Abstract
Due to heavy anthropogenic influence and variation of the environmental conditions in the Baltic Sea, reproductive disorders are becoming a major environmental concern. We show here an increasing prevalence of gonadal malformations in the Baltic herring (Clupea harengus membras), a key species of the Baltic ecosystem and important in commercial fishery. During 1987–2014, the spawning herring population in the Archipelago Sea (AS) (North Baltic Sea, Finland) was monitored annually and analyzed for gross morphology of the gonads [total number (n) of analyzed fish = 38 284]. Four different types of malformations were repeatedly found and named as asymmetric, rudimentary, segmented, and branched gonads, but also hermaphroditic gonads and miscellaneous (unidentified) disorders were recorded. In 2013, additional samplings (n of fish analyzed = 541) showed similar malformations in herring from the Bothnian Sea. In some gonad types, histological examination revealed disintegration of seminiferous tubules and hyperplasia of the interstitial tissue. In 2014, the overall prevalence of malformations was still relatively low in the AS (frequency = 0–3.4 %; n = 750) and had apparently minimal effect on population recruitment. However, an increasing trend in the time-series (GLM; F = 32.65; p < 0.001) and a significantly higher prevalence in the Bothnian Sea (frequency = 0.7–5.0 %; n = 541; χ 2 = 6.24; p < 0.05) suggest that gonadal malformations may become a new threat for fish in the Baltic Sea. The observed gonad atrophies may be due to environmental endocrine disruption; however, also other explanations may exist and potential explanations are discussed.
References
Airaksinen, R., A. Hallikainen, P. Rantakokko, P. Ruokojärvi, P.J. Vuorinen, R. Parmanne, M. Verta, J. Mannio, 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.
Aneer, G. 1987. High natural mortality of Baltic herring (Clupea harengus) eggs caused by algal exudates? Marine Biology 94: 163–169.
Arukwe, A., and A. Goksøyr. 2003. Eggshell and egg yolk protein in fish: Hepatic proteins for the next generation: Oogenetic, population, and evolutionary implications of endocrine disruption. Comparative Hepatology 2: 1–21.
Bagenal, T.B., and E. Braum. 1971. Eggs and early life history. In Methods for assessment of fish production in fresh waters. IBP handbook No 3, ed. W.E. Ricker, 166–198. Oxford: Blackwell Scientific Publications.
Barton, B.A., and G.K. Iwama. 1991. Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of the corticosteroids. Annual Review of Fish Diseases 1: 3–26.
Bengtsson, B.-E., C. Hill, Å. Bergman, I. Brandt, N. Johansson, C. Magnhagen, A. Södergren, and J. Thulin. 1999. Reproductive disturbances in Baltic fish: A synopsis of the FiRe project. Ambio 28: 2–8.
Bernet, D., T. Wahli, C. Kueng, and H. Segner. 2004. Frequent and unexplained gonadal abnormalities in whitefish (central alpine Coregonus sp.) from an alpine oligotrophic lake in Switzerland. Diseases of Aquatic Organisms 61: 137–148.
Bernet, D., A. Liedtke, D. Bittner, R.I.L. Eggen, S. Kipfer, C. Küng, C.R. Largiader, M.J.-F. Suter, et al. 2008. Gonadal malformations in whitefish from Lake Thun: Defining the case and evaluating the role of EDCs. Chimia 62: 383–388.
Billard, R., C. Bry, and C. Gillet. 1981. Stress, environment and reproduction in teleost fish. In Stress and fish, ed. A.D. Pickering, 185–208. London: Academic Press.
Breitholtz, M., C. Hill, and B.-E. Bengtsson. 2001. Toxic substances and reproductive disorders in Baltic fish and crustaceans. Ambio 30: 210–216.
Bucholtz, R.H., J. Tomkiewicz, and J. Dalskov. 2008. Manual to determine gonadal maturity of herring (Clupea harengus L.). DTU Aqua-report 197-08. Charlottenlund: National Institute of Aquatic Resources.
Coady, K.K., M.B. Murphy, D.L. Villeneuve, M. Hecker, P.D. Jones, J.A. Carr, K.R. Solomon, E.E. Smith, et al. 2005. Effects of atrazine on metamorphosis, growth, laryngeal and gonadal development, aromatase activity, and sex steroid concentrations in Xenopus laevis. Ecotoxicology and Environmental Safety 62: 160–173.
Colborn, T., F.S. von Saal, and A.M. Soto. 1993. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environmental Health Perspectives 101: 378–384.
DeFalco, T., and B. Capel. 2009. Gonad morphogenesis in vertebrates: Divergent means to a convergent end. Annual Review of Cell and Developmental Biology 25: 457–482.
