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Phylogeny of the Gas‐Exchange System: Red Cell Function

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Abstract

The sections in this article are:

1 Evolution of Hemoglobin Molecule
2 Hemoglobin Function Inside Red Cells
2.1 Red Cell Metabolism
2.2 Allosteric Controllers of Hemoglobin Function
2.3 Red Cell pH
3 Oxygen Capacity of Blood
4 Hematopoiesis in Ectothermic Vertebrates
5 Oxygen Dissociation Curve and the Environment
5.1 Adaptations to Temperature
5.2 Adaptations to Hypoxia
5.3 Transition From Water Breathing to Air Breathing
6 Organismic Adaptations
6.1 Oxygen Uptake and Metabolic Machinery
6.2 Allometry
6.3 Circulatory Shunts
7 Conclusion
Figure 1. Figure 1.

Probable scheme for development of the Hb tetramer and cofactors that modulate Hb function. DPG, diphosphoglycerate; IPP, inositol pentaphosphate.

From Bunn 23
Figure 2. Figure 2.

Mechanisms controlling 2,3‐diphosphoglycerate (2,3‐DPG) metabolism and Hb‐O2 affinity of human red blood cells during hypoxia. ODC, O2 dissociation curve.

Adapted from Gerlach and Duhm (134)
Figure 3. Figure 3.

Mechanisms controlling O2 affinity and intracellular pH of nucleated red blood cells.

From Wood and Lenfant 129, by courtesy of Marcel Dekker, Inc
Figure 4. Figure 4.

Effect of Hb concentration on blood flow/O2 uptake ratio (blood convection requirement) in different vertebrates.

From Len‐fant et al. (136)
Figure 5. Figure 5.

Effect of pH on O2 affinity (P50) of whole blood in salamanders. DE‐A, Dicamptodon ensatus, adult; DE‐L, D. ensatus, larvae; TG‐W, Taricha granulosa, warm acclimated; TG‐C, T. granulosa, cold acclimated (121; S. C. Wood, unpublished observations). SS, Salamandra salamandra; AM‐L, Ambystoma mexicanum, lung form; AM‐G, A. mexicanum, gill form (133). TC‐C, Triton cristatus, cold acclimated (137). A, Amphiuma means; N, Necturus maculosa 77. C, Cryptobranchus (139).

Figure 6. Figure 6.

Dual effect of temperature (direct and pH‐mediated) on the O2 affinity of blood in the African tree frog, Chiromantis petersi. ΔH, apparent enthalpy.

Data from Johansen et al. 65
Figure 7. Figure 7.

Pattern of thermal acclimation of Hb function seen in some fishes and amphibians. Acutely measured temperature coefficient does not change (solid lines), but long‐term coefficient is reduced (dashed line).

Figure 8. Figure 8.

Two‐compartment model of O2 transport applicable to animals with central vascular or intracardiac shunts.

From Wood 124


Figure 1.

Probable scheme for development of the Hb tetramer and cofactors that modulate Hb function. DPG, diphosphoglycerate; IPP, inositol pentaphosphate.

From Bunn 23


Figure 2.

Mechanisms controlling 2,3‐diphosphoglycerate (2,3‐DPG) metabolism and Hb‐O2 affinity of human red blood cells during hypoxia. ODC, O2 dissociation curve.

Adapted from Gerlach and Duhm (134)


Figure 3.

Mechanisms controlling O2 affinity and intracellular pH of nucleated red blood cells.

From Wood and Lenfant 129, by courtesy of Marcel Dekker, Inc


Figure 4.

Effect of Hb concentration on blood flow/O2 uptake ratio (blood convection requirement) in different vertebrates.

From Len‐fant et al. (136)


Figure 5.

Effect of pH on O2 affinity (P50) of whole blood in salamanders. DE‐A, Dicamptodon ensatus, adult; DE‐L, D. ensatus, larvae; TG‐W, Taricha granulosa, warm acclimated; TG‐C, T. granulosa, cold acclimated (121; S. C. Wood, unpublished observations). SS, Salamandra salamandra; AM‐L, Ambystoma mexicanum, lung form; AM‐G, A. mexicanum, gill form (133). TC‐C, Triton cristatus, cold acclimated (137). A, Amphiuma means; N, Necturus maculosa 77. C, Cryptobranchus (139).



