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Persistent organic pollutants in Baltic herring (Clupea harengus)—an aspect of gender

  • Sophia Schubert
  • Nadia Keddig
  • Wolfgang Gerwinski
  • Jan Neukirchen
  • Ulrike Kammann
  • Michael Haarich
  • Reinhold Hanel
  • Norbert Theobald
Article

Abstract

Persistent organic pollutants (POPs) are monitored regularly in water, sediment, and biota in the Baltic Sea. Lipophilic substances are measured in remarkable concentrations especially in the fatty parts of fish, such as herring (Clupea harengus). However, less lipophilic POPs, e.g. perfluorinated compounds (PFCs), can also be detected. For the first time to our knowledge, this study provides a broad range of contaminant concentrations simultaneously measured in filet, liver, and gonads of both sexes of Baltic herring. We analysed organochlorines, polybrominated diphenyl ethers (PBDEs), and PFCs in mature autumn-spawning individuals and found distinct organ pollutant pattern for all POPs in both sexes. POP concentrations found in the gonads of both sexes indicate that not only females but also males tend to reduce contaminants via reproduction. However, sex-dependent differences could be identified for hexachlorobenzene, PBDEs, and were most remarkable for PFCs. This transfer of contaminants to the gonads in both male and female herring is being underestimated, as it may directly affect the general reproduction success as well as the healthy development of the next generation. Hence, the accumulation of contaminants in the gonads should be considered one possible threat to a healthy wildlife as its achievement is stated by the Baltic Sea Action Plan. Inclusion of a periodic monitoring of POP concentrations in gonads of fish may be an important bioeffect measure to assess the environmental status of biota in the Baltic Sea.

Keywords

Baltic Sea Perfluorinated compounds Organochlorines Polybrominated diphenyl ethers Tissue distribution 

