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Hibernation and Gas Exchange

William K. Milsom, Donald C. Jackson

10.1002/cphy.c090018

Source: Volume 1, Issue 1, January 2011

Published online: January 2011

Full Article on Wiley Online Library



Abstract

Hibernation in endotherms and ectotherms is characterized by an energy‐conserving metabolic depression due to low body temperatures and poorly understood temperature‐independent mechanisms. Rates of gas exchange are correspondly reduced. In hibernating mammals, ventilation falls even more than metabolic rate leading to a relative respiratory acidosis that may contribute to metabolic depression. Breathing in some mammals becomes episodic and in some small mammals significant apneic gas exchange may occur by passive diffusion via airways or skin. In ectothermic vertebrates, extrapulmonary gas exchange predominates and in reptiles and amphibians hibernating underwater accounts for all gas exchange. In aerated water diffusive exchange permits amphibians and many species of turtles to remain fully aerobic, but hypoxic conditions can challenge many of these animals. Oxygen uptake into blood in both endotherms and ectotherms is enhanced by increased affinity of hemoglobin for O2 at low temperature. Regulation of gas exchange in hibernating mammals is predominately linked to CO2/pH, and in episodic breathers, control is principally directed at the duration of the apneic period. Control in submerged hibernating ectotherms is poorly understood, although skin‐diffusing capacity may increase under hypoxic conditions. In aerated water blood pH of frogs and turtles either adheres to alphastat regulation (pH ∼8.0) or may even exhibit respiratory alkalosis. Arousal in hibernating mammals leads to restoration of euthermic temperature, metabolic rate, and gas exchange and occurs periodically even as ambient temperatures remain low, whereas body temperature, metabolic rate, and gas exchange of hibernating ectotherms are tightly linked to ambient temperature. © 2011 American Physiological Society. Compr Physiol 1:397‐420, 2011.

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Figure 1. Figure 1.

Schematic diagram of the changes in body temperature (Tb), oxygen consumption (metabolic rate, O2), breathing frequency (fv), heart rate (fH), respiratory quotient (RQ), and oxygen pulse of a dormouse entering torpor at an ambient temperature of 5°C (horizontal line in upper panel). Data are modified and redrawn from Elvert and Heldmaier 48,49. The vertical lines demark the dramatic increase in metabolic rate and ventilation rate with a corresponding fall in the oxygen pulse that precede entrance into torpor.
Figure 2. Figure 2.

Changes in metabolic rate (TMR), core body temperature (Tcore), and torpor bout length (TBL) in arctic ground squirrels in steady‐state hibernation at different ambient temperatures. Symbols represent mean ± SE. From Barnes and Buck 2. Note the constant metabolic rate despite the differences in body temperature over the ambient temperature range from 0 to 16°C.
Figure 3. Figure 3.

Changes in the respiratory quotient (RQ), body temperature (Tb), and metabolic rate (MR) throughout one bout of daily torpor (approximately 5 h) in Peromyscus maniculatus. Note the dramatic drop in RQ at the onset of entrance into torpor and the rise in RQ at the onset of arousal. Redrawn from Nestler 160.
Figure 4. Figure 4.

Differential pressure recordings from a pneumotachograph illustrating the breathing pattern of golden‐mantled ground squirrels under various circumstances. The top three traces were taken during early entrance into hibernation (A), later during entrance into hibernation (B), and arousal from hibernation (C). The next three traces were taken from an animal in hibernation at 5°C (D), in hibernation at 2°C (E), and in hibernation at 5°C on 1% halothane anesthesia (F). The final two traces were taken during the early and late stages of a single bout of hibernation (one breathing episode from each trace is enlarged to show the details of the episode. (All traces are from Milsom; McArthur; Webb and Zimmer; unpublished.
Figure 5. Figure 5.

Respiratory airflow traces illustrating the breathing patterns of a golden‐mantled ground squirrel during progressive cooling in hypothermia. The panel on the right hand side of each trace is an expanded 30 s view of the second minute of the trace. From Zimmer and Milsom 237.
Figure 6. Figure 6.

Respiratory airflow traces illustrating the breathing patterns of golden‐mantled ground squirrels at the onset of arousal from hibernation under natural conditions and following administration of MK‐801 in a vagotomized animal. (Harris and Milsom, unpublished). Note the absence of episodic breathing in hibernation and the waxing and waning of ventilation during arousal following MK‐801 and vagotomy.
Figure 7. Figure 7.

(A) An example of a central neural arousal associated with a breathing episode in a ground squirrel hibernating at 5°C. Note the large burst of high‐frequency neural activity (top) and muscle activity (middle) during the first half of the breathing episode (bottom). Also note the tachycardia in the heart rate artifact present on both the electroencephalographic (EEG) and electromyography (EMG) traces. The effects of changing ambient temperature are also shown on the occurrence of central neural arousals with a breathing episode (B), the occurrence of breathing episodes with a central neural arousal (C) and the resting background level of EEG and EMG activity during steady‐state hibernation (D). From Zimmer and Milsom 236.
Figure 8. Figure 8.

Traces of O2 uptake and CO2 production in a hibernating dormouse at an ambient temperature of 5°C. Zero checks for both variables are shown at the beginning and end of the traces. Note the levels of oxygen consumption and CO2 production during the apneic periods. From Wilz et al. 233.
Figure 9. Figure 9.

(A) Effects of changing inspired O2 or CO2 on the air convection requirement (ΔVE/ΔVo2) of euthermic and hibernating Columbian and golden‐mantled ground squirrels expressed as the % change from air‐breathing values. From McArthur and Milsom 142. (B) The % change in ventilation (right axis) and arterial oxygen saturation (SaO2, left axis) as a function of arterial PO2 in intact and carotid body denervated (CBX) golden‐mantled ground squirrels during euthermia (right panel) and hibernation (left panel). Based on data in Webb and Milsom 229.
Figure 10. Figure 10.

Schematic representation of the changes occurring in heart rate (fH), stroke volume (SV), cardiac output (Q), total peripheral resistance (TPR), viscosity of peripheral (p), and central (c) arterial blood, as well as systolic, diastolic, and pulse pressure during entrance into hibernation of a hedgehog at 5°C. Based on data in Kirkebö 102.
Figure 11. Figure 11.

(A) The relationship between heart rate and body temperature during a consecutive entrance into and arousal from hibernation in a California ground squirrel; modified from Strumwasser 193. (B) Blood pressure of a thirteen‐lined ground squirrel entering hibernation. Thoracic temperature is 29.5°C, and skipped beats are evident. (C) Same animal 10 min after treatment with atropine. From Lyman and O'Brien 126. (D) Blood pressure and electroencephalographic of a thirteen‐lined ground squirrel entering hibernation. Thoracic temperature is 15°C and rhythmic asystoles are evident along with interpolated premature beats following each asystole. (E) At a thoracic temperature of 11°C, heart rate becomes uniform but extra systoles with no pulse pressure are still present. From Lyman and O'Brien 126.
Figure 12. Figure 12.

ECG and ventilatory airflow of a golden‐mantled ground squirrel at progressively lower temperatures. At 15°C (A) and 10°C (B) ventilation is accompanied by a tachycardia and periods of arrhythmia consisting of alternating tachycardia and bradycardia occur with increasing regularity throughout the apnea between breathing episodes. Over time at 5°C (C) both the arrhythmias and ventilation tachycardia disappear. (Heart rate is evident in the breathing traces in A and B). From Milsom et al. 156.
Figure 13. Figure 13.

Whole blood oxygen equilibrium curves for hibernating (open symbols) and summer active (filled symbols) ground squirrels generated at 7°C (pH 7.46) and 37°C (pH 7.49). Half saturation PO2 for winter and summer animals at 7°C was 5.8 ± 0.1 and 6.9 ± 0.2 Torr, respectively; P50 at 37°C were 15.3 ± 0.1 and 18.1 ± 0.5 Torr, respectively. Horizontal bars are ± 1 SEM; temperature coefficients (Δlog P50/ΔT°C) were calculated at blood pH 7.46 for the hibernator and pH 7.49 for the summer active squirrels. From Maginniss et al. 132.
Figure 14. Figure 14.

