificial fruit’ boxes that had doors on opposite, differently coloured ends for access to food. One option was blocked during the demonstration phase, creating consistent demonstrations of one possible solution. Following demonstrations we found a significantly higher participation rate and same-door manipulation in groups with female models compared to groups with male models. These differences appeared to be owing to selective attention of bystanders to female model behaviour rather than owing to female tolerance. Our results demonstrate the favoured role of dominant females as a source for ‘directed’ social learning in a species with female philopatry. Our findings imply that migration does not necessarily lead to an exchange of socially acquired information within populations, potentially causing highly localized traditions.     

The role of conformity in foraging when personal and social information conflict

There is currently considerable interest in the interplay betweenpersonal and social information in decision-making processes.Two experiments are presented exploring the relative use ofprior personal information and subsequent social informationin foraging decisions of guppies. Experiment 1 tested the assumptionthat when the use of information acquired through personal experienceis not costly, conflicting social information will be ignored.The assumption was confirmed because, when given a choice betweenfeeding at two food patches, at one of which they had previouslyseen conspecifics feed, individual fish with prior experienceof feeding at the alternative site chose the alternative, whereasfish with no prior experience chose the site at which theirconspecifics had fed. Experiment 2 tested theoretical predictionsthat when the use of information acquired through personal experienceis potentially costly, conflicting social information will beweighed more heavily than will personal information. The predictionwas confirmed because, when given a choice between feeding attwo food patches, one at which they had previously seen conspecificsfeed and one behind a visual barrier, individual fish with priorexperience of feeding behind the barrier chose the site at whichtheir conspecifics had fed. These findings suggest that conformitycan promote social learning in naïve individuals, but priorexperience can insulate individuals from conformity providedthe costs of relying on that experience are small. In addition,the experiments highlight the fact that personal and socialinformation are not always weighed equally.     

Observational learning in chimpanzees and children studied through 'ghost' conditions

Emulation has been distinguished from imitation as a form of observational learning because it focuses not on the model's actions but on the action's environmental results. Whether a species emulates, imitates or displays only simpler observational learning is expected to have profound implications for its capacity for cultural transmission. Chimpanzees' observational learning has been suggested to be primarily emulative, but this is an inference largely based upon low fidelity copying in experiments when comparing chimpanzees with humans rather than direct testing. Here we test directly for emulation learning by chimpanzees and children using a 'ghost' condition in which a sliding door obscuring a reward was moved to left or right with no agent visible, a context associated with the only published evidence for emulation learning in a non-human species (pigeons). Both children and chimpanzees matched the observed direction of ghost door movement on their first test trial. This is the first evidence for emulation in a non-human primate in the restricted context of a ghost condition. However, only the children continued to match in later trials. Individuals of both species continued to match with 99% or better fidelity when viewing a conspecific model operates the door. We conclude that chimpanzees can and will display emulation learning when the task is as simple as the present one, which contrasts with a failure to do so in a more complex manipulative task tested earlier. However, even with a simple task, emulation alone creates only fleeting fidelity compared with the opportunity to copy a conspecific, when considerable conformity is displayed.     

Individual variation in the rate of use of tree-hole tools among wild orang-utans: implications for hominin evolution

Primate tool use varies among species, populations, and individuals. Individual variation is especially poorly understood. Orang-utans in the Sumatran swamp forest of Suaq Balimbing varied widely in rates of tool use to extract honey, ants or termites from tree holes and in the degree to which they specialized on this tree-hole tool use. We tested whether individual variation was best explained by effects of social dominance, habitat differences, or by opportunities for socially learning the skills during ontogeny. There was no evidence for the first two hypotheses. However, we found a strong relationship between tool use specialization and mean female party size, which was used as a proxy for the opportunities for socially mediated learning in a foraging context during their development. This use was justified because females are rather philopatric and their mean party size remained stable over time, thus reflecting long-term tendencies. The correlation was not an artifact of a direct effect of party size on tool use tendencies, and did not hold for males, the dispersing sex. Thus, variation in the number of opportunities for social learning explains tool use variation within populations, corroborating hypotheses for between-population variation. The emergence of human culture was accompanied by vastly improved mechanisms of social learning. In order for these improvements to be favored by natural selection, the cultural potential must have actually been expressed. Thus, a combination of strong sociability and a reliance on tool-using or other technical skills acquired through social learning must have characterized early hominins.     

