1. Ecology

Both prey and predator features predict the individual predation risk and survival of schooling prey

  1. Jolle Wolter Jolles  Is a corresponding author
  2. Matthew MG Sosna
  3. Geoffrey PF Mazué
  4. Colin R Twomey
  5. Joseph Bak-Coleman
  6. Daniel I Rubenstein
  7. Iain D Couzin  Is a corresponding author
  1. Centre for Research on Ecology and Forestry Applications, Spain
  2. Princeton University, United States
  3. University of Sydney, Australia
  4. University of Pennsylvania, United States
  5. University of Washington, United States
  6. Max Planck Institute of Animal Behavior, Germany
https://doi.org/10.7554/eLife.76344
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Cite this article
  1. Jolle Wolter Jolles
  2. Matthew MG Sosna
  3. Geoffrey PF Mazué
  4. Colin R Twomey
  5. Joseph Bak-Coleman
  6. Daniel I Rubenstein
  7. Iain D Couzin
(2022)
Both prey and predator features predict the individual predation risk and survival of schooling prey
eLife 11:e76344.
https://doi.org/10.7554/eLife.76344
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Abstract

Predation is one of the main evolutionary drivers of social grouping. While it is well appreciated that predation risk is likely not shared equally among individuals within groups, its detailed quantification has remained difficult due to the speed of attacks and the highly-dynamic nature of collective prey response. Here, using high-resolution tracking of solitary predators (Northern pike) hunting schooling fish (golden shiners), we not only provide insights into predator decision-making, but show which key spatial and kinematic features of predator and prey predict the risk of individuals to be targeted and to survive attacks. We found that pike tended to stealthily approach the largest groups, and were often already inside the school when launching their attack, making prey in this frontal 'strike zone' the most vulnerable to be targeted. From the prey's perspective, those fish in central locations, but relatively far from, and less aligned with, neighbours, were most likely to be targeted. While the majority of attacks were successful (70%), targeted individuals that did manage to avoid being captured exhibited a higher maximum acceleration response just before the attack and were further away from the pike's head. Our results highlight the crucial interplay between predators' attack strategy and response of prey underlying the predation risk within mobile animal groups.

Data availability

Associated datasets are available on Mendeley Data (doi: 10.17632/bszk9ztryp.1).

The following data sets were generated

Article and author information

Author details

  1. Jolle Wolter Jolles

    Centre for Research on Ecology and Forestry Applications, Bellaterra, Spain
    For correspondence
    j.w.jolles@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9905-2633

  2. Matthew MG Sosna

    Department of Ecology and Evolutionary Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Geoffrey PF Mazué

    School of Life and Environmental Sciences, University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.

  4. Colin R Twomey

    Department of Biology, University of Pennsylvania, Pennsylvania, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Joseph Bak-Coleman

    eScience Institute, University of Washington, Washington, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Daniel I Rubenstein

    Department of Ecology and Evolutionary Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Iain D Couzin

    Department of Collective Behaviour, Max Planck Institute of Animal Behavior, Konstanz, Germany
    For correspondence
    icouzin@ab.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8556-4558

Funding

Alexander von Humboldt-Stiftung

  • Jolle Wolter Jolles

Ministerio de Ciencia e Innovación (CEX-2018-000828-S)

  • Jolle Wolter Jolles

National Science Foundation (1701289)

  • Matthew MG Sosna

Universität Konstanz

  • Jolle Wolter Jolles

John S. and James L. Knight Foundation

  • Joseph Bak-Coleman

Office of Naval Research Global (N00014-64019-1-2556)

  • Iain D Couzin

HORIZON EUROPE Marie Sklodowska-Curie Actions (860949)

  • Iain D Couzin

Deutsche Forschungsgemeinschaft (EXC 2117-422037984)

  • Iain D Couzin

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Jenny Tung, Duke University, United States

Ethics

Animal experimentation: This study was performed in strict accordance with the standards set forth by the ASAB/ABS Guidelines for the Treatment of Animals in Behavioural Research (2012) and the guidelines for predation experiments described by Huntingford (1984). Specifically, staged predation events, whereby live predators could interact freely with and consume their prey, were necessary to quantify normal predatory and anti-predator behaviour as well as individual fitness and thereby realise the novel objectives of our study, going beyond previous work using predator cues or models or with virtual prey. We thereby acquired highly detailed data of all attacks, something that would not have been possible in the wild and with the aim to get the maximum possible information from each trial (c.f. Huntingford, 1984). We were able to reduce the number of fish used in the experiments by conducting repeated exposures, combining biological (different groups) and technical (independent repeated measures) replicates. Although shiners may experience stress during the staged predation encounters, the testing conditions with a group size of 40 fish, which reflects the size of shiner shoals observed in the wild (Hall et al., 1979; Krause et al., 2000), and the large open tank, enable shiners to hide among others and escape attacks. All animal care and experimental procedures were approved by the institutional animal care and use committee (IACUC) protocols (#2068-16) of Princeton University.

Version history

  1. Preprint posted: December 14, 2021 (view preprint)
  2. Received: December 14, 2021
  3. Accepted: July 18, 2022
  4. Accepted Manuscript published: July 19, 2022 (version 1)
  5. Version of Record published: August 3, 2022 (version 2)

Copyright

© 2022, Jolles et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jolle Wolter Jolles
  2. Matthew MG Sosna
  3. Geoffrey PF Mazué
  4. Colin R Twomey
  5. Joseph Bak-Coleman
  6. Daniel I Rubenstein
  7. Iain D Couzin
(2022)
Both prey and predator features predict the individual predation risk and survival of schooling prey
eLife 11:e76344.
https://doi.org/10.7554/eLife.76344

Share this article

https://doi.org/10.7554/eLife.76344

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