Physiology of hibernation under the ice by turtles and frogs

Journal of Experimental Zoology Part A: Ecological Genetics and Physiology

Volumn 313 A, Issue 6, 2010, Pages 311-327

  Jackson, Donald C ^a   Ultsch, Gordon R ^b  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ICE;

ANIMAL; ARTICLE; FROG; HIBERNATION; OXYGEN CONSUMPTION; PHYSIOLOGY; TURTLE;

ANIMALS; HIBERNATION; ICE; OXYGEN CONSUMPTION; RANIDAE; TURTLES;

ANURA; CHELYDRIDAE; CHRYSEMYS; TESTUDINES; VERTEBRATA;

EID: 77953529853     PISSN: 19325223     EISSN: 19325231     Source Type: Journal    
DOI: 10.1002/jez.603     Document Type: Article

References (132)

1. Ackerman RA, White FN. 1979. Cyclic carbon dioxide exchange in the turtle Pseudemys scripta. Physiol Zool 52:378-389.
2. Arnett T. 2003. Regulation of bone cell function by acid-base balance. Proc Nutr Soc 62:511-520.
3. Belkin DA. 1963. Anoxia: tolerance in reptiles. Science 139:492-493.
4. Belkin DA. 1964. Variation in heart rate during voluntary diving in the turtle Pseudemys concinna. Copeia 1964:321-330.
5. Belkin DA. 1968. Aquatic respiration and underwater survival of two freshwater turtle species. Respir Physiol 4:1-14.
6. Bickler PE, Buck LT. 2007. Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145-170.
7. Boutilier RG. 2001. Mechanisms of cell survival in hypoxia and hypothermia. J Exp Biol 204:3171-3181.
8. Boutilier RG, St Pierre J. 2002. Adaptive plasticity of skeletal muscle energetics in hibernating frogs: mitochondrial proton leak during metabolic depression. J Exp Biol 205:2287-2296.
9. Boutilier R, Donohoe PH, Tattersall GJ, West TG. 1997. Hypometabolic homeostasis in overwintering aquatic amphibians. J Exp Biol 200:387-400.
10. Bradford DF. 1983. Winterkill, oxygen relations and energy metabolism of a submerged dormant amphibian, Rana muscosa. Ecology 64:1171-1183.
11. Bradford DF. 1984. Water and osmotic balance in overwintering tadpoles and frogs, Rana muscosa. Physiol Zool 57: 474-480.
12. Brand M. 2003. Approximate yield of ATP from glucose, designed by Donald Nicholson. Biochem Mol Biol Educ 31:2-4.
13. Brenner FJ. 1969. The role of temperature and fat deposition in hibernation and reproduction in two species of frogs. Herpetologica 25:105-113.
14. Brenner FJ, Brenner PE. 1969. The influence of light and temperature on body fat and reproductive conditions of Rana pipiens. Ohio J Sci 69:305-312.
15. Buck LT, Land SC, Hochachka PW. 1993. Anoxia-tolerant hepatocytes: model system for study of reversible metabolic suppression. Am J Physiol 265:R49-R56.
16. Burggren WW, Moalli R. 1984. ''Active'' regulation of cutaneous gas exchange by capillary recruitment in amphibians: experimental evidence and a revised model for skin respiration. Respir Physiol 55:379-392.
17. Burggren WW, Shelton G. 1979. Gas exchange and transport during intermittent breathing in chelonian reptiles. J Exp Biol 82:75-92.
18. Bushinsky DA. 2001. Acid-base imbalance and the skeleton. Eur J Nutr 40:238-244.
19. Byrne JJ, White RJ. 1975. Cyclic changes in liver and muscle glycogen, tissue lipid, and blood glucose in a naturally occurring population of Rana catesbeiana. Comp Biochem Physiol A 50:709-715.
20. Christiansen J, Penney D. 1973. Anaerobic glycolysis and lactic acid accumulation in cold submerged Rana pipiens. J Comp Physiol 87:237-245.
21. Congdon JD, Tinkle DW. 1982. Reproductive energetics of the painted turtle (Chrysemys picta). Herpetologica 38:228-237.
