Summary
The effects of different salinities and concentrations of copper, mercury and cadmium ions on the gills of Jaera nordmanni are investigated by means of light and electron microscopy. After exposure to 10% and 50% sea water the gill epithelium cells show a marked uniformity in appearance, possessing characteristically large, sub-cuticular spaces which are prominent between microvilli. With exposure to the heavy metal ions a similar sequence of histological and ultrastructural changes occur in all the gill epithelial cells, culminating in cell breakdown. The ultrastructural changes include distended microvilli, dilated endoplasmic reticulum, dissociated ribosomes, diffuse (swollen) cytoplasm, swollen mitochondria and a basal membrane withdrawn from the basal lamina. An increase in the number of haemocytes is also commonly observed in the haemolymph spaces during heavy metal ion exposure. The significance of the morphological changes undergone by the gill epithelial cells after exposure to different salinities and heavy metal ion concentration, are discussed in relation to the physiological functioning of the gill.
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Baker, J.T.P.: Histological and electron microscopical observations on copper poisoning in the winter flounder Pseudopleuronectes americanus. J. Fish. Res. Bd. Canada 26, 2785–2793 (1969)
Bauchau, A.G., De Browner, M.: Ultrastructure des hemocytes d'Eriocheir sinensis, Crustacé Décapode Brachyoure. J. Microscopie 15, 171–180 (1972)
Berridge, M.J., Gupta, B.L.: Fine-structural changes in relation to ion and water transport in rectal papillae of the blowfly, Calliphora. J. Cell Sci. 2, 89–112 (1967)
Bielawski, J.: Chloride transport and water intake into isolated gills of crayfish. Comp. Biochem. Physiol. 13, 423–432 (1964)
Bielawski, J.: Energetics of ion transport in the gills of the crayfish Astacus leptodactylus Esch. Comp. Biochem. Physiol. 39B, 649–657 (1971)
Bielawski, J., Kwinto, B.: Swelling of mitochondria in crayfish gills. Protoplasma 76, 161–166 (1973)
Brown, B., Ashanullah, M.: Effect of heavy metals on mortality and growth. Mar. Poll. Bull. 2, 182–188 (1971)
Bryan, G.W.: The effects of heavy metals (other than mercury) on marine and estuarine organisms. Proc. roy. Soc. B 177, 389–410 (1971)
Bubel, A., Jones, M.B.: Fine structure of the gills of Jaera nordmanni (Rathke) (Crustacea, Isopoda). J. mar. biol. Ass. U.K. 54, 737–743 (1974)
Chinnayya, B.: Effect of heavy metals on the oxygen consumption by the shrimp, Caridina rajadhari. Bouvier Indian J. exp. Biol. 9, 277–278 (1971)
Corner, E.D.S., Sparrow, B.W.: The modes of action of toxic agents. I. Observations on the poisoning of certain crustaceans by copper and mercury. J. mar. biol. Ass. U.K. 35, 531–548 (1956)
Ernster, L., Siekevitz, P., Palade, G.E.: Enzyme-structure relationships in the endoplasmic reticulum of rat liver. J. Cell Biol. 15, 541–562 (1962)
Evans, P.D.: The free amino acid pool of haemocytes of Carcinus maenas (L.). J. exp. Biol. 56, 501–507 (1972)
Fairbanks, V.F.: Copper sulfate-induced haemolytic anemia. Arch. intern. Med. 120, 428–432 (1967)
Fisher, J.M.: Fine-structural observations of the gill filaments of the fresh-water crayfish. Astacus pallipes lereboullet. Tiss. Cell 4, 287–299 (1972)
Forbes, A.T.: Osmotic and sodium regulation in Jaera albifrons Leach (Crustacea: Isopoda). Comp. Biochem. Physiol. 47A, 109–116 (1974)
Fromter, E.: The route of passive ion movement through the epithelium of Necturus gall bladder. J. Membrane Biol. 8, 259–301 (1972)
Gardner, G.R., Yevich, P.P.: Histological and hematological responses of an estuarine-teleost to cadmium. J. Fish. Res. Bd. Canada 27, 2185–2196 (1970)
Green, D.E., Asai, J., Harris, R.A., Penniston, J.T.: Conformational basis of energy transformations in membrane systems. III. Configurational changes in the mitochondrial inner membrane induced by changes in functional states. Arch. Biochem. Biophys. 125, 684–705 (1968)
Green, J.: The biology of estuarine animals. 401 pp. London: Sidgwick and Jackson 1968
Harris, R.R.: Aspects of sodium regulation in a brackish-water and a marine species of the isopod genus Sphaeroma. Mar. Biol. 12, 18–27 (1972)
Hearing, V., Vernick, S.H.: Fine structure of the blood cells of the lobster, Homarus americanus. Chesapeake Sciences 8, 170–186 (1967)
Hochachka, P.W., Somero, G.N., Schneider, D.E., Freed, J.M.: The organization and control of metabolism in the crustacean gill. Comp. Biochem. Physiol. 33, 529–548 (1970).
