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Putting the energetic-savings hypothesis underground: fossoriality does not affect metabolic rates in amphibians

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Abstract

By living underground, fossorial animals may be challenged by limited gas exchange due to prolonged exposure to low oxygen levels (hypoxia) and carbon dioxide buildup (hypercarbia) in their burrows. The negative effects of hypoxia and hypercarbia generally relate to changes in breathing and energy metabolism. In mammals, reduced metabolic rates are a common adaptation to a fossorial lifestyle. It is unclear, however, whether fossoriality exerted a similar selection pressure over the metabolism of fossorial ectotherms. In this study, we tested whether fossorial amphibians showed reduced metabolic rates compared to non-fossorial and aquatic ones in a phylogenetic framework. We found that whole-organism resting metabolic rates varied according to body mass and temperature. However, our analyses did not support the hypothesis of lowered energy expenditure in fossorial species. We suggest that the intrinsically low energetic requirements of amphibians, coupled with their relatively small body sizes, and ability to breathe through both lungs and skin, potentially circumvented the energetic and respiratory challenges imposed by fossoriality. Our analyses further suggest that species from higher latitudes have higher metabolic rates than those from lower latitudes regardless of lifestyle. This finding supports a mechanism of negative compensation in metabolic responses, whereby species from cooler habitats would be able to sustain relatively high activity levels despite thermal constraints. This view of energetics in the context of fossoriality integrates central tenets of eco-physiological theory (metabolic scaling, metabolic variation along environmental gradients) and comparative physiology (control of bimodal breathing). Ultimately, our work contributes to a broader understanding of the metabolic correlates in vertebrate ectotherms.

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Data availability

The data and code necessary to reproduce our analyses are available at https://hdl.handle.net/10464/16621.

Code availability

The data and code necessary to reproduce our analyses are available at https://hdl.handle.net/10464/16621.

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Acknowledgements

We thank Leonardo Servino for helping us obtain geographic coordinates for the species in our dataset. We also thank the two anonymous reviewers whose comments helped improve our manuscript. Research funding was provided by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to GJT (RGPIN-2020-05089).

Funding

Research funding was provided by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to GJT (RGPIN-2020–05089).

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DG and GJT conceived the idea. DG conducted the literature review. DG performed the analyses with input from GJT. DG and GJT wrote the manuscript.

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Correspondence to Danilo Giacometti.

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Giacometti, D., Tattersall, G.J. Putting the energetic-savings hypothesis underground: fossoriality does not affect metabolic rates in amphibians. Evol Ecol 37, 761–777 (2023). https://doi.org/10.1007/s10682-023-10253-5

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