Figure 6.

Dual effect of temperature (direct and pH‐mediated) on the O2 affinity of blood in the African tree frog, Chiromantis petersi. ΔH, apparent enthalpy.

Data from Johansen et al. 65


Figure 7.

Pattern of thermal acclimation of Hb function seen in some fishes and amphibians. Acutely measured temperature coefficient does not change (solid lines), but long‐term coefficient is reduced (dashed line).



Figure 8.

Two‐compartment model of O2 transport applicable to animals with central vascular or intracardiac shunts.

From Wood 124
References
 1. Adamson, J. W., and C. Finch. Hemoglobin function, oxygen affinity, and erythropoietin. Annu. Rev. Physiol. 37: 351–369, 1975.
 2. Ambersom, W. R., J. Flexner, and F. R. Steggerada. On the use of Ringer‐Locke solutions containing hemoglobin as a substitute for normal blood in mammals. J. Cell. Comp. Physiol. 5: 359–364, 1934.
 3. Armentrout, D., and F. L. Rose. Some physiological responses to anoxia in the great plains toad, Bufo cognatus. Comp. Biochem. Physiol. A Comp. Physiol. 39: 447–455, 1971.
 4. Barcroft, J. Features in the Architecture of Physiological Function. London: Cambridge Univ. Press, 1934, p. 40.
 5. Barnikol, W. K. R., and O. Burkhard. The fine structure of O2 binding in animals: Rana esculenta (Abstract). Pfluegers Arch. 379: R27, 1979.
 6. Barra, D. F., F. Bossa, J. Bonaventura, and M. Brunori. Hemoglobin components from trout (Salmo irideus): determination of the carboxyl and amino terminal sequences and their functional implications. FEBS Lett. 35: 151–154, 1973.
 7. Bartels, H. Comparative physiology of oxygen transport in mammals. Lancet 2: 599–604, 1964.
 8. Bartels, H. (editor). Prenatal Respiration. Amsterdam: North‐Holland, 1970, p. 50. (Frontiers Biol. Ser. 17.)
 9. Bartels, H., and C. Bauer. Relation between oxygen dissociation curve and tissue oxygenation. Forsvarsmedicin 5: 227–233, 1969.
 10. Bartholomew, G. A. Body temperature and energy metabolism. In: Animal Physiology: Principles and Adaptations (4th ed.), edited by M. S. Gordon. New York: Macmillan, 1972, p. 298–368.
 11. Bartlett, G. R. Phosphate compounds in red cells of reptiles, amphibians, and fish. Comp. Biochem. Physiol. A Comp. Physiol. 55: 211–214, 1976.
 12. Battaglia, F. C., H. McGaughey, E. L. Makowski, and G. Meschia. Postnatal changes in oxygen affinity of sheep red cells: a dual role of diphosphoglyceric acid. Am. J. Physiol. 219: 217–221, 1970.
 13. Bauer, C. On the respiratory function of haemoglobin. Rev. Physiol. Biochem. Pharmacol. 70: 1–31, 1974.
 14. Bauer, C., and W. Jelkmann. Carbon dioxide governs the oxygen affinity of crocodile blood. Nature Lond. 269: 825–827, 1977.
 15. Bauer, C., I. Ludwig, and M. Ludwig. Different effects of 2,3‐diphosphoglycerate and adenosine triphosphate on the oxygen affinity of adult and foetal human haemoglobin. Life Sci. 7: 1339–1343, 1968.
 16. Benesch, R., and R. E. Benesch. The chemistry of the Bohr effect. I. The reaction of N‐ethylmaleimide with the oxygen‐linked acid groups of hemoglobin. J. Biol. Chem. 236: 405–410, 1961.
 17. Benesch, R., and R. E. Benesch. The effect of organic phosphates from the human erythrocyte on the allosteric properties of hemoglobin. Biochem. Biophys. Res. Commun. 26: 162–167, 1967.
