Abstract
The surface morphology of the gill epithelium of the dogfish Scyliorhinus canicula L. (collected near Barcelona, Spain, in February–March, 1981) was studied by scanning electron microscopy. Pavement cells exhibited either surface microvilli or microridges, which were randomly distributed on both the primary (afferent and efferent sides and interlamellar spaces) and secondary epithelium. Chloride cell apical regions on the afferent side displayed characteristics closer to freshwater than to marine teleosts: no apical pits were detected; chloride cells displayed longer microvilli than those of adjacent cells. Two morphologically different cell types were identified: a large chloride cell and a smaller cell (probably a chloride cell too), measuring 4 to 7 μm and 1 μm, respectively, the latter being dominant in the interlamellar spaces. Apart from pavement cells, the mucous cell was the prevalent cell type on the efferent region. The respiratory epithelium consisted of a mozaic of typical epithelial cells; some chloride and mucous cells were present, mainly located at the base of the secondary lamellae. Surface morphological changes were monitored after exposing the dogfish to subacute zinc treatment: 10 ppm Zn (ZnSO4) for 3 wk. The chloride cell was the only cell type that underwent any modifications: microvilli became longer and tips were swollen following Zn treatment. The results are discussed in relation to a previous study on the effects of zinc sulphate on chloride cell response and heavy metal distribution in excretory organs of the dogfish.
Similar content being viewed by others
Literature Cited
Ahuja, S. K.: Chloride-cell and mucous cell response to chloride and sulphate-enriched media in the gills of Gambusia affinis affinis (Baird and Girard) and Catla catla (Hamilton). J. exp. Zool. 173, 231–250 (1970)
Burger, J. W. and W. N. Hess: Function of the rectal gland in the spiny dogfish, Squalus acanthias. Comp. Biochem. Physiol 19, 649–653 (1960)
Conte, F. P. and D. H. Lin: Kinetics of cellular morphogenesis in gill epithelium during seawater adaptation of Oncorhyncus (Walbaum). Comp. Biochem. Physiol. 23, 945–957 (1967)
Crespo, S. and J. Balasch: Mortality, accumulation and distribution of zinc in the gill system of the dogfish following zinc treatment. Bull. envir. Contam. Toxicol. 24, 940–944 (1980)
Crespo, S., R. Flos, J. Balasch and G. Alonso: Zinc in the gills of the dogfish (Scyliorhinus canicula L.) related to experimental aquatic zinc pollution. Comp. Biochem. Physiol. 63C, 261–266 (1979)
Crespo, S., E. Soriano, C. Sampera and J. Balasch: Zinc and copper distribution in excretory organs of the dogfish Scyliorhinus canicula and chloride cell response following treatment with zinc sulphate. Mar. Biol. 65, 117–123 (1981)
Doyle, W. L. and D. Gorecki: The so-called chloride cell of the fish gill. Physiol. Zoöl. 34, 81–85 (1961)
Dunel, S. and P. Laurent: Ultrastructure of marine teleost gill epithelia: SEM and TEM study of the chloride cell apical membrane. J. Morph. 165, 175–186 (1980a)
Dunel, S. and P. Laurent: Functional organisation of the gill vasculature in different classes of fish. In: Epithelial transport in the lower vertebrates, pp 37–58. Ed. by B. Lahlou, Malta: C.U.P. 1980b
Ehlers, U. and B. Ehlers: Paddle cilia and discocilia — genuine structures? Observations on cilia of sensory cells in marine Turbellaria. Cell Tissue Res 192, 489–501 (1978)
Evans, D. H.: Salt transport mechanisms in branchial epithelia. In: Animals and environmental fitness, pp 61–78. Ed. by R. Gilles. Oxford and New York: Pergamon Press 1980a
Evans, D. H.: Kinetic study of ion transport by fish gill epithelium. Am. J. Physiol. 238, 224–330 (1980b)
Hickman, C. P. and B. F. Trump: The kidney. In: Fish physiology, pp 91–239. Ed. by W. S. Hoar and D. J. Randall: New York: Academic Press 1969
Hootman, S. R. and C. W. Philpott: Accessory cells in teleost branchial epithelium. Am. J. Physiol. 238, 199–206 (1980)
Hossler, F. E.: The gill arch of the mullet Mugil cephalus. III. Rate of response to salinity changes. Am. J. Physiol. 238, 160–165 (1980)
Hossler, F. E., J. R. Ruby and T. D. McIlwain: The gill arch of the mullet Mugil cephalus. I. Surface ultrastructure. J. exp. Zool. 208, 379–398 (1979a)
Hossler, F. E., J. R. Ruby and T. D. McIlwain: The gill arch of the mullet Mugil cephalus. II. Modification in surface ultrastructure and Na, K-ATPase content during adaptation to various salinities. J. exp. Zool 208, 399–405 (1979b)
Hughes, G. M.: Scanning electron microscopy of the respiratory surfaces of the trout gills. J. Zool., Lond. 187, 443–453 (1979)
Hughes G. M. and D. E. Wright: A comparative study of the ultrastructure of the water-blood pathway in the secondary lamellae of teleost and elasmobranch fishes-benthic forms. Z. Zellforsch. 104, 478–493 (1970)
Karnaky, K. J., Jr.: Ion-secreting epithelia: chloride cells in the head-region of Fundulus heteroclitus. Am. J. Physiol. 238, 185–198 (1980)
