Individual and social factors affecting the ability of American crows to solve and master a string pulling task

Crows and other birds in the family Corvidae regularly share information to learn the identity and whereabouts of dangerous predators, but can they use social learning to solve a novel task for a food reward? Here, we examined the factors affecting the ability of 27 wild-caught American crows to solve a common string pulling task in a laboratory setting. We split crows into two groups; one group was given the task after repeatedly observing a conspecific model the solution and the other solved in the absence of conspecific models. We recorded the crows’ estimated age, sex, size, body condition, level of nervousness, and brain volume using DICOM images from a CT scan. Although none of these variables were statistically significant, crows without a conspecific model and large brain volumes consistently mastered the task in the minimum number of days, whereas those with conspecific models and smaller brain volumes required varying and sometimes a substantial number of days to master the task. We found indirect evidence that body condition might also be important for motivating crows to solve the task. Crows with conspecific models were no more likely to initially solve the task than those working the puzzle without social information, but those that mastered the task usually copied the method most frequently demonstrated by their knowledgeable neighbors. These findings suggest that brain volume and possibly body condition may be factors in learning new tasks and that crows can use social learning to refine their ability to obtain a novel food source, although they must initially learn to access it themselves.     

Simple Mechanisms Can Explain Social Learning in Domestic Dogs (Canis familiaris)

Recent studies have suggested that domestic dogs (Canis familiaris) engage in highly complex forms of social learning. Here, we critically assess the potential mechanisms underlying social learning in dogs using two problem‐solving tasks. In a classical detour task, the test dogs benefited from observing a demonstrator walking around a fence to obtain a reward. However, even inexperienced dogs did not show a preference for passing the fence at the same end as the demonstrator. Furthermore, dogs did not need to observe a complete demonstration by a human demonstrator to pass the task. Instead, they were just as successful in solving the problem after seeing a partial demonstration by an object passing by at the end of the fence. In contrast to earlier findings, our results suggest that stimulus enhancement (or affordance learning) might be a powerful social learning mechanism used by dogs to solve such detour problems. In the second task, we examined whether naïve dogs copy actions to solve an instrumental problem. After controlling for stimulus enhancement and other forms of social influence (e.g. social facilitation and observational conditioning), we found that dogs’ problem solving was not influenced by witnessing a skilful demonstrator (either an unknown human, a conspecific or the dog’s owner). Together, these results add to evidence suggesting that social learning may often be explained by relatively simple (but powerful) mechanisms.     

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.     

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.     

An evaluation of the efficacy of video displays for use with chimpanzees (Pan troglodytes)

Video displays for behavioral research lend themselves particularly well to studies with chimpanzees (Pan troglodytes), as their vision is comparable to humans', yet there has been no formal test of the efficacy of video displays as a form of social information for chimpanzees. To address this, we compared the learning success of chimpanzees shown video footage of a conspecific compared to chimpanzees shown a live conspecific performing the same novel task. Footage of an unfamiliar chimpanzee operating a bidirectional apparatus was presented to 24 chimpanzees (12 males, 12 females), and their responses were compared to those of a further 12 chimpanzees given the same task but with no form of information. Secondly, we also compared the responses of the chimpanzees in the video display condition to responses of eight chimpanzees from a previously published study of ours, in which chimpanzees observed live models. Chimpanzees shown a video display were more successful than those in the control condition and showed comparable success to those that saw a live model. Regarding fine-grained copying (i.e. the direction that the door was pushed), only chimpanzees that observed a live model showed significant matching to the model's methods with their first response. Yet, when all the responses made by the chimpanzees were considered, comparable levels of matching were shown by chimpanzees in both the live and video conditions.     

Communication of food quality in captiveMacaca nemestrina and free-rangingAteles geoffroyi

While observational learning and social communication of feeding behavior have been demonstrated several times for edible foods, to date there has been no experimental evidence for learning to avoid distasteful or inedible foods by social cues in primates. A series of experiments on captive pigtail macaques (Macaca nemestrina) and free-ranging spider monkeys (Ateles geoffroyi) was performed to determine if members of these two species would avoid a food item that was rejected by a conspecific. The results indicated that, while individuals were capable of learning to avoid a distasteful food after personal experience, social cues were not sufficient to prevent other individuals from tasting the rejected foods or for discriminating between neutral and distasteful items. The results are discussed in terms of spacing patterns and visual access in the natural foraging situation.     