European Union. 2008. Directive 2008/56/EC of the European Parliament and of the Council, 17.6.2008, establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Official Journal of the European Union L 164/19.
Gadd, T., M. Jakava-Viljanen, H. Tapiovaara, P. Koski, and L. Sihvonen. 2011. Epidemiological aspects of viral haemorrhagic septicaemia virus genotype II isolated from Baltic herring, Clupea harengus membras L. Journal of Fish Diseases 34: 517–529.
Gercken, J., L. Förlin, and J. Andersson. 2006. Developmental disorders in larvae of eelpout (Zoarces viviparus) from German and Swedish Baltic coastal waters. Marine Pollution Bulletin 53: 497–507.
Guillette Jr., L.J., D.A. Crain, M.P. Gunderson, S.A.E. Kools, M.R. Milnes, E.F. Orlando, A.A. Rooney, and A.R. Woodward. 2000. Alligators and endocrine disrupting contaminants: A current perspective. American Zoologist 40: 438–452.
Hecker, M., M.B. Murphy, K.K. Coady, D.L. Villeneuve, P.D. Jones, J.A. Carr, K.R. Solomon, E.E. Smith, et al. 2006. Terminology of gonadal anomalies in fish and amphibians resulting from chemical exposures. Review of Environmental Contamination and Toxicology 187: 103–131.
HELCOM. 2004. Dioxins in the Baltic Sea. Report of the Helsinki Commission—Baltic Marine Environment Protection Commission, 19 pp.
HELCOM. 2007. Climate change in the Baltic Sea area—HELCOM Thematic Assessment in 2007. In Baltic Sea Environment Proceedings No. 111.
HELCOM. 2010. Hazardous substances in the Baltic Sea—An integrated thematic assessment of hazardous substances in the Baltic Sea. In Baltic Sea Environment Proceedings No. 120B.
Henderson, A.C., A.J. Reeve, and A. Ambu-Ali. 2014. Microanatomy of the male and female reproductive tracts in the long-tailed butterfly ray Gymnura poecilura, an elasmobranch with unusual characteristics. Journal of Fish Biology 84: 297–313.
Herrmann, J., G. Kanisch, and S. P. Nielsen. 2013. Radioactive substances—137Cs in fish and surface waters. HELCOM Core Indicator Report. Online: http://www.helcom.fi/Core%20Indicators/HELCOM_CoreIndicator_Radioactivesubstances.pdf
Hänninen, J., and I. Vuorinen. 2015. Riverine tot-P loading and seawater concentrations in the Baltic Sea during the 1970s to 2000—transfer function modeling based on the total runoff. Environmental Monitoring and Assessment 187: 343.
Hänninen, J., I. Vuorinen, and P. Hjelt. 2000. Climatic factors in the Atlantic control the oceanographic and ecological changes in the Baltic Sea. Limnology and Oceanography 45: 703–710.
Kääriä, J., M. Naarminen, J. Eklund, N. Jönsson, G. Aneer, and M. Rajasilta. 2001. A tagging experiment on spring-spawning Baltic herring (Clupea harengus membras) in southwest Finland in 1990-1998. In Herring: Expectations for a new millennium, ed. F. Funk, J. Blackburn, D. Hay, A.J. Paul, R. Stephenson, R Toresen, and D. Witherell, 599–609. Alaska Sea Grant College Program AK-SG-01-04, 2001.
Laine, P. 2003. Regulation of reproductive success in Baltic herring (Clupea harengus membras): Individual effort meets the environment. Annales Universitatis Turkuensis, Ser. AII. TOM. 166. PhD Thesis. University of Turku.
Lehtonen, K.K., D. Schiedek, A. Köhler, T. Lang, P.J. Vuorinen, L. Förlin, J. Baršiene, J. Pempkowiak, et al. 2006. The BEEP project in the Baltic Sea: Overview of results and outline for a regional biological effects monitoring strategy. Marine Pollution Bulletin 53: 523–537.
Lindegren, M., Ö. Östman, and A. Gårdmark. 2011. Interacting trophic forcing and the population dynamics of herring. Ecology 92: 1407–1413.
Marmon, S.K., P. Liljelind, and I. Undeland. 2009. Removal of lipids, dioxins, and polychlorinated biphenyls during production of protein isolates from Baltic herring (Clupea harengus) using pH-shift processes. Journal of Agricultural and Food Chemistry 57: 7819–7825.
