The social learning of tool use by orangutans (Pongo pygmaeus)

Very little is known about the social learning of orangutans (Pongo pygmaeus), especially in the context of problem-solving situations such as tool use. Sixteen orangutans were presented with a rake-like tool and desirable but out-of-reach food. Eight subjects observed a human demonstrator use the tool in one way, while another eight observed the demonstrator use the tool in another way. Subjects behaved identically in the two experimental conditions, showing no effect of the type of demonstration observed. Analysis of individual learning curves suggested that a large component of individual trial-and-error learning was at work, even for two subjects who received additional trials with an orangutan demonstrator. This pattern of results suggests that subjects were paying attention to the general functional relations in the task and to the results obtained by the demonstrator, but not to the actual methods of tool use demonstrated. It is concluded that subjects in both conditions were employing emulation learning, not imitative learning.     

Innovative Individuals Are Not Always the Best Demonstrators: Feeding Innovation and Social Transmission in Serinus canaria

Background

Feeding innovation occurs when individuals choose a novel, unknown type of food and/or acquire new feeding skills. Here we studied feeding innovation and social transmission of the new feeding habit in canaries. Adult canaries eat a wide variety of seeds but avoid larger ones such as those of sunflowers. We determined whether adults of both sexes are equally prone to innovate when confronted with sunflower seeds and whether free-interactions facilitate transmission of the new feeding habit in a sex-dependent manner.

Methodology/Principal Findings

First we determined which sex was more innovative, i.e., was more successful at husking and eating the novel seeds. Males were clearly more innovative than females. Due to this, experienced males served as model for either male or female observers in three different conditions (free interaction with a demonstrator, visual interaction with a demonstrator placed behind a transparent wall and access to seeds in the presence of a non-demonstrating bird). During free interactions, the new feeding habit was only transmitted to females. In contrast, transmission of seed handling to male observers only occurred if demonstrator and observer were separated by the transparent wall. Indeed, aggressive behaviors between males prevented social transmission during free interactions. Finally, we studied the influence of the less innovative females in feeding-habit transmission. First, we obtained female demonstrators by making them freely interact with male demonstrators. Once they acquired innovative responses to sunflower seeds we studied feeding-habit transmission towards male and female observers. Observers of both sexes learned during free interactions with female demonstrators. No aggressive behavior occurred. Males were also able to learn after visual interactions with the female demonstrator.

Conclusions/Significance

Our results show that the most innovative individuals (males) are not always the best demonstrators, and that social relationship and sex are crucial factors for the spread of a new feeding habit among canaries. These factors determine the kind of interaction between individuals and the time spent together, thus affecting the transmission of novel habits within the population.     

Video demonstrations seed alternative problem-solving techniques in wild common marmosets

Studies of social learning and tradition formation under field conditions have recently gained momentum, but suffer from the limited control of socio-ecological factors thought to be responsible for transmission patterns. The use of artificial visual stimuli is a potentially powerful tool to overcome some of these problems. Here, in a field experiment, we used video images of unfamiliar conspecifics performing virtual demonstrations of foraging techniques. We tested 12 family groups of wild common marmosets. Six groups received video demonstrations (footage of conspecifics either pulling a drawer open or pushing a lid upwards, in an ‘artificial fruit’); the other six groups served as controls (exposed to a static image of a conspecific next to the fruit). Subjects in video groups were more manipulative and successful in opening the fruit than controls; they were also more likely to use the technique they had witnessed and thus could serve as live models for other family members. To our knowledge, this is the first study that used video demonstrations in the wild and demonstrated the potent force of social learning, even from unfamiliar conspecifics, under field conditions.     

