Foraging zebra finches (Taeniopygia guttata) are public information users rather than conformists

Social learning enables adaptive information acquisition provided that it is not random but selective. To understand species typical decision-making and to trace the evolutionary origins of social learning, the heuristics social learners use need to be identified. Here, we experimentally tested the nature of majority influence in the zebra finch. Subjects simultaneously observed two demonstrator groups differing in relative and absolute numbers (ratios 1 : 2/2 : 4/3 : 3/1 : 5) foraging from two novel food sources (black and white feeders). We find that demonstrator groups influenced observers'' feeder choices (social learning), but that zebra finches did not copy the majority of individuals. Instead, observers were influenced by the foraging activity (pecks) of the demonstrators and in an anti-conformist fashion. These results indicate that zebra finches are not conformist, but are public information users.     

Foraging nine-spined sticklebacks prefer to rely on public information over simpler social cues

Social animals can observe others' behavior and in the processacquire information of varying quality about a given resource.Theoretical models predict that blind copying of others' behavioris more likely when individuals are only able to observe thedecisions (here "social cues") of others rather than the cues(here "public information") on which such decisions are based.We investigated information use by nine-spined sticklebacks(Pungitius pungitius) in a two-patch foraging context. Socialcues were provided by the number of demonstrator fish presentat each patch (two versus six), which either conflicted withthe demonstrators' observed feeding rate at each patch (publicinformation) or was the only information available. Consistentwith predictions, observers preferred the patch previously associatedwith six demonstrators when social cues were the only availablesource of information but preferred the patch previously associatedwith two demonstrators ("rich" patch) when also provided withpublic information. On the bases of these experiments, we arguethat it is because these fish preferentially base decisionson public information rather than social cues that they canpotentially avoid engaging in erroneous informational cascades.Thus, the availability of public information can help socialanimals make adaptive decisions.     

The Effect of Familiarity with Demonstrators on Social Learning in Three‐Spined Sticklebacks (Gasterosteus aculeatus)

Social learning is an important process in the spread of information, especially in changing environments where inherited behaviors may not remain relevant. In many species, the decision of whom to trust to have reliable information depends on the relationship between individuals. Many fish species, including three‐spined sticklebacks, preferentially associate with familiar individuals. Previous studies in three‐spined sticklebacks have provided mixed evidence about the effect of familiarity on social learning in this species. Therefore, this study further explores familiarity and social learning in sticklebacks, specifically from a demonstrator‐focused perspective. We found that in a food patch discrimination task, individuals with unfamiliar demonstrators performed significantly better than those with familiar demonstrators. In a problem‐solving task, we found that focal fish attended to the behavior of demonstrators, but we did not detect an effect of familiarity on performance, and indeed the proportion of individuals to solve the task after observing demonstrators was low. These results suggest that sticklebacks have a preference for unfamiliar demonstrators, but that the use of social information varies depending on context.     

The Importance of Validating Experimental Setups: Lessons from Studies of Food Choice Copying in Zebra Finches

The use of social information for foraging decisions has attracted much research attention. One line of research makes use of experimental assays of food choice copying to study whether specific traits of demonstrators influence whether or not an onlooking individual will copy their behavior. For instance, Benskin (Animal Behaviour, 64, 2002 and 823) reported that captive juvenile zebra finches always copied the foraging decision made by a male wearing red color rings as opposed to one wearing green rings. Here, we report an attempt to examine the generalizability of this finding using another zebra finch population. Our experiment did not show any effect of male ring color on onlooker's food choice and further revealed various population‐specific differences in behavior, for instance, in aversion toward novel feeding sources. We therefore conducted two follow‐up experiments to test the validity of the behavioral assay. These experiments revealed that zebra finches of our population often do not copy demonstrator food choice at all, and that copying, if it occurs, may be sensitive to very specific conditions of the experimental setup. Problematically, after testing a total of 124 onlookers (60 in the first experiment, 32 in the second, and 32 in the third), we still cannot confidently say whether or when our birds copy from demonstrators. Hence, we emphasize the risks of adopting experimental procedures that have proven successful in one study, without extensively validating them for the own study. The seemingly more rewarding follow‐up experiments can bear high risks of yielding false‐positive findings that can then be misinterpreted as justification for an actually uninformative experimental procedure.     

Social learning in young-of-the-year perch encountering a novel food type

Young-of-the-year perch Perca fluviatilis were presented with a novel food type, dry feed, in the presence or absence of demonstrators, who were experienced to the feed. Most inexperienced fish lost mass in the beginning of the study, but untrained fish in the presence of demonstrators already had positive average growth during the first time period. There was a positive correlation between boldness and body mass change. Both social environment and individual characteristics thus seem to affect learning in perch.     

