Abstract
The gonads of sea urchins undergo large changes in mass during their gametogenic cycle. In addition, they have relatively low aerobic capacities and are poorly perfused by the circulatory system and thus are continually hypoxic or anoxic. The present study of Strongylocentrotus droebachiensis investigates seasonal changes in the relationships among mass of the ovaries, pH and PO2 of the perivisceral coelomic fluid which bathes the ovaries, and partitioning of ovary energy metabolism into its anaerobic and aerobic components. S. droebachiensis were collected at Blue Hill Falls, Maine, USA, from August 1982 to March 1984. We found that from 76 to 92% of the heat dissipated by isolated ovaries of the sea urchin S. droebachiensis derives from anaerobic energy metabolism at partial pressures of oxygen prevailing in vivo. Ovaries from S. droebachiensis have the capacity to produce large amounts of lactate under imposed anoxia, but lactate accounts for only 37% of the total anoxic heat dissipation, which suggests that other end products of anaerobiosis are present. Seasonal changes in pH and PO2 of the perivisceral coelomic fluid can be explained by a complex relationship among changes in temperature, reproductive condition, and anaerobic and aerobic metabolism in the ovaries, gut and body wall. Seasonal changes in the buffering capacity of the perivisceral coelomic fluid must be determined before the effects of respiratory and metabolic acid production on the acid-base status of the coelomic fluid can be fully understood.
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Literature cited
Aketa, K.: Quantitative analysis of lactic acid and related compounds in sea urchin eggs at the time of fertilization. Embryologia 3, 267–278 (1957)
Aketa, K.: Some comparative remarks on the transient change in lactic acid content in sea urchin eggs following fertilization. Expl Cell. Res. 3, 192–194 (1964)
Allen, W. V.: Interorgan transport of lipids in the purple sea urchin, Strongylocentrotus purpuratus. Comp. Biochem. Physiol. 47A, 1297–1311 (1974)
Belman, B. W. and A. C. Giese: Oxygen consumption of an asteroid and an echinoid from the Antarctic. Biol. Bull. mar. biol. Lab., Woods Hole 146, 157–164 (1974)
Curtin, N. A. and R. C. Woledge: Energy changes and muscular contraction. Physiol. Rev. 58, 690–761 (1978)
Diehl, W. J., III, L. McEdward, E. Proffitt, V. Rosenberg and J. Lawrence: The response of Luidia clathrata (Echinodermata: Asteroidea) to hypoxia. Comp. Biochem. Physiol. 62A, 669–671 (1979)
Ellington, W. R.: Glucose degradation and respiratory metabolism in starfish tissue. Fedn Proc. Fedn Am. Socs exp. Biol. 34, p. 466 (1975)
Ellington, W. R.: Intermediary metabolism. In: Echinoderm nutrition, pp 395–415. Ed. by M. Jangoux and J. M. Lawrence. Rotterdam: Balkema 1982
Ellington, W. R. and C. S. Hammen: Metabolic compensation to reduced oxygen tensions in the sea cucumber, Sclerodactyla briareus. J. comp. Physiol. 122, 347–358 (1977)
Ellington, W. R. and J. M. Lawrence: Malic and lactic dehydrogenase activities and ratios in regular and irregular echinoids. Comp. Biochem. Physiol. 45B, 727–730 (1973)
Farmanfarmaian, A.: The respiratory physiology of echinoderms. In: Physiology of Echinodermata, pp 245–265. Ed. by R. A. Boolootian. New York: John Wiley & Sons 1966
Giese, A. C.: Physiology of the echinoderm body wall. Thalassia jugosl. 12, 153–163 (1976)
Giese, A. C., A. Farmanfarmaian, S. Hilden and P. Doezem: Respiration during the reproductive cycle in the sea urchin, Strongylocentrotus purpuratus. Biol. Bull. mar. biol. Lab., Woods Hole 130, 192–201 (1966)
Gnaiger, E.: Direct and indirect calorimetry in the study of animal anoxibiosis. A review and the concept of ATP turnover. In: Thermal analysis, pp 547–552. Ed. by W. Hemminger. Basel: Birkhäuser 1980
Gnaiger, E.: Heat dissipation and energetic efficiency in animal anoxibiosis: economy contra power. J. exp. Zool. 228, 471–490 (1983a)
Gnaiger, E.: Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In: Polarographic oxygen sensors. pp 337–345. Ed. by E. Gnaiger and H. Forstner. Berlin: Springer-Verlag 1983b
Greenwood, P. J.: Growth, respiration and tentative energy budgets for two populations of the sea urchin Parechinus angulosus (Leske). Estuar. cstl mar. Sci. 10, 347–367 (1980)
Hansen, C. A. and B. D. Sidell: Atlantic hagfish cardiac muscle: metabolic basis of tolerance to anoxia. Am. J. Physiol. 244, R356-R362 (1983)
Holland, L. Z., A. C. Giese and J. H. Phillips: Studies of the perivisceral coelomic fluid protein concentration during seasonal and nutritional changes in the purple sea urchin. Comp. Biochem. Physiol. 21, 361–371 (1967)
Itzhaki, R. F. and D. M. Gill: A micro-biuret method for estimating proteins. Analyt. Biochem. 9, 401–410 (1964)
