Skip to main content
SpringerLink
Log in

Ultrastructural biomarkers as tools to characterize the health status of fish in contaminated streams

  • Published:
Journal of Aquatic Ecosystem Stress and Recovery

Abstract

Ultrastructural biomarkers in gill, liver, andkidney of brown trout (Salmo truttaf. fario) and stone loach (Barbatulabarbatula) were investigated over afive year period. The cellular damage of theorgans was assessed semi-quantitatively basedon a three-step classification ofultrastructural responses. Data obtained forfish exposed under semi-field conditions in twodifferently polluted test streams and in thelaboratory demonstrated that the ultrastructureof the organs can be correlated with differentpollutant exposure conditions. Cellular damagewas generally more severe in fish exposed to acomplexly polluted stream than in those exposedto a moderately polluted stream or to tap waterin the laboratory. Histopathological effects inliver and gill of trout were more pronounced inferal fish than in transplanted fish, whereasresponses in the kidney in both species, and inliver and gill of loach, were similar forintroduced and feral fish. In a laboratoryexperiment where trout were exposed todifferent mixtures of pollutants includingpesticides, PAH, and ammonia, only theultrastructure of kidney and liver showedsignificant differences between the threeexperimental set-ups. In a recovery experiment,where trout were transferred from thesemi-field condition back to the laboratory,ultrastructural investigations showed adifferential capacity of the respective organsto recover from stress under field conditions.Kidney and liver fully recovered after threemonths under control condition whereas gillsdemonstrated only partial recovery.

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

  • Abi-Ayad, A. & P. Kestemont, 1994. Comparison of the nutrional status of goldfish (Carassius auratus) larvae fed with live, mixed or dry diet. Aquaculture 128: 163-176.

    Google Scholar 

  • Abel, P. D. & J. F. Skidmore, 1975. Toxic effects of an anionic detergent on the gills of rainbow trout. Water Res. 9: 759-765.

    Google Scholar 

  • Adam, S., M. Pawert, R. Lehmann, B. Roth, E. Müller & R. Triebskorn, 2001. Physicochemical and morphological characterization of two small polluted streams in southwest Germany, J. Aquat. Ecosyst. Stress. Recov. 8: 179-194.

    Google Scholar 

  • Adams, S. M., K. L. Shepard, M. S. Greeley, B. D. Jimenez, M. G. Ryon, L. R. Shugart & J. F. McCarthy, 1989. The use of bioindicators for assessing the effects of pollutant stress on fish. Mar. Environ. Res. 28: 459-464.

    Google Scholar 

  • Adams, S. M., M. S. Greeley & M. G. Ryon, 2000. Evaluating effects of contaminants on fish health at multiple levels of biological organization: Extrapolating from lower to higher levels. Human Ecol. Risk Ass. 6(1): 15-27.

    Google Scholar 

  • Alazemi, B. M., J. W. Lewis & E. B. Andrews, 1996. Gill damage in the freshwater fish Gnathonemus petersii (Family: Mormyridae) exposed to selected pollutants: An ultrastructural study. Environ. Technol. 17: 225-238.

    Google Scholar 

  • Arias, I. M., W. B. Jacoby, H. Popper, D. Schachter & D. A. Schafritz, 1988. The Liver: Biology and Pathobiology. Raven Press, New York.

    Google Scholar 

  • Au, D. W. T., R. S. S. Wu, B. S. Zhou & P. K. S. Lam, 1999. Relationship between ultrastructural changes and EROD activities in liver of fish exposed to Benzo[a]pyrene. Env. Poll. 104(2): 235-247.

    Google Scholar 

  • Behrens, A. & H. Segner, 2001. Hepatic biotransformation enzymes of fish exposed to non-point source pollution in small streams. J. Aquat. Ecosyst. Stress. Recov. 8: 281-297.

    Google Scholar 

  • Beier, S. & W. Traunspurger, 2001. The meiofauna community of two small German streams as indicators of pollution. J. Aquat. Ecosyst. Stress. Recov. 8: 387-405.

