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9 - Surviving without any oxygen

Published online by Cambridge University Press:  05 June 2012

By
Göran E. Nilsson
Edited by
Göran E. Nilsson
Göran E. Nilsson
Affiliation:
Universitetet i Oslo
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Summary

Introduction

Most vertebrates cannot survive more than a few minutes without any oxygen. As pointed out in Chapter 1, the high intrinsic rate of oxygen consumption of the brain makes it one of the first organs to fail in anoxia. While medical science struggles to find ways to counteract anoxic tissue damage, unfortunately with quite limited success, evolution has solved this problem a few times, as revealed by the few vertebrates that can survive months without any oxygen. The best-studied examples of such anoxia-tolerant vertebrates are the crucian carp (Carassius carassius) and some North American freshwater turtles in the genera Trachemys and Chrysemys.

It is not a coincidence that these extremely anoxia-tolerant vertebrates are aquatic. The access to oxygen may be temporarily halted in many aquatic habitats, either because water oxygen content becomes severely depleted (see Chapters 1 and 5), or because lung breathers such as turtles lose their access to air for long periods, especially during overwintering. A particularly longlasting and extreme oxygen depletion occurs in many small, ice-covered lakes and ponds in the northern hemisphere. Due to a thick ice cover, which blocks oxygen diffusion as well as light needed for photosynthesis, these waters may become anoxic for several months (Holopainen and Hyvärinen, 1985; Ultsch, 1989). It is under such conditions that crucian carp and turtles have evolved their ability to survive long periods of anoxia.

Type
Chapter
Information
Respiratory Physiology of Vertebrates
Life With and Without Oxygen
 , pp. 300 - 328
Publisher: Cambridge University Press
Print publication year: 2010

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References

Bickler, P. E. (1992). Cerebral anoxia tolerance in turtles, regulation of intracellular calcium and pH. Am. J. Physiol. Regul. Integr. Comp. Physiol., 263, R1298–302.CrossRefGoogle Scholar
Bickler, P. E. (1998). Reduction in NMDA receptor activity in cerebrocortex of turtles (Chrysemys picta) during 6 wk of anoxia. Am. J. Physiol. Regul. Integr. Comp. Physiol., 275, R86–91.CrossRefGoogle ScholarPubMed
Bickler, P. E. (2004). Clinical perspectives, neuroprotection lessons from hypoxia-tolerant organisms. J. Exp. Biol., 207, 3243–9.CrossRefGoogle ScholarPubMed
Bickler, P. E. and Donohoe, P. H. (2002). Adaptive responses of vertebrate neurons to hypoxia. J. Exp. Biol., 205, 3579–86.Google ScholarPubMed
Bickler, P. E. and Hansen, B. M. (1998). Hypoxia-intorerant neonatal CA1 neurons: relationship of survial to evoked glutamate release and glutamate receptor-mediated calcium changes in hippocampal slices. Dev. Brain. Res., 106, 57–69.CrossRefGoogle Scholar
Bickler, P. E., Donohoe, P. H. and Buck, L. T. (2000). Hypoxia-induced silencing of NMDA receptors in turtle neurons. J. Neurosci., 20, 3522–8.CrossRefGoogle ScholarPubMed
Buck, L. T. and Bickler, P. E. (1995). Role of adenosine in NMDA receptor modulation in the cerebral-cortex of an anoxia-tolerant tutle (Chrysemys picta belli). J. Exp. Biol., 198, 1621–8.Google Scholar