 18. Benesch, R., and R. E. Benesch. Homos and heteros among the hemos. Science Wash. DC 185: 905–908, 1974.
 19. Benesch, R. E., R. Benesch, and C. I. Yu. The oxygenation of hemoglobin in the presence of 2,3‐diphosphoglycerate. Effect of temperature, pH, ionic strength, and hemoglobin concentration. Biochemistry 8: 2567–2571, 1969.
 20. Bennett, A. F., and J. Ruben. High altitude adaptation and anaerobiosis in sceloporine lizards. Comp. Biochem. Physiol. A Comp. Physiol. 50: 105–108, 1975.
 21. Bonaventura, J., C. Bonaventura, and B. Sullivan. Hemoglobins and hemocyanins: comparative aspects of structure and function. J. Exp. Zool. 194: 155–174, 1975.
 22. Bonaventura, J., and S. C. Wood. Respiratory pigments: overview. Am. Zool. 20: 5–6, 1980.
 23. Bunn, H. F. Evolution of mammalian hemoglobin function. Blood 58: 189–197, 1981.
 24. Burke, J. D. Vertebrate blood oxygen capacity and body weight. Nature Lond. 212: 46–48, 1966.
 25. Carey, F. H. Warm fish. In: A Companion to Animal Physiology, edited by C. R. Taylor, K. Johansen, and L. Bolis. Cambridge, UK: Cambridge Univ. Press, 1982, p. 216–223.
 26. Chanutin, A., and R. R. Curnish. Factors influencing the electrophoretic patterns of red cell hemolysates analyzed in cacodylate buffers. Arch. Biochem. Biophys. 106: 433–439, 1964.
 27. Chanutin, A., and R. R. Curnish. Effect of organic and inorganic phosphates on the oxygen equilibrium of human erythrocytes. Arch. Biochem. Biophys. 121: 96–102, 1967.
 28. Coates, M. L. Hemoglobin function in the vertebrates: an evolutionary model. J. Mol. Evol. 6: 285–307, 1975.
 29. Dawson, W. R., and T. L. Poulson. Oxygen capacity of lizard blood. Am. Midl. Nat. 68: 154–163, 1962.
 30. Dejours, P. (editor). Principles of Comparative Respiratory Physiology. Amsterdam: North‐Holland, 1975.
 31. Dejours, P., W. F. Garey, and H. Rahn. Comparison of ventilatory and circulatory flow rates between animals in various physiological conditions. Respir. Physiol. 9: 108–117, 1970.
 32. DeVenuto, F., H. I. Friedman, J. R. Neville, and C. C. Peck. Appraisal of hemoglobin solution as a blood substitute. Surg. Gynecol. Obstet. 149: 417–436, 1979.
 33. Douglas, E. L., W. A. Friedl, and G. V. Pickwell. Fishes in oxygen‐minimum zones: blood oxygenation characteristics. Science Wash. DC 191: 957–959, 1976.
 34. Duhm, J. The effect of 2,3‐DPG and other organic phosphates on the Donnan equilibrium and the oxygen affinity of human blood. In: Oxygen Affinity of Hemoglobin and Red Cell Acid‐Base Status, edited by M. Rørth and P. Astrup. Copenhagen: Munksgaard, 1972, p. 583–598. (Alfred Benzon Symp., 4th, 1971.)
 35. Eaton, J. W., T. D. Skelton, and E. Berger. Survival at extreme altitude: protective effect of increased hemoglobin‐oxygen affinity. Science Wash. DC 183: 743–744, 1974.
 36. Eaton, W. A. The relationship between coding sequences and function in haemoglobin. Nature Lond. 284: 183–185, 1980.
 37. Eddy, F. B. Oxygen uptake by rainbow trout blood Salmo gairdneri. J. Fish Biol. 10: 87–90, 1977.
 38. Edsall, J. T. Hemoglobin and the origins of the concept of allosterism. Federation Proc. 39: 226–235, 1980.
 39. Else, P. L., and A. J. Hulbert. Comparison of the “mammal machine” and the “reptile machine”: energy production. Am. J. Physiol. 240 (Regulatory Integrative Comp. Physiol. 9): R3–R9, 1981.