Reduction of aerobic metabolic rate of the frog Rana temporaria submerged in normoxic (aerated) water at 3°C for 90 days and in progressively hypoxic water for 90 days. From Donohoe and Boutilier 43.
Figure 15. Figure 15.

Arterial blood PCO2 of softshell turtles (Apalone spinifera) submerged in normoxic (aerated) water at 3°C for 220 days. Unpublished data from G.R. Ultsch and S.A. Reese.
Figure 16. Figure 16.

Total O2 consumption (solid line) and O2 supplied by extrapulmonary gas exchange in three species of freshwater turtles (dashed lines). Total O2 consumption and extrapulmonary uptake are based on data from the painted turtle (Chrysemys picta bellii); from Herbert and Jackson 87. Total O2 consumption is assumed to be the same in the other two species. Extrapulmonary uptake by the softshell turtle (Apalone spinifera) is an estimate but is based on the observation that this species can supply all its O2 by this pathway even at 10°C 217. Extrapulmonary uptake by the map turtle (Graptemys geographica) is also an estimate but is based on the observation that can supply all its O2 by this pathway at 3°C 172.
Figure 17. Figure 17.

Diagram depicting flux of O2 from surrounding aerated water into the blood and thence to the cells of a painted turtle submerged at 3°C (A). Because measured arterial blood PO2 is so low (∼1 torr), the gradient from the water to the blood and thus the diffusion resistance of this step are far greater than the gradient from the blood to the cells and the diffusion resistance of this step. Blood O2‐binding curve (B) Redrawn from Maginniss et al. 134 reveals that affinity for O2 is very high and that even at this low Po2, blood may have an O2 saturation of about 5 to 10%.
Figure 18. Figure 18.

The rate of O2 consumption of submerged adult frog (Rana pipiens) at 3°C as a function of PO2 of the water. Pc is the critical O2 tension. The constancy of O2 uptake down to water PO2 of below 40 torr provides evidence for the regulation of skin‐diffusing capacity in this animal. From Ultsch et al. 222.


Figure 1.

Schematic diagram of the changes in body temperature (Tb), oxygen consumption (metabolic rate, O2), breathing frequency (fv), heart rate (fH), respiratory quotient (RQ), and oxygen pulse of a dormouse entering torpor at an ambient temperature of 5°C (horizontal line in upper panel). Data are modified and redrawn from Elvert and Heldmaier 48,49. The vertical lines demark the dramatic increase in metabolic rate and ventilation rate with a corresponding fall in the oxygen pulse that precede entrance into torpor.



Figure 2.

Changes in metabolic rate (TMR), core body temperature (Tcore), and torpor bout length (TBL) in arctic ground squirrels in steady‐state hibernation at different ambient temperatures. Symbols represent mean ± SE. From Barnes and Buck 2. Note the constant metabolic rate despite the differences in body temperature over the ambient temperature range from 0 to 16°C.



Figure 3.

Changes in the respiratory quotient (RQ), body temperature (Tb), and metabolic rate (MR) throughout one bout of daily torpor (approximately 5 h) in Peromyscus maniculatus. Note the dramatic drop in RQ at the onset of entrance into torpor and the rise in RQ at the onset of arousal. Redrawn from Nestler 160.



Figure 4.

Differential pressure recordings from a pneumotachograph illustrating the breathing pattern of golden‐mantled ground squirrels under various circumstances. The top three traces were taken during early entrance into hibernation (A), later during entrance into hibernation (B), and arousal from hibernation (C). The next three traces were taken from an animal in hibernation at 5°C (D), in hibernation at 2°C (E), and in hibernation at 5°C on 1% halothane anesthesia (F). The final two traces were taken during the early and late stages of a single bout of hibernation (one breathing episode from each trace is enlarged to show the details of the episode. (All traces are from Milsom; McArthur; Webb and Zimmer; unpublished.



Figure 5.

Respiratory airflow traces illustrating the breathing patterns of a golden‐mantled ground squirrel during progressive cooling in hypothermia. The panel on the right hand side of each trace is an expanded 30 s view of the second minute of the trace. From Zimmer and Milsom 237.



Figure 6.

Respiratory airflow traces illustrating the breathing patterns of golden‐mantled ground squirrels at the onset of arousal from hibernation under natural conditions and following administration of MK‐801 in a vagotomized animal. (Harris and Milsom, unpublished). Note the absence of episodic breathing in hibernation and the waxing and waning of ventilation during arousal following MK‐801 and vagotomy.



Figure 7.

(A) An example of a central neural arousal associated with a breathing episode in a ground squirrel hibernating at 5°C. Note the large burst of high‐frequency neural activity (top) and muscle activity (middle) during the first half of the breathing episode (bottom). Also note the tachycardia in the heart rate artifact present on both the electroencephalographic (EEG) and electromyography (EMG) traces. The effects of changing ambient temperature are also shown on the occurrence of central neural arousals with a breathing episode (B), the occurrence of breathing episodes with a central neural arousal (C) and the resting background level of EEG and EMG activity during steady‐state hibernation (D). From Zimmer and Milsom 236.



Figure 8.

Traces of O2 uptake and CO2 production in a hibernating dormouse at an ambient temperature of 5°C. Zero checks for both variables are shown at the beginning and end of the traces. Note the levels of oxygen consumption and CO2 production during the apneic periods. From Wilz et al. 233.



Figure 9.

(A) Effects of changing inspired O2 or CO2 on the air convection requirement (ΔVE/ΔVo2) of euthermic and hibernating Columbian and golden‐mantled ground squirrels expressed as the % change from air‐breathing values. From McArthur and Milsom 142. (B) The % change in ventilation (right axis) and arterial oxygen saturation (SaO2, left axis) as a function of arterial PO2 in intact and carotid body denervated (CBX) golden‐mantled ground squirrels during euthermia (right panel) and hibernation (left panel). Based on data in Webb and Milsom 229.



Figure 10.

Schematic representation of the changes occurring in heart rate (fH), stroke volume (SV), cardiac output (Q), total peripheral resistance (TPR), viscosity of peripheral (p), and central (c) arterial blood, as well as systolic, diastolic, and pulse pressure during entrance into hibernation of a hedgehog at 5°C. Based on data in Kirkebö 102.



Figure 11.

(A) The relationship between heart rate and body temperature during a consecutive entrance into and arousal from hibernation in a California ground squirrel; modified from Strumwasser 193. (B) Blood pressure of a thirteen‐lined ground squirrel entering hibernation. Thoracic temperature is 29.5°C, and skipped beats are evident. (C) Same animal 10 min after treatment with atropine. From Lyman and O'Brien 126. (D) Blood pressure and electroencephalographic of a thirteen‐lined ground squirrel entering hibernation. Thoracic temperature is 15°C and rhythmic asystoles are evident along with interpolated premature beats following each asystole. (E) At a thoracic temperature of 11°C, heart rate becomes uniform but extra systoles with no pulse pressure are still present. From Lyman and O'Brien 126.



Figure 12.

ECG and ventilatory airflow of a golden‐mantled ground squirrel at progressively lower temperatures. At 15°C (A) and 10°C (B) ventilation is accompanied by a tachycardia and periods of arrhythmia consisting of alternating tachycardia and bradycardia occur with increasing regularity throughout the apnea between breathing episodes. Over time at 5°C (C) both the arrhythmias and ventilation tachycardia disappear. (Heart rate is evident in the breathing traces in A and B). From Milsom et al. 156.



Figure 13.

