Freezing tolerance of the European water frogs: The good, the bad, and the ugly

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 288, Issue 6 57-6, 2005, Pages

  Voituron, Yann ^a   Joly, Pierre ^a   Eugène, Michel ^b   Barré, Hervé ^a  

^a UNIVERSITÉ LYON 1   (France)

^b SAINT LOUIS HOSPITAL   (France)

Author keywords

Cold hardiness; Glucose; Ice content; Osmolality

Indexed keywords

GLUCOSE; GLYCOGEN; LACTIC ACID;

ANIMAL TISSUE; ARTICLE; BODY MASS; CHEMICAL ANALYSIS; COLD ACCLIMATIZATION; CONTROLLED STUDY; CRYOPROTECTION; FREEZING TOLERANCE; FROG; GLUCOSE BLOOD LEVEL; GLYCOGEN LIVER LEVEL; HIBERNATION; LACTATE BLOOD LEVEL; METABOLISM; NONHUMAN; OSMOLALITY; PRIORITY JOURNAL; SPECIES COMPARISON; SURVIVAL;

ANIMALS; BODY WATER; DEHYDRATION; FREEZING; GLYCOGEN; ICE; MAGNETIC RESONANCE SPECTROSCOPY; OSMOLAR CONCENTRATION; RANA ESCULENTA; RANA RIDIBUNDA; RANIDAE; SURVIVAL;

EID: 19444368748     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00711.2004     Document Type: Article

References (54)