 40. Flores, G., and E. Frieden. Induction and survival of hemoglobin‐less and erythrocyte‐less tadpoles and young bull‐frogs. Science Wash. DC 159: 101–103, 1968.
 41. Frans, A., Z. Turek, H. Yokota, and F. Kreuzer. Effect of variations in blood hydrogen ion concentration on pulmonary gas exchange of artificially ventilated dogs. Pfluegers Arch. 380: 35–39, 1979.
 42. Gahlenbeck, H., and H. Bartels. Temperaturadaptation der Sauerstoffaffinitat des Blutes von Rana esculenta L. Z. Vgl. Physiol. 59: 232–240, 1968.
 43. Gahlenbeck, H., and H. Bartels. Blood gas transport properties in gill and lung forms of the axolotl (Ambystoma mexicanum). Respir. Physiol. 9: 175–182, 1970.
 44. Garby, L., and J. H. Meldon (editors). The Respiratory Functions of Blood. New York: Plenum, 1977, p. 282.
 45. Gerlach, E., and J. Duhm. 2,3‐DPG metabolism of red cells: regulation and adaptive changes during hypoxia. In: Oxygen Affinity of Hemoglobin and Red Cell Acid‐Base Status, edited by M. Rørth and P. Astrup. Copenhagen: Munksgaard, 1972, p. 552–569. (Alfred Benzon Symp., 4th, 1971.)
 46. Gilbert, W. Why genes in pieces? Nature Lond. 271: 501, 1978.
 47. Gillen, R. G., and A. Riggs. The haemoglobins of a fresh‐water teleost, Cichlasoma cyanoguttatum (Baird and Girard). I. The effects of phosphorylated organic compounds upon the oxygen equilibria. Comp. Biochem. Physiol. B Comp. Biochem. 38: 585–595, 1971.
 48. Goniakowska, L. The respiration of erythrocytes of some amphibia in vitro. Bull. Acad. Pol. Sci. Ser. Sci. Biol. 18: 793–797, 1970.
 49. Goodman, M. G., W. Moore, and G. Matsuda. Darwinian evolution in the genealogy of haemoglobin. Nature Lond. 253: 603–608, 1975.
 50. Gratzer, W. B., and A. C. Allison. Multiple haemoglobins. Biol. Rev. Camb. Philos: Soc. 35: 459–503, 1960.
 51. Greenwald, I. A new type of phosphoric acid compound isolated from blood with some remarks on the effect of substitution on the notation of l‐glyceric acid. J. Biol. Chem. 63: 339–349, 1925.
 52. Grigg, G. Temperature‐induced changes in the oxygen equilibrium curve of the blood of the brown bullhead, Ictalurus nebulosus. Comp. Biochem. Physiol. 29: 1203–1223, 1969.
 53. Gulliver, G. On red blood corpuscles. Proc. Zool. Soc. Lond. p. 474–495, 1875.
 54. Haab, P. E., J. Piiper, and H. Rahn. Simple method for rapid determination of an O2 dissociation curve of the blood. J. Appl. Physiol. 15: 1148–1149, 1960.
 55. Hansen, V. K., and K. G. Wingstrand. Further studies on the non‐nucleated erythrocytes of Maurolicus mulleri, and comparison with the red cells of related fishes. Dana‐Rep. Carlsberg Found. 54: 3–14, 1960.
 56. Hashimoto, K., Y. Yamaguchi, and F. Matsura. Comparative studies on the two hemoglobins of salmon. IV. Oxygen dissociation curve. Bull. Jpn. Soc. Sci. Fish. 26: 827–830, 1960.
 57. Heisler, N. Comparative aspects of acid‐base regulation. In: Acid‐Base Regulation in Animals, edited by N. Heisler. Amsterdam: Elsevier, in press.
 58. Hemmingsen, A. M. Energy metabolism as related to body size and respiratory surfaces and its evolution. Rep. Steno. Mem. Hosp. Nord. Insulinlab. 9: 1–110, 1960.
 59. Hemmingsen, E. A., and E. L. Douglas. Respiratory characteristics of the haemoglobin‐free fish Chaenocephalus aceratus. Comp. Biochem. Physiol. 33: 733–744, 1970.