Whole blood oxygen equilibrium curves for hibernating (open symbols) and summer active (filled symbols) ground squirrels generated at 7°C (pH 7.46) and 37°C (pH 7.49). Half saturation PO2 for winter and summer animals at 7°C was 5.8 ± 0.1 and 6.9 ± 0.2 Torr, respectively; P50 at 37°C were 15.3 ± 0.1 and 18.1 ± 0.5 Torr, respectively. Horizontal bars are ± 1 SEM; temperature coefficients (Δlog P50/ΔT°C) were calculated at blood pH 7.46 for the hibernator and pH 7.49 for the summer active squirrels. From Maginniss et al. 132.



Figure 14.

Reduction of aerobic metabolic rate of the frog Rana temporaria submerged in normoxic (aerated) water at 3°C for 90 days and in progressively hypoxic water for 90 days. From Donohoe and Boutilier 43.



Figure 15.

Arterial blood PCO2 of softshell turtles (Apalone spinifera) submerged in normoxic (aerated) water at 3°C for 220 days. Unpublished data from G.R. Ultsch and S.A. Reese.



Figure 16.

Total O2 consumption (solid line) and O2 supplied by extrapulmonary gas exchange in three species of freshwater turtles (dashed lines). Total O2 consumption and extrapulmonary uptake are based on data from the painted turtle (Chrysemys picta bellii); from Herbert and Jackson 87. Total O2 consumption is assumed to be the same in the other two species. Extrapulmonary uptake by the softshell turtle (Apalone spinifera) is an estimate but is based on the observation that this species can supply all its O2 by this pathway even at 10°C 217. Extrapulmonary uptake by the map turtle (Graptemys geographica) is also an estimate but is based on the observation that can supply all its O2 by this pathway at 3°C 172.



Figure 17.

Diagram depicting flux of O2 from surrounding aerated water into the blood and thence to the cells of a painted turtle submerged at 3°C (A). Because measured arterial blood PO2 is so low (∼1 torr), the gradient from the water to the blood and thus the diffusion resistance of this step are far greater than the gradient from the blood to the cells and the diffusion resistance of this step. Blood O2‐binding curve (B) Redrawn from Maginniss et al. 134 reveals that affinity for O2 is very high and that even at this low Po2, blood may have an O2 saturation of about 5 to 10%.



Figure 18.

The rate of O2 consumption of submerged adult frog (Rana pipiens) at 3°C as a function of PO2 of the water. Pc is the critical O2 tension. The constancy of O2 uptake down to water PO2 of below 40 torr provides evidence for the regulation of skin‐diffusing capacity in this animal. From Ultsch et al. 222.

