Skip to main content
Log in

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

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

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.

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

Similar content being viewed by others

References

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bignert, A., Nyberg, E., Asplund, L., Eriksson, U. (2010) Comments concerning the national Swedish contaminant monitoring programme in marine biota, 2010. Natural History 157.

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • Fent, K. (2013). Ökotoxikologie (4th ed.). Stuttgart: Georg Thieme Verlag KG.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • Hansen, P., Westernhagen, H. V., & Rosenthal, H. (1985). Chlorinated hydrocarbons and hatching success in Baltic herring spring Spawners. Marine Environmental Research, 15, 59–76.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • HELCOM (2007b). Baltic Sea action plan. Krakow, Poland: HELCOM.

    Google Scholar 

  • 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 

  • HELCOM. (2015) Manual for Marine Monitoring in the COMBINE Program of HELCOM. COMBINE Manual 416.

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kime, D. E. (1995). The effects of reproduction in fish. Reviews in Fish Biology and Fisheries, 5, 52–96.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Klinkhardt, M. (1996). Der Hering: Clupea harengus. Magdeburg: Spektrum Akad. Verlag.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Lubzens, E., Young, G., Bobe, J., & Cerdà, J. (2010). Oogenesis in teleosts: how eggs are formed. General and Comparative Endocrinology, 165, 367–389.

    Article  CAS  Google Scholar 

  • Mackay, D., & Fraser, A. (2000). Bioaccumulation of persistent organic chemicals: mechanisms and models. Environmental Pollution, 110, 375–391.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 2

  • OSPAR. (2005) Assessment of data collected under the Co-ordinated Environmental Monitoring Programme (CEMP), 1–250.

  • OSPAR. (2009) Background Document on CEMP Assessment Criteria for QSR 2010. Monitoring and Assessment Ser 24.

  • OSPAR (2012). JAMP guidelines for monitoring contaminants in biota. Monitoring Guidelines, 1999-02 re, 1–122.

    Google Scholar 

  • OSPAR Commission. (2010) Agreement on CEMP assessment criteria for the QSR 2010. Monitoring and Assessment

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Pikkarainen, A.-L., & Parmanne, R. (2006). Polichlorinated biphenyls and organochlorine pesticides in Baltic herring 1985–2002. Marine Pollution Bulletin, 52, 1304–1309.

    Article  CAS  Google Scholar 

  • R Core Team. (2014) R: A language and environment for statistical computing.

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sophia Schubert or Nadia Keddig.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Sophia Schubert and Nadia Keddig contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schubert, S., Keddig, N., Gerwinski, W. et al. Persistent organic pollutants in Baltic herring (Clupea harengus)—an aspect of gender. Environ Monit Assess 188, 368 (2016). https://doi.org/10.1007/s10661-016-5363-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-016-5363-7

Keywords

Navigation