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Survival and metabolism of Rana arvalis during freezing

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Abstract

Freeze tolerance and changes in metabolism during freezing were investigated in the moor frog (Rana arvalis) under laboratory conditions. The data show for the first time a well-developed freeze tolerance in juveniles of a European frog capable of surviving a freezing exposure of about 72 h with a final body temperature of −3°C. A biochemical analysis showed an increase in liver and muscle glucose in response to freezing (respectively, 14-fold and 4-fold between 4 and −1°C). Lactate accumulation was only observed in the liver (4.1 ± 0.8 against 16.6 ± 2.4 μmol g−1 fresh weight (FW) between 4 and −1°C). The quantification of the respiratory metabolism of frozen frogs showed that the aerobic metabolism persists under freezing conditions (1.4 ± 0.7 μl O2 g−1 FW h−1 at −4°C) and decreases with body temperature. After thawing, the oxygen consumption rose rapidly during the first hour (6-fold to 16-fold) and continued to increase for 24 h, but at a lower rate. In early winter, juvenile R. arvalis held in an outdoor enclosure were observed to emerge from ponds and hibernate in the upper soil and litter layers. Temperature recordings in the substratum of the enclosure suggested that the hibernacula of these juvenile frogs provided sheltering from sub-zero air temperatures and reduced the time spent in a frozen state corresponding well with the observed freeze tolerance of the juveniles. This study strongly suggests that freeze tolerance of R. arvalis is an adaptive trait necessary for winter survival.

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Acknowledgments

We express our gratitude to Thomas Sorensen for assistance with collecting frogs and Christina Richardson for critically reading the manuscript. This work was supported by a research grant from the C.N.R.S. France for Y.V. and a grant from the Danish Science Research Council (# 21-01-0518) for M.H. and H.R. The present investigation was carried out according to the ethical principles laid down by the European Convention for the protection of Vertebrate Animals used for Experimental and Scientific purposes (Council of Europe No. 123, Strasbourg, 1985).

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Authors and Affiliations

  1. Ecologie des Hydrosystème Fluviaux (U.M.R. CNRS 5023), Université Claude Bernard Lyon1, Université de Lyon, Bât. Darwin C, 69622, Villeurbanne Cedex, France

    Yann Voituron

  2. Department of Science, Systems and Models, Roskilde University, Universitetvej 1, P.O. Box 260, 4000, Roskilde, Denmark

    Louise Paaschburg & Hans Ramløv

  3. Department of Terrestrial Ecology, National Environmental Research Institute, University of Aarhus, Vejlsøvej 25, P.O. Box 314, 8600, Silkeborg, Denmark

    Martin Holmstrup

  4. Laboratoire de Physiologie Intégrative, Cellulaire et Moléculaire UMR 5123, Université Claude Bernard Lyon 1, Université de Lyon, 43 bd du 11 Novembre 1918, 69622, Villeurbanne Cedex, France

    Hervé Barré

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  1. Yann Voituron
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  2. Louise Paaschburg
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  3. Martin Holmstrup
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  4. Hervé Barré
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  5. Hans Ramløv
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Correspondence to Yann Voituron.

Additional information

Communicated by G. Heldmaier.

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Voituron, Y., Paaschburg, L., Holmstrup, M. et al. Survival and metabolism of Rana arvalis during freezing. J Comp Physiol B 179, 223–230 (2009). https://doi.org/10.1007/s00360-008-0307-3

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  • DOI: https://doi.org/10.1007/s00360-008-0307-3

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