Skip to main content
Log in

Histopathologic Biomarkers in Three Spined Sticklebacks, Gasterosteus aculeatus, from Several Rivers in Southern England that Meet the Freshwater Fisheries Directive

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

This study demonstrates the utility and sensitivity of histopathologic biomarkers by recording lesions to the gill, liver and spleen in three spined sticklebacks (Gasterosteus aculeatus) from several rivers in Southern England which broadly comply with the water quality directives to protect fish health. The main study site was the Letcombe Brook system near Wantage, graded 1 (good) to 3 (fair) by the Environment Agency, using the River Ecosystem (RE) Class system. Sites with similar grades on the rivers Erme, Clyst, Exe and Plym were also selected in Devon. A normal condition factor (0.9±0.02, mean±S.E., n=90), the presence of food in the stomach, and the whole body ionic composition (Na, K, Mg, Ca, Cu, Zn) suggested that fish were generally healthy. All fish showed some minor incidence of gill and liver lesions, even in the best (grade RE1) river water quality. Scoring the percentage of branchial secondary lamellae showing lesions did not reflect water quality because of biotic factors such as parasite load. However, fatness of secondary lamellae (length/width) increased in lower class rivers. Hepatic fatty change and focal necrosis was related to river quality grades with fatty change increasing from 0.8% to 12% of total liver area in grade RE1 and RE2 rivers, respectively. The gross anatomy of the spleen showed normal red and white pulp, and sinusoid space varied between 11% and 34% of the tissue area, but was not correlated with river grade. Overall, we conclude that histopathologic lesions are present in fish even when water quality meets the Freshwater Fisheries Directive. The Directive therefore only partly protects fish health. The incidence of fatty change in the liver, or fatness of secondary lamellae, in adult three spined sticklebacks are suggested as simple but sensitive histopathologic biomarkers which may be used to protect freshwater fishes as a novel alternative approach to water quality based Directives. We propose histopathologic biomarkers of the three spined stickleback for routine monitoring of fish health in EU freshwaters.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams, S.M., Ham, K.D., Greeley, M.S., LeHew, R.F., Hinton, D.E. and Saylor, C.F. (1996). Downstream gradients in bioindicator responses: point source contaminants effect on fish health. Can. J. Fisheries Aquat. Sci. 53, 2177–87.

    Google Scholar 

  • Braunbeck, T. (1998). Cytological alterations in fish hepatocytes following in vivo and in vitro sublethal exposure to xenobiotics-structural biomarkers of environmental contamination. In T. Braunbeck, D.E. Hinton and B. Streit (eds). Fish Ecotoxicology, pp. 61–140. Basel Switzerland: Birkhäuser Verlag.

    Google Scholar 

  • Bernet, D., Schmidt, H., Meier, W., Burkhardt-Holm, P. and T. Wahli, (1999). Histopathology in fish: proposal for a protocol to assess aquatic pollution. J. Fish Dis. 22, 25–34.

    Google Scholar 

  • Blom, S., Norrgren, L. and Förlin, L. (1998). Sublethal effects in caged rainbow trout during remedial activites in Lake Järnsjön. Ambio. 27, 411–8.

    Google Scholar 

  • Chevalier, G., Gauthier, L. and Moreau, G. (1985). Histopathological and electron microscope studies of gills of brook trout, Salvelinus alpinus, from acidified lakes. Can. J. Zool. 63, 2062–70.

    Google Scholar 

  • Couch, J.A. (1975). Histopathological effects of pesticides and related chemicals on the liver of fishes. In W.E. Ribelin, and G. Migaki (eds). The Pathology of Fishes, pp. 559–84. Madison: University of Wisconsin Press.

    Google Scholar 

  • Couch, J.A. (1984). Histopathology and enlargement of the pituitary of a teleost exposed to the herbicide trifluralin. J. Fish Dis. 7, 157–63.

    Google Scholar 

  • Couillard, C.M., Williams, P.J., Courtenay, S.C. and Rawn, G.P. (1999). Histopathological evaluation of Atlantic tomcod (Microgadus tomcod) collected at estuarine sites receiving pulp and paper mill effluent. Aquat. Toxicol. 44, 263–78.

    Google Scholar 

  • Environment Agency, (1996). Local Environment Agency Plan: Tamar Estuary and Tributaries (July 1996). Environment Agency, Bodmin Cornwall, UK.

