Skip to main content
SpringerLink
Log in

Morphological and morphometrical changes in chloride cells of the gills of Pimephales promelas after chronic exposure to acid water

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Fathead minnows, Pimephales promelas, were exposed for 129 days to Lake Superior water acidified with sulfuric acid by means of a flow-through toxicant injection system. The effects of chronic acid stress (pH 6.5, 6.0, 5.5, 5.0) on gill histology were examined. Most of the histological effects were seen at pH 5.5 and 5.0 and were confined primarily to changes in numbers, distribution, and morphology of chloride cells. At low pH levels there tend to be more chloride cells in the gill epithelium and an increased percentage of these cells in the secondary lamellae. In contrast to normal chloride cells, chloride cells from fish exposed to low pH frequently had apical pits while some had bulbous apical evaginations. The occurrence of structural changes in chloride cells during exposure to acid water suggests that chloride cells may be involved in acclimation to acid stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahuja SK (1970) Chloride cell and mucus 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

    Google Scholar 

  • Beamish RJ (1976) Acidification of lakes in Canada by acid precipitation and resulting effects on fishes. Water Air Soil Pollut 6:501–514

    Google Scholar 

  • Bennett HS, Wyrick AD, Lee SW, McNeil JH (1976) Science and art in preparing tissues embedded in plastic for light microscopy, with special reference to glycol methacrylate, glass knives and simple stains. Stain Technol 51:71–97

    Google Scholar 

  • Bierther M (1970) Die Chloridzellen des Stichlings. Z Zellforsch 107:421–446

    Google Scholar 

  • Biesinger KE, Christensen GM (1972) Effects of various metals on survival, growth, reproduction, and metabolism of Daphnia magna. J Fish Res Board Can 29:1691–1700

    Google Scholar 

  • Booth JH, Jansz GF, Holeton GF (1982) Cl-, K+, and acid-base balance in rainbow trout during exposure to and recovery from, sublethal environmental acidification. Can J Zool 60:1123–1130

    Google Scholar 

  • Bornancin M, de Renzis G, Naon K (1980) Cl--HCO +3 -ATPase in gills of the rainbow trout: evidence for its microsomal localization. Am J Physiol 238:R251-R259

    Google Scholar 

  • Bradley TJ (1981) Improved visualization of apical vesicles in chloride cells using an osmium quick-fix technique. J Exp Zool 217:185–198

    Google Scholar 

  • Cronan CS, Schofield CL (1979) Aluminium leaching response to acid precipitation — effects on high elevation watersheads in the Northeast. Science 204:304–306

    Google Scholar 

  • Daye PG, Garside ET (1976) Histopathologic 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 

  • DeFoe DL (1975) Multichannel toxicant system for flow-through bioassays. J Fish Res Board Can 32:544–546

    Google Scholar 

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

    Google Scholar 

  • Eddy FB, Lomholt JP, Weber RE, Johansen K (1977) Blood respiratory properties of rainbow trout (Salmo gairdneri) kept in water of high CO2 tension. J Exp Biol 67:37–47

    Google Scholar 

  • Evans DH (1975) Ionic exchange mechanisms in fish gills. Comp Biochem Physiol 51A:491–495

    Google Scholar 

  • Fromm PO (1980) A review of some physiological and toxicological responses of freshwater fish to acid stress. Environ Biol Fish 5:79–93

    Google Scholar 

  • Heisler N (1982) Transepithelial ion transfer processes as mechanisms for fish acid-base regulation in hypercapnia and lactacidosis. Can J Zool 60:1108–1122

    Google Scholar 

  • Henricksen A, Wright RF (1978) Concentrations of heavy metals in small Norwegian lakes. Water Res 12:101–112

    Google Scholar 

  • Hossler FE, Ruby JR, McIlwain TD (1979) 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 208:403–410

    Google Scholar 

  • Hultberg H, Stenson J (1970) Effects of acidity on the fish fauna of two small lakes in Bohuslan, southwestern Sweden. Fauna Flora (Stockh) 1:11–20

    Google Scholar 

  • Istin M, Maren T (1971) Effect of dissolved CO2 on sodium uptake by the gill of a fresh water fish, Carassius auratus. Bull Mt Desert Isl Biol Lab 11:46–47

    Google Scholar 

  • Laurent P, Dunel S (1980) Morphology of gill epithelia in fish. Am J Physiol 238:R147-R159

    CAS  PubMed  Google Scholar 

  • Lee RM, Gerking SD, Jezierska B (1983) Electrolyte balance and energy mobilization in acid-stressed rainbow trout, Salmo gairdneri, and their relation to reproductive success. Environ Biol Fish 8:115–123

    Google Scholar 

  • Leino RL, Anderson JG, McCormick JH (1983) Development of apical pits in chloride cells of the gills of Pimephales promelas after chronic exposure to acid water. In: Bailey GW (ed) Proc Annu Meet Electron Microsc Soc Am, 41st. San Francisco Press, San Francisco, pp 462–463

    Google Scholar 

  • Leivestad H, Muniz IP (1976) Fish kill at low pH in a Norwegian river. Nature 259:391–392

