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Disturbance cues function as a background risk cue but not as an associative learning cue in tadpoles

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Abstract

Chemical information has an important role in the sensory ecology of aquatic species. For aquatic prey, chemical cues are a vital source of information related to predator avoidance and risk assessment. For instance, alarm cues are released by prey that have been injured by predators. In addition to providing accurate information about current risk, repeated exposure to alarm cues can elicit a fear response to novel stimuli (neophobia) in prey. Another source of chemical information is disturbance cues, released by prey that have been disturbed or harassed (but not injured) by a predator. While disturbance cues have received much less attention than alarm cues, they appear to be useful as an early warning signal of predation risk and have the potential to be used as a priming cue for learning. In this study, we used wood frog (Lithobates sylvaticus) tadpoles to test whether repeated exposure to disturbance cues during the embryonic stage can induce neophobic behaviour. Three weeks following repeated exposure to disturbance cues, tadpoles showed reduced activity when exposed to a novel odour, but they no longer displayed an antipredator response to disturbance cues. In a second experiment, we found that tadpoles failed to learn that a novel odour was dangerous following a pairing with disturbance cues, whereas alarm cues facilitated such learning. Our results add to the growing body of information about disturbance cues and provide evidence of their function as an embryonic risk cue but not as an associative learning cue.

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All data from this study are included as supplementary information.

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Funding

Funding for this work was provided by the Natural Sciences and Engineering Research Council of Canada and the Mexican National Council for Science and Technology (CONACYT; Grant number: 452400).

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Authors and Affiliations

  1. Department of Biology, University of Saskatchewan, Saskatoon, SK, Canada

    Ita A. E. Rivera-Hernández & Adam L. Crane

  2. Instituto de Neuroetología, Universidad Veracruzana, VER, Xalapa-Enríquez, Mexico

    Ita A. E. Rivera-Hernández

  3. Department of Biology, Concordia University, Montreal, QC, Canada

    Adam L. Crane

  4. Biomedical Sciences, WCVM, University of Saskatchewan, Saskatoon, SK, Canada

    Michael S. Pollock & Maud C. O. Ferrari

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  1. Ita A. E. Rivera-Hernández
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  2. Adam L. Crane
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  4. Maud C. O. Ferrari
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Contributions

IAERH, ALC, and MCOF designed the study. IAERH and ALC conducted the experiments and analyzed the data. All authors contributed to writing the manuscript, have approved it for publication and agree to be held accountable for its content.

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Correspondence to Ita A. E. Rivera-Hernández.

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The field collection of the wood frog egg clutches was approved by the Saskatchewan Ministry of Environment (Scientific Research Permit #18FW071). This study was conducted at the University of Saskatchewan and was approved by the University’s Animal Research Ethics Board (protocol #20060014).

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Rivera-Hernández, I.A.E., Crane, A.L., Pollock, M.S. et al. Disturbance cues function as a background risk cue but not as an associative learning cue in tadpoles. Anim Cogn 25, 881–889 (2022). https://doi.org/10.1007/s10071-022-01599-4

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