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Physiological responses to freezing in hatchlings of freeze-tolerant and -intolerant turtles

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Abstract

Freeze tolerance is a complex cold-hardiness adaptation that has independently evolved in a diverse group of organisms, including several ectothermic vertebrates. Because little is known about the mechanistic basis for freeze tolerance in reptiles, we compared responses to experimental freezing in winter-acclimatized hatchlings representing nine taxa of temperate North American turtles, including ones that tolerated freezing and others that did not. Viability rates of hatchlings frozen to −3°C for 72 h ranged from 0 to 100%. Tolerance to freezing was poor in Sternotherus odoratus, Graptemys geographica and Trachemys scripta, intermediate in Chelydra serpentina, and high in Emydoidea blandingii, Chrysemys picta bellii, C. p. marginata, Malaclemys terrapin, and Terrapene ornata, and generally reflected the winter thermal ecology of each taxon. Plasma activity of lactate dehydrogenase (LDH), a novel in vivo index of freeze/thaw damage, corroborated viability assessments and demonstrated that cryoinjury occurred even in surviving turtles. Irrespective of taxon, cryoinjury tended to be higher in smaller individuals and in those having relatively low water contents; however, bases for these associations were not apparent. Screening for certain organic osmolytes that might promote freezing survival by colligatively reducing ice content and limiting cell dehydration showed that the plasma of unfrozen (control) turtles contained small quantities of glucose (1.3–5.8 mmol l−1) and lactate (0.6–3.2 mmol l−1) and modest amounts of urea (range of mean values for all taxa 8.2–52.3 mmol l−1). Frozen/thawed turtles of all taxa accumulated modest amounts of glucose and lactate that jointly raised the plasma solute concentration by 30–100 mmol l−1. We conclude that organic osmolytes accumulated both before and during freezing may promote survival in species that have evolved a tolerance to freezing, but are not necessarily accumulated for that purpose.

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Acknowledgments

We thank P. Myer and the Connealy and Davis families for granting us permission to collect turtles on their lands. We also thank S. Dinkelacker for providing some of the hatchlings, and M. Elnitsky and T. Muir for commenting on the manuscript. Collecting permits were obtained from the Nebraska Game and Parks Commission, Indiana Department of Natural Resources, and New Jersey Division of Fish and Wildlife. Experimental procedures were approved by the Animal Care and Use Committee of Miami University. This work was funded by grants from the National Science Foundation (IBN 98017087 and IOB 0416750) to JPC and by the Miami University Summer Workshop (PJB).

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  1. Department of Zoology, Miami University, Oxford, OH, 45056, USA

    Jon P. Costanzo, Patrick J. Baker & Richard E. Lee Jr

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  1. Jon P. Costanzo
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  2. Patrick J. Baker
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  3. Richard E. Lee Jr
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Correspondence to Jon P. Costanzo.

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Communicated by H.V. Carey

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Costanzo, J.P., Baker, P.J. & Lee, R.E. Physiological responses to freezing in hatchlings of freeze-tolerant and -intolerant turtles. J Comp Physiol B 176, 697–707 (2006). https://doi.org/10.1007/s00360-006-0092-9

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  • DOI: https://doi.org/10.1007/s00360-006-0092-9

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