Buck, L. T. and Bickler, P. E. (1998). Adenosine and anoxia reduce N-methyl-D-aspartate receptor open probability in turtle cerebrocortex. J. Exp. Biol., 201, 289–97.Google ScholarPubMed
Chen, J., Zhu, J. X., Wilson, I. and Cameron, J. S. (2005). Cardioprotective effects of KATP channel activation during hypoxia in goldfish Carassius auratus. J. Exp. Biol. 208, 2765–72.CrossRefGoogle Scholar
Congleton, J. L. (1974). The respiratory response of asphyxia of Typhlogobius californiensis (Teleostei, Gobiidae) and some related gobies. Biol. Bull., 146, 186–205.CrossRefGoogle ScholarPubMed
Ellefsen, S., Sandvik, G. K., Larsen, H. K., Stensløkken, K. O., Hov, D. A. S.,Kristensen, T. A. and Nilsson, G. E. (2008). Expression of genes involved in excitatory neurotransmission in anoxic crucian carp (Carassius carassius) brain. Physiol. Genomics, 35, 5–17.CrossRefGoogle ScholarPubMed
Ellefsen, S., Stenslokken, K. O., Fagernes, C. E., Kristensen, T. A. and Nilsson, G. E. (2009). Expression of genes involved in GABAergic neurotransmission in anoxic crucian carp brain (Carassius carassius). Physiol. Genomics, 36, 61–8.CrossRefGoogle Scholar
Erecinska, M. and Silver, I. A. (1994). Ions and energy in mammalian brain. Prog. Neurobiol., 43, 37–71.CrossRefGoogle ScholarPubMed
Fagernes, C., Ellefsen, S., Stenslokken, K. O., Berenbrink, M. and Nilsson, G. (2008). Molecular background to ethanol production in crucian carp (Carassius carassius). Comp. Biochem. Physiol., 150A (Suppl. 1), S112.CrossRefGoogle Scholar
Feng, Z.-C., Rosenthal, M. and Sick, T. J (1988a). Suppression of evoked potentials with continued ion transport during anoxia in turtle brain. Am. J. Physiol. Regul. Integr. Comp. Physiol., 255, R478–84.CrossRefGoogle ScholarPubMed
Feng, Z.-C., Sick, T. J. and Rosenthal, M. (1988b). Orthodromic field potentials and recurrent inhibition during anoxia in turtle brain. Am. J. Physiol. Regul. Integr. Comp. Physiol., 255, R485–91.CrossRefGoogle ScholarPubMed
Fernandes, J. A., Lutz, P. L., Tannenbaum, A., Todorov, A. T., Liebovitch, L. and Vertes, R. (1997). Electroencephalogram activity in the anoxic turtle brain. Am. J. Physiol. Regul. Integr. Comp. Physiol., 273, R911–19.CrossRefGoogle ScholarPubMed
Franks, N. P. (2008). General anaesthesia, from molecular targets to neuronal pathways of sleep and arousal. Nature Rev. Neurosci., 9, 370–86.CrossRefGoogle ScholarPubMed
Fraser, K. P., Houlihan, D. F., Lutz, P. L., Leone-Kabler, S., Manuel, L. and Brechin, J. G (2001). Complete suppression of protein synthesis during anoxia with no post-anoxia protein synthesis debt in the red-eared slider turtle Trachemys scripta elegans. J. Exp. Biol., 204, 4353–60.Google ScholarPubMed
Gerschenfeld, H. M. (1973). Chemical transmission in invertebrate central nervous systems and neuromuscular junctions. Physiol. Rev., 53, 1–119.CrossRefGoogle ScholarPubMed
Ghai, H. S. and Buck, L. T. (1999). Acute reduction in whole cell conductance in anoxic turtle brain. Am. J. Physiol. Regul. Integr. Comp. Physiol., 277, R887–93.CrossRefGoogle ScholarPubMed
Hicks, J. M. T. and Farrell, A. P. (2000a). The cardiovascular responses of the red eared slider (Trachemys scripta) acclimated to either 22 or 5°C. I. Effects of anoxia exposure on in vivo cardiac performance. J. Exp. Biol., 203, 3765–74.Google ScholarPubMed
Hicks, J. M. T. and Farrell, A. P. (2000b). The cardiovascular responses of the red eared slider (Trachemys scripta). acclimated to either 22 or 5°C. II. Effects of anoxia on adrenergic and cholinergic control. J. Exp. Biol., 203, 3775–84.Google ScholarPubMed
