M. M. Webster

Cognitive culture: theoretical and empirical insights into social learning strategies

Research into social learning (learning from others) has expanded significantly in recent years, not least because of productive interactions between theoretical and empirical approaches. This has been coupled with a new emphasis on learning strategies, which places social learning within a cognitive decision-making framework. Understanding when, how and why individuals learn from others is a significant challenge, but one that is critical to numerous fields in multiple academic disciplines, including the study of social cognition.

Personality and social context

There has been considerable interest among biologists in the phenomenon of non‐human animal personality in recent years. Consistent variations among individuals in their behavioural responses to ecologically relevant stimuli, often relating to a trade‐off between level of risk and reward, have been recorded in a wide variety of species, representing many animal taxa. Research into behavioural variation among individuals has major implications for our understanding of ecological patterns and processes at scales from the level of the individual to the level of the population. Until recently, however, many studies that have considered the broader ecological implications of animal personality have failed to take into account the crucial moderating effect of social context. It is well documented that social processes, such as conformity and facilitation, exert considerable influence on the behaviour of grouping animals and hence that isolated individuals may often behave in a qualitatively as well as quantitatively different manner to those in groups. Recently, a number of studies have begun to address aspects of this gap in our knowledge and have provided vital insights. In this review we examine the state of our knowledge on the relationship between individual personality and sociality. In doing so we consider the influence of the social context on individual personality responses, the interaction between the collective personalities of group members and the expression of those personalities in the individual, and the influence of the personalities of group members on group structure and function. We propose key areas of focus for future studies in order to develop our understanding of this fundamentally important area.

Lessons from animal teaching

Many species are known to acquire valuable life skills and information from others, but until recently it was widely believed that animals did not actively facilitate learning in others. Teaching was regarded as a uniquely human faculty. However, recent studies suggest that teaching might be more common in animals than previously thought. Teaching is present in bees, ants, babblers, meerkats and other carnivores but is absent in chimpanzees, a bizarre taxonomic distribution that makes sense if teaching is treated as a form of altruism. Drawing on both mechanistic and functional arguments, we integrate teaching with the broader field of animal social learning, and show how this aids understanding of how and why teaching evolved, and the diversity of teaching mechanisms.

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 copying1 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.

Boldness is influenced by social context in threespine sticklebacks (Gasterosteus aculeatus)

Summary Boldness refers to the extent to which animals balance risk against benefits when engaging in such behaviors as foraging, exploration or resource competition. Evidence suggests that individuals can behave strategically, acting boldly in situations when doing so is adaptive, whilst avoiding risk when the rewards are correspondingly lower. In this study we sought to determine the effects of social context upon the boldness of threespine sticklebacks (Gasterosteus aculeatus). We found that when individuals were tested alone, those that were more active were more likely to resume foraging sooner when subjected to a simulated predator attack in a separate test, and also consumed more prey in foraging competition trials. We found no effect of group size upon the relative ability of individuals to effectively compete for prey. Group size did affect other behaviours however: focal fish were more active and resumed foraging more rapidly when tested in groups that they did when tested alone. Finally, individual social information use was not correlated with behaviour in other contexts. Two competing hypotheses, the adaptation and the constraint hypotheses have been posited to explain the presence and prevalence of individual variation in boldness; our findings offer partial support for the former of these.

Social learning strategies and predation risk: minnows copy only when using private information would be costly

Animals can acquire information from the environment privately, by sampling it directly, or socially, through learning from others. Generally, private information is more accurate, but expensive to acquire, while social information is cheaper but less reliable. Accordingly, the ‘costly information hypothesis’ predicts that individuals will use private information when the costs associated with doing so are low, but that they should increasingly use social information as the costs of using private information rise. While consistent with considerable data, this theory has yet to be directly tested in a satisfactory manner. We tested this hypothesis by giving minnows (Phoxinus phoxinus) a choice between socially demonstrated and non-demonstrated prey patches under conditions of low, indirect and high simulated predation risk. Subjects had no experience (experiment 1) or prior private information that conflicted with the social information provided by the demonstrators (experiment 2). In both experiments, subjects spent more time in the demonstrated patch than in the non-demonstrated patch, and in experiment 1 made fewer switches between patches, when risk was high compared with when it was low. These findings are consistent with the predictions of the costly information hypothesis, and imply that minnows adopt a ‘copy-when-asocial-learning-is-costly’ learning strategy.

Social recognition in wild fish populations.

The ability of animals to gather information about their social and physical environment is essential for their ecological function. Odour cues are an important component of this information gathering across taxa. Recent laboratory studies have revealed the importance of flexible chemical cues in facilitating social recognition of fishes. These cues are known to be mediated by recent habitat experience and fishes are attracted to individuals that smell like themselves. However, to be relevant to wild populations, where animals may move and forage freely, these cues would have to be temporally flexible and allow spatial resolution. Here, we present data from a study of social recognition in wild populations of three-spined sticklebacks (Gasterosteus aculeatus). Focal fish preferentially associated with conspecifics from the same habitat as themselves. These preferences were changed and updated following translocation of the focal fish to a different site. Further investigation revealed that association preferences changed after 3 h of exposure to different habitat cues. In addition to temporal flexibility, the cues also allowed a high degree of spatial resolution: fish taken from sites 200 m apart produced cues that were sufficiently different to enable the focal fish to discriminate and associate with fish captured near their own home site. The adaptive benefits of this social recognition mechanism remain unclear, though they may allow fish to orient within their social environment and gain current local information.

Habitat-specific chemical cues influence association preferences and shoal cohesion in fish

The structure of social animal groups can be dynamic, characterized by high rates of group fission and fusion. Despite this, group composition is often well ordered by factors such as species, body size and by numerous other phenotypic traits. Research in shoaling fishes has revealed that individuals refine group membership decisions still further and are capable of assimilating chemical cues pertaining to recent habitat and prey use by prospective group mates, preferring to associate with others whose recent resource use history closely matches their own. In this study, we firstly examined the dynamics of the formation and breakdown of these preferences, revealing that they can be acquired and replaced in a matter of just a few hours. Using such cues enables individuals to accurately assess the resource use of conspecifics, allowing them to indirectly sample the local environment while reducing the chances of acquiring outdated information that can precipitate maladaptive behaviors. Secondly, we found that shoals composed of individuals with shared recent habitat use history were more cohesive compared to those where the constituent individuals differed in recent habitat use. Increased shoal cohesion may reduce predation risk, and could enhance the ability of individuals to detect and use social information.

Turbidity and foraging rate in threespine sticklebacks: The importance of visual and chemical prey cues

In aquatic habitats turbidity can affect the foraging efficiency of visual predators, directly influencing their capacity to detect prey. In a laboratory study we tested the effect of different loads of suspended sediment upon the foraging rates of threespine sticklebacks (Gasterosteus aculeatus). We compared the foraging rates of fish under a series of different turbidity treatments, testing fish originating from four habitats within a single drainage basin that differed in a number of environmental parameters including turbidity. Although we found habitat specific differences in foraging rates, these did not correspond to local turbidity levels. The findings of a follow up experiment revealed habitat-specific variation in boldness, which may be indirecly linked to the observed differences in foraging rate. The main finding of our study was that turbidity alone had no impact upon their prey capture rates, but that high turbidity in combination with saturation with prey odour extract caused prey capture rates to fall significantly. This suggests that olfactory cues can be more important than visual cues in determining foraging performance in this species, potentially influencing how they cope with naturally occurring periods of turbidity, and how they adapt to human-induced eutrophication.

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 animals 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.