Environmental Science and Pollution Research

, Volume 22, Issue 15, pp 11822–11839 | Cite as

Impact of wastewater on fish health: a case study at the Neckar River (Southern Germany) using biomarkers in caged brown trout as assessment tools

  • Krisztina Vincze
  • Volker Scheil
  • Bertram Kuch
  • Heinz R. Köhler
  • Rita Triebskorn
Research Article


The present work describes a field survey aiming at assessing the impact of a sewage treatment plant (STP) effluent on fish health by means of biomarkers. Indigenous fish were absent downstream of the STP. To elucidate the reason behind this, brown trout (Salmo trutta f. fario) were exposed in floating steel cages up- and downstream of a STP located at the Neckar River near Tübingen (Southern Germany), for 10 and 30 days. A combination of biomarker methods (histopathological investigations, analysis of the stress protein Hsp70, micronucleus test, B-esterase assays) offered the possibility to investigate endocrine, geno-, proteo- and neurotoxic effects in fish organs. Biological results were complemented with chemical analyses on 20 accumulative substances in fish tissue. Even after short-term exposure, biomarkers revealed clear evidence of water contamination at both Neckar River sites; however, physiological responses of caged brown trout were more severe downstream of the STP. According to this, similar bioaccumulation levels (low μg/kg range) of DDE and 12 polycyclic aromatic hydrocarbons (PAHs) were detected at both sampling sites, while up to fourfold higher concentrations of four PAHs, methyl-triclosan and two synthetic musks occurred in the tissues of downstream-exposed fish. The results obtained in this study suggest a constitutive background pollution at both sites investigated at the Neckar River and provided evidence for the additional negative impact of the STP Tübingen on water quality and the health condition of fish.


Histopathology Stress protein Hsp70 Micronucleus test B-esterase Bioaccumulation 



























Dry weight










Heat shock protein








4-nitrophenyl acetate


4-nitrophenyl valerate


Polycyclic aromatic hydrocarbon






Sewage treatment plant



The authors acknowledge the Carl Zeiss Foundation and the Foundation of the Landesnaturschutzverband (LNV) Baden-Württemberg for their financial support. We also thank Simon Schwarz for advice on the statistics, Alexandra Scheil and Bálint Nagy for comments on the manuscript, Stefanie Krais for the introduction to the B-esterase assays, and Andreas Dieterich, Anja Henneberg, Carla Lorenz, Diana Maier, Katharina Peschke and Paul Thellmann for their assistance and help in the field.