 60. Hochachka, P. W., and G. N. Somero. Strategies of Biochemical Adaptation. Philadelphia, PA: Saunders, 1973, p. 841–842.
 61. Hock, R. J. Animals in high altitudes: reptiles and amphibians. In: Handbook of Physiology. Adaptation to the Environment, edited by D. B. Dill and E. F. Adolph. Washington, DC: Am. Physiol. Soc., 1964, sect. 4, chapt. 53, p. 841–842.
 62. Holle, J. P., M. Meyer, and P. Scheid. Oxygen affinity of duck blood determined by in vivo and in vitro technique. Respir. Physiol. 29: 355–361, 1977.
 63. Houston, A. H., and D. Cyr. Thermoacclimatory variation in the haemoglobin systems of goldfish. (Carassius auratus) and rainbow trout (Salmo gairdneri). J. Exp. Biol. 61: 455–461, 1974.
 64. Hoyt, R. W. Respiratory Function in Tiger Salamanders: Effects of Metamorphosis and Hypoxia. Albuquerque: Univ. of New Mexico, 1981. PhD Thesis.
 65. Hutchison, V. H., H. B. Haines, and G. Engbretson. Aquatic life at high altitude: respiratory adaptations in the Lake Titicaca frog, Telmatobius culeus. Respir. Physiol. 27: 115–129, 1976.
 66. Jackson, D. C., and K. Schmidt‐Nielsen. Heat production during diving in the fresh water turtle, Pseudemys scripta. J. Cell. Physiol. 67: 225–231, 1966.
 67. Johansen, K. Cardiovascular support of metabolic functions in vertebrates. In: Lung Biology in Health and Disease. Evolution of Respiratory Processes: A Comparative Approach, edited by S. C. Wood and C. Lenfant. New York: Dekker, 1979, vol. 13, p. 107–192.
 68. Johansen, K., and C. Lenfant. A comparative approach to the adaptability of O2‐Hb affinity. In: Oxygen Affinity of Hemoglobin and Red Cell Acid‐Base Status, edited by M. Rørth and P. Astrup. Copenhagen: Munksgaard, 1972, p. 750–780. (Alfred Benzon Symp., 4th, 1971.)
 69. Johansen, K., G. Lykkeboe, S. Kornerup, and G. M. O. Maloiy. Temperature insensitive O2 binding in blood of the tree frog, Chiromantis petersi. J. Comp. Physiol. 136: 71–76, 1980.
 70. Johansen, K., G. Lykkeboe, R. E. Weber, and G. M. O. Maloiy. Respiratory properties of blood in awake and estivating lungfish, Protopterus amphibius. Respir. Physiol. 27: 335–345, 1976.
 71. Johansen, K., and R. E. Weber. On the adaptability of haemoglobin function to environmental conditions. In: Perspectives in Experimental Biology. Zoology and Botany, edited by P. Spencer Davis and N. Sunderland. New York: Pergamon, 1976, vol. 1, p. 219–234.
 72. Jones, D. R. Oxygen consumption and heart rate of several species of anurans and amphibians during submergence. Comp. Biochem. Physiol. 20: 691–707, 1967.
 73. Jones, D. R. Theoretical analysis of factors which may limit the maximum oxygen uptake of fish: the oxygen cost of the cardiac and branchial pumps. J. Theor. Biol. 32: 341–349, 1971.
 74. Klotz, I. M., and T. A. Klotz. Oxygen carrying proteins: a comparison of the oxygenation reaction in hemocyanin with that in hemoglobin. Science Wash. DC 121: 477–480, 1955.
 75. Krogh, A. Comparative Physiology of Respiratory Mechanisms. Philadelphia: Univ. of Pennsylvania Press, 1941.
 76. Krogh, A., and I. Leitch. The respiratory functions of the blood in fishes. J. Physiol. Lond. 52: 288–297, 1919.
 77. Lahiri, S. Blood oxygen affinity and alveolar ventilation in relation to body weight in mammals. Am. J. Physiol. 229: 529–536, 1975.
