Summary
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(1)
Artificially ventilated curarised frogs consumed 23% less oxygen than animals breathing naturally but their respiratory quotient was significantly increased. Artificial ventilation maintained arterial oxygen tension at normal levels but arterial carbon dioxide tension fell significantly. When 90% of the haemoglobin was combined with carbon monoxide oxygen consumption was reduced by 40% and the respiratory quotient was increased.
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(2)
During apnoea both normal animals and those exposed to carbon monoxide showed reductions in oxygen uptake of about 45%. Heart rate also declined by 20–40%. During apnoea respiratory quotient of both groups of animals was significantly elevated. In normal animals arterial and venous oxygen tensions fell during apnoea, arterial tensions to 20% of the ventilation value and venous oxygen tensions to a slightly higher value. Arterial oxygen content fell from 9.6 vols % to 3 vols %. Arterial carbon dioxide tensions and contents increased during the apnoea and arterial pH fell.
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(3)
When ventilation was restored frogs consumed about 109–130 μl more oxygen in the first 10 min than in comparable periods before the apnoea. However, animals with 90% of the haemoglobin combined with carbon monoxide showed only a gradual return to the pre-apnoeic level of oxygen consumption. Heart rate, respiratory quotient and blood gas tensions returned to pre-apnoeic levels within 30 min of the resumption of artificial ventilation. The excess oxygen consumed during the first 10 min was equal to the amount of oxygen calculated to have been removed from the oxygen store of the blood during apnoea.
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It is concluded that the blood has a function in maintaining oxygen metabolism in both ventilated and apnoeic frogs but that oxygen stores, including that of the blood, make little contribution to oxygen metabolism during apnoea and appear to be replenished immediately lung ventilation is restored.
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References
Andersen, H. T.: The elicitation of physiological responses to diving. Oslo: Universitetsforlaget, 1963.
Andersen, H. T.: Physiological adaptations in diving vertebrates. Physiol. Rev.46 (2), 212–243 (1966).
Andersen, H. T., Hustvedt, B. E., Løvø, A.: Acid-base changes in diving ducks. Acta physiol. scand.63, 128–132 (1965).
Aubert, H.: Über den Einfluß der Temperatur auf die Kohlensäure Ausscheidung und die Lebensfähigkeit der Frösche in sauerstoffloser Luft. Arch. Anat. Physiol.26, 293–323 (1881).
Belkin, D.: Anaerobiosis in diving turtles. (Abstract). Physiologist5, 105–112 (1962).
Blazka, P.: The anaerobic metabolism of fish. Physiol. Zool.31, 117–128 (1958).
Bohr, C.: Über die Haut- und Lungenatmung der Frösche. Skand. Arch. Physiol.10, 74 (1900).
Czopek, J.: The vascularization of the respiratory surfaces of some Salientia. Zoologica Pol.6, 101–134 (1955).
Czopek, J.: Vascularization of respiratory surfaces in some Caudata. Copeia, 576–587 (1962).
Derrickson, M. B., Amberson, W. R.: Blood volume in lower vertebrates. Biol. Bull. Woods Hole67, 329–345 (1934).
Dolk, H. E., Postma, N.: Über die Haut- und die Lungenatmung vonRana temporaria. Z. vergl. Physiol.5, 417–444 (1927).
Gahlenbeck, H., Bartels, H.: Temperatur Adaptation der Sauerstoffaffinität des Blutes vonRana esculenta L. Z. vergl. Physiol.59, 232–240 (1968).
Graaf, A. R. de: Investigations into the distribution of blood in the heart and aortic arches ofXenopus laevis (Daud). J. exp. Biol.34, (2), 143–172 (1957).
Graaf, A. R. de: A note on the oxygen requirements ofXenopus laevis. J. exp. Biol.34 (2), 173–176 (1957).
Grehant: C. R. Soc. Biol. (Paris)39, 198 (1887). (cited by Nicloux, 1923).
Hall, F. G.: Hemoglobin functions in the blood ofBufo marinus. J. cell. Physiol.68 (1), 69–74 (1966).