Möllmann, C., G. Kornilovs, M. Fetter, and F.W. Köster. 2005. Climate, zooplankton, and pelagic fish growth in the central Baltic Sea. ICES Journal of Marine Science 62: 1270–1280.
Omotosho, J.S. 1987. Abnormal development in the ovaries of Oreochromis niloticus Linn (Perciformes: Cichlidae) in Nigeria. Revista de Biologia Tropical 35: 83–85.
Parenti, L.R., and H.J. Grier. 2004. Evolution and phylogeny of gonad morphology in bony fishes. Integrative and Comparative Biology 44: 333–348.
Pulliainen, E., K. Korhonen, L. Kankaanranta, and K. Mäki. 1992. Non-spawning burbot on the northern coast of the Bothnian Bay. Ambio 21: 170–175.
Rajasilta, M., J. Eklund, J. Kääriä, and K. Ranta-aho. 1989. The deposition and mortality of the eggs of the Baltic herring, Clupea harengus membras L., on different substrates in the south-western archipelago of Finland. Journal of Fish Biology 34: 417–427.
Rajasilta, M., J. Eklund, N. Jönsson, T. Lorenz, and P. Laine. 1999. Intensive monitoring of spawning populations of the Baltic herring (Clupea harengus membras L.). Study Report EU 96-068. Archipelago Research Institute, University of Turku. Online: http://www.utu.fi/fi/yksikot/tyyk/saaristomeren-tutkimuslaitos/tutkimus/Documents/seili3.pdf.
Rajasilta, M., J. Eklund, J. Hänninen, I. Vuorinen, and P. Laine. 2015. Female Baltic herring Clupea harengus allocate resources from growth to reproduction in poor feeding conditions. Journal of Fish Biology 86: 575–591.
Reno, P.W. 1998. Factors involved in the dissemination of disease in fish populations. Journal of Aquatic Animal Health 10: 160–171.
Rönkkönen, S., E. Ojaveer, T. Raid, and M. Viitasalo. 2004. Long-term changes in Baltic herring (Clupea harengus membras) growth in the Gulf of Finland. Canadian Journal of Fisheries and Aquatic Science 61: 219–229.
Sadovy, Y., and D.Y. Shapiro. 1987. Criteria for the diagnosis of hermaphroditism in fishes. Copeia 1987: 136–156.
Sjöblom, V. 1961. Wanderungen des Strömlings (Clupea harengus L.) in einigen Schären- und Hochseegebieten der Nördlichen Ostsee. Annales Zoologici Soc ‘Vanamo’ TOM. 23. PhD Thesis. University of Helsinki.
van Damme, C.J.G., M. Dickey-Collas, A.D. Rijnsdorp, and O.S. Kjesbu. 2009. Fecundity, atresia, and spawning strategies of Atlantic herring (Clupea harengus). Canadian Journal of Fisheries and Aquatic Science 66: 2130–2141.
Vuorinen, I., J. Hänninen, M. Rajasilta, P. Laine, J. Eklund, F. Montesino-Pouzols, F. Corona, K. Junker, et al. 2015. Scenario simulations of future salinity and ecological consequences in the Baltic Sea and adjacent North Sea areas—implications for environmental monitoring. Ecological Indicators 50: 196–205.
Westernhagen, H.V., V. Dethlefsen, P. Cameron, J. Berg, and G. Fürstenberg. 1988. Developmental defects in pelagic fish embryos from the western Baltic. Helgoländer Meeresuntersuchungen 42: 13–36.
Wiklund, T., L. Lounasheimo, J. Lom, and G. Bylund. 1996. Gonadal impairment in roach Rutilus rutilus from Finnish coastal areas of the northern Baltic Sea. Diseases of Aquatic Organisms 26: 163–171.
Wootton, R.J., and C. Smith. 2015. Reproductive biology of teleost fishes. Oxford: Wiley-Blackwell.
Acknowledgments
Our thanks are due to Jan Eklund for reading the ages of herring and colleagues assisting in the basic treatment of fish samples and especially to the fishermen, who provided the fish samples over the years. Financial support for the work has been obtained from the Ministry of Agriculture and Forestry in Finland, the European Union (96-068), Turku University Foundation, and Jenny and Antti Wihuri Foundation. Dr. Robert Badeau from Aura Professional English Consulting, LTD, (www.auraenglish.com) is acknowledged for the language content editing of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rajasilta, M., Elfving, M., Hänninen, J. et al. Morphological abnormalities in gonads of the Baltic herring (Clupea harengus membras): Description of types and prevalence in the northern Baltic Sea. Ambio 45, 205–214 (2016). https://doi.org/10.1007/s13280-015-0717-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13280-015-0717-x