    Google Scholar 

  • Förlin, L., Haux, C., Karlsonn-Norrgren, L., Runn, P. and Larsson, A. (1986). Biotransformation enzyme activities and histopathology in rainbow trout, Salmo gairdneri, treated with cadmium. Aquat. Toxicol. 8, 51–64.

    Google Scholar 

  • Grady, A.W., Mclaughlin, R.M., Caldwell, C.W., Schmitt, C.J. and Stalling, D.L. (1992). Flow cytometry, morphometry and histopathology as biomarkers of benzo[a]pyrene exposure in brown bullheads (Ameiurus nebulosus). J. Appl. Toxicol. 12, 165–77.

    Google Scholar 

  • Hampton, J.A., Lantz, R.C., Goldblatt, P.J., Laurén, D.J. and Hinton, D.E. (1988). Functional units in rainbow trout (Salmo gairdneri, Richardson) liver: II. The biliary system. Anatom. Record. 221, 619–34.

    Google Scholar 

  • Hampton, J.A., McCuskey, P.A., McCuskey, R.S. and Hinton, D.E. (1985). Functional units in rainbow trout (Salmo gairdneri) liver: I. Arrangement and histochemical properties of hepatocytes. Anatom. Record. 213, 166–75.

    Google Scholar 

  • Handy, R.D. and Depledge, M.H. (1999). Physiological responses: their measurement and use as environmental biomarkers in ecotoxicology. Ecotoxicology 8, 329–49.

    Google Scholar 

  • Handy, R.D., Sims, D.W., Giles, A., Campbell, H.A. and Musonda, M.M. (1999). Metabolic trade-off between locomotion and detoxification for maintenance of blood chemistry and growth parameters by rainbow trout (Oncorhynchus mykiss) during chronic dietary exposure to copper. Aquat. Toxicol. 47, 23–41.

    Google Scholar 

  • Hinton, D.E. and Laurén, D.J. (1990). Integrative histopathological approaches to detecting effects of environmental stressors on fish. In S.M. Adams (ed.). Biological Indicators of Stress in Fish, pp. 51–66. American Fisheries Society, Bethesda Maryland, USA.

    Google Scholar 

  • Hinton, D.E., Baumann, P.C., Gardner, G.R., Hawkins, W.E., Hendricks, J.D., Murchelano, R.A. and Okihiro, M.S. (1992). In R.J. Hugget, R.A. Kimerle, P.M. Mehrle and H.L. Bergman (eds). Biomarkers, Biochemical, Physiological and Histological Markers of Anthropogenic Stress, pp. 201–12. Boca Raton: Lewis Publishers, SETAC publication.

    Google Scholar 

  • Hinton, D.E. and Couch, J.A. (1998). Architectural pattern, tissue and cellular morphology in livers of fishes; relationship to experimentally-induced neoplastic responses. In T. Braunbeck, D.E. Hinton and B. Streit (eds). Fish Ecotoxicology, pp. 141–64. Basel Switzerland: Birkhäuser Verlag.

    Google Scholar 

  • Holdway, D.A., Brennan, S.E. and Ahokas, J.T. (1995). Short review of selected fish biomarkers of xenobiotic exposure with an example using fish hepatic mixed-function oxidase. Aus. J. Ecol. 20, 34–44.

    Google Scholar 

  • Holm, G., Norrgren, L. and Lindén, O. (1991). Reproductive and histopathological effects of long-term experimental exposure to bis(tributyltin)oxide (TBTO) on the three-spined stickleback, Gasterosteus aculeatus Linnaeus. J. Fish Biol. 38, 373–86.

    Google Scholar 

  • Hughes, G.M. (1984). General anatomy of the gills. In W.S. Hoar and D.J. Randall (eds). Fish Physiology, pp. 1–72. New York: Academic Press.

    Google Scholar 

  • Hughes, G.M. and Perry, S.F. (1976). Morphometric study of trout gills: a light-microscopic method suitable for the evaluation of pollutant action. J. Exp. Biol. 64, 447–60.

    Google Scholar 

  • Leino, R.L., Wilkinson, P. and Anderson, J.G. (1987). Histopathological changes in the gills of the pearl dace, Semotilus margarita, and fathead minnows, Pimephales promelas, from experimentally acidified Canadian lakes. Can. J. Fisheries Aquat. Sci. 44(suppl.), 126–34.

    Google Scholar 

  • Livingstone, D.R. and Goldfarb, P.S. (1998). Biomonitoring in the aquatic environment: use of cytochrome P450 1A and other molecular biomarkers in fish and mussels. In J.M. Lynch, and A. Wiseman (eds). Environmental Biomonitoring: The Biotechnology Ecotoxicology Interface, pp. 101–29. Cambridge: Cambridge University Press.

