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Anoxia tolerance and freeze tolerance in hatchling turtles

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Abstract

Freezing survival in hatchling turtles may be limited by ischemic anoxia in frozen tissues and the associated accumulation of lactate and reactive oxygen species (ROS). To determine whether mechanisms for coping with anoxia are also important in freeze tolerance, we examined the association between capacities for freezing survival and anoxia tolerance in hatchlings of seven species of turtles. Tolerance to freezing (−2.5°C) was high in Emydoidea blandingii, Chrysemys picta, Terrapene ornata, and Malaclemys terrapin and low in Graptemys geographica, Chelydra serpentina, and Trachemys scripta. Hatchlings survived in a N2 atmosphere at 4°C for periods ranging from 17 d (M. terrapin) to 50 d (G. geographica), but survival time was not associated with freeze tolerance. Lactate accumulated during both stresses, but plasma levels in frozen/thawed turtles were well below those found in anoxia-exposed animals. Activity of the antioxidant enzyme catalase in liver increased markedly with anoxia exposure in most species, but increased with freezing/thawing only in species with low freeze tolerance. Our results suggest that whereas oxygen deprivation occurs during somatic freezing, freeze tolerance is not limited by anoxia tolerance in hatchling turtles.

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References

  • Baker PJ, Costanzo JP, Iverson JB, Lee RE (2003) Adaptations to terrestrial overwintering of hatchling northern map turtles, Graptemys geographica. J Comp Physiol B 173:643–651

    Google Scholar 

  • Baker PJ, Costanzo JP, Herlands R, Wood RC, Lee RE (2004) A tolerance for freezing promotes winter survival of hatchlings of the northern diamondback terrapin, Malaclemys terrapin. Integrative and Comparative Biology 43:964 (abstract)

    Google Scholar 

  • Churchill TA, Storey KB (1991) Metabolic responses to freezing by organs of hatchling painted turtles Chrysemys picta marginata and C. p. bellii. Can J Zool 69:2978–2984

    Google Scholar 

  • Churchill TA, Storey KB (1992a) Natural freezing survival by painted turtles Chrysemys picta marginata and C. picta bellii. Am J Physiol 262:R530-R537

    Google Scholar 

  • Churchill TA, Storey KB (1992b) Responses to freezing exposure of hatchling turtles Trachemys scripta elegans: factors influencing the development of freeze tolerance by reptiles. J Exp Biol 167:221–233

    Google Scholar 

  • Costanzo JP, Iverson JB, Wright MF, Lee RE (1995) Cold hardiness and overwintering strategies of hatchlings in an assemblage of northern turtles. Ecology 76:1772–1785

    Google Scholar 

  • Costanzo JP, Litzgus JD, Iverson JB, Lee RE (2000) Seasonal changes in physiology and development of cold hardiness in the hatchling painted turtle, Chrysemys picta. J Exp Biol 203:3459–3470

    Google Scholar 

  • Costanzo JP, Dinkelacker SA, Iverson JB, Lee RE (2004) Physiological ecology of overwintering in the hatchling painted turtle: multiple-scale variation in response to environmental stress. Physiol Biochem Zool 77:74–99

    Google Scholar 

  • Crocker CE, Graham TE, Ultsch GR, Jackson DC (2000) Physiology of common map turtles (Graptemys geographica) hibernating in the Lamoille River, Vermont. J Exp Zool 286:143–148

    Google Scholar 

  • Dinkelacker SA, Costanzo JP, Iverson JB, Lee RE (2004) Cold-hardiness and dehydration resistance of hatchling Blanding’s turtles (Emydoidea blandingii): implications for overwintering in a terrestrial habitat. Can J Zool 82:594–600

    Google Scholar 

  • Dinkelacker SA, Costanzo JP, Iverson JB, Lee RE (2005) Survival and physiological responses of hatchling Blanding’s turtles (Emydoidea blandingii) to submergence in normoxic and hypoxic water under simulated winter conditions. Physiol Biochem Zool Accepted for publ

  • Donohoe PH, Boutilier RG (1999) The use of extracellular lactate as an oxidative substrate in the oxygen-limited frog. Respir Physiol 116:171–179

    Google Scholar 

  • Ferreira MVR, Alencastro ACR, Hermes-Lima M (2003) Role of antioxidant defenses during estivation and anoxia exposure in the freshwater snail Biomphalaria tenagophila (Orbigny, 1835). Can J Zool 81:1239–1248

    Google Scholar 

  • Fleck RA, Benson EE, Bremner DH, Day JG (2003) A comparative study of antioxidant protection in cryopreserved unicellular algae Euglena gracilis and Haematococcus pluvialis. Cryo-Lett 24:213–228

    Google Scholar 

  • Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Google Scholar 

  • Greenway SC, Storey KB (1999) Discordant responses of mitogen-activated protein kinases to anoxia and freezing exposures in hatchling turtles. J Comp Physiol B 169:521–527

    Google Scholar 

  • Hemmings SJ, Storey KB (2000) Hepatic changes in the freeze-tolerant turtle Chrysemys picta marginata in response to freezing and thawing. Cell Biochem Funct 18:175–186

    Google Scholar 

  • Hermes-Lima M, Storey KB (1993) Antioxidant defenses in the tolerance of freezing and anoxia by garter snakes. Am J Physiol 265:R646-R652

