Social learning in animals: categories and mechanisms.

Imitation and local enhancement: Detrimental effects of consensus definitions on analyses of social learning in animals

Human cognition is distinguished by our ability to adapt to different environments and circumstances. Yet the mechanisms driving adaptive behavior have predominantly been studied in separate asocial and social contexts, with an integrated framework remaining elusive. Here, we use a collective foraging task in a virtual Minecraft environment to integrate these two fields, by leveraging automated transcriptions of visual field data combined with high-resolution spatial trajectories. Our behavioral analyses capture both the structure and temporal dynamics of social interactions, which are then directly tested using computational models sequentially predicting each foraging decision. These results reveal that adaptation mechanisms of both asocial foraging and selective social learning are driven by individual foraging success (rather than social factors). Furthermore, it is the degree of adaptivity—of both asocial and social learning—that best predicts individual performance. These findings not only integrate theories across asocial and social domains, but also provide key insights into the adaptability of human decision-making in complex and dynamic social landscapes.

Social learning has been documented in a wide diversity of animals. In free-living animals, however, it has been difficult to discern whether animals learn socially by observing other group members or asocially by acquiring a new behaviour independently. We addressed this challenge by developing network-based diffusion analysis (NBDA), which analyses the spread of traits through animal groups and takes into account that social network structure directs social learning opportunities. NBDA fits agent-based models of social and asocial learning to the observed data using maximum-likelihood estimation. The underlying learning mechanism can then be identified using model selection based on the Akaike information criterion. We tested our method with artificially created learning data that are based on a real-world co-feeding network of macaques. NBDA is better able to discriminate between social and asocial learning in comparison with diffusion curve analysis, the main method that was previously applied in this context. NBDA thus offers a new, more reliable statistical test of learning mechanisms. In addition, it can be used to address a wide range of questions related to social learning, such as identifying behavioural strategies used by animals when deciding whom to copy.

Chapter 7 - Developing a Theory of Animal Social Learning

Group living animals use social and asocial cues to predict the presence of reward or punishment in the environment through associative learning. The degree to which social and asocial learning share the same mechanisms is still a matter of debate. We have used a classical conditioning paradigm in zebrafish, in which a social (fish image) or an asocial (circle image) conditioned stimulus (CS) have been paired with an unconditioned stimulus (US=food), and we have used the expression of the immediate early gene c-fos to map the neural circuits associated with each learning type. Our results show that the learning performance is similar to social and asocial CSs. However, the brain regions activated in each learning type are distinct and a community analysis of brain network data reveals segregated functional submodules, which seem to be associated with different cognitive functions involved in the learning tasks. These results suggest that, despite localized differences in brain activity between social and asocial learning, they share a common learning module and social learning also recruits a specific social stimulus integration module. Therefore, our results support the occurrence of a common general-purpose learning module, that is differentially modulated by localized activation in social and asocial learning.

This case study examines how the Hampton Roads Sea Level Rise Preparedness and Resilience Intergovernmental Planning Pilot Project, a whole-of-government and whole-of-community approach to planning for and adapting to sea level rise, addressed coastal resilience in a southeastern Virginia watershed that spans multiple jurisdictions. Meeting the challenge of sea level rise requires that actors across multiple sectors—citizens, community organizations, industry and government—understand the risks and work together to make critical decisions regarding adaptation strategies and actions. The case study area includes Little Creek Amphibious Base, which is bordered by the cities of Norfolk and Virginia Beach. Adaptation responses to sea level rise by the military base and the local governments will impact each other and the residents of the area, but no cooperative agreements are in place for a joint or collaborative response. This case study examines public and private infrastructure at risk, the infrastructure interdependencies, and mechanisms for providing collaborative solutions. Engagement of area residents and other stakeholders is also integral to the process of adaptation, which includes educating about sea level rise risk and provides a mechanism for social learning that enables stakeholders to participate in critical adaptation decisions. The case study demonstrates a method to improve resiliency in the case study area and inform a regional, multi-sectoral response to sea level rise adaptation strategies.

Classical ethology and behavioral ecology did not pay much attention to learning. However, studies of social learning in nature reviewed here reveal the near-ubiquity of reliance on social information for skill acquisition by developing birds and mammals. This conclusion strengthens the plausibility of the cultural intelligence hypothesis for the evolution of intelligence, which assumes that selection on social learning abilities automatically improves individual learning ability. Thus, intelligent species will generally be cultural species. Direct tests of the cultural intelligence hypothesis require good estimates of the amount and kind of social learning taking place in nature in a broad variety of species. These estimates are lacking so far. Here, we start the process of developing a functional classification of social learning, in the form of the social learning spectrum, which should help to predict the mechanisms of social learning involved. Once validated, the categories can be used to estimate the cognitive demands of social learning in the wild.