Hubschman, J.H.: Effects of copper on the crayfish Orconectes rusticus (Girard) II. Mode of toxic action. Crustaceana 12, 141–150 (1967)
Johnston, M.A., Elder, H.Y., Davies, P.S.: Cytology of Carcinus haemocytes and their function in carbohydrate metabolism. Comp. Biochem. Physiol. 46A, 569–581 (1973)
Jones, J.R.E.: The effect of ionic copper on the oxygen consumption of Gammarus pulex and Polycelis nigra. J. exp. Biol. 18, 153–161 (1942)
Jones, M.B.: Osmoregulation in the Jaera albifrons group of species (Isopoda, Asellota). J. mar. Biol. Ass. U.K. 52, 419–427 (1972a)
Jones, M.B.: Effects of salinity on the survival of the Jaera albifrons leach group of species (Crustacea: Isopoda). J. exp. mar. Biol. Ecol. 9, 231–237 (1972b)
Jones, M.B.: Influence of salinity and temperature on the toxicity of mercury to marine and brackish-water isopods (Crustacea). Estuar. coast. mar. Sci. 7, 425–431 (1973)
Jones, M.B.: Effects of copper on survival and osmoregulation in marine and brackish-water isopods (Crustacea). Proc. 9th Europ. mar. biol. Symp., p. 419–431 (H. Barmes ed.). The Aberdeen University Press 1975
Kaye, G.I., Wheeler, H.O., Whitlock, R.T., Lane, N.: Fluid transport in rabbit gall bladder. A combined physiological and electron microscopic study. J. Cell Biol. 30, 237–268 (1966)
Kerkut, G.A., Munday, K.A.: The effect of copper on the tissue respiration of the crab, Carcinus maenas. Cah. Biol. mar. 3, 27–35 (1962)
Keyhani, E.: Morphological changes in yeast cell mitochondria grown at various copper concentrations. Exp. Cell Res. 81, 73–78 (1973)
Leaf, A.: Regulation of intracellular fluid volume and disease. Amer. J. Med. 49, 291–295 (1970)
Lewis, S.D., Lewis, L.M.: The effect of zinc and copper on the osmolality of blood serum of the channel catfish, Ictalurus punctatus Rafinesque, and golden shiner, Notemigonous crysoleucas Mitchill. Trans. Amer. Fish. Soc. 100, 639–643 (1971)
Lockwood, A.P.M., Inman, C.B.E., Courtenay, T.H.: The influence of environmental salinity on the water fluxes of the amphipod crustacean Gammarus duebeni. J. exp. Biol. 58, 137–148 (1973)
Mount, D.I., Stephan, C.E.: A method for detecting cadmium poisoning in fish. J. Wildlife Manage. 31, 168–172 (1967)
Naylor, E.: British Marine Isopods, Synopses of British Fauna (New Series). London and New York: Academic Press, The Linnean Society 3, 1–86 (1972)
O'Hara, J.: Cadmium uptake by fiddler crabs exposed to temperature and salinity stress. J. Fish. Res. Bd. Canada 30, 846–848 (1973a)
O'Hara, J.: The influence of temperature and salinity on the toxicity of cadmium to the fiddler crab, Uca pugilator. Fish. Bull 71, 149–153 (1973b)
Oschman, J.L., Wall, B.J., Gupta, B.L.: Cellular basis of water transport. Symp. Soc. exp. Biol. 28, 305–350 (1974)
Peters, R.A.: A study of the toxic action of copper. In: The biochemistry of copper. Proceeding of the Symposium on Copper in Biological Systems. (Peisach, J., Aisen, P., Blumberg, W.E., eds.). New York and London: Academic Press 1966