22. Congdon JD, Dunham AE, Tinkle DW. 1982. Energy budgets and life histories of reptiles. In: Gans C, Pough FH, editors. Biology of the reptilia, Vol 13. New York: Academic Press. p 233-271.
23. Congdon JD, Dunham AE, van Loben Sels RD. 1994. Demographics of common snapping turtle (Chelydra serpentina): implications for conservation and management of long-lived organisms. Am Zool 34:397-408.
24. Congdon JD, Nagle RD, Kinney OM, Osentoski M, Avery HW, van Loben Sels RC, Tinkle DW. 2000. Nesting ecology and embryo mortality: implications for hatching success and demography of Blanding's turtles (Emydoidea blandingii). Chelonian Conserv Biol 3:569-579.
25. Crawford KM. 1994. Patterns of energy substrate utilization in overwintering painted turtles, Chrysemys picta. Comp Biochem Physiol A 109:495-502.
26. Crocker CE, Feldman RA, Ultsch GR, Jackson DC. 2000a. Overwintering behavior and physiology of eastern painted turtles (Chrysemys picta picta) in Rhode Island. Can J Zool 78:936-942.
27. Crocker CE, Graham TE, Ultsch GR, Jackson DC. 2000b. Physiology of common map turtles (Graptemys geographica) hibernating in the Lamoille River, Vermont. J Exp Zool (Mol Dev Evol) 286:143-148.
28. Czopek J. 1965. Quantitative studies on the morphology of respiratory surfaces in amphibians. Acta Anat 62:296-323.
29. Davis EC, Jackson DC. 2007. Lactate uptake by skeletal bone in anoxic turtles, Trachemys scripta. Comp Biochem Physiol A 146:299-304.
30. Daw JC, Wenger DP, Berne RM. 1967. Relationship between cardiac glycogen and tolerance to anoxia in the western painted turtle, Chrysemys picta bellii. Comp Biochem Physiol 22:69-73.
31. Donohoe PH, Boutilier RG. 1998. The protective effects of metabolic rate depression in hypoxic cold submerged frogs. Respir Physiol 111:325-336.
32. Donohoe PH, West TG, Boutilier RG. 1998. Respiratory, metabolic, and acid-base correlates of aerobic metabolic rate reduction in overwintering frogs. Am J Physiol 274:R704-R710.
33. Donohoe PH, West TG, Boutilier RG. 2000. Factors affecting membrane permeability and ionic homeostasis in the coldsubmerged frog. J Exp Biol 203:405-414.
34. Dunson WA. 1960. Aquatic respiration in Trionyx spinifer asper. Herpetologica 16:277-283.
35. Elmberg J. 1990. Long-term survival, length of breeding season, and operational sex ratios in a boreal population of common frogs, Rana temporaria L. J Zool 68:121-127.
36. Emerson DN. 1967. Preliminary study on seasonal liver lipids and glycogen, and blood sugar levels in the turtle Graptemys pseudogeographica (Gray) from South Dakota. Herpetologica 23:68-70.
37. Feder ME, Burggren WW. 1985. Cutaneous gas exchange in vertebrates: design, patterns, control and implications. Biol Rev 60:1-45.
38. Galbraith DA, Brooks RJ. 1987. Survivorship of adult females in a northern population of common snapping turtles, Chelydra serpentina. Can J Zool 65:1581-1586.
39. Gatten RE. 1981. Anaerobic metabolism in freely diving painted turtles (Chrysemys picta). J Exp Zool (Mol Dev Evol) 216:377-385.
40. Gatz RN, Crawford EC, Piiper J. 1975. Kinetics of inert gas equilibration in an exclusively skin-breathing salamander, Desmognathus fuscus. Respir Physiol 24:15-29.
41. Gordos MA, Franklin CE. 2002. Diving behavior of two bimodally respiring turtles, Rheodytes leukops and Emydura macquarii, in a natural setting. J Zool 258:335-342.
42. Graham TE, Butler BO. 1993. Metabolic rates of wintering Blanding's turtles, Emydoidea blandingii. Comp Biochem Physiol A 106: 663-665.
