Christos C. Ioannou

Collective States, Multistability and Transitional Behavior in Schooling Fish

The spontaneous emergence of pattern formation is ubiquitous in nature, often arising as a collective phenomenon from interactions among a large number of individual constituents or sub-systems. Understanding, and controlling, collective behavior is dependent on determining the low-level dynamical principles from which spatial and temporal patterns emerge; a key question is whether different group-level patterns result from all components of a system responding to the same external factor, individual components changing behavior but in a distributed self-organized way, or whether multiple collective states co-exist for the same individual behaviors. Using schooling fish (golden shiners, in groups of 30 to 300 fish) as a model system, we demonstrate that collective motion can be effectively mapped onto a set of order parameters describing the macroscopic group structure, revealing the existence of at least three dynamically-stable collective states; swarm, milling and polarized groups. Swarms are characterized by slow individual motion and a relatively dense, disordered structure. Increasing swim speed is associated with a transition to one of two locally-ordered states, milling or highly-mobile polarized groups. The stability of the discrete collective behaviors exhibited by a group depends on the number of group members. Transitions between states are influenced by both external (boundary-driven) and internal (changing motion of group members) factors. Whereas transitions between locally-disordered and locally-ordered group states are speed dependent, analysis of local and global properties of groups suggests that, congruent with theory, milling and polarized states co-exist in a bistable regime with transitions largely driven by perturbations. Our study allows us to relate theoretical and empirical understanding of animal group behavior and emphasizes dynamic changes in the structure of such groups.

The Dynamics of Coordinated Group Hunting and Collective Information Transfer among Schooling Prey

Predator-prey interactions are vital to the stability of many ecosystems. Yet, few studies have considered how they are mediated due to substantial challenges in quantifying behavior over appropriate temporal and spatial scales. Here, we employ high-resolution sonar imaging to track the motion and interactions among predatory fish and their schooling prey in a natural environment. In particular, we address the relationship between predator attack behavior and the capacity for prey to respond both directly and through collective propagation of changes in velocity by group members. To do so, we investigated a large number of attacks and estimated per capita risk during attack and its relation to the size, shape, and internal structure of prey groups. Predators were found to frequently form coordinated hunting groups, with up to five individuals attacking in line formation. Attacks were associated with increased fragmentation and irregularities in the spatial structure of prey groups, features that inhibit collective information transfer among prey. Prey group fragmentation, likely facilitated by predator line formation, increased (estimated) per capita risk of prey, provided prey schools were maintained below a threshold size of approximately 2 m(2). Our results highlight the importance of collective behavior to the strategies employed by both predators and prey under conditions of considerable informational constraints.

Predation risk as a driving force for sexual segregation: a cross-population comparison.

Sexual segregation is widespread throughout the animal kingdom. Although a number of hypotheses have been proposed to account for observed patterns, the generality of the mechanisms remains debated. One possible reason for this is the focus on segregation patterns in large mammals such as ungulates, where the majority of studies are descriptions of a single population. Here, we present the results of a cross‐population comparison of patterns of sexual segregation in the Trinidadian guppy, Poecilia reticulata. We relate observed patterns to experimental quantification of predation risk and sexual harassment of females by males in eight populations. We find that the degree of segregation increases with predation risk, with deeper waters becoming increasingly female biased. Furthermore, we observed that levels of male harassment are lower in deeper water but only in those rivers that contain major guppy predators. We conclude that sexual segregation in guppies is consistent with the predation risk hypothesis: sexual segregation results from a combination of predation risk driving males (the more vulnerable sex) into less risky habitats and females gaining benefits of reduced sexual harassment by remaining in high‐predation environments.