    Google Scholar 

  • Bindon, S. D., J. C. Fenwick & S. F. Perry, 1993. Branchial chloride cell proliferation in the rainbow trout, Oncorhynchus mykiss: Implications for gas transfer. Can. J. Zool. 72: 1395-1402.

    Google Scholar 

  • Bindon, S. D., K. M. Gilmour, J. C. Fenwick & S. F. Perry, 1994. The effects of branchial chloride cell proliferation on respiratory function in the rainbow trout Onchorhynchus mykiss. J. Exp. Biol. 197: 47-63.

    Google Scholar 

  • Böhmer, J., A. Zenker, B. Ackermann & B. Kappus, 2001. Macrozoobenthos communities and biocoenotic assessment of ecological status in relation to degree of human impact in small streams in southwest Germany. J. Aquat. Ecosyst. Stress. Recov. 8: 407-419.

    Google Scholar 

  • Braunbeck, T., 1992. Cytological alterations in isolated hepatocytes from rainbow trout induced by 4-chloroaniline. Aquat. Toxicol. 22: 57-65.

    Google Scholar 

  • Braunbeck, T., 1998. Cytological alterations in fish hepatocytes following in vivo and in vitro sublethal exposure to xenobiotics-structural biomarkers of environmental contaminations. In: Hinton, D. J., T. Braunbeck & B. Streit (eds), Fish Ecotoxicology. Birkhäuser Verlag, Basel: 61-139.

    Google Scholar 

  • Braunbeck, T. & A. Völkl, 1993. Toxicant-induced cytological alterations in fish liver as biomarkers of environmental pollution? A case study on hepatocellular effects of dinitro-o-cresol in golden ide (Leuciscus idus melanotus). In: Braunbeck, T., W. Hanke & H. Segner (eds), Fish Ecotoxicology and Ecophysiology. VCH Verlagsgesellschaft, Weinheim: 55-80.

    Google Scholar 

  • Braunbeck, T. & S. Appelbaum, 1999. Ultrastructural alterations in the liver and intestine of carp Cyprinus carpio induced orally by ultra-low doses of endosulfan. Dis. Aquat. Org. 36: 183-200.

    Google Scholar 

  • Brown, J. A., S. M. Taylor & C. J. Gray, 1983. Glomerular ultrastructure of the trout, Salmo gairdneri. Cell. Tissue Res. 230: 203-218.

    Google Scholar 

  • Bucher, F. & R. Hofer, 1993. The effects of treated domestic sewage on three organs (gills, kidney, liver) of brown trout (Salmo trutta). Wat. Res. 27(2): 255-261.

    Google Scholar 

  • Burckhardt-Holm, P., Y. Oulmi, A. Schroeder, V. Storch & T. Braunbeck, 1999. Toxicity of 4-chloroaniline in early life stages of zebrafish (Danio rerio): II. Cytopathology and regeneration of liver and gills after prolonged exposure to waterborne 4-chloroaniline. Arch. Environ. Contam. Toxicol. 37: 85-102.

    Google Scholar 

  • Chevalier, G. L., L. Gautheir & G. Morea, 1985. Histopathological and electron microscopy studies of gills of brook trout (Salvelinus fontinalis), from acidified lakes. Can. J. Zool. 63: 2062-2070.

    Google Scholar 

  • Clarke, D. J., B. Burchell & S. G. George, 1992. Differential expression and induction of UDP-glucuronosyltransferase isoforms in hepatic and extrahepatic tissues of a fish, Pleuronectes platessa: Immunochemical and functional characteristics. Toxicol. Appl. Pharmacol. 115(1): 130-136.

    Google Scholar 

  • Clifton-Hadley, R. S., D. Bucke & R. H. Richards, 1984. Proliferative kidney disease of salmonid fish. A review. J. Fish Dis. 7: 363-377.

    Google Scholar 

  • Couch, J. A., 1975. Histopathological effects of pesticides and related chemicals on the liver of fishes. In: Ribelin, W. E. & G. Migaki (eds), The Pathology of Fishes. Madison, University Press of Wisconsin 23: 559-584.

