Ashley J. W. Ward

Quorum decision-making facilitates information transfer in fish shoals

Despite the growing interest in collective phenomena such as “swarm intelligence” and “wisdom of the crowds,” little is known about the mechanisms underlying decision-making in vertebrate animal groups. How do animals use the behavior of others to make more accurate decisions, especially when it is not possible to identify which individuals possess pertinent information? One plausible answer is that individuals respond only when they see a threshold number of individuals perform a particular behavior. Here, we investigate the role of such “quorum responses” in the movement decisions of fish (three-spine stickleback, Gasterosteus aculeatus). We show that a quorum response to conspecifics can explain how sticklebacks make collective movement decisions, both in the absence and presence of a potential predation risk. Importantly our experimental work shows that a quorum response can reduce the likelihood of amplification of nonadaptive following behavior. Whereas the traveling direction of solitary fish was strongly influenced by a single replica conspecific, the replica was largely ignored by larger groups of four or eight sticklebacks under risk, and the addition of a second replica was required to exert influence on the movement decisions of such groups. Model simulations further predict that quorum responses by fish improve the accuracy and speed of their decision-making over that of independent decision-makers or those using a weak linear response. This study shows that effective and accurate information transfer in groups may be gained only through nonlinear responses of group members to each other, thus highlighting the importance of quorum decision-making.

Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus)

Behavioural variation is known to occur between individuals of the same population competing for resources. Individuals also vary with respect to their boldness or shyness. An individual’s position along the shy-bold axis may be defined as the extent to which it is willing to trade off potentially increased predation risks for possible gains in resources. Similarly, group living may be interpreted as a trade-off between anti-predatory tactics and foraging efficiency. The responses of three-spined sticklebacks (Gasterosteus aculeatus) were tested across four social contexts to assess relative boldness or shyness and to further examine whether their behaviour would be consistent within and between contexts. Individuals displayed consistent responses within and between the first two contexts: those individuals which resumed foraging rapidly after a simulated aerial predator attack also displayed low shoaling tendencies. Such fish were deemed to be bold, whilst those which displayed the converse behaviour, slow resumption of foraging and a high shoaling tendency, were deemed to be shy. In a third context, bold individuals out-competed shy conspecifics for food. Boldness was also positively correlated with growth over a 6-week period. The position adopted by an individual within a group is usually interpreted as a trade-off between predation risk and foraging efficiency—both are greater at the front of a mobile group. Bold individuals showed significantly stronger tendencies towards front positions than shy conspecifics. The results suggest that, contrary to some previous studies on other animals, bold or shy behaviour in sticklebacks is consistent between contexts.

Inferring the rules of interaction of shoaling fish

Collective motion, where large numbers of individuals move synchronously together, is achieved when individuals adopt interaction rules that determine how they respond to their neighbors’ movements and positions. These rules determine how group-living animals move, make decisions, and transmit information between individuals. Nonetheless, few studies have explicitly determined these interaction rules in moving groups, and very little is known about the interaction rules of fish. Here, we identify three key rules for the social interactions of mosquitofish (Gambusia holbrooki): (i) Attraction forces are important in maintaining group cohesion, while we find only weak evidence that fish align with their neighbor’s orientation; (ii) repulsion is mediated principally by changes in speed; (iii) although the positions and directions of all shoal members are highly correlated, individuals only respond to their single nearest neighbor. The last two of these rules are different from the classical models of collective animal motion, raising new questions about how fish and other animals self-organize on the move.

Assortative interactions and social networks in fish

The mechanisms underpinning the structure of social networks in multiple fish populations were investigated. To our knowledge this is the first study to provide replication of social networks and therefore probably the first that allows general conclusions to be drawn. The social networks were all found to have a non-random structure and exhibited ‘social cliquishness’. A number of factors were observed to contribute to this structuring. Firstly, social network structure was influenced by body length and shoaling tendency, with individuals interacting more frequently with conspecifics of similar body length and shoaling tendency. Secondly, individuals with many social contacts were found to interact with each other more often than with other conspecifics, a phenomenon known as a ‘positive degree correlation’. Finally, repeated interactions between pairs of individuals occurred within the networks more often than expected by random interactions. The observed network structures will have ecological and evolutionary implications. For example, the occurrence of positive degree correlations suggests the possibility that pathogens and information (that are socially transmitted) could spread very fast within the populations. Furthermore, the occurrence of repeated interactions between pairs of individuals fulfils an important pre-requisite for the evolution of reciprocal altruism.