43. Graham TE, Forsberg JE. 1991. Aquatic oxygen uptake by naturally hibernating wood turtles Clemmys insculpta. Copeia 1991: 836-838.
44. Graham TE, Graham AA. 1992. Metabolism and behavior of wintering common map turtles, Graptemys geographica, in Vermont. Can Field Nat 106:517-519.
45. Graham TE, Guimond RW. 1995. Aquatic oxygen consumption by wintering red-bellied turtles. J Herpetol 29:471-474.
46. Guppy M, Withers PC. 1999. Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 74:1-40.
47. Herbert CV, Jackson DC. 1985a. Temperature effects on the responses to prolonged submergence in the turtle Chrysemys picta bellii. I. Blood acid-base and ionic changes during and following anoxic submergence. Physiol Zool 58:655-669.
48. Herbert CV, Jackson DC. 1985b. Temperature effects on the responses to prolonged submergence in the turtle Chrysemys picta bellii. II. Metabolic rate, blood acid-base and ionic changes, and cardiovascular function in aerated and anoxic water. Physiol Zool 58: 670-681.
49. Hochachka PW. 1982. Anaerobic metabolism: living without oxygen. In: Taylor CR, Johansen K, Bolis L, editors. A companion to animal physiology. Cambridge, UK: Cambridge University Press. p 138-150.
50. Hochachka PW, Mommsen TP. 1983. Protons and anaerobiosis. Science 219:1391-1397.
51. Hochachka PW, Somero GN. 2002. Biochemical adaptation: mechanisms and process in physiological evolution. Oxford: Oxford University Press
52. Hochachka PW, Buck LT, Doll CJ, Land SC. 1996. Unifying theory of hypoxic tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93:9493-9498.
53. Hulse AC, McCoy CJ, Censky EJ. 2001. Amphibians and reptiles of Pennsylvania and the Northeast. Ithaca, New York: Cornell University Press.
54. Hutchison VH, Whitford WG, Kohl M. 1968. Relation of body size and surface area to gas exchange in anurans. Physiol Zool 41: 65-85.
55. Iverson JB. 1984. Proportional skeletal mass in turtles. Florida Sci 47: 1-11.
56. Jackson DC. 1968. Metabolic depression and oxygen depletion in the diving turtle. J Appl Physiol 24: 503-509.
57. Jackson DC. 1997. Lactate accumulation in the shell of the turtle, Chrysemys picta bellii, during anoxia at 3 and 101C. J Exp Biol 200:2295-2300.
58. Jackson DC. 2000. Living without oxygen: lessons from the freshwater turtle. Comp Biochem Physiol A. 125:299-315.
59. Jackson DC. 2002. Hibernating without oxygen: physiological adaptations of the painted turtle. J Physiol 543:731-737.
60. oC: the role of calcium lactate formation. Respir Physiol 49:159-174.
61. Jackson DC, Heisler N. 1983. Intracellular and extracellular acid-base and electrolyte status of submerged anoxic turtles at 31C. Respir Physiol 53: 187-201.
62. Jackson DC, Heisler N. 1984. The contribution of the alkaline pericardial fluid of freshwater turtles to acid buffering during prolonged anoxia. J Exp Biol 109:55-62.
63. Jackson DC, Silverblatt H. 1974. Respiration and acid-base status of turtles following experimental dives. Am J Physiol 226:903-909.
64. Jackson DC, Ultsch GR. 1982. Long-term submergence at 31C of the turtle, Chrysemys picta bellii, in normoxic and severely hypoxic water. II. extracellular ionic responses to extreme lactic acidosis. J Exp Biol 96:29-43.
65. Jackson DC, Toney VI, Okamoto S. 1996. Lactate distribution and metabolism during and after anoxia in the turtle, Chrysemys picta bellii. Am J Physiol 271:R409-R416.
66. Jackson DC, Goldberger Z, Visuri S, Armstrong RN. 1999. Ionic exchanges of turtle shell in vitro and their relevance to shell function in the anoxic turtle. J Exp Biol 202:513-520.
67. Jackson DC, Crocker CE, Ultsch GR. 2000a. Bone and shell contribution to lactic acid buffering of submerged turtles Chrysemys picta bellii at 31C. Am J Physiol 278:R1564-R1571.