Reproductive state affects reliance on public information in sticklebacks

The degree to which animals use public and private sources of information has important implications for research in both evolutionary ecology and cultural evolution. While researchers are increasingly interested in the factors that lead individuals to vary in the manner in which they use different sources of information, to date little is known about how an animal''s reproductive state might affect its reliance on social learning. Here, we provide experimental evidence that in foraging ninespine sticklebacks (Pungitius pungitius), gravid females increase their reliance on public information generated by feeding demonstrators in choosing the richer of two prey patches than non-reproductive fish, while, in contrast, reproductive males stop using public information. Subsequent experiments revealed reproductive males to be more efficient asocial foragers, less risk-averse and generally less social than both reproductive females and non-reproductives. These findings are suggestive of adaptive switches in reliance on social and asocial sources of information with reproductive condition, and we discuss the differing costs of reproduction and the proximate mechanisms that may underlie these differences in information use. Our findings have important implications for our understanding of adaptive foraging strategies in animals and for understanding the way information diffuses through populations.     

SOCIAL LEARNERS REQUIRE PROCESS INFORMATION TO OUTPERFORM INDIVIDUAL LEARNERS

Humans exhibit a rich and complex material culture with no equivalent in animals. Also, social learning, a crucial requirement for culture, is particularly developed in humans and provides a means to accumulate knowledge over time and to develop advanced technologies. However, the type of social learning required for the evolution of this complex material culture is still debated. Here, using a complex and opaque virtual task, the efficiency of individual learning and two types of social learning (product‐copying and process‐copying) were compared. We found that (1) individuals from process‐copying groups outperformed individuals from product‐copying groups or individual learners, whereas access to product information was not a sufficient condition for providing an advantage to social learners compared to individual learners; (2) social learning did not seem to affect the exploration of the fitness landscape; (3) social learning led to strong within‐group convergence and also to between‐group convergence, and (4) individuals used widely variable social learning strategies. The implications of these results for cumulative culture evolution are discussed.     

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.     

The evolutionary basis of human social learning

Humans are characterized by an extreme dependence on culturally transmitted information. Such dependence requires the complex integration of social and asocial information to generate effective learning and decision making. Recent formal theory predicts that natural selection should favour adaptive learning strategies, but relevant empirical work is scarce and rarely examines multiple strategies or tasks. We tested nine hypotheses derived from theoretical models, running a series of experiments investigating factors affecting when and how humans use social information, and whether such behaviour is adaptive, across several computer-based tasks. The number of demonstrators, consensus among demonstrators, confidence of subjects, task difficulty, number of sessions, cost of asocial learning, subject performance and demonstrator performance all influenced subjects' use of social information, and did so adaptively. Our analysis provides strong support for the hypothesis that human social learning is regulated by adaptive learning rules.     

Effects of Conformism on the Cultural Evolution of Social Behaviour

Models of cultural evolution study how the distribution of cultural traits changes over time. The dynamics of cultural evolution strongly depends on the way these traits are transmitted between individuals by social learning. Two prominent forms of social learning are payoff-based learning (imitating others that have higher payoffs) and conformist learning (imitating locally common behaviours). How payoff-based and conformist learning affect the cultural evolution of cooperation is currently a matter of lively debate, but few studies systematically analyse the interplay of these forms of social learning. Here we perform such a study by investigating how the interaction of payoff-based and conformist learning affects the outcome of cultural evolution in three social contexts. First, we develop a simple argument that provides insights into how the outcome of cultural evolution will change when more and more conformist learning is added to payoff-based learning. In a social dilemma (e.g. a Prisoner’s Dilemma), conformism can turn cooperation into a stable equilibrium; in an evasion game (e.g. a Hawk-Dove game or a Snowdrift game) conformism tends to destabilize the polymorphic equilibrium; and in a coordination game (e.g. a Stag Hunt game), conformism changes the basin of attraction of the two equilibria. Second, we analyse a stochastic event-based model, revealing that conformism increases the speed of cultural evolution towards pure equilibria. Individual-based simulations as well as the analysis of the diffusion approximation of the stochastic model by and large confirm our findings. Third, we investigate the effect of an increasing degree of conformism on cultural group selection in a group-structured population. We conclude that, in contrast to statements in the literature, conformism hinders rather than promotes the evolution of cooperation.     

Social learning about egg-laying substrates in fruitflies

Social learning, defined as learning from other individuals, has had dramatic effects on some species, including humans, in whom it has generated a rich culture. As a first step in examining the evolution of and mechanisms underlying social learning in insects, we tested for social learning in fruitflies (Drosophila melanogaster). Focal females (observers) that experienced novel food together with mated females (models), who had laid eggs on that food, subsequently exhibited a stronger preference for laying eggs on that food over another novel food compared with focal females that experienced the food alone. We observed no social learning, however, when observers experienced food with potentially more ambiguous social information provided by the presence of either virgin models or aggregation pheromone. This first documentation of social learning about egg-laying substrates in fruitflies builds on recent data indicating intricate use of social information by fruitflies and opens up exciting avenues for research on the evolution and neurogenetics of social learning using biology''s major model system.     

