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Acta Parasitologica

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Volume 59, Issue 3


Metazoan parasites from herring (Clupea harengus L.) as biological indicators in the Baltic Sea

Patrick Unger
  • Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental Sciences, University of Rostock, Justus-von-Liebig-Weg 6, 18059, Rostock, Germany
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/ Sven Klimpel
  • Institute for Ecology, Evolution and Diversity, Biodiversity and Climate Research Centre, Senckenberg Gesellschaft für Naturforschung, Goethe-University, Max-von-Laue-Straße 13, 60438, Frankfurt am Main, Germany
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/ Thomas Lang / Harry Palm
  • Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental Sciences, University of Rostock, Justus-von-Liebig-Weg 6, 18059, Rostock, Germany
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Published Online: 2014-08-15 | DOI: https://doi.org/10.2478/s11686-014-0276-5


Zoographical distribution of metazoan fish parasites in herring, Clupea harengus, from the Baltic Sea was analysed in order to use them as potential biological indicators. A total of 210 herring from six different sampling sites were investigated, harbouring 12 different parasite species [five digeneans (D), one cestode (C), three nematodes (N) and three acanthocephalans (A)]. The distribution of the parasite species differed according to region, with a distinct gradient of decreasing species richness towards the east of the Baltic Sea. The western localities at Kiel Bay, Rügen and Poland had the highest parasite diversity, including the marine parasite species Anisakis simplex (s.s.) (N), Brachyphallus crenatus and Hemiurus luehei (both D). The eastern localities had low parasite species richness, predominated by the freshwater digenean Diplostomum spathaceum. We could identify three different Baltic herring stocks, the spring-spawning herring of the western Baltic reaching from the Kattegat to the German and Polish coast, the stock of the central Baltic proper and the northern stock of C. harengus var. membras of the Gulf of Finland. The limited distribution of the herring parasites within the Baltic Sea enables their use as biological indicators for migration patterns and stock separation. The acanthocephalan Pomphorhynchus laevis that has already been used as an accumulation bioindicator for heavy metals was only recorded for the western herring stocks. However, the presence of mainly generalistic parasites and their uneven distribution patterns make their use as indicators for regional environmental and global change more difficult.

Keywords: Fish parasites; Atlantic herring; Clupea harengus; zoogeographic distribution; biological indicators; Baltic Sea

  • [1] Arthur J.R., Arai H.P. 1984. Annotated Checklist and Bibliography of Parasites of Herring (Clupea harengus L.). Canadian Special Publication of Fisheries and Aquatic Sciences, 70, 1–26. Google Scholar

  • [2] Bekkevold D., Andre C., Dahlgren T.G., Clausen L.A.W., Torstensen E., Mosegaard H., Carvalho G.R., et al. 2005. Environmental correlates of population differentiation in Atlantic herring. Evolution, 59, 2656–2668. DOI: 10.1111/j.0014-3820.2005.tb00977.x. http://dx.doi.org/10.1111/j.0014-3820.2005.tb00977.xCrossrefGoogle Scholar

  • [3] Bush O., Lafferty A.D., Lotz J.M., Shostak A.W. 1997. Parasitology meets ecology on his own terms. Margolis et al. revisited. Journal of Parasitology, 83, 575–583. http://dx.doi.org/10.2307/3284227CrossrefGoogle Scholar

  • [4] Campana S.E., Casselman J.M. 1993. Stock discrimination using otolith shape analysis. Canadian Journal of Fisheries and Aquatic Sciences, 50, 1062–1083. http://dx.doi.org/10.1139/f93-123CrossrefGoogle Scholar

  • [5] Dutt S. 1958. Number of pectoral fin rays in the spring and autumn spawning herring in Kiel Bay. Rapports et Proce’s-Verbaux des Reúnions du Conseil International pour l’Exploration de la Mer, 143, 109–113. Google Scholar

  • [6] Ellemann G. 1989. Danish experiences, legislation and eating habits in relation to nematodes in fish and fish products. In: (Eds. H. Möller), Nematode Problems in North Atlantic Fish. Report from a Workshop in Kiel, 3—4 April 1989. ICES CM 1989/F, 6, 27–28. Google Scholar

