Revealing the hidden networks of interaction in mobile animal groups allows prediction of complex behavioral contagion

Abstract

Coordination among social animals requires rapid and efficient transfer of information among individuals, which may depend crucially on the underlying structure of the communication network. Establishing the decision-making circuits and networks that give rise to individual behavior has been a central goal of neuroscience. However, the analogous problem of determining the structure of the communication network among organisms that gives rise to coordinated collective behavior, such as is exhibited by schooling fish and flocking birds, has remained almost entirely neglected. Here, we study collective evasion maneuvers, manifested through rapid waves, or cascades, of behavioral change (a ubiquitous behavior among taxa) in schooling fish (Notemigonus crysoleucas). We automatically track the positions and body postures, calculate visual fields of all individuals in schools of ∼150 fish, and determine the functional mapping between socially generated sensory input and motor response during collective evasion. We find that individuals use simple, robust measures to assess behavioral changes in neighbors, and that the resulting networks by which behavior propagates throughout groups are complex, being weighted, directed, and heterogeneous. By studying these interaction networks, we reveal the (complex, fractional) nature of social contagion and establish that individuals with relatively few, but strongly connected, neighbors are both most socially influential and most susceptible to social influence. Furthermore, we demonstrate that we can predict complex cascades of behavioral change at their moment of initiation, before they actually occur. Consequently, despite the intrinsic stochasticity of individual behavior, establishing the hidden communication networks in large self-organized groups facilitates a quantitative understanding of behavioral contagion.T he social transmission of behavioral change is central to collective animal behavior. For many mobile groups, such as schooling fish and flocking birds, social contagion can be fast, resulting in dramatic waves of response (1-6). Such waves are evident in particular when individuals are under threat of attack from predators (1). Despite the ubiquity and importance of behavioral contagion, and the fact that survival depends on how individual interactions scale to collective properties (2), we still know very little about the sensory basis and mechanism of such coordinated collective response.In the early 20th century, Edmund Selous proposed that rapid waves of turning in large flocks of birds resulted from a direct transference of thoughts among animals: "They must think collectively, all at the same time. . . a flash out of so many brains" (3). By the mid-1950s, however, attention had turned from telepathy to synchrony arising from the rapid transmission of local behavioral response to neighbors, with some of the first experimental studies of cascading behavioral change undertaken by Dimitrii Radakov (4). Radakov (4) hand-traced the paths of each fish, frame-by-fram...

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