References
 1. Abe AS. Estivation in South American amphibians and reptiles. Brazil J Med Bio Res 28: 1241–1247, 1995.
 2. Barnes BM, Buck L. Hibernation in the extreme: Burrow and body temperatures, metabolism, and limits to torpor bout length in Arctic ground squirrels. In: Heldmaier G, Klingenspor M, editors. Life in the Cold. Heidelberg: Springer Verlag, 2000, p. 65–72.
 3. Barnes BM, Carey HV. Life in the Cold; Evolution, Mechanisms, Adaptation, and Application. Proceedings of the 12th International Hibernation Symposium. University of Alaska, Fairbanks; Institute of Arctic Biology, Fairbanks, Alaska, 2004.
 4. Barnes BM, Omtzigt C, Daan S. Hibernators periodically arouse in order to sleep. In: Carey C, Florant GL, Wunder B, Horwitz B, editors. Life in the Cold. Boulder, CO: Westview, 1993, p. 555–558.
 5. Barr RE, Silver IA. Oxygen tension in the abdominal cavity of hedgehogs during arousal from hibernation. Respir Physiol 16: 16–21, 1972.
 6. Barros RCH, Zimmer ME, Branco LGS, Milsom W.K. Hypoxic metabolic response of the golden‐mantled ground squirrel. J App Physiol 91: 603–61, 2001.
 7. Bartels H, Schmelzle R, Ulrich S. Comparative studies of the respiratory function of mammalian blood. V. Insectivora: Shrew, mole and non‐hibernating hedgehog. Respir Physiol 7: 278–286, 1969.
 8. Baudinette RV. Physiological correlates of burrow gas conditions in the California ground squirrel. Comp Biochem Physiol 48A: 733–743, 1974.
 9. Belkin DA. Anoxia: Tolerance in reptiles. Science 139: 492–493, 1963.
 10. Belkin DA. Aquatic respiration and underwater survival of two freshwater turtle species. Respir Physiol 4: 1–14, 1968.
 11. Bennett AF, Dawson WR. Metabolism. In: Gans C, Dawson WR, editors. Biology of the Reptilia. Vol. 5, Physiology A, New York: Academic Press, 1976, pp. 127–223.
 12. Bharma S, Milsom WK. Acidosis and metabolic rate in golden‐mantled ground squirrels (Spermophilus lateralis). Respir Physiol 94: 337–351, 1993.
 13. Bickler PE. CO2 balance of a heterothermic rodent: Comparison of sleep, torpor, and awake states. Am J Physiol 246: R49–R55, 1984.
 14. Biewald G‐A, Raths P. Die chronotrope Vaguswirkung auf das Hamsterherz unter dem Einfluss von Winterschlaf und Hypothermie. Pflügers Arch 268: 530–544, 1959.
 15. Biörck G, Johansson B, Schmid H. Reactions of hedgehogs, hibernating and non‐hibernating, to the inhalation of oxygen, carbon dioxide, and nitrogen. Acta Physiol Scand 37: 71–83, 1956.
 16. Birchard GF, Gobbs DF, Tenney SM. Effect of perinatal hypercapnia on the adult ventilatory response to carbon dioxide. Respir Physiol 57: 341–347, 1984.
 17. Boggs DF, Kilgore DL Jr, Birchard GF. Respiratory physiology of burrowing mammals and birds. Comp Biochem Physiol 77A: 1–7, 1984.
 18. Boggs DF. Hypoxic ventilatory control and hemoglobin oxygen affinity. In: Sutton JR, Houston CS, Coates G Jr, editors. Hypoxia and The Brain. Burlington, VT: Queen City Press, 1995, pp. 69–88.
 19. Boutilier RG, Donohoe PH, Tattersall GJ, West TG. Hypometabolic homeostasis in overwintering aquatic amphibians. J Exp Biol 200: 387–400, 1997.
 20. Boutilier RG, McDonald DG, Toews DP. The effects of enforced activity on ventilation, circulation and blood acid‐base balance in the aquatic gill‐less urodele, Cryptobranchus alleganiensis: A comparison with the semi‐terrestrial anuran, Bufo marinus. J Exp Biol 84: 289–302, 1980.
 21. Bullard RW, Funkhouser GE. Estimated regional blood flow by rubidium 86 distribution during arousal from hibernation. Am J Physiol 203: 266–270, 1962.
 22. Burggren WW, Moalli R. “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, 1984.
 23. Burlington RF, Darvish A. Low‐temperature performance of isolated working hearts from a hibernator and a non‐hibernator. Physiol Zool 61: 387–395, 1988.
 24. Burlington RF, Dean MS, Jones SB. Coronary autoregulation and metabolism in hypothermic rat and ground squirrel hearts. Am J Physiol 256: R357–R365, 1989.
 25. Burlington RF, Maher TJ, Sidel CM. Effect of hypoxia on blood gases, acid‐base balance and in vitro myocardial function in a hibernator and a non‐hibernator. Fed Proc 28: 1042–1046, 1969.
 26. Burlington RF, Milsom WK. The cardiovascular system in hibernating mammals: Recent advances. In: Malan M, Canguilhem B, editors. Living in the Cold II. Paris: Colloque INSERM: John Libbey Eurotext Ltd, pp. 235–242, 1989.
 27. Burlington RF, Milsom WK. Differential effects of acetylcholine on coronary flow in isolated hypothermic hearts from rats and ground squirrels. J Exp Biol 185: 17–24, 1993.
 28. Burlington RF, Whitten BK. Red cell 2,3‐diphosphoglycerate in hibernating ground squirrels. Comp Biochem Physiol 38A: 469–471, 1971.
 29. Caprette DR, Senturia JB. Isovolumetric performance of isolated ground squirrel and rat hearts at low temperature. Am J Physiol 247: R722–R727, 1984.
 30. Carey C, Florant GL, Wunder BA, Horowitz B. Life in the Cold: Ecological, Physiological and Molecular Mechanisms. Boulder: Westview Press, 1993.
 31. Carey HV, Andrews MT, Martin SL. Mammalian hibernation: Cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83: 1153–1181, 2003.
 32. Chapman RC, Bennett AF. Physiological correlates of burrowing in rodents. Comp Biochem Physiol 51A: 599–603, 1995.
 33. Chatfield PO, Lyman CP. Circulatory changes during process of arousal in the hibernating hamster. Am J Physiol 163: 566–574, 1950.
 34. Chatonnet F, Thoby‐Brisson M, Abadie V, Dominguez del TE, Champagnat J, Fortin G. Early development of respiratory rhythm generation in mouse and chick. Respir Physiol Neurobiol 131: 5–13, 2002.
 35. Clausen G. Acid‐base balance in the hedgehog Erinaceus europaeus L. during Hibernation, hypothermia, cooling and rewarming. Arbok Univ Bergen, Mat Naturvitensk Ser 6: 1–11, 1966.
 36. Clausen G, Ersland A. The respiratory properties of the blood of the hibernating hedgehog Erinaceus europaeus L. Respir Physiol 5: 221–233, 1968.
 37. Costanzo JP, Lee RE. Biophysical and physiological responses promoting freeze tolerance in vertebrates. News Physiol Sci 9: 252–256, 1994.
 38. Crocker CE, Graham TE,. Ultsch GR, Jackson DC. Physiology of common map turtles (Graptemys geographica) hibernating in the Lamoille River, Vermont. J Exp Zoo 286: 143–148, 2000.
 39. Darden TR. Respiratory adaptations of a fossorial mammal, the pocket gopher (Thomomys bottae). J Comp Physiol 78: 121–137, 1972.
 40. Dawe AR, Morrison PR. Characteristics of the hibernating heart. Am Heart J 49: 367–384, 1955.
 41. Dejours P. Principles of Comparative Respiratory Physiology. Amsterdam: Elsevier/North Holland Biomedical Press, 1981.
 42. Dolk HE, Postma N. Über die Haut und die Lungenatmung von Rana temporaria. Z Vergl Physiol 5: 417–444, 1927.
 43. Donohoe PH, Boutilier RG. The protective effects of metabolic rate depression in hypoxic cold submerged frogs. Respir Physiol 111: 325–336, 1998.
 44. Donohoe PH, West TG, Boutilier RG. Respiratory, metabolic, and acid‐base correlates of aerobic metabolic rate reduction in overwintering frogs. Am J Physiol 274: R704–R710l, 1998.
 45. Drew, KL, Harris MB, LaManna JC, Smith MA, Zhu XW, Ma YL Hypoxia tolerance in mammalian heterotherms. J Exp Biol 207: 3155–3162, 2004.
 46. Duker G, Sjoquist PO, Johansson BW. Monophasic action potentials during induced hypothermia in hedgehog and guinea pig heart. Am J Physiol 253: H1083–H1088, 1987.
 47. Eliassen E. Cardiovascular pressures in the hibernating hedgehog, with special regard to the pressure changes during arousal. Årbok for Universitetet I Bergen, Matematisk‐Naturvitenskapelig Serie No 6L: 1–27, 1960.
 48. Elvert R, Heldmaier G. Retention of carbon dioxide during entrance into torpor in dormice. In: Heldmaier G, Klingenspor M, editors. Life in the Cold. Heidelberg: Springer Verlag, 2000, p. 179–186.
