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

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          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”.

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          Critical population density triggers rapid formation of vast oceanic fish shoals.

          Similarities in the behavior of diverse animal species that form large groups have motivated attempts to establish general principles governing animal group behavior. It has been difficult, however, to make quantitative measurements of the temporal and spatial behavior of extensive animal groups in the wild, such as bird flocks, fish shoals, and locust swarms. By quantifying the formation processes of vast oceanic fish shoals during spawning, we show that (i) a rapid transition from disordered to highly synchronized behavior occurs as population density reaches a critical value; (ii) organized group migration occurs after this transition; and (iii) small sets of leaders significantly influence the actions of much larger groups. Each of these findings confirms general theoretical predictions believed to apply in nature irrespective of animal species.
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            Fish population and behavior revealed by instantaneous continental shelf-scale imaging.

            Until now, continental shelf environments have been monitored with highly localized line-transect methods from slow-moving research vessels. These methods significantly undersample fish populations in time and space, leaving an incomplete and ambiguous record of abundance and behavior. We show that fish populations in continental shelf environments can be instantaneously imaged over thousands of square kilometers and continuously monitored by a remote sensing technique in which the ocean acts as an acoustic waveguide. The technique has revealed the instantaneous horizontal structural characteristics and volatile short-term behavior of very large fish shoals, containing tens of millions of fish and stretching for many kilometers.
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              Behavioral responses of herring (Clupea harengus) to 1-2 and 6-7 kHz sonar signals and killer whale feeding sounds.

              Military antisubmarine sonars produce intense sounds within the hearing range of most clupeid fish. The behavioral reactions of overwintering herring (Clupea harengus) to sonar signals of two different frequency ranges (1-2 and 6-7 kHz), and to playback of killer whale feeding sounds, were tested in controlled exposure experiments in Vestfjorden, Norway, November 2006. The behavior of free ranging herring was monitored by two upward-looking echosounders. A vessel towing an operational naval sonar source approached and passed over one of them in a block design setup. No significant escape reactions, either vertically or horizontally, were detected in response to sonar transmissions. Killer whale feeding sounds induced vertical and horizontal movements of herring. The results indicate that neither transmission of 1-2 kHz nor 6-7 kHz have significant negative influence on herring on the received sound pressure level tested (127-197 and 139-209 dB(rms) re 1 microPa, respectively). Military sonars of such frequencies and source levels may thus be operated in areas of overwintering herring without substantially affecting herring behavior or herring fishery. The avoidance during playback of killer whale sounds demonstrates the nature of an avoidance reaction and the ability of the experimental design to reveal it.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                29 January 2014
                : 9
                : 1
                : e86726
                Affiliations
                [1 ]Institute of Marine Research, Bergen, Norway
                [2 ]Florida International University, Biscayne Bay Campus, Marine Sciences Building, North Miami, Florida, United States of America
                [3 ]National Marine Fisheries Service, Alaska Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, Washington, United States of America
                University of Plymouth, United Kingdom
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GR KB ADR GJM NOH. Performed the experiments: GR KB ADR GJM NOH. Analyzed the data: GR KB ADR GJM NOH. Contributed reagents/materials/analysis tools: GR KB ADR GJM NOH. Wrote the paper: GR KB ADR GJM NOH.

                Article
                PONE-D-13-23526
                10.1371/journal.pone.0086726
                3906054
                2570f1c8-d726-41ec-96b7-83bb2150dfaf
                Copyright @ 2014

                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 5 June 2013
                : 16 December 2013
                Page count
                Pages: 9
                Funding
                This work was financed by the Norwegian Research Council (grant 204229/F20). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Community Ecology
                Species Interactions
                Ecological Environments
                Marine Environments
                Behavioral Ecology
                Marine Biology
                Fisheries Science
                Marine Ecology
                Population Biology
                Population Dynamics
                Predator-Prey Dynamics
                Zoology
                Ichthyology

                Uncategorized
                Uncategorized

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