68. Jackson DC, Ramsey AL, Paulson JM, Crocker CE, Ultsch GR. 2000b. Lactic acid buffering by bone and shell in anoxic softshell and painted turtles. Physiol Biochem Zool 73:290-297.
69. Jackson DC, Crocker CE, Ultsch GR. 2001a. Mechanisms of homeostasis during long term diving and anoxia in turtles. Zoology-Anal Complex Sy 103:150-156.
70. Jackson DC, Wang T, Koldkjaer P, Taylor EW. 2001b. Lactate sequestration in the carapace of the crayfish Austropotamobius pallipes during exposure in air. J Exp Biol 204:941-946.
71. Jackson DC, Andrade DV, Abe AS. 2003. Lactate sequestration by osteoderms of the broad-nose caiman, Caiman latirostris, following capture and forced submergence. J Exp Biol 206:3601-3606.
72. Jackson DC, Rauer EM, Feldman RA, Reese SA. 2004. Avenues of extrapulmonary oxygen uptake in western painted turtles (Chrysemys picta bellii) at 101C. Comp Biochem Physiol A 139:221-227.
73. Jackson DC, Taylor SE, Asare VS, Villarnovo D, Gall JM, Reese SA. 2007. Comparative shell buffering properties correlate with anoxia tolerance in freshwater turtles. Am J Physiol 292:R1008-R1015.
74. Jiang S, Claussen DL. 1992. A bioenergetic budget for overwintering newts (Notophthalmus viridescens) from southern Ohio: their fat reserves and aerobic metabolic rates in water. Comp Biochem Physiol A 101:743-750.
75. Kelly DA, Storey KB. 1988. Organ-specific control of glycolysis in anoxic turtles. Am J Physiol 255:R774-R779.
76. King P, Heatwole H. 1994. Partitioning of aquatic oxygen uptake among different respiratory surfaces in a freely diving pleurodiran turtle, Elseya latisternum. Copeia 1994:802-806.
77. Knickerbocker DL, Lutz PL. 2001. Slow ATP loss and the defense of ion homeostasis in the anoxic frog brain. J Exp Biol 204:3547-3551.
78. Koskela P, Pasanen S. 1974. The wintering of the common frog, Rana temporaria L. in northern Finland. Aquilo Ser Zool 15:1-7.
79. Lannoo M, Gallant AL, Nanjappa P, Blackburn L, Hendricks R. 2005. Species accounts. In: Lannoo M, editor. Amphibian declines: the conservation status of United States species. Berkeley, CA: University of California Press. p. 349-914.
80. Leivestad H. 1960. The effect of prolonged submersion on the metabolism and the heart rate in the toad (Bufo bufo). Univ Bergen Arbok Naturvitenskop Rekke 5:1-15.
81. Licht LE. 1991. Habitat selection of Rana pipiens and Rana sylvatica during exposure to warm and cold temperatures. Am Midl Nat 125:259-268.
82. Lutz PL, Rosenthal M, Sick TJ. 1985. Living without oxygen: turtle brain as a model of anaerobic metabolism. Mol Physiol 8:411-425.
83. Manion JJ, Cory L. 1952. Winter kill of Rana pipiens in shallow ponds. Herpetologica 8:32.
84. Martof B. 1956. Growth and development of the green frog, Rana clamitans, under natural conditions. Am Midl Nat 55:101-117.
85. Merrell DJ. 1977. Life history of the leopard frog, Rana pipiens, in Minnesota. Occas Pap Bell Mus Nat Hist Univ Minne 15:1-23.
86. Milton SL. 2008. The physiology and anatomy of anoxia tolerance in the freshwater turtle brain. In: Wyneken J, Godfrey MW, Bels V, editors. Biology of turtles. Boca Raton FL: CRC Press. p 301-344.
87. Partata WA, Marques M. 1994. Effects of fasting and seasonal variations in brain glycogen disposition in the turtle (Chrysemys dorbigni). Comp Biochem Physiol A 107:727-730.
