Consistent Individual Differences Drive Collective Behavior and Group Functioning of Schooling Fish

Jolle W Jolles,Neeltje J Boogert,Vivek H Sridhar,Iain D Couzin,Andrea Manica

doi:10.1016/j.cub.2017.08.004

Abstract

SummaryThe ubiquity of consistent inter-individual differences in behavior (“animal personalities”) [1, 2] suggests that they might play a fundamental role in driving the movements and functioning of animal groups [3, 4], including their collective decision-making, foraging performance, and predator avoidance. Despite increasing evidence that highlights their importance [5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16], we still lack a unified mechanistic framework to explain and to predict how consistent inter-individual differences may drive collective behavior. Here we investigate how the structure, leadership, movement dynamics, and foraging performance of groups can emerge from inter-individual differences by high-resolution tracking of known behavioral types in free-swimming stickleback (Gasterosteus aculeatus) shoals. We show that individual’s propensity to stay near others, measured by a classic “sociability” assay, was negatively linked to swim speed across a range of contexts, and predicted spatial positioning and leadership within groups as well as differences in structure and movement dynamics between groups. In turn, this trait, together with individual’s exploratory tendency, measured by a classic “boldness” assay, explained individual and group foraging performance. These effects of consistent individual differences on group-level states emerged naturally from a generic model of self-organizing groups composed of individuals differing in speed and goal-orientedness. Our study provides experimental and theoretical evidence for a simple mechanism to explain the emergence of collective behavior from consistent individual differences, including variation in the structure, leadership, movement dynamics, and functional capabilities of groups, across social and ecological scales. In addition, we demonstrate individual performance is conditional on group composition, indicating how social selection may drive behavioral differentiation between individuals.

Highlights

We first determined the behavioral tendencies of 125 fish by exposing them to two classic personality assays and tracking their movements
We found consistent individual differences in fish’s proximity to a confined shoal of conspecifics (RC = 0.58, 0.46–0.68), classically used to define ‘‘sociability’’ [30, 31], 2862 Current Biology 27, 2862–2868, September 25, 2017 a 2017 The Author(s)
Based on the detailed tracking data, we found that individual fish slowed down the closer they were to the confined shoal and that fish that consistently stayed closer to the shoal swam at consistently lower speeds. This was even the case when controlling for boundary effects (r123 = À0.79, p = 0.001) and when measured in the asocial boldness assay. These results show that a fundamental link exists between social proximity and speed and concord with the general observation that slowmoving individuals tend to form more cohesive groups [25]

Summary

Introduction

We first determined the behavioral tendencies of 125 fish by exposing them to two classic personality assays and tracking their movements (see Figure S1). We found consistent interindividual variation in fish’s tendency to leave a refuge and explore an open environment (repeatability RC = 0.48, 95% confidence intervals: 0.33–0.60). This exploratory tendency, which is traditionally referred to as ‘‘boldness’’ since it may increase potential predation risk [28], was positively linked to individuals’ food consumption even in the safety of the holding compartment [29], reflecting an intrinsic higher motivation for food. We found consistent individual differences in fish’s proximity to a confined shoal of conspecifics (RC = 0.58, 0.46–0.68), classically used to define ‘‘sociability’’ [30, 31]

Methods

Findings

Conclusion