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Escape-hatching decisions show adaptive ontogenetic changes in how embryos manage ambiguity in predation risk cues

Abstract

As animals develop, their capacities to sense cues, assess threats, and perform actions change, as do the relative costs and benefits that underlie behavioural decisions. We presented ambiguous cues to test if hatching decisions of red-eyed treefrogs, Agalychnis callidryas, change developmentally following adaptive predictions based on changing costs of decision errors. These arboreal embryos hatch prematurely to escape from egg predators, cued by vibrations in attacks. Young embryos modulate hatching based on the frequency and temporal properties of cues, reducing false alarms that unnecessarily expose them to risk in the water. Since the cost of false alarms decreases developmentally, we hypothesized that hatching responses to ambiguous cues would increase. We tested this using vibration playbacks at two ages, with two sets of 3 stimuli. We matched sampling costs and varied ambiguity in either temporal or frequency properties, so one stimulus elicited high hatching (positive control) and two elicited low hatching but differed in ambiguity, based on prior results with younger embryos. Older embryos hatched faster, indicating reduced cue sampling. They responded strongly to both clear threat cues and ambiguous stimuli but little when either property clearly indicated low risk. In both experiments, we saw the greatest ontogenetic change in response to the more ambiguous stimulus. These playback experiments improve our understanding of how embryos facing risk tradeoffs make adaptive decisions based on incidental cues from predators. Ambiguity in incidental cues is ubiquitous and developmental changes in behaviour due to ontogenetic adaptation of decision processes are likely to be widespread.

Significance statement

Animals must use imperfect information to guide their behavior, and the costs of decision errors often change with development. We found the decision rules that embryos apply to ambiguous cues to deploy escape behavior change developmentally, matching adaptive predictions based on changing cost–benefit tradeoffs. Our results, consistent across two different forms of ambiguity, suggest selection has shaped behavioral development to improve how embryos use ambiguous incidental cues for defense. This work both extends and generalizes earlier experiments varying the cost of information. It cautions against oversimplifying assumptions about embryo information use—at least for species and in contexts where a history of strong selective tradeoffs may have honed their capacity to make a key decision well—and demonstrates the value of vibration playbacks and embryo hatching behavior for research in animal cognition.

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Data availability

The data collected for and analyzed in this paper is available on Dryad (https://doi.org/10.5061/dryad.cnp5hqc4t).

Code availability

Custom code is available upon request.

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Acknowledgements

We thank Ana Ospina, Rachel Snyder, Adeline Almanzar, María José Salazar Nicholls, Chloe Fouilloux, and Estefany Caroline Guevara Molina for assistance during field research. We thank members of the Gamboa Frog Group at STRI, Team Treefrog at BU, and Peter Buston for multiple discussions of this research and helpful comments on the manuscript. Finally, we thank the editor and two anonymous reviewers for constructive comments and suggestions that helped us to improve this manuscript.

Funding

This research was funded by the National Science Foundation (IOS-1354072 to KMW and JGM).

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Affiliations

Authors

Contributions

Conceptualization: JJ and KMW.

Methodology: JJ, JGM, and KMW.

Software: JJ and JGM.

Validation: JJ and KMW.

Formal analysis: JJ.

Investigation: JJ and KMW.

Data curation: JJ.

Writing—original draft: JJ.

Writing—review and editing: JJ, JGM, and KMW.

Visualization: JJ.

Supervision: KMW.

Project administration: KMW.

Funding acquisition: JGM and KMW.

Corresponding author

Correspondence to Julie Jung.

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Ethics approval

All applicable international, national, and institutional guidelines for the use of animals were followed. This research was conducted under permits from the Panamanian Environmental Ministry (SE/A-55–17 and SC/A-10–18) and approved by the Institutional Animal Care and Use Committee of the Smithsonian Tropical Research Institute (2017–0601-2020–2).

Conflict of interest

The authors declare no competing interests.

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Communicated by A. Taylor Baugh

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Jung, J., McDaniel, J.G. & Warkentin, K.M. Escape-hatching decisions show adaptive ontogenetic changes in how embryos manage ambiguity in predation risk cues. Behav Ecol Sociobiol 75, 141 (2021). https://doi.org/10.1007/s00265-021-03070-9

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Keywords

  • Phenotypic plasticity
  • Embryo decisions
  • Biotremology
  • Environmentally cued hatching
  • Mechanosensory vibration cues
  • Uncertainty