Vertebrate Cryobiology

 

Books

Lee, R. E., G. J. Warren, and L. V. Gusta (eds.). 1995. Biological Ice Nucleation and its Applications. APS Press, St. Paul. 370 pp.

Reviews & Book Chapters

(student authors in boldface)

Costanzo, J. P. and Lee, R. E. 2013. Commentary: Avoidance and tolerance of freezing in ectothermic vertebrates. Journal of Experimental Biology 216, 1961-1967. | PDF

Costanzo, J. P. 2012. Extreme cold hardiness in ectotherms. Nature Education Knowledge 3:1-10. | PDF

Costanzo, J. P., R. E. Lee, and G. R. Ultsch. 2008. Physiological ecology of overwintering in hatchling turtles. Journal of Experimental Zoology 309A: 297-379. | PDF

Baker, P. J., J. P. Costanzo, and R. E. Lee. 2004. Environmental physiology of terrestrial hibernation in hatchling turtles. In: Life in the Cold: Evolution, Mechanisms, Adaptation, and Application (eds. B. M. Barnes and H. V. Carey), pp. 329-338. Twelfth International Hibernation Symposium. Biological Papers of the University of Alaska. Number 27. Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska, USA. | PDF

Lee, R. E. and J. P. Costanzo. 1998. Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annual Review of Physiology 60: 55-72. | PDF

Costanzo, J. P. and R. E. Lee. 1996. Mini-review: ice nucleation in freeze-tolerant vertebrates. CryoLetters 17: 111-118. | PDF

Costanzo, J. P. and R. E. Lee. 1995. Supercooling and ice nucleation in vertebrate ectotherms. In: Biological Ice Nucleation and its Applications (eds. R. E. Lee, G. J. Warren and L. V. Gusta), pp. 221-238. APS Press, St. Paul. | PDF

Costanzo, J. P., R. E. Lee, A. L. DeVries, T. Wang and J. R. Layne. 1995. Survival mechanisms of vertebrate ectotherms at subfreezing temperatures: applications in cryomedicine. FASEB Journal 9: 351-358. | PDF

Layne, J. R. and R. E. Lee. 1995. Adaptations of frogs to survive freezing. Climate Research 5: 53-59. | PDF

Costanzo, J. P. and R. E. Lee. 1994. Biophysical and physiological responses promoting freeze tolerance in vertebrates. News in Physiological Sciences 9: 252-256. | PDF

Lee, R. E. and J. P. Costanzo. 1993. Integrated physiological responses promoting anuran freeze tolerance. In: Life in the Cold: Ecological, Physiological, and Molecular Mechanisms (eds. C. Carey, G. L. Florant, B. A. Wunder and B. Horwitz), pp. 501-510. Westview Press, Boulder. | PDF

Lee, R. E. 1988. Freeze tolerance and adaptation to low temperature in insects and frogs. In: Low Temperature Biotechnology: Emerging Applications and Engineering Contributions BED Vol. 10, HTD Vol. 98 (eds. J. J. McGrath and K. R. Diller), pp. 81-90. American Society of Mechanical Engineers, New York. | PDF

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Refereed Articles

(student authors in boldface)

2015-

Rosendale, A. R., Lee, R. E. and J. P. Costanzo. 2015. Seasonal variation and freezing response of glucose transporter 2 in liver of the wood frog: implications for geographic variation in freeze tolerance. Journal of Zoology 297: 132-138. | PDF

do Amaral, M. C., Lee, R. E., and J. P. Costanzo. 2015. Hepatocyte responses to in vitro freezing and β-adrenergic stimulation: insights into the extreme freeze tolerance of subarctic Rana sylvatica. Journal of Experimental Zoology 323A: 89-96. | PDF

Costanzo, J. P., Reynolds, A. M., do Amaral, M. C., Rosendale, A. J., and R. E. Lee. 2015. Cryoprotectants and extreme freeze tolerance in a subarctic population of the wood frog. PLoS ONE 10(2): e0117234 | PDF