  1. Abdel-Moneim AM, Al-Kahtani MA, Elmenshawy OM (2012) Histopathological biomarkers in gills and liver of Oreochromis niloticus from polluted wetland environments, Saudi Arabia. Chemosphere 88(8):1028–1035. doi: 10.1016/j.chemosphere.2012.04.001 CrossRefGoogle Scholar
  2. Abrahamson A, Andersson C, Jönsson ME, Fogelberg O, Örberg J, Brunström B, Brandt I (2007) Gill EROD in monitoring of CYP1A inducers in fish—a study in rainbow trout (Oncorhynchus mykiss) caged in Stockholm and Uppsala waters. Aquat Toxicol 85(1):1–8. doi: 10.1016/j.aquatox.2007.07.013 CrossRefGoogle Scholar
  3. Aguayo S, Muñoz MJ, de la Torre A, Roset J, de la Peña E, Carballo M (2004) Identification of organic compounds and ecotoxicological assessment of sewage treatment plants (STP) effluents. Sci Total Environ 328(1–3):69–81. doi: 10.1016/j.scitotenv.2004.02.013 CrossRefGoogle Scholar
  4. Al-Ghais SM (2013) Acetylcholinesterase, glutathione and hepatosomatic index as potential biomarkers of sewage pollution and depuration in fish. Mar Pollut Bull 74(1):183–186. doi: 10.1016/j.marpolbul.2013.07.005 CrossRefGoogle Scholar
  5. Al-Sabti K, Metcalfe CD (1995) Fish micronuclei for assessing genotoxicity in water. Mutat Res 343:121–135CrossRefGoogle Scholar
  6. Amin AB, Mortensen L, Poppe T (1992) Histology atlas, normal structure of salmonids. Offset Nord AS, NorwayGoogle Scholar
  7. Ayllón F, Suciu R, Gephard S, Juanes F, Garcia-Vazquez E (2000) Conventional armament wastes induce micronuclei in wild brown trout Salmo trutta. Mutat Res Genet Toxicol Environ Mutagen 470(2):169–176. doi: 10.1016/S1383-5718(00)00101-7 CrossRefGoogle Scholar
  8. Bedoux G, Roig B, Thomas O, Dupont V, Le Bot B (2012) Occurrence and toxicity of antimicrobial triclosan and by-products in the environment. Environ Sci Pollut Res Int 19(4):1044–1065. doi: 10.1007/s11356-011-0632-z CrossRefGoogle Scholar
  9. Bernet D, Schmidt H, Wahli T, Burkhardt-Holm P (2001) Effluent from a sewage treatment works causes changes in serum chemistry of brown trout (Salmo trutta L.). Ecotoxicol Environ Saf 48(2):140–147. doi: 10.1006/eesa.2000.2012 CrossRefGoogle Scholar
  10. Boettcher M, Grund S, Keiter S, Kosmehl T, Reifferscheid G, Seitz N, Rocha PS, Hollert H, Braunbeck T (2010) Comparison of in vitro and in situ genotoxicity in the Danube River by means of the comet assay and the micronucleus test. Mutat Res Genet Toxicol Environ Mutagen 700(1–2):11–17. doi: 10.1016/j.mrgentox.2010.04.016 CrossRefGoogle Scholar
  11. Brack W, Schirmer K, Erdinger L, Hollert H (2005) Effect-directed analysis of mutagens and ethoxyresorufin-O-deethylase inducers in aquatic sediments. Environ Toxicol Chem 24(10):2445–2458. doi: 10.1897/05-078r.1 CrossRefGoogle Scholar
  12. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254. doi: 10.1016/0003-2697(76)90527-3 CrossRefGoogle Scholar
  13. Braunbeck T, Brauns A, Keiter S, Hollert H, Schwartz P (2009) Fish populations under stress—the example of the Lower Neckar River (Fischpopulationen unter Stress—das Beispiel des Unteren Neckars). Environ Sci Eur (UWSF) 21(2):197–211. doi: 10.1007/s12302-009-0044-6 Google Scholar
  14. Carballo M, Aguayo S, de la Torre A, Muñoz MJ (2005) Plasma vitellogenin levels and gonadal morphology of wild carp (Cyprinus carpio L.) in a receiving rivers downstream of sewage treatment plants. Sci Total Environ 341(1–3):71–79. doi: 10.1016/j.scitotenv.2004.08.021 CrossRefGoogle Scholar
  15. Carlsson G, Norrgren L (2004) Synthetic musk toxicity to early life stages of zebrafish (Danio rerio). Arch Environ Contam Toxicol 46(1):102–105. doi: 10.1007/s00244-003-2288-2 CrossRefGoogle Scholar
