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The effects of aluminum and acid on the gill morphology in rainbow trout, Salmo gairdneii

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The objective was to determine the effects of acid and aluminum in acidified hard and soft water on the histology and morphometry of rainbow trout gills, and to determine relevant toxicity indicators within the gill tissue. Acid and aluminum promoted measurable primary epithelial hyperplasia which proved to be a reliable biological indicator of acid and aluminum contamination and possibly of some predictive value. Low levels of aluminum and acid resulted in hypertrophied chloride cells, suggesting a role in adapting to the contaminants. High concentrations of aluminum (>10 μmolI-1) caused chloride cell necrosis and consequently a decline in cell numbers over time. Aluminum precipitates accumulating within the chloride cell cytoplasm probably lead to impaired function prior to cell degeneration. The morphological alterations resulted in a decrease in water space between secondary lamellae (up to 40% within 14 d) which may reduce the efficiency of gas exchange. Twice the aluminum was required in hard water to elicit a similar soft water tissue response. Pathological changes were more severe with aluminum at pH 5.2 than at pH 4.7; results of aluminum speciation suggest that both labile and non-labile fractions are responsible for the induction of gill lesions. Low levels of aluminum may protect fish from the effects of high hydrogen ion concentration.

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References cited

  • Baker, J.P. 1981. Aluminum toxicity to fish as related to acid precipitation and Adirondack surface water quality. Ph.D. Thesis, Cornell University, Ithaca. 441 pp.

  • Baker, J.P. & C.L. Schofield. 1982. Aluminum toxicity to fish in acidic waters. Water Air Soil Pollut. 18: 289–309.

    Google Scholar 

  • Brown, D.J.A. 1983. Effect of calcium and aluminum concentrations on the survival of brown trout (Salmo trutta) at low pH. Bull. Environ. Contam. Toxicol. 30: 582–587.

    Google Scholar 

  • Brown, S.B., J.G. Eales, R.E. Evans & T.J. Hara. 1984. Interrenal, thyroidal, and carbohydrate responses of rainbow trout (Salmo gairdneri) to environmental acidification. Can. J. Fish. Aquat. Sci. 41: 36–45.

    Google Scholar 

  • Brumbaugh, W.G. & D.A. Kane. 1985. Variability of aluminum in organs and whole bodies of smallmouth bass Micropterus dolomieui. Environ. Sci. Technol. 19: 828–831.

    Google Scholar 

  • Buergel, P.M. & R.A. Soltero. 1983. The distribution and accumulation of aluminum in rainbow trout following a whole-lake alum treatment. J. Freshwater Ecol. 2: 37–44.

    Google Scholar 

  • Campbell, P.G.C., M. Bisson, R. Buogie, A. Tessier & J. Villeneuve. 1983. Speciation of aluminum in acidic freshwater. Anal. Chem. 55: 2246–2252.

    Google Scholar 

  • Chevalier, G., L. Gauthier & G. Moreau. 1985. Histopathological and electron microscopic studies of gills of brook trout, Salvelinus fontinalis, from acidified lakes. Can. J. Zool. 63: 2062–2070.

    Google Scholar 

  • Cleveland, L., E.E. Little, S.J. Hamilton, D.R. Buckler & J.B. Hunn. 1986. Interactive toxicity of aluminum and acidity to early life stages of brook trout. Trans. Amer. Fish.Soc. 115: 610–620.

    Google Scholar 

  • Cronan, C.S. & C.L. Schofield. 1979. Aluminum leaching response to acidic precipitation: effects on high elevation watersheds in the northeast. Science 204: 304–306.

    Google Scholar 

  • Daye, P.G. & E.T. Garside. 1976. Histopathological changes in surficial tissues of brook trout, Salvelinus fontinalis (Mitchill), exposed to acute and chronic levels of pH. Can. J. Zool. 54: 2140–2155.

    Google Scholar 

  • Driscoll, C. 1984. A procedure for the fractionation of aqueous aluminum in dilute acidic waters. Int. J. Environ. Anal. Chem. 16: 267–283.