 49. Elvert R, Heldmaier G. Cardiorespiratory and metabolic reactions during entrance into torpor in dormice, Glis glis. J Exp Biol 208: 1373–1383, 2005.
 50. Endres G. Observations on certain physiological processes of the marmot‐III, IV, and V. Proc Roy Soc Lond Ser B, 107: 241–247, 1930.
 51. Endres G, Taylor H. Observations on certain physiological processes of the marmot. II. The respiration. Proc Roy Soc Lond Ser B, 107: 230–240, 1930.
 52. Ernst CH. Temperature‐activity relationship in the painted turtle, Chrysemys picta. Copeia 1971: 217–222, 1972.
 53. Feder ME, Burggren WW. Cutaneous gas exchange in vertebrates: Design, patterns, control and implications. Biol Rev 60: 1–45, 1985.
 54. Feldman JL, Smith JC, Ellenberger HH, Connelly CA, Liu GS, Greer JJ, Lindsay AD, Otto MR. Neurogenesis of respiratory rhythm and pattern: Emerging concepts. Am J Physiol 259: R879–R886, 1990.
 55. Fong AY, Zimmer MB, Milsom WK. The conditional nature of the “Central Rhythm Generator” and the production of episodic breathing. Respir Physiol Neurobiol 168: 179–187, 2009.
 56. Fortin G, Champagnat J, Lumsden, A. Onset and maturation of branchio‐motor activities in the chick hindbrain. Neuroreport 5: 1149–1152, 1994.
 57. Frappell PB, Baudinette RV, MacFarlane PM, Wiggins PR, Shimmin G. Ventilation and metabolism in a large semifossorial marsupial: The effect of graded hypoxia and hypercapnia. Physiol Biochem Zool 75: 77–82, 2002.
 58. Frappell PB, Mortola JP. Hamsters vs. rats: Metabolic and ventilatory response to development in chronic hypoxia. J Appl Physiol 77: 2748–2752, 1994.
 59. Full RJ. Locomotion without lungs: Energetics and performance of a lungless salamander. Am J Physiol 251: R775–R780, 1986.
 60. Garland RJ, Milsom WK. End‐tidal gas composition is not correlated with episodic breathing in hibernating ground squirrels. Can J Zool 72: 1141–1148, 1994.
 61. Gatz RN, Crawford ED, Piiper J. Kinetics of inert gas equilibration in an exclusively skin‐breathing salamander, Desmognathus fuscus. Respir Physiol 24: 15–29, 1975.
 62. Geiser F. Reduction of metabolism during hibernation and daily torpor in mammals and birds: Temperature effect or physiological inhibition. J Comp Physiol B 158: 25–37, 1988.
 63. Glass ML, Boutilier RG, Heisler N. Ventilatory control of arterial P02 in the turtle Chrysemys picta bellii: Effects of temperature and hypoxia. J Comp Physiol B 151: 145–153, 1983.
 64. Goodrich CA. Acid‐base balance in euthermic and hibernating marmots. Am J Physiol 224: 1185–1189, 1973.
 65. Gordos M, Franklin CE. Diving behaviour of two Australian bimodally respiring turtles, Rheodytes leukops and Emydura macquarii, in a natural setting. J Zool (Lond) 258: 335–342, 2002.
 66. Gottlieb G, Jackson DC. The importance of pulmonary ventilation in respiratory control in the bullfrog. Am J Physiol 230: 608–613, 1976
 67. Greer JJ, Funk GD, Ballanyi K. Preparing for the first breath: Prenatal maturation of respiratory neural control. J Physiol 570: 437–444, 2006.
 68. Gubinov NF, Berkalo LV, Zhegunov GF, Utyevsky AM. Binding of [3H]‐dihydroalprenolol to plasma membranes of cardiac cells from a hibernator. Rep Ukranian SSR Acad Sci 3: 70–72, 1988.
 69. Guimond RW, Hutchison VH. The effect of temperature and photoperiod on gas exchange in the leopard frog, Rana pipiens. Comp Biochem Physiol 27: 177–195, 1968
 70. Hall FG. Hemoglobin and oxygen: Affinities in seven species of Sciuridae. Science 148: 1350–1351, 1965.
 71. Hammel HT, Dawson TJ Abrams RM, Andersen HT. Total calorimetric measurements on Citellus lateralis in hibernation. Physiol Zool 41: 341–357, 1968.
 72. Hanson A, Johansson BW. Myocardial lactate concentration in guinea pigs, normothermic and hypothermic, and hedgehogs, in a hibernating and nonhibernating state. Acta Physiol Scand 53: 137–14, 1961.
 73. Harkness DR, Roth S, Goldman P. Studies on the red blood cell oxygen affinity and 2,3‐diphosoglyceric acid in the hibernating woodchuck (Marmota monax). Comp Biochem Physiol 48A: 591–599, 1974.
 74. Harris MB, Milsom WK. The ventilatory response to hypercapnia in hibernating golden‐mantled ground squirrels. Physiol Zool 67: 739–755, 1994.
 75. Harris MB, Milsom WK. Parasympathetic influence on heart rate in euthermic and hibernating ground squirrels. J Exp Biol 198: 931–937, 1995.
 76. Harris MB, Milsom WK. Is hibernation facilitated by an inhibition of arousal? In: Heldmaier G, Klingenspor M, editors. Life In The Cold. Berlin: Springer‐Verlag, pp 241–250, 2000.
 77. Hatcher JD, Chiu LK, Jennings DB. Anemia is a stimulus to aortic and carotid chemoreceptors in the cat. J Appl Physiol 44: 696–702, 1978.
 78. Hays GC, Webb PI, Speakman JR. Arrhythmic breathing in torpid pipistrelle bats, Pipistrellus pipistrellus. Respir Physiol 85: 185–192, 1991.
 79. Hayward JD. Abnormal concentrations of respiratory gases in rabbit burrows. J Mammal 47: 723–724, 1966.
 80. Heistand WA, Rochold WT, Stemmler FW, Stullken DE, Wiebers JE. Comparative hypoxic resistance of hibernators and non‐hibernators. Physiol Zool 23: 264–269, 1950.
 81. Heldmaier G, Elvert R. How to enter torpor: Thermodynamic and physiological mechanisms of metabolic depression. In: Life in the Cold: Evolution, Mechanisms, Adaptation, and Application. Proceedings of the 12th International Hibernation Symposium. University of Alaska, Fairbanks; Institute of Arctic Biology, Fairbanks, Alaska. p. 185–198, 2004.
 82. Heldmaier G, Klinginspor M, Werneyer M, Lampi BJ, Brooks SP.J., Storey KB. Metabolic adjustments during daily torpor in the Djungarian hamster. Am J Physiol 276: E896–E906, 1999.
 83. Heldmaier G, Ruf T. Body temperature and metabolic rate during natural hypothermia in endotherms. J Comp Physiol B 162: 696–706, 1992.
 84. Heldmaier G, Steiger R, Ruf T. Suppression of metabolic rate in hibernation. In: Carey C, Florant GL, Wunder B, Horwitz B, editors. Life in the Cold: Ecological, Physiological, and Molecular Mechanisms. San Francisco: Westview Press, p. 545–548, 1993.
 85. Heller, HC. Hibernation: Neural aspects. Ann Rev Physiol 41: 305–321, 1979.
 86. Herbert CV, Jackson DC. 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, 1985a.
 87. Herbert CV, Jackson DC. 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, 1985b.
 88. Herreid CF, Bretz WL, Schmidt‐Nielsen K. Cutaneous gas exchange in bats. Am J Physiol 215: 506–508, 1968.
 89. Holloway DA, Heath AG. Ventilatory changes in the golden hamster, Mesocricetus auratus, compared with the laboratory rat, Rattus norvegicus during hypercapnia and/or hypoxia. Comp Biochem Physiol 77A: 267–273, 1984.
 90. Howell BJ, Baumgardner FW, Bondi K, Rahn H. Acid‐base balance in cold‐blooded vertebrates as a function of body temperature. Am J Physiol 218: 600–606, 1970.
 91. Hudson JW, Deavers DR. Metabolism, pulmocutaneous water loss and respiration of eight species of ground squirrels from different environments. Comp Biochem Physiol 45A: 69–100, 1973.
 92. Jackson DC. How a turtle's shell helps it survive prolonged anoxic acidosis. News Physiol Sci 15: 181–185, 2000.
 93. Jackson DC, Crocker CE, Ultsch GR. Bone and shell contribution to lactic acid buffering of submerged turtles Chrysemys picta bellii at 3°C. Am J Physiol 278: R1564–R1571, 2000.
 94. Jackson DC, Palmer SE, Meadow WL. The effects of temperature and carbon dioxide breathing on ventilation and acid‐base status of turtles. Respir Physiol 20: 131–146, 1974.
 95. Jackson DC, Rauer EM, Feldman RA, Reese SA. Avenues of extrapulmonary oxygen uptake in western painted turtles (Chrysemys picta bellii) at 10°C. Comp Biochem Physiol A 139: 221–227, 2004.