  16. Carney Almroth B, Albertsson E, Sturve J, Förlin L (2008) Oxidative stress, evident in antioxidant defences and damage products, in rainbow trout caged outside a sewage treatment plant. Ecotoxicol Environ Saf 70(3):370–378. doi: 10.1016/j.ecoenv.2008.01.023 CrossRefGoogle Scholar
  17. de la Torre FR, Salibián A, Ferrari L (2007) Assessment of the pollution impact on biomarkers of effect of a freshwater fish. Chemosphere 68(8):1582–1590. doi: 10.1016/j.chemosphere.2007.02.033 CrossRefGoogle Scholar
  18. EBT—Disposal Operating Tübingen (Entsorgungsbetriebe Tübingen) (2005) Service Report 2004 (Anerkennung Dienstleistung 2004). Accessed 8 July 2013
  19. Eckwert H, Alberti G, Kohler H-R (1997) The induction of stress proteins (Hsp) in Oniscus asellus (Isopoda) as a molecular marker of multiple heavy metal exposure: I. Principles and toxicological assessment. Ecotoxicology 6(5):249–262. doi: 10.1023/a:1018682928839 CrossRefGoogle Scholar
  20. Eggen RI, Behra R, Burkhardt-Holm P, Escher BI, Schweigert N (2004) Peer reviewed: challenges in ecotoxicology. Environ Sci Technol 38(3):58A–64ACrossRefGoogle Scholar
  21. Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95. doi: 10.1016/0006-2952(61)90145-9 CrossRefGoogle Scholar
  22. Escher BI, Allinson M, Altenburger R, Bain PA, Balaguer P, Busch W, Crago J, Denslow ND, Dopp E, Hilscherova K, Humpage AR, Kumar A, Grimaldi M, Jayasinghe BS, Jarosova B, Jia A, Makarov S, Maruya KA, Medvedev A, Mehinto AC, Mendez JE, Poulsen A, Prochazka E, Richard J, Schifferli A, Schlenk D, Scholz S, Shiraishi F, Snyder S, Su G, Tang JYM, Burg BVD, Linden SCVD, Werner I, Westerheide SD, Wong CKC, Yang M, Yeung BHY, Zhang X, Leusch FDL (2013) Benchmarking organic micropollutants in wastewater, recycled water and drinking water with in vitro bioassays. Environ Sci Technol 48(3):1940–1956. doi: 10.1021/es403899t CrossRefGoogle Scholar
  23. Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70(1):603CrossRefGoogle Scholar
  24. Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20(1):37–45CrossRefGoogle Scholar
  25. Grizzle JM, Horowitz SA, Strength DR (1988) Caged fish as monitors of pollution: effects of chlorinated effluent from a wastewater treatment plant. J Am Water Resour Assoc 24(5):951–959. doi: 10.1111/j.1752-1688.1988.tb03009.x CrossRefGoogle Scholar
  26. Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 86(11–12):377–384. doi: 10.1016/j.lfs.2009.12.015 CrossRefGoogle Scholar
  27. Haberbosch R, Hoffmann R, Wnuck H (2012) Fish fauna and fishing of the Middle Neckar River (Vom Wildfluss zur Wasserstraße - Fischfauna und Fischerei im Mittleren Neckar), 1st edn. VFG Service und Verlags GmbH, SuttgartGoogle Scholar
  28. Hallare AV, Köhler HR, Triebskorn R (2004) Developmental toxicity and stress protein responses in zebrafish embryos after exposure to diclofenac and its solvent, DMSO. Chemosphere 56(7):659–666. doi: 10.1016/j.chemosphere.2004.04.007 CrossRefGoogle Scholar
  29. Henneberg A, Bender K, Blaha L, Giebner S, Kuch B, Kohler HR, Maier D, Oehlmann J, Richter D, Scheurer M, Schulte-Oehlmann U, Sieratowicz A, Ziebart S, Triebskorn R (2014) Are in vitro methods for the detection of endocrine potentials in the aquatic environment predictive for in vivo effects? Outcomes of the projects SchussenAktiv and SchussenAktivplus in the Lake Constance Area, Germany. PLoS ONE 9(6):e98307. doi: 10.1371/journal.pone.0098307 CrossRefGoogle Scholar
  30. Hofmann GE (1999) Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. Am Zool 39:889–900Google Scholar
