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Ontogenetic reduction in thermal tolerance is not alleviated by earlier developmental acclimation in Rana temporaria

  • Physiological ecology – original research
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Abstract

Complex life-histories may promote the evolution of different strategies to allow optimal matching to the environmental conditions that organisms can encounter in contrasting environments. For ectothermic animals, we need to disentangle the role of stage-specific thermal tolerances and developmental acclimation to predict the effects of climate change on spatial distributions. However, the interplay between these mechanisms has been poorly explored. Here we study whether developmental larval acclimation to rearing temperatures affects the thermal tolerance of subsequent terrestrial stages (metamorphs and juveniles) in common frogs (Rana temporaria). Our results show that larval acclimation to warm temperatures enhances larval heat tolerance, but not thermal tolerance in later metamorphic and juvenile stages, which does not support the developmental acclimation hypothesis. Further, metamorphic and juvenile individuals exhibit a decline in thermal tolerance, which would confer higher sensitivity to extreme temperatures. Because thermal tolerance is not enhanced by larval developmental acclimation, these ‘risky’ stages may be forced to compensate through behavioural thermoregulation and short-term acclimation to face eventual heat peaks in the coming decades.

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Acknowledgements

We thank Florentino Braña, Miguel Carretero, Silvia Matesanz, and Ross Alford (editor) and two anonymous reviewers for helpful comments that improved previous versions of the manuscript. We thank the staff from the Principality of Asturias and the Governing Council of Castile-León for providing the permits to conduct this investigation. We are also grateful to two anonymous reviewers for their helpful comments.

Funding

This research was supported by MINECO (CGL2012-40246) and MEC (CGL2017-86924-P) Grants. U.E.U. was supported by a Ph.D. award (BES-2013-063203) from MEC.

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Authors and Affiliations

Authors

Contributions

UEU and AGN designed the study; AGN collected the experimental animals, UEU, MS, and ASP performed the experiment; UEU and MS analysed data; all authors contributed to the writing.

Corresponding author

Correspondence to Urtzi Enriquez-Urzelai.

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Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed. Field work was carried out under the Government of the Principality of Asturias Permit No. 2015/008130 and 2016/001092. Experiments were carried out under the Ethics Board for Animal Experimentation of the University of Oviedo Permit No. 8-INV-2012. The members of the research team have approved licenses by the Service of Animal Welfare and Production of the Principality of Asturias to design (license type C; A.G.N) and execute (license type B; U.E.U.) experimental protocols with animals.

Data accessibility

Data supporting this article are available from the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.643q7g2.

Additional information

Communicated by Ross Andrew Alford.

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Enriquez-Urzelai, U., Sacco, M., Palacio, A.S. et al. Ontogenetic reduction in thermal tolerance is not alleviated by earlier developmental acclimation in Rana temporaria. Oecologia 189, 385–394 (2019). https://doi.org/10.1007/s00442-019-04342-y

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  • DOI: https://doi.org/10.1007/s00442-019-04342-y

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