 78. Leftwich, F. B., and J. D. Burke. Blood oxygen capacity in Ranid frogs. Am. Midl. Nat. 72: 241–248, 1964.
 79. Lenfant, C., and C. Aucutt. Oxygen uptake and change in carbon dioxide tension in human blood stored at 37C. J. Appl. Physiol. 20: 503–508, 1965.
 80. Lenfant, C., and K. Johansen. Respiratory adaptations in selected amphibians. Respir. Physiol. 2: 247–260, 1967.
 81. Lenfant, C., K. Johansen, and G. C. Grigg. Respiratory properties of blood and pattern of gas exchange in the lungfish Neoceratodus forsteri. Respir. Physiol. 2: 1–21, 1966.
 82. Lenfant, C., K. Johansen, and D. Hanson. Bimodal gas exchange and ventilation‐perfusion relationship in lower vertebrates. Federation Proc. 29: 1124–1129, 1970.
 83. Lenfant, C., J. Torrance, E. English, C. A. Finch, C. Reynafarje, C. Ramos, and J. Faura. Effect of altitude on oxygen finding by hemoglobin and on organic phosphate levels. J. Clin. Invest. 47: 2652–2656, 1968.
 84. Lutz, P. L., I. S. Longmuir, J. V. Tuttle, and K. Schmidt‐Nielsen. Dissociation curve of bird blood and effect of red cell oxygen consumption. Respir. Physiol. 17: 269–275, 1973.
 85. Lykkeboe, G., and R. E. Weber. Changes in the respiratory properties of the blood in the carp, Cyprinus carpio, induced by diurnal variation in ambient oxygen tension. J. Comp. Physiol. 128: 117–125, 1978.
 86. MacFarlane, H. T., and A. H. T. Robb‐Smith (editors). Functions of the Blood. New York: Academic, 1961.
 87. Maginniss, L. A., Y. K. Song, and R. B. Reeves. Oxygen equilibria of ectotherm blood containing multiple hemoglobins. Respir. Physiol. 42: 329–343, 1980.
 88. McCutcheon, F. J., and F. G. Hall. Hemoglobin in the amphibia. J. Cell Comp. Physiol. 9: 191–197, 1937.
 89. Morpurgo, G., P. A. Battaglia, and T. Leggio. Negative Bohr effect in newt haemolysates and its regulation. Nature Lond. 225: 76–77, 1970.
 90. Morse, M. D., D. E. Cassals, and M. Holder. The position of the oxygen dissociation curve of the blood in cyanotic congenital heart disease. J. Clin. Invest. 29: 1098–1103, 1950.
 91. Parer, J. T. Oxygen transport in human subjects with hemoglobin variants having altered oxygen affinity. Respir. Physiol. 9: 43–49, 1970.
 92. Perutz, M. F. Stereochemistry of cooperative effects in haemoglobin. Nature Lond. 228: 726–739, 1970.
 93. Perutz, M. F. Nature of haem‐haem interaction. Nature Lond. 237: 495–499, 1970.
 94. Pough, F. H. The effect of temperature on oxygen capacity of reptile blood. Physiol. Zool. 49: 141–151, 1976.
 95. Pough, F. H. Ontogenetic change in molecular and functional properties of blood of garter snakes, Thamnophis sirtalis. J. Exp. Zool. 201: 47–55, 1977.
 96. Powers, D. A. Molecular ecology of teleost fish hemoglobins: strategies for adaptation to changing environments. Am. Zool. 20: 139–162, 1980.
 97. Powers, D. A., J. P. Martin, R. L. Garlick, and H. J. Fyhn. The effect of temperature on the oxygen equilibrium of fish haemoglobin in relation to environmental thermal variability. Comp. Biochem. Physiol. A Comp. Physiol. 62: 82–94, 1979.
 98. Prothero, J. W. Maximal oxygen consumption in various animals and plants. Comp. Biochem. Physiol. A Comp. Physiol. 64: 463–466, 1979.
 99. Rahn, H. Evolution of the gas transport system in vertebrates. Proc. R. Soc. Med. 59: 493–494, 1966.