    Google Scholar 

  • Daoust, P. Y., G. Wobeser & J. D. Newstead, 1984. Acute pathological effects of inorganic mercury and copper in gills of rainbow trout. Vet. Patholol. 21: 93-101.

    Google Scholar 

  • Devos, E., P. Devos & M. Cornet, 1998. Effect of cadmium on the cytoskeleton and morphology of gill chloride cells in parr and smolt Atlantic salmon (Salmo salar). Fish Physiol. Biochem. 18: 15-27.

    Google Scholar 

  • Diaz, J. P., L. Mani-Ponset, E. Guyot & R. Connes, 1998. Hepatic choleatasis during the post-embryonic development of fish larvae. J. Exp. Zool. 280: 277-287.

    Google Scholar 

  • Dietze, U., T. Braunbeck, W. Honnen, H.-R. Köhler, J. Schwaiger, H. Segner, R. Triebskorn & G. Schüürmann, 2001. Chemometric discrimination between streams based on chemical, limnological and biological data taken from freshwater fishes and their interrelationships. J. Aquat. Ecosyst. Stress. Recov. 8: 319-336.

    Google Scholar 

  • Drewett, N. & P. D. Abel, 1983. Pathology of lindane poisoning and of hypoxia in the brown trout, (Salmo trutta). J. Fish Biol. 23: 373-384.

    Google Scholar 

  • Evans, D. H., 1987. The fish gill: Site of action and model for toxic effects of environmental pollutants. Environ. Health Perspect. 71: 47-58.

    Google Scholar 

  • Fischer-Scherl, T., A. Veeser, R. W. Hoffman, C. Kühnhauser, R.-D. Negele & T. Euringmann, 1991. Morphological effects of acute and chronic atrazine exposure in rainbow trout (Oncorhynchus mykiss). Arch. Environ. Contamin. Toxicol. 20: 454-461.

    Google Scholar 

  • Ghadially, F. N., 1988. Ultrastructural Pathology of the Cell and Matrix, Vol. I + I. Butterworths, London, 1340 pp.

    Google Scholar 

  • Gluth, G., D. Freitag, W. Hanke & F. Kortes, 1985. Accumulation of pollutant in fish. Comp. Biochem. Physiol. 81C: 273-277.

    Google Scholar 

  • Goss, G. G., P. Laurent & S. F. Perry, 1992. Evidence for a morphological component in acid-base regulation during environmental hypercapnia in the brown bullhead (Ictalurus nebulosus). Cell Tiss. Res. 268: 539-552.

    Google Scholar 

  • Hacking, M. A., J. Budd & K. Hodson, 1978. The ultrastructure of the liver of the rainbow trout: normal structure and modifications after chronic administration of a polychlorinated biphenyl Aroclor 1254. Can. J. Zool. 56: 477-491.

    Google Scholar 

  • Hawkes, J. W., 1980. The effects of xenobiotics on fish tissue: morphological studies. Fed. Proc. 39: 3230-3236.

    Google Scholar 

  • Hentschel, H. & M. Elger, 1992. The vertebrate kidney: A comparative approach. Verh. Dtsch. Zool. Ges. 85(2): 297-314.

    Google Scholar 

  • Hinton, D. E. & D. J. Lauren, 1990a. Liver structural alterations accompanying chronic toxicity in fishes: potential biomarkers of exposure. In: McCarthy, J. F. (ed.), Biomarkers of Environmental Contamination, Vol. 2. Lewis, Boca Raton: 17-57.

    Google Scholar 

  • Hinton, D. E. & D. J. Lauren, 1990b. Integrative histopathological approaches to detecting effects of environmental stressors on fishes. Am. Fish. Soc. Symp. 8: 51-66.

    Google Scholar 

  • Hinton, E. D., P. C. Baumann, G. R. Gardner, W. E. Hawkins, J. D. Hendricks, J. D. Murchelano & M. S. Okihiro, 1992. Histopathological biomarkers. In: Hugget et al. (eds), Biomarkers, Biochemical, Physiological and Histological Markers of Anthropogenic Stress. SETAC Publication, Lewis Publishers, London: 155-189.