Notes

Acknowledgments

The authors thank Elke Hammermeister, Dagmar Korte, and Helga Wolter for their skilful technical assistance as well as Werner Wosniok for his thematic support. This study was incorporated into the research project ‘MERIT-MSFD: Methods for detection and assessment of risks for the marine ecosystem due to toxic contaminants in relation to the implementation of the European Marine Strategy Framework Directive’. It was supported by a grant (grant number 10017012) from the German Federal Ministry of Transport and Digital Infrastructure and the German Maritime and Hydrographic Agency.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Ahrens, L., Vorkamp, K., Lepom, P., Bersuder, P., Theobald, N., Ebinghaus, R., et al. (2010). Dermination of perfluoroalkyl compounds in water, sediment, and biota. ICES Techniques in Marine Environmental Sciences, 48, 16.Google Scholar
  2. Airaksinen, R., Hallikainen, A., Rantakokko, P., Ruokojärvi, P., Vuorinen, P. J., Parmanne, R., et al. (2014). Time trends and congener profiles of PCDD/Fs, PCBs, and PBDEs in Baltic herring off the coast of Finland during 1978-2009. Chemosphere, 114, 165–171.CrossRefGoogle Scholar
  3. Berger, U., Glynn, A., Holmström, K. E., Berglund, M., Ankarberg, E. H., & Törnkvist, A. (2009). Fish consumption as a source of human exposure to perfluorinated alkyl substances in Sweden - analysis of edible fish from Lake Vättern and the Baltic Sea. Chemosphere, 76, 799–804.CrossRefGoogle Scholar
  4. Bignert, A., Olsson, M., Persson, W., Jensen, S., Zakrisson, S., Litzén, K., et al. (1998). Temporal trends of organochlorines in northern Europe, 1967-1995. Relation to global fractionation, leakage from sediments and international measures. Environmental Pollution, 99, 177–198.CrossRefGoogle Scholar
  5. Bignert, A., Nyberg, E., Asplund, L., Eriksson, U. (2010) Comments concerning the national Swedish contaminant monitoring programme in marine biota, 2010. Natural History 157.Google Scholar
  6. Bucholtz, R. H., Tomkiewicz, J., & Dalskov, J. (2008). Manual to determine gonadal maturity of herring (Clupea harengus L.). DTU Aqua-report 197–08. Charlottenlund: National Institute of Aquatic Resources.Google Scholar
  7. Burreau, S., Broman, D., & Örn, U. (2000). Tissue distribution of 2,2′,4,4′-tetrabromo[14C]diphenyl ether ([14C]-PBDE 47) in pike (Esox lucius) after dietary exposure—a time series study using whole body autoradiography. Chemosphere, 40, 977–985.CrossRefGoogle Scholar
  8. Casini, M., Kornilovs, G., Cardinale, M., Möllmann, C., Grygiel, W., Jonsson, P., et al. (2011). Spatial and temporal density dependence regulates the condition of Central Baltic Sea clupeids: compelling evidence using an extensive international acoustic survey. Population Ecology, 53, 511–523.CrossRefGoogle Scholar
  9. Dabrowska, H., Bernard, E., Barska, I., & Radtke, K. (2009). Inter-tissue distribution and evaluation of potential toxicity of PCBs in Baltic cod (Gadus morhua L.). Ecotoxicology and Environmental Safety, 72, 1975–1984.CrossRefGoogle Scholar
  10. Elskus, A. A., Collier, T. K., & Monosson, E. (2005). Interaction between lipids and persistant organic pollutant in fish. In T. P. Mommsen & T. W. Moon (Eds.), Biochemistry and molecular biology of fishes, vol. 6 (pp. 119–152). Amsterdam: Elsevier.Google Scholar
  11. EU (2013). Directive 2013/39/EU of the European Parliament and of the council of 12 August 2013 amending directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy. European Parliament and Council of the European Union. Official Journal of the European Union, 226, 1–17.Google Scholar
  12. Ewald, G., & Larsson, P. (1994). Partitioning of 14C-labelled 2,2′,4,4′-tetrachlorobiphenyl between water and fish lipids. Environmental Toxicology and Chemistry, 13, 15771580.CrossRefGoogle Scholar
  13. Fent, K. (2013). Ökotoxikologie (4th ed.). Stuttgart: Georg Thieme Verlag KG.Google Scholar
  14. Galassi, S., Bettinetti, R., Neri, M. C., Jeannot, R., Dagnac, T., Bristeau, S., et al. (2008). A multispecies approach for monitoring persistent toxic substances in the Gulf of Gdansk (Baltic Sea). Ecotoxicology and Environmental Safety, 69, 39–48.CrossRefGoogle Scholar
