Scrounging facilitates social learning in common marmosets, Callithrix jacchus

doi:10.1006/anbe.2003.2145

Animal Behaviour

Volume 65, Issue 6, June 2003, Pages 1085-1092

https://doi.org/10.1006/anbe.2003.2145 Get rights and content

Abstract

We investigated the effect of close social interaction on the ability to learn a new behaviour via observation. The task chosen involved sliding a small door horizontally to gain access to a food reward. We divided 59 common marmosets into five groups that received different pretest experience: observation of a trained demonstrator through wire mesh (O); joint interaction with a trained demonstrator allowing the possibility of scrounging (S); individual interaction with the apparatus (I); joint interaction with another naı̈ve individual (J); and no prior experience (control, C). Significantly more individuals from the scrounging group learned the new behaviour, compared with the group (O) that had purely observational experience. When animals from group O were later allowed to interact jointly with a trained demonstrator, the success rate of this group significantly increased. Social interaction with the demonstrator may have facilitated learning because it allowed subjects to understand the relation between the apparatus and the food or because social support facilitated interaction with the apparatus. However, results from the other conditions suggest that these factors alone do not account for the size of the effect. Thus, contrary to previous investigations of this phenomenon, scrounging facilitated social learning. This result probably depended on a complex interaction of a number of factors, including individual learning opportunities, social support and closer attention to the demonstrator. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour

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Citation Excerpt :
Likewise, marmosets who were administered with a combination of video demonstrations (purely observational learning) and live demonstrations (both social and observational learning) more aptly learned the relationship between the test apparatus and the enclosed fruit, in comparison to those who only experienced observational learning, or marmosets who were paired with naïve (inexperienced) individuals (Caldwell and Whiten, 2003). Thus, facilitation of social learning involves an interplay of the individual learning characteristics, social closeness, and attention to the demonstrator (Caldwell and Whiten, 2003; Caldwell and Whiten, 2004). Inter-individual differences, including sex and personality traits, can influence social-cognitive abilities in humans (Geary et al., 2000; Cotto et al., 2010; Becker et al., 2012) and animals (Réale et al., 2007; Dougherty and Guillette, 2018; Gartland et al., 2021).
Social-cognitive processes facilitate the use of environmental cues to understand others, and to be understood by others. Animal models provide vital insights into the neural underpinning of social behaviours. To understand social cognition at even deeper behavioural, cognitive, neural, and molecular levels, we need to develop more representative study models, which allow testing of novel hypotheses using human-relevant cognitive tasks. Due to their cooperative breeding system and relatively small size, common marmosets (Callithrix jacchus) offer a promising translational model for such endeavours. In addition to having social behavioural patterns and group dynamics analogous to those of humans, marmosets have cortical brain areas relevant for the mechanistic analysis of human social cognition, albeit in simplified form. Thus, they are likely suitable animal models for deciphering the physiological processes, connectivity and molecular mechanisms supporting advanced cognitive functions. Here, we review findings emerging from marmoset social and behavioural studies, which have already provided significant insights into executive, motivational, social, and emotional dysfunction associated with neurological and psychiatric disorders.
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The relative importance of individual and social learning in acquiring complex technological skills in animals is debated, especially the influence of processes allowing high copying fidelity (namely, imitation and teaching). We investigated how immature wild chimpanzees, Pan troglodytes troglodytes, acquired the technique for extracting underground honey. This technique is interesting because (1) adults perform exploration, pounding and perforation in nonrandom but highly flexible action sequences to locate underground bee nests, (2) they have individual preferences for how to perforate the ground and (3) the nests are deeply buried and concealed, making success difficult to achieve. We analysed the behaviour of 16 immatures recorded by camera traps at 50 sites, and tested the influence of individual attributes (namely, age and sex) and maternal behaviour; we also tested whether mothers provided learning opportunities for their offspring. We found that, as they aged, immatures of both sexes progressively matched adults' behaviour in action sequences and observed their social models more continuously. Immature males used the most common grip type used by adults for perforating (namely, the coordinated use of hands and feet) progressively more as they aged, but no effect of maternal preferences was detected. Thus, the adult technique was probably acquired via a combination of physical maturation (i.e. increased body strength and motor coordination) and observational learning, although individual learning could not be completely ruled out. Finally, the proportion of time mothers spent inactive at bee nest sites was high when they were accompanied by young daughters and decreased as daughters aged, while the opposite pattern was found for sons. Mothers may thus stimulate learning by immatures by adjusting their behaviour according to their offspring's sex and age. Overall, we showed that immature chimpanzees acquired this complex tool use behaviour via a combination of social and nonsocial learning processes, including potential maternal stimulation.
Personality-dependent differences in problem-solving performance in a social context reflect foraging strategies
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Individuals develop innovative behaviours to solve foraging challenges in the face of changing environmental conditions. Little is known about how individuals differ in their tendency to solve problems and in their subsequent use of this solving behaviour in social contexts. Here we investigated whether individual variation in problem-solving performance could be explained by differences in the likelihood of solving the task, or if they reflect differences in foraging strategy. We tested this by studying the use of a novel foraging skill in groups of great tits (Parus major), consisting of three naive individuals with different personality, and one knowledgeable tutor. We presented them with multiple, identical foraging devices over eight trials. Though birds of different personality type did not differ in solving latency; fast and slow explorers showed a steeper increase over time in their solving rate, compared to intermediate explorers. Despite equal solving potential, personality influenced the subsequent use of the skill, as well as the pay-off received from solving. Thus, variation in the tendency to solve the task reflected differences in foraging strategy among individuals linked to their personality. These results emphasize the importance of considering the social context to fully understand the implications of learning novel skills.
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Despite extensive research on social learning in humans and animals, the mechanisms of social learning and the causes of its success or failure are still being debated. In the case of social foraging, there is conflicting evidence as to whether scrounging on conspecifics' food finding facilitates social learning or, rather, inhibits learning of food-related cues. In house sparrows, Passer domesticus, social learning has previously been shown to be inhibited during scrounging. In the present study, we found that hand-reared fledgling house sparrows that were imprinted on a mother model and scrounged on the food that she found readily learned the colour chosen by the mother as a food-related cue. However, our experiment also demonstrated that this social learning may indeed be less effective when it is not mediated by active search: fledglings following a mother model that pointed at the location of the seeds, forcing them to dig actively in the sand, developed a stronger preference for the target colour than fledglings whose mother had exposed the seeds for them. The latter were much more sensitive to information that they had acquired from independent search, which may explain a wide spectrum of variable results in social learning and highlight the potential importance of mechanistic details in its evolution.
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It is well recognized that animals can acquire a new response by observing the behavior of others, however there remains some controversy concerning the mechanisms responsible for this learning. Of particular interest is observational learning, which is presumed to have occurred when an organism copies an improbable action or action-outcome that it has observed and the matching behavior cannot be explained by an alternative mechanism. Psychologists have been especially interested in the form of observational learning known as imitation and in how to distinguish imitation from other processes. To successfully make this distinction, one must distinguish imitation (the copying of the demonstrated behavior) from the degree to which behavioral similarity results from (i) predisposed behavior, (ii) increased motivation resulting from the presence of another animal, (iii) attention drawn to a place or object, (iv) learning about the way the environment works. Several of the processes that may be involved in observational learning are reviewed, including social facilitation, stimulus enhancement, several kinds of emulation, and various forms of imitation.
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Experimental studies on traditions in animals have focused almost entirely on the initial transmission phase in captive populations. We conducted an open diffusion field experiment with 13 groups of wild common marmosets, Callithrix jacchus. Seven groups contained individuals that were already familiar with the task (‘push or pull’ box) and thus served as potential models for naïve individuals. Additionally, in four groups one individual was trained for one of the two possible techniques and in two control groups no skilled individuals were present. First, we investigated whether experienced individuals would remember how to solve the task even after 2 years without exposure and whether they would still prefer their learned technique. Second, we tested whether naïve individuals would learn socially from their skilled family members and, more importantly, whether they would use the same technique. Third, we conducted several test blocks to see whether the individual and/or group behaviour would persist over time. Our results show that wild common marmosets were able to memorize, learn socially and maintain preferences of foraging techniques. This field experiment thus reveals a promising approach to studying social learning in the wild and provides the basis for long-term studies on tradition formation.

