Skip to main content
Log in

PAH metabolites, GST and EROD in European eel (Anguilla anguilla) as possible indicators for eel habitat quality in German rivers

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The stock of the European eel (Anguilla anguilla L.) continues to decline and has reached a new minimum in 2011. Poor health status of the spawners due to organic contaminants is one of the possible causes for this dramatic situation. Polycyclic aromatic hydrocarbons (PAHs) are ubiquitous contaminants, which are rapidly metabolized in vertebrates. EROD (ethoxyresorufin-O-deethylase) and GST (glutathione-S-transferase) are two enzymes involved in PAH detoxification in fish. In this study, PAH metabolites as well as EROD and GST activity in a large, comprising dataset of more than 260 migratory and pre-migratory eels from five large German river basin districts were used to describe PAH exposure and its metabolism as possible indicators for the habitat quality for eels. Eel from the river Elbe appear to be moderately contaminated with PAH. Highest mean values of PAH metabolites were analysed in fish from the river Rhine. However, the results suggest that contaminants such as PAH are metabolized in the fish and may have contributed to EROD activity in eels caught from the Elbe estuary to 600 km upstream. Since the eel’s onset of cessation of feeding is closely linked to maturation and migration, we propose bile pigments as new indicators contributing to identify the proportion of migratory eel, which is crucial information for eel management plans. We showed that PAH metabolites normalized to bile pigments as well as EROD could be used to describe the habitat quality and might be suitable parameters in search for suitable stocking habitats.

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.

Fig 1
Fig 2
Fig. 3
Fig 4
Fig 5

Similar content being viewed by others

References

  • Agradi E, Baga R, Cillo F, Ceradini S, Heltai D (2000) Environmental contaminants and biochemical response in eel exposed to Po river water. Chemosphere 41(10):1555–1562

    Article  CAS  Google Scholar 

  • Belpaire CGJ, Goemans G, Geeraerts C, Quataert P, Parmentier K, Hagel P, De Boer J (2009) Decreasing eel stocks: survival of the fattest? Ecol freshw fish 18:197–214

    Article  Google Scholar 

  • Beyer J, Egaas E, Hylland K, Waagbo R, Goksoyr A (1997) Time- and dose-dependent biomarker responses in flounder (Platichthys flesus L) exposed to benzo[a]pyrene, 2,3,3’,4,4’,5-hexachlorobiphenyl (PCB-156) and cadmium. Biomarkers 2(1):35–44

    Article  CAS  Google Scholar 

  • BFG (2008): WSV Sedimentmanagement Tideelbe-Strategien und Potenziale-eine Systemstudie. Federal Institute of Hydrology (BFG), Koblenz, Germany, Report BfG-1584, June 2008

  • Bonacci S, Corsi I, Chiea R, Regoli F, Focardi S (2003) Induction of EROD activity in European eel (Anguilla anguilla) experimentally exposed to benzo a pyrene and beta-naphthoflavone. Environ Int 29(4):467–473

    Article  CAS  Google Scholar 

  • Brinkmann M, Hudjetz S, Cofalla C, Roger S, Kammann U, Zhang X, Wiseman S, Giesy J, Hecker M, Schüttrumpf H, Wölz J, Hollert H (2010) A combined hydraulic and toxicological approach to assess re-suspended sediments during simulated flood events. Part I—multiple biomarkers in rainbow trout. J Soils Sediments 10:1347–1361

    Article  CAS  Google Scholar 

  • Brinkmann M, Hudjetz S, Kammann U, Hennig M, Kuckelkorn J, Chinoraks M, Cofalla C, Wiseman S, Giesy JP, Schäffer A, Hecker M, Wölz J, Schüttrumpf H, Hollert H (2013) How flood events affect rainbow trout: evidence of a biomarker cascade in rainbow trout after exposure to PAH contaminated sediment suspensions. Aquat Toxicol 128–129:13–24

    Article  Google Scholar 

  • Buet A, Banas D, Vollaire Y, Coulet E, Roche H (2006) Biomarker responses in European eel (Anguilla anguilla) exposed to persistent organic pollutants. A field study in the Vaccarès lagoon (Camargue, France). Chemosphere 65(10):1846–1858

