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The scent of fear makes sea urchins go ballistic

BACKGROUND: Classic ecological formulations of predator–prey interactions often assume that predators and prey interact randomly in an information-limited environment. In the field, however, most prey can accurately assess predation risk by sensing predator chemical cues, which typically trigger som...

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Autores principales: Pagès, Jordi F., Bartumeus, Frederic, Romero, Javier, Alcoverro, Teresa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8502380/
https://www.ncbi.nlm.nih.gov/pubmed/34627405
http://dx.doi.org/10.1186/s40462-021-00287-1
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author Pagès, Jordi F.
Bartumeus, Frederic
Romero, Javier
Alcoverro, Teresa
author_facet Pagès, Jordi F.
Bartumeus, Frederic
Romero, Javier
Alcoverro, Teresa
author_sort Pagès, Jordi F.
collection PubMed
description BACKGROUND: Classic ecological formulations of predator–prey interactions often assume that predators and prey interact randomly in an information-limited environment. In the field, however, most prey can accurately assess predation risk by sensing predator chemical cues, which typically trigger some form of escape response to reduce the probability of capture. Here, we explore under laboratory-controlled conditions the long-term (minutes to hours) escaping response of the sea urchin Paracentrotus lividus, a key species in Mediterranean subtidal macrophyte communities. METHODS: Behavioural experiments involved exposing a random sample of P. lividus to either one of two treatments: (i) control water (filtered seawater) or (ii) predator-conditioned water (with cues from the main P. lividus benthic predator—the gastropod Hexaplex trunculus). We analysed individual sea urchin trajectories, computed their heading angles, speed, path straightness, diffusive properties, and directional entropy (as a measure of path unpredictability). To account for the full picture of escaping strategies, we followed not only the first instants post-predator exposure, but also the entire escape trajectory. We then used linear models to compare the observed results from control and predators treatments. RESULTS: The trajectories from sea urchins subjected to predator cues were, on average, straighter and faster than those coming from controls, which translated into differences in the diffusive properties and unpredictability of their movement patterns. Sea urchins in control trials showed complex diffusive properties in an information-limited environment, with highly variable trajectories, ranging from Brownian motion to superdiffusion, and even marginal ballistic motion. In predator cue treatments, variability reduced, and trajectories became more homogeneous and predictable at the edge of ballistic motion. CONCLUSIONS: Despite their old evolutionary origin, lack of cephalization, and homogenous external appearance, the trajectories that sea urchins displayed in information-limited environments were complex and ranged widely between individuals. Such variable behavioural repertoire appeared to be intrinsic to the species and emerged when the animals were left unconstrained. Our results highlight that fear from predators can be an important driver of sea urchin movement patterns. All in all, the observation of anomalous diffusion, highly variable trajectories and the behavioural shift induced by predator cues, further highlight that the functional forms currently used in classical predator–prey models are far from realistic. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40462-021-00287-1.
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spelling pubmed-85023802021-10-20 The scent of fear makes sea urchins go ballistic Pagès, Jordi F. Bartumeus, Frederic Romero, Javier Alcoverro, Teresa Mov Ecol Research BACKGROUND: Classic ecological formulations of predator–prey interactions often assume that predators and prey interact randomly in an information-limited environment. In the field, however, most prey can accurately assess predation risk by sensing predator chemical cues, which typically trigger some form of escape response to reduce the probability of capture. Here, we explore under laboratory-controlled conditions the long-term (minutes to hours) escaping response of the sea urchin Paracentrotus lividus, a key species in Mediterranean subtidal macrophyte communities. METHODS: Behavioural experiments involved exposing a random sample of P. lividus to either one of two treatments: (i) control water (filtered seawater) or (ii) predator-conditioned water (with cues from the main P. lividus benthic predator—the gastropod Hexaplex trunculus). We analysed individual sea urchin trajectories, computed their heading angles, speed, path straightness, diffusive properties, and directional entropy (as a measure of path unpredictability). To account for the full picture of escaping strategies, we followed not only the first instants post-predator exposure, but also the entire escape trajectory. We then used linear models to compare the observed results from control and predators treatments. RESULTS: The trajectories from sea urchins subjected to predator cues were, on average, straighter and faster than those coming from controls, which translated into differences in the diffusive properties and unpredictability of their movement patterns. Sea urchins in control trials showed complex diffusive properties in an information-limited environment, with highly variable trajectories, ranging from Brownian motion to superdiffusion, and even marginal ballistic motion. In predator cue treatments, variability reduced, and trajectories became more homogeneous and predictable at the edge of ballistic motion. CONCLUSIONS: Despite their old evolutionary origin, lack of cephalization, and homogenous external appearance, the trajectories that sea urchins displayed in information-limited environments were complex and ranged widely between individuals. Such variable behavioural repertoire appeared to be intrinsic to the species and emerged when the animals were left unconstrained. Our results highlight that fear from predators can be an important driver of sea urchin movement patterns. All in all, the observation of anomalous diffusion, highly variable trajectories and the behavioural shift induced by predator cues, further highlight that the functional forms currently used in classical predator–prey models are far from realistic. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40462-021-00287-1. BioMed Central 2021-10-09 /pmc/articles/PMC8502380/ /pubmed/34627405 http://dx.doi.org/10.1186/s40462-021-00287-1 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Pagès, Jordi F.
Bartumeus, Frederic
Romero, Javier
Alcoverro, Teresa
The scent of fear makes sea urchins go ballistic
title The scent of fear makes sea urchins go ballistic
title_full The scent of fear makes sea urchins go ballistic
title_fullStr The scent of fear makes sea urchins go ballistic
title_full_unstemmed The scent of fear makes sea urchins go ballistic
title_short The scent of fear makes sea urchins go ballistic
title_sort scent of fear makes sea urchins go ballistic
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8502380/
https://www.ncbi.nlm.nih.gov/pubmed/34627405
http://dx.doi.org/10.1186/s40462-021-00287-1
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