Journal of Comparative Physiology B

, Volume 160, Issue 2, pp 137–143 | Cite as

Supercooling and freeze-tolerance in the European wall lizard, Podarcis muralis, with a revisional history of the discovery of freeze-tolerance in vertebrates

  • Dennis L. Claussen
  • Mikal D. Townsley
  • Richard G. Bausch
Article

Summary

Wall lizards were collected in the fall of 1988 from a population introduced in 1951 into Cincinnati, OH. They were acclimated to 5 °C for several weeks prior to testing at sub-zero temperatures. Eleven super-cooled lizards were removed from the cooling chamber prior to crystallization after between 15 min and 26 h at body temperatures ranging from -2.2 to -5.9 °C. With the exception of one individual supercooled to-5.0 °C, all lizards recovered fully. The crystallization temperatures of 15 lizards which froze ranged from -0.6 to -6.4 °C. Frozen lizards were stiff with a distinct blue color, which faded upon thawing at 3 °C. The ice contents of frozen lizards were determined calorimetrically and/or estimated from a theoretical model, the two methods being generally in close agreement. Remarkably, five individuals recovered fully from exposures as long as 2 h and with as much as 28% of their body water frozen. Although these animals are not as tolerant as certain other vertebrates they are clearly able to withstand freezing under some circumstances. Failure to survive freezing was attributed either to excessive ice accumulation during a prolonged freeze or to excessive supercooling prior to freezing, which induced a large initial surge of ice formation upon crystallization. Our results accord with those of Weigmann (1929). We accordingly recognize him as the first to demonstrate freeze-tolerance in vertebrates, and we further recognize P. muralis as the first vertebrate known to survive freezing.

Key words

Freeze-tolerance Supercooling Lizards Podarcis muralis 

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References

  1. Cameron AT, Brownlee TI (1913) The effect of low temperature on the frog. Trans R Soc Can 7:107–124Google Scholar
  2. Claussen DL, Costanzo JP (1990) A simple model for estimating the ice content of freezing ectotherms. J Thermal Biol (In Press)Google Scholar
  3. Costanzo JP (1988) Recovery from ice-entombment in garter snakes. Herp Rev 19:76–77Google Scholar
  4. Costanzo JP, Claussen DL (1990) Natural freeze tolerance in the terrestrial turtle, Terrapene carolina. J Exp Zool (In Press)Google Scholar
  5. Costanzo JP, Claussen DL, Lee RE Jr (1988) Natural freeze-tolerance in a reptile. Cryo-Lett 9:380–385Google Scholar
  6. Hedeen SE (1984) The establishment of Podarcis muralis in Cincinnati, Ohio. Herp Rev 15:70–71Google Scholar
  7. Knauthe K (1891) Methe Erfahrungen über das Verhalten von Amphibien und Fischen gegenüber der Kälte. Zoolog Anz 14:104–106Google Scholar
  8. Kodis T (1898) Die Unterkühlung der tierischen und pflanzlichen Gewebe. Zbl Physiol 12:593–595Google Scholar
  9. Layne JR, Jr, Lee RE Jr (1987) Freeze-tolerance and the dynamics of ice formation in wood frogs (Rana sylvatica) from southern Ohio. Can J Zool 65:2062–2065Google Scholar
  10. Layne JR, Jr, Lee RE Jr (1989) Seasonal variation in freeze-tolerance and ice content of the tree frog Hyla versicolor. J Exp Zool 249:133–137Google Scholar
  11. Lee RE Jr, Lewis E (1985) Effects of temperature and duration of exposure on tissue ice formation in the gall fly, Eurosta solidaginis (Diptera, Tephritidae). Cryo-Lett 6:25–34Google Scholar
  12. Lotshaw DP (1977) Temperature adaptation and effects of thermal acclimation in Rana sylvatica and Rana catesbeiana. Comp Biochem Physiol 56A:287–294Google Scholar
  13. Lowe CH, Lardner PJ, Halpern EA (1971) Supercooling in reptiles and other vertebrates. Comp Biochem Physiol 39A:125–135Google Scholar
  14. MacArthur DL, Dandy JWT (1982) Physiological aspects of overwintering in the boreal chorus frog (Pseudacris triseriata maculata). Comp Biochem Physiol 72A:137–141Google Scholar
  15. Müller-Erzbach W (1891) Die Widerstandsfähigkeit des Frosches gegen das Einfrieren. Zoolog Anz 14:383–384Google Scholar
  16. Musacchia XJ, Sievers ML (1956) Effects of induced cold torpor on blood of Chrysemys picta. Am J Physiol 187:99–102Google Scholar
  17. Packard GC, Packard MJ, McDaniel PL, McDaniel LL (1989) Tolerance of hatchling painted turtles to subzero temperatures. Can J Zool 67:828–830Google Scholar
  18. Paukstis GL, Shuman RD, Janzen FJ (1989) Supercooling and freeze-tolerance in hatchling painted turtles (Chrysemys picta). Can J Zool 67:1082–1084Google Scholar
  19. Réaumur (de) RA (1737) Des chenilles qui vivent en société. In: Mortier P (ed) Mémoires pour servir à l'histoire des Insectes. Vol 2. Amsterdam, pp 153–225. cited in Vannier G (1986) Accroissement de la capacite de surfusion chez les adultes de Chrysoperla carnea (Insectes Nevropteres) entrant en diapause hivernale. Neuroptera Internat 4:71–82Google Scholar
  20. Schmid WD (1982) Survival of frogs in low temperature. Science 215:697–698Google Scholar
  21. Spellerberg IF (1972) Temperature tolerances of southeast Australian reptiles examined in relation to reptile thermoregulatory behaviour and distribution. Oecologia 9:23–46Google Scholar
  22. Spellerberg IF (1976) Adaptations of reptiles to cold. In: d'A Bellairs A, Cox CB (ed) Morphology and biology of reptiles. Linnacean Soc Symp, Series 3, pp 261–285Google Scholar
  23. Storey KB (1984) Freeze-tolerance in the frog, Rana sylvatica. Experientia 40:1261–1262Google Scholar
  24. Storey KB (1985) Freeze-tolerance in terrestrial frogs. Cryo-Lett 6:115–134Google Scholar
  25. Storey KB, Storey JM (1988) Freeze-tolerance in animals. Physiol Rev 68:27–84Google Scholar
  26. Storey KB, Storey JM, Brooks SPJ, Churchill TA, Brooks RJ (1988) Hatchling turtles survive freezing during winter hibernation. Proc Natl Acad Sci 85:8350–8354Google Scholar
  27. Street D (1979) The reptiles of northern and central Europe. B.T. Batsford Ltd, LondonGoogle Scholar
  28. Weigmann R (1929) Die Wirkung starker Abkühlung auf Amphibien und Reptilien. Z Wiss Zool 134:641–692Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • Dennis L. Claussen
    • 1
  • Mikal D. Townsley
    • 1
  • Richard G. Bausch
    • 1
  1. 1.Department of ZoologyMiami UniversityOxfordUSA

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