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Changes in osmotic water permeability of the eel gills during seawater and freshwater adaptation

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Summary

Changes in osmotic water permeability of the isolated gills of the Japanese eel,Anguilla japonica were studied during transfer to seawater or to fresh water. The water permeability increased gradually during the course of seawater transfer and attained a maximal level after 2 weeks. The water permeability of the freshwater eel gills was reduced when calcium ions were added to the incubation medium at a concentration of 1 mM, where-as no effect of the ion was observed on the gills of the seawater-adapted eel even at a higher concentration (10 mM). In contrast to seawater transfer, the water permeability decreased to a low level almost immediately (3 h) after transfer from seawater to fresh water. The acute reduction of the water permeability was also seen in the gills of the hypophysectomized eel after transfer to fresh water.

The gradual increase in the gill water permeability during seawater transfer is correlated with an increase in the number of chloride cells. In scanning electron microscopy, chloride cells of seawater-adapted eel gills exhibit a pit-like structure, which was larger than in the freshwater eel. On transfer from seawater to fresh water, the pit diameter became smaller within 6 h. Hypophysectomy did not affect the change in gill surface structures during transfer to fresh water. The junctions between the chloride cells of seawater eel gills are reported to be of the leaky type. The parallel change in osmotic water permeability and in pit size of the chloride cells during seawater or freshwater transfer or after hypophysectomy suggests that these cells could provide a major route of water as well as ion movement.

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References

  • Bentley PJ (1971) Endocrines and osmoregulation. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Bern HA, Bisbee CA, Collie NL, Foskett JK, Hughes B, Loretz CA, Marshall WS (1981) Failure of ovine prolactin to elicit rapid responses by osmoregulatory surfaces. Gen Comp Endocrinol 44:128–130

    Google Scholar 

  • Clarke WC, Bern HA (1980) Comparative endocrinology of prolactin. In: Li CH (ed) Hormonal proteins and peptides, vol VIII. Academic Press, New York, pp 106–143

    Google Scholar 

  • Diamond, JM (1974) Tight and leaky junctions of epithelia: a perspective on kisses in the dark. Fed Proc 33:2220–2224

    Google Scholar 

  • Ernst SA, Dodson WB, Karnaky KJ Jr (1978) Structural diversity of zonulae occludentes in seawater-adapted killifish opercular epithelium. J Cell Biol 79:242

    Google Scholar 

  • Evans DH (1979) Fish. In: Maloiy GMD (ed) Comparative physiology of osmoregulation in animals, vol 1. Academic Press, New York, pp 305–390

    Google Scholar 

  • Foskett JK, Scheffey C (1982) The chloride cell: definitive identification as the salt-secretory cell in teleosts. Science 215:164–166

    Google Scholar 

  • Foskett JK, Logsdon CD, Turner T, Machen TE, Bern HA (1981) Differentiation of the chloride extrusion mechanism during seawater adaptation of a teleost fish, the cichlidSarotherodon mossambicus. J Exp Biol 93:209–224

    Google Scholar 

  • Foskett JK, Machen TE, Bern HA (1982a) Chloride secretion and conductance of teleost opercular membrane: effects of prolactin. Am J Physiol 242:R380-R389

    Google Scholar 

  • Foskett JK, Hubbard GM, Machen TE, Bern HA (1982b) Effects of epinephrine, glucagon and vasoactive intestinal polypeptide on chloride secretion by teleost opercular membrane. J Comp Physiol 146:27–34

    Google Scholar 

  • Fromter E, Diamond JM (1972) Route of passive ion permeation in epithelia. Nature 8:259–301

    Google Scholar 

  • Gallis JL, Belloc F, Lasserre P, Boisseau J (1979) Freshwater adaptation in the euryhaline teleost,Chelon labrosus. II. Effects of continuance of adaptation, cortisol treatment, and environmental calcium on water influx in isolated gill. Gen Comp Endocrinol 38:11–20

    Google Scholar 

  • Hirano T (1977) Prolactin and hydromineral metabolism in vertebrates. Gunma Symp Endocrinol 14:45–59

    Google Scholar 

  • Hirano T, Mayer-Gostan N (1978) Endocrine control of osmoregulation in fish. In: Gaillard PJ, Boer HH (eds) Comparative endocrinology. Elsevier/North-Holland Biomedical Press, Amsterdam, pp 209–212

    Google Scholar 

  • Hirano T, Kamiya M, Saishu S, Utida S (1967) Effects of hypophysectomy and urophysectomy on water and sodium transport in isolated intestine and gills of Japanese eel (Anguilla japonica). Endocrinol Jpn 14:182–186