Lamprecht, W., P. Stein, F. Heniz and H. Weisser: Creatine phosphate. In: Methods of enzymatic analysis, pp 1777–1785. Ed. by H. U. Bergmeyer. New York: Academic Press 1974
Larson, B. R., R. L. Vadas and M. Keser: Feeding and nutritional ecology of the sea urchin Strongylocentrotus drobachiensis in Maine, USA. Mar. Biol. 59, 49–62 (1980)
Lawrence, J. M. and J. E. M. Lane: The utilization of nutrients by post-metamorphic echinoderms. In: Echinoderm nutrition, pp 331–371. Ed. by M. Jangoux and J. M. Lawrence. Rotterdam: Balkema 1982
Livingstone, D. R.: Invertebrate and vertebrate pathways of anaerobic metabolism: evolutionary considerations. J. geol. Soc. Lond. 140, 27–38 (1983)
Livingstone, D. R., A. DeZwaan, M. Leopold and E. Marteijn: Studies on the phylogenetic distribution of pyruvate oxidoreductases. Biochem. Syst. Ecol. 11, 415–425 (1983)
Lowry, O. H., and J. V. Passonneau: Lactate. In: Methods of enzymatic analysis, pp 1468–1472. Ed. by H. U. Bergmeyer. New York: Academic Press 1974
Mattisson, A. G. M.: Cytochrome c, cytochrome oxidase, and respiratory intensity in some types of invertebrate muscles. Ark. Zool. 12, 143–163 (1959)
Miller, R. J. and K. H. Mann: Ecological energetics of the seaweed zone in a marine bay on the Atlantic coast of Canada. III. Energy transformations by sea urchins. Mar. Biol. 18, 99–114 (1973)
Minakami, S. and C. H. DeVerdier: Calorimetric study on human erythrocyte glycolysis: heat production in various metabolic conditions. Eur. J. Biochem. 65, 451–460 (1976)
Pamatmat, M. M.: Simultaneous direct and indirect calorimetry. In: Polarographic oxygen sensors, pp 167–175. Ed. by E. Gnaiger and H. Forstner. Berlin: Springer-Verlag 1983
Parry, G. D.: The influence of the cost of growth on ectotherm metabolism. J. theor. Biol. 101, 453–477 (1983)
Perlzweig, W. A. and E. S. G. Barron: Lactic acid and carbohydrate in sea urchin eggs under aerobic and anaerobic conditions. J. biol. Chem. 79, 19–26 (1928)
Reeves, R. B.: An imidazole alphastat hypothesis for vertebrate acid-base regulation: tissue carbon dioxide content and body temperature in bullfrogs. Respir. Physiol. 14, 219–236 (1972)
Reeves, R. B. and H. Rahn: Patterns in vertebrate acid-base regulation: a comparative approach. In: Evolution of the respiratory processes, pp 225–252. Ed. by S. C. Wood and C. Lenfant. New York: Dekker 1979
Rothchild, Lord: Acid production after fertilization of sea urchin eggs. J. exp. Biol. 35, 843–849 (1958)
Sarch, M. N.: Die Pufferung der Körperflüssigkeiten bei Echinodermen. Z. vergl. Physiol. 14, 525–545 (1931)
Shick, J. M.: Physiological and behavioral responses to hypoxia and hydrogen sulfide in the infaunal asteroid Ctenodiscus crispatus. Mar. Biol. Lett. 2, 225–236 (1981)
Shick, J. M.: Respiratory gas exchange in the echinoderms. In: Echinoderm studies, Vol. 1. pp 67–110. Ed. by M. Jangoux and J. M. Lawrence. Rotterdam: Balkema 1983
Shick, J. M., A. DeZwaan, and A. M. T. DeBont: Anoxic metabolic rate in the mussel Mytilus edulis L. estimated by simultaneous direct calorimetry and biochemical analysis. Physiol. Zoöl. 56, 56–63 (1983)
Somero, G. N.: pH-temperature interactions on proteins: principles of optimal pH and buffer system design. Mar. Biol. Lett. 2, 163–178 (1981)
Theede, H., A. Ponat, K. Hiroki and C. Schlieper: Studies on the resistance of marine bottom invertebrates to oxygen-deficiency and hydrogen sulphide. Mar. Biol. 2, 325–337 (1969)
Webster, S. K. and A. C. Giese: Oxygen consumption of the purple sea urchin with special reference to the reproductive cycle. Biol. Bull. mar. biol. Lab., Woods Hole 148, 165–180 (1975)
White, F. N. and G. N. Somero: Acid-base regulation and phospholipid adaptation to temperature: time courses and physiological significance of modifying the milieu for protein function. Physiol. Rev. 62, 40–90 (1982)
Zammit, V. A. and E. A. Newsholme: The maximum activities of hexokinase, phosphorylase, phosphofructokinase, Glycerol phosphate dehydrogenase, lactate dehydrogenase, octopine dehydrogenase, phosphoenolpyruvate carboxykinase, nucleoside diphosphate kinase, glutamate-oxaloacetate transaminase and arginine kinase in relation to carbohydrate utilization in muscle from marine invertebrates. Biochem. J. 160, 447–462 (1976)
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Communicated by J. M. Lawrence, Tampa
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Bookbinder, L.H., Shick, J.M. Anaerobic and aerobic energy metabolism in ovaries of the sea urchin Strongylocentrotus droebachiensis . Marine Biology 93, 103–110 (1986). https://doi.org/10.1007/BF00428659
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DOI: https://doi.org/10.1007/BF00428659