The scent of fear makes sea urchins go ballistic

Abstract 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 tri...

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Main Authors: Jordi F. Pagès, Frederic Bartumeus, Javier Romero, Teresa Alcoverro
Format: Article
Language:English
Published: BMC 2021-10-01
Series:Movement Ecology
Subjects:
Online Access:https://doi.org/10.1186/s40462-021-00287-1
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author Jordi F. Pagès
Frederic Bartumeus
Javier Romero
Teresa Alcoverro
author_facet Jordi F. Pagès
Frederic Bartumeus
Javier Romero
Teresa Alcoverro
author_sort Jordi F. Pagès
collection DOAJ
description Abstract 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.
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spelling doaj.art-a4e750553ba14109a2079476dab804882022-12-21T21:47:51ZengBMCMovement Ecology2051-39332021-10-019111210.1186/s40462-021-00287-1The scent of fear makes sea urchins go ballisticJordi F. Pagès0Frederic Bartumeus1Javier Romero2Teresa Alcoverro3Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Universitat de BarcelonaCentre d’Estudis Avançats de Blanes (CEAB-CSIC)Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Universitat de BarcelonaCentre d’Estudis Avançats de Blanes (CEAB-CSIC)Abstract 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.https://doi.org/10.1186/s40462-021-00287-1Animal movementChemical cueEscape responseFearPredator–prey
spellingShingle Jordi F. Pagès
Frederic Bartumeus
Javier Romero
Teresa Alcoverro
The scent of fear makes sea urchins go ballistic
Movement Ecology
Animal movement
Chemical cue
Escape response
Fear
Predator–prey
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 Animal movement
Chemical cue
Escape response
Fear
Predator–prey
url https://doi.org/10.1186/s40462-021-00287-1
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