  15. Gerst, M., Ferling, H., Römer, C., Schwaiger, J. (2008) PFT-Wirkungen auf die Aquatische Umwelt. In: Münchner Beiträge zur Abwasser-, Fischerei- und Flussbiologie. Band 59: Persistente Perfluorverbindungen - eine Gefahr für Mensch und Umwelt. München: Bayrisches Landesamt für Umwelt.Google Scholar
  16. Hansen, P., Westernhagen, H. V., & Rosenthal, H. (1985). Chlorinated hydrocarbons and hatching success in Baltic herring spring Spawners. Marine Environmental Research, 15, 59–76.CrossRefGoogle Scholar
  17. He, J., Yang, D., Wang, C., Liu, W., Liao, J., Xu, T., et al. (2011). Chronic zebrafish low dose decabrominated diphenyl ether (BDE-209) exposure affected parental gonad development and locomotion in F1 offspring. Ecotoxicology, 20, 1813–1822.CrossRefGoogle Scholar
  18. HELCOM (2007a). HELCOM red list of threatened and declining species of lampreys and fishes of the Baltic Sea. Baltic Sea Environment Proceedings, 109, 42.Google Scholar
  19. HELCOM (2007b). Baltic Sea action plan. Krakow, Poland: HELCOM.Google Scholar
  20. HELCOM (2010). Hazardous substances in the Baltic Sea. An integrated thematic assessment of hazardous substances in the Baltic Sea. Sea Environment Proceedings, 120 B, 119.Google Scholar
  21. HELCOM. (2015) Manual for Marine Monitoring in the COMBINE Program of HELCOM. COMBINE Manual 416.Google Scholar
  22. Henderson, R., & Almatar, S. (1989). Seasonal changes in the lipid composition of herring (Clupea harengus) in relation to gonad maturation. Journal of the Marine Biological Association of the UK, 69, 323–334.CrossRefGoogle Scholar
  23. Isosaari, P., Hallikainen, A., Kiviranta, H., Vuorinen, P. J., Parmanne, R., Koistinen, J., et al. (2006). Polychlorinated dibenzo-p-dioxins, dibenzofurans, bi-phenyls, naphthalenes and polybrominated diphenyl ethers in the edible fish caught from the Baltic Sea and lakes in Finland. Environmental Pollution, 141, 213–225.CrossRefGoogle Scholar
  24. Kammann, U., Landgraff, O., & Steinhart, H. (1993). Distribution of aromatic organochlorines in livers and reproductive organs of male and female dabs from the German bight. Marine Pollution Bulletin, 26, 629–635.CrossRefGoogle Scholar
  25. Karl, H., & Ruoff, U. (2007). Dioxins, dioxin-like PCBs and chloroorganic contaminants in herring, Clupea harengus, from different fishing grounds of the Baltic Sea. Chemosphere, 67, 90–95.CrossRefGoogle Scholar
  26. Karl, H., Bladt, A., Rottler, H., Ludwigs, R., & Mathar, W. (2010). Temporal trends of PCDD, PCDF and PCB levels in muscle meat of herring from different fishing grounds of the Baltic Sea and actual data of different fish species from the western Baltic Sea. Chemosphere, 78, 106–112.CrossRefGoogle Scholar
  27. Kime, D. E. (1995). The effects of reproduction in fish. Reviews in Fish Biology and Fisheries, 5, 52–96.CrossRefGoogle Scholar
  28. Kiviranta, H., Vartiainen, T., Parmanne, R., Hallikainen, A., & Koistinen, J. (2003). PCDD/fs and PCBs in Baltic herring during the 1990s. Chemosphere, 50, 1201–1216.CrossRefGoogle Scholar
  29. Klinkhardt, M. (1996). Der Hering: Clupea harengus. Magdeburg: Spektrum Akad. Verlag.Google Scholar
  30. Knickmeyer, R., & Steinhart, H. (1989). On the distribution of polychlorinated biphenyl congeners and hexachlorobenzene in different tissues of DAB (Limanda limanda) from the North Sea. Chemosphere, 19, 1309–1320.CrossRefGoogle Scholar
  31. Koistinen, J., Kiviranta, H., Ruokojärvi, P., Parmanne, R., Verta, M., Hallikainen, A., et al. (2008). Organohalogen pollutants in herring from the northern Baltic Sea: concentrations, congener profiles and explanatory factors. Environmental Pollution, 154, 172–183.CrossRefGoogle Scholar
  32. Koponen, J., Airaksinen, R., Hallikainen, A., Vuorinen, P.J., Mannio, J. (2014) Perfluoroalkyl acids in various edible Baltic, freshwater, and farmed fish in Finland. Chemosphere.Google Scholar
  33. Lana, N. B., Berton, P., Covaci, A., Ciocco, N. F., Barrera-Oro, E., Atencio, A., et al. (2014). Fingerprint of persistent organic pollutants in tissues of Antarctic notothenioid fish. Science of the Total Environment, 499, 89–98.CrossRefGoogle Scholar