    Google Scholar 

  • Hossler FE, Ruddy JR, McIlwain TD (1979) The gill arch of the mullet,Mugil cephalus. I. Surface ultrastructure. II. Modification in surface ultrastructure and Na, K-ATPase content during adaptation to various salinities. J Exp Zool 208:379–406

    Google Scholar 

  • Isaia J, Hirano T (1975) Effects of environmental salinity changes on osmotic permeability of the isolated gill of the eel,Anguilla anguilla L. J Physiol (Paris) 70:737–747

    Google Scholar 

  • Isaia J, Masoni A (1976) The effects of calcium and magnesium on water and ionic permeabilities in the seawater adapted eel,Anguilla anguilla L. J Comp Physiol 109:221–233

    Google Scholar 

  • Kamiya M (1967) Changes in ion and water transport in isolated gills of the cultured eel during the course of salt adaptation. Annot Zool Jpn 40:123–129

    Google Scholar 

  • Karnaky KJ Jr (1980) Ion-secreting epithelia: chloride cells in the head region ofFundulus heteroclitus. Am J Physiol 238:R185-R198

    Google Scholar 

  • Karnaky KJ Jr, Degan KJ, Zadunaisky JA (1977) Chloride transport across isolated opercular epithelium of killifish: a membrane rich in chloride cells. Science 195:203–205

    Google Scholar 

  • Lam T (1969) The effect of prolactin on osmotic influx of water in isolated gills of the marine threespine sticklebackGasterosteus aculeatus L. formtrachurus. Comp Biochem Physiol 31:909–913

    Google Scholar 

  • Loretz CA, Bern HA (1982) Prolactin and osmoregulation in vertebrates. Neuroendocrinology 35:292–304

    Google Scholar 

  • Maetz J (1971) Fish gills: Mechanisms of salt transfer in fresh water and seawater. Philos Trans R Soc Lond [Biol] 262:209–249

    Google Scholar 

  • Maetz J, Bornancin M (1975) Biochemical and biophysical aspects of salt excretion by chloride cells in teleosts. Fortschr Zool 23:322–362

    Google Scholar 

  • Motais R, Isaia J, Rankin JC, Maetz J (1969) Adaptive changes of the water permeability of the teleostean gill epithelium in relation to external salinity. J Exp Biol 51:529–546

    Google Scholar 

  • Ogawa M (1973) The effect of bovine prolactin, seawater and environmental calcium on water influx in isolated gills of the euryhaline teleosts,Anguilla japonica andSalmo gairdneri. Comp Biochem Physiol [A] 49:545–555

    Google Scholar 

  • Ogawa M (1974) The effects of prolactin, cortisol and calciumfree environment on water influx in isolated gills of Japanese eel,Anguilla japonica. Comp Biochem Physiol [A] 52:539–543

    Google Scholar 

  • Ogawa M, Yagasaki M, Yamazaki F (1973) The effect of prolactin on water influx in isolated gills of the goldfish,Carassius auratus L. Comp Biochem Physiol [A] 44:1177–1183

    Google Scholar 

  • Ogasawara T, Hirano T (1983) Effects of prolactin and environmental calcium on osmotic water permeability of the gills in the eel,Anguilla japonica. Gen Comp Endocrinol

  • Oide M, Utida S (1967) Changes in water and ion transport in isolated intestine of the eel during salt adaptation and migration. Mar Biol 1:102–106

    Google Scholar 

  • Sardet C, Pisam M, Maetz J (1979) The surface epithelium of teleostean fish gills: Cellular and junctional adaptation of the chloride cell in relation to salt adaptation. J Cell Biol 80:96–117

    Google Scholar 

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

    Google Scholar 

  • Shuttleworth TJ, Freeman FH (1974) Net fluxes of water in the isolated gills ofAnguilla dieffenbachii. J. Exp Biol 60:769–781

    Google Scholar 

  • Wendelaar Bonga SE, Meij JCA Van der (1981) Effect of ambient osmolarity and calcium on prolactin cell activity and osmotic water permeability of the gills in the teleostSarotherodon mossambicus. Gen Comp Endocrinol 43:432–442

    Google Scholar 

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Authors and Affiliations

  1. Ocean Research Institute, University of Tokyo, 164, Nakano, Tokyo, Japan

    Tsuyoshi Ogasawara & Tetsuya Hirano

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  1. Tsuyoshi Ogasawara
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  2. Tetsuya Hirano
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This paper is a portion of a thesis presented to Hokkaido University by t. Ogasawara in partial fulfilment of the requirements for Doctor of Fisheries

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Ogasawara, T., Hirano, T. Changes in osmotic water permeability of the eel gills during seawater and freshwater adaptation. J Comp Physiol B 154, 3–11 (1984). https://doi.org/10.1007/BF00683210

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