    Google Scholar 

  • Driscoll, C.T. Jr., J.P. Baker, J.J. Bisogni Jr. & C.L. Schofield. 1980. Effects of aluminum speciation on fish in dilute acidified waters. Nature (London) 284: 161–164.

    Google Scholar 

  • Edwards, J.E. 1967. Methods for the demonstration of intercellular substances of the connective tissues. pp. 240–268. In: R. McClung Jones(ed.) McClung's Handbook of Microscopical Technique, 3rd ed., Hafner Publishing Co., New York.

    Google Scholar 

  • Evans, D.H., J.B. Claiborne, L. Farmer, C. Mallery & E.J. Krasny, Jr. 1982. Fish gill ionic transport: methods and models. Biol. Bull. 163: 108–130.

    Google Scholar 

  • Freeman, R.A. & W.H. Everhart. 1971. Toxicity of aluminum hydroxide complexes in neutral and basic media to rainbow trout. Trans. Amer. Fish. Soc. 100: 644–658.

    Google Scholar 

  • Fromm, P.O. 1980. A review of some physiological and toxicological responses of freshwater fish to acid stress. Env. Biol. Fish. 5: 79–93.

    Google Scholar 

  • Gagen, C.J. & W.E. Sharpe. 1987. Net sodium loss and mortality of three salmonid species exposed to a stream acidified by atmospheric deposition. Bull. Environ. Contam. Toxicol. 39: 7–14.

    Google Scholar 

  • Giles, M.A., H.S. Majewski & B. Hobden. 1984. Osmoregulatory and hematological responses of rainbow trout (Salmo gairdneri) to extended environmental acidification. Can. J. Fish. Aquat. Sci. 41: 1686–1694.

    Google Scholar 

  • Haines, T.A. 1981. Acidic precipitation and its consequences for aquatic ecosystems: a review. Trans. Amer. Fish. Soc. 111: 669–707.

    Google Scholar 

  • Harvey, H.H. 1980. Widespread and diverse changes in the biota of North American lakes and rivers coincident with acidification. pp. 93–98. In: D. Drablos & A. Tollan (ed.) Ecological Impact of Acid Precipitation, SNSF Project, Aas, Norway.

  • Henriksen, A., O.K. Skogheim & B.O. Rosseland. 1984. Episodic changes in pH and aluminum-speciation kill fish in a Norwegian salmon river. Vatten 40: 255–260.

    Google Scholar 

  • Hughes, G.M. 1973. Respiratory responses to hypoxia in fish. Amer. Zool. 13: 475–489.

    Google Scholar 

  • Hughes, G.M., S.F. Perry & V.M. Brown. 1979. A morphometric study of effects of nickel, chromium and cadmium on the secondary lamellae of rainbow trout gills. Water Res. 13: 665–679.

    Google Scholar 

  • Jagoe, C.H. & T.A. Haines. 1983. Alterations in gill epithelial morphology of yearling sunapee trout exposed to acute acid stress. Trans. Amer. Fish. Soc. 112: 689–695.

    Google Scholar 

  • Jagoe, C.H., T.A. Haines & D.R. Buckler. 1987. Abnormal gill development in Atlantic salmon (Salmo salar) fry exposed to aluminum at low pH. Annls. Soc. r. zool. Belg. 117: 375–386.

    Google Scholar 

  • Karlsson-Norrgren, L., I. Björklund, O. Ljungberg & P. Runn. 1986a. Acid water and aluminum exposure: experimentally induced gill lesions in brown trout, Salmo trutta L. J. Fish Diseases 9: 11–25.

    Google Scholar 

  • Karlsson-Norrgren, L., W. Dickson, O. Ljungberg & P. Runn. 1986b. Acid water and aluminum exposure: gill lesions and aluminum accumulation in farmed brown trout, Salmo trutta L. J. Fish Diseases 9: 1–9.

