From cells to recapture rates: responses and recovery of a wild fish after an experimental exposure to a widely used herbicide

Abstract

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 2 weeks, but not at 3 months 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 3 months, 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.