Adaptations to terrestrial overwintering of hatchling northern map turtles, Graptemys geographica
Abstract
We conducted a 3-year field and laboratory study of winter biology in hatchlings of the northern map turtle (Graptemys geographica). At our study area in northern Indiana, hatchlings routinely overwintered in their natal nests, emerging after the weather warmed in spring. Winter survival was excellent despite the fact that hatchlings were exposed frequently to subfreezing temperatures (to −5.4 °C). In the laboratory, cold-acclimated hatchlings exhibited low rates of evaporative water loss (mean=2.0 mg g−1 day−1), which would enable them to conserve body water during winter. Laboratory-reared hatchlings were intolerant of freezing at −2.5 °C for 24 h, conditions that are readily survived by freeze-tolerant species of turtles. Winter survival of hatchling G. geographica probably depended on their extensive capacity for supercooling (to −14.8 °C) and their well-developed resistance to inoculative freezing, which may occur when hatchlings contact ice and ice-nucleating agents present in nesting soil. Supercooled hatchlings survived a brief exposure to −8 °C. Others, held at −6 °C for 5 days, maintained ATP concentrations at control levels, although they did accumulate lactate and glucose, probably in response to tissue hypoxia. Therefore, anoxia tolerance, as evidenced by the viability of hatchlings exposed to N2 gas for 8 days, may promote survival during exposure to subfreezing temperatures.
Keywords
Dehydration Freeze tolerance Supercooling Anoxia Inoculative freezingAbbreviations
- EWL
evaporative water loss
- FPeq
equilibrium freezing point
- INA
ice-nucleating agents
- Tc
temperature of crystallization
Notes
Acknowledgements
We are grateful to P. Meyer and S. Rock for assistance with the field portion of this study, and to J. Flynn for advice on the experimental design and statistical analyses. We thank two anonymous reviewers for providing constructive comments on the manuscript. This project was conducted in partial fulfillment of the requirements for the M.S. degree, Department of Zoology, Miami University, awarded to P. Baker. Experimental procedures were approved by the Institutional Animal Care and Use Committee of Miami University (protocol 466). Financial support was provided by the National Science Foundation (IBN 98017087) and the Miami University Summer Research Fund.
References
- Bickham JW, Lamb T, Minx P, Patton JC (1996) Molecular systematics of the genus Clemmys and the intergeneric relationships of the emydid turtles. Herpetologica 52:89–97Google Scholar
- Breckenridge W (1944) Reptiles and amphibians of Minnesota. University of Minnesota Press, Minneapolis, pp 202Google Scholar
- Cahn AR (1937) The turtles of Illinois. Illinois Biological Monographs, University of Illinois, Urbana, pp 218Google Scholar
- Churchill TA, Storey KB (1992a) Natural freezing survival by painted turtles Chrysemys picta marginata and C. picta bellii. Am J Physiol 262:R530–R537PubMedGoogle 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 167:221–233PubMedGoogle Scholar
- Claussen DL, Kim Y (1993) The effects of cooling, freezing, and thawing on cardiac and skeletal muscle of the turtle, Chrysemys picta. J Therm Biol 18:91–101CrossRefGoogle Scholar
- Costanzo JP, Claussen DL (1990) Natural freeze tolerance in the terrestrial turtle, Terrapene carolina. J Exp Zool 254:228–232Google Scholar
- Costanzo JP, Iverson JB, Wright MF, Lee RE (1995) Cold hardiness and overwintering strategies of hatchlings in an assemblage of northern turtles. Ecology 76:1772–1785Google Scholar
- Costanzo JP, Litzgus JD, Iverson JB, Lee RE (1998) Soil hydric characteristics and environmental ice nuclei influence supercooling capacity of hatchling painted turtles, Chrysemys picta. J Exp Biol 201:3105–3112PubMedGoogle Scholar
- Costanzo JP, Litzgus JD, Iverson JB, Lee RE (2000a) Ice nuclei in soil compromise cold hardiness of hatchling painted turtles, Chrysemys picta. Ecology 81:346–360Google Scholar
- Costanzo JP, Litzgus JD, Iverson JB, Lee RE (2000b) Seasonal changes in physiology and development of cold hardiness in the hatchling painted turtle, Chrysemys picta. J Exp Biol 203:3459–3470PubMedGoogle Scholar
- Costanzo JP, Jones EE, Lee RE (2001a) Physiological responses to supercooling and hypoxia in the hatchling painted turtle, Chrysemys picta. J Comp Physiol B 171:335–340CrossRefPubMedGoogle Scholar
- Costanzo JP, Litzgus JD, Iverson JB, Lee RE (2001b) Cold-hardiness and evaporative water loss in hatchling turtles. Physiol Biochem Zool 74:510–519CrossRefPubMedGoogle Scholar