  • [7] FAO. 2012. The State of World Fisheries and Aquaculture 2012. Rome, 1–209. Google Scholar

  • [8] Galli P., Crosa G., Mariniello L., Ortis M., D’Amelio S. 2001. Water quality as a determinant of the composition of fish parasite communities. Hydrobiologia, 452, 173–179. http://dx.doi.org/10.1023/A:1011958422446CrossrefGoogle Scholar

  • [9] Garey J.R., Near T.J, Nonnemacher M.R., Nadler S.A. 1996. Molecular evidence for Acanthocephala as a subtaxon Rotifera. Molecular Phylogenetics and Evolution, 43, 287–292. http://dx.doi.org/10.1007/BF02338837CrossrefGoogle Scholar

  • [10] Grabda J. 1974. The dynamics of the nematode larvae Anisakis simplex (Rud.) invasion in the south-western Baltic herring (Clupea harengus L.). Acta Ichthyologica et Piscatoria, 4, 3–21. Google Scholar

  • [11] Grahl-Nielsen O., Ulvund K.A. 1990. Distinguishing populations of herring by chemometry of fatty acids. American Fisheries Society Symposium, 7, 566–571. Google Scholar

  • [12] Gröger J., Gröhsler T. 2001. Comparative analysis of alternative statistical models for differentiation of herring stocks based on meristic characters. Journal of Applied Ichthyology, 17, 207–219. DOI: 10.1046/j.1439-0426.2001.00254.x. http://dx.doi.org/10.1046/j.1439-0426.2001.00254.xCrossrefGoogle Scholar

  • [13] Hammond P.S., Bearzi G., Bjørge A., Forney K., Karczmarski L., Kasuya T., Perrin W.F, Scott M.D., Wang J.Y., Wells R.S., Wilson B. 2008. Phocoena phocoena (Baltic Sea subpopulation). In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2. Google Scholar

  • [14] Hansson S., Larsson U., Johansson S. 1990. Selective predation by herring and mysids, and zooplankton community structure in a Baltic Sea coastal area. Journal of Plankton Research, 12, 1099–1116. http://dx.doi.org/10.1093/plankt/12.5.1099CrossrefGoogle Scholar

  • [15] Hemmingsen W., MacKenzie K. 2013. Latitudinal variations in the occurrence of some cod parasites along the west coast of Norway. Marine Biology Research, 9,4, 431–436. DOI: 10.1080/17451000.2012.742548. http://dx.doi.org/10.1080/17451000.2012.742548CrossrefGoogle Scholar

  • [16] Herreras M.V., Kaarstad S.E., Balbuena J.A., Kinze C.C., Raga J.A. 1997. Helminth parasites of the digestive tract of the harbour porpoise Phocoena phocoena in Danish waters: a comparative geographical analysis. Diseases of Aquatic Organisms, 28, 163–167. http://dx.doi.org/10.3354/dao028163CrossrefGoogle Scholar

  • [17] King D.P.F., Ferguson A., Moffett L.J.J. 1987. Aspects of the population genetics of herring. Clupea harengus, around the British Isles and in the Baltic Sea. Fisheries Research, 6, 35–52. http://dx.doi.org/10.1016/0165-7836(87)90005-1CrossrefGoogle Scholar

  • [18] Klimpel S., Palm H.W. 2011: Anisakid nematode (Ascaridoidea) life cycles and distribution: Increasing zoonotic potential in the time of climate change? Parasitology Research Monographs 2, Springer-Verlag, Heidelberg, Germany, 1–22. DOI: 10.1007/978-3-642-21396-0_11. CrossrefGoogle Scholar

  • [19] Klinkhardt M. 1996. Der Hering: Clupea harengus. Westarp Wissenschaften, Magdeburg; Spektrum Akademischer Verlag, Heidelberg, 230 pp. (In German) Google Scholar