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2010-2014

Rosendale, A. J., Lee, R. E., and J. P. Costanzo. 2014. Effect of physiological stress on expression of glucose transporter 2 in liver of the wood frog, Rana sylvatica. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 321A: 566-576. | PDF

Rosendale, A. J., Costanzo, J. P., Kiss, A. J., and R. E. Lee. 2014. Identification and expression of a putative facilitative urea transporter in three species of true frogs (Ranidae): implications for terrestrial adaptation. Advances in Biology 2014, Article ID 148276, 11 pages http://dx.doi.org/10.1155/2014/148276 | PDF

Costanzo, J. P., do Amaral, M. C., Rosendale, A. J., and R. E. Lee. 2014. Seasonality of freeze tolerance in a subarctic population of the wood frog, Rana sylvatica. International Journal of Zoology, 2014, Article ID 750153, 13 pages http://dx.doi.org/10.1155/2014/750153:13 | PDF

Reynolds AM, Lee RE, Jr., and Costanzo JP (2014) Membrane adaptation in phospholipids and cholesterol in the widely distributed, freeze-tolerant wood frog, Rana sylvatica. Journal of Comparative Physiology B 184:371-383 | PDF

Rosendale A. J., Philip, B. N., Lee, R. E., and J. P. Costanzo. 2014. Cloning, characterization, and expression of glucose transporter 2 in the freeze-tolerant wood frog, Rana sylvatica. Biochimica et Biophysica Acta (BBA) - General Subjects 1840:1701-1711 | PDF

Do Amaral, M. C., Lee, R. E., and J. P. Costanzo. 2013. Enzymatic regulation of glycogenolysis in a subarctic population of the wood frog: implications for extreme freeze tolerance. PLoS ONE 8:e79169 | PDF

Costanzo, J. P., do Amaral, M. C., Rosendale, A. J., and R. E. Lee. 2013. Hibernation physiology, freezing adaptation, and extreme freeze tolerance in a northern population of the wood frog. Journal of Experimental Biology 216:3461-3473 | PDF

Baker, P. J., Costanzo, J. P., Iverson, J. B., and R. E. Lee. 2013. Seasonality and interspecific and intraspecific asynchrony in emergence from the nest by hatchling freshwater turtles.Canadian Journal of Zoology 91, 451-461. | PDF

Muir, T. M., B. D. Dishong, R. E. Lee, and J. P. Costanzo. 2013. Energy use and management of energy reserves in hatchling turtles (Chrysemys picta) exposed to variable winter conditions. Journal of Thermal Biology 38, 324-330. | PDF

Rosendale, A. J ., R. E. Lee, and J. P. Costanzo. 2012. Seasonal variation and response to osmotic challenge in urea transporter expression in the dehydration- and freeze-tolerant wood frog, Rana sylvatica. Journal of Experimental Zoology. 317A:401-409. | PDF

Kiss, A. J., T. J. Muir, R. E. Lee, and J. P. Costanzo. 2011. Seasonal variation in the hepatoproteome of the dehydration- and freeze-tolerant wood frog, Rana sylvatica. International Journal of Molecular Sciences. 12:8406-8414. | PDF

Baker, P. J., J. B. Iverson, R. E. Lee, and J. P. Costanzo. 2010. Winter severity and phenology of spring emergence from the nest in freshwater turtles. Naturwissenschaften 97:607-615. | PDF

Muir, T. J., J. P. Costanzo, and R. E. Lee. 2010. Urea-induced hypometabolism in the hibernating wood frog (Rana sylvatica) is not reflected in isolated mitochondria. Journal of Comparative Physiology B 180: 1183-1189. | PDF

Muir, T. J., J. P. Costanzo, and R. E. Lee. 2010. Evidence for urea-induced hypometabolism in isolated organs of dormant ectotherms. Journal of Experimental Zoology 313A: 28-34. | PDF

Muir, T. J., J. P. Costanzo, and R. E. Lee. 2010. Brief chilling to subzero temperature increases cold hardiness in the hatchling painted turtle (Chrysemys picta). Physiological and Biochemical Zoology 83: 174-181. | PDF

