Freshwater environments are biodiversity hotspots under multiple pressures, including pesticide exposure. S-metolachlor, a widely used herbicide, can induce genotoxic, cytotoxic and physiological effects in captive fish, but we have a limited understanding of the effects of exposure to S-metolachlor in free-living vertebrates. We carried out an original field experiment using integrative approaches across biological levels and temporal scales. The implantation of slow-release implants, an approach to mimic increasing exposure to S-metolachlor of wildlife in realistic multistress conditions, was coupled to a capture-mark-recapture monitoring of bullheads (Cottus perifretum) living in an agriculturally impacted stream. Thanks to our long-term monitoring programme, we evidenced high levels of metolachlor and its metabolites (metolachlor ESA and metolachlor OXA) in water bodies with strong monthly variations. S-metolachlor levels did not differ between treated and control fish and were moderate in bullhead tissues, likely because of xenobiotic metabolism and excretion. S-metolachlor exposure increased erythrocyte abnormalities and the neutrophil/lymphocyte (N/L) ratios. These cellular and physiological damages were observed at 2weeks, but not at 3months after the manipulation. This suggests a recovery, likely owing to cell turnover. We also found an increase of body mass of treated fish compared to control fish, and this mass gain persisted at 3months, suggesting obesogenic effects of S-metolachlor. Antioxidant levels, telomere length and recapture rate were not affected by the experimental treatment. In conclusion, we provide evidence for transient and specific cellular alterations induced by low concentrations of S-metolachlor and long-term mass gain in a wild vertebrate. This study paves the way for integrative field experiments to better understand the impacts of pollutants on fish populations.
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