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Disturbance cues facilitate associative learning of predators in a coral reef fish

Abstract

Aquatic prey can gauge predation risk using chemical information, including chemical alarm cues — released when prey are injured, disturbance cues — released when prey are threatened, or the odour of the predator itself. While a lot of work has focused on alarm cues, disturbance cues remained poorly studied in freshwater systems, and has been virtually omitted in marine ones. In the current study, we document the first evidence of disturbance cue use in a marine fish. Juvenile damselfish Pomacentrus nagasakiensis were exposed to cues from undisturbed or disturbed conspecifics, a water control (negative control) and conspecific alarm cues (positive control). Juveniles displayed increased antipredator responses when exposed to alarm cues and disturbed conspecifics, but not when exposed to undisturbed ones. In addition, we demonstrated that disturbance cues, just like alarm cues, could mediate learned predator recognition, a phenomenon undemonstrated in freshwater fishes. Given disturbance cues are thought to be comprised of nitrogenous waste, it has been hypothesised that the constant and dilute release of such products in the hypotonic freshwater environment results in a high level of ‘background chemical’ noise masking subsequent releases. Extending this hypothesis, we propose that in the marine environment, disturbance cues are more easily detected due to low background noise.

Significance statement

Prey animals must accurately assess their current predation risk. Aquatic prey rely on chemical cues to gain information on risk. These cues can include odours released when nearby prey are damaged or disturbed, or the odour of a known predator. Prey exposed to a novel odour for the first time must learn if the odour is an indication of risk or benign. This is accomplished when the odour of a known risk (e.g. cues released from a damaged individual) is paired with a novel odour (e.g. a novel predator). In the current paper, we show for the first time that coral reef fishes can use disturbance cues (cues released when prey are chased or otherwise disturbed) as a ‘known risk’ and when paired with a novel odour, are subsequently able to respond to the novel odour when presented alone.

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Data availability

The datasets generated during and/or analysed during the current study are not publicly available but are uploaded as supplementary material.

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Acknowledgements

We thank the Lizard Island Research Station staff and our volunteers. Additionally, we thank the reviewers for improving the quality of the manuscript.

Funding

Research funds were provided by the Australian Research Council Centre of Excellence for Coral Reef Studies (EI140100117; MIM), an Australian Research Council Discovery Grant (DP 170103372; MIM, MCOF, DPC), and NSERC funding (MCOF, DPC).

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Correspondence to Michael S. Pollock.

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All research was conducted in accordance with the James Cook University (JCU) Animal Ethics guidelines with approval from the JCU Animal Ethics Committee (approval A2408).

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The authors declare no competing interests.

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Communicated by J. G. Frommen.

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Pollock, M.S., Hoyle, Z., Mccormick, M.I. et al. Disturbance cues facilitate associative learning of predators in a coral reef fish. Behav Ecol Sociobiol 75, 149 (2021). https://doi.org/10.1007/s00265-021-03088-z

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Keywords

  • Anti-predator behaviour
  • Chemical alarm cue
  • Disturbance cue
  • Predator–prey
  • Risk assessment