Hochachka, P. W. (1986). Defense strategies against hypoxia and hypothermia. Science, 231, 234–41.CrossRefGoogle ScholarPubMed
Hochachka, P. W. and Somero, G. N. (2002). Biochemical Adaptation, Mechanism and Process in Physiological Evolution. Oxford: Oxford University Press.Google Scholar
Holopainen, I. J. and Hyvärinen, H. (1985). Ecology and physiology of crucian carp (Carassius carassius (L.)) in small Finnish ponds with anoxic conditions in winter. Verh. Internat. Verein. Limnol., 22, 2566–70.Google Scholar
Hylland, P. and Nilsson, G. E. (1999). Extracellular levels of amino acid neurotransmitters during anoxia and forced energy deficiency in crucian carp brain. Brain Res., 823, 49–58.CrossRefGoogle ScholarPubMed
Hylland, P., Nilsson, G. E. and Lutz, P. L (1994). Time course of anoxia induced increase in cerebral blood flow rate in turtles: evidence for a role of adenosine. J. Cereb. Blood Flow Metab., 14, 877–81.CrossRefGoogle ScholarPubMed
Hylland, P., Nilsson, G. E. and Johansson, D. (1995). Anoxic brain failure in an ectothermic vertebrate, release of amino acids and K+ in rainbow trout thalamus. Am. J. Physiol. Regul. Integr. Comp. Physiol., 269, R1077–84.CrossRefGoogle Scholar
Hyvärinen, H., Holopainen, I. J. and Piironen, J. (1985). Anaerobic wintering of crucian carp (Carassius carassius L.). I. Annual dynamics of glycogen reserves in nature. Comp. Biochem. Physiol., 82A, 797–803.CrossRefGoogle Scholar
Jackson, D. C. (1968). Metabolic depression and oxygen depletion in the diving turtle. J. Appl. Physiol., 24, 503–9.CrossRefGoogle ScholarPubMed
Jackson, D. C. (2002). Hibernation without oxygen, physiological adaptations in the painted turtle. J. Physiol., 543, 731–7.CrossRefGoogle ScholarPubMed
Jackson, D. C., Taylor, S. E., Asare, V. S., Villarnovo, D., Gall, J. M. and Reese, S. A. (2007.). Comparative shell buffering properties correlate with anoxia tolerance in freshwater turtles. Am. J. Physiol. Regul. Integr. Comp. Physiol., 292, R1008–15.CrossRefGoogle ScholarPubMed
Jibb, L. A. and Richards, J. G. (2008). AMP-activated protein kinase activity during metabolic rate depression in the hypoxic goldfish, Carassius auratus. J. Exp. Biol., 211, 3111–22.CrossRefGoogle ScholarPubMed
Johansson, D. and Nilsson, G. E. (1995). Roles of energy status, Kadenosine triphosphate channels, and channel arrest in fish brain K+ gradient dissipation during anoxia. J. Exp. Biol., 198, 2575–80.Google Scholar
Johansson, D., Nilsson, G. E. and Døving, K. B. (1997). Anoxic depression of light-evoked potentials in retina and optic tectum of crucian carp. Neurosci. Lett., 237, 73–6.CrossRefGoogle ScholarPubMed
Johansson, D., Nilsson, G. E. and Törnblom, E. (1995). Effects of anoxia on energy metabolism in crucian carp brain slices studied with microcalorimetry. J. Exp. Biol., 198, 853–9.Google ScholarPubMed
Johnson, E. M., Koike, T. and Franklin, J. (1992). A ‘calcium set-point hypothesis’ of neuronal dependence on neurotrophic factor. Exp. Neurol., 115, 163–6.CrossRefGoogle Scholar
Johnston, I. A. and Bernard, L. M. (1983). Utilization of the ethanol pathway in carp following exposure to anoxia. J. Exp. Biol., 104, 73–8.Google Scholar
Koopowitz, H. and Keenan, L. (1982). The primitive brain of platyhelminthes. Trends Neurosci., 5, 77–9.CrossRefGoogle Scholar