88. Pasanen S, Koskela P. 1974. Seasonal and age variation in the metabolism of the common frog, Rana temporaria L., in Northern Finland. Comp Biochem Physiol A 47:635-654.
89. Penney DG. 1974. Effects of prolonged diving anoxia on the turtle Pseudemys scripta elegans. Comp Biochem Physiol A 47: 933-941.
90. Peterson CC, Greenfields D. 2001. Negative test for cloacal drinking in a semi-aquatic turtle (Trachemys scripta) with comments on the functions of cloacal bursae. J Exp Zool (Mol Dev Evol) 290: 247-254.
91. Pinder AW. 1987. Cutaneous diffusing capacity increases during hypoxia in cold submerged bullfrogs (Rana catesbeiana). Respir Physiol 70:85-95.
92. Pinder AW, Storey KB, Ultsch GR. 1992. Estivation and hibernation. In: Feder ME, Burggren WW, editors. Environmental physiology of the amphibians. Chicago: The University of Chicago Press. p 250-274.
93. Poyart CF, Bursaux E, Fréminet A. 1975. The bone CO2 compartment: evidence for a bicarbonate pool. Respir Physiol 25:89-99.
94. 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.
95. 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.
96. Reese SA, Jackson DC, Ultsch GR. 2003. Hibernation in freshwater turtles: softshell turtles (Apalone spinifera) are the most intolerant of anoxia among northern North American species. J Comp Physiol B 173:263-268.
97. Reese SA, Stewart ER, Crocker CE, Jackson DC, Ultsch GR. 2004. Geographic variation of the physiological response to overwintering in the painted turtle (Chrysemys picta). Physiol Biochem Zool 77:619-630.
98. Reeves RB. 1963. Control of glycogen utilization and glucose uptake in the anaerobic turtle heart. Am J Physiol 205:23-29.
99. Robin ED, Vester JW, Murdaugh HV, Millen JE. 1964. Prolonged anaerobiosis in a vertebrate: anaerobic metabolism in the freshwater turtle. J Cell Comp Physiol 63:287-297.
100. Robin ED, Robin DA, Ackerman R, Lewiston N, Hance AJ, Caligiuri M, Theodore J. 1981. Prolonged diving and recovery in the freshwater turtle, Pseudemys scripta-I. lung and blood gases, pH, lactate concentrations and ''cation'' gap. Comp Biochem Physiol 70A:359-364.
101. Schulz C, Thuy M, Wegener G. 1991. Heat production of frogs under normoxic and hypoxic conditions: a microcalorimetric study using a gas flow system. Thermochim Acta 187:71-78.
102. 31P-NMR study. Am J Physiol 272: R6-R15.
103. Simkiss K. 1968. Calcium and carbonate metabolism in the frog (Rana temporaria) during respiratory acidosis. Am J Physiol 214: 627-634.
104. Smith CL. 1950. Seasonal changes in blood sugar, fat body, liver glycogen, and gonads in the common frog, Rana temporaria. J Exp Biol 26:412-429.
105. Smith HW. 1929. The inorganic composition of the body fluids of the Chelonia. J Biol Chem 82:651-661.
106. Staples JF, Buck LT. 2009. Matching cellular metabolic supply and demand in energy-stressed animals. Comp Biochem Physiol A 153:95-105.
107. Stecyk JAW, Overgaard J, Farrell AP, Wang T. 2004. a-adrenergic regulation of systemic peripheral resistance and blood flow distribution in the turtle (Trachemys scripta). J Exp Biol 207: 269-283.
108. Stewart ER, Reese SA, Ultsch GR. 2004. The physiology of hibernation in Canadian leopard frogs (Rana pipiens) and bullfrogs (Rana catesbeiana). Physiol Biochem Zool 77:65-73.
109. Stewart PA. 1983. Modern quantitative acid-base chemistry. Can J Physiol Pharmacol 61:1442-1461.
110. Storey, KB. 1996. Metabolic adaptations supporting anoxia tolerance in reptiles: recent advances. Comp Physiol Biochem B 113:23-35.
111. Tattersall GJ, Boutilier RG. 1997. Balancing hypoxia and hypothermia in cold-submerged frogs. J Exp Biol 200:1031-1038.