Age-dependent social learning in a lizard

Evidence of social learning, whereby the actions of an animal facilitate the acquisition of new information by another, is taxonomically biased towards mammals, especially primates, and birds. However, social learning need not be limited to group-living animals because species with less interaction can still benefit from learning about potential predators, food sources, rivals and mates. We trained male skinks (Eulamprus quoyii), a mostly solitary lizard from eastern Australia, in a two-step foraging task. Lizards belonging to ‘young’ and ‘old’ age classes were presented with a novel instrumental task (displacing a lid) and an association task (reward under blue lid). We did not find evidence for age-dependent learning of the instrumental task; however, young males in the presence of a demonstrator learnt the association task faster than young males without a demonstrator, whereas old males in both treatments had similar success rates. We present the first evidence of age-dependent social learning in a lizard and suggest that the use of social information for learning may be more widespread than previously believed.     

When and how well can human‐socialized capuchins match actions demonstrated by a familiar human?

Capuchin monkeys have provided uneven evidence of matching actions they observe others perform. In accord with theories emphasizing the attentional salience of object movement and spatial relationships, we predicted that human-reared monkeys would better match events in which a human demonstrator moved an object into a new relation with another object or surface than other kinds of actions. Three human-reared capuchins were invited repeatedly by a familiar human to perform a fixed set of actions upon objects or upon their bodies, using the "Do as I do" procedure. Actions directed at the body were matched less reliably than actions involving objects, and actions were matched best when the monkey looked at the demonstration for at least 2 sec and performed its action within a few seconds after the demonstration. The most commonly matched actions were those that one monkey performed relatively often when the experiment began. One monkey partially reproduced three novel actions (out of 48 demonstrations), all three involving moving or placing objects, and two of which it also performed following other demonstrations. These findings contribute convergent evidence that capuchin monkeys display social facilitation of activity, enhanced interest in particular objects and emulation of spatial outcomes. This pattern can support the development of shared manipulative skills, as evident in traditions of foraging and tool use in natural settings. The findings do not suggest that human rearing substantively altered capuchins' ability or interest in matching the actions of a familiar human, although visual attention to the human demonstrator may have been greater in these monkeys than in normally reared monkeys.     

Social learning of fear and safety is determined by the demonstrator's racial group

Social learning offers an efficient route through which humans and other animals learn about potential dangers in the environment. Such learning inherently relies on the transmission of social information and should imply selectivity in what to learn from whom. Here, we conducted two observational learning experiments to assess how humans learn about danger and safety from members (‘demonstrators'') of an other social group than their own. We show that both fear and safety learning from a racial in-group demonstrator was more potent than learning from a racial out-group demonstrator.     

If at first you don't succeed… Studies of ontogeny shed light on the cognitive demands of habitual tool use

Many species use tools, but the mechanisms underpinning the behaviour differ between species and even among individuals within species, depending on the variants performed. When considering tool use ‘as adaptation’, an important first step is to understand the contribution made by fixed phenotypes as compared to flexible mechanisms, for instance learning. Social learning of tool use is sometimes inferred based on variation between populations of the same species but this approach is questionable. Specifically, alternative explanations cannot be ruled out because population differences are also driven by genetic and/or environmental factors. To better understand the mechanisms underlying routine but non-universal (i.e. habitual) tool use, we suggest focusing on the ontogeny of tool use and individual variation within populations. For example, if tool-using competence emerges late during ontogeny and improves with practice or varies with exposure to social cues, then a role for learning can be inferred. Experimental studies help identify the cognitive and developmental mechanisms used when tools are used to solve problems. The mechanisms underlying the route to tool-use acquisition have important consequences for our understanding of the accumulation in technological skill complexity over the life course of an individual, across generations and over evolutionary time.     

Experimental evidence for limited vocal recognition in a wild primate: implications for the social complexity hypothesis

Although monitoring social information is a key aspect of the social complexity hypothesis, surprisingly little work has compared social knowledge across different species of wild animals. In the present study, I use playback experiments to test for individual recognition in wild male geladas (Theropithecus gelada) to compare with published accounts of social knowledge in chacma baboons (Papio ursinus). Geladas and baboons are closely related primates living in socially complex groups that differ dramatically in group size—geladas routinely associate with more than 10 times the number of conspecifics than do baboons. Using grunts from non-rival males to simulate approaches, I examined the strength of a subject male''s response when the ‘approach’ was from the direction of (i) non-rival males (control), or (ii) rival males (a more salient stimulus if playback grunts are not recognized by the subject). I compared responses separately based on the degree of social overlap between the caller and the subject. Responses indicate that male geladas, unlike baboons, do not use vocalizations to recognize all of the individuals they regularly encounter. This represents, to my knowledge, the first documented evidence of ‘missing’ social knowledge in a natural primate population. The sharp distinction between baboons and geladas suggests that geladas are either unable or unmotivated to keep track of the individual identity of other males in their multi-level society—even males with whom they have a large degree of social overlap. Thus, these results are consistent with the central assumption of the social complexity hypothesis that social cognition is costly.     