Mirror-induced social facilitation in stumptailed macaques (Macaca arctoides)

Seven adult female stumptailed macaques (Macaca arctoides) were confronted alternately with their reflection in a mirror and with the mirror covered. The reflection elicited significantly more visual attention and social responding than the control stimulus, replicating previous findings. Mirror-image stimulation did not significantly affect the subjects' manipulation of unfamiliar objects, but it did increase bout-lengths of episodes of drinking from a bottle containing orange juice. Possible explanations for the ability of the mirror to induce social facilitation of drinking but not of object manipulation are discussed, along with possible underlying mechanisms. Mirror-induced social facilitation is further evidence that monkeys interpret their reflection as a conspecific.     

Higher frequency of social learning in China than in the West shows cultural variation in the dynamics of cultural evolution

Cultural evolutionary models have identified a range of conditions under which social learning (copying others) is predicted to be adaptive relative to asocial learning (learning on one''s own), particularly in humans where socially learned information can accumulate over successive generations. However, cultural evolution and behavioural economics experiments have consistently shown apparently maladaptive under-utilization of social information in Western populations. Here we provide experimental evidence of cultural variation in people''s use of social learning, potentially explaining this mismatch. People in mainland China showed significantly more social learning than British people in an artefact-design task designed to assess the adaptiveness of social information use. People in Hong Kong, and Chinese immigrants in the UK, resembled British people in their social information use, suggesting a recent shift in these groups from social to asocial learning due to exposure to Western culture. Finally, Chinese mainland participants responded less than other participants to increased environmental change within the task. Our results suggest that learning strategies in humans are culturally variable and not genetically fixed, necessitating the study of the ‘social learning of social learning strategies'' whereby the dynamics of cultural evolution are responsive to social processes, such as migration, education and globalization.     

Artificially generated cultural variation between two groups of captive monkeys, Colobus guereza kikuyuensis

The majority of studies of social learning in primates have tested subjects in isolation and investigated the effects of learning over very short periods of time. We aimed to test for social learning in two social groups of colobus monkeys, Colobus guereza kikuyuensis. Subjects were shown video footage of familiar monkeys either pushing or pulling a plastic flap to obtain a food reward, while they were given simultaneous access to the same apparatus. Action frequencies showed a significant difference between the two groups, with the pull group performing a higher proportion of pulls to pushes, compared with the push group. Copying persisted even in later sessions during which the demonstration footage was not being shown. We conclude that we successfully generated two contrasting behavioural traditions in these groups of monkeys. We do not know how long this contrast in behaviour would have persisted had we been able to continue testing for an even longer period of time, but further studies using similar designs and even longer test periods would have the power to confirm whether stable behavioural variation can be sustained between groups of monkeys, supported by social transmission.     

Old,socially housed rhesus monkeys manipulate objects

Recent research has indicated that old, individually housed monkeys show little interest in novel objects. Yet unanswered is whether this effect is caused primarily by age or housing condition. The purpose of this study was to assess the role of social living in promoting responsiveness to objects. We measured the rates of object manipulation in older animals, assessed responsiveness over time to particular objects as a measure of habituation, and examined social influences on object use. Several social groups of rhesus monkeys that contained older adults were studied. These groups were housed in indoor pens or in an outdoor enclosure, and all monkeys had continuous access to a variety of objects in their home environment. In contrast to previous studies of individually housed monkeys, our group-housed monkeys showed sustained interest in objects. Old monkeys manipulated objects extensively, and this response was all the more significant, given that the objects were not novel. Monkeys housed in an outdoor enclosure showed object manipulation patterns that were not different from monkeys housed in indoor pens. However, females exhibited much higher object-related responses than males. Social facilitation played a role in the reactions of some monkeys to objects. Patterns of social facilitation as well as avoidance were present in two of the three indoor groups that were observed. Failure to manipulate objects in rhesus macaques appears to be more a function of individual housing than of old age. Factors such as environmental complexity, social needs, and early experience should be considered in order to understand why individually housed rhesus monkeys are unresponsive to objects. © 1993 Wiley-Liss, Inc.     

Sex-specific asymmetries in communication sound perception are not related to hand preference in an early primate

Background  

Left hemispheric dominance of language processing and handedness, previously thought to be unique to humans, is currently under debate. To gain an insight into the origin of lateralization in primates, we have studied gray mouse lemurs, suggested to represent the most ancestral primate condition. We explored potential functional asymmetries on the behavioral level by applying a combined handedness and auditory perception task. For testing handedness, we used a forced food-grasping task. For testing auditory perception, we adapted the head turn paradigm, originally established for exploring hemispheric specializations in conspecific sound processing in Old World monkeys, and exposed 38 subjects to control sounds and conspecific communication sounds of positive and negative emotional valence.     