Social enhancement can create adaptive,arbitrary and maladaptive cultural traditions

Many animals are known to learn socially, i.e. they are able to acquire new behaviours by using information from other individuals. Researchers distinguish between a number of different social-learning mechanisms such as imitation and social enhancement. Social enhancement is a simple form of social learning that is among the most widespread in animals. However, unlike imitation, it is debated whether social enhancement can create cultural traditions. Based on a recent study on capuchin monkeys, we developed an agent-based model to test the hypotheses that (i) social enhancement can create and maintain stable traditions and (ii) social enhancement can create cultural conformity. Our results supported both hypotheses. A key factor that led to the creation of cultural conformity and traditions was the repeated interaction of individual reinforcement and social enhancement learning. This result emphasizes that the emergence of cultural conformity does not necessarily require cognitively complex mechanisms such as ‘copying the majority’ or group norms. In addition, we observed that social enhancement can create learning dynamics similar to a ‘copy when uncertain’ learning strategy. Results from additional analyses also point to situations that should favour the evolution of learning mechanisms more sophisticated than social enhancement.     

The ethological analysis of imitation

Theorists and experimental researchers have long debated whether animals are able to imitate. A variety of definitions of imitation have been proposed to describe this complex form of social learning. Experimental research on imitation has often been hampered by either a too loose 'anthropomorphic' approach or by too narrow 'behaviourist' definitions. At present neither associative nor cognitive theories are able to offer an exhaustive explanation of imitation in animals. An ethological approach to imitation offers a different perspective. By integrating questions on function, mechanism, development and evolution one can identify possible directions for future research. At present, however, we are still far from developing a comprehensive theory of imitation. A functional approach to imitation shows that, despite some evidence for imitative learning in food processing in apes, such learning has not been shown to be involved in the social transmission of either tool-use skills or communicative signals. Recently developed procedures offer possible ways of clarifying the role of imitation in tool use and visual communication. The role of imitation in explorative play in apes is also investigated and the available data suggest that copying during play might represent a behavioural homologue of human imitation. It is proposed that the ability to copy the behaviour of a companion is under a strong genetic influence in many social species. Many important factors have not been examined experimentally, e.g. the effect of the demonstrator, the influence of attention and memory and the ability to generalize. The potential importance of reinforcement raises the possibility that copying abilities serving divergent functions might be partly under the control of different mechanisms.     

Social enhancement and social inhibition of foraging behaviour in hatchery-reared Atlantic salmon

The results of two experiments showed that observation of a trained conspecific Atlantic salmon Salmo salar significantly increased the rate at which naïve hatchery-reared fish accepted novel, live prey items, whereas the presence of an untrained conspecific actually decreased learning rates due to social inhibition. Pre-release training involving exposure of hatchery-reared fish to live prey items in the presence of pre-trained demonstrators would result in a significant enhancement in their foraging success on release and help prevent starvation, which is thought to be one of the principal causes of post-release mortality in hatchery-reared fishes.     

Social learning of prey location in hatchery-reared Atlantic salmon

Naïve, hatchery-reared Atlantic salmon Salmo salar parr were paired with demonstrators that had been pre-trained to accept live prey from the surface or from the benthos. After 6 days of observing demonstrators through a clear perspex partition the naïve fish's benthic foraging skills were tested. The results revealed that hatchery-reared Atlantic salmon can be taught to target benthic prey items by observation alone and social learning protocols can be utilized to dramatically increase benthic foraging success. The results are discussed with reference to refining hatchery-rearing practices with a view to improving the post-release survival of hatchery fishes. The role of learning, and in particular social learning, in the development foraging behaviour is highlighted.     

From fish to fashion: experimental and theoretical insights into the evolution of culture

Recent years have witnessed a re-evaluation of the cognitive capabilities of fishes, including with respect to social learning. Indeed, some of the best experimental evidence for animal traditions can be found in fishes. Laboratory experimental studies reveal that many fishes acquire dietary, food site and mating preferences, predator recognition and avoidance behaviour, and learn pathways, through copying other fishes. Concentrating on foraging behaviour, we will present the findings of laboratory experiments that reveal social learning, behavioural innovation, the diffusion of novel behaviour through populations and traditional use of food sites. Further studies reveal surprisingly complex social learning strategies deployed by sticklebacks. We will go on to place these observations of fish in a phylogenetic context, describing in which respects the learning and traditionality of fish are similar to, and differ from, that observed in other animals. We end by drawing on theoretical insights to suggest processes that may have played important roles in the evolution of the human cultural capability.     