 96. Jackson DC, Ultsch GR. Physiology of hibernation under the ice by turtles and frogs. J Exp Zool 311A: 1–17, 2010.
 97. Johansen K, Krog J, Reite O. Autonomic nervous influence on the heart of hypothermic hibernator. Ann Acad Sci Fenn Ser A 71: 245–254, 1964.
 98. Johansson BW Jr. Heart and circulation in hibernators. In: Fisher KC, Dawe AR, Lyman CP, Schönbaum E, South FEJr, editors. Mammalian Hibernation III. New York: American Elsevier, p. 200–218, 1967.
 99. Jones SB, Romano FD. Functional characteristics and responses to adrenergic stimulation of isolated heart preparations from hypothermic and hibernating subjects. Cryobiology 21: 615–226, 1984.
 100. Kent KM, Pierce EC II. Acid‐base characteristics of hibernating animals. J Appl Physiol 23: 336–340, 1967.
 101. King P, Heatwole H. Partitioning of aquatic oxygen uptake among different respiratory surfaces in a freely diving pleurodian turtle, Elseya latisternum. Copeia 1994: 802–806, 1994.
 102. Kirkebö A. Cardiovascular investigations on hedgehogs during arousal from the hibernating state. Acta Physiol Scand 73: 394–406, 1968.
 103. Kramm C, Sattrup G, Baumann R, Bartels H. Respiratory function of blood in hibernating and non‐hibernating hedgehogs. Respir Physiol 25: 311–318, 1975.
 104. Kreienbuhl G, Strittmatter J, Ayim E. Blood gases of hibernating hamsters and dormice. Pflugers Arch 366: 67–172, 1976.
 105. Kristoffersson R, Soivio A. Hibernation in the hedgehog Erinaceus europaeus. Changes of respiratory pattern, heart rate and body temperature in response to gradually decreasing or increasing ambient temperature. Ann Acad Sci Fenn Ser A 4 82: 3–17, 1964.
 106. Kristoffersson R, Soivio A. Duration of hypothermia periods and type of respiration in the hibernating golden hamster, Mesocricetus auratus Waterh. Ann Zool Fenn 3: 66–67, 1966.
 107. Krogh A. On the cutaneous and pulmonary respiration of the frog. Skand Arch Physiol 15: 328–419, 1904.
 108. Kuhnen G. O2 and CO2 concentrations in burrows of euthermic and hibernating golden hamsters. Comp Biochem Physiol A 84: 517–522, 1986.
 109. Kuhnen G, Petersen P, Wünnenberg W. Hibernation in golden hamsters (Mesocricetus auratus, W.) exposed to 5% CO2. Experientia 39: 1346–1347, 1983.
 110. Lahiri S, Mulligan E, Nichino T, Mokashi A, Davies, RO. Relative responses of aortic body and carotid body chemoreceptors to carboxyhemoglobinemia. J Appl Physiol 50: 580–586, 1981.
 111. Landau BR, Dawe AR. Respiration in the hibernation of the 13‐lined ground squirrel. Am J Physiol 194: 75–82, 1958.
 112. Larkin EC, Simmond RC, Ulveda F, Williams WT. Responses of some hematological parameters of active and hibernating squirrels (Spermophilus mexicanus) upon exposure to hypobaric and isobaric hyperoxia. Comp Biochem Physiol 43A: 757–770, 1972.
 113. Larkin JE, Heller HC. Sleep after arousal from hibernation is not homeostatically regulated. Am J Physiol 276: R522–R529, 1999.
 114. Lee M, Choi I, Park K. Activation of stress signaling molecules in bat brain during arousal from hibernation. J Neurochem 82: 867–873, 2002.
 115. Leitner LM, Malan A. Possible role of the arterial chemoreceptors in the ventilatory responses of the anesthetized marmot to changes in inspired PO2 and PCO2. Comp Biochem Physiol 45A: 953–959, 1973.
 116. Lutz PL, Milton SL. Negotiating brain anoxia survival in the turtle. J Exp Biol 207: 3141–3147, 2004.
 117. Lyman CP. Effect of increased CO2 on respiration and heart rate of hibernating hamsters and ground squirrels. Am J Physiol 167: 638–643, 1951.
 118. Lyman CP. Oxygen consumption, body temperature and heart rate of woodchucks entering hibernation. Am J Physiol 194: 83–91, 1958.
 119. Lyman CP. Circulation in mammalian hibernation. In: Handbook of Physiology. Circulation, Vol. 3, sec. 2. Baltimore, MD, Williams and Wilkins, 1965, pp. 1967–1989.
 120. Lyman CP. Entering hibernation. In: Lyman CP, Willis JS, Malan A, Wang LCH, editors. Hibernation and Torpor in Mammals and Birds. New York, Academic Press, 1982a, pp. 37‐53.
 121. Lyman CP. The mystery of the periodic arousal. In: Lyman CP, Willis JS, Malan A, Wang LCH, editors. Hibernation and Torpor in Mammals and Birds. New York, Academic Press, 1982b, pp. 92‐103.
 122. Lyman CP, Chatfield PO. Physiology of hibernation in animals. Physiol Rev 35: 403–425, 1955.
 123. Lyman CP, Hastings AB. Total CO, of hamsters and ground squirrels during hibernation. Am J Physiol 167: 633–637, 1951.
 124. Lyman CP, O'Brien RC. Circulatory changes in the thirteen‐lined ground squirrel during the hibernating cycle. Bull Mus Comp Zool 124: 353–372, 1960.
 125. Lyman CP, O'Brien RC. Autonomic control of circulation during the hibernating cycle in ground squirrels. J Physiol Lond 168: 477–499, 1963.
 126. Lyman CP, Willis JS, Malan A, Wang L C. H. Hibernation and Torpor in Mammals and Birds. New York, Academic Press, 1982.
 127. Ma YL, Zhu X, Rivera PM, Tøien O, Barnes BM, LaManna J.C, Smith M, Drew KL. Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels. Am J Physiol 289: R1297–R1306, 2005.
 128. Mackenzie JA, Jackson DC. The effect of temperature on cutaneous CO2 loss and conductance in the bullfrog. Respir Physiol 32: 3l3‐323, 1978.
 129. MacLean GS. Respiratory physiology of a semi‐fossorial mammal Tamias striatus. Physiologist 21: 75, 1978.
 130. MacLean GS. Blood viscosity of two mammalian hibernators: Spermophilus tridecemlineatus and Tamias striatus. Physiol Zool 54: 122–131, 1981.
 131. Maginniss LA, Ekelund SA, Ultsch GR. Blood oxygen transport in common map turtles during simulated hibernation. Physiol Biochem Zool 77: 232–241, 2003.
 132. Maginniss LA, Milsom WK. Effects of hibernation on blood oxygen transport in the golden mantled ground squirrel. Respir Physiol 95: 195–208, 1994.
 133. Maginniss LA, Song YK, Reeves RB. Oxygen equilibrium of ectotherm blood containing multiple hemoglobins. Respir Physiol 42: 329–343, 1980.
 134. Maginniss LA, Tapper SS, Miller LS. Effects of chronic cold and submergence on blood oxygen transport in the turtle, Chrysemys picta. Respir Physiol 53: 15–29, 1983.
 135. Malan A. Ventilation measured by body plethysmography in hibernating mammals and poikilotherms. Respir Physiol 17: 32–44, 1973.
 136. Malan A. Blood acid‐base state at a variable temperature. A graphical representation. Respir Physiol 31: 259–275, 1977.
 137. Malan A. Respiration and acid‐base state in hibernation. In Lyman CP, Willis JS, Malan A, Wang LCH, editors. Hibernation and Torpor in Mammals and Birds. New York: Academic Press, 1982.
 138. Malan A, Arens H, Waechter A. Pulmonary respiration and acid‐base state in hibernating marmots and hamsters. Respir Physiol 17: 45–61, 1973.
 139. Malan A, Mioskowski G. pH‐temperature interactions on protein function and hibernation. GDP binding to brown adipose tissue mitochondria. J Comp Physiol B 158: 487–493, 1988.
 140. Malan A, Mioskowski G, Calgari C. Time‐course of blood acid‐base state during arousal from hibernation in the European hamster. J Comp Physiol B 158: 495–500, 1988.
 141. Malan A, Rodeau J L, Daull F. Intracellular pH in hibernation and respiratory acidosis in the European hamster. J Comp Physiol B 153: 251–258, 1985.
 142. McArthur MD, Milsom WK. Ventilation and respiratory sensitivity of euthermic Columbian and golden‐mantled ground squirrels (Spermophilus columbianus and Spermophilus lateralis) during the summer and winter. Physiol Zool 64: 921–939, 1991a.
 143. McArthur MD, Milsom WK. Changes in ventilation and respiratory sensitivity associated with hibernation in Columbian (Spermophilus columbianus) and Golden‐mantled (Spermophilus lateralis) ground squirrels. Physiol Zool 64: 940–959, 1991b.
 144. McLaughlin DW, Meints RH. A study of hibernator erythropoietic responses to simulated high altitude. Comp Biochem Physiol 42A: 655–666, 1972.