Prima facie, the acquisition of novel behaviors in animals through observation of conspecifics seems straightforward. There are, however, various mechanisms through which the behavior of animals can be altered from observing others. These mechanisms range from simple hard-wired contagious processes to genuine learning by observation, which differ fundamentally in cognitive complexity. They range from social facilitation and local enhancement to true social learning. The different learning mechanisms are the subject of this review, largely because research on learning by observation can be confounded by difficulties in interpretation owing to the looming possibility of associative learning infecting experimental results. While it is often assumed that horses are capable of acquiring new behavior through intra-species observation, research on social learning in horses includes a variety of studies some of which may overestimate the possession of higher mental abilities. Assuming such abilities in their absence can have welfare implications, e.g., isolating stereotypical horses on the assumption that these behaviors can be learned though observation by neighboring horses. This review summarizes the definitions and criteria for the various types of social transmission and social learning and reviews the current documentation for each type in horses with the aim of clarifying whether horses possess the ability to learn through true social learning. As social ungulates, horses evolved in open landscapes, exposed to predators and grazing most of the day. Being in close proximity to conspecifics may theoretically offer an opportunity to learn socially, however anti-predator vigilance and locating forage may not require the neural complexity of social learning. Given the significant energetic expense of brain tissue, it is likely that social facilitation and local enhancement may have been sufficient in the adaptation of equids to their niche. As a consequence, social learning abilities may be maladaptive in horses. Collectively, the review proposes a novel differentiation between social transmission (social facilitation, local, and stimulus enhancement) and social learning (goal emulation, imitation). Horses are undoubtedly sensitive to intra-species transfer of information but this transfer does not appear to satisfy the criteria for social learning, and thus there is no solid evidence for true social learning in horses.

Previous empirical work on animal social learning has found that many species lack the ability to learn entire action sequences solely through reliance on social information. Conversely, acquiring action sequences through asocial learning can be difficult due to the large number of potential sequences arising from even a small number of base actions. In spite of this, several studies report that some primates use action sequences in the wild. We investigate how social information can be integrated with asocial learning to facilitate the learning of action sequences. We formalize this problem by examining how learners using temporal difference learning, a widely applicable model of reinforcement learning, can combine social cues with their own experiences to acquire action sequences. The learning problem is modeled as a Markov decision process. The learning of nettle processing by mountain gorillas serves as a focal example. Through simulations, we find that the social facilitation of component actions can combine with individual learning to facilitate the acquisition of action sequences. Our analysis illustrates that how even simple forms of social learning, combined with asocial learning, generate substantially faster learning of action sequences compared to asocial processes alone, and that the benefits of social information increase with the length of the action sequence and the number of base actions.

In many animal species, the juvenile period is under strong selection, leading to a concentration of social learning during this stage as an efficient strategy for young individuals to acquire skills essential for survival. However, as social learning is not always adaptive, juveniles need to be strategic in when, who, and what to copy. In species with extended parental care, parents are often preferred sources of information, leading to stable intergenerational transmission of knowledge. However, little is known about transmission pathways in species with limited periods of parental care, and their implication for cultural inheritance. Here, we investigate social learning strategies during development in a model species with a dependence period of a few weeks, the great tit (Parus major). Using fully automated two-option foraging puzzles, we diffused knowledge about the puzzle through breeding populations and then constrained parental individuals' choices such that parents either (1) both had knowledge of the same option, (2) had conflicting knowledge of the two options, or (3) had no knowledge of how to solve the puzzle. We then tracked solving behavior of 229 newly fledged juveniles over 10 weeks. Parental solving frequency during dependence strongly predicted knowledge acquisition by offspring, suggesting intergenerational cultural inheritance. However, detailed investigation of learning pathways revealed siblings as the most important role models for social learning, followed by nonparental adults and parents. Furthermore, offsprings' option choices were not predicted by parental choices, but instead influenced by the broader social environment, with evidence for a conformist learning bias. Overall, by using large-scale experimental manipulation of parental behavior, our study offers new insights into social learning pathways and mechanisms of cultural inheritance in r-selected species with limited parental care and multiple offspring. Our findings provide a stark contrast to most previously studied systems exhibiting multigenerational cultures, where cultural transmission overwhelmingly occurs from parents to offspring, and give insights into the more variable transmission routes that might occur across socially learning species.