    Google Scholar 

  • Hofer, R. & R. Lackner, 1995. Fischtoxikologie. Theorie und Praxis. Gustav Fischer Stuttgart, 164 pp.

    Google Scholar 

  • Hoffmann, R. & H. Dangschat, 1981. A note on the occurrence of proliferative kidney disease in Germany. Bull. Europ. Ass. Fish Pathol. 1: 33.

    Google Scholar 

  • Honnen, W., K. Rath, T. Schlegel, A. Schwinger & D. Frahne, 2001. Chemical analyses of water, sediment and biota in two small streams in southwest Germany. J. Aquat. Ecosyst. Stress. Recov., 8: 195-213.

    Google Scholar 

  • Hugla, J. L. & J. P. Thome, 1999. Effects of polychlorinated biphenyls on liver ultrastructure, hepatic monooxygenases, and reproductive success in the barbel. Ecotoxicol. Environ. Saf. 42: 265-273.

    Google Scholar 

  • Jacobs, D., E. F. Esmond, E. L. Melisky & C. H. Hocutt, 1981. Morphological changes in gill epithelia of heat-stressed rainbow trout, Salmo gairdneri: Evidence in support of a temperatureinduced surface area change hypothesis. Can. J. Fish. Aquat. Sci. 38: 16-22.

    Google Scholar 

  • Jagoe, C. H., V. E. Matey, T. A. Haines & V. T. Komov, 1993. Effect of berryllium on fish in acid water is analogous to aluminium toxicity. Aquat. Toxicol. 24(3-4): 241-256.

    Google Scholar 

  • Kammenga, J. E, R. Dallinger, M. H. Donker, H.-R. Köhler, V. Simonsen, R. Triebskorn & J. M. Weeks, 2000. Biomarkers in terrestrial invertebrates for ecotoxicological soil risk assessment. Rev. Environ. Contam. Toxicol. 164: 93-147.

    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 

  • Karnovsky, M. J., 1971. Use of ferrocyanide-reduced osmium tetroxide in electric microscopy. J. Cell Biol. 51: 284.

    Google Scholar 

  • Kieffer, J. D. & B. L. Tufts, 1996. The influence of environmental temperature on the role of the rainbow trout gill in correcting the acid-base disturbance following exhausting exercise. Physiol. Zool. 69: 1301-1323.

    Google Scholar 

  • Köhler, A. 1990. Identification of contaminant-induced cellular and subcellular lesions in the liver of flounder (Platychthys flesus L.) caught at different polluted estuaries. Aquat. Toxicol. 16: 271-294.

    Google Scholar 

  • Köhler, H.-R., C. Bartussek, H. Eckwert, K. Farian, S. Gränzer, T. Knigge & N. Kunz, 2001. The hepatic 70 stress protein (hsp70) response to interacting abiotic parameters in fish exposed to various levels of pollution. J. Aquat. Ecosyst. Stress Recov. 8: 261-279.

    Google Scholar 

  • Konradt, J. & T. Braunbeck, 2001. Alterations at selected metabolic enzymes in fish following long-term exposure to contaminated streams. J. Aquat. Ecosyst. Stress Recov. 8: 299-318.

    Google Scholar 

  • Laurent, P. & S. F. Perry, 1990. Effects of cortisol on gill chloride cell morphology and ionic uptake in the freshwater trout, Salmo gairdneri. Cell Tissue Res. 259: 429-442.

    Google Scholar 

  • Laurent, P. & S. F. Perry, 1991. Environmental effects on fish gill morphology. Physiol. Zool. 64: 4-25.

    Google Scholar 

  • Laurent, P. & S. F. Perry, 1995. Morphological Basis of acid-base and ionic regulation in fish. In: Advances in Comparative and Environmental Physiology, Vol. 22. Springer-Verlag, Berlin: 91-118.

    Google Scholar 

  • Luckenbach, T., M. Kilian, R. Triebskorn & A. Oberemm, 2001. Fish early life stage tests as a tool to assess embryotoxic potentials in small streams. J. Aquat. Ecosyst. Stress. Recov. 8: 355-370.