 145. McNab BK. The influence of body size on the energetics and distribution of fossorial and burrowing mammals. Ecology 60: 1010–1021, 1979.
 146. Mellen NM, Janczewski WA, Bocchiaro CM, Feldman JL. Opioid‐induced quantal slowing reveals dual networks for respiratory rhythm generation. Neuron 37: 821–826, 2003.
 147. Milsom WK. Control of arrhythmic breathing in aerial breathers. Can J Zool 66: 99–108, 1988.
 148. Milsom WK. Control of breathing in hibernating mammals. In: Lung Biology in Health and Disease; Volume 56: Strategies of Physiological Adaptation. New York: Marcel Dekker Inc., 1992, Ch. 7, p 119–148.
 149. Milsom WK. Cardiorespiratory stimuli: receptor cell versus whole animal. Amer Zool 37: 3–11, 1997.
 150. Milsom WK. Phylogeny of CO2/H+ chemoreception in vertebrates. Respir Physiol Neurobiol 131: 29–41, 2002.
 151. Milsom WK, Andrade DV, Brito SP, Toledo LF, Wang T, Abe AS. Seasonal changes in daily metabolic patterns of tegu lizards (Tupinambis merianae) placed in the cold (17 degrees) and dark. Physiol Biochem Zool 81: 165–175, 2008.
 152. Milsom WK, Burlington RF, Burleson ML. Vagal influence on heart rate in hibernating ground squirrels. J Exp Biol 185: 25–32, 1993.
 153. Milsom WK, Chatburn J, Zimmer MB. Pontine influences on respiratory control in ectothermic and heterothermic vertebrates. Respir Physiol Neurobiol 143: 263–280, 2004.
 154. Milsom WK, Harris MB, Reid SG. Do descending influences alternate to produce episodic breathing? Respir Physiol 110: 307–317, 1997.
 155. Milsom WK, Reid SG, Meier JT, Kinkead R. Central respiratory pattern generation in the bullfrog, Rana catesbeiana. Comp Biochem Physiol A 124: 253–264, 1999.
 156. Milsom WK, Zimmer MB, Harris MB. Vagal control of cardiorespiratory function in hibernation. Exp Physiol 86: 791–796, 2001.
 157. Morris S, Curtin A, Thompson M. Heterothermy, torpor, respiratory gas exchange, water balance and the effect of feeding in Gould's long‐eared bat, Nyctophilus gouldi. J Exp Biol 197: 309–335, 1994.
 158. Mortola JP, Gautier H. Interaction between metabolism and ventilation: effects of respiratory gases and temperature. In: Dempsey JA, Pack AI, Lenfant C, editors. Lung Biology in Health and Disease. Vol 79. New York: Dekker, 1995, pp 1011–1064.
 159. Musacchia XJ, Volkert WA. Blood gases in hibernating and active ground squirrels: HbO, affinity at 6° and 38°C. Am J Physiol 221: 128–130, 1971.
 160. Nestler JR. Relationship between respiratory quotient and metabolic rate during entry to and arousal from daily torpor in deer mice (Peromyscus maniculatus). Physiol Zool 63: 504–515, 1990.
 161. Nicol S, Andersen NA, Mesch U. Metabolic rate and ventilatory pattern in the echidna during hibernation and arousal. In: Augee, ML, editor. Platypus and Echidnas. Sydney: Royal Zoological Society of New South Wales, 1992, pp. 150–159.
 162. O'Shea JE. Temperature sensitivity of cardiac muscarinic receptors of bat atria and ventricle. Comp Biochem Physiol C 86: 365–370, 1987.
 163. O'Shea JE, Evans BK. Innervation of bat heart: Cholinergic and adrenergic nerves innervate all chambers. Am J Physiol 249: H876–H882, 1985.
 164. Ortmann S, Heldmaier G. Regulation of body temperature and energy requirements of hibernating alpine marmots (Marmota marmota). Am J Physiol 278: R698–R704, 2000.
 165. Osborne PG, Hashimoto M. State‐dependent regulation of cortical blood flow and respiration in hamsters: Response to hypercapnia during arousal from hibernation. J Physiol Lond 547: 963–970, 2003.
 166. Osborne S, Milsom WK. Ventilation is coupled to metabolic demands during progressive hypothermia in rodents. Respir Physiol 92: 305–318, 1993.
 167. Packard GC, Packard MJ. Natural freeze‐tolerance in hatchling painted turtles? Comp Biochem Physiol A 134: 233–246, 2003.
 168. Pajunen I. Body temperature, heart rate, breathing pattern, weight loss and periodicity of hibernation in the Finnish garden dormouse Eliomys quercinus L. Ann Zool Fenn 7: 251–266, 1970.
 169. Peterson CC, Greenshields D. Negative test for cloacal drinking in a semi‐aquatic turtle (Trachemys scripta), with comments on the function of cloacal bursae. J Exp Zool 290: 247–254, 2001.
 170. Pinder AW. Cutaneous diffusing capacity increases during hypoxia in cold submerged bullfrogs (Rana catesbeiana). Respir Physiol 70: 85–95, 1987.
 171. Poczopko P. Further investigations on the cutaneous vasomotor reflexes in the edible frog in connexion with the problem of regulation of the cutaneous respiration in frogs. Zool Poloniae 8: 161–175, 1957.
 172. Popovic V. Cardiac output in hibernating ground squirrels. Am J Physiol 207: 1345–1348, 1964.
 173. Rahn H, Paganelli CV. Gas exchange in gas gills of diving insects. Respir Physiol 5: 145–164, 1968.
 174. Reese SA, Crocker CE, Carwile ME, Jackson DC, Ultsch GR. The physiology of hibernation in common map turtles (Graptemys geographica). Comp Biochem Physiol A 130: 331–340, 2001.
 175. Reese SA, Jackson DC, Ultsch GR. 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, 2003.
 176. 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.
 177. Reeves RB. An imidazole alphastat hypothesis for vertebrate acid‐base regulation: Tissue carbon dioxide content and body temperature in bullfrogs. Respir Physiol 14: 219–236, 1972.
 178. Reeves RB. The effect of temperature on the oxygen equilibrium curve of human blood. Respir Physiol 42: 317–328, 1980.
 179. Reid SG, Meier JT, Milsom WK. The influence of descending inputs on breathing pattern formation in the isolated bullfrog brainstem‐spinal cord. Respir Physiol 120: 197–211, 2000.
 180. Rismiller PD, Heldmaier G. The effect of photoperiod on temperature selection in the European Green Lizard, Lacerta viridis. Oecologia 53: 222–226.
 181. Rodeau JL, Malan A. A two‐compartment model of blood acid‐base state at constant or variable temperature. Respir Physiol 36: 5–30, 1979.
 182. Schäfer KE, Wünnenberg W. Threshold temperatures for shivering in acute and chronic hypercapnia. J Appl Physiol 41: 67–70, 1976.
 183. Senturia JB, Campbell TA, Caprette DR. Cardiovascular changes in hibernation and hypothermia. In: Heller HC, Musacchia XJ, Wang LCH, editors. Living in the Cold: Physiological and Biochemical Adaptations. New York: Elsevier, 1986, pp. 557–564.
 184. Shams I, Avivi A, Nevo E. Oxygen and carbon dioxide fluctuations in burrows of subterranean blind mole rats indicate tolerance to hypoxic‐hypercapnic stresses. Comp Biochem Physiol 142A: 376–382, 2005.
 185. Snapp BD, Heller HC. Suppression of metabolism during hibernation in ground squirrels (Citellus lateralis). Physiol Zool 54: 297–307, 1981.
 186. Snyder GK, Nestler JR. Relationships between body temperature, thermal conductance, Q10 and energy metabolism during daily torpor and hibernation in rodents. J Comp Physiol B 159: 667–675, 1990.
 187. St. Clair RC, Gregory PT. Factors affecting the northern range limit of painted turtles (Chrysemys picta): Winter acidosis or freezing? Copeia 1990: 1083–1089, 1990.
 188. St. John WM. Integration of peripheral and central chemoreceptors stimuli by pontine and medullary respiratory centers. Fed Proc 36: 3421–3427, 1977.
 189. Stewart ER, Reese SA, Ultsch GR. The physiology of hibernation in Canadian leopard frogs (Rana pipiens) and bullfrogs (Rana catesbeiana). Physiol Biochem Zool 77: 65–73, 2004.
 190. Storey KB. Life in a frozen state: Adaptive strategies for natural freeze tolerance in amphibians and reptiles. Am J Physiol 258: R559–R568, 1990.
 191. Storey KB, Storey JM. Freeze tolerance in ectothermic vertebrates. Ann Rev Physiol 54: 610–637, 1992.
