Both prey and predator features predict the individual predation risk and survival of schooling prey
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).
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Data for: Both Prey and Predator Features Determine Predation Risk and Survival of Schooling PreyMendeley, doi:10.17632/bszk9ztryp.1.
Article and author information
Author details
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.
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.
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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Further reading
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Prey must balance predator avoidance with feeding, a central dilemma in prey refuge theory. Additionally, prey must assess predatory imminence—how close threats are in space and time. Predatory imminence theory classifies defensive behaviors into three defense modes: pre-encounter, post-encounter, and circa-strike, corresponding to increasing levels of threat—–suspecting, detecting, and contacting a predator. Although predatory risk often varies in spatial distribution and imminence, how these factors intersect to influence defensive behaviors is poorly understood. Integrating these factors into a naturalistic environment enables comprehensive analysis of multiple defense modes in consistent conditions. Here, we combine prey refuge and predatory imminence theories to develop a model system of nematode defensive behaviors, with Caenorhabditis elegans as prey and Pristionchus pacificus as predator. In a foraging environment comprised of a food-rich, high-risk patch and a food-poor, low-risk refuge, C. elegans innately exhibits circa-strike behaviors. With experience, it learns post- and pre-encounter behaviors that proactively anticipate threats. These defense modes intensify with predator lethality, with only life-threatening predators capable of eliciting all three modes. SEB-3 receptors and NLP-49 peptides, key stress regulators, vary in their impact and interdependence across defense modes. Overall, our model system reveals fine-grained insights into how stress-related signaling regulates defensive behaviors.