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Tolerance and ultrastructural responses of branchial chloride cells to salinity changes in the euryhaline teleost Oreochromis mossambicus

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Abstract

The changes of intercellular organization and junctional structures in branchial chloride cells reflect respective functions in different salinities. Under TEM, leaky junctions and intercellular digitations occurred between branchial chloride cells of Oreochromis mossambicus Peters adapted to seawater, but not in those adapted to freshwater. The fish transferred directly to 30‰ S seawater from freshwater died within 6 h, and their chloride cells developed neither leaky junctions nor interdigitations. The fishes acclimated to 20‰ S seawater for 12 h did not develop the characteristics of seawater-adapted chloride cells and died after transfer to 30‰ S seawater. The fish acclimated to 20‰ S seawater for 24 h started to develop seawater-adapted chloride cells, and were able to survive when transferred to 30‰ S seawater. Thus, the development of leaky junctions and interdigitations in branchial chloride cells appears to correlate to seawater adaptation in O. mossambicus. These changes of seawater-adapted chloride cells seem to be associated with the increase of ion permeability in the gill of teleosts adapted to seawater rather than those adapted to freshwater.

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Literature cited

  • Assem, H. and W. Hanke: Volume regulation of muscle cells in the eurhyaline teleost, Tilapia mossambica. Comp. Biochem. Physiol. 64 A, 17–23 (1979)

    Google Scholar 

  • Claude, P.: Morphological factors influencing transepithelial permeability: a model for the resistance of the zonulae occludentes. J. Mem. Biol. 39, 219–232 (1978)

    Google Scholar 

  • Claude, P. and A. Goodenough: Fracture faces of zonulae occludentes from “tight” and “leaky” epithelia. J. Cell Biol. 58, 390–400 (1973)

    Google Scholar 

  • Doyle, W. L.: Cytological changes in chloride cells following altered ionic media. J. exp. Zool. 199, 427–434 (1977)

    Google Scholar 

  • Doyle, W. L. and F. H. Epstein: Effects of cortisol treatment and osmotic adaptation on the chloride cells in the eel Anguilla rostrata. Cytobiologie 6, 58–73 (1972)

    Google Scholar 

  • Duffey, M. E., B. Hainau, S. Ho and C. J. Bentzel: Regulation of epithelial tight junction permeability by cyclic AMP. Nature, Lond. 204, 451–453 (1981)

    Google Scholar 

  • Dunel, S. and P. Laurent: Ultrastructure of marine teleost gill epithelia: SEM and TEM study of the chloride cell apical membrane. J. Morphol. 165, 175–186 (1980)

    Google Scholar 

  • Epstein, F. H., A. I. Katz and G. E. Pickford: Sodium and potassium-activated adenosine triphosphatase of gills: role in adaptation of teleosts to seawater. Science, Wash. D.C. 156, 1245–1247 (1967)

    Google Scholar 

  • Epstein, F. H., J. Maetz and G. DeRenzis: Active transport of chloride by the teleost gill: inhibition by thocyanate. Am. J. Physiol. 224, 1295–1299 (1973)

    Google Scholar 

  • Epstein, F. H., P. Silva and G. Kormanik: Role of Na-K-ATPase in chloride cell function. Am. J. Physiol. 238, R246–250 (1980)

    Google Scholar 

  • Ernst, S. A., W. C. Dodson and K. J. Karnaky: Structural diversity of occluding junctions in the low-resistance chloride-secreting opercular epithelium of seawater-adapted killifish (Fundulus heteroclitus). J. Cell Biol. 87, 488–497 (1980)

    Google Scholar 

  • Evans, D. H.: Fish. In: Comparative physiology of osmoregulation in animals. Vol. 1., pp 305–390. Ed. by G. M. O. Maloiy. London: Academic Press 1979

    Google Scholar 

  • Foskett, J. K., C. D. Logsdon, T. Turner, T. E. Machen and H. A. Bern: Differentiation of the chloride extrusion mechanism during seawater adaptation of a teleost fish, the cichlid Sarotherodon mossambicus. J. exp. Biol. 93, 209–224 (1981)