    Google Scholar 

  • Mallat, 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 

  • Mathieu, A., P. Lemaire, S. Carriere, P. Drai, J. Giudicelli & M. Lafaurie, 1991. Seasonal and sex-linked variations in hepatic and extrahepatic biotransformation activities in striped mullet (Mullus barbatus). Ecotoxicol. Environ. Saf. 22: 45-57.

    Google Scholar 

  • Mayer-Gostan, N., S. E. Wendelaar Bonga & P. H. M. Balm, 1987. Mechanism of hormone actions on gill transport. In: Pang, P. K. T. & M. P. Schreibmann (eds), Vertebrate Endocrinology: Fundamentals and Biomedical Implications, Vol. 2. Academic press, Orlando: 211-238.

    Google Scholar 

  • Meinelt, T., R. Krüger, M. Pietrock, R. Osten & C. Steinberg, 1997. Mercury pollution and macrophage centres in pike (Esox lucius) tissues. Env. Sci. Poll. Res. 4(1): 32-36.

    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 

  • Mueller, M. E., D. A. Sanchez & H. L. Bergman, 1991. Nature and time course of acclimation to aluminium in juvenile brook trout (Salvelinus fontinalis). II. Gill histology. Can. J. Fish Aquat. Sci. 48: 2016-2027.

    Google Scholar 

  • Olson, K. R. & P. O. Fromm, 1973. A scanning electron microscope study of secondary lamellae and chloride cells of rainbow trout (Salmo gairdneri). Z. Zellforsch. Mikrosk. Anat. 143: 439-449.

    Google Scholar 

  • Pawert, M., E. Müller & R. Triebskorn, 1998. Ultrastructural changes in fish gills as biomarker to assess small stream pollution. Tissue Cell 30: 617-626.

    Google Scholar 

  • Perry, S., 1998. Relationships between branchial chloride cells and gas transfer in freshwater fish. Comp. Biochem. Physiol. 119A: 9-16.

    Google Scholar 

  • Perry, S. F. & P. Laurent, 1993. Environmental effects on fish gill structure and function. In: Rankin, J. C. & F. B. Jensen (eds), Fish Physiology. Chapman & Hall, London: 231-264.

    Google Scholar 

  • Pesonen, M., T. B. Andersson, V. Sorri & M. Korkalainen, 1999. Biochemical and ultrastructural changes in the liver of baltic salmon sac fry suffering from high mortality (M74). Environ. Toxicol. Chem. 18: 1007-1013.

    Google Scholar 

  • Pratap, H. B. & S. E. Wendelaar Bonga, 1993. Effects of ambient and dietry cadmium on pavement cells, chloride cells, and Na+/K+-ATPase activity in the gills of the freshwater teleost Oreochromis mossambicus at normal and high calcium levels in the ambient water. Aquat. Toxicol. 26: 133-155.

    Google Scholar 

  • Pritchard, J. B. & J. R. Bend, 1984. Mechanisms controlling the renal excretion of xenobiotics in fish: effects of chemical structure. Drug Metab. Rev. 15(4): 655-671.

    Google Scholar 

  • Reader, J. P., T. R. K. Dalziel, R. Morris, M. D. J. Sayer & C. H. Dempsey, 1991. Episodic exposure to acid and aluminium in soft water: survival and recovery of brown trout, Salmo trutta L. J. Fish Biol. 39: 181-196.

    Google Scholar 

  • Reynolds, E. S., 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17: 208-212.

    Google Scholar 

  • Rez, G., 1986. Electron microscopic approaches to environmental toxicity. Acta Biol. Hung. 37: 31-45.

    Google Scholar 

  • Rowan, D. J. & J. B. Rasmussen, 1992. Why don't Great Lakes fish reflect environmental concentrations of organic contaminants? An analysis of between-lake variability in the ecological partioning of PCB and DDT. Great Lakes Research, pp. 724-741.

  • Sachs, L., 1984. Angewandte Statistik. Springer Verlag, Berlin/Heidelberg.

    Google Scholar 

  • Schmidt, H., D. Bernet, T. Wahli, W. Meier & P. Burkhardt-Holm, 1999. Active biomonitoring with brown trout and rainbow trout in diluted sewage plant effluents. J. Fish Biol. 54: 585-596.