1. Anholt BR, Hotz H, Guex GD, and Semlitsch RD. Annual variation in over-winter survival of the water frog Rana lessonae and its hemiclonal associate Rana esculenta. Ecology 84: 391-397, 2003.
2. Baust JB and Lee RE. Population differences in antifreeze/cryoprotectant accumulation patterns in an Antarctic insect. Oikos 40: 120-124, 1983.
3. Berger L. Embryonal and larval development of F1 generation of green frogs different combinations. Acta Zool 12: 123-124, 1967.
4. Berger L. Hibernation of the European water frogs (Rana esculenta complex). Zool Poloniae 29: 57-72, 1982.
5. Berger L. Morphology of the F1 generation of various crosses within Rana esculenta complex. Acta Zool 12: 321-324, 1968.
6. Bergmeyer HU. Methods of Enzymatic Analysis. Weinhem: VCH, 1985.
7. Byrne JJ and White RJ. Cyclic changes in liver and muscle glycogen tissue lipid and blood glucose in a naturally occurring population of Rana catesbeiana. Comp Biochem Physiol 50A: 709-715, 1975.
8. Civantos E, Salvador A, and Veiga JP. Body size and microhabitat affect winter survival of hatchling Psammodromus algirus lizards. Copeia 1999: 1112-1117, 1999.
9. Claussen DL and Zani PA. Allometry of cooling, supercooling, and freezing in the freeze-tolerant turtle Chrysemys picta. Am J Physiol Regul Integr Comp Physiol 261: R626-R632, 1991.
10. Colon L. L'hybridogénèse dans le Complexe Rana klepton esculenta. Apport des Marqueurs Génétiques (PhD thesis). Lyon, France: Lyon1 Univ., 2004.
11. Costanzo JP and Lee RE. Cryoprotectant production capacity of the freeze-tolerant wood frog, Rana sylvatica. Can J Zool 71: 71-75, 1993.
12. Costanzo JP and Lee RE. Supercooling and ice nucleation in vertebrate ectotherms. In: Biological Ice Nucleation and Its Applications, edited by Lee RE, Warren GJ, and Gusta LV. St. Paul, MN: Am. Phytopathol. Soc. Press, 1994.
13. Costanzo JP, Lee RE, and Lortz PH. Physiological responses of freeze-tolerant and intolerant frogs: clues to evolution of anuran freeze tolerance. Am J Physiol Regul Integr Comp Physiol 265: R721-R725, 1993.
14. Costanzo JP, Litzgus JD, Larson JL, Iverson JB, and Lee RE. Characteristics of nest soil, but not geographic origin, influence cold hardiness of hatchling painted turtles. J Therm Biol 26: 65-73, 2001.
15. Costanzo JP, Wright MF, and Lee RE. Freeze-tolerance as an overwintering adaptation in cope's gry treefrog (Hyla chrysoscelis). Copeia 2: 565-569, 1992.
16. Dziewulska-Szwajkowska D, Lozinzka-Gabska M, and Dzugaj A. Rana esculenta L. liver Fru-P2ase and G-6-Pase activity and Fru-2,6-P2 concentration after acclimation at 5 and 25°C. Comp Biochem Physiol A 118A: 745-751, 1997.
17. Graf JD and Polls Pelaz M. Evolutionary genetics of the Rana esculenta complex. In: Evolution and Ecology of Unisexual Vertebrates, edited by Dawley R and Bogart J. New York: New York State Museum, 1989, p. 289-301.
18. Grossenbacher K. Atlas de Distribution des Amphibiens de Suisse. Neuchatel, Switzerland: Musée d'Histoire Naturelle de Neuchatel, 1988.
19. Holenweg AK. Survival in adults of the water frog Rana lessonae and its hybridogenetic associate Rana esculenta. Can J Zool 79: 652-661, 2001.
20. Holenweg AK and Reyer HU. Hibernation behavior of Rana lessonae and R. esculenta in their natural habitat. Oecologia (Berl) 123: 41-47, 2000.
21. Joly P. The future of the selfish hemiclone: a neodarwinian approach of waterfrog evolution. Mitt Mus Natur Berlin 77: 31-38, 2001.
22. King PA, Rosholt MN, and Storey KB. Adaptations of plasma membrane glucose transport facilitate cryoprotectant distribution in freeze-tolerant frogs. Am J Physiol Regul Integr Comp Physiol 265: R1036-R1042, 1993.
23. Lada GA, Borkin LJ, and Vinogradov AE. Distribution, population systems and reproductive behavior of green frogs (hybridogenetic Rana esculenta complex) in the central Chernozem territory of Russia. Russian J Herpetol 2: 46-57, 1995.
24. Layne JR. Freeze tolerance and cryoprotectant mobilization in the gray treefrog (Hyla versicolor). J Exp Zool 283: 221-225, 1999.
25. Layne JR. Postfreeze survival and muscle function in the leopard frog (Rana pipiens) and the wood frog (Rana sylvatica). J Therm Biol 17: 121-124, 1992.
26. Layne JR and Jones AL. Freeze tolerance in the gray treefrog: cryoprotectant mobilization and organ dehydration. J Exp Zool 290: 1-5, 2001.
27. Layne JR and Lee RE. Freeze tolerance and the dynamics of ice formation in wood frogs (Rana sylvatica) from southern Ohio. Can J Zool 65: 2062-2065, 1987.
28. Layne JR and Lee RE. The importance of body tissue composition to calorimetric assessments of ice content in whole animals. J Therm Biol 16: 61-64, 1991.
29. Lynch M. Destabilizing hybridization, general-purpose genotypes and geographic parthenogenesis. Q Rev Biol 59: 257-285, 1984.
30. Morand A and Joly P. Habitat variability and space utilization by the amphibian communities of the French Upper-Rhône floodplain. Hydrobiologia 300-301: 249-257, 1995.
31. Packard GC and Janzen FJ. Interpopulational variation in the cold-tolerance of hatchling painted turtles. J Therm Biol 21: 183-190, 1996.
32. Pagano A, Crochet PA, Graf JD, Joly P, and Lodé T. Distribution and habitat use of water frog hybrid complexes in France. Global Ecol Biogeogr 10: 433-441, 2001.
33. Pagano A, Joly P, and Hotz H. Taxon compostion and genetic variation of water frogs in the Mid-Rhône floodplain. C R Acad Sci Serie III 320: 759-766, 1997.
34. Pagano A, Joly P, Plenet S, Lehman A, and Grolet O. Breeding habitat partitioning in the Rana esculenta complex: The intermediate niche hypothesis supported. Ecoscience 8: 294-300, 2001.
35. Peters RH. The Ecological Implications of Body Size. Cambridge, UK: Cambridge Univ. Press, 1983.
36. Plenet S, Hervant F, and Joly P. Ecology of the hybridogenetic Rana esculenta complex: differential oxygen requirements of tadpoles. Evol Ecol 14: 13-23, 2000.
37. Plenet S, Pagano A, Joly P, and Fouillet P. Variation of plastic responses to oxygen availability within the hybridogenetic Rana esculenta complex. J Evol Biol 13: 20-28, 2000.
38. Schmid W. Survival of frogs in low temperature. Science 215: 697-698, 1982.
39. Schmidt-Nielsen K. Animal Physiology: Adaptation and Environment. Cambridge, UK: Cambridge Univ. Press, 1979.
40. Semlitsch RD. Adaptive genetic variation in growth and development of tadpoles of the hybridogenetic Rana esculenta complex. Evolution 47: 1805-1818, 1993.
41. Semlitsch RD. Effects of different predators on the survival and development of tadpoles from the hybridogenetic Rana esculenta complex. Oikos 67: 40-46, 1993.
42. Semlitsch RD and Reyer HU. Performance of tadpoles from the hybridogenetic Rana esculenta complex: interactions with pond drying and interspecific competition. Evolution 46: 665-676, 1992.
43. Storey KB and Storey JM. Freeze tolerance and intolerance as strategies of winter survival in terrestrially-hibernating amphibians. Comp Biochem Physiol 83A: 613-617, 1986.
44. Storey KB and Storey JM. Freeze tolerance in animals. Physiol Rev 68: 27-84, 1988.
45. Storey KB and Storey JM. Freeze tolerant frogs: cryoprotectants and tissue metabolism during freeze-thaw cycles. Can J Zool 64: 49-56, 1986.
46. Storey KB and Storey JM. Persistence of freeze tolerance in terrestrially hibernating frogs after spring emergence. Copeia: 720-726, 1987.
47. Swanson DL, Graves BM, and Koster KL. Freezing tolerance/intolerance and cryoprotectant synthesis in terrestrially overwintering anurans in the great plains, USA. J Comp Physiol [B] 166: 110-119, 1996.
48. Tanaka K. Seasonal and latitudinal variation in supercooling ability of the house spider, Achaearanea tepidariorum (Araneae: Theridiidae). Funct Ecol 10: 185-192, 1996.
49. Tattersall GJ. Balancing hypoxia and hypothermia in cold-submerged frogs. J Exp Biol 200: 1031-1038, 1997.
50. Turner HG and Nopp H. Heterosis in the common European water frog. Naturwissenschaften 66: 268-269, 1979.
51. Vogiatzis AK and Loumbourdis NS. Exposure of Rana ridibunda to lead. II. Impact of lead on various parameters of liver metabolism of the frog Rana ridibunda. J Appl Toxicol 21: 269-274, 2001.
52. Voituron Y, Eugène M, and Barré H. Survival and metabolic responses to freezing by the water frog (Rana ridibunda). J Exp Zool 299A: 118-126, 2003.
53. Voituron Y, Heulin B, and Surget-Groba Y. Comparison of the cold hardiness capacities of the oviparous and viviparous forms of Lacerta vivipara. J Exp Zool 301A: 367-373, 2004.
54. Vorburger C. Consequence of Clonal Inheritance in the Hybridogenetic Water Frog Rana esculenta. Zurich: Univ. of Zurich, 2001.