    Article  CAS  Google Scholar 

  • Clevestam PD, Ogonowski M, Sjöberg NB, Wickström H (2011) Too short to spawn? Implications of small body size and swimming distance on successful migration and maturation of the European eel Anguilla anguilla. J Fish Biol 78:1073–1089

    Article  CAS  Google Scholar 

  • Council Regulation (EC) No 1100/2007 of 18 September 2007 establishing measures for the recovery of the stock of European eel

  • Durif C, Dufour S, Elie P (2005) The silvering process of Anguilla anguilla: a new classification from yellow resident to silver migrating stage. J Fish Biol 66:1025–1043

    Article  Google Scholar 

  • European Commission (2008). Council Regulation (EC) No 199/2008 of 25 February 2008 concerning the establishment of a community framework for the collection, management and use of data in the fisheries sector and support for scientific advice regarding the Common Fisheries Policy, L60, 1–12

  • European Commission (2010). Commission Decision No 2010/93/EU of 18 December 2009 adopting a multiannual community programme for the collection, management and use of data in the fisheries sector for the period 2011–2013, L41/8 –l41/71

  • Federal Environment Agency (2012): Daten zur Umwelt–Umweltzustand in Deutschland. http://www.umweltbundesamt-daten-zur-umwelt.de/umweltdaten/public/document/downloadImage.do?ident=25401 (accessed 23.5.2013)

  • Federal Environment Ministry (2010): Die Wasserrahmenrichtlinie–auf dem Weg zu guten Gewässern. http://www.bmu.de/fileadmin/bmu-import/files/pdfs/allgemein/application/pdf/broschuere_wasserrahmenrichtlinie_bf.pdf (accessed 23.5.3013)

  • Fenet H, Casellas C, Bontoux J (1996) Hepatic enzymatic activities of the European eel Anguilla anguilla as a tool for biomonitoring freshwater streams: laboratory and field caging studies. Water Sci Technol 33(6):321–329

    Article  CAS  Google Scholar 

  • Graynoth E (1999) Improved otolith preparation, ageing and back-calculation techniques for New Zealand freshwater eels. Fish Res 42:137–146

    Article  Google Scholar 

  • Grossbard ML, Boyer JL, Gorden ER (1987) The excretion pattern of biliverdin and bilirubin in bile of the small skate (Raja erinacea). J Comp Physiol B 157:61–66

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139

    CAS  Google Scholar 

  • Hahn ME, Merson RR, Karchner SI (2005) Xenobiotic receptors in fish: structural and functional diversity and evolutional insights. In: Mommsen TP, Moon TW (eds) Biochemistry and molecular biology of fishes. Elsevier, Amsterdam, pp 191–232

    Google Scholar 

  • Heise S, Claus E, Heininger P, Krämer T, Krüger F, Schwartz R, Förstner U (2005): Studie zur Schadstoffbelastung der Sedimente im Elbeeinzugsgebiet-Ursachen und Trends. Hamburg Port Authority Report

  • HELCOM (2012) Helsinki Commission Baltic Marine Environment Protection Commission 33rd Meeting Helsinki, Finland, 6–7 March 2012 HELCOM 33/2012

  • Hewitt S, Fenet H, Casellas C (1998) Induction of EROD activity in European eel (Anguilla anguilla) by different polychlorobiphenyls (PCBs). Water Sci Technol 38(7):245–252

    Article  CAS  Google Scholar 

  • ICES (2009), International Council for the Exploration of the Sea, ICES CM 2009/ACOM: 48, Workshop on Age Reading of European and American Eel (WKAREA)

  • ICES (2011a) International Council for the Exploration of the Sea ICES CM 2011 /ACOM: 18, Report of the 2011 session of the joint EIFAAC/ICES Working Group on eels. Lisbon, Portugal. See http://www.ices.dk/reports/ACOM/2011/WGEEL/wgeel_2011.pdf

  • ICES (2011b), International Council for the Exploration of the Sea, ICES CM 2011/ACOM: 43, Report of the Workshop on Age Reading of European and American Eel (WKAREA2)

  • Jessop BM (2010) Geographic effects on American eel (Anguilla rostrata) life history, characteristics and strategies. Can J Fish Aquat Sci 310:237–244