  31. Kerambrun E, Sanchez W, Henry F, Amara R (2011) Are biochemical biomarker responses related to physiological performance of juvenile sea bass (Dicentrarchus labrax) and turbot (Scophthalmus maximus) caged in a polluted harbour? Comp Biochem Physiol C: Toxicol Pharmacol 154(3):187–195. doi: 10.1016/j.cbpc.2011.05.006 Google Scholar
  32. Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999–2000: a national reconnaissance. Environ Sci Technol 36(6):1202–1211. doi: 10.1021/es011055j CrossRefGoogle Scholar
  33. Köhler H-R, Eckwert H, Triebskorn R, Bengtsson G (1999) Interaction between tolerance and 70kDa stress protein (hsp70) induction in collembolan populations exposed to long-term metal pollution. Appl Soil Ecol 11(1):43–52. doi: 10.1016/S0929-1393(98)00127-9 CrossRefGoogle Scholar
  34. Köhler HR, Sandu C, Scheil V, Nagy-Petrica EM, Segner H, Telcean I, Stan G, Triebskorn R (2007) Monitoring pollution in river Mures, Romania, Part III: biochemical effect markers in fish and integrative reflection. Environ Monit Assess 127(1–3):47–54. doi: 10.1007/s10661-006-9257-y CrossRefGoogle Scholar
  35. Laguerre C, Sanchez-Hernandez JC, Köhler HR, Triebskorn R, Capowiez Y, Rault M, Mazzia C (2009) B-type esterases in the snail Xeropicta derbentina: an enzymological analysis to evaluate their use as biomarkers of pesticide exposure. Environ Pollut 157(1):199–207. doi: 10.1016/j.envpol.2008.07.003 CrossRefGoogle Scholar
  36. Lange C, Kuch B, Metzger JW (2015) Occurrence and fate of synthetic musk fragrances in a small German river. J Hazard Mater 282C:34–40. doi: 10.1016/j.jhazmat.2014.06.027 CrossRefGoogle Scholar
  37. Leino RL, Jensen KM, Ankley GT (2005) Gonadal histology and characteristic histopathology associated with endocrine disruption in the adult fathead minnow (Pimephales promelas). Environ Toxicol Pharmacol 19(1):85–98. doi: 10.1016/j.etap.2004.05.010 CrossRefGoogle Scholar
  38. Leticia A-G, Gerardo G-B (2008) Determination of esterase activity and characterization of cholinesterases in the reef fish Haemulon plumieri. Ecotoxicol Environ Saf 71(3):787–797. doi: 10.1016/j.ecoenv.2008.01.024 CrossRefGoogle Scholar
  39. Liang X, Nie X, Ying G, An T, Li K (2013) Assessment of toxic effects of triclosan on the swordtail fish (Xiphophorus helleri) by a multi-biomarker approach. Chemosphere 90(3):1281–1288. doi: 10.1016/j.chemosphere.2012.09.087 CrossRefGoogle Scholar
  40. Lindström-Seppä P, Oikari A (1990) Biotransformation and other toxicological and physiological responses in rainbow trout (Salmo gairdneri Richardson) caged in a lake receiving effluents of pulp and paper industry. Aquat Toxicol 16(3):187–204. doi: 10.1016/0166-445X(90)90037-P CrossRefGoogle Scholar
  41. Lindström A, Buerge IJ, Poiger T, Bergqvist P-A, Müller MD, Buser H-R (2002) Occurrence and environmental behavior of the bactericide triclosan and its methyl derivative in surface waters and in wastewater. Environ Sci Technol 36(11):2322–2329. doi: 10.1021/es0114254 CrossRefGoogle Scholar
  42. Liu Y, Beckingham B, Ruegner H, Li Z, Ma L, Schwientek M, Xie H, Zhao J, Grathwohl P (2013) Comparison of sedimentary PAHs in the rivers of Ammer (Germany) and Liangtan (China): differences between early- and newly-industrialized countries. Environ Sci Technol 47(2):701–709. doi: 10.1021/es3031566 CrossRefGoogle Scholar
  43. Livingstone DR (1998) The fate of organic xenobiotics in aquatic ecosystems: quantitative and qualitative differences in biotransformation by invertebrates and fish. Comp Biochem Physiol A Mol Integr Physiol 120(1):43–49. doi: 10.1016/s1095-6433(98)10008-9 CrossRefGoogle Scholar