The effect of ostensive cues on dogs’ performance in a manipulative social learning task

In contrast to animal social learning (e.g. dogs learning from observing another dog), humans typically teach by attracting the attention of the learner. Also during the training of dogs, humans tend to attract their attention in a similar way. Here, we investigated dogs’ ability to learn both from a dog and a human demonstrator in a manipulative task, where the models demonstrated which part of a box to manipulate in order to get a food reward. We varied the communicative context both during the dog and during the human demonstration comparably: a second experimenter directed the attention of the subjects to the model (dog/human ostensive demonstration) or remained silent (dog/human non-ostensive demonstration). Moreover, we investigated whether the training level of the dogs (well-trained vs. untrained) affected how the dogs performed in the manipulative tasks after the different demonstrations.We found that better trained dogs showed significantly better problem solving abilities. They paid more attention to the human demonstration than to the dog model, whereas such a difference in attentiveness of the less trained dogs was not found. Despite slight differences in paying attention to the different demonstrators, the presence of human or the dog demonstrators exerted equally effectiveness on the test performance of the dogs. However, the effectiveness of the demonstrations was significantly reduced if ostensive cues were given during the demonstrations by a second experimenter. Analysis of attentiveness and activity of the observer dogs during the demonstrations indicates that the reason for this negative effect was a combination of distracted attention paid to the demonstration and a higher level of excitement in the ostensive than in the non-ostensive demonstrations.This study suggests that third party communication during demonstration attracts dogs’ attention to the communicator instead of paying close attention to the model. We suggest that precise timing and synchronization of attention-calling and demonstration is necessary to avoid this distracting effect.     

Environmental Unpredictability and the Value of Social Information for Foraging Starlings

Environmental and behavioral cues are useful sources of information that allow group foraging individuals to improve their foraging success. Few studies to date, however, have examined how varying degrees of environmental unpredictability may affect when and how individuals use the social information they obtain in foraging groups. In this experiment, European starlings (Sturnus vulgaris) were tested to determine in which type of environment, predictable or unpredictable, social information would be the most valuable. Subjects were placed under one of four conditions: an unpredictable environment with either (1) an informing demonstrator bird or (2) an uninforming demonstrator; or a predictable environment with either (3) an informing demonstrator or (4) an uninforming demonstrator. Environmental predictability was manipulated by altering the meaning of available color cues. Subjects in the unpredictable environment that had an informing demonstrator performed significantly better than subjects in an unpredictable environment with an uninforming demonstrator, although only on the second day of testing. Subjects in both the predictable conditions performed similarly to each other. The results suggest that social information is more valuable to individuals in an unpredictable environment than it is in a predictable environment; however, there appears to be a time lag in the ability of the birds to recognize the value of this information.     

Genetic basis in motor skill and hand preference for tool use in chimpanzees (Pan troglodytes)

Chimpanzees are well known for their tool using abilities. Numerous studies have documented variability in tool use among chimpanzees and the role that social learning and other factors play in their development. There are also findings on hand use in both captive and wild chimpanzees; however, less understood are the potential roles of genetic and non-genetic mechanisms in determining individual differences in tool use skill and laterality. Here, we examined heritability in tool use skill and handedness for a probing task in a sample of 243 captive chimpanzees. Quantitative genetic analysis, based on the extant pedigrees, showed that overall both tool use skill and handedness were significantly heritable. Significant heritability in motor skill was evident in two genetically distinct populations of apes, and between two cohorts that received different early social rearing experiences. We further found that motor skill decreased with age and that males were more commonly left-handed than females. Collectively, these data suggest that though non-genetic factors do influence tool use performance and handedness in chimpanzees, genetic factors also play a significant role, as has been reported in humans.     