Learning and imitation as a function of social status in macaque monkeys (Macaca nemestrina)

Learning and imitation were examined in animals selected from two groups of sixteen pigtail monkeys. There were significant differences in performance on a cued-alternation task as a function of both social status within the stable group, and prior exposure to a social model. High status animals responded more frequently, but were less successful in acquiring appropriate response delay. Exposure to the model improved response latencies and acquisition of response delay for all subjects. However, model exposure did not improve alternation performance. Results are discussed in terms of prior social experience of the subjects, general learning strategies, and differential sensitivity to multiple reinforcement contingencies. Findings are related to ethological concepts of imitation, and field reports on primate social learning.     

Three models of song learning: Evidence from behavior

Research on avian song learning has traditionally been based on an instructional model, as exemplified by the sensorimotor model of song development. Several large-scale, species-wide field studies of learned birdsongs have revealed that variation is narrowly restricted to certain aspects of song structure. Other aspects are sufficiently stereotyped and so widely shared by species' members that they qualify as species-specific universals. The limitations on natural song variation are difficult to reconcile with a fully open, instructive model of song learning. An alternative model based on memorization by selection postulates a system of innate neural templates that facilitate the recognition and rapid memorization of conspecific song patterns. Behavioral evidence compatible with this model includes learning preferences, rapid conspecific song learning, and widespread ocurrence of species-specific song universals that are recognized innately but fail to develop in songs of social isolates. A third model combines instruction, in the memorization phase, with selection during song production. An overproduced repertoire of plastic songs previously memorized by instruction is winnowed by selection imposed during social interactions at the time of adult song crystallization. Selection during production is well established as a factor in the song development of several species, in the form of action-based learning. The possible role of selective processes in song memorization merits further neurobiological investigation. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 501–516, 1997     

Partner effects on food consumption in brown capuchin monkeys

It has been claimed that capuchin monkeys (Cebus apella) show inequity aversion in relation to food rewards for a simple exchange task. However, other factors may affect the willingness of a monkey to consume foods of high or low value in the presence of a conspecific. In this study, pairs of monkeys were presented with unequally valued foods, but without any task-performance: they simply received the food under four experimental conditions. By looking at the rate of collection and consumption of low-valued cucumber slices we expected to see variation dependent on whether the partner either had 1) cucumber (equity), 2) grape (inequity), 3) inaccessible cucumber or 4) inaccessible grape. Testing 12 adult capuchin monkeys, our findings differed from those of other authors in that the monkeys failed to show negative reactions to inequity, but rather responded with scramble competition (i.e., fast food collection) in the presence of a conspecific without access to food. They also showed facilitated consumption in the presence of a conspecific consuming high-valued food. Possibly, (in)equity plays a different role if food serves as a reward for a task rather than if it is simply made available for consumption.     

Individual differences in learning behaviours in humans: Asocial exploration tendency does not predict reliance on social learning

A number of empirical studies have suggested that individual differences in asocial exploration tendencies in animals may be related to those in social information use. However, because the ‘exploration tendency’ in most previous studies has been measured without considering the information-gathering processes, it is yet hard to conclude that the animal asocial exploration strategies may be tied to social information use. Here, we studied human learning behaviour in both asocial and social two-armed bandit tasks. By fitting reinforcement learning models including asocial and/or social decision processes, we measured each individual's (1) asocial exploration tendency and (2) social information use. We found consistent individual differences in the exploration tendency in the asocial tasks. We also found substantive heterogeneity in the adopted learning strategies in the social task: Nearly one-third of participants used predominantly the copy-when-uncertain strategy, while the remaining two-thirds were most likely to have relied only on asocial learning. However, we found no significant individual association between the exploration frequency in the asocial task and the use of the social information in the social task. Our results suggest that the social learning strategies may be independent from the asocial exploration strategies in humans.     