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2005-2009

Schiller, T. M., J. P. Costanzo, and R. E. Lee. 2008.  Urea production capacity in the wood frog (Rana sylvatica) varies with season and experimentally induced hyperuremia.  Journal of Experimental Zoology 309A: 484-493. | PDF

Costanzo, J. P. and R. E. Lee. 2008. Urea loading enhances freezing survival and postfreeze recovery in a terrestrially hibernating frog. Journal of Experimental Biology 211: 2969-2975. | PDF

Costanzo, J. P., M. Marjanovic, E. A. Fincel and R. E. Lee. 2008. Urea loading enhances postfreeze performance of frog skeletal muscle. Journal of Comparative Physiology B 178: 413-420. | PDF

Muir, T. J., J. P. Costanzo, and R. E. Lee. 2008. Metabolic depression induced by urea in organs of the wood frog, Rana sylvatica: effects of season and temperature. Journal of Experimental Zoology 309A: 111-116. | PDF

Baker, P. J., J. P. Costanzo, and R. E. Lee. 2007. Oxidative stress and antioxidant capacity of a terrestrially hibernating hatchling turtle. Journal of Comparative Physiology B 177: 875-883. | PDF

Muir, T. J., J. P. Costanzo, and R. E. Lee. 2007. Osmotic and metabolic responses to dehydration and urea-loading in a dormant, terrestrially hibernating frog. Journal of Comparative Physiology B 177: 917-926. | PDF

Costanzo, J. P., P. J. Baker, and R. E. Lee. 2006. Physiological responses to freezing in hatchlings of freeze-tolerant and -intolerant turtles. Journal of Comparative Physiology B 176: 697-707. | PDF

Baker, P. J., J. P. Costanzo, R. Herlands, R. C. Wood, and R. E. Lee. 2006. Inoculative freezing promotes winter survival in hatchling diamondback terrapin, Malaclemys terrapin. Canadian Journal of Zoology 84: 116-124. | PDF

Costanzo, J. P. and R. E. Lee. 2005. Cryoprotection by urea in a terrestrially hibernating frog. Journal of Experimental Biology 208: 4079-4089. | PDF

Dinkelacker, S. A., J. P. Costanzo, J. B. Iverson, and R. E. Lee. 2005. Survival and physiological responses of hatchling Blanding's turtles (Emydoidea blandingii) to submergence in normoxic and hypoxic water under simulated winter conditions. Physiological and Biochemical Zoology 78: 356-363. | PDF

Dinkelacker, S. A., J. P. Costanzo, and R. E. Lee. 2005. Anoxia tolerance and freeze tolerance in hatchling turtles. Journal of Comparative Physiology B 175: 209-217. | PDF

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2000-2004

Dinkelacker, S. A., J. P. Costanzo, J. B. Iverson, and R. E. Lee. 2004. Cold-hardiness and dehydration resistance of hatchling Blanding’s turtles (Emydoidea blandingii): implications for overwintering in a terrestrial habitat. Canadian Journal of Zoology 82: 594-600. | PDF

Costanzo, J. P., S. A. Dinkelacker, J. B. Iverson, and R. E. Lee. 2004. Physiological ecology of overwintering in the hatchling painted turtle: multiple-scale variation in response to environmental stress. Physiological and Biochemical Zoology 77: 74-99. | PDF

Baker, P. J., J. P. Costanzo, J. B. Iverson and R. E. Lee. 2003. Adaptations to terrestrial overwintering of hatchling northern map turtles, Graptemys geographica. Journal of Comparative Physiology B 173: 643-651. | PDF

Costanzo, J. P., P. J. Baker, S. A. Dinkelacker and R. E. Lee. 2003. Endogenous and exogenous ice-nucleating agents constrain supercooling in the hatchling painted turtle. Journal of Experimental Biology 206: 477-485. | PDF

Irwin, J. T., J. P. Costanzo and R. E. Lee. 2003. Postfreeze reduction of locomotor endurance in the freeze-tolerant wood frog, Rana sylvatica. Physiological and Biochemical Zoology 76: 331-338. | PDF