    Google Scholar 

  • Foskett, J. K. and C. Scheffey: The chloride cells: definitive identification as the salt-secretory cell in teleosts. Science, Wash. D.C. 215, 164–166 (1982)

    Google Scholar 

  • Fromter, E. and J. Diamond: Route of passive ion permeation in epithelia. Nature, Lond. 235, 9–13 (1972)

    Google Scholar 

  • Girard, J. P. and P. Payan: Ion exchanges through respiratory and chloride cells in freshwater- and seawater-adapted teleosteans. Am. J. Physiol. 238, R260–268 (1980)

    Google Scholar 

  • Hegab, A. and W. Hanke: Electrolyte changes, cell volume regulation and hormonal influences during acclimation of rainbow trout (Salmo gairdnerii) to salt water. Comp. Biochem. Physiol. 83 A, 47–52 (1986)

    Google Scholar 

  • Hootman, S. R. and C. W. Philpott: Rapid isolation of chloride cells from pinfish gill. Anat. Rec. 190, 687–720 (1978)

    Google Scholar 

  • Hootman, S. R. and C. W. Philpott: Ultracytochemical localization of Na+, K+-activated ATPase in chloride cells from gills of a euryhaline teleost. Anat. Rec. 193, 99–130 (1979)

    Google Scholar 

  • Hootman, S. R. and C. W. Philpott: Accessory cells in teleost branchial epithelium. Am. J. Physiol. 238, R199–206 (1980)

    Google Scholar 

  • Hossler, F. E.: Gill arch of the mullet, Mugil cephalus III. Rate of response to salinity change. Am. J. Physiol. 238, R160–164 (1980)

    Google Scholar 

  • Hossler, F. E., G. Musil, K. J. Karnaky and F. H. Epstein: Surface ultrastructure of gill arch of the killifish, Fundulus heteroclitus, from seawater and freshwater, with special reference to morphology of apical crypts of chloride cells. J. Morphol. 185, 377–386 (1985)

    Google Scholar 

  • Hwang, P. P. and R. Hirano: Effects of environmental salinity on intercellular organization and junctional structure of chloride cells in early stages of teleost development. J. exp. Zool. 236, 115–126 (1985)

    Google Scholar 

  • Iwata, M., T. Hirano and S. Hasegawa: Behavior and sodium regulation of chum salmon fry during transition into seawater. Aquaculture 28, 133–142 (1982)

    Google Scholar 

  • Kachar, B. and P. P. da Silva: Rapid massive assembly of tight junction strands. Science, Wash. D.C. 213, 541–544 (1981)

    Google Scholar 

  • Karnaky, K. J.: Ion-secreting epithelia: chloride cells in the head region of Fundulus heteroclitus. Am. J. Physiol. 238, R185–198 (1980)

    Google Scholar 

  • Karnaky, K. J., S. A. Ernst and C. W. Philpott: Teleost chloride cell. I. Response of pupfish Cyprinodon variegatus gill Na,K-ATPase and chloride cell fine structure to various high salinity environments. J. Cell Biol. 70, 144–156 (1976)

    Google Scholar 

  • Karnovsky, M. S.: A formaldehyde-glutaldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27, 137 A (1965)

    Google Scholar 

  • Keys, A. B. and E. N. Willmer: “Chloride secreting cells” in the gills of fishes, with special reference to the common eel. J. Physiol. Lond. 76, 368–378 (1932)

    Google Scholar 

  • Kottra, G. and E. Fromter: Functional properties of the paracellular pathway in some leaky epithelia. J. exp. Biol. 106, 217–229 (1983)

    Google Scholar 

  • Laurent, P. and S. Dunel: Morphology of gill epithelia in fish. Am. J. Physiol. 238, R147–159 (1980)

    Google Scholar 

  • Madara, J.: Increase in guinea pig small intestinal transepithelial resistance induced by osmotic loads are accompanied by rapid alterations in absorptive-cell tight-junction structure. J. Cell Biol. 97, 125–136 (1983)