A preliminary study of food transfer in Sichuan snub-nosed monkeys (Rhinopithecus roxellana)

Food transfer happens regularly in a few nonhuman primates species that are also characterized by remarkable social tolerance. Sichuan snub-nosed monkeys (Rhinopithecus roxellana), or golden monkeys, which exhibit high social tolerance in their social relationships are thus of interest to see whether tolerance would extend to food transfer. In this study, branch feeding activity was observed in a semi-captive group of Sichuan snub-nosed monkeys, which consisted of 10 subjects that included a one-male unit (OMU) and an all-male unit (AMU). We recorded 1,275 food interactions over 27 days, and 892 instances of food transfer. The most commonly observed types of food transfer behavior were co-feeding (62.1%) and relaxed claim (22.8%). Of 892 food transfers, 756 (84.8%) took place in the OMU, most of which were among adults (34.7%) and among juveniles (42.1%). The transfer success rate was high in both the cases (87.9% for adults and 78.9% for juveniles). Food transfer in the AMU took place less often than that among adults in the OMU though with similar high transfer success. Food transfer between the OMU and AMU was limited to juvenile males from the OMU and adults from the AMU. These results provide the first evidence of food transfer in golden monkeys and suggest that tolerant social relationships in golden monkeys make transfer possible.     

α8‐Integrins are required for hippocampal long‐term potentiation but not for hippocampal‐dependent learning

Integrins are heterodimeric transmembrane cell adhesion receptors that are essential for a wide range of biological functions via cell–matrix and cell–cell interactions. Recent studies have provided evidence that some of the subunits in the integrin family are involved in synaptic and behavioral plasticity. To further understand the role of integrins in the mammalian central nervous system, we generated a postnatal forebrain and excitatory neuron‐specific knockout of α8‐integrin in the mouse. Behavioral studies showed that the mutant mice are normal in multiple hippocampal‐dependent learning tasks, including a T‐maze, non‐match‐to‐place working memory task for which other integrin subunits like α3‐ and β1‐integrin are required. In contrast, mice mutant for α8‐integrin exhibited a specific impairment of long‐term potentiation (LTP) at Schaffer collateral–CA1 synapses, whereas basal synaptic transmission, paired‐pulse facilitation and long‐term depression (LTD) remained unaffected. Because LTP is also impaired in the absence of α3‐integrin, our results indicate that multiple integrin molecules are required for the normal expression of LTP, and different integrins display distinct roles in behavioral and neurophysiological processes like synaptic plasticity.     

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.     

Early experience affects learning performance and neophobia in a cooperatively breeding cichlid

The ability to respond flexibly to environmental challenges, for instance by learning or by responding appropriately to novel stimuli, may be crucial for survival and reproductive success. Experiences made during early ontogeny can shape the degree of behavioural flexibility maintained by individuals during later life. In natural habitats, animals are exposed to a multitude of social and non‐social ecological factors during early ontogeny, but their relative influences on future learning ability and behavioural flexibility are only poorly understood. In the cooperatively breeding cichlid Neolamprologus pulcher, we investigated whether early social and predator experiences shape the learning performance, flexibility, and response to novelty of adults. Fish were reared either with or without parents and helpers and with or without perceived predation risk in a full‐factorial experiment. We investigated the influence of these treatments on learning performance and flexibility in a spatial acquisition and reversal learning task. To test for response to novelty, we performed a neophobia test. We found that fish reared with predator experience, but without the presence of older group members outperformed fish with other rearing backgrounds in reversal learning and that individuals, which had been reared in a socially more complex environment together with older group members responded less neophobic toward a novel object than individuals reared among siblings only. Comparative evidence from fish and rats suggests that these developmental effects may be driven by the cues of safety perceived in the presence of guarding parents.     

Transfer index and mediational learning in tufted capuchins (Cebus apella)

The transfer index (TI) is a discrimination reversal paradigm that requires the achievement of a given prereversal criterion of accuracy. The mediational learning (ML) paradigm is a modification of the TI procedure that features the presentation of three different reversal conditions designed to assess whether prereversal learning is based on purely associative processes or mediated by the use of a strategy (win-stay/lose-shift). These two paradigms have been used with apes and several Old World monkey species, proving to be effective tools for the comparison of species on the basis of their transfer abilities and the nature of their learning processes. However, among New World monkeys, only the squirrel monkey has been tested. Capuchin (Cebusspp.) adaptability and their mastery in using tools have led to controversial interpretations of their cognitive and learning skills. We evaluated their mode of learning and the transfer of learning using the TI and the ML paradigms. We tested four tufted capuchins (Cebus apella)in a WGTA using a variety of stimulus object pairs. The results show that they possess rather good transfer abilities and one subject showed an associative learning mode. None of the subjects showed evidence of learning mediated by a win-stay/lose-shift strategy.