The Effect of Prey Density on Predators: Conspicuousness and Attack Success Are Sensitive to Spatial Scale

In contrast to the numerous studies that have examined the response of predators to prey group size, little is known about how prey density affects prey detection and the accuracy of attacks. We demonstrate that increasing the density of Daphnia magna swarms increases conspicuousness to a natural predator, the three‐spined stickleback. Denser areas of groups were more conspicuous, as the fish attacked prey in denser parts of the group than would be expected if they attacked the nearest prey upon entering the feeding chamber. The spatial error of attacks also increased with the density around the target; hence, different stages of predation (searching for vs. successfully attacking prey) seem to select for opposing responses to prey density. However, whereas the effect of density on target selection only occurred using a global measure of density (average interindividual distance), the effect on attack error was only significant using a local measure of density (Voronoi polygon area). We believe this effect of spatial scale reflects the reduction in the number of prey in the visual field of the predator as an attack progresses, providing a perceptual basis for the importance of spatial scale in density‐dependent processes.

Potential Leaders Trade Off Goal-Oriented and Socially Oriented Behavior in Mobile Animal Groups

Leadership is widespread across the animal kingdom. In self-organizing groups, such as fish schools, theoretical models predict that effective leaders need to balance goal-oriented motion, such as toward a known resource, with their tendency to be social. Increasing goal orientation is predicted to increase decision speed and accuracy, but it is also predicted to increase the risk of the group splitting. To test these key predictions, we trained fish (golden shiners, Notemigonus crysoleucas) to associate a spatial target with a food reward (“informed” individuals) before testing each singly with a group of eight untrained fish who were uninformed (“naive”) about the target. Informed fish that exhibited faster and straighter paths (indicative of greater goal orientation) were more likely to reach their preferred target and did so more quickly. However, such behavior was associated with a tendency to leave untrained fish behind and, therefore, with failure to transmit their preference to others. Either all or none of the untrained fish stayed with the trained fish in the majority of trials. Using a simple model of self-organized coordination and leadership in groups, we recreate these features of leadership observed experimentally, including the apparent consensus behavior among naive individuals. Effective leadership thus requires informed individuals to appropriately balance goal-oriented and socially oriented behavior.

Towards of a firmer explanation of large shoal formation, maintenance and collective reactions in marine fish

Avoiding predation is generally seen as the most common explanation for why animals aggregate. However, it remains questionable whether the existing theory provides a complete explanation of the functions of large shoals formation in marine fishes. Here, we consider how well the mechanisms commonly proposed to explain enhanced safety of group living prey explain fish shoals reaching very large sizes. By conceptually re-examining these mechanisms for large marine shoals, we find little support from either empirical studies or classical models. We address first the importance of reassessing the functional theory with predator-dependent models and the need to consider factors other than predation to explain massive fish shoals. Second, we argue that taking into account the interplay between ultimate benefits and proximate perspectives is a key step in understanding large fish shoals in marine ecosystems. Third, we present the growing body of evidence from field studies that identify shoal internal structure as an important feature for how large shoals can form, maintain and react as a coordinated unit to external stimuli. In particular, we consider a mechanistic basis of local rules of interaction for group formation and collective dynamic properties that can account for groups reaching very large sizes. Recent research in collective animal behaviour has shifted focus from the importance of global properties (group size) to local properties (local density and information transfer). In contrast to studies of fish shoals in the laboratory, the difficulty in measuring behaviour in large shoals in marine systems remains a major constraint to further work. Advances in acoustical observation have shown the greatest potential to provide data that can link proximate mechanisms in, and ultimate functions of, large marine fish shoals.

