Behavioral syndrome persists over metamorphosis in a pond-breeding amphibian

Abstract

In recent years, behavioral ecology has shifted from assuming animal behavior is infinitely plastic and situation specific to recognizing that behavior can be limited in its plasticity and correlated across different ecological situations. At the center of this new framework are behavioral syndromes or consistent individual differences in behavioral tendencies. Over the past decade, numerous studies have identified the evolutionary mechanisms and ecological implications of behavioral syndromes. However, the persistence of behavioral syndromes over ontogeny remains an open question. Species with complex life cycles present an interesting system in which to test the persistence of behavioral syndromes, because such life histories are thought to evolve when correlations between life stages are costly. In this study, we tested the hypothesis that behavioral tendencies of species with complex life histories are consistent within a life stage (before or after metamorphosis) but not between life stages. We experimentally assayed the activity, boldness, and exploration of spotted salamanders (Ambystoma maculatum) before and after metamorphosis. We found most behaviors to be at least moderately repeatable. Additionally, there was support for a behavioral syndrome within the larval stage as well as between larval behaviors and juvenile boldness. Our results reject the adaptive decoupling hypothesis and instead suggest that behavioral syndromes in species with complex life cycles can be maintained over metamorphosis.

Significance statement

A central prediction of behavioral syndromes is that individual behavioral consistency should be maintained over the life of an organism. However, in species with complex life cycles, evolution is thought to act independently on each stage, leading to the prediction that behavioral syndromes should not persist over metamorphosis. We tested for behavioral correlations over metamorphosis by assaying salamander activity, boldness, and exploration in larval and juvenile salamanders. We found support for behavioral syndromes within and between life stages. These findings contradict the predictions of complex life cycle evolution and instead suggest that behavioral syndromes may span metamorphosis. However, because support for the persistence of syndromes over metamorphosis varies between taxa, we caution researchers against extrapolating inferences from the larval stage to the juvenile stage.

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Data availability

The data generated and analyzed during the current study are available in the figshare repository, https://doi.org/10.6084/m9.figshare.7255868.

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Acknowledgments

We thank L. Weiskopf, D. Westfall, C. Kimball, and E. Wedekind for monitoring pond mesocosms and J. Burkhart for assisting with animal care. This manuscript was greatly improved by comments from the Semlitsch lab, Rex Cocroft, and two anonymous reviewers.

Funding

This work was funded by the US Department of Defense SERDP (RC-2155 and RC-2703), National Science Foundation (DEB-0943941 to BHO and DEB-1620046). AMK was supported by the University of Missouri Undergraduate Mentoring in Research Program, and BHO was supported by a University of Missouri Life Sciences Fellowship and Trans World Airline Scholarship.

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Correspondence to Brittany H. Ousterhout.

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The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in this study were in accordance with the ethical standards of the University of Missouri Animal Care and Use Committee (8402) and collected under Missouri Department of Conservation permit no. 16463.

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Communicated by N. A. Dochtermann

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Koenig, A.M., Ousterhout, B.H. Behavioral syndrome persists over metamorphosis in a pond-breeding amphibian. Behav Ecol Sociobiol 72, 184 (2018). https://doi.org/10.1007/s00265-018-2595-2

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Keywords

  • Ambystoma maculatum
  • Boldness
  • Complex life history
  • Personality
  • Temperament