Critical Social Learning: A Solution to Rogers's Paradox of Nonadaptive Culture

Alan Rogers (1988) presented a game theory model of the evolution of social learning, yielding the paradoxical conclusion that social learning does not increase the fitness of a population. We expand on this model, allowing for imperfections in individual and social learning as well as incorporating a "critical social learning" strategy that tries to solve an adaptive problem first by social learning, and then by individual learning if socially acquired behavior proves unsatisfactory. This strategy always proves superior to pure social learning and typically has higher fitness than pure individual learning, providing a solution to Rogers's paradox of nonadaptive culture. Critical social learning is an evolutionarily stable strategy (ESS) unless cultural transmission is highly unfaithful, the environment is highly variable, or social learning is much more costly than individual learning. We compare the model to empirical data on social learning and on spatial variation in primate cultures and list three requirements for adaptive culture.     

Protective behavior or ‘true’ tool use? Scrutinizing the tool use behavior of ants

In the genus Aphaenogaster, workers use tools to transport liquid food to the colony. During this behavior, ants place or drop various kinds of debris into liquids or soft food, and then, they carry the food‐soaked tools back to the nest. According to some authors, this behavior is not "true" tool use because it represents two separate processes: a defense response to cover the dangerous liquid and a transport of food. Here, we investigated the debris dropping and retrieving behavior of the ant Aphaenogaster subterranea to establish which of the two hypotheses is more probable by conducting manipulative experiments. We tested the responses of eight colonies (a) to liquid food (honey‐water) and nonfood liquids (water) in different distances from the nest and (b) to nonthreatening liquids previously covered or presented as small droplets. We also tested whether the nutritional condition of colonies (i.e., starved or satiated) would affect the intensity and rate of debris dropping. Our results were consistent with the tool‐using behavior hypothesis. Firstly, ants clearly differentiated between honey‐water and water, and they directed more of their foraging effort toward liquids farther from the nest. Secondly, ants performed object dropping even into liquids that did not pose the danger of drowning or becoming entangled. Lastly, the nutritional condition of colonies had a significant effect on the intensity and rate of object dropping, but in the opposite direction than we expected. Our results suggest that the foraging behavior of A. subterranea is more complex than that predicted by the two‐component behavior hypothesis and deserves to be considered as "true" tool use.     

Avoidance of potentially harmful food cannot be socially transmitted between rats

The social transmission of food preferences(STFP) is a behavioural task of olfactory memory, in which an observer rat learns safe food odours from a demonstrator rat, and shows preference for this odour in a subsequent choice test. However, previous studies have failed to detect the transmission of information about food of potential danger and food aversion using STFP test. In this study, we tested how demonstrators' health affects the exchange of odour information and whether observers can learn danger information from an unhealthy demonstrator. As expected, the observer rat formed an odour preference after interacting with a demonstrator rat that had just eaten food containing a new odour, however, odour preference rather than aversion was also formed after interacting with a demonstrator rat injected with LiCl(used to induce gastric malaise). Furthermore, anaesthetized demonstrator rats and half-anaesthetized demonstrator rats, which showed obvious motor deficits suggesting an unhealthy state, also socially transmitted food preferences to observers. These results suggest that the social transmission of food preferences task is independent of a demonstrators' health, and that information about dangerous foods cannot be transmitted using this behavioural task.     