    Google Scholar 

  • Mallatt, J. (1985). Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can. J. Fisheries Aquat. Sci. 42, 630–48.

    Google Scholar 

  • Matthiessen, P. and Brafield, A.E. (1973). The effects of dissolved zinc on the gills of the stickleback Gasterosteus aculeatus (L). J. Fish Biol. 5, 607–613.

    Google Scholar 

  • Matthiessen, P. and Brafield, A.E. (1977). Uptake and loss of dissolved zinc by the stickleback Gasterosteus aculeatus. J. Fish Biol. 10, 399–410.

    Google Scholar 

  • McCarthy, J.F. and Shugart, L.R. (1990). Biomarkers of Environmental Contamination. Boca Raton Florida, USA: Lewis Publishers.

    Google Scholar 

  • Norrgren, L., Pettersson, U., Örn, S. and Bergqvist, P.-A. (2000). Environmental monitoring of the Kafue River, located in the Copperbelt, Zambia. Arch. Environ. Contam. Toxicol. 38, 334–41.

    Google Scholar 

  • NRA, (1994). Implementation of the EC Freshwater Fish Directive. Water Quality Requirements for the Support of Fish LifeReport of the National Rivers Authority, Water Quality Series No. 20. London: HMSO publishers.

    Google Scholar 

  • Peakall, D.B. (1994). The role of biomarkers in environmental assessment. (1). Introduction. Ecotoxicology 3, 157–60.

    Google Scholar 

  • Sawcer, K.E., Yeomans, W.E. and Thorpe, G.H.G. (1999). Enhanced chemiluminescence as an indicator of water quality. J. Chartered Institution Water Environ. Manag. 13, 170–6.

    Google Scholar 

  • Schwaiger, J., Bucher, F., Ferling, H., Kalbfus, W., Negele, R.D. (1992). A prolonged toxicity study on the effects of sublethal concentrations of bis(tri-n-butylin)oxide (TBTO): histopathological and histochemical findings in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 23, 31–48.

    Google Scholar 

  • Schwaiger, J., Wanke, R., Adam, S., Pawert, M., Honnen, W. and Triebskorn, R. (1997). The use of histopathological indicators to evaluate contaminant-related stress in fish. J. Aquat. Ecosyst. Stress Recov. 6, 75–86.

    Google Scholar 

  • Svobodová, Z., Lloyd, R., Máchová, J. and Vykusová, B. (1993). Water Quality and Fish Health. European Inland Fisheries Advisory Committee (EIFAC) Technical Paper No. 54. Rome: F.A.O.

    Google Scholar 

  • Teh, S.J., Adams, S.M. and Hinton, D.E. (1997). Histopathologic biomarkers in feral freshwater fish populations exposed to different types of contaminant stress. Aquat. Toxicol. 37, 51–70.

    Google Scholar 

  • Wendelaar Bonga, S.E. (1978). The effects of changes in external sodium, calcium, and magnesium concentrations on prolactin cells, skin, and plasma electrolytes of Gasterosteus aculeatus. General Comparat. Endocrinol. 34, 265–75.

    Google Scholar 

  • Wesley, J.B., Price, D.J., Shaw, J.R., Spromberg, J.A., Wigginton, A.J. and Hogstrand, C. (2000). Metal body burden and biological sensors as ecological indicators. Environ. Toxicol. Chem. 19, 1199–212.

    Google Scholar 

  • Wootton, R.J. and Smith, C. (2000). A long-term study of a short-lived fish: the demography of Gasterosteus aculeatus. Behaviour. 137, 981–97.

    Google Scholar 

  • Yasutake, W.T. and Wales, J.H. (1983). Microscopic Anatomy of Salmonids: An Atlas. pp. 91–5. Washington DC: United States Department of the Interior, Fish and Wildlife Service, Resource Publication 150.

    Google Scholar 

  • Yeomans, W.E., Chubb, J.C. and Sweeting, R.A. (1997). Use of protozoan communities for pollution monitoring. Parassitologia 39, 201–12.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R.D. Handy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Handy, R., Runnalls, T. & Russell, P. Histopathologic Biomarkers in Three Spined Sticklebacks, Gasterosteus aculeatus, from Several Rivers in Southern England that Meet the Freshwater Fisheries Directive. Ecotoxicology 11, 467–479 (2002). https://doi.org/10.1023/A:1021061402491

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1021061402491

Navigation