    Google Scholar 

  • Hermes-Lima M, Zenteno-Savin T (2002) Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp Biochem Physiol C 133:537–556

    Google Scholar 

  • Hermes-Lima M, Storey JM, Storey KB (1998) Antioxidant defenses and metabolic depression. The hypothesis of preparation for oxidative stress in land snails. Comp Biochem Physiol B 120:437–448

    Google Scholar 

  • Jackson DC (2000) How a turtle’s shell helps it survive prolonged anoxic acidosis. News Physiol Sci 15:181–185

    Google Scholar 

  • Joanisse DR, Storey KB (1996a) Oxidative damage and antioxidants in Rana sylvatica, the freeze tolerant wood frog. Am J Physiol 271:R545–553

    Google Scholar 

  • Joanisse DR, Storey KB (1996b) Oxidative stress and antioxidants in overwintering larvae of cold-hardy goldenrod gall insects. J Exp Biol 199:1483–1491

    Google Scholar 

  • Joanisse DR, Storey KB (1998) Oxidative stress and antioxidants in stress and recovery of cold-hardy insects. Ins Biochem Mole Biol 28:23–30

    Google Scholar 

  • Packard MJ, Packard GC (2004) Accumulation of lactate by frozen painted turtles (Chrysemys picta) and its relationship to freeze tolerance. Physiol Biochem Zool 77:433–439

    Google Scholar 

  • Packard GC, Packard MJ, Lang JW, Tucker JK (1999) Tolerance for freezing in hatchling turtles. J Herpetol 33:536–543

    Google Scholar 

  • Reese SA, Crocker CE, Carwile ME, Jackson DC, Ultsch GR (2001) The physiology of hibernation in common map turtles (Graptemys geographica). Comp Biochem Physiol A 130:331–340

    Google Scholar 

  • Reese SA, Jackson DC, Ultsch GR (2002) The physiology of overwintering in a turtle that occupies multiple habitats, the common snapping turtle (Chelydra serpentina). Physiol Biochem Zool 75:432–438

    Google Scholar 

  • Reese SA, Jackson DC, Ultsch GR (2003) Hibernation in freshwater turtles: softshell turtles (Apalone spinifera) are the most intolerant of anoxia among North American species. J Comp Physiol B 173:263–268

    Google Scholar 

  • Reese SA, Ultsch GR, Jackson DC (2004) Lactate accumulation, glycogen depletion, and shell composition of hatchling turtles under simulated aquatic hibernation. J Exp Biol 207:2889–2895

    Google Scholar 

  • Rifkind JM, Abugo O, Levy A, Monticone R, Heim J (1993) Formation of free radicals under hypoxia. In: Hochachka PW, Lutz PL, Sick T, Rosenthal M, Van den Thillart G (eds) Surviving Hypoxia: Mechanisms of Control and Adaptation. CRC, Boca Raton, pp 509–525

    Google Scholar 

  • Rubinsky B, Hong J-S, Storey KB (1994) Freeze tolerance in turtles: visual analysis by microscopy and magnetic resonance imaging. Am J Physiol 267:R1078-R1088

    Google Scholar 

  • Stephens PR, Wiens JJ (2003) Ecological diversification and phylogeny of emydid turtles. Biol J Linn Soc 79:577–610

    Google Scholar 

  • Storey KB, Storey JM (1988) Freeze tolerance in animals. Physiol Rev 68:27–84

    Google Scholar 

  • Storey KB, Storey JM, Brooks SPJ, Churchill TA, Brooks RJ (1988) Hatchling turtles survive freezing during winter hibernation. Proc Nat’l Acad Sci USA 85:8350–8354

    Google Scholar 

  • Ultsch GR, Jackson DC (1995) Acid-base status and ion balance during simulated hibernation in freshwater turtles from the northern portions of their ranges. J Exp Zool 273:482–493

    Google Scholar 

  • Ultsch GR, Reese SA (2005) Ecology and physiology of overwintering. In: Brooks RJ, Steyermark AC, Finkler MS (eds) The Biology of the Snapping Turtle. Smithsonian Institute Press, Washington D.C. (in press)

  • Willmore WG, Storey KB (1997) Glutathione systems and anoxia tolerance in turtles. Am J Physiol 273:R219-R225

    Google Scholar 

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Acknowledgements

Collecting permits were obtained from the Nebraska Game and Parks Commission, Indiana Department of Natural Resources, and New Jersey Division of Fish and Wildlife. Animal care and experimental procedures were approved by the Animal Care and Use Committee of Miami University in accordance with guidelines established by the U.S. Public Health Service. We thank P. Myer and the Connealy and Davis families for granting us permission to collect turtles on their lands. We also thank P. Baker for providing some of the hatchlings, and M. Elnitsky and L. Hayes for commenting on earlier drafts of the manuscript. This work was funded by grants from the NSF (IBN 98017087 and IBN 0416750) to JPC and by the Miami University Summer Workshop to SAD.

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Correspondence to S. A. Dinkelacker.

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Communicated by G. Heldmaier

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Dinkelacker, S.A., Costanzo, J.P. & Lee, R.E. Anoxia tolerance and freeze tolerance in hatchling turtles. J Comp Physiol B 175, 209–217 (2005). https://doi.org/10.1007/s00360-005-0478-0

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  • DOI: https://doi.org/10.1007/s00360-005-0478-0

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