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Frog embryos use multiple levels of temporal pattern in risk assessment for vibration-cued escape hatching

Abstract

Stereotyped signals can be a fast, effective means of communicating danger, but animals assessing predation risk must often use more variable incidental cues. Red eyed-treefrog, Agalychnis callidryas, embryos hatch prematurely to escape from egg predators, cued by vibrations in attacks, but benign rain generates vibrations with overlapping properties. Facing high false-alarm costs, embryos use multiple vibration properties to inform hatching, including temporal pattern elements such as pulse durations and inter-pulse intervals. However, measures of snake and rain vibration as simple pulse-interval patterns are a poor match to embryo behavior. We used vibration playbacks to assess if embryos use a second level of temporal pattern, long gaps within a rhythmic pattern, as indicators of risks. Long vibration-free periods are common during snake attacks but absent from hard rain. Long gaps after a few initial vibrations increase the hatching response to a subsequent vibration series. Moreover, vibration patterns as short as three pulses, separated by long periods of silence, can induce as much hatching as rhythmic pulse series with five times more vibration. Embryos can retain information that increases hatching over at least 45 s of silence. This work highlights that embryo behavior is contextually modulated in complex ways. Identical vibration pulses, pulse groups, and periods of silence can be treated as risk cues in some contexts and not in others. Embryos employ a multi-faceted decision-making process to effectively distinguish between risk cues and benign stimuli.

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Data availability

The data generated during the current study are publicly available at Dryad (https://doi.org/10.5061/dryad.cnp5hqc4t).

Code availability

All code required to reproduce the analysis and figures shown here is available at https://github.com/drjuliejung/gaps.

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Acknowledgements

We thank Ana Ospina, Rachel Snyder, and Adeline Almanzar for assistance with egg collection and care in 2017, members of the Gamboa Frog Group for discussion of experiments in 2013 and 2017, and members of the Egg Science Research Group at Boston University for comments on the manuscript.

Funding

This research was funding by the Smithsonian Tropical Research Institute, the National Science Foundation (IOS-1354072 to KMW and JGM, CNS-1018266 and CNS-1117039 to MC), and Boston University.

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Authors and Affiliations

Authors

Contributions

Conceptualization: JJ, JGM, MG, MC and KMW. Methodology: JJ, JGM, MG, MC, and KMW. Software: JJ, MG, MC, and JGM. Validation: JJ, MG and KMW. Formal analysis: JJ. Investigation: JJ, MG. Resources: KMW. Data curation: JJ, MG. Writing—original draft: JJ. Writing—review and editing: JJ and KMW. Visualization: JJ. Supervision: KMW. Project administration: KMW. Funding acquisition: KMW, JGM and MC.

Corresponding author

Correspondence to Julie Jung.

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Conflict of interest

The authors declare that they have no conflict of interest that is relevant to the content of this article.

Ethics approval

This research was conducted under permits from the Panamanian Environmental Ministry (SC/A-11-13, SE/A-55-17) and approved by the Institutional Animal Care and Use Committee of the Smithsonian Tropical Research Institute (100625-1008-15-A4, 2017-0601-2020-2-A1).

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Jung, J., Guo, M., Crovella, M.E. et al. Frog embryos use multiple levels of temporal pattern in risk assessment for vibration-cued escape hatching. Anim Cogn (2022). https://doi.org/10.1007/s10071-022-01634-4

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  • DOI: https://doi.org/10.1007/s10071-022-01634-4

Keywords

  • Biotremology
  • Embryo behavior
  • Environmentally cued hatching
  • Incidental cues
  • Information processing
  • Vibration playback