Quinn, D.J., Lane, C.E.: Ionic regulation and Na+-K+ stimulated ATP'ase activity in the land crab, Cardisoma guanhumi. Comp. Biochem. Physiol. 19, 533–543 (1966)
Rabin, H.: Hemocytes, hemolymph, and defense reactions in crustaceans. Res. J. reticuloendothel. Soc. 7, 195–207 (1970)
Schweiger, G.: Die toxikologische Einwirkung von Schwermetallsalzen auf Fische und Fischnährtiere. Arch. Fischereiwiss. 8, 54–78 (1967)
Shaw, J.: The absorption of chloride ions by the crayfish, Astacus pallipes (Lereboullet). J. exp. Biol. 37, 557–572 (1960)
Stang-Voss, C.: Zur Ultrastruktur der Blutzellen wirbelloser Tiere. V. Über die Hemocyten von Astacus astacus (L.) (Crustacea). Z. Zellforsch. 122, 68–75 (1971)
Stirling, C.E.: Radioautographic localization of sodium pump sites in rabbit intestine. J. Cell Biol. 53, 704–714 (1972)
Stoner, C.D., Sirak, H.D.: Osmotically-included alterations in volume and ultrastructure of mitochondria isolated from rat liver and bovine heart. J. Cell Biol. 43, 521–538 (1969)
Thurberg, F.P., Dawson, M.A., Collier, R.S.: Effects of copper and cadmium on osmoregulation and oxygen consumption in two species of estuarine crabs. Mar. Biol. 23, 171–175 (1973)
Toney, M.E.: Morphology of the blood cells of some crustacea. Growth 22, 35–50 (1958)
Tormey, J.M., Diamond, J.M.: The ultrastructural route of fluid transport in rabbit gall bladder. J. gen. Physiol. 50, 2031–2060 (1067)
Trump, B.F., Bulger, R.E.: Experimental modification of lateral and basilar plasma membranes and extracellular compartments in the flounder nephron. Fed. Proc. 30, 22–41 (1971)
Vernberg, W.B., O'Hara, J.: Temperature-salinity stress and mercury uptake in the fiddler crab Uca pugilator. J. Fish Res. Bd. Canada 29, 1491–1494 (1972)
Vernberg, W.B., Vernberg, J.: The synergistic effects of temperature, salinity, and mercury on survival and metabolism of the adult fiddler crab, Uca pugilator. Fish. Bull. 70, 415–421 (1972)
Voegtlin, C., Johnson, J.M., Dyer, H.A.: Protoplasmic action of copper and gold. Proc. nat. Acad. Sci. (Wash.) 11, 344–345 (1925)
Wright, E.M., Smulders, A.P., Tormey, J.M.: The role of the lateral intercellular spaces and solute polarization effects in the passive flows of water across the rabbit gall bladder. J. Membrane Biol. 7, 198–219 (1972)
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The author wishes to thank Dr. M.B. Jones and Mr. R.H. Moore for setting up the experiments and to Professor E. Naylor for providing laboratory facilities at the Department of Marine Biology, University of Liverpool, Port Erin, Isle of Man. This work was supported by a Ministry of Defence (Navy) Contract No. AT/2198/010/CDL.
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Bubel, A. Histological and electron microscopical observations on the effects of different salinities and heavy metal Ions, on the gills of Jaera nordmanni (Rathke) (Crustacea, Isopoda). Cell Tissue Res. 167, 65–95 (1976). https://doi.org/10.1007/BF00220160
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DOI: https://doi.org/10.1007/BF00220160