Fast and accurate decisions through collective vigilance in fish shoals

Although it has been suggested that large animal groups should make better decisions than smaller groups, there are few empirical demonstrations of this phenomenon and still fewer explanations of the how these improvements may be made. Here we show that both speed and accuracy of decision making increase with group size in fish shoals under predation threat. We examined two plausible mechanisms for this improvement: first, that groups are guided by a small proportion of high-quality decision makers and, second, that group members use self-organized division of vigilance. Repeated testing of individuals showed no evidence of different decision-making abilities between individual fish. Instead, we suggest that shoals achieve greater decision-making efficiencies through division of labor combined with social information transfer. Our results should prompt reconsideration of how we view cooperation in animal groups with fluid membership.

Consensus Decision Making by Fish

Decisions reached through consensus are often more accurate, because they efficiently utilize the diverse information possessed by group members [1-3]. A trust in consensus decision making underlies many of our democratic political and judicial institutions [4], as well as the design of web tools such as Google, Wikipedia, and prediction markets [5, 6]. In theory, consensus for the option favored by the majority of group members will lead to improved decision-making accuracy as group size increases [2, 4]. Although group-living animals are known to utilize social information [7-10], little is known about whether or not decision accuracy increases with group size. In order to reach consensus, group members must be able to integrate the disparate information they possess. Positive feedback, resulting from copying others, can spread information quickly through the group, but it can also result in all individuals making the same, possibly incorrect, choice [8, 11, 12]. On the other hand, if individuals never copy each other, their decision making remains independent and they fail to benefit from information exchange [4]. Here, we show how small groups of sticklebacks (Gasterosteus aculeatus) reach consensus when choosing which of two replica fish to follow. As group size increases, the fish make more accurate decisions, becoming better at discriminating subtle phenotypic differences of the replicas. A simple quorum rule proves sufficient to explain our observations, suggesting that animals can make accurate decisions without the need for complicated comparison of the information they possess. Furthermore, although submission to peers can lead to occasional cascades of incorrect decisions, these can be explained as a byproduct of what is usually accurate consensus decision making.

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.

Fish shoal composition: mechanisms and constraints

Observations were made on three fish species (banded killifish (Fundulus diaphanus), golden shiner (Notemigonus crysoleucas) and white sucker (Catostomus commersoni)) in a temperate lake (New Brunswick, Canada) in order to investigate the relationship between shoal choice behaviour of individual fishes and shoal composition. Encounters between shoals were observed to take place every 1.1 min per shoal and an encounter lasted 3.7s on average. The duration of shoal encounters was influenced by shoal size but not by differences between shoals in either body length or species. Conversely, the outcome of shoal encounters (i.e. whether or not an individual changes shoal) was influenced by body length and species differences but not by shoal size. Together, these results suggest that encounter duration itself is unlikely to have an important influence on encounter outcome. The collection of ten entire fish shoals showed that they were assorted by species and body length. A simulation model demonstrated that individual shoal choice behaviour alone could account for the generation and maintenance of the observed levels of size assortedness of shoals without invoking the existence of other sorting mechanisms such as differential swimming speeds. However, the generation of species assortedness was not predicted by the model. Furthermore, our data suggest that fish density acts as a constraint on shoal choice, influencing both shoal size and composition. This work has implications for studies on information transfer and reciprocal altruism within populations.

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.

Association patterns and shoal fidelity in the three-spined stickleback

We investigated pairwise association patterns and shoal fidelity in free–ranging, individual three–spine sticklebacks (Gasterosteus aculeatus) by capturing entire shoals of sticklebacks and tagging each shoal member with a unique individual mark before releasing the shoal at the point of capture. We recaptured tagged fishes in the study area on five subsequent days, noting their identity, their location and the individuals with which they were associated. Stable partner associations between fishes were observed which might provide the basis for shoal fidelity via social networks. These results suggest the potential for the kinds of inter–individual association patterns assumed by models of predator inspection and ‘tit–for–tat’ behaviours in free–ranging fishes.