- Costanzo JP, Litzgus JD, Larson JL, Iverson JB, Lee RE (2001c) Characteristics of nest soil, but not geographic origin, influence cold hardiness of hatchling painted turtles. J Therm Biol 26:65–73CrossRefPubMedGoogle Scholar
- Costanzo JP, Baker PJ, Dinkelacker SA, Lee RE (2003) Endogenous and exogenous ice-nucleating agents constrain supercooling in the hatchling painted turtle. J Exp Biol 206:477–485CrossRefPubMedGoogle Scholar
- Ewert MA, Legler JM (1978) Hormonal induction of oviposition in turtles. Herpetologica 34:314–318Google Scholar
- Gibbons JW, Nelson DH (1978) The evolutionary significance of delayed emergence from the nest by hatchling turtles. Evolution 32:297–303Google Scholar
- Gregory PT (1982) Reptilian hibernation. In: Gans C, Pough FH (eds) Biology of the Reptilia. Academic Press, New York, pp 53–154Google Scholar
- Hartley LM, Packard MJ, Packard GC (2000) Accumulation of lactate by supercooled hatchlings of the painted turtle (Chrysemys picta): implications for overwinter survival. J Comp Physiol B 170:45–50CrossRefPubMedGoogle Scholar
- Lee RE, Costanzo JP (1998) Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Ann Rev Physiol 60:55–72Google Scholar
- Mautz WJ (1982) Patterns of evaporative water loss. In: Gans C, Pough FH (eds) Biology of the Reptilia. Academic Press, New York, pp 443–482Google Scholar
- Nagy KA, Morafka DJ, Yates RA (1997) Young desert tortoise survival: energy, water, and food requirements in the field. Chelonian Conserv Biol 2:396–404Google Scholar
- Newman HH (1906) The habits of certain tortoises. J Comp Neurol Psychol 16:126–152Google Scholar
- Obbard ME, Brooks RJ (1981) Fate of overwintered clutches of the common snapping turtle (Chelydra serpentina) in Algonquin Park, Ontario. Can Field Nat 95:350–352Google Scholar
- Packard GC, Packard MJ (1999) Limits of supercooling and cold-tolerance in hatchling painted turtles (Chrysemys picta). Cryo Letters 20:55–60Google Scholar
- Packard GC, Packard MJ (2001) The overwintering strategy of hatchling painted turtles, or how to survive in the cold without freezing. Bioscience 51:199–207Google Scholar
- Packard GC, Ruble KA, Packard MJ (1993) Hatchling snapping turtles overwintering in natural nests are inoculated by ice in frozen soil. J Therm Biol 18:185–188CrossRefGoogle Scholar
- Packard GC, Packard MJ, Lang JW, Tucker JK (1999) Tolerance for freezing in hatchling turtles. J Herpetol 33:536–543Google Scholar
- Packard GC, Packard MJ, Lang JW (2000) Why hatchling Blanding's turtles don't overwinter inside their nest. Herpetologica 56:367–374Google Scholar
- Pappas MJ, Brecke BJ, Congdon JD (2000) The Blanding's turtles (Emydoidea blandingii) of Weaver Dunes, Minnesota. Chel Conserv Biol 3:557–568Google 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 130:331–340CrossRefGoogle Scholar
- Sims PA, Packard GC, Chapman PL (2001) The adaptive strategy for overwintering by hatchling snapping turtles (Chelydra serpentina). J Herpetol 35:514–517Google Scholar
- Storey KB, Storey JM (1996) Natural freezing survival in animals. Ann Rev Ecol Syst 27:365–386CrossRefGoogle Scholar
- Storey KB, Storey JM, Brooks SPJ, Churchill TA, Brooks RJ (1988) Hatchling turtles survive freezing during winter hibernation. Proc Natl Acad Sci USA 85:8350–8354PubMedGoogle Scholar
- Tucker JK, Paukstis GL (1999) Post-hatching substrate moisture and overwintering hatchling turtles. J Herpetol 33:608–615Google Scholar
- Ultsch GR (1989) Ecology and physiology of hibernation and overwintering among freshwater fishes, turtles, and snakes. Biol Rev 64:435–516Google 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 273:482–493Google Scholar
- Vogt RC (1980) Natural history of the map turtles Graptemys pseudogeographica and G. ouachitensis in Wisconsin. Tulane Stud Zool Bot 22:17–48Google Scholar
- Vogt RC (1981) Natural history of amphibians and reptiles in Wisconsin. Milwaukee Public Museum, Milwaukee, Wisconsin, pp 205Google Scholar
- Wilbur HM (1975) The evolutionary and mathematical demography of the painted turtle Chrysemys picta. Ecology 56:64–77Google Scholar
- Willard R, Packard GC, Packard MJ, Tucker JK (2000) The role of the integument as a barrier to penetration of ice into overwintering hatchlings of the painted turtle (Chrysemys picta). J Morph 246:150–159CrossRefPubMedGoogle Scholar
- Wilson DS, Nagy KA, Tracy CR, Morafka DJ, Yates RA (2001) Water balance in neonate and juvenile desert tortoises, Gopherus agassizii. Herpetol Monogr 15:158–170Google Scholar