Consensus and experience trump leadership, suppressing individual personality during social foraging

A variety of mechanisms express and suppress individual behavioral tendencies during group decision-making in fish. Whether individual behavior in social settings correlates with behavior when individuals are alone is a fundamental question in collective behavior. However, evidence for whether behavior correlates across asocial and social settings is mixed, and no study has linked observed trends with underlying mechanisms. Consistent differences between individuals in boldness, which describes willingness to accept reward over risk, are likely to be under strong selection pressure. By testing three-spined sticklebacks (Gasterosteus aculeatus) in a risky foraging task alone and repeatedly in shoals, we demonstrate that the expression of boldness in groups is context-specific. Whereas personality is repeatable in a low-risk behavior (leaving a refuge), the collectively made consensus decision to then cross the arena outweighs leadership by bolder individuals, explaining the suppression of personality in this context. However, despite this social coordination, bolder individuals were still more likely to feed. Habituation and satiation over repeated trials degrade the effect of personality on leaving the refuge and also whether crossing the arena is a collective decision. The suppression of personality in groups suggests that individual risk-taking tendency may rarely represent actual risk in social settings, with implications for the evolution and ecology of personality variation.

The social context of cannibalism in migratory bands of the mormon cricket

Cannibalism has been shown to be important to the collective motion of mass migratory bands of insects, such as locusts and Mormon crickets. These mobile groups consist of millions of individuals and are highly destructive to vegetation. Individuals move in response to attacks from approaching conspecifics and bite those ahead, resulting in further movement and encounters with others. Despite the importance of cannibalism, the way in which individuals make attack decisions and how the social context affects these cannibalistic interactions is unknown. This can be understood by examining the decisions made by individuals in response to others. We performed a field investigation which shows that adult Mormon crickets were more likely to approach and attack a stationary cricket that was side-on to the flow than either head- or abdomen-on, suggesting that individuals could reduce their risk of an attack by aligning with neighbours. We found strong social effects on cannibalistic behaviour: encounters lasted longer, were more likely to result in an attack, and attacks were more likely to be successful if other individuals were present around a stationary individual. This local aggregation appears to be driven by positive feedback whereby the presence of individuals attracts others, which can lead to further crowding. This work improves our understanding of the local social dynamics driving migratory band formation, maintenance and movement at the population level.

Individuals that are consistent in risk-taking benefit during collective foraging

It is well established that living in groups helps animals avoid predation and locate resources, but maintaining a group requires collective coordination, which can be difficult when individuals differ from one another. Personality variation (consistent behavioural differences within a population) is already known to be important in group interactions. Growing evidence suggests that individuals also differ in their consistency, i.e. differing in how variable they are over time, and theoretical models predict that this consistency can be beneficial in social contexts. We used three-spined sticklebacks (Gasterosteus aculeatus) to test whether the consistency in, as well as average levels of, risk taking behaviour (i.e. boldness) when individuals were tested alone affects social interactions when fish were retested in groups of 2 and 4. Behavioural consistency, independently of average levels of risk-taking, can be advantageous: more consistent individuals showed higher rates of initiating group movements as leaders, more behavioural coordination by joining others as followers, and greater food consumption. Our results have implications for both group decision making, as groups composed of consistent individuals are more cohesive, and personality traits, as social interactions can have functional consequences for consistency in behaviour and hence the evolution of personality variation.

The anti-predator role of within-nest emergence synchrony in sea turtle hatchlings

Group formation is a common behaviour among prey species. In egg-laying animals, despite the various factors that promote intra-clutch variation leading to asynchronous hatching and emergence from nests, synchronous hatching and emergence occurs in many taxa. This synchrony may be adaptive by reducing predation risk, but few data are available in any natural system, even for iconic examples of the anti-predator function of group formation. Here, we show for the first time that increased group size (number of hatchlings emerging together from a nest) reduces green turtle (Chelonia mydas) hatchling predation. This effect was only observed earlier in the night when predation pressure was greatest, indicated by the greatest predator abundance and a small proportion of predators preoccupied with consuming captured prey. Further analysis revealed that the effect of time of day was due to the number of hatchlings already killed in an evening; this, along with the apparent lack of other anti-predatory mechanisms for grouping, suggests that synchronous emergence from a nest appears to swamp predators, resulting in an attack abatement effect. Using a system with relatively pristine conditions for turtle hatchlings and their predators provides a more realistic environmental context within which intra-nest synchronous emergence has evolved.