Hemmingsen, A.: Energy metabolism as related to body size and respiratory surfaces and its evolution. Rep. Steno Mem. Hosp.9, 1–110 (1960).
Hutchison, V. H., Whitford, W. G., Kohl, M.: Relation of body size and surface area to gas exchange in anurans. Physiol. Zool.41 (1), 65–85 (1968).
Irving, L., Scholander, P. F., Grinnell, S. W.: Experimental studies of the respiration of sloths. J. cell. comp. Physiol.20, 189–210 (1942).
Jones, D. R.: Experiments on amphibian respiratory and circulatory systems. In: Experiments in physiology and biochemistry, vol. 3., ed. by G. A. Kerkut. London and New York: Academic Press 1970.
Jones, D. R.: Oxygen consumption and heart rate of several species of anuran amphibia during submergence. Comp. Biochem. Physiol.20, 691–707 (1967).
Jones, D. R., Shelton, G.: Factors influencing submergence and the heart rate in the frog. J. exp. Biol.41, 417–431 (1964).
Krogh, A.: On the cutaneous and pulmonary respiration of the frog. Skand. Arch. Physiol.15, 328–419 (1904).
Leggio, T., Morpurgo, G.: Dissociation curves of toad haemoglobin and a hypothesis for the cause of hibernation. Nature (Lond.)219 (5153), 493–494 (1968).
Leivestad, H.: The effect of prolonged submersion on the metabolism and the heart rate in the toad. Arbok. Univ. Bergen,5, 1–15 (1960).
Lenfant, C., Johansen, K.: Respiratory adaptations in selected amphibians. Resp. Physiol.2, 247–260 (1967).
Mären, T. H.: Carbonic anhydrase: Chemistry, physiology, and inhibition. Physiol. Rev.47 (4), 595–781 (1967).
McCutcheon, F. H.: Hemoglobin function during the life history of the bullfrog. J. cell. comp. Physiol.8, 63–81 (1936).
Menon, K. R.: A comparative study of blood volume in some vertebrates. J. Univ. Bombay.20 (5), 47–51 (1952).
Nicloux, M.: Considérations générals sur l'intoxication oxycarbonique et la quantité minima d'oxygène nécessaire dans le sang pour assurer la vie; leur intérêt thérapeutique. C. R. Soc. Biol. (Paris)89, 1311–1334 (1923).
Peyrot, A., Pennisi, F., Biciotti, M.: Mesure du volume total et du pourcentage du sang chez le triton crete (Triturus cristatus carnifex (Laur). Dosage par dilution radio-isotopique. Z. vergl. Physiol.50, 88–90 (1965).
Piiper, J.: Physiologial equilibria of gas cavities in the body. In: Handbook of physiology, sec. 3., Respiration, vol. II, p. 1205–1218, eds. W. O. Fenn and H. Rahn. Washington, D. C.: Amer. Physiol. Soc. 1965.
Poczopko, P.: Cutaneous vasomotor response in the edible frog (Rana esculenta L.) to changes in carbon dioxide and oxygen concentration. Bull. Acad. pol. Sci. Cl. II, Ser. Sci. biol.4, 397–403 (1956).
Poczopko, P.: Further investigations on the cutaneous vasomotor reflexes in the edible frog with connexion with the problem of regulation of cutaneous respiration in frogs. Zoologica Pol.8, 161–175 (1957).
Poczopko, P.: On the seasonal variability of cutaneous vasomotor reflexes in the edible frog (Rana esculenta L.) Zoologica Pol.9, 115–129 (1958).
Poczopko, P.: Respiratory exchange inRana esculenta L. in different respiratory media. Zoologiea Pol.10, 45–55 (1959).
Prosser, C. L., Brown, F. A.: Comparative animal physiology, sec. ed. Philadelphia: W. B. Saunders Co. 1961.
Prosser, C. L., Weinstein, S. J. F.: Comparison of blood volumes in animals with open and closed circulatory systems. Physiol. Zool.23, 113–124 (1950).
Rahn, H.: Gasometric method for measurement of tissue oxygen tension. Fed. Proc.16, 685–688 (1957).