    Google Scholar 

  • Schmidt, H., H. Posthaus, A. Busato, T. Wahli, W. Meier & P. Burkhardt-Holm, 1998. Transient increase in chloride cell number and heat shock protein expression (hsp 70) in brown trout (Salmo trutta fario) exposed to sudden temperature elevation. Biol. Chem. 379: 1227-1233.

    Google Scholar 

  • Schoor, W. P. & J. A. Couch, 1979. Correlation of mixed-function oxidase activity with ultrastructural changes in the liver of a marine fish. Cancer Biochem. Biophys. 4: 95-103.

    Google Scholar 

  • Schramm, M., E. Müller & R. Triebskorn, 1998. Brown trout (Salmo trutta f. Fario) liver ultrastructure as a biomarker for assessment of small stream pollution. Biomarkers 3: 93-108.

    Google Scholar 

  • Schramm, M., A. Behrens, T. Braunbeck, H. Eckwert, H.-R. Köhler, J. Konradt, E. Müller, M. Pawert, J. Schwaiger, H. Segner & R. Triebskorn, 2000. Cellular, histological and biochemical biomarkers. In: Gerhardt, A. (ed.), Biomonitoring of Polluted Water, Vol. 9. Reviews on actual topics: 33-63.

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

    Google Scholar 

  • Schwaiger, J., 2001. Histopathological alterations and parasite infection in fish: indicators of multiple stress factors. J. Aquat. Ecosyst. Stress. Recov. 8: 231-240.

    Google Scholar 

  • Segner, H. & T. Braunbeck, 1988. Hepatocellular adaptation to extreme nutrional conditions in ide, Leuciscus idus melanotus L. (Cyprinidae). A morphofunctional analysis. Fish Physiol. Biochem. 5: 79-97.

    Google Scholar 

  • Siligato, S. & J. Böhmer, 2001. Using indicators of fish health at mutiple levels of biological organization to assess effects of stream pollution in southwest Germany. J. Aquat. Ecosyst. Stress. Recov. 8: 371-386.

    Google Scholar 

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

    Google Scholar 

  • Smart, G., 1976. The effect of ammonia exposure on gill structure of the rainbow trout (Salmo gairdneri). J. Fish. Biol. 8: 471-475.

    Google Scholar 

  • Soivio, A. & H. Tuurula, 1981. Structural and circulatory responses to hypoxia in the secondary lamellae of Salmo gairdneri gills at two temperatures. J. Comp. Physiol. 145: 37-43.

    Google Scholar 

  • Stebbing, A. R. D., 1985. A possible synthesis. In: Bayne, B. L. (ed.), The Effect of Stress and Pollution on Marine Animals. Praeger, New York.

    Google Scholar 

  • Storch, V., 1988. Cell and environment: A link between morphology and ecology. Biologia ambiental actas del congreso de biologia ambiental 1: 179-191.

    Google Scholar 

  • Streit, B., 1998. Bioaccumulation of contaminants in fish. In: Braunbeck, T., D. E. Hinton & B. Streit (eds), Fish Ecotoxicology. Birkhäuser Verlag, Basel: 353-387.

    Google Scholar 

  • Temmink, J. H. M., P. J. Bouwmeister, P. de Jong & J. H. J. van den Berg, 1983. An ultrastructural study of chromate-induced hyperplasia in the gill of rainbow trout (Salmo gairdneri). Aquat. Toxicol. 4: 165-179.

    Google Scholar 

  • Triebskorn, R., H.-R. Köhler, T. Zahn, G. Vogt, M. Ludwig, S. Rumpf, M. Kratzmann, G. Alberti & V. Storch, 1991. Invertebrate cells as targets for hazardous substances. Z. Angew. Zool. 78: 277-287.

    Google Scholar 

  • Triebskorn, R., H.-R. Köhler, W. Honnen, M. Schramm, S. M. Adams & E. F. Müller, 1997. Induction of heat shock proteins, changes in liver ultrastructure, and alterations of fish behaviour: Are these biomarkers related and are they useful to reflect the state of pollution in the field?. J. Aquat. Ecosyst. Stress Recov. 6: 57-73.