    Google Scholar 

  • McDonald DG, Wood CM (1981) Branchial and renal acid and ion fluxes in the rainbow trout, Salmo gairdneri, at low environmental pH. J Exp Biol 93:101–118

    Google Scholar 

  • McDonald DG, Hobe H, Wood CM (1980) The influence of calcium on the physiological responses of the rainbow trout, Salmo gairdneri, to low environmental pH. J Exp Biol 88:109–131

    Google Scholar 

  • McWilliams PG, Potts WTW (1978) The effects of pH and calcium concentrations on gill potentials in the brown trout, Salmo trutta. J Comp Physiol 126:277–286

    Google Scholar 

  • Morgan M, Tovell PWA (1973) The structure of the gill of the trout, Salmo gairdneri (Richardson). Z Zellforsch 142:147–162

    Google Scholar 

  • Mount DI (1973) Chronic effect of low pH on fathead minnow survival, growth and reproduction. Water Res 7:987–993

    Google Scholar 

  • Neville CM (1979) Sublethal effects of environmental acidification on rainbow trout (Salmo gairdneri). J Fish Res Board Can 36:84–87

    Google Scholar 

  • Nie NH, Hull HC, Jenkens JG, Steinbrenner K, Bent DH (1975) Statistical package for the social sciences, 2nd ed. McGraw-Hill, New York

    Google Scholar 

  • Nieminen M, Korhonen I, Laitinen M (1982) Effects of pH on the gill ATPase activity and blood composition of whitefish (Coregonus peled) and trout (Salmo trutta fario). Comp Biochem Physiol 72A:637–642

    Google Scholar 

  • Packer RK (1979) Acid-base balance and gas exchange in brook trout (Salvelinus fontinalis) exposed to acidic environments. J Exp Biol 79:127–134

    Google Scholar 

  • Packer RK, Dunson WA (1970) Effects of low environmental pH on blood pH and sodium balance of brook trout. J Exp Zool 174:65–72

    Google Scholar 

  • Packer RK, Dunson WA (1972) Anoxia and sodium loss associated with the death of brook trout at low pH. Comp Biochem Physiol 41(A):17–26

    Google Scholar 

  • Payen P, Mayer-Gostan N, Pang PKT (1981) Site of calcium uptake in the fresh water trout gill. J Exp Zool 216:345–347

    Google Scholar 

  • Philpott CW (1968) Functional implications of the cell surface: the plasmalemma and surface associated polyanions. In: Porter R, O'Connor M (eds) Ciba Foundation Study Group 32. Little and Brown, Boston, pp 109–116

    Google Scholar 

  • Philpott CW (1980) Tubular system membranes of teleost chloride cells: osmotic response and transport sites. Am J Physiol 238:R171-R184

    Google Scholar 

  • Philpott CW, Copeland DE (1963) Fine structure of chloride cells from three species of Fundulus. J Cell Biol 18:109–116

    Google Scholar 

  • Randall DJ, Perry SF, Heming TA (1982) Gas transfer and acidbase regulation in salmonoids. Comp Biochem Physiol 73 B:93–103

    Google Scholar 

  • Revel JP (1964) A stain for the ultrastructural location of acid mucopolysaccharides. J Microsc 3:535–544

    Google Scholar 

  • Romanenko VD, Krisal'nyy VA (1977) Some features of ion exchange in fish during their adaptation to a higher CO2 content in the water. Gidrobiol Zh 13:83–86

    Google Scholar 

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

    Google Scholar 

  • Schindler DW, Turner MA (1982) Biological, chemical and physical responses of lakes to experimental acidification. Water Air Soil Pollut 18:259–271

    Google Scholar 

  • Schofield CL (1976) Eake acidification in the Adirondack Mountains of New York: causes and consequences. USDA Forest Serv Gen Tech Rep NE-23

  • Schofield CL (1977) Acid snow-melt effects on water quality and fish survival in the Adirondack Mountains of New York State. U.S. NTIS Report PB-277801

  • Threadgold L, Houston A (1964) An electron microscope study of the chloride cell of Salmo salar E. Exp Cell Res 34:1–23

    Google Scholar 

  • Ultsch GR (1978) Oxygen consumption as a function of pH in three species of freshwater fishes. Copeia 2:272–279

    Google Scholar 

  • Ultsch GR, Ott ME, Heisler N (1981) Acid-base and electrolyte status in carp (Cyprinus carpio) exposed to low environmental pH. J Exp Biol 93:65–80

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical Anatomy, School of Medicine, University of Minnesota, Duluth, MN, USA

    Richard L. Leino & J. Howard McCormick

  2. U.S. Environmental Protection Agency, Environmental Research Laboratory, Duluth, MN, USA

    Richard L. Leino & J. Howard McCormick

Authors
  1. Richard L. Leino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Howard McCormick
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Leino, R.L., McCormick, J.H. Morphological and morphometrical changes in chloride cells of the gills of Pimephales promelas after chronic exposure to acid water. Cell Tissue Res. 236, 121–128 (1984). https://doi.org/10.1007/BF00216521

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00216521

Key words

Search

Navigation