Irwin, J. T. and R. E. Lee. 2003. Geographic variation in energy storage and physiological responses to freezing in the gray treefrogs Hyla versicolor and H. chrysoscelis. Journal of Experimental Biology 206: 2859-2867. | PDF

Costanzo, J. P., E. E. Jones and R. E. Lee. 2001. Physiological responses to supercooling and hypoxia in the hatchling painted turtle, Chrysemys picta. Journal of Comparative Physiology B 171: 335-340. | PDF

Costanzo, J. P., J. D. Litzgus, J. B. Iverson and R. E. Lee. 2001. Cold-hardiness and evaporative water loss in hatchling turtles. Physiological and Biochemical Zoology 74: 510-519. | PDF

Costanzo, J. P., J. D. Litzgus, J. L. Larson, J. B. Iverson and R. E. Lee. 2001. Characteristics of nest soil, but not geographic origin, influence cold hardiness of hatchling painted turtles. Journal of Thermal Biology 26: 65-73. | PDF

Costanzo, J. P., J. D. Litzgus, J. B. Iverson and R. E. Lee. 2000. Seasonal changes in physiology and development of cold hardiness in the hatchling painted turtle, Chrysemys picta. Journal of Experimental Biology 203: 3459-3470. | PDF

Frisbie, M. P., J. P. Costanzo and R. E. Lee. 2000. Physiological and ecological aspects of low-temperature tolerance in embryos of the wood frog, Rana sylvatica. Canadian Journal of Zoology 78: 1032-1041. | PDF

Costanzo, J. P., J. D. Litzgus, J. B. Iverson and R. E. Lee. 2000. Ice nuclei in soil compromise cold hardiness of hatchling painted turtles, Chrysemys picta. Ecology 81: 346-360. | PDF

Woodhams, D. C., J. P. Costanzo, J. D. Kelty and R. E. Lee. 2000. Cold hardiness in two helminth parasites of the freeze-tolerant wood frog, Rana sylvatica. Canadian Journal of Zoology 78: 1085-1091. | PDF

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1995-1999

Litzgus, J. D., J. P. Costanzo, R. J. Brooks and R. E. Lee. 1999. Phenology and ecology of hibernation in spotted turtles (Clemmys guttata) near the northern limit of their range. Canadian Journal of Zoology 77: 1348-1357. | PDF

Irwin, J. T., J. P. Costanzo and R. E. Lee. 1999. Terrestrial hibernation in the northern cricket frog, Acris crepitans. Canadian Journal of Zoology 77: 1240-1246. | PDF

Costanzo, J. P., J. D. Litzgus and R. E. Lee. 1999. Behavioral responses of hatchling painted turtles (Chrysemys picta) and snapping turtles (Chelydra serpentina) at subzero temperatures. Journal of Thermal Biology 24: 161-166. | PDF

Costanzo, J. P., A. A. Allenspach and R. E. Lee. 1999. Electrophysiological and ultrastructural correlates of cryoinjury in sciatic nerve from the freeze-tolerant wood frog, Rana sylvatica. Journal of Comparative Physiology B 169: 351-359. | PDF

Costanzo, J. P., J. M. Bayuk and R. E. Lee. 1999. Inoculation by environmental ice nuclei in the freeze-tolerant wood frog, Rana sylvatica. Journal of Experimental Zoology 284: 7-14. | PDF

Layne, J. R., J. P. Costanzo and R. E. Lee. 1998. Freeze duration influences postfreeze survival in the frog Rana sylvatica. Journal of Experimental Zoology 290: 197-201. | PDF

Beesley, S. G., J. P. Costanzo and R. E. Lee. 1998. Cryopreservation of spermatozoa from freeze-tolerant and -intolerant anurans. Cryobiology 37: 155-162. | PDF

Costanzo, J. P., J. D. Litzgus, J. B. Iverson and R. E. Lee. 1998. Soil hydric characteristics and environmental ice nuclei influence supercooling capacity of hatchling painted turtles, Chrysemys picta. Journal of Experimental Biology 201: 3105-3112. | PDF

Costanzo, J. P., J. A. Mugnano, H. M. Wehrheim and R. E. Lee. 1998. Osmotic and freezing tolerance in spermatozoa of freeze-tolerant and -intolerant frogs. American Journal of Physiology 275: R713-R719. | PDF