Riggs, A. F.: The metamorphosis of hemoglobin in the bullfrog. J. gen. Physiol.35, 23–10 (1951).
Robin, E. D., Vester, J. W., Murdaugh, M. V., Millen, J. E.: Prolonged anaerobiosis in a vertebrate: anaerobic metabolism in the freshwater turtle. J. cell. comp. Physiol.63 (3), 287–297 (1964).
Rose, F. L., Drotman, R. B.: Anaerobiosis in a frog,Rana pipens. J. exp. Zool.166 (3), 427–432 (1967).
Rubner, M.: Über den Einfluß der Körpergröße auf Stoff- und Kraftwechsel. Z. Biol.19, 535–562 (1883).
Salthe, S. N.: Comparative catalytic studies of lactic dehydrogenases in the amphibia: environmental and physiological correlations. Comp. Biochem. Physiol.16, 393–408 (1965).
Scholander, P. F.: Volumetric respirometer for aquatic animals. Rev. sci. Instr.20, 885–887 (1949).
Scholander, P. F.: Experimental investigations on the respiratory function in diving mammals and birds. Hvalråd. Skr.22, 1–131 (1940).
Severinghaus, J. W., Stupel, M., Bradley, A. F.: Accuracy of blood pH and pCO2 determinations. J. appl. Physiol.9, 189–196 (1956a).
Severinghaus, J. W., Stupel, M., Bradley, A. F.: Variations of serum carbonic pK1 with pH and temperature. J. appl. Physiol.9, 197–200 (1956b).
Shelton, G.: The effect of lung ventilation on blood flow to the lungs and body of the amphibian,Xenopus laevis. Resp. Physiol.9, 183–196 (1970).
Simkiss, K.: Calcium and carbonate metabolism in the frog (Rana temporaria) during respiratory acidosis. Amer. J. Physiol.214 (3), 627–634 (1968).
Strawinski, S.: Vascularization of respiratory surfaces in ontogeny of the edible frog.Rana esculenta L. Zoologica Pol.7, 327–365 (1956).
Sulze, W.: Über die physiologische Bedeutung des Kalksäckchenapparates der Amphibien. Pflügers Arch. ges. Physiol.246, 250–257 (1942).
Szarski, H.: The structure of respiratory organs in relation to body size in amphibia. Evolution, Lancaster, Pa.18 (1), 118–126 (1964).
Theorell, H.: Kristallinisches Myoglobin. I. Mitteilung: Kristallisieren und Reinigung des Myoglobins sowie vorläufige Mitteilung über sein Molekulargewicht. Biochem. Z.252, 1–7 (1932).
Van Liew, H. D.: Oxygen and carbon dioxide tensions in tissue and blood of normal and acidotic rats. J. appl. Physiol.25, 575–580 (1968).
Whitford, W. G., Hutchison, V. H.: Body size and metabolic rate in salamanders. Physiol. Zool.40 (2) 127–133 (1967).
Whitford, W. G., Hutchison, V. H.: Gas exchange in salamanders. Physiol. Zool.38 (3), 228–242 (1965).
Wilson, B., Hansard, S. L., Cole, B. T.: Total blood volume of the turtle and the frog. Proc. La. Acad. Sci.23, 45–52 (1960).
Wolvekamp, H. P.: Untersuchungen über den Sauerstofftransport durch Blutpigmente beiHelix, Rana undPlanorbis. Z. vergl. Physiol.16, 1–38 (1932).
Wolvekamp, H. P., Lodewijks, J. M.: Über die Sauerstoffbindung durch Hämoglobin von Fröschen (Rana esculenta undRana temporaria). Z. vergl. Physiol.20, 382–387 (1934).
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I am grateful to Mr. B. Eddy for performing the measurements of blood gas contents and to Dr. R. L. Saunders for some technical assistance. Part of this work was supported by an operating grant from the National Research Council of Canada.
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Jones, D.R. Anaerobiosis and the oxygen debt in an anuran amphibian,Rana esculenta (L.). J. Comp. Physiol. 77, 356–382 (1972). https://doi.org/10.1007/BF00694941
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DOI: https://doi.org/10.1007/BF00694941