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Exposure of zebrafish to an environmental mixture of persistent organic pollutants triggers an increase in anxiety-like syndrome but does not affect boldness in unexposed offspring

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Abstract

Polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) are persistent organic pollutants (POPs) that are present as complex mixtures in all environmental compartments, including aquatic ecosystems. However, little is known about the effects of such complex mixtures on teleost behaviour. In this study, zebrafish (Danio rerio) were chronically exposed to an environmentally relevant mixture (MIX) containing 22 PCB and 7 PBDE congeners through diet from 5 days post fertilization onwards. MIX-exposed F0 fish produced offspring (F1 and F2 generations) that were fed using plain food and grown until adulthood. In each generation, five behavioural traits (i.e. boldness, activity, sociality, exploration and anxiety) were evaluated by the mean of different experimental set-ups. Two distinct behavioural syndromes were identified: boldness, positively correlated to activity and exploration; and anxiety, associated with low sociality. F0 fish did not display any behavioural disruption resulting from POP exposure whereas F1 MIX fish were bolder than fish from other generations but did not differ significantly from F1 controls. F2 MIX fish displayed a higher anxiety syndrome than F2 controls. This is of particular importance since such behavioural changes in offspring generations may have persistent ecological consequences, may affect fitness and hence cause detrimental effects on wild fish populations exposed to POP mixtures.

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Data availability

The datasets used during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We thank Christine Jarc, Lucette Joassard and Didier Leguay from Ifremer (LRH) for their valuable help in running this long-lasting experiment and Véronique Loizeau, Catherine Munschy, Nathalie Olivier, Karine Héas-Moisan and Xavier Philippon from Ifremer (LBCO) for their realization of PCB and PBDE analyses and interpretation. The authors thank Emilie Levavasseur (emilie.levavasseur@laposte.net) for the zebrafish drawing in Fig. 1. We also thank the three anonymous reviewers for helpful comments of the previous version of the manuscript.

Funding

This work was supported by the French National Research Agency, project Fish’N’POPs (ANR-13-CESA-020). SA received a PhD grant from Ifremer to conduct this research.

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Authors

Contributions

Conceptualization: SA, XC and MLB. Data curation: SA, MB and XC. Formal analysis: SA and XC. Funding acquisition: XC and MLB. Investigation: SA, MB and XC. Methodology: SA, XC and MLB. Project administration: XC and MLB. Supervision: XC and MLB. Visualization: SA. Writing — original draft: SA.

Corresponding author

Correspondence to Sébastien Alfonso.

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Ethics approval and consent to participate

The study was conducted under the approval of the Animal Care Committee of Poitou–Charentes # 84 COMETHEA (France) under the project authorization number CE2012-23 and followed the recommendations of the Directive 2010/63/EU.

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Not applicable.

Competing interests

The authors declare no competing interests.

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Responsible Editor: Bruno Nunes

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Alfonso, S., Blanc, M., Cousin, X. et al. Exposure of zebrafish to an environmental mixture of persistent organic pollutants triggers an increase in anxiety-like syndrome but does not affect boldness in unexposed offspring. Environ Sci Pollut Res 30, 21439–21452 (2023). https://doi.org/10.1007/s11356-022-23689-z

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  • DOI: https://doi.org/10.1007/s11356-022-23689-z

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  1. Sébastien Alfonso