Early naturalists explained field observations of social influences on animal learning in terms of spoken language, deliberate tuition of one animal by another, or intentional imitation. During the first half of the present century, experimental psychologists analyzed instances of social learning by animals in laboratory tasks as special cases of operant or classical conditioning. Neither of these traditional approaches provided much insight into the complex processes that often support animal social learning. By combining ethological focus on social learning as it occurs in natural habitat with analytical techniques developed in the psychological laboratory, contemporary researchers have made considerable progress in describing the many ways in which social interactions influence behavioural development in animals. The author's investigations of social influences on food selection by Norway rats provide one example of such an ethopsychological approach to the study of animal social learning.

Social learning involves the acquisition of information from other individuals and is a behavioural strategy found in a wide range of taxa from insects to humans. Traditionally, research in this field has concentrated on learning from members of the same species; however, there is increasing evidence for social learning across species boundaries. Owing to the ecological overlap of many species, it makes sense that such heterospecific social learning is common, and in some cases, information from another species may be more profitable than that provided by members of the same species. Here, we review the existing literature about learning from individuals of different species. We discuss the cognitive mechanisms underlying this form of information gathering and highlight the importance of past experience and innate predispositions in the formation of interspecific learning events. In many cases, seemingly complex forms of ‘copying’ from members of other species can be explained by relatively simple forms of conditioning.

A species is deemed cultural when there exists behavioural variation across populations that can be at least partly attributed to social learning. Understood in this way, culture has been found in all species of great apes. However some ape behaviours have additionally been claimed to be culture-dependent, implying that copying social learning mechanisms underlie their acquisition (as it occurs in human culture). If that was the case, these ape behaviours should have become locally restricted as a consequence of the unavoidable copying errors accumulated during their transmission between connected individuals. Based on this logic we developed the "Method of Local Restriction" in order to identify potential cases of culture-dependent forms in great apes which distribution is compatible with acquisition via copying (i.e. these behaviours are restricted to a single ape population). After conducting an exhaustive literature search across ape species, populations and behavioural domains, we found that the vast majority of great ape behaviours re-appear in unconnected populations and therefore do not necessarily rely on copying to be acquired. However, we found 25 locally restricted behaviours, three of which were locally unique to a single population of a single great ape species. These behaviours represent the best available candidates of culture-dependent forms in great apes, which reliance on copying social learning should be tested in targeted experiments. Overall our results suggest that great ape cultures are sustained by different learning mechanisms from those at play in human cultures, namely by individual learning mediated by non-copying social learning mechanisms.

Social learning in robotics has largely focused on imitation learning. Here we take a broader view and are interested in the multifaceted ways that a social partner can influence the learning process. We implement four social learning mechanisms on a robot: stimulus enhancement, emulation, mimicking, and imitation, and illustrate the computational benefits of each. In particular, we illustrate that some strategies are about directing the attention of the learner to objects and others are about actions. Taken together these strategies form a rich repertoire allowing social learners to use a social partner to greatly impact their learning process. We demonstrate these results in simulation and with physical robot ‘playmates’.

Conservation translocations are increasingly used in species’ recovery. Their success often depends upon maintaining or restoring survival-relevant behaviour, which is socially learned in many animals. A lack of species- or population-appropriate learning can lead to the loss of adaptive behaviour, increasing the likelihood of negative human interactions and compromising animals’ ability to migrate, exploit resources, avoid predators, integrate into wild populations, reproduce and survive. When applied well, behavioural tools can address deficiencies in socially learned behaviours and boost survival. However, their use has been uneven between species and translocation programmes, and behaviour commonly contributes to translocation failure. Critically, current international guidance (e.g. the International Union for Conservation of Nature’s translocation guidelines) does not directly discuss social learning or its facilitation. We argue that linking knowledge about social learning to appropriate translocation strategies will enhance guidance and direct future research. We offer a framework for incorporating animal social learning into translocation planning, implementation, monitoring and evaluation across wild and captive settings. Our recommendations consider barriers practitioners face in contending with logistics, time constraints and intervention cost. We emphasize that stronger links between researchers, translocation practitioners and wildlife agencies would increase support for social learning research, and improve the perceived relevance and feasibility of facilitating social learning.This article is part of the theme issue ‘Animal culture: conservation in a changing world’.