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Acclimation capacity of the three-spined stickleback (Gasterosteus aculeatus, L.) to a sudden biological stress following a polymetallic exposure

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Abstract

To get closer to the environmental reality, ecotoxicological studies should no longer consider the evaluation of a single pollutant, but rather combination of stress and their interaction. The aim of this study was to determine if responses of a fish to a sudden biological stress could be modified by a prior exposure to a chemical stress (a polymetallic contamination). For this purpose, in situ experiment was conducted in three ponds in the Haute-Vienne department (France). One pond was chosen for its high uranium concentration due to uranium mine tailings, and the two other ponds, which were not submitted to these tailings. Three-spined sticklebacks (Gasterosteus aculeatus) were caged in these ponds for 14 days. After this period, fish were submitted to a biological stress, exerted by lipopolysaccharides injection after anesthesia, and were sacrificed 4 days after these injections for multi-biomarkers analyses (leucocyte viability, phagocytic capacity and reactive oxygen species production, antioxidant peptide and enzymes, lipid peroxidation and DNA damage). The pond which received uranium mine tailings had higher metallic concentrations. Without biological stress, sticklebacks caged in this pond presented an oxidative stress, with increasing of reactive oxygen species levels, modification of some parts of the antioxidant system, and lipid peroxidation. Caging in the two most metal-contaminated ponds resulted in an increase of susceptibility of sticklebacks to the biological stress, preventing their phagocytic responses to lipopolysaccharides and modifying their glutathione contents and glutathione-S-transferase activity.

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Acknowledgments

The authors are deeply grateful to the owners of the different ponds for having allowed this experiment. S. Pierrisnard, D. Orjollet, V. Camilleri, L. Carasco and S. Frelon are acknowledged for their help with laboratory analyses. This work was partly supported by IRSN, the financial support of the 181 DRC 46 program of the French Ministry for Ecology and Sustainable Development, and the ECCOREV research federation.

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Authors and Affiliations

  1. UMR-I 02 SEBIO (Stress Environnementaux et Biosurveillance des milieux aquatiques), Institut National de l’Environnement Industriel et des Risques (INERIS), BP 2, 60550, Verneuil-En-Halatte, France

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

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

    Antoine Le Guernic, Magali Floriani, Claire Della Vedova, Isabelle Cavalié, Christelle Adam-Guillermin & Béatrice Gagnaire

  3. UFR Sciences Exactes et Naturelles, UMR-I 02 SEBIO, Université de Reims Champagne-Ardenne (URCA), Campus Moulin de la Housse, B.P. 1039, 51687, Reims, France

    Antoine Le Guernic, Alain Geffard & Stéphane Betoulle

Authors
  1. Antoine Le Guernic
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  2. Wilfried Sanchez
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  3. Olivier Palluel
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  4. Anne Bado-Nilles
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  14. Béatrice Gagnaire
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Correspondence to Antoine Le Guernic.

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Ethical statement

These experiments were 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 anaesthetic 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).

Appendices

Annex 1

See Table 5.

Table 5 Effects of LPS injections on fish biomarkers obtained during the preliminary experiment
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Annex 2

See Fig. 5.

Fig. 5
figure 5

Temperature (°C) inside cages according to ponds and to experiment date. Temperature was recorded each hour using probes

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Annex 3

See Fig. 6.

Fig. 6
figure 6

Transmission electron microscopy observations of leucocyte phagocytosis from stickleback spleen. Black circles represent fluorescent microbeads ingested. a, b and c: granulocytes; d: lymphocyte

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Le Guernic, A., Sanchez, W., Palluel, O. et al. Acclimation capacity of the three-spined stickleback (Gasterosteus aculeatus, L.) to a sudden biological stress following a polymetallic exposure. Ecotoxicology 25, 1478–1499 (2016). https://doi.org/10.1007/s10646-016-1699-6

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