Krumschnabel, G., Biasi, C. and Wieser, W. (2000). Action of adenosine on energetics, protein synthesis and K+ homeostasis in teleost hepatocytes. J. Exp. Biol., 203, 2657–65.Google Scholar
Lipton, P. (1999). Ischemic cell death in brain neurons. Physiol. Rev., 79, 1431–568.CrossRefGoogle ScholarPubMed
Lutz, P. L. and Leone-Kabler, S. A. (1995). Upregulation of GABAA receptor during anoxia in the turtle brain. Am. J. Physiol. Regul. Integr. Comp. Physiol., 268, R1332–5.CrossRefGoogle ScholarPubMed
Lutz, P. L. and Nilsson, G. E. (1997). Contrasting strategies for anoxic brain survival: glycolysis up or down. J. Exp. Biol., 200, 411–9.Google ScholarPubMed
Lutz, P. L., McMahon, P., Rosenthal, M. and Sick, T. J (1984). Relationships between aerobic and anaerobic energy production in turtle brain in situ. Am. J. Physiol. Regul. Integr. Comp. Physiol., 247, R740–4.CrossRefGoogle ScholarPubMed
Lutz, P. L., Nilsson, G. E. and Prentice, H. (2003). The Brain Without Oxygen, 3rd edn. Dordrecht: Kluwer Academic Publishers.Google Scholar
Lutz, P. L., Rosenthal, M. and Sick, T. (1985). Living without oxygen, turtle brain as a model of anaerobic metabolism. Mol. Physiol., 8, 411–25.Google Scholar
McGeer, P. L. and McGeer, E. G. (1989). Amino acid neurotransmitters. In Basic Neurochemistry, ed. Siegel, G. J., Agranoff, B. and Alberts, R. W.. New York: Raven Press, pp. 311–32.Google Scholar
Mendelsohn, B. A., Kassebaum, B. L. and Gitlin, J. D. (2008). The zebrafish embryo as a dynamic model of anoxia tolerance. Dev. Dyn., 237, 1780–8.CrossRefGoogle ScholarPubMed
Milton, S. L, and Lutz, P. L. (1998). Low extracellular dopamine levels are maintained in the anoxic turtle brain. J. Cereb. Blood Flow Metab. 18, 803–7.CrossRefGoogle Scholar
Milton, S. L., Dirk, L. J., Kara, L. F. and Prentice, H. M (2008). Adenosine modulates ERK1/2, PI3K/Akt, and p38MAPK activation in the brain of the anoxia-tolerant turtle Trachemys scripta. J. Cereb. Blood Flow. Metab. 28, 1469–77.CrossRefGoogle ScholarPubMed
Milton, S. L., Thompson, J. W. and Lutz, P. L. (2002). Mechanisms for maintaining extracellular glutamate in the anoxic turtle striatum. Am. J. Physiol. Regul. Integr. Comp. Physiol., 282, R1317–23.CrossRefGoogle ScholarPubMed
Mourik, J., Raeven, P., Steur, K. and Addink, A. D. F. (1982). Anaerobic metabolism of red skeletal muscle of goldfish, Carassius auratus (L.). FEBS Lett 137, 111–14.Google ScholarPubMed
Nilsson, G. E. (1988). A comparative study of aldehyde dehydrogenase and alcohol dehydrogenase activity in crucian carp and three other vertebrates, apparent adaptations to ethanol production. J. Comp. Physiol. B 158, 479–85.CrossRefGoogle ScholarPubMed
Nilsson, G. E. (1990a). Long term anoxia in crucian carp, changes in the levels of amino acid and monoamine neurotransmitters in the brain, catecholamines in chromaffin tissue, and liver glycogen. J. Exp. Biol., 150, 295–320.Google ScholarPubMed
Nilsson, G. E. (1990b). Distribution of aldehyde dehydrogenase and alcohol dehydrogenase in summer acclimatized crucian carp (Carassius carassius L.). J. Fish Biol. 36, 175–9.CrossRefGoogle Scholar
Nilsson, G. E. (1991). The adenosine receptor blocker aminophylline increases anoxic ethanol production in crucian carp. Am. J. Physiol. Regul. Integr. Comp. Physiol., 261, R1057–60.CrossRefGoogle Scholar
Nilsson, G. E. (1992). Evidence for a role of GABA in metabolic depression during anoxia in crucian carp (Carassius carassius L.). J. Exp. Biol., 164, 243–59.Google Scholar