  • [20] Kornilovs G., Sidrevics L., Dippner J.W. 2001. Fish and zooplankton interaction in the Central Baltic Sea. ICES Journal of Marine Science, 58, 579–588. http://dx.doi.org/10.1006/jmsc.2001.1062CrossrefGoogle Scholar

  • [21] Køie M., Fagerholm H.P. 1995. The life cycle of Contracaecum osculatum (Rudolphi, 1802) sensu stricto (Nematoda, Ascaridoidea, Anisakidae) in view of experimental infections. Parasitology Research, 81, 481–489. http://dx.doi.org/10.1007/BF00931790CrossrefGoogle Scholar

  • [22] Køie M. 1992. Life cycle and structure of the fish digenean Brachyphallus crenatus (Hemiuridae). Journal of Parasitology, 78, 338–343. http://dx.doi.org/10.2307/3283485CrossrefGoogle Scholar

  • [23] Köhn J., Gosselck F. 1989. Malakostracen der Ostsee. Mitteilungen aus dem Zoologischen Museum in Berlin, 65, 8–21. (In German) Google Scholar

  • [24] Landsberg J.H., Blakesley B.A., Reese R.O., McRae G., Forstchen P.R. 1998. Parasites of fish as indicators of environmental stress. Environmental Monitoring and Assessment, 51, 211–232. http://dx.doi.org/10.1023/A:1005991420265CrossrefGoogle Scholar

  • [25] Lang T., Damm U., Weber W., Neudecker T., Kühlmorgen-Hille G. 1990. Infestation of herring (Clupea harengus L.) with Anisakis sp. Larvae in the western Baltic. Archiv für Fischereiwissenschaft, 40, 101–117. Google Scholar

  • [26] MacKenzie K. 1983. Parasites as biological tags in fish population studies. Advances in Applied Biology, 7, 251–331. Google Scholar

  • [27] MacKenzie K. 1987. Parasites as indicators of host populations. International Journal for Parasitology, 17, 345–352. http://dx.doi.org/10.1016/0020-7519(87)90109-3CrossrefGoogle Scholar

  • [28] MacKenzie K., Williams H.H., Williams B., McVicah A.H., Siddall R. 1995. Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in parasitology, 35, 85–144. http://dx.doi.org/10.1016/S0065-308X(08)60070-6CrossrefGoogle Scholar

  • [29] MacKenzie K., Abaunza P. 2005. Parasites as biological tags. In: (Eds. Cadrin S.X., Friedland K.D., Waldman J.R.), Stock Identification Methods: Applications in Fisheries Science. San Diego, CA: Elsevier Academic Press, 211–226. http://dx.doi.org/10.1016/B978-012154351-8/50012-5CrossrefGoogle Scholar

  • [30] Magurran A.E. 1988. Ecological diversity and its measurement. Croom Helm, London, 1–179. http://dx.doi.org/10.1007/978-94-015-7358-0CrossrefGoogle Scholar

  • [31] Nachev M., Schertzinger G., Sures B. 2013. Comparison of the metal accumulation capacity between the acanthocephalan Pomphorhynchus laevis and larval nematodes of the genus Eustrongylides sp. infecting barbel (Barbus barbus). Parasites & Vectors, 6,21, 1–8. Google Scholar

  • [32] Nehring D., Matthäus W. 1991. Current Trends in Hydrographic and Chemical Parameters and Eutrophication in the Baltic Sea. International Review of Hydrobiology, 76, 297–316. CrossrefGoogle Scholar

  • [33] Nickol B.B., Helle E., Valtonen E.T. 2002. Corynosoma magdaleni in gray seals from the Gulf of Bothnia, with emended descriptions of Corynosoma strumosum and Corynosoma magdaleni. Journal of Parasitology, 88, 1222–1229. DOI: 10.1645/0022-3395(2002)088. http://dx.doi.org/10.1645/0022-3395(2002)088[1222:CMIGSF]2.0.CO;2CrossrefGoogle Scholar

  • [34] O`Neill G., Whelan J. 2002. The occurrence of Corynosoma strumosum in grey seal, Halichoerus grypus, caught off the Atlantic coast of Ireland. Journal of Helminthology, 76, 231–234. DOI: 10.1076/JOH2002117. http://dx.doi.org/10.1079/JOH10.1076/2002117CrossrefGoogle Scholar