 100. Rappoport, S., and G. M. Guest. Distribution of acid‐soluble phosphorus in the blood cells of various vertebrates. J. Biol. Chem. 138: 269–282, 1941.
 101. Reeves, R. B., and H. Rahn. Patterns in vertebrate acid‐base regulation. In: Lung Biology in Health and Disease. Evolution of Respiratory Processes: A Comparative Approach, edited by S. C. Wood and C. Lenfant. New York: Dekker, 1979, vol. 13, p. 225–252.
 102. Riggs, A. The nature and significance of the Bohr effect in mammalian hemoglobin. J. Gen. Physiol. 4: 737–752, 1960.
 103. Riggs, A. Factors in the evolution of hemoglobin function. Federation Proc. 35: 2115–2118, 1976.
 104. Root, R. W. The respiratory function of blood of marine fishes. Biol. Bull. Woods Hole 61: 427–456, 1931.
 105. Root, R. W., L. Irving, and E. C. Black. The effect of hemolysis upon the combination of oxygen with the blood of some marine fishes. J. Cell. Comp. Physiol. 13: 303–313, 1939.
 106. Rossoff, L., R. Zeldin, E. Hew, and A. Aberman. Changes in blood P50. Effects on oxygen delivery when arterial hypoxemia is due to shunting. Chest 77: 142–146, 1980.
 107. Scheid, P., and T. Kawashiro. Metabolic changes in avian blood and their effects on determination of blood gases and pH. Respir. Physiol. 23: 291–300, 1975.
 108. Schmidt‐Nielsen, K. Animal Physiology. Cambridge, UK: Cambridge Univ. Press, 1978.
 109. Schmidt‐Nielsen, K., and J. L. Larimer. Oxygen dissociation curves of mammalian blood in relation to body size. Am. J. Physiol. 195: 424–428, 1958.
 110. Schmidt‐Nielsen, K., and C. R. Taylor. Red blood cells: why or why not? Science Wash. DC 162: 274–275, 1968.
 111. Schweiger, H. G. Pathways of metabolism in nucleate and anucleate erythrocytes. Int. Rev. Cytol. 13: 135–201, 1962.
 112. Scott, A. F., H. F. Bunn, and A. H. Brush. Functional aspects of hemoglobin evolution in the mammals. J. Mol. Evol. 8: 311–316, 1976.
 113. Shappell, S. D., and C. Lenfant. Physiological role of the oxyhemoglobin dissociation curve. In: The Red Blood Cell (2nd ed.), edited by D. M. Surgenor. New York: Academic, 1974, p. 842–873.
 114. Shoubridge, E. A., and P. W. Hochachka. Ethanol: novel end product of vertebrate anaerobic metabolism. Science Wash. DC 209: 308–309, 1980.
 115. Snyder, G. K. Erythrocyte evolution: the significance of the Fahraeus‐Lindqvist phenomenon. Respir. Physiol. 19: 271–278, 1973.
 116. Snyder, G. K. Blood corpuscles and blood hemoglobins: a possible example of coevolution. Science Wash. DC 195: 412–413, 1977.
 117. Soivio, A., M. Nikinmaa, and K. Westman. The blood oxygen binding properties of hypoxic Salmo gairdneri. J. Comp. Physiol. 136: 83–87, 1980.
 118. Stamatoyannopoulos, G., A. J. Bellingham, and C. Lenfant. Abnormal hemoglobins with high and low oxygen affinity. Annu. Rev. Med. 22: 221–234, 1971.
 119. Sullivan, B., and A. Riggs. Haemoglobin: reversal of oxidation and polymerization in turtle red cells. Nature Lond. 204: 1098–1099, 1964.
 120. Taketa, F., and M. A. Nickerson. Hemoglobin of the aquatic salamander, Cryptobranchus. Comp. Biochem. Physiol. A Comp. Physiol. 46: 583–591, 1973.
 121. Toews, D., and D. MacIntyre. Blood respiratory properties of a viviparous amphibian. Nature Lond. 266: 464–465, 1977.