    Google Scholar 

  • Kammann U (2007) PAH metabolites in bile fluids of dab (Limanda limanda) and flounder (Platichthys flesus)—spatial distribution and seasonal changes. Environ Sci Pollut Res 14:102–108

    Article  CAS  Google Scholar 

  • Kammann U, Askem C, Dabrowska H, Grung M, Kirby MF, Koivisto P, Lucas C, McKenzie M, Meier S, Robinson C, Tairova ZM, Tuvikene A, Vuorinen PJ, Strand J (2013): Interlaboratory proficiency testing for measurement of the PAH metabolite 1-hydroxypyrene in fish bile for marine environmental monitoring, J AOAC Int 96(3):635–641

    Google Scholar 

  • Kammann U, Gercken J (2010) PAK-Metaboliten in Aalmuttern (Zoarces viviparus) aus der Wismar-Bucht. Umweltwiss Schadst Forsch 22:541–546

    Article  CAS  Google Scholar 

  • Kammann U, Lang T, Wosniok W (2012) Biological effects monitoring in marine research. Environ Sci Eur 24:1

    Article  Google Scholar 

  • Keiter S, Grund S, van Bavel B, Hagberg J, Engwall M, Kammann U, Klempt M, Manz W, Olsman H, Braunbeck T, Hollert H (2008) Activities and identification of aryl hydrocarbon receptor agonists in sediments from the Danube river. Anal Bioanal Chem 390:2009–2019

    Article  CAS  Google Scholar 

  • Krahn MM, Myers MS, Burrows DG, Malins DC (1984) Determination of metabolites of xenobiotics in the bile of fish from polluted waterways. Xenobiotica 14:633–646

    Article  CAS  Google Scholar 

  • Leaver MJ, George SG (1998) A piscine glutathione S-transferase which efficiently conjugates the end-products of lipid peroxidation. Mar Environ Res 46(1–5):71–74

    Article  CAS  Google Scholar 

  • Maria VL, Correia AC, Santos MA (2005) Anguilla anguilla L. liver EROD induction and genotoxic responses after retene exposure. Ecotox Environ Safe 61(2):230–238

    Article  CAS  Google Scholar 

  • Marohn L, Jakob E, Hanel R (2013) Implications of facultative catadromy in Anguilla anguilla. Does individual migratory behavior influence eel spawner quality? J Sea Res 77:100–106

    Article  Google Scholar 

  • Marohn L, Rehbein H, Kündiger R, Hanel R (2008) The suitability of cytochrome-P4501A1 as a biomarker for PCB contamination in European eel (Anguilla anguilla). J Biotechnol 136(3–4):135–139

    Article  CAS  Google Scholar 

  • McCormick JH, Podoliak HA (1984) Gallbladder color and relative fullness as a field technique for estimating time since last feeding in brook trout. N Am J Fish Manag 4:566–568

    Article  Google Scholar 

  • Nagel F, Kammann U, Wagner C, Hanel R (2012a) Metabolites of polycyclic aromatic hydrocarbons (PAHs) in bile as biomarkers of pollution in European eel (Anguilla anguilla) from German rivers. Arch Environ Contam Toxicol 62:254–263

    Article  CAS  Google Scholar 

  • Nagel F, Wagner C, Hanel R, Kammann U (2012b) The silvering process in European eel (Anguilla anguilla) influences PAH metabolite concentration in bile fluid—consequences for monitoring. Chemosphere 87(1):91–96

    Article  CAS  Google Scholar 

  • OSPAR (1998) JAMP Guidelines for contaminant-specific biological effects monitoring. Oslo and Paris Commission, London, UK

    Google Scholar 

  • Palstra AP, Ginneken VJT, Murk AJ, Thillart GEEJM (2006) Are dioxin-like contaminants responsible for the eel (Anguilla anguilla) drama? Naturwissenschaften 93:145–148

    Article  CAS  Google Scholar 

  • Palstra AP, van den Thillart GE (2010) Swimming physiology of European silver eels (Anguilla anguilla L.): energetic costs and effects on sexual maturation and reproduction. Fish Physiol Biochem 36(3):297–322

    Article  CAS  Google Scholar 

  • Pankhurst NW (1982) Relation of visual changes to the onset of sexual maturation in the European eel Anguilla anguilla (L.). J Fish Biol 21:127–140