Nilsson, G. E. (2001). Surviving anoxia with the brain turned on. News Physiol. Sci. 16, 218–21.Google ScholarPubMed
Nilsson, G. E. and Lutz, P. L. (1991). Release of inhibitory neurotransmitters in response to anoxia in turtle brain. Am. J. Physiol. Regul. Integr. Comp. Physiol., 261, R32–7.CrossRefGoogle ScholarPubMed
Nilsson, G. E. and Lutz, P. L. (1992). Adenosine release in the anoxic turtle brain, a possible mechanism for anoxic survival. J. Exp. Biol., 162, 345–51.Google Scholar
Nilsson, G. E. and Lutz, P. L. (1993). Role of GABA in hypoxia tolerance, metabolic depression and hibernation – possible links to neurotransmitter evolution. Comp. Biochem. Physiol., 105C, 329–36.Google Scholar
Nilsson, G. E. and Lutz, P. L. (2004). Anoxia tolerant brains. J. Cereb. Blood Flow Metab., 24, 475–86.CrossRefGoogle ScholarPubMed
Nilsson, G. E. and Renshaw, G. M. C. (2004). Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J. Exp. Biol., 207, 3131–9.CrossRefGoogle Scholar
Nilsson, G. E., Hylland, P. and Löfman, C. O. (1994). Anoxia and adenosine induce increased cerebral blood flow in crucian carp. Am. J. Physiol. Regul. Integr. Comp. Physiol., 267, R590–5.CrossRefGoogle ScholarPubMed
Nilsson, G. E., Pérez-Pinzón, M., Dimberg, K. and Winberg, S. (1993b). Brain sensitivity to anoxia in fish as reflected by changes in extracellular potassium-ion activity. Am. J. Physiol. Regul. Integr. Comp. Physiol., 264, R250–3.CrossRefGoogle Scholar
Nilsson, G. E., Rosén, P. and Johansson, D. (1993a). Anoxic depression of spontaneous locomotor activity in crucian carp quantified by a computerized imaging technique. J. Exp. Biol., 180, 153–63.Google Scholar
Paajanen, V. and Vornanen, M. (2004). Regulation of action potential duration under acute heat stress by by IKATP and IK1 in fish cardiac myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol., 286, R405–15.CrossRefGoogle Scholar
Pamenter, M. E., Shin, D. S. and Buck, L. T. (2008b). Adenosine A1 receptor activation mediates NMDA receptor activity in a pertussis toxin-sensitive manner during normoxia but not anoxia in turtle cortical neurons. Brain Res., 1213, 27–34.CrossRefGoogle Scholar
Pamenter, M. E., Shin, D. S. and Buck, L. T. (2008c). AMPA receptors undergo channel arrest in the anoxic turtle cortex. Am. J. Physiol. Regul. Integr. Comp. Physiol., 294, R606–13.CrossRefGoogle ScholarPubMed
Pamenter, M. E., Shin, D. S., Cooray, M. and Buck, L. T. (2008a). Mitochondrial ATP-sensitive K+ channels regulate NMDAR activity in the cortex of the anoxic western painted turtle. J. Physiol., 586, 1043–58.CrossRefGoogle ScholarPubMed
Pek, M, and Lutz, P. L. (1997). Role for adenosine in ‘channel arrest’ in the anoxic turtle brain. J. Exp. Biol., 200, 1913–17.Google Scholar
Pek, M. and Lutz, P. L. (1998). K+adenosine triphosphate channel activation provides transient protection in anoxic turtle brain. Am. J. Physiol. Regul. Integr. Comp. Physiol., 275, R2023–7.Google Scholar
Pérez-Pinzón, M. A., Lutz, P. L., Sick, T., Rosenthal, M. (1993). Adenosine, a ‘retaliatory’ metabolite, promotes anoxia tolerance in turtle brain. J. Cereb. Blood Flow Metab. 13, 728–32.CrossRefGoogle ScholarPubMed
Peréz-Pinzón, M. A., Rosenthal, M., Sick, T. J., Lutz, P. L., Pablo, J. and Mash, D. (1992). Down-regulation of sodium channels during anoxia, a putative survival strategy of turtle brain. Am. J. Physiol. Regul. Integr. Comp. Physiol., 262, R712–15.CrossRefGoogle ScholarPubMed