  • [35] Palm H.W., Klimpel S., Bucher C. 1999. Checklist of metazoan fish parasites of German coastal waters. Berichte aus dem Institut für Meereskunde an der Christian-Albrecht Universität, Kiel Nr. 307, 148 pp. Google Scholar

  • [36] Palm H.W., Klimpel S. 2007. Evolution of parasitic life in the ocean. Trends in Parasitology, 23, 1–2. http://dx.doi.org/10.1016/j.pt.2006.11.001CrossrefGoogle Scholar

  • [37] Palm H.W. 2011. Fish Parasites as Biological Indicators in a Changing World: Can We Monitor Environmental Impact and Climate Change? In: Mehlhorn H. Progress in Parasitology, Parasitology Research Monographs 2, 223–250. DOI 10.1007/978-3-642-21396-0_12. CrossrefGoogle Scholar

  • [38] Podolska M., Horbowy J., Wyszynski M. 2006. Discrimination of Baltic herring populations with respect to Anisakis simplex larvae infection. Journal of Fish Biology, 68, 1241–1256. DOI: 10.1111/j.0022-1112.2006.01004.x. http://dx.doi.org/10.1111/j.0022-1112.2006.01004.xCrossrefGoogle Scholar

  • [39] Popiel J. 1958. Preliminary results of the gill-raker counts in springspawners of the Gulf of Gdansk. ICES Document CM 1958/Herring Committee, 50. Google Scholar

  • [40] Rajasilta M., Eklund J., Laine P., Jönsson N., Lorenz T. 2006. Intensive monitoring of spawning populations of the Baltic herring (Clupea harengus membras L.). Final Report of the Study Project Ref. No. 96-068, SEILI Archipelago Research Institute Publications, 3, Turku, 75 pp. Google Scholar

  • [41] Remane A. 1958. Ökologie des Brackwassers. In: (Eds. Remane A., Schlieper C.) Die Biologie des Brackwasses. Die Binnengewässer, 12, 216 pp. (In German) Google Scholar

  • [42] Reimer L.W. 1970. Digene Trematoden und Cestoden der Ostseefische als natürliche Fischmarken. Parasitologische Schriftenreihe, 20, 144 pp. (In German) Google Scholar

  • [43] Riemann F. 1988. Introduction to the study of meiofauna. In: (Eds. Higgins R.P., Thiel H.) Smithsonian Institution Press, 293–301. Google Scholar

  • [44] Rudstam L.G., Hansson S., Johansson S., Larsson U. 1992. Dynamics of planktivory in a coastal area of the northern Baltic Sea. Marine Ecology Progress Series, 80, 159–173. http://dx.doi.org/10.3354/meps080159CrossrefGoogle Scholar

  • [45] Ryman N., Lagercrantz U., Andersson L., Chakraborty R., Rosenberg R. 1984. Lack of correspondence between genetic and morphologic variability patterns in Atlantic herring (Clupea harengus). Heredity, 53, 687–704. http://dx.doi.org/10.1038/hdy.1984.127CrossrefGoogle Scholar

  • [46] Sanger F., Nicklen S., Coulson A.R. 1977. DNA sequencing with chainterminating inhibitors. Proceedings of the National Academy of Sciences of the United States of America, 74, 5463–5467. Google Scholar

  • [47] Shih H.H. 2004. Parasitic helminth fauna of the cutlass fish, Trichiurus lepturus L., and the differentiation of four anisakid nematode third-stage larvae by nuclear ribosomal DNA sequences. Parasitology Research, 93, 188–195. DOI: 10.1007/s00436-004-1095-7. http://dx.doi.org/10.1007/s00436-004-1095-7CrossrefGoogle Scholar

  • [48] Siebert U., Weiss R., Frank H., Benke H., Frese K. 2001. Post mortem findings in harbour porpoises (Phocoena phocoena) from the German North and Baltic Seas. Journal of Comparative Pathology, 124(2/3), 102–114. DOI: 10.1053/jcpa.2000.043. http://dx.doi.org/10.1053/jcpa.2000.0436CrossrefGoogle Scholar