    Article  Google Scholar 

  • Pujolar JM, Milan M, Marino IAM, Capoccioni F, Ciccotti E, Belpaire C, Covaci A, Malarvannan G, Patarnello T, Bargelloni L, Zane L, Maes GE (2013) Detecting genome-wide gene transcription profiles associated with high pollution burden in the critically endangered European eel. Aquat Toxicol 132–133:157–164

    Article  Google Scholar 

  • Richards A (1989): Growth variation of wild and cultured populations of the European eel Anguilla anguilla, L. PhD Thesis, University of Edinburgh, 189 pp

  • Richardson DM, Gubbins MJ, Davis IM, Moffat CF, Pollard PM (2004) Effects of feeding status on biliary PAH metabolite and biliverdin concentrations in plaice (Pleuronectes platessa). Environ Toxicol Phar 17(2):79–85

    Article  CAS  Google Scholar 

  • Ruddock PJ, Bird DJ, McEvoy J, Peters LD (2003) Bile metabolites of polycyclic aromatic hydrocarbons (PAHs) in European eels Anguilla anguilla from United Kingdom estuaries. Sci Total Environ 301:105–117

    Article  CAS  Google Scholar 

  • Schlenk D, Handy R, Steinert S, Depledge MH, Benson W (2008) Biomarkers. In: Di Giulio RT, Hinton DE (eds) The toxicology of fishes. Boca Raton, CRC Taylor & Francis

    Google Scholar 

  • Stachel B, Mariani G, Umlauf G (2011) Götz R (2011): Dioxine und PCBs in Feststoffen aus der Elbe, ihren Nebenflüssen und der Nordsee (Längsprofilaufnahme 2008). FGG Elbe, Report September

    Google Scholar 

  • Sühring R, Möller A, Freese M, Pohlmann J-D, Wolschke H, Sturm R, Xie Z, Hanel R, Ebinghaus R (2013) Brominated flame retardants and dechloranes in eels from German Rivers. Chemosphere 90(1):118–124

    Article  Google Scholar 

  • Tairova ZM, Strand J, Chevalier J, Andersen O (2012) PAH biomarkers in common eelpout (Zoarces viviparus) from Danish waters. Mar Environ Res 5:45–53

    Article  Google Scholar 

  • Teles M, Santos MA, Pacheco M (2004) Responses of European eel (Anguilla anguilla L.) in two polluted environments: in situ experiments. Ecotox Environ Safe 58(3):373–378

    Article  CAS  Google Scholar 

  • Tesch FW (2003) The eel. Blackwell Science, Oxford, UK

    Book  Google Scholar 

  • Todd PR (1980) Size and age of migrating New Zealand freshwater eels (Anguilla spp.). New Zeal J Mar Fresh 14:283–293

    Article  Google Scholar 

  • van den Thillart G, Dufour S, Rankin JC (2008) Spawning migration of the European eel—reproduction index, a useful tool for conservation management in Fish & Fisheries Series 30. Springer, New York

    Google Scholar 

  • van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • van der Oost R, Goksøyr A, Celander M, Heida H, Vermeulen NPE (1996) Biomonitoring of aquatic pollution with feral eel (Anguilla anguilla) II. Biomarkers: pollution-induced biochemical responses. Aquat Toxicol 36(3–4):189–222

    Article  Google Scholar 

  • Whyte JJ, Jung RE, Schmitt CJ, Tillitt DE (2000) Ethoxyresorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit Rev Toxicol 30(4):347–570

    Article  CAS  Google Scholar 

  • Woelz J, Engwall M, Maletz S, Takner HO, 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 15:536–553

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was partly financed by the EU Data Collection Framework (2008/949/EC). The authors wish to thank Alexander Schulz for his skillful assistance in HPLC analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ulrike Kammann.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kammann, U., Brinkmann, M., Freese, M. et al. PAH metabolites, GST and EROD in European eel (Anguilla anguilla) as possible indicators for eel habitat quality in German rivers. Environ Sci Pollut Res 21, 2519–2530 (2014). https://doi.org/10.1007/s11356-013-2121-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-2121-z

Keywords

Navigation