Immature gannets follow adults in commuting flocks providing a potential mechanism for social learning

Group travel is a familiar phenomenon among birds but the causes of this mode of movement are often unclear. For example, flocking flight may reduce flight costs, enhance predator avoidance or increase foraging efficiency. In addition, naive individuals may also follow older, more experienced conspecifics as a learning strategy. However, younger birds may be slower than adults so biomechanical and social effects on flock structure may be difficult to separate. Gannets are wide‐ranging (100s–1000s km) colonial seabirds that often travel in V or echelon‐shaped flocks. Tracking suggests that breeding gannets use memory to return repeatedly to prey patches 10s–100s km wide but it is unclear how these are initially discovered. Public information gained at the colony or by following conspecifics has been hypothesised to play a role, especially during early life. Here, we address two hypotheses: 1) flocking reduces flight costs and 2) young gannets follow older ones in order to locate prey. To do so, we recorded flocks of northern gannets commuting to and from a large colony and passing locations offshore and used a biomechanical model to test for age differences in flight speeds. Consistent with the aerodynamic hypothesis, returning flocks were significantly larger than departing flocks, while, consistent with the information gathering hypothesis, immatures travelled in flocks more frequently than adults and these flocks were more likely to be led by adults than expected by chance. Immatures did not systematically occupy the last position in flocks and had similar theoretical airspeeds to adults, making it unlikely that they follow, rather than lead, for biomechanical reasons. We therefore conclude that while gannets are likely to travel in flocks in part to reduce flight costs, the positions of immatures in those flocks may result in a flow of information from adults to immatures, potentially leading to social learning.     

Social learning and mother's behavior in manipulative tasks in infant marmosets

High levels of social tolerance are considered to promote social learning, as they allow direct observation of a manipulating conspecific and facilitate scrounging. Owing to tolerance toward infants, infancy is thought to be especially suited for learning socially transmitted behaviors. Despite this, few studies have investigated social learning of infants, particularly in manipulative tasks where observation might be most helpful. Here, we investigated (1) the influence of social learning on task acquisition in infant marmosets, and (2) whether the mother augments her behavior in a way that may enhance social learning by her infants. We tested infant and juvenile marmosets in four different complex foraging‐related tasks, featuring large living insects (two tasks) or artificially embedded prey (two tasks). Each individual observed the mother solving two of the tasks and served as a control in the other two tasks. Observers manipulated more and succeeded sooner than control animals, suggesting that observing the mother promoted learning either directly or by decreasing neophobia. Moreover, the data suggest that learning in 11–15 week‐old infants might be promoted actively by the mother. She solved the tasks, consumed less food, and consumed it later than when foraging with older offspring or alone. Furthermore, the results indicate the possible importance of the third and fourth month of infancy as the crucial ontogenetic period for social learning in marmosets, corroborating recent observations of free‐living common marmosets. Am. J. Primatol. 71:503–509, 2009. © 2009 Wiley‐Liss, Inc.     

Selectivity in social and asocial learning: investigating the prevalence,effect and development of young children's learning preferences

Culture evolution requires both modification and faithful replication of behaviour, thus it is essential to understand how individuals choose between social and asocial learning. In a quasi-experimental design, 3- and 5-year-olds (176), and adults (52) were presented individually with two novel artificial fruits, and told of the apparatus'' relative difficulty (easy versus hard). Participants were asked if they wanted to attempt the task themselves or watch an experimenter attempt it first; and then had their preference either met or violated. A significant proportion of children and adults (74%) chose to learn socially. For children, this request was efficient, as observing a demonstration made them significantly quicker at the task than learning asocially. However, for 5-year-olds, children who selected asocial learning were also found to be highly efficient at the task, showing that by 5 years children are selective in choosing a learning strategy that is effective for them. Adults further evidenced this trend, and also showed selectivity based on task difficulty. This is the first study to examine the rates, performance outcomes and developmental trajectory of preferences in asocial and social learning, ultimately informing our understanding of innovation.     

Insights from social transmission of information in rodents

Direct exposure to stimuli in their environment is not the only way that animals learn about important information. Individuals can infer fear from a social context through observation. Like humans, rats are very social animals, and may learn to infer information about their environment through their interactions with conspecifics. Here, we first review different models for social transmission of information in rodents. Second, we examine different modes of communication that are important to social learning. Then, we cover the different proximate factors that are thought to modulate the social transmission of information. Next, we identify social and environmental conditions that impact social learning, and finally, we conclude by revisiting social transmission through the lens of the Tinbergen framework.     

A social learning model of conflict and cooperation in human societies

Patterns of conflict and cooperation both within and between societies may be related to the degree of cultural similarity within and between the same societies. A simple model of social learning is used to predict patterns of conflict and cooperation in hypothetical societies that differ in the roles of relatives and nonrelatives in the enculturation of children. The model is illustrated by comparing its predictions to known differences in the patterns of conflict between males inpatrilocal and matrilocal societies.