  34. Larsson, P., Okla, L., & Collvin, L. (1993). Reproductive status and lipid content as factors in PCB, DDT and HCH contamination of a population of pike (Esox lucius L.). Environmental Toxicology and Chemistry, 12, 855–861.Google Scholar
  35. Lubzens, E., Young, G., Bobe, J., & Cerdà, J. (2010). Oogenesis in teleosts: how eggs are formed. General and Comparative Endocrinology, 165, 367–389.CrossRefGoogle Scholar
  36. Mackay, D., & Fraser, A. (2000). Bioaccumulation of persistent organic chemicals: mechanisms and models. Environmental Pollution, 110, 375–391.CrossRefGoogle Scholar
  37. Nyholm, J. R., Norman, A., Norrgren, L., Haglund, P., & Andersson, P. L. (2008). Maternal transfer of brominated flame retardants in zebrafish (Danio rerio). Chemosphere, 73, 203–208.CrossRefGoogle Scholar
  38. OSPAR. (1997) Agreed ecotoxicological assessment criteria for trace metals, PCBs, PAHs, TBT and some organochlorine pesticides. In: Joint Meeting of the Oslo and Paris Commissions. Brussel, p 2Google Scholar
  39. OSPAR. (2005) Assessment of data collected under the Co-ordinated Environmental Monitoring Programme (CEMP), 1–250.Google Scholar
  40. OSPAR. (2009) Background Document on CEMP Assessment Criteria for QSR 2010. Monitoring and Assessment Ser 24.Google Scholar
  41. OSPAR (2012). JAMP guidelines for monitoring contaminants in biota. Monitoring Guidelines, 1999-02 re, 1–122.Google Scholar
  42. OSPAR Commission. (2010) Agreement on CEMP assessment criteria for the QSR 2010. Monitoring and Assessment Google Scholar
  43. Papoulias, D. M., Tillitt, D. E., Talykina, M. G., Whyte, J. J., & Richter, C. a. (2014). Atrazine reduces reproduction in Japanese medaka (Oryzias latipes). Aquatic Toxicology, 154, 230–239.CrossRefGoogle Scholar
  44. Parmanne, R., Hallikainen, A., Isosaari, P., Kiviranta, H., Koistinen, J., Laine, O., et al. (2006). The dependence of organohalogen compound concentrations on herring age and size in the Bothnian Sea, northern Baltic. Marine Pollution Bulletin, 52, 149–161.CrossRefGoogle Scholar
  45. Peltonen, H. (2002). Age determination of Baltic herring from whole otoliths and from neutral red stained otolith cross sections. ICES Journal of Marine Science, 59, 323–332.CrossRefGoogle Scholar
  46. Peng, H., Wei, Q., Wan, Y., Giesy, J. P., Li, L., & Hu, J. (2010). Tissue distribution and maternal transfer of poly- and perfluorinated compounds in Chinese sturgeon (Acipenser sinensis): implications for reproductive risk. Environmental Science & Technology, 44, 1868–1874.CrossRefGoogle Scholar
  47. Pikkarainen, A.-L., & Parmanne, R. (2006). Polichlorinated biphenyls and organochlorine pesticides in Baltic herring 1985–2002. Marine Pollution Bulletin, 52, 1304–1309.CrossRefGoogle Scholar
  48. R Core Team. (2014) R: A language and environment for statistical computing.Google Scholar
  49. Reindl, A. R., Falkowska, L., Szumiło, E., & Staniszewska, M. (2013). Residue of chlorinated pesticides in fish caught in the southern Baltic. Oceanological and Hydrobiological Studies, 42, 251–259.Google Scholar
  50. Rolland, M. R. (2000). Ecoepidemiology of the effects of pollution on reproduction and survival of early life stages in teleosts. Fish and Fisheries, 1, 41–72.CrossRefGoogle Scholar
  51. Roose, P., Albaigés, J., Bebianno, M. J., Camphuysen, C., Cronin, M., de Leeuw, J., et al. (2011). Chemical pollution in Europe’s seas: Programmes, practices and priorities for research. In J. B. Calewaert & N. McDonough (Eds.), Marine board position paper 16 (p. p 108). Belgium: Ostend.Google Scholar
  52. Roots, O., Zitko, V., Kiviranta, H., Rantakokko, P., & Ruokojärvi, P. (2009). Concentrations and profiles of brominated diphenyl ethers (BDEs) in Baltic and Atlantic herring. Oceanologia, 51, 515–523.CrossRefGoogle Scholar
  53. Roots, O., Zitko, V., Kiviranta, H., Rantakokko, P., & Ruokojärvi, P. (2010). Polybrominated diphenyl ethers in Baltic herring from Estonian waters, 2006–2008. Russian Journal of General Chemistry, 80, 2721–2730.CrossRefGoogle Scholar
  54. Serrano, R., Blanes, M. A., & López, F. J. (2008). Maternal transfer of organochlorine compounds to oocytes in wild and farmed gilthead sea bream (Sparus aurata). Chemosphere, 70, 561–566.CrossRefGoogle Scholar