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^f1: Correspondence and present address: C. Caldwell, School of Psychology, Washington Singer Laboratories, University of Exeter, Exeter EX4 4QG, U.K.

^f2: A. Whiten is at the School of Psychology, University of St Andrews, St Andrews, Fife KY16 9JU, U.K.

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Animal Behaviour

Abstract

References (21)

Producers and scroungers: a general model and its application to captive flocks of house sparrows

Animal Behaviour

Effects of the knowledge of partners on learning rates in zebra finches, Taeniopygia guttata

Animal Behaviour

Push or pull: an experimental study on imitation in marmosets

Animal Behaviour

On the relation between social dynamics and social learning

Animal Behaviour

Social learning in common ravens, Corvus corax

Animal Behaviour

Scrounging prevents cultural transmission of food-finding behaviour in pigeons

Animal Behaviour

Scrounger numbers and the inhibition of social learning in pigeons

Behavioural Processes

Social learning in small flocks of laying hens

Animal Behaviour

Cultural transmission of feeding behaviour in the black rat (Rattus rattus)

True imitation in marmosets

Animal Behaviour

Cited by (71)

The marmoset as a model for investigating the neural basis of social cognition in health and disease

Acquisition of a complex extractive technique by the immature chimpanzees of Loango National Park, Gabon

Personality-dependent differences in problem-solving performance in a social context reflect foraging strategies

The importance of active search for effective social learning: An experimental test in young passerines

Cognitive and Noncognitive Aspects of Social Learning

Memory, transmission and persistence of alternative foraging techniques in wild common marmosets

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Scrounging facilitates social learning in common marmosets, Callithrix jacchus