Podrabsky, J. E., Lopez, J. P., Fan, T. W. M.Higashi, R. and Somero, G. N (2007). Extreme anoxia tolerance in embryos of the annual killifish Austrofundulus limnaeus, insights from a metabolomics analysis. J. Exp. Biol., 210, 2253–66.CrossRefGoogle ScholarPubMed
Rausch, R. N., Crawshaw, L. I. and Wallace, H. L (2000). Effects of hypoxia, anoxia, and endogenous ethanol on thermoregulation in goldfish, Carassius auratus. Am. J. Physiol. Regul. Integr. Comp. Physiol., 278, R545–55.CrossRefGoogle ScholarPubMed
Restifo, L. L. and White, K. (1990). Molecular and genetic approaches to neurotransmitter and neuromodulator systems in Drosophila. In Advances in Insect Physiology, Vol. 22, ed. Evans, P. D. and Wigglesworth, V. B.. London: Academic Press, pp. 115–219.Google Scholar
Rosati, A. M., Traversa, U., Lucchi, R. and Poli, A. (1995). Biochemical and pharmacological evidence for the presence of A1 but not A2a adenosine receptors in the brain of the low vertebrate teleost Carassius auratus (goldfish). Neurochem. Int., 26, 411–23.CrossRefGoogle Scholar
Shoubridge, E. A. and Hochachka, P. W. (1980). Ethanol, novel endproduct in vertebrate anaerobic metabolism. Science 209, 308–9.CrossRefGoogle Scholar
Sick, T. J., Pérez-Pinzón, M., Lutz, P. L. and Rosenthal, M. (1993). Maintaining coupled metabolism and membrane function in anoxic brain, a comparison between the turtle and rat. In Surviving Hypoxia, Mechanisms of Control and Adaptation, ed. Hochachka, P. W., Lutz, P. L., Sick, T., Rosenthal, M. and Thillart, G.. Boca Raton: CRC Press, pp. 351–63.Google Scholar
Sick, T. J., Rosenthal, M., LaManna, J. C. and Lutz, P. L. (1982). Brain potassium homeostasis, anoxia, and metabolic inhibition in turtles and rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 243, R281–8.CrossRefGoogle ScholarPubMed
Siesjö, B. K. (1978). Brain Energy Metabolism, Chichester: Wiley.Google ScholarPubMed
Smith, R. W., Houlihan, D. F., Nilsson, G. E. and Brechin, J. G. (1996). Tissue specific changes in protein synthesis rates in vivo during anoxia in crucian carp. Am. J. Physiol. Regul. Integr. Comp. Physiol., 271, R897–904.CrossRefGoogle ScholarPubMed
Stecyk, J. A. W., Overgaard, J., Farrell, A. P. and Wang, T. (2004a). Alpha-adrenergic regulation of systemic peripheral resistance and blood flow distribution in the turtle Trachemys scripta during anoxic submergence at 5°C and 21°C. J. Exp. Biol., 207, 269–83.CrossRefGoogle Scholar
Stecyk, J. A. W., Stensløkken, K.-O., Farrell, A. P. and Nilsson, G. E. (2004b). Maintained cardiac pumping in anoxic crucian carp. Science, 306, 77.CrossRefGoogle ScholarPubMed
Stensløkken, K.-O., Ellefsen, S., Stecyk, J. A. W., Dahl, M. B.Nilsson, G. E. and Vaage, J. (2008b). Differential regulation of AMP-activated kinase and AKT kinase in response to oxygen availability in crucian carp (Carassius carassius). Am. J. Physiol. Regul. Integr. Comp. Physiol., 295, R1803–14.CrossRefGoogle Scholar
Stensløkken, K.-O., Milton, S. L., Lutz, P. L., et al. (2008a). Effect of anoxia on the electroretinogram of three anoxia-tolerant vertebrates. Comp. Biochem. Physiol. 150A, 395–403.CrossRefGoogle Scholar
Storey, K. B. (1996). Metabolic adaptations supporting anoxia tolerance in reptiles, recent advances. Comp. Biochem. Physiol., 113B, 23–35.CrossRefGoogle Scholar