Simulated Trust: A cheap social learning strategy

Animals use heuristic strategies to determine from which conspecifics to learn socially. This leads to directed social learning. Directed social learning protects them from copying non-adaptive information. So far, the strategies of animals, leading to directed social learning, are assumed to rely on (possibly indirect) inferences about the demonstrator’s success. As an alternative to this assumption, we propose a strategy that only uses self-established estimates of the pay-offs of behavior. We evaluate the strategy in a number of agent-based simulations. Critically, the strategy’s success is warranted by the inclusion of an incremental learning mechanism. Our findings point out new theoretical opportunities to regulate social learning for animals. More broadly, our simulations emphasize the need to include a realistic learning mechanism in game-theoretic studies of social learning strategies, and call for re-evaluation of previous findings.     

Familiarity affects social network structure and discovery of prey patch locations in foraging stickleback shoals

Numerous factors affect the fine-scale social structure of animal groups, but it is unclear how important such factors are in determining how individuals encounter resources. Familiarity affects shoal choice and structure in many social fishes. Here, we show that familiarity between shoal members of sticklebacks (Gasterosteus aculeatus) affects both fine-scale social organization and the discovery of resources. Social network analysis revealed that sticklebacks remained closer to familiar than to unfamiliar individuals within the same shoal. Network-based diffusion analysis revealed that there was a strong untransmitted social effect on patch discovery, with individuals tending to discover a task sooner if a familiar individual from their group had previously done so than if an unfamiliar fish had done so. However, in contrast to the effect of familiarity, the frequency with which individuals had previously associated with one another had no effect upon the likelihood of prey patch discovery. This may have been due to the influence of fish on one another''s movements; the effect of familiarity on discovery of an empty ‘control’ patch was as strong as for discovery of an actual prey patch. Our results demonstrate that factors affecting fine-scale social interactions can also influence how individuals encounter and exploit resources.     

Conspecific and heterospecific information use in bumblebees

Heterospecific social learning has been understudied in comparison to interactions between members of the same species. However, the learning mechanisms behind such information use can allow animals to be flexible in the cues that are used. This raises the question of whether conspecific cues are inherently more influential than cues provided by heterospecifics, or whether animals can simply use any cue that predicts fitness enhancing conditions, including those provided by heterospecifics. To determine how freely social information travels across species boundaries, we trained bumblebees (Bombus terrestris) to learn to use cues provided by conspecifics and heterospecific honey bees (Apis mellifera) to locate valuable floral resources. We found that heterospecific demonstrators did not differ from conspecifics in the extent to which they guided observers'' choices, whereas various types of inorganic visual cues were consistently less effective than conspecifics. This was also true in a transfer test where bees were confronted with a novel flower type. However, in the transfer test, conspecifics were slightly more effective than heterospecific demonstrators. We then repeated the experiment with entirely naïve bees that had never foraged alongside conspecifics before. In this case, heterospecific demonstrators were equally efficient as conspecifics both in the initial learning task and the transfer test. Our findings demonstrate that social learning is not a unique process limited to conspecifics and that through associative learning, interspecifically sourced information can be just as valuable as that provided by conspecific individuals. Furthermore the results of this study highlight potential implications for understanding competition within natural pollinator communities.     

Social learning of foraging sites and escape routes in wild Trinidadian guppies

We describe two field experiments with wild guppies, Poecilia reticulata, in Trinidad that demonstrated that guppies can acquire foraging and predator escape-response information from conspecifics. In the foraging experiment, subjects were presented with two distinctly marked feeders in their home rivers. One feeder contained a conspecific shoal in a transparent container. Guppies preferred to enter the feeder containing this artificial shoal over the other feeder. In a test phase, the artificial shoal was removed and the feeders replaced at the testing site after a 5-min delay. More guppies entered the feeder that had contained the artificial shoal over the other feeder, a difference that can be explained only by the fish learning the characteristics or location of the feeder during the training phase. We suggest that subjects acquired a foraging patch preference through a propensity to approach feeding conspecifics, a local enhancement process. In the predator escape-response experiment, na?ve ‘observer’ guppies could avoid an approaching trawl net by escaping through either a hole to which ‘demonstrator’ guppies had been trained or through an alternative hole. When the demonstrators were present, the na?ve observers escaped more often and more rapidly by the demonstrated route than the alternative route. When the demonstrators were removed, observers maintained a route preference according to the training of their demonstrators, which suggests that the observers had learned an escape route through following or observing their more knowledgeable conspecifics. Thus, both experiments reveal that guppies can socially learn in the wild. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.