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The Swimbladder of Deep-Sea Fish: The Swimbladder Wall is a Lipid-Rich Barrier to Oxygen Diffusion

Published online by Cambridge University Press:  11 May 2009

J. B. Wittenberg
Affiliation:
Department of Physiology, Albert Einstein College of Medicine, New York, New York 10461, U.S.A.
D. E. Copeland
Affiliation:
Marine Biological Laboratory, Woods Hole, Massachusetts 02543, U.S.A.
F R. L. Haedrich
Affiliation:
Memorial University of Newfoundland, St John's A1B 3X9, Canada.
J. S. Child
Affiliation:
Marine Biological Laboratory, Woods Hole, Massachusetts 02543, U.S.A.

Extract

The swimbladder of teleost fishes is a gas-filled sac which serves primarily to make the fish neutrally buoyant in sea water, but occasionally assumes other functions. The gas contained in the swimbladder is largely oxygen, at a pressure very close to the external hydrostatic pressure. The difference in gas partial pressure between the gaseous contents of the swimbladder and the blood and tissue fluids is large in fishes living at any considerable depth, for the hydrostatic pressure increases about 1 atm with each 10 m depth, while the partial pressures of gases in sea water and body fluids are relatively independent of depth and together give a pressure of only about 1 atm. The difference in partial pressure of oxygen alone across the wall of the swimbladder of a fish living at 3000 m depth is close to 300 atm.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1980