  44. Logan DT (2007) Perspective on ecotoxicology of PAHs to fish. Hum Ecol Risk Assess Int J 13(2):302–316. doi: 10.1080/10807030701226749 CrossRefGoogle Scholar
  45. Maier D, Blaha L, Giesy JP, Henneberg A, Köhler H-R, Kuch B, Osterauer R, Peschke K, Richter D, Scheurer M, Triebskorn R (2014) Biological plausibility as a tool to associate analytical data for micropollutants and effect potentials in wastewater, surface water, and sediments with effects in fishes. Water Res. doi: 10.1016/j.watres.2014.08.050
  46. Markwell MAK, Haas SM, Bieber LL, Tolbert NE (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87(1):206–210. doi: 10.1016/0003-2697(78)90586-9 CrossRefGoogle Scholar
  47. Matozzo V, Formenti A, Donadello G, Marin MG (2012) A multi-biomarker approach to assess effects of triclosan in the clam Ruditapes philippinarum. Mar Environ Res 74:40–46. doi: 10.1016/j.marenvres.2011.12.002 CrossRefGoogle Scholar
  48. Moore MN, Depledge MH, Readman JW, Paul Leonard DR (2004) An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res Fundam Mol Mech Mutagen 552(1–2):247–268. doi: 10.1016/j.mrfmmm.2004.06.028 CrossRefGoogle Scholar
  49. Nicolas J-M (1999) Vitellogenesis in fish and the effects of polycyclic aromatic hydrocarbon contaminants. Aquat Toxicol 45(2–3):77–90. doi: 10.1016/S0166-445X(98)00095-2 CrossRefGoogle Scholar
  50. Oikari A (2006) Caging techniques for field exposures of fish to chemical contaminants. Aquat Toxicol 78(4):370–381Google Scholar
  51. Oikari A, Holmbom B, Ånäs E, Miilunpalo M, Kruzynski G, Castrén M (1985) Ecotoxicological aspects of pulp and paper mill effluents discharged to an inland water system: distribution in water, and toxicant residues and physiological effects in caged fish (Salmo gairdneri). Aquat Toxicol 6(3):219–239. doi: 10.1016/0166-445X(85)90006-2 CrossRefGoogle Scholar
  52. Oliveira M, Gravato C, Guilhermino L (2012) Acute toxic effects of pyrene on Pomatoschistus microps (Teleostei, Gobiidae): mortality, biomarkers and swimming performance. Ecol Indic 19:206–214. doi: 10.1016/j.ecolind.2011.08.006 CrossRefGoogle Scholar
  53. Osterauer R, Köhler H-R (2008) Temperature-dependent effects of the pesticides thiacloprid and diazinon on the embryonic development of zebrafish (Danio rerio). Aquat Toxicol 86(4):485–494. doi: 10.1016/j.aquatox.2007.12.013 CrossRefGoogle Scholar
  54. Palanikumar L, Kumaraguru AK, Ramakritinan CM, Anand M (2012) Biochemical response of anthracene and benzo [a] pyrene in milkfish Chanos chanos. Ecotoxicol Environ Saf 75:187–197. doi: 10.1016/j.ecoenv.2011.08.028 CrossRefGoogle Scholar
  55. Pawert M, Muller E, Triebskorn R (1998) Ultrastructural changes in fish gills as biomarker to assess small stream pollution. Tissue Cell 30(6):617–626CrossRefGoogle Scholar
  56. Peakall DB (1994) The role of biomarkers in environmental assessment (1). Introduction. Ecotoxicol Environ Saf 3:157–160CrossRefGoogle Scholar
  57. Rault M, Collange B, Mazzia C, Capowiez Y (2008) Dynamics of acetylcholinesterase activity recovery in two earthworm species following exposure to ethyl-parathion. Soil Biol Biochem 40(12):3086–3091. doi: 10.1016/j.soilbio.2008.09.010 CrossRefGoogle Scholar
  58. Reynaud S, Deschaux P (2006) The effects of polycyclic aromatic hydrocarbons on the immune system of fish: a review. Aquat Toxicol 77(2):229–238. doi: 10.1016/j.aquatox.2005.10.018 CrossRefGoogle Scholar