Karnaky, K. J., Jr., K. J. Degnan and J. A. Zadunaisky: Chloride transport across isolated opercular epithelium of killifish: a membrane rich in chloride cells. Science, N.Y. 195, 203–205 (1977)
Karnaky, J. K., Jr., S. A. Ernst and C. W. Philpott: Teleost chloride cell. I. Response of pupfish Cyprinidon variegatus gill Na, K-ATPase and chloride cell fine structure to various high salinity environments. J. Cell Biol. 70, 144–156 (1976)
Katz, B.: Relationship of the physiology of aquatic organisms to the lethality of toxicants: a broad overview with emphasis on membrane permeability. Aquat. Toxicol. (A.S.T.M.) Ref. STP 667, 62–79 (1979)
Kendall, M. W. and J. E. Dale: Scanning and transmission electron microscopic observations of rainbow trout (Salmo gairdneri) gill. J. Fish. Res. Bd Can. 36, 1072–1079 (1979)
Kikuchi, S.: Mitochondria-rich (chloride) cells in the gill epithelia from four species of stenohaline fresh water teleosts. Cell Tissue Res. 180, 87–98 (1977)
Kirsch, R., R. Meens et M. F. Meister: Osmorégulation chez les téléostéens marins: role des branchies et du tube digestif. Bull. Soc. zool. Fr. 106, 31–37 (1981)
Laurent, P. and S. Dunel: Morphology of gill epithelia in fish. Am. J. Physiol. 238, 147–159 (1980)
Lewis, S. V. and I. C. Potter: A scanning electron study microscope of the gills of the lamprey Lampetra fluviatilis (L.). Micron 7, 205–211 (1976)
Lock, R. A. C., P. M. J. M. Cruijsen and A. P. Overbeeke: Effects of mercuric chloride and methylmercuric chloride on the osmoregulatory function of the gills in rainbow trout, Salmo gairdneri Richardson. Comp. Biochem. Physiol. 68 C, 151–159 (1981)
Lock, R. A. C. and A. P. Van Overbeeke: Effects of mercuric chloride and methylmercuric chloride on mucus secretion in rainbow trout, Salmo gairdneri Richardson. Comp. Biochem. Physiol. 69 C, 67–73 (1981)
Maetz, J.: Fish gills: mechanisms of salt transfer in freshwater and seawater. Phil. Trans. R. Soc. (Ser. B) 262, 209–249 (1971)
Marshall, W. S. and R. S. Nishioka: Relation of mitochondriarich chloride cells to active chloride transport in the skin of a marine teleost. J. exp. Zool. 214, 147–156 (1980)
McLeod, M. G.: Effects of salinity and starvation on the alimentary canal anatomy of the rainbow trout, Salmo gairdneri Richardson. J. Fish Biol. 12, 71–79 (1978)
Olson, K. R. and P. O. Fromm: A scanning electron microscopic study of secondary lamellae and chloride cells of rainbow trout (Salmo gairdneri). Z. Zellforsch. mikrosk. Anat. 143, 439–449 (1973)
Olson, K. R. and B. Kent: The microvasculature of the elasmobranch gill. Cell Tissue Res. 209, 49–65 (1980)
Patrick, J., J. Michael, M. N. Golden, B. E. Golden and P. J. Hilton: Effect of zinc on leucocyte sodium transport in vitro. Clin. Sci. molec. Med. 54, 585–587 (1978)
Payan, P. and J. Maetz: Branchial sodium transport mechanisms in Scyliorhinus canicula: evidence for Na+/NH4 and Na+ H+ exchanges and for a role of carbonic anhydrase. J. exp. Biol. 58, 487–502 (1973)
Peek, W. D. and J. H. Youson: Ultrastructure of chloride cell in young adults of the anadromous sea lamprey, Petromyzon marinus L. in fresh water and during adaptation to seawater. J. Morph. 160, 143–164 (1979)
Philpott, C. W.: Tubular system membranes of teleost chloride cells: osmotic response and transport sites. Am. J. Physiol. 238, 171–184 (1980)
Rajbanshi, V.: The architecture of the gill surface of the catfish Heteropneutes fossilis (Bloch): SEM study. J. Fish Biol. 10, 325–329 (1977)
Rothstein, A.: Cell membrane as site of action of heavy metals. Fedn Proc. Fedn Am. Socs exp. Biol. 18, 1026–1038 (1959)
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. 103, 247–264 (1970)
Skidmore, J. F.: Respiration and osmoregulation in rainbow trout with gills damaged by Zn sulphate. J. exp. Biol. 52, 481–494 (1970)
Sperry, D. G. and R. J. Wasserug: A proposed function for microridges on epithelial cells. Anat. Rec. 185, 253–258 (1976)
Sutherland, J. and C. W. Majors: Internal heavy metal changes as a consequence of exposure of Mytilus edulis, the blue mussel, to elevated external cooper levels. Comp. Biochem. Physiol. 68 C, 63–67 (1981)
Varanasi, V., P. A. Robish and D. C. Malins: Structural alterations in fish epidermal mucus produced by water-borne lead and mercury. Nature, Lond. 258, p. 431 (1975)
Western, J. R. H.: Feeding and digestion in two cottid fishes, the freshwater Cottus gobio L. and the marine Enophrys bubalis (Euphrasen). J. Fish Biol. 3, 225–246 (1971)
Wright, D. F.: The structure of the gills of the elasmobranch S. canicula L. Z. Zellforsch. 144, 489–509 (1973)
Author information
Authors and Affiliations
Additional information
Communicated by J. M. Pérès, Marseille
Rights and permissions
About this article
Cite this article
Crespo, S. Surface morphology of dogfish (Scyliorhinus canicula) gill epithelium, and surface morphological changes following treatment with zinc sulphate: A scanning electron microscope study. Marine Biology 67, 159–166 (1982). https://doi.org/10.1007/BF00401281
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00401281