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References

Battino, R., Evans, F. D. & Danforth, W. F., 1968. The solubilities of seven gases in olive oil with reference to theories of transport through the cell membrane. Journal of the American Oil Chemists Society, 45, 830833.CrossRefGoogle ScholarPubMed
Biot, J. B., 1807. Sur la nature de l'air contenu dans la vessie natatoire des poissons. Mémoires physique Chimie Société d'Arcuiel, 1, 252281.Google Scholar
Bohr, C., 1893. The influence of vagus section on gas disengagement in the air-bladder of fishes. Journal of Physiology, 15, 494500.CrossRefGoogle Scholar
Brown, D. S. & Copeland, D. E., 1977. Overlapping platelets: a diffusion barrier in the teleost swimbladder. Science, New York, 197, 383384.CrossRefGoogle ScholarPubMed
Brown, D. S. & Copeland, D. E., 1978. Layered membranes: a diffusion barrier to gases in the teleostean swimbladder. Tissue and Cell, 10, 785796.CrossRefGoogle Scholar
Cohen, D. M., 1977. Swimming performance of the gadoid fish Antimora rostrata at 2400 meters. Deep-Sea Research, 24, 275277.CrossRefGoogle Scholar
Denton, E. J., Liddicoat, J. D. & Taylor, D. W., 1970. Impermeable ‘silvery’ layers in fish. Journal of Physiology, 207, 6465P.Google ScholarPubMed
Denton, E. J., Liddicoat, J. D. & Taylor, D. W., 1972. The permeability to gases of the swimbladder of the conger eel (Conger conger). Journal of the Marine Biological Association of the United Kingdom, 52, 727746.CrossRefGoogle Scholar
Finkelstein, A., 1976. Water and nonelectrolyte permeability of lipid bilayer membranes. Journal of General Physiology, 68, 127135.CrossRefGoogle ScholarPubMed
Finkelstein, A. & Cass, A., 1968. Permeability and electrical properties of thin lipid membranes. Journal of General Physiology, 52, 145172.CrossRefGoogle ScholarPubMed
Folch, J., Lees, M. & Sloane-Stanley, G. H., 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226, 497509.CrossRefGoogle ScholarPubMed
Haedrich, R. L., Rowe, G. T. & Polloni, P. T., 1975. Zonal and faunal composition of epibenthic populations on the continental slope south of New England. Journal of Marine Research, 33, 191212.Google Scholar
Haedrich, R. L., Rowe, G. T. & Polloni, P. T., 1979. The megabenthic fauna in the deep sea south of New Zngland, Marine Biology. (In the Press.)CrossRefGoogle Scholar
Iwamoto, T., 1975. The abyssal fish Antimora rostrata (Günther). Comparative Biochemistry and Physiology, 52B, 711.Google Scholar
Josephson, R. V., Holtz, R. B., Misock, J. P. & Phleger, C. F., 1975. Composition and partial protein characterization of swimbladder foam from deep-sea fish Coryphaenoides acrolepis and Antimora rostrata. Comparative Biochemistry and Physiology 52B, 9195.Google Scholar
Kuhn, H. J. & Marti, E., 1966. The active transport of oxygen and carbon dioxide into the swimbladder of fish. Journal of General Physiology, 49, 12091220.CrossRefGoogle ScholarPubMed
Kuhn, W., Ramel, A., Kuhn, H. J. & Marti, E., 1963. The filling mechanism of the swimbladder. Generation of high pressures through hairpin countercurrent multiplication. Experientia, 19, 497511.CrossRefGoogle ScholarPubMed
Kutchai, H. & Steen, J. B., 1971. The permeability of the swimbladder. Comparative Biochemistry and Physiology, 39A, 119123.CrossRefGoogle Scholar
Lapennas, G. N. & Schmidt-Nielsen, K., 1977. Swimbladder permeability to oxygen. Journal of Experimental Biology, 67, 175196.CrossRefGoogle Scholar
Marshall, N. B., 1960. Swimbladder structure of deep-sea fishes in relation to their systematics and biology. ‘Discovery’ Reports, 31, 1122.Google Scholar
Marshall, N. B., 1965. Systematic and biological studies of the Macrourid fishes (AnacanthiniTeleostii). Deep-Sea Research, 12, 299322.Google Scholar
Melchior, D. L. & Steim, J. M., 1976. Thermotropic transitions in biomembranes. Annual Review of Biophysics and Bioengineering, 5, 205238.CrossRefGoogle ScholarPubMed
Nielsen, J. G. & Munk, O., 1964. A hadal fish (Bassogigas profundissimus) with a functional swimbladder. Nature, London, 204, 594595.CrossRefGoogle Scholar
Norton, W. T. & Autilio, L. A., 1966. The lipid composition of purified bovine brain myelin. Journal of Neurochemistry, 13, 213222.CrossRefGoogle ScholarPubMed
Patton, S. & Thomas, A. J., 1971. Composition of lipid foams from swimbladders of two deep ocean fish species. Journal of Lipid Research, 12, 331335.CrossRefGoogle ScholarPubMed
Phleger, C. F., 1971. Pressure effects on cholesterol and lipid synthesis by the swimbladder of an abyssal Coryphaenoides species. American Zoologist, 11, 559570.CrossRefGoogle Scholar
Phleger, C. F., 1975. Lipid synthesis by Antimora rostrata, an abyssal codling from the Kona coast. Comparative Biochemistry and Physiology, 52B, 9799.Google Scholar
Phleger, C. F. & Benson, A. A., 1971. Cholesterol and hyperbaric oxygen in swimbladders of deep sea fishes. Nature, London, 230, 122.CrossRefGoogle ScholarPubMed
Phleger, C. F., Benson, A. A. & Yayanos, A. A., 1973. Pressure effect on squalene-2,3-oxide cyclization in fish. Comparative Biochemistry and Physiology, 45B, 241247.Google Scholar
Phleger, C. F. & Holtz, R. B., 1973. The membranous lining of the swimbladder in deep sea fishes. I. Morphology and chemical composition. Comparative Biochemistry and Physiology, 45B, 867873.Google Scholar
Polloni, P. T., Haedrich, R. L., Rowe, G. T. & Clifford, C. H., 1979. The size-depth relationship in deep-ocean animals Internationale Revue der gesamten Hydrobiologie, 64, 3745.CrossRefGoogle Scholar
Ross, L. G., 1976. The permeability to oxygen of the swimbladder of the mesopelagic fish Ceratoscopelus maderensis. Marine Biology, 37, 8387.CrossRefGoogle Scholar
Scholander, P. F., Van Dam, L., Claff, C. L. & Kanwisher, J. W., 1955. Microgasometric determination of dissolved oxygen and nitrogen. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 109, 328334.CrossRefGoogle Scholar
Searcy, R. L. & Berquist, L. M., 1960. A new color reaction for the quantitation of serum cholesterol. Clinica chimica acta, 5, 192199.CrossRefGoogle ScholarPubMed
Smith, K. L. & Hessler, R. R., 1974. Respiration of benthopelagic fishes: in-situ measurements at 1230 meters. Science, New York, 184, 7273.CrossRefGoogle ScholarPubMed
Szabo, G., Eisenman, G., Laprade, R., Ciani, S. M. & Krasne, S., 1973. Experimentally observed effects of carriers on the electrical properties of bilayer membranes. Equilibrium domain. In Membranes, vol. 2, Lipid Bilayers and Antibiotics (ed. Eisenman, G.), pp. 179328New York: Marcel Dekker Inc. [See especially pp. 265–269.].Google ScholarPubMed
Wilhelm, E. & Battino, R., 1973. Thermodynamic functions of the solubilities of gases in liquids at 25 °C. Chemical Reviews, 73, 19.CrossRefGoogle Scholar
Woodland, W. N. F., 1911. On the structure and function of the gas glands and retia mirabilia associated with the gas bladder of some teleostean fishes, with notes on the teleost pancreas. Proceedings of the Zoological Society of London, 1911, 183–248.CrossRefGoogle Scholar
Woodland, W. N. F., 19101913. Notes on the structure and mode of the ‘oval’ in the pollack (Gadus pollachius) and mullet (Mugil cheld). Journal of the Marine Biological Association of the United Kingdom, 9, 561565.CrossRefGoogle Scholar