  59. Rickwood CJ, Galloway TS (2004) Acetylcholinesterase inhibition as a biomarker of adverse effect. A study of Mytilus edulis exposed to the priority pollutant chlorfenvinphos. Aquat Toxicol 67(1):45–56. doi: 10.1016/j.aquatox.2003.11.004 CrossRefGoogle Scholar
  60. Rocha PS, Luvizotto GL, Kosmehl T, Bottcher M, Storch V, Braunbeck T, Hollert H (2009) Sediment genotoxicity in the Tiete River (Sao Paulo, Brazil): in vitro comet assay versus in situ micronucleus assay studies. Ecotoxicol Environ Saf 72(7):1842–1848. doi: 10.1016/j.ecoenv.2009.04.013 CrossRefGoogle Scholar
  61. Rodriguez-Cea A, Ayllon F, Garcia-Vazquez E (2003) Micronucleus test in freshwater fish species: an evaluation of its sensitivity for application in field surveys. Ecotoxicol Environ Saf 56(3):442–448. doi: 10.1016/S0147-6513(03)00073-3 CrossRefGoogle Scholar
  62. Rodrı́guez-Fuentes G, Gold-Bouchot G (2000) Environmental monitoring using acetylcholinesterase inhibition in vitro. A case study in two Mexican lagoons. Mar Environ Res 50(1–5):357–360. doi: 10.1016/S0141-1136(00)00062-3 CrossRefGoogle Scholar
  63. Sanchez-Hernandez JC, Mazzia C, Capowiez Y, Rault M (2009) Carboxylesterase activity in earthworm gut contents: potential (eco)toxicological implications. Comp Biochem Physiol C: Toxicol Pharmacol 150(4):503–511. doi: 10.1016/j.cbpc.2009.07.009 Google Scholar
  64. Satoh T, Hosokawa M (1998) The mammalian carboxylesterases: from molecules to functions. Annu Rev Pharmacol Toxicol 38:257–288. doi: 10.1146/annurev.pharmtox.38.1.257 CrossRefGoogle Scholar
  65. Scheil V, Zürn A, Köhler H-R, Triebskorn R (2010) Embryo development, stress protein (Hsp70) responses, and histopathology in zebrafish (Danio rerio) following exposure to nickel chloride, chlorpyrifos, and binary mixtures of them. Environ Toxicol 25(1):83–93. doi: 10.1002/tox.20477 Google Scholar
  66. Schnell S, Martin-Skilton R, Fernandes D, Porte C (2009) The interference of nitro- and polycyclic musks with endogenous and xenobiotic metabolizing enzymes in carp: an in vitro study. Environ Sci Technol 43(24):9458–9464. doi: 10.1021/es902128x CrossRefGoogle Scholar
  67. Schwaiger J, Ferling H, Mallow U, Wintermayr H, Negele RD (2004) Toxic effects of the non-steroidal anti-inflammatory drug diclofenac. Part I: histopathological alterations and bioaccumulation in rainbow trout. Aquat Toxicol 68(2):141–150. doi: 10.1016/j.aquatox.2004.03.014 CrossRefGoogle Scholar
  68. Schwaiger J, Wanke R, Adam S, Pawert M, Honnen W, Triebskorn R (1997) The use of histopathological indicators to evaluate contaminant-related stress in fish. J Aquat Ecosyst Stress Recover 6(1):75–86. doi: 10.1023/a:1008212000208 CrossRefGoogle Scholar
  69. Silva AG, Martinez CBR (2007) Morphological changes in the kidney of a fish living in an urban stream. Environ Toxicol Pharmacol 23(2):185–192. doi: 10.1016/j.etap.2006.08.009 CrossRefGoogle Scholar
  70. Simmons DB, Marlatt VL, Trudeau VL, Sherry JP, Metcalfe CD (2010) Interaction of Galaxolide(R) with the human and trout estrogen receptor-alpha. Sci Total Environ 408(24):6158–6164. doi: 10.1016/j.scitotenv.2010.09.027 CrossRefGoogle Scholar
  71. Tetreault GR, Bennett CJ, Cheng C, Servos MR, McMaster ME (2012) Reproductive and histopathological effects in wild fish inhabiting an effluent-dominated stream, Wascana Creek, SK, Canada. Aquat Toxicol 110–111:149–161. doi: 10.1016/j.aquatox.2012.01.004 CrossRefGoogle Scholar
  72. Thophon S, Kruatrachue M, Upatham ES, Pokethitiyook P, Sahaphong S, Jaritkhuan S (2003) Histopathological alterations of white seabass, Lates calcarifer, in acute and subchronic cadmium exposure. Environ Pollut 121(3):307–320. doi: 10.1016/S0269-7491(02)00270-1 CrossRefGoogle Scholar