Mugnano, J. A., J. P. Costanzo, S. G. Beesley and R. E. Lee. 1998. Evaluation of glycerol and dimethyl sulfoxide for the cryopreservation of spermatozoa from the wood frog (Rana sylvatica). CryoLetters 19: 249-254. | PDF

Costanzo, J. P., J. T. Irwin and R. E. Lee. 1997. Freezing impairment of male reproductive behaviors of the freeze-tolerant wood frog, Rana sylvatica. Physiological Zoology 70: 158-16. | PDF

Costanzo, J. P., P. A. Callahan, R. E. Lee and M. F. Wright. 1997. Frogs reabsorb glucose from urinary bladder. Nature 389: 343-344. | PDF

Layne, J. R., R. E. Lee and M. Cutwa. 1996. Post-hibernation excretion of glucose in urine of the freeze tolerant frog Rana sylvatica. Journal of Herpetology 30: 85-87. | PDF

Costanzo, J. P. and R. E. Lee. 1996. Mini-review: Ice nucleation in freeze-tolerant vertebrates. CryoLetters 17: 111-118. | PDF

Costanzo, J. P., R. E. Lee, A. L. DeVries, T. Wang and J. R. Layne. 1995. Survival mechanisms of vertebrate ectotherms at subfreezing temperatures: Applications in cryomedicine. FASEB Journal 9: 351-358. | PDF

Mugnano, J. A., T. Wang, J. R. Layne, A. L. DeVries and R. E. Lee. 1995. Antifreeze glycoproteins promote lethal intracellular freezing of rat cardiomyocytes at high subzero temperatures. American Journal of Physiology 269 (Regulatory Integrative Comparative Physiology 38): R474-479. | PDF

Costanzo, J. P., J. B. Iverson, M. F. Wright and R. E. Lee. 1995. Cold hardiness and overwintering strategies of hatchlings in an assemblage of northern turtles. Ecology 76: 1772-1785. | PDF

Costanzo, J. P., C. Grenot and R. E. Lee. 1995. Supercooling, ice inoculation, and freeze tolerance in the European common lizard, Lacerta vivipara. Journal of Comparative Physiology 165: 238-244. | PDF

Layne, J. R. and R. E. Lee. 1995. Adaptations of frogs to survive freezing. Climate Research 5: 53-59. | PDF

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1990-1994

Kling, K. B., J. P. Costanzo and R. E. Lee. 1994. Post-freeze recovery of peripheral nerve function in the freeze-tolerant wood frog, Rana sylvatica. Journal of Comparative Physiology 164: 316-320. | PDF

Costanzo, J. P. and R. E. Lee. 1994. Biophysical and physiological responses promoting freeze tolerance in vertebrates. News in Physiological Sciences 9: 252-256. | PDF

Costanzo, J. P. and R. E. Lee. 1993. Cryoprotectant production capacity in the freeze-tolerant wood frog, Rana sylvatica. Canadian Journal of Zoology 71: 71-75. | PDF

Costanzo, J. P., R. E. Lee and M. F. Wright. 1993. Physiological responses to freezing in the freeze-tolerant turtle, Terrapene carolina. Journal of Herpetology 27: 117-120. | PDF

Costanzo, J. P., R. E. Lee and P. H. Lortz. 1993. Glucose concentration regulates freeze tolerance in the wood frog Rana sylvatica. Journal of Experimental Biology 181: 145-155. | PDF

Costanzo, J. P., R. E. Lee and P. H. Lortz. 1993. Physiological responses of freeze-tolerant and intolerant frogs: Clues to evolution of anuran freeze tolerance. American Journal of Physiology 265 (Regulatory Integrative Comparative Physiology 34): R721-725. | PDF

Costanzo, J. P., M. F. Wright and R. E. Lee. 1992. Freeze tolerance as an overwintering adaptation in Cope's gray tree frog (Hyla chrysoscelis). Copeia 1992: 565-569. | PDF