 192. Stormont RT, Foster MA, Pfeiffer C. Plasma pH, CO2, content of the blood and “tissue gas” tensions during hibernation. Proc Soc Exp Biol Med 42: 56–59, 1939.
 193. Strumwasser F. Thermoregulatory, brain and behavioral mechanisms during entrance into hibernation in the squirrel Citellus beecheyi. Am J Physiol 196: 15–22, 1959.
 194. Strumwasser F. Some physiological principles governing hibernation in Citellus beecheyi. Bull Mus Comp Zool 124: 285–320, 1960.
 195. Studier EH, Baca TP. Atmospheric conditions in artificial rodent burrows. Southwest Nat 13: 401–410, 1968.
 196. Svilha A, Bowman C. Oxygen carrying capacity of the blood of dormant ground squirrels. Am J Physiol 171: 479–481, 1952.
 197. Szewczak JM, Jackson DC. Apneic oxygen uptake in the torpid bat Eptesicus fuscus. J Exp Biol 173: 217–227, 1992.
 198. Tahti H. Effects of changes in CO, and O, concentrations in the inspired gas on respiration in the hibernating hedgehog (Erinaceus europaeus L.) Ann Zool Fenn 12: 183–187, 1975.
 199. Tahti H, Soivio A. Blood gas concentration, acid‐base balance and blood pressure in hedgehogs in the active state and in hibernation with periodic respiration. Ann Zool Fenn 12: 188–192, 1975.
 200. Tattersall GJ, Boutilier RG. Balancing hypoxia and hypothermia in cold‐submerged frogs. J Exp Biol 200: 1031–1038, 1997.
 201. Tattersall GJ, Boutilier RG. Does behavioural hypothermia promote post‐exercise recovery in cold‐submerged frogs? J Exp Biol 202: 609–622, 1999a.
 202. Tattersall GJ, Boutilier RG. Constant set points for pH and PCO2 in cold submerged skin‐breathing frogs. Resp Physiol 118: 49–59, 1999b.
 203. Tattersall GJ, Milsom WK. Transient peripheral warming accompanies the hypoxic metabolic response in the golden‐mantled ground squirrel. J Exp Biol 206: 33–42, 2003.
 204. Tattersall GJ, Ultsch GR. Physiological ecology of aquatic overwintering in ranid frogs. Biol Rev 83: 119–140, 2008.
 205. Temple GE, Musacchia XJ. Erythrocyte 2,3‐diphosphoglycerate concentrations in hibernating, hypothermic and rewarming hamsters. Proc Soc Exp Biol Med 148: 588–592, 1975.
 206. Tenney SM, Boggs DF. Comparative mammalian respiratory control. In: Handbook of Physiology. Section 3. The Respiratory System. Vol. 2, Control of Breathing, Part I. Bethesda, MD, Am Physiol Soc, 1986.
 207. Thomas DW, Cloutie D, Gagne DC. Arrhythmic breathing, apnea and non‐steady state oxygen uptake in hibernating little brown bats (Myotis lucifugus). J Exp Biol 149: 395–406, 1990.
 208. Trachsel L, Edgar DM, Heller HC. Are ground squirrels sleep deprived during hibernation? Am J Physiol 260: R1123–R1129, 1991.
 209. Twente JA, Twente JW. Concentrations of L‐lactate in the tissues of Citellus laterais after known intervals of hibernating periods. J Mammal 49: 541–544, 1968.
 210. Twente JW, Twente JA. Autonomic regulation of hibernation by Citellus and Eptesicus. In: Wang LCH, Hudson JW, editors. Strategies in the Cold: Natural Torpor and Thermogenesis. New York: Academic Press, 1978, pp. 327–373.
 211. Twente JW, Twente JA, Moy RM. Regulation of arousal from hibernation by temperature in three species of Citellus. J Appl Physiol 42: 191–195, 1977.
 212. Ultsch GR. Ecology and physiology of hibernation and overwintering among freshwater fishes, turtles, and snakes. Biol Rev 64: 435–516, 1989.
 213. Ultsch GR. The ecology of overwintering among turtles: Where turtles overwinter and its consequences. Biol Rev 81: 339–367, 2006.
 214. Ultsch GR, Brainerd EL, Jackson DC. Lung collapse among aquatic reptiles and amphibians during long‐term diving. Comp Biochem Physiol A 139: 111–115, 2004.
 215. Ultsch GR, Carwile ME, Crocker CE, Jackson DC. The physiology of hibernation among painted turtles: The eastern painted turtle, Chrysemys picta picta. Physiol Biochem Zool 72: 493–501, 1999.
 216. Ultsch GR, Cochran BM. Physiology of northern and southern musk turtles (Sternotherus odoratus) during simulated hibernation. Physiol Zool 67: 263–281, 1994.
 217. Ultsch GR, Herbert CV, Jackson DC. The comparative physiology of diving in North American freshwater turtles. I. submergence tolerance, gas exchange, and acid‐base balance. Physiol Zool 57: 620–631, 1984.
 218. Ultsch GR, Jackson DC. Long‐term submergence at 3°C 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, 1982a.
 219. Ultsch GR, Jackson DC. Long‐term submergence at 3°C of the turtle, Chrysemys picta bellii, in normoxic and severely hypoxic water. III. Effects of changes in ambient PO2 and subsequent air breathing. J Exp Biol 97: 87–99, 1982b.
 220. Ultsch GR, Jackson DC. 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, 1995.
 221. Ultsch GR, Jackson DC. pH and temperature in ectothermic vertebrates. Bull Alabama Mus Nat Hist 18: 1–41, 1996.
 222. Ultsch GR, Reese SA, Stewart ER. Physiology of hibernation in Rana pipiens: metabolic rate, critical oxygen tension, and the effects of hypoxia on several plasma variables. J Exp Zool 301A: 169–176, 2004.
 223. Vasilakos K, Wilson RJ, Kimura N, Remmers JE. Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats. J Neurobiol 62: 369–385, 2005.
 224. Wang LCH, Hudson JW. Temperature regulation in normothermic and hibernating eastern chipmunks Tamias striatus. Comp Biochem Physiol 38A: 59–90, 1970.
 225. Wang Z‐X, Sun N‐Z, Sheng W‐F. Aquatic respiration in softshelled turtles, Trionyx sinensis. Comp Biochem Physiol A 92: 593–598, 1989.
 226. Warren DE, Reese SA, Jackson DC. The factors that limit survival of red‐eared slider turtles, Trachemys scripta, during long‐term anoxic submergence at 3°C. Physiol Biochem Zool 79: 736–744, 2006.
 227. Wasser JS. Seasonal variations in plasma and tissue chemistry in water snakes, Nerodia sipedon. Copeia 1990: 399–408, 1990.
 228. Wasser JS Inman KC, Arendt EA, Lawler RG, Jackson DC. 31P‐NMR measurements of intracellular pH and high energy phosphate concentrations in isolated, perfused, working turtle hearts during anoxia and acidosis. Am J Physiol 259: R521–R530, 1990.
 229. Webb CL, Milsom WK. Ventilatory responses to acute and chronic hypoxic hypercapnia in the ground squirrel. Respir Physiol 98: 137–152, 1994.
 230. West JB, Hughes‐Jones P. Pulsatile gas flow in bronchi caused by the heart beat. J Appl Physiol 16: 697–702, 1961.
 231. Williams DD, Rausch RL. Seasonal carbon dioxide and oxygen concentrations in the dens of hibernating mammals (Sciuridae). Comp Biochem Physiol 38: 59–90, 1973.
 232. Wilz M, Heldmaier G. Comparison of hibernation, estivation and daily torpor in the edible dormouse, Glis glis. J Comp Physiol B 170: 511–521, 2000.
 233. Wilz M, Milsom WK, Heldmaier G. Intermittent ventilation in hibernating dormice—Is ventilation always necessary to meet metabolic demands? In: Heldmaier G, Klingenspor M, editors. Life in the Cold, Heidelberg: Springer Verlag, pp 169–178, 2000.
 234. Withers PC. Metabolic, respiratory and haematological adjustments of the little pocket mouse to circadian torpor cycles. Respir Physiol 31: 295–307, 1977.
 235. Wood SC. Cardiovascular shunts and oxygen transport in lower vertebrates. Am J Physiol 247: R3–RI4, 1984.
 236. Zimmer MB, Milsom WK. Effects of changing ambient temperature on metabolic, heart, and ventilation rates during steady state hibernation in golden‐mantled ground squirrels (Spermophilus lateralis). Physiol Biochem Zool 74: 714–723, 2001.
 237. Zimmer MB, Milsom WK. Ventilatory pattern and chemosensitivity in unanesthetized, hypothermic ground squirrels (Spermophilus lateralis). Respir Physiol Neurobiol 133: 49–63, 2002.

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Article Title: Hibernation and Gas Exchange
 

How to Cite

William K. Milsom, Donald C. Jackson. Hibernation and Gas Exchange. Compr Physiol 2011, 1: 397-420. doi: 10.1002/cphy.c090018