  73. Triebskorn R, Adam S, Casper H, Honnen W, Pawert M, Schramm M, Schwaiger J, Köhler H-R (2002) Biomarkers as diagnostic tools for evaluating effects of unknown past water quality conditions on stream organisms. Ecotoxicology 11:451–465CrossRefGoogle Scholar
  74. Triebskorn R, Casper H, Scheil V, Schwaiger J (2007) Ultrastructural effects of pharmaceuticals (carbamazepine, clofibric acid, metoprolol, diclofenac) in rainbow trout (Oncorhynchus mykiss) and common carp (Cyprinus carpio). Anal Bioanal Chem 387(4):1405–1416. doi: 10.1007/s00216-006-1033-x CrossRefGoogle Scholar
  75. Triebskorn R, Telcean I, Casper H, Farkas A, Sandu C, Stan G, Colarescu O, Dori T, Kohler HR (2008) Monitoring pollution in River Mures, Romania, part II: metal accumulation and histopathology in fish. Environ Monit Assess 141(1–3):177–188. doi: 10.1007/s10661-007-9886-9 CrossRefGoogle Scholar
  76. Vethaak AD, Jol JG, Meijboom A, Eggens ML, Rheinallt T, Wester PW, van de Zande T, Bergman A, Dankers N, Ariese F, Baan RA, Everts JM, Opperhuizen A, Marquenie JM (1996) Skin and liver diseases induced in flounder (Platichthys flesus) after long-term exposure to contaminated sediments in large-scale mesocosms. Environ Health Perspect 104(11):1218–1229CrossRefGoogle Scholar
  77. Vincze K, Graf K, Scheil V, Köhler H-R, Triebskorn R (2014) Embryotoxic and proteotoxic effects of water and sediment from the Neckar River (Southern Germany) to zebrafish (Danio rerio) embryos. Environ Sci Eur 26(3):1–13Google Scholar
  78. Walker CH (1995) Biochemical biomarkers in ecotoxicology—some recent developments. Sci Total Environ 171(1–3):189–195. doi: 10.1016/0048-9697(95)04720-6 CrossRefGoogle Scholar
  79. Wester PW, van der Ven LTM, Vethaak AD, Grinwis GCM, Vos JG (2002) Aquatic toxicology: opportunities for enhancement through histopathology. Environ Toxicol Pharmacol 11(3–4):289–295. doi: 10.1016/S1382-6689(02)00021-2 CrossRefGoogle Scholar
  80. Wheelock C, Phillips B, Anderson B, Miller J, Miller M, Hammock B (2008) Applications of carboxylesterase activity in environmental monitoring and toxicity identification evaluations (TIEs). In: Whitacre D (ed) Reviews of Environmental Contamination and Toxicology, vol 195. Springer, New York, pp 117–178. doi: 10.1007/978-0-387-77030-7_5 CrossRefGoogle Scholar
  81. Wogram J, Sturm A, Segner H, Liess M (2001) Effects of parathion on acetylcholinesterase, butyrylcholinesterase, and carboxylesterase in three-spined stickleback (Gasterosteus aculeatus) following short-term exposure. Environ Toxicol Chem 20(7):1528–1531CrossRefGoogle Scholar
  82. Wolz J, Engwall M, Maletz S, Olsman Takner H, van Bavel B, Kammann U, Klempt M, Weber R, Braunbeck T, Hollert H (2008) Changes in toxicity and Ah receptor agonist activity of suspended particulate matter during flood events at the rivers Neckar and Rhine—a mass balance approach using in vitro methods and chemical analysis. Environ Sci Pollut Res Int 15(7):536–553. doi: 10.1007/s11356-008-0056-6 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Krisztina Vincze
    • 1
  • Volker Scheil
    • 1
  • Bertram Kuch
    • 2
  • Heinz R. Köhler
    • 1
  • Rita Triebskorn
    • 1
    • 3
  1. 1.Animal Physiological EcologyUniversity of TübingenTübingenGermany
  2. 2.Institute for Sanitary Engineering, Water Quality and Solid Waste ManagementUniversity of StuttgartStuttgartGermany
  3. 3.Steinbeis-Transfer Center for Ecotoxicology and EcophysiologyRottenburgGermany

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