 122. Tracy, C. R. Minimum size of mammalian homeotherms: role of the thermal environment. Science Wash. DC 198: 1034–1035, 1977.
 123. Turek, Z., and F. Kreuzer. Effects of shifts of the O2 dissociation curve upon alveolar‐arterial O2 gradients in computer models of the lung with ventilation‐perfusion mismatching. Respir. Physiol. 45: 133–139, 1972.
 124. Van Den Thillart, G. Adaptations offish energy metabolism to hypoxia and anoxia. Mol. Physiol. 2: 49–61, 1982.
 125. Vinegar, A., and S. D. Hillyard. The effects of altitude on oxygen‐binding parameters of the blood of the iguanid lizards, Sceloporus jarrovi and Sceloporus occidentalis. Comp. Biochem. Physiol. A Comp. Physiol. 43: 317–320, 1972.
 126. Weathers, W. W., and J. J. McGrath. Acclimation to simulated altitude in the lizard, Dipsosaurus dorsalis. Comp. Biochem. Physiol. A Comp. Physiol. 42: 263–268, 1977.
 127. Weber, R. E., S. C. Wood, and J. P. Lomholt. Temperature acclimation and oxygen binding properties of blood and multiple haemoglobins of rainbow trout. J. Exp. Biol. 65: 333–345, 1976.
 128. White, F. N., and G. Ross. Circulatory changes during experimental diving in the turtle. Am. J. Physiol. 211: 15–18, 1966.
 129. Wood, S. C. Effect of metamorphosis on blood respiratory properties and erythrocyte adenosine triphosphate level of the salamander, Dicamptodon ensatus. Respir. Physiol. 12: 53–65, 1971.
 130. Wood, S. C. Adaptation of red blood cell function to hypoxia and temperature in ectothermic vertebrates. Am. Zool. 20: 163–172, 1980.
 131. Wood, S. C. Effect of O2 affinity on arterial Po2 in animals with central vascular shunts. J. Appl. Physiol. 53: 1360–1364, 1982.
 132. Wood, S. C. Cardiovascular shunts and oxygen transport in lower vertebrates. Am. J. Physiol. 247 (Regulatory Integrative Comp. Physiol. 16): R3–R14, 1984.
 133. Wood, S. C., J. W. Hicks, and R. K. Dupre. Hypoxic reptiles: hearts, heat, and hemoglobin. Am. Zool. In press.
 134. Wood, S. C., and K. Johansen. Adaptation to hypoxia by increased HbO2 affinity and decreased red cell ATP concentration. Nature New Biol. 237: 278–279, 1972.
 135. Wood, S. C., K. Johansen, and R. E. Weber. Haemoglobin in the coelacanth. Nature Lond. 239: 283–285, 1972.
 136. Wood, S. C., and C. Lenfant. Respiration: mechanics, control, and gas exchange. In: Biology of the Reptilia, edited by C. Gans and W. R. Dawson. New York: Academic, 1976, vol. 5, p. 225–274.
 137. Wood, S. C., and C. Lenfant. Oxygen transport and oxygen delivery. In: Lung Biology in Health and Disease. Evolution of Respiratory Processes: A Comparative Approach, edited by S. C. Wood and C. Lenfant. New York: Dekker, 1979, vol. 13, p. 193–223.
 138. Woodson, R. D. Physiological significance of oxygen dissociation curve shifts. Crit. Care Med. 7: 368–373, 1979.
 139. Zaaijer, J. P., and P. Wolvekamp. Some experiments on the hemoglobin oxygen affinity in the blood of the ramshorn (Planorbis corneus L.). Acta Physiol. Pharmacol. Neerl. 7: 56–77, 1958.

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How to Cite

Stephen C. Wood, Claude Lenfant. Phylogeny of the Gas‐Exchange System: Red Cell Function. Compr Physiol 2011, Supplement 13: Handbook of Physiology, The Respiratory System, Gas Exchange: 131-146. First published in print 1987. doi: 10.1002/cphy.cp030408