112. Tattersall GJ, Boutilier RG. 1999a. Behavioural oxy-regulation by coldsubmerged frogs in heterogeneous oxygen environments. J Exp Biol 200:1031-1038.
113. Tattersall GJ, Boutilier RG. 1999b. Constant set points for pH and PCO2 in cold-submerged skin-breathing frogs. Respir Physiol 118:49-59.
114. Tattersall GJ, Ultsch GR. 2008. Physiological ecology of aquatic overwintering in ranid frogs. Biol Rev 83:119-140.
115. Ultsch GR. 1985. The viability of nearctic freshwater turtles submerged in anoxia and normoxia at 3 and 101C. Comp Biochem Physiol A 81:607-611.
116. Ultsch GR. 1988. Blood gases, hematocrit, plasma ion concentrations, and acid-base status of musk turtles (Sternotherus odoratus) during simulated hibernation. Physiol Zool 61:78-94.
117. Ultsch GR. 2006. The ecology of overwintering among turtles: where turtles overwinter and its consequences. Biol Rev 81: 339-367.
118. Ultsch GR, Cochran BM. 1994. Physiology of northern and southern musk turtles (Sternotherus odoratus) during simulated hibernation. Physiol Zool 67:263-281.
119. Ultsch GR, Jackson DC. 1982. Long-term submergence at 31C of the turtle, Chrysemys picta bellii, in normoxic and severely hypoxic water. I. survival, gas exchange and acid-base status. J Exp Biol 96:11-28.
120. Ultsch GR, Reese SA, Stewart ER. 2004. Physiology of hibernation in Rana pipiens: Metabolic rate, critical oxygen tension, and the effects of hypoxia on several plasma variables. J Exp Zool (Mol Dev Evol) 301A:169-176.
121. Wang ZX, Sun NZ, Sheng WF. 1989. Aquatic respiration in softshelled turtles, Trionyx sinensis. Comp Biochem Physiol A 92:593-598.
122. Warburton SJ. 1992. Calcium metabolism in anoxic poikilotherms: painted turtles (Chrysemys picta bellii) and bullfrogs (Rana catesbeiana). Ph.D. dissertation, Brown University.
123. Warburton SJ, Jackson DC. 1995. Turtle (Chrysemys picta bellii) shell mineral content is altered by exposure to prolonged anoxia. Physiol Zool 68:783-798.
124. Warren DE, Jackson DC. 2005. The role of mineralized tissue in the buffering of lactic acid during anoxia and exercise in the leopard frog, Rana pipiens. J Exp Biol 208:1117-1124.
125. Warren DE, Jackson DC. 2008. Lactate metabolism in anoxic turtles: an integrative review. J Comp Physiol B 178:133-148.
126. Warren DE, Reese SA, Jackson DC. 2006. The factors that limit survival of red-eared slider turtles, Trachemys scripta, during longterm anoxic submergence at 31C. Physiol Biochem Zool 79: 736-744.
127. Wasser JS, Jackson DC. 1988. Acid-base balance and the control of respiration during anoxic and anoxic-hypercapnic gas breathing in turtles. Respir Physiol 71:213-226.
128. Wasser JS, Warburton SJ, Jackson DC. 1991. Extracellular and intracellular acid-base effects of submergence anoxia and nitrogen breathing in turtles. Respir Physiol 83:239-252.
129. Wegener G, Krause U. 1993. Environmental and exercise anaerobiosis in frogs. In: Hochachka PW, Lutz PL, Sick T, Rosenthal M, van den Thillart G, editors. Surviving hypoxia: mechanisms of control and adaptation. Boca Raton, FL: CRC Press. p 217-236.
130. West TG, Boutilier RG. 1998. Metabolic suppression in anoxic frog muscle. J Comp Physiol B 168:273-280.
131. Wilbur HM. 1975. Evolutionary and mathematical demography of turtle Chrysemys picta. Ecology 56:64-77.
132. Willis YL, Moyle DL, Baskett TS. 1956. Emergence, breeding, hibernation, movements and transformation of the bullfrog, Rana catesbeiana, in Missouri. Copeia 1956:30-41.