Suzue, T, Wu, G.-B. and Furukawa, T. (1987). High susceptibility to hypoxia of afferent synaptic transmission in the goldfish sacculus. J. Neurophysiol., 58, 1066–79.CrossRefGoogle ScholarPubMed
Ultsch, G. R. (1985). The viability of nearctic freshwater turtles submerged in anoxia and normoxia at 3 and 10°C. Comp. Biochem. Physiol., 81A, 607–11.CrossRefGoogle Scholar
Ultsch, G. R. (1989). Ecology and physiology of hibernation and overwintering among freshwater fishes, turtles and snakes. Biol. Rev., 64, 435–516.CrossRefGoogle Scholar
Ultsch, G. R. and Jackson, D. C. (1982). Long-term submergence at 3°C of the turtle Chrysemys picta belli in normoxic and severely hypoxic water I. Survival, gas exchange and acid-base status. J. Exp. Biol., 96, 11–28.Google Scholar
Usherwood, P. N. R. (1978). Amino acids as neurotransmitters. Adv. Comp. Physiol. Biochem., 7, 227–309.CrossRefGoogle ScholarPubMed
Raaij, M. T. M., Breukel, B.-J., Thillart, G. E. E. J. M. and Addink, A. D. F. (1994). Lipid metabolism of goldfish, Carassius auratus (L.) during normoxia and anoxia. Indications for fatty acid chain elongation. Comp. Biochem. Physiol., 107B, 75–84.Google Scholar
Waarde, A., Thillart, G. and Verhagen, M. (1993). Ethanol formation and pH regulation in fish. In Surviving Hypoxia, Mechanisms of Control and Adaptation, ed. Hochachka, P. W., Lutz, P. L., Sick, T., Rosenthal, M. and Thillart, G.. Boca Raton: CRC Press, pp. 157–70.Google Scholar
Waversveld, J., Addink, A. D. F. and Thillart, G. (1989). Simultaneous direct and indirect calorimetry on normoxic and anoxic goldfish. J. Exp. Biol., 142, 325–35.Google Scholar
Vornanen, M. (1994). Seasonal adaptation of crucian carp (Carassius carassius L.). heart, glycogen stores and lactate dehydrogenase activity. Can. J. Zool., 72, 433–42.CrossRefGoogle Scholar
Vornanen, M. and Paajanen, V. (2004). Seasonality of dihydropyridine receptor binding in the heart of an anoxia-tolerant vertebrate, the crucian carp (Carassius carassius L.). Am. J. Physiol. Regul. Integr. Comp. Physiol., 287, R1263–9.CrossRefGoogle Scholar
Vornanen, M. and Paajanen, V. (2006). Seasonal changes in glycogen content and Na+-K+-ATPase activity in the brain of crucian carp. Am. J. Physiol. Regul. Integr. Comp. Physiol., 291, R1482–9.CrossRefGoogle ScholarPubMed
Vornanen, M., Stecyk, J. A. W. and Nilsson, G. E. (2009). The anoxia-tolerant crucian carp (Carassius carassius L.). In Fish Physiology, Vol. 27, Hypoxia. ed. Richards, J. G., Farrell, A. P. and Brauner, C.. Amsterdam: Elesevier/Academic Press.Google Scholar
Warren, D. E., Reese, S. A. and Jackson, D. C (2006). Tissue glycogen and extracellular buffering limit the survival of red-eared slider turtles during anoxic submergence at 3°C. Physiol. Biochem. Zool. 79, 736–44.CrossRefGoogle ScholarPubMed
Wilkie, M. P., Pamenter, M. E., Alkabie, S., Carapic, D., Shin, D. S. and Buck, L. T. (2008). Evidence of anoxia-induced channel arrest in the brain of the goldfish (Carassius auratus). Comp. Biochem. Physiol., 148C, 355–62.Google Scholar
Wood, S. C., Dupre, R. K. and Hicks, J. W. (1985). Voluntary hypothermia in hypoxic animals. Acta. Physiol. Scand. 124 (Suppl. 542), 46.Google Scholar
Zipfel, G. J., Babcock, D. J., Lee, J. M. and Choi, D. W. (2000). Neuronal apoptosis after CNS injury, the roles of glutamate and calcium. J. Neurotrauma, 17, 857–69.CrossRefGoogle ScholarPubMed

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