Experimental Evidence of Threat-Sensitive Collective Avoidance Responses in a Large Wild-Caught Herring School

Guillaume Rieucau,Nils Olav Handegard,Kevin M Boswell,Gavin J Macaulay,Alex De Robertis,Mark Briffa

doi:10.1371/journal.pone.0086726

Abstract

Aggregation is commonly thought to improve animals' security. Within aquatic ecosystems, group-living prey can learn about immediate threats using cues perceived directly from predators, or from collective behaviours, for example, by reacting to the escape behaviours of companions. Combining cues from different modalities may improve the accuracy of prey antipredatory decisions. In this study, we explored the sensory modalities that mediate collective antipredatory responses of herring (Clupea harengus) when in a large school (approximately 60 000 individuals). By conducting a simulated predator encounter experiment in a semi-controlled environment (a sea cage), we tested the hypothesis that the collective responses of herring are threat-sensitive. We investigated whether cues from potential threats obtained visually or from the perception of water displacement, used independently or in an additive way, affected the strength of the collective avoidance reactions. We modified the sensory nature of the simulated threat by exposing the herring to 4 predator models differing in shape and transparency. The collective vertical avoidance response was observed and quantified using active acoustics. The combination of sensory cues elicited the strongest avoidance reactions, suggesting that collective antipredator responses in herring are mediated by the sensory modalities involved during threat detection in an additive fashion. Thus, this study provides evidence for magnitude-graded threat responses in a large school of wild-caught herring which is consistent with the “threat-sensitive hypothesis”.

Highlights

Schooling behaviour has been considered primarily as an adaptation that confers security advantages to gregarious fishes [1,2,3] through the action of several mechanisms such as a greater power of predator detection [4,5], the numerical dilution of risk and abatement effect [1], predator confusion [6,7] or coordinated evasive manoeuvres [1,8]
Schooling fish can learn about immediate threats using visual [10,11], chemical [12,13] acoustical or hydraulic cues, sensed by the mechanoreceptors located in the lateral line system, that emanate from the predator’s swimming movement [14,15] or indirectly from the sensory information produced by the avoidance behaviour of risk-aware school members [16,17]
Our results show that herring collective antipredator responses are mediated by the sensory modalities involved during threat detection

Summary

Introduction

Schooling behaviour has been considered primarily as an adaptation that confers security advantages to gregarious fishes [1,2,3] through the action of several mechanisms such as a greater power of predator detection [4,5], the numerical dilution of risk and abatement effect [1], predator confusion [6,7] or coordinated evasive manoeuvres [1,8]. Schooling fish can learn about immediate threats using visual [10,11], chemical [12,13] acoustical or hydraulic cues, sensed by the mechanoreceptors located in the lateral line system, that emanate from the predator’s swimming movement [14,15] or indirectly from the sensory information produced by the avoidance behaviour of risk-aware school members [16,17]. Several mechanisms have been proposed to explain an efficient transmission of undamped information within schools: waves of agitation [19,20,21], fast pressure pulses emitted by startled fish [22], and compressional density waves that can occur over very large distances, e.g. 10’s to 100’s of km [21,23]

Methods

Results

Conclusion