Disentangling and modeling interactions in fish with burst-and-coast swimming reveal distinct alignment and attraction behaviors.

Daniel S Calovi,Hugues Chaté,Valentin Lecheval,Alfonso Pérez Escudero,Alexandra Litchinko,Ugo Lopez,Guy Theraulaz,Andrea Cavagna,Clément Sire

doi:10.1371/journal.pcbi.1005933

Abstract

The development of tracking methods for automatically quantifying individual behavior and social interactions in animal groups has open up new perspectives for building quantitative and predictive models of collective behavior. In this work, we combine extensive data analyses with a modeling approach to measure, disentangle, and reconstruct the actual functional form of interactions involved in the coordination of swimming in Rummy-nose tetra (Hemigrammus rhodostomus). This species of fish performs burst-and-coast swimming behavior that consists of sudden heading changes combined with brief accelerations followed by quasi-passive, straight decelerations. We quantify the spontaneous stochastic behavior of a fish and the interactions that govern wall avoidance and the reaction to a neighboring fish, the latter by exploiting general symmetry constraints for the interactions. In contrast with previous experimental works, we find that both attraction and alignment behaviors control the reaction of fish to a neighbor. We then exploit these results to build a model of spontaneous burst-and-coast swimming and interactions of fish, with all parameters being estimated or directly measured from experiments. This model quantitatively reproduces the key features of the motion and spatial distributions observed in experiments with a single fish and with two fish. This demonstrates the power of our method that exploits large amounts of data for disentangling and fully characterizing the interactions that govern collective behaviors in animals groups.

Highlights

The study of physical or living self-propelled particles—active matter—has certainly become a booming field, notably involving biologists and physicists, often working together
Quantify, and model the interactions involved in the control and coordination of burst-and-coast swimming in the fish Hemigrammus rhodostomus
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Summary

Introduction

The study of physical or living self-propelled particles—active matter—has certainly become a booming field, notably involving biologists and physicists, often working together. Physical examples of active matter include self-propelled Janus colloids [1,2,3,4,5,6,7,8], vibrated granular matter [9,10,11], or self-propulsion mediated by hydrodynamical effects [12, 13], whereas biological examples are obviously ubiquitous: bacteria, cells, fish, humans, and speaking, most animals. A fish or a pedestrian wishing to avoid a physical obstacle or another individual will modify its intrinsic velocity in order to never touch it. In some species of fish, individuals tend to explicitly align their heading to that of their neighbors

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Discussion

Conclusion