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In situ effects of metal contamination from former uranium mining sites on the health of the three-spined stickleback (Gasterosteus aculeatus, L.)

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Abstract

Human activities have led to increased levels of various pollutants including metals in aquatic ecosystems. Increase of metallic concentrations in aquatic environments represents a potential risk to exposed organisms, including fish. The aim of this study was to characterize the environmental risk to fish health linked to a polymetallic contamination from former uranium mines in France. This contamination is characterized by metals naturally present in the areas (manganese and iron), uranium, and metals (aluminum and barium) added to precipitate uranium and its decay products. Effects from mine releases in two contaminated ponds (Pontabrier for Haute-Vienne Department and Saint-Pierre for Cantal Department) were compared to those assessed at four other ponds outside the influence of mine tailings (two reference ponds/department). In this way, 360 adult three-spined sticklebacks (Gasterosteus aculeatus) were caged for 28 days in these six ponds before biomarker analyses (immune system, antioxidant system, biometry, histology, DNA integrity, etc.). Ponds receiving uranium mine tailings presented higher concentrations of uranium, manganese and aluminum, especially for the Haute-Vienne Department. This uranium contamination could explain the higher bioaccumulation of this metal in fish caged in Pontabrier and Saint-Pierre Ponds. In the same way, many fish biomarkers (antioxidant and immune systems, acetylcholinesterase activity and biometric parameters) were impacted by this environmental exposure to mine tailings. This study shows the interest of caging and the use of a multi-biomarker approach in the study of a complex metallic contamination.

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Acknowledgments

The authors are deeply grateful to the owners of the different ponds for having allowed this environmental study. R. Amara, E. Kerambrun, K. Gombeau, S. Pierrisnard, D. Orjollet, V. Camilleri, N. Piasecki, M. Blachon and A. Bertrand are acknowledged for their help with field experiments and laboratory analyses. Special thanks to S. Frelon for its strong participation in metal analyses and advice. This work was partly supported by IRSN and the financial support of the 181 DRC 46 Program of the French Ministry for Ecology and Sustainable Development. The authors are grateful to International Science Editing for their help in correcting the English form of this paper.

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Authors and Affiliations

  1. Institut de Radioprotection et de Sûreté Nucléaire (IRSN), PRP-ENV/SERIS/LECO, Centre de Cadarache, 13115, Saint-Paul-Lez-Durance, France

    Antoine Le Guernic, Isabelle Cavalié, Christelle Adam-Guillermin & Béatrice Gagnaire

  2. Institut National de l’Environnement Industriel et des Risques (INERIS), UMR-I 02 (INERIS, Université de Reims Champagne-Ardenne, Université du Havre) SEBIO (Stress Environnementaux et Biosurveillance des milieux aquatiques), BP 2, 60550, Verneuil-en-Halatte, France

    Antoine Le Guernic, Wilfried Sanchez, Anne Bado-Nilles, Olivier Palluel, Cyril Turies, Edith Chadili & Jean-Marc Porcher

  3. Université de Reims Champagne-Ardenne, UMR-I 02 (INERIS, Université de Reims Champagne-Ardenne, Université du Havre) SEBIO (Stress Environnementaux et Biosurveillance des milieux aquatiques), Moulin de la Housse, BP 1039, 51687, Reims, France

    Antoine Le Guernic, Laurence Delahaut, Alain Geffard & Stéphane Betoulle

Authors
  1. Antoine Le Guernic
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  2. Wilfried Sanchez
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  3. Anne Bado-Nilles
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  4. Olivier Palluel
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  6. Edith Chadili
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  7. Isabelle Cavalié
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  8. Laurence Delahaut
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  9. Christelle Adam-Guillermin
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  11. Alain Geffard
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  12. Stéphane Betoulle
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  13. Béatrice Gagnaire
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Corresponding author

Correspondence to Antoine Le Guernic.

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The authors declare that they have no conflict of interest.

Ethical approval

This experiment was conducted in accordance with the European Commission’s recommendation 2007/526/EC on revised guidelines for the accommodation and care of animals used for experimental and other scientific purposes. The registration number for ethics of INERIS Laboratory is the B60-769-02. For sampling, to avoid bias in the immune responses, no anesthetic overdose can be used for euthanasia of sticklebacks. Indeed, in the 2010/63/EU Directive of the European Parliament and the 22 September 2010 Council about the protection of animals used for scientific purposes, this option is envisaged “if anesthesia is incompatible with the purpose of the procedure”. Therefore, sticklebacks were rapidly sacrificed by cervical dislocation followed by destruction of the brain. This method has been approved by the Committee No. 96-CREMEAP (Regional Ethics Committee in Animal Experimentation of Picardy).

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Le Guernic, A., Sanchez, W., Bado-Nilles, A. et al. In situ effects of metal contamination from former uranium mining sites on the health of the three-spined stickleback (Gasterosteus aculeatus, L.). Ecotoxicology 25, 1234–1259 (2016). https://doi.org/10.1007/s10646-016-1677-z

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  • DOI: https://doi.org/10.1007/s10646-016-1677-z

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