    Google Scholar 

  • Triebskorn, R., J. Böhmer, T. Braunbeck, W. Honnen, H.-R. Köhler, R. Lehmann, A. Oberemm, J. Schwaiger, H. Segner, G. Schüürmann & W. Traunspurger, 2001. The project VALIMAR (VALIdation of bioMARkers for the assessment of small stream pollution): objectives, experimental design, summary of results, and recommendations for the application of biomarkers in risk assessment. J. Aquat. Ecosyst. Stress recov. 8: 161-178.

    Google Scholar 

  • Ultsch, G. R., M. E. Ott & N. Heisler, 1980. Standard metabolic rate, critical oxygen tension and aerobic scope for spontaneous activity of trout (Salmo gairdneri) in acidified water. Comp. Biochem. Physiol. 67A: 329-335.

    Google Scholar 

  • Verreth, J., V. Storch & H. Segner, 1987. A comparative study on the nutritional quality of decapsuled Artemia cysts, microencapsulated egg diets and enriched dry feeds of Clarias gariepinus (Burchell) larvae. Aquaculture 63: 269-282.

    Google Scholar 

  • Walker, R. L., C. M. Wood & H. L. Bergman, 1991. Effects of long-term preexposure to sublethal concentrations of acid and aluminium on the ventilatory response to aluminium challenge in brook trout (Salvelinus fontinalis). Can. J. Fish. Aquat. Sci. 48: 1989-1995.

    Google Scholar 

  • Weinstein, J. E., J. T. Oris & D. H. Taylor, 1997. An ultrastructural examination of the mode of UV-induced toxic action of fluoranthene in the fathead minnow, Pimephales promelas. Aquat. Toxicol. 39: 1-22.

    Google Scholar 

  • Wendelaar Bonga, S. E., G. Flik, P. H. M. Balm & J. C. A. van der Meij, 1990. The ultrastructure of chloride cells in the gills of the teleost Oreochromis mossambicus during exposure to acidified water. Cell Tissue Res. 259: 575-585.

    Google Scholar 

  • Wendelaar Bonga, S. E. & R. A. C. Lock, 1992. Toxicants and osmoregulation in fish. Neth. J. Zool. 42: 478-493.

    Google Scholar 

  • Woodworth, J. G., B. L. Munday & D. Campin, 1998. Evaluation of biomarkers for exposure of fish to eucalypt-based pulp mill effluent and for determination of routes of exposure. Env. Toxicol. Water Qual. 13: 285-296.

    Google Scholar 

  • Wu, W. Z., Zhou, B. S., Xu, Y., Schramm, K.-W. & A. Kettrup, 1999. Cytological and biochemical alterations in Carassius auratus hepatocytes from exposure to sediment containing dioxins and related compounds. Arch. Environ. Contam. Toxicol. 37: 358-363.

    Google Scholar 

  • Zahn, T., Arnold, H., Braunbeck, T., 1996. Cytological and biochemical response of R1 cells and isolated hepatocytes from rainbow trout (Oncorhynchus mykiss) to subacute in vitro exposure to disulfoton. Exp. Toxicol. Pathol. 48: 47-64.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Animal Physiological Ecology, University of Tübingen, Konrad-Adenauer-Str. 20, D-72072, Tübingen, Germany

    Maike Gernhöfer, Michael Pawert, Michael Schramm, Ewald Müller & Rita Triebskorn

  2. Steinbeis-Transfer Center for Ecotoxicology and Ecophysiology Rottenburg, Kreuzlingerstr. 1, D-72108, Rottenburg, Germany

    Rita Triebskorn

Authors
  1. Maike Gernhöfer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Pawert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Schramm
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ewald Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rita Triebskorn
    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

Gernhöfer, M., Pawert, M., Schramm, M. et al. Ultrastructural biomarkers as tools to characterize the health status of fish in contaminated streams. Journal of Aquatic Ecosystem Stress and Recovery 8, 241–260 (2001). https://doi.org/10.1023/A:1012958804442

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1012958804442

Search

Navigation