  • [49] Smith J.W., Wootten R. 1978. Anisakis and Anisakiasis. Advances in Parasitology, 16, 93–148. http://dx.doi.org/10.1016/S0065-308X(08)60573-4CrossrefGoogle Scholar

  • [50] Sparholt H. 1994. Fish species interactions in the Baltic Sea. Dana 10, 131–162. Google Scholar

  • [51] Szostakowska B., Myjak P., Wyszynski M., Pietkiewicz H., Rokicki J. 2005. Prevalence of Anisakin Nematodes in Fish from southern Baltic Sea. Polish Journal of Microbiology, 54, 41–45. Google Scholar

  • [52] Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Research, 24, 4876–4882. http://dx.doi.org/10.1093/nar/25.24.4876CrossrefGoogle Scholar

  • [53] Verweyen L., Klimpel S., Palm H.W. 2011. Molecular Phylogeny of the Acanthocephala (Class Palaeacanthocephala) with a Paraphyletic Assemblage of the Orders Polymorphida and Echinorhynchida. PLoS ONE 6(12), 1–9. DOI: 10.1371/journal.pone.0028285. http://dx.doi.org/10.1371/journal.pone.0028285CrossrefGoogle Scholar

  • [54] Wasmund N., Andrushaitis A., Łysiak-Pastuszak E., Müller-Karulis B., Nausch G., Neumann T., Ojaveer H., Olenina I., Postel L., Witek Z. 2001. Trophic Status of the South-Eastern Baltic Sea: A Comparison of Coastal and Open Areas. Estuarine, Coastal and Shelf Science, 53, 849–864. DOI: 10.1006/ecss.2001.0828. http://dx.doi.org/10.1006/ecss.2001.0828CrossrefGoogle Scholar

  • [55] Wunschmann A., Siebert U., Frese K., Weiss R., Lockyer C., Heide-Jorgensen M.P., Müller G., Baumgärtner W. 2001. Evidence of infectious diseases in harbour porpoises (Phocoena phocoena) hunted in the waters of Greenland and by-caught in the German North Sea and Baltic Sea. Veterinary Record, 148, 715–720. DOI: 10.1136/vr.148.23.715. http://dx.doi.org/10.1136/vr.148.23.715CrossrefGoogle Scholar

  • [56] Zander C.D. 1998. Parasit-Wirt-Beziehungen: Einführung in die ökologische Parasitologie. Springer-Verlag, Berlin, 184 pp. (In German) http://dx.doi.org/10.1007/978-3-642-58838-9CrossrefGoogle Scholar

  • [57] Zander C.D., Reimer L.W., Barz K., Dietel G., Strohbach U. 2000. Parasite communities of the Salzhaff (Northwest Mecklenburg, Baltic Sea). II. Guild communities, with special regard to snails, benthic crustaceans, and small-sized fish. Parasitology Research, 86, 359–372. DOI: 10.1007/s004360050562. http://dx.doi.org/10.1007/s004360050681CrossrefGoogle Scholar

  • [58] Zander C.D., Reimer L.W. 2002. Parasitism at the ecosystem level in the Baltic Sea. Cambridge University Press, Parasitology, 124, 119–134. DOI: 10.1017/S0031182002001567 CrossrefGoogle Scholar

  • [59] Zhu X.Q., Gasser R.B., Jacobs D.E., Hung G.C., Chilton N.B. 2000. Relationships among some ascaridoid nematodes based on ribosomal DNA sequence data. Parasitology Research, 86, 738–744. DOI: 10.1007/PL00008561. http://dx.doi.org/10.1007/PL00008561CrossrefGoogle Scholar

About the article

Published Online: 2014-08-15

Published in Print: 2014-09-01

Citation Information: Acta Parasitologica, Volume 59, Issue 3, Pages 518–528, ISSN (Online) 1896-1851, DOI: https://doi.org/10.2478/s11686-014-0276-5.

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© 2014 W. Stefański Institute of Parasitology, PAS. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

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