Cognitive requirements for tool use by New Caledonian crows (Corvus moneduloides)

Abstract

Cumulative technological evolution has been suggested to explain the existence of different pandanus tool designs manufactured by New Caledonian crows. Circumstantial evidence from the distribution of the three tool designs that they manufacture suggests transmission of the designs probably involves accurate social learning, a characteristic considered essential for the cumulative evolution of tools. Recently, Kenward et al. (2005) reported that four hand‐raised crows developed basic stick tool use without social learning. This finding cast doubt on the importance of social learning in the evolution of crows’ pandanus tools in the wild. Here, we report that a naïve male crow at Parc Zoo‐Forestier, Nouméa, developed proficient stick tool use without social input in 2002. In 2004, four captive crows, including the naïve male, that were inexperienced with pandanus material were given an opportunity to use and/or manufacture pandanus tools. Only two of the four birds used the tools but none manufactured tools. Our preliminary findings and the work with the four hand‐raised crows keep open the possibility that the evolution of crows’ pandanus tool designs is based on social learning. We propose that social learning and a disposition to develop basic tool use without social input are both essential cognitive requirements for cumulative technological evolution.     

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.     

Learning to fear and cope with a natural stressor: individually and socially acquired corticosterone and avoidance responses to biting flies

Animals learn to recognize and respond to a variety of dangerous factors, with biting and blood-feeding flies being among the most prevalent of natural stressors. Here we describe the behavioral avoidance and hormonal (corticosterone) stress responses to biting fly exposure and the roles of individual and social learning in the acquisition of these fear-associated responses. Male mice exposed to a single 30-min session of attack by intact biting flies (stable fly, Stomoxys calcitrans L.) exhibited increased plasma corticosterone levels and active self-burying responses to avoid the flies. When exposed 24 h later to altered flies whose biting mouth parts were removed and were incapable of biting, the mice displayed conditioned increases in corticosterone and avoidance responses. This conditioned increase in corticosterone and self-burying was also acquired through social learning without direct individual experience with the intact biting flies. Fly naive "observer" mice that witnessed other "demonstrator" mice being attacked by biting flies, but were not exposed to intact flies themselves, displayed increases in corticosterone levels and self-burying to avoid flies when exposed 24 h later to altered flies. The social learning was not due to social facilitation or sensitization. Observers had to witness the self-burying avoidance responses of the demonstrator to the biting flies in order to subsequently recognize a potential threat to themselves and display the appropriate responses. These individually and socially acquired conditioned fear responses are likely part of the mechanisms that allow animals to defend themselves from biting and blood-feeding arthropods.     

Individual consistency and flexibility in human social information use

Copying others appears to be a cost-effective way of obtaining adaptive information, particularly when flexibly employed. However, adult humans differ considerably in their propensity to use information from others, even when this ‘social information’ is beneficial, raising the possibility that stable individual differences constrain flexibility in social information use. We used two dissimilar decision-making computer games to investigate whether individuals flexibly adjusted their use of social information to current conditions or whether they valued social information similarly in both games. Participants also completed established personality questionnaires. We found that participants demonstrated considerable flexibility, adjusting social information use to current conditions. In particular, individuals employed a ‘copy-when-uncertain’ social learning strategy, supporting a core, but untested, assumption of influential theoretical models of cultural transmission. Moreover, participants adjusted the amount invested in their decision based on the perceived reliability of personally gathered information combined with the available social information. However, despite this strategic flexibility, participants also exhibited consistent individual differences in their propensities to use and value social information. Moreover, individuals who favoured social information self-reported as more collectivist than others. We discuss the implications of our results for social information use and cultural transmission.     

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.     

Oral tool use by captive orangutans (Pongo pygmaeus)

Eight captive orangutans (Pongo pygmaeus) were given wooden blocks embedded with raisins and bamboo as raw material for tool making in a study of manual laterality. In about three quarters of the raisin extraction bouts, the orangutans held the tool in the lips or teeth rather than in their hands. Three adult males and 2 adult females showed extreme (> or =92%) preference for oral tool use, a subadult male and an adult female used oral tools about half the time, and 1 adult female preferred manual tool use. Most oral tool users made short tools (approx. 4-10 cm long) that were held in the lips and (probably) supported by the tongue. Preference for oral tool use does not correlate with body weight, age or sex, but it may be related to hand size or individual preference. This is the first report of customary oral tool use as the norm in captive orangutans; it resembles the behavioral patterns reported by van Schaik et al. and Fox et al. in nature.