    Google Scholar 

  • Karlsson-Norrgren, L., P. Runn, C. Haux & L. Förlin. 1985. Cadmium-induced changes in gill morphology of zebrafish, Brachydanio rerio (Hamilton-Buchanan), and rainbow trout, Salmo gairdneri Richardson. J. Fish Biol. 27: 81–95.

    Google Scholar 

  • Karnaky, K.J. Jr., L.B. Kinter, W.B. Kinter & C.E. Stirling. 1976. Teleost chloride cell. 11 Autoradiographic localization of gill Na, K-ATPase in killifish (Fundulus heteroclitus) adapted to low and high salinity environments. J. Cell Biol. 70: 157–177.

    Google Scholar 

  • Klaverkamp, J.F., S.B. Brown, R.E. Evans, H.S. Majewski, D. Metner & H. Freeman. 1986. Biochemical and cellular indicators of acid and starvation induced stress in Atlantic salmon from Nova Scotia rivers. Society of Environmental Toxicology and Chemistry, 7th annual meeting, Abstract 247: 126.

    Google Scholar 

  • Laurent, P. & S. Dunel. 1980. Morphology of gill epithelia in fish. Amer. J. Physiol. 238: R147–R159.

    Google Scholar 

  • LaZerte, B.D. 1984. Forms of aqueous aluminum in acidified catchments of central Ontario: a methodological analysis. Can. J. Fish. Aquat. Sci. 41: 766–776.

    Google Scholar 

  • Leino, R.L. & J.H. McCormick. 1984. Morphological and morphometrical changes in chloride cells of the gill of Pimephales promelas after chronic exposure to acid water. Cell Tissue Res. 236: 121–128.

    Google Scholar 

  • Leivestad, H. 1982. Physiological effects of acid stress on fish. pp. 157–164. In: R.E. Johnson(ed.) Acid Rain/Fishes, American Fisheries Society Publication, Bethesda.

    Google Scholar 

  • Mallatt, J. 1985. Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can. J. Fish. Aquat. Sci. 42: 630–648.

    Google Scholar 

  • Marshall, W.S. 1985. Paracellular ion transport in trout opercular epithelium models osmoregulatory effects of acid precipitation. Can. J. Zool. 61: 1816–1822.

    Google Scholar 

  • May, H.M., P.A. Helmke & M.L. Jackson. 1979. Gibbsite solubility and thermodynamic properties of hydroxyl-aluminum ions in aqueous solution at 25°C. Geochim. Cosmochim. Acta 43: 861–868.

    Google Scholar 

  • McCormick, J.H., K.M. Jensen, R.L. Leino & G.N. Stokes. 1987. Fish blood osmolality, gill histology and oocyte atresia as early warning acid stress indicators. Annls. Soc. r. zool. Belg. 117: 309–391.

    Google Scholar 

  • McDonald, D.G. 1983. The effects of H+ upon the gills of freshwater fish. Can. J. Zool. 61: 691–703.

    Google Scholar 

  • McWilliams, P.G. 1983. An investigation of the loss of bound calcium from the gills of the brown trout, Salmo trutta, in acid media. Comp. Biochem. Physiol. A 74: 107–116.

    Google Scholar 

  • Merz, W.A. 1967. Die Streckenmessung an gerichteten Strukturen im Mikroscop and ihr Anwendung zur Bestimmung von Oberflachen-Volumen-Relationen im Knockengewebe. Mikroskopie 22: 132–142.

    Google Scholar 

  • Morgan, M. & P.W.A. Tovell. 1973. The structure of the gill of the trout, Salmo gairdneri (Richardson). Z. Zellforsch. mikrosk. Anat. 142: 147–162.

    Google Scholar 

  • Muniz, L.P. & H. Leivested. 1980. Toxic effects of aluminum on the brown trout, Salmo trutta L. pp. 320–321. In: Proceedings of an International Conference on Ecological Impact of Acid Precipitation. SNSF Project, ISBN 82-90376-07-3, Norway.