Costanzo, J. P., R. E. Lee, and M. F. Wright. 1992. Cooling rate influences cryoprotectant distribution and organ dehydration in freezing wood frogs. Journal of Experimental Zoology 26: 373-378. | PDF

Lee, R. E., J. P. Costanzo, E. C. Davidson and J. R. Layne. 1992. Dynamics of body water during freezing and thawing in a freeze-tolerant frog (Rana sylvatica). Journal of Thermal Biology 17: 263-266. | PDF

Layne, J. R. and R. E. Lee. 1991. The importance of body tissue composition to calorimetric assessments of ice content in whole animals. Journal of Thermal Biology 16: 61-64. | PDF

Costanzo, J. P., R. E. Lee and M. F. Wright. 1991. Effect of cooling rate on the survival of frozen wood frogs, Rana sylvatica. Journal of Comparative Physiology B. 161: 225-229. | PDF

Costanzo, J. P., R. E. Lee and M. F. Wright. 1991. Glucose loading prevents freezing injury in rapidly cooled frogs. American Journal of Physiology 261 (Regulatory Integrative Comparative Physiology 30): R1549-1553. | PDF

Costanzo, J. P. and R. E. Lee. 1991. Freeze-thaw injury in erythrocytes of the freeze-tolerant wood frog, Rana sylvatica. American Journal of Physiology 261 (Regulatory Integrative Comparative Physiology 30): R1346-1350. | PDF

Claussen, D. L. and Costanzo, J. P. 1990. A simple model for estimating the ice content of freezing ectotherms. Journal of Thermal Biology 15: 223-231. | PDF

Costanzo, J. P. and D. L. Claussen. 1990. Natural freeze tolerance in the terrestrial turtle, Terrapene carolina. Journal of Experimental Zoology 254: 228-232. | PDF

Layne, J. R., R. E. Lee and J. L. Huang. 1990. Inoculation triggers freezing at high subzero temperatures in a freeze-tolerant frog (Rana sylvatica) and insect (Eurosta solidaginis). Canadian Journal of Zoology 68: 506-510. | PDF

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1985-1989

Costanzo, J. P. 1989. Conspecific scent trailing by garter snakes during autumn: further evidence for the use of pheromones in den location. Journal of Chemical Ecology 15: 2531-2538. | PDF

Costanzo, J. P. 1989. Effects of humidity, temperature, and submergence behavior on survivorship and energy use in hibernating garter snakes, Thamnophis sirtalis. Canadian Journal of Zoology 67: 2486-2492. | PDF

Costanzo, J. P. 1989. A physiological basis for prolonged submergence in hibernating garter snakes Thamnophis sirtalis: evidence for an energy-sparing adaptation. Physiological Zoology 62: 580-592. | PDF

Layne, R. E. and R. E. Lee. 1989. Seasonal variation in freeze tolerance and ice content of the tree frog Hyla versicolor. Journal of Experimental Zoology 249: 133-137. | PDF

Layne, J. R., R. E. Lee and T. L. Heil. 1989. Freezing-induced changes in the heart rate of wood frogs (Rana sylvatica). American Journal of Physiology 257 (Regulatory Integrative Comparative Physiology 26): R1046-R1049. | PDF

Costanzo, J. P., Claussen, D. L. and R. E. Lee. 1988. Natural freeze tolerance in a reptile. Cryo-Letters 9: 380-385. | PDF

Layne, J. R. and R. E. Lee. 1987. Freeze tolerance and the dynamics of ice formation in wood frogs (Rana sylvatica) from southern Ohio. Canadian Journal of Zoology 65: 2062-2065. | PDF

Costanzo, J. P. 1986. Influences of hibernaculum microenvironment on the winter life history of the garter snake, Thamnophis sirtalis. Ohio Journal of Science 86: 199-204. | PDF

Costanzo, J. P. 1985. The bioenergetics of hibernation in the eastern garter snake Thamnophis sirtalis sirtalis. Physiological Zoology 58: 682-692. | PDF

1980-1984

Costanzo, J. P. 1982. Heating and cooling rates of Terrapene ornata and Chrysemys picta in water. Bios 53: 159-166. | PDF

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