    Google Scholar 

  • Maetz, J.: Fish gills: mechanisms of salt transfer in freshwater and seawater. Phil. Trans. R. Soc. Lond. B 262, 209–249 (1971)

    Google Scholar 

  • Moreno, J. H.: Blockage of cation permeability across the tight junctions of gallbladder and other leaky epithelia. Nature, Lond. 251, 150–151 (1974)

    Google Scholar 

  • Payan, P., J. P. Girard and N. Mayer-Gostan: Branchial ion movements in teleosts: the roles of respiratory and chloride cells. In: Fish physiology, Vol. X, B., pp 39–63. Ed. by W. S. Hoar and D. J. Randall. Orlando: Academic Press 1984

    Google Scholar 

  • Philpott, C. W.: Tubular system membranes of teleost chloride cells: osmotic response and transport sites. Am. J. Physiol. 238, R171–184 (1980)

    Google Scholar 

  • Philpott, C. W. and D. E. Copeland: Fine structure of chloride cells from three species of Fundulus. J. Cell Biol. 18, 389–404 (1963)

    Google Scholar 

  • Pisam, M.: Membraneous systems in the “chloride cell” of teleostean fish gill; their modifications in response to salinity of environment. Anat. Rec. 200, 401–414 (1981)

    Google Scholar 

  • Potts, W. T. W., M. A. Foster, P. P. Rudy and H. G. Parry: Sodium and water balance in the cichlid teleost Tilapia mossambica. J. exp. Biol. 47, 461–470 (1967)

    Google Scholar 

  • Reynolds, E. S.: The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J. Cell. Biol. 17, 208–211 (1963)

    Google Scholar 

  • Riddle, C. V. and S. A. Ernst: Structural simplicity of the Zonula occludens in the electrolyte secreting epithelium of the avian salt gland. J. Membr. Biol. 45, 21–35 (1979)

    Google Scholar 

  • Sardet, C., M. Pisam and J. Maetz: The surface epithelium of teleostean fish gills. J. Cell Biol. 80, 96–117 (1979)

    Google Scholar 

  • Sargent, J. R., A. J. Thomson and M. Bonancin: Activities and localization of succinic dehydrogenase and Na+/K+-activated adenosine triphosphatase in the gills of fresh water and sea water eels (Anguilla anguila). Comp. Biochem. Physiol. 51B, 75–79 (1975)

    Google Scholar 

  • Shirai, N. and S. Utida: Development and degeneration of the chloride cell during seawater and freshwater adaptation of the Japanese eel, Anguilla japonica. Z. Zellforsch. mikrosk. Anat. 103, 247–264 (1970)

    Google Scholar 

  • Silva, P., R. Solomon, K. Spokes and F. H. Epstein: Ouabain inhibition of gill Na-K-AtPase: relationship to active chloride transport. J. exp. Zool. 199, 419–426 (1977)

    Google Scholar 

  • Thomson, A. J. and J. R. Sargent: Changes in the levels of chloride cells and (Na++K+-dependent ATPase in the gills of yellow and silver eels adapting to seawater. J. exp. Zool. 200, 33–40 (1977)

    Google Scholar 

  • Utida, S., M. Kamiya and N. Shirai: Relationship between the activity of Na-K-activated adensionetriphosphatase and the number of chloride cells in eel gills with special reference to seawater adaptation. Comp. Biochem. Physiol. 38A, 443–448 (1971)

    Google Scholar 

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  1. Institute of Zoology, Academia Sinica, Nankang, 11529, Taipei, Taiwan Republic of China

    P. P. Hwang

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Communicated by M. Anraku, Tokyo

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Hwang, P.P. Tolerance and ultrastructural responses of branchial chloride cells to salinity changes in the euryhaline teleost Oreochromis mossambicus . Mar. Biol. 94, 643–649 (1987). https://doi.org/10.1007/BF00431411

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  • DOI: https://doi.org/10.1007/BF00431411

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