  55. Sprague, M., Dick, J. R., Medina, A., Tocher, D. R., Bell, J. G., & Mourente, G. (2012). Lipid and fatty acid composition, and persistent organic pollutant levels in tissues of migrating Atlantic bluefin tuna (Thunnus thynnus, L.) broodstock. Environmental Pollution, 171, 61–71.CrossRefGoogle Scholar
  56. Strandberg, B., Bandh, C., van Bavel, B., Bergqvist, P.A., Broman, D., Näf, C., Pettersen, H., Rappe, C. (1998a) Concentrations, biomagnification and spatial variation of organochlorine compounds in a pelagic food web in the northern part of the Baltic Sea. Science of the Total Environment.Google Scholar
  57. Strandberg, B., Strandberg, L., Van Bavel, B., Bergqvist, P. A., Broman, D., Falandysz, J., et al. (1998b). Concentrations and spatial variations of cyclodienes and other organochlorines in herring and perch from the Baltic Sea. Science of the Total Environment, 215, 69–83.CrossRefGoogle Scholar
  58. Sühring, R., Freese, M., Schneider, M., Schubert, S., Pohlmann, J.-D., Alaee, M., et al. (2015). Maternal transfer of emerging brominated and chlorinated flame retardants in European eels. Science of the Total Environment, 530-531, 209–218.CrossRefGoogle Scholar
  59. Szlinder-Richert, J., Barska, I., Mazerski, J., & Usydus, Z. (2008). Organochlorine pesticides in fish from the southern Baltic Sea: levels, bioaccumulation features and temporal trends during the 1995-2006 period. Marine Pollution Bulletin, 56, 927–940. doi: 10.1016/j.marpolbul.2008.01.029.CrossRefGoogle Scholar
  60. Szlinder-Richert, J., Barska, I., Mazerski, J., & Usydus, Z. (2009). PCBs in fish from the southern Baltic Sea: levels, bioaccumulation features, and temporal trends during the period from 1997 to 2006. Marine Pollution Bulletin, 58, 85–92.CrossRefGoogle Scholar
  61. Theobald, N., Gerwinski, W., Caliebe, C., Haarich, M. (2007) Entwicklung und Validierung einer Methode zur Bestimmung von polyfluorierten organischen Substanzen in Meerwasser, Sedimenten und Biota; Untersuchungen zum Vorkommen dieser Schadstoffe in der Nord- und Ostsee. Umweltforschungsplan des Bundesministeriums für Umwelt, Naturschutz und Reakt 1–134.Google Scholar
  62. Ullah, S., Huber, S., Bignert, A., & Berger, U. (2014). Temporal trends of perfluoroalkane sulfonic acids and their sulfonamide-based precursors in herring from the Swedish west coast 1991-2011 including isomer-specific considerations. Environment International, 65, 63–72.CrossRefGoogle Scholar
  63. Ungerer, J. R., & Thomas, P. (1996). Role of very low density lipoproteins in the accumulation of o’,p’-DDT in fish ovaries during gonadal recrudescence. Aquatic Toxicology, 35, 183–195.CrossRefGoogle Scholar
  64. Von Westernhagen, H., Dethlefsen, V., Cameron, P., & Janssen, D. (1987). Chlorinated-hydrocarbon residues in gonads of marine fish and effects on reproduction. Sarsia, 72, 419–422.CrossRefGoogle Scholar
  65. Waszak, I., Dabrowska, H., & Góra, A. (2012). Bioaccumulation of polybrominated diphenyl ethers (PBDEs) in flounder (Platichthys flesus) in the southern Baltic Sea. Marine Environmental Research, 79, 132–141.CrossRefGoogle Scholar
  66. Webster, L., Russell, M., Hussy, I., & Moffat, C. F. (2009). A review of brominated flame retardats (BFRs) in the aquatic environment and the development of an analytical technique for their analysis in environmental samples. Fisheries Research Services Internal Report, 06, 46.Google Scholar
  67. Webster, L., Roose, P., Bersuder, P., Kottermann, M., Haarich, M., & Vorkamp, K. (2013). Determination of polychlorinated biphenyls in sediment and biota. ICES Techniques in Marine Environmental Sciences, 53, 18.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Sophia Schubert
    • 1
  • Nadia Keddig
    • 1
  • Wolfgang Gerwinski
    • 2
  • Jan Neukirchen
    • 2
  • Ulrike Kammann
    • 1
  • Michael Haarich
    • 1
  • Reinhold Hanel
    • 1
  • Norbert Theobald
    • 2
  1. 1.Thünen Institute of Fisheries EcologyHamburgGermany
  2. 2.German Maritime and Hydrographic AgencyHamburgGermany

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