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Journal of Experimental Biology partnership with Dryad

Hibernation physiology, freezing adaptation and extreme freeze tolerance in a northern population of the wood frog
Jon P. Costanzo, M. Clara F. do Amaral, Andrew J. Rosendale, Richard E. Lee, Jr

SUMMARY

We investigated hibernation physiology and freeze tolerance in a population of the wood frog, Rana sylvatica, indigenous to Interior Alaska, USA, near the northernmost limit of the species' range. Winter acclimatization responses included a 233% increase in the hepatic glycogen depot that was subsidized by fat body and skeletal muscle catabolism, and a rise in plasma osmolality that reflected accrual of urea (to 106±10 μmol ml−1) and an unidentified solute (to ~73 μmol ml−1). In contrast, frogs from a cool-temperate population (southern Ohio, USA) amassed much less glycogen, had a lower uremia (28±5 μmol ml−1) and apparently lacked the unidentified solute. Alaskan frogs survived freezing at temperatures as low as −16°C, some 10–13°C below those tolerated by southern conspecifics, and endured a 2-month bout of freezing at −4°C. The profound freeze tolerance is presumably due to their high levels of organic osmolytes and bound water, which limits ice formation. Adaptive responses to freezing (−2.5°C for 48 h) and subsequent thawing (4°C) included synthesis of the cryoprotectants urea and glucose, and dehydration of certain tissues. Alaskan frogs differed from Ohioan frogs in retaining a substantial reserve capacity for glucose synthesis, accumulating high levels of cryoprotectants in brain tissue, and remaining hyperglycemic long after thawing. The northern phenotype also incurred less stress during freezing/thawing, as indicated by limited cryohemolysis and lactate accumulation. Post-glacial colonization of high latitudes by R. sylvatica required a substantial increase in freeze tolerance that was at least partly achieved by enhancing their cryoprotectant system.

FOOTNOTES

  • AUTHOR CONTRIBUTIONS

    J.P.C. and M.C.F.A conceived the study; J.P.C., M.C.F.A and A.J.R. designed the experiments and collected the data; J.P.C. analyzed the data and wrote the paper; J.P.C., M.C.F.A, A.J.R. and R.E.L. contributed substantially to interpreting the data and developing the manuscript and take full responsibility for the content of the paper.

  • COMPETING INTERESTS

    No competing interests declared.

  • FUNDING

    This work was supported by the National Science Foundation [IOS1022788 to J.P.C.]; and the Portuguese Science and Technology Foundation (Fundação para a Ciência e Tecnologia, Ministério da Educação e Ciência, Portugal) [SFRH/BD/63151/2009 to M.C.F.A.].

  • LIST OF SYMBOLS AND ABBREVIATIONS

    FPeq
    equilibrium freezing/melting point (°C)
    GDH
    glutamate dehydrogenase
    Hb
    hemoglobin
    HSI
    hepatosomatic index (g dry liver g−1 dry body × 100)
    Tb
    body temperature (°C)
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