  • Oronsaye, J.A.O. & A.E. Brafield. 1984. The effect of dissolved cadmium on the chloride cells of the gills of the stickleback, Gasterosteus aculeatus L. J. Fish Biol. 25: 253–258.

    Google Scholar 

  • Pagenkopf, G.K. 1983. Gill surface interaction model for tracemetal toxicity to fishes: role of complexation, pH, and water hardness. Environ. Sci. Technol. 17: 342–347.

    Google Scholar 

  • Pang, P.K.T. 1983. Evolution of control of epithelial transport in vertebrates. J. Exp. Biol. 106: 283–299.

    Google Scholar 

  • Payan, P., N. Mayer-Gostan & P.K.T. Pang. 1981. Site of calcium uptake in the fresh water trout gill. J. Exp. Zool. 216: 345–347.

    Google Scholar 

  • Playle, R, J. Gleed, R. Jonasson & J.R. Kramer. 1982. Comparison of atomic absorption spectrometric, pectrophotometric, and fluorimetric methods for determination of aluminum in water. Anal. Chim. Acta 134: 369–373.

    Google Scholar 

  • Schoeffeniels, E. 1967. Cellular aspects of membrane permeability. Pergamon Press, Oxford. 266 pp.

    Google Scholar 

  • Schofield, C.L. & J.R. Trojnar. 1980. Aluminum toxicity to brook trout (Salvelinus fontinalis) in acidified waters. Environ. Sci. Res. 17: 341–366.

    Google Scholar 

  • Skidmore, J.F. & P.W.A. Tovell. 1972. Toxic effects of zinc sulphate on the gills of rainbow trout. Water Res. 6: 217–230.

    Google Scholar 

  • Soivio, A. & H. Tuurala. 1981. Structural and circulatory responses to hypoxia in the secondary lamellae of Salmo gairdneri gills at two temperatures. J. Comp. Physiol. 145: 37–44.

    Google Scholar 

  • Southwood, T.R.E. 1978. Ecological methods, with particular reference to the study of insect populations. 2nd ed., John Wiley & Sons, New York. 524 pp.

    Google Scholar 

  • Staurnes, M., T. Sigholt & O.B. Reite. 1984. Reduced carbonic anhydrase and Na-sbnd;K ATPase activity in gills of salmonids exposed to aluminum-containing acid water. Experientia 40: 226–227.

    Google Scholar 

  • Wendelaar Bonga, S.E. & L.H.T. Dederen. 1986. Effects of acidified water on fish. Endeavour, new series 10: 198–202.

    Google Scholar 

  • Winer, B.J. (ed.) 1971. Statistical principles in experimental design. 2nd ed., McGraw-Hill Book Co., New York. 907 pp.

  • Wright, R.F. & E.T. Gjessing. 1976. Acid precipitation: changes in the chemical composition of lakes. Ambio 5: 219–223.

    Google Scholar 

  • Wyllie, A.H. 1981. Cell death: a new classification separating apoptosis from necrosis. pp 9–34. In: I.D. Bowen & R.A. Lockshin(ed.) Cell Death in Biology and Pathology, Chapman and Hall, London.

    Google Scholar 

  • Youson, J.H. & C.M. Neville. 1987. Deposition of aluminum in the gill epithelium of rainbow trout (Salmo gairdneri Richardson) subjected to sublethal concentrations of the metal. Can. J. Zool. 65: 647–656.

    Google Scholar 

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  1. Department of Fisheries and Oceans, Freshwater Institute, Central and Arctic Region, Winnipeg, Manitoba, R3T 2N6, Canada

    Robert E. Evans, Scott B. Brown & Toshiaki J. Hara

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  1. Robert E. Evans
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Evans, R.E., Brown, S.B. & Hara, T.J. The effects of aluminum and acid on the gill morphology in rainbow trout, Salmo gairdneii . Environ Biol Fish 22, 299–311 (1988). https://doi.org/10.1007/BF00004895

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