Field surveys reveal the presence of anti-androgens in an effluent-receiving river using stickleback-specific biomarkers

This study was designed to assess whether the removal of endocrine disrupting chemicals (EDCs) and other substances from a Waste Water Treatment Works (WWTW) effluent (receiving water: R. Ray, Swindon, UK) by granular activated carbon (GAC) affected biomarkers of exposure to EDCs [vitellogenin (VTG) and spiggin] in male and female three-spined sticklebacks in the receiving water. A nearby river (R. Ock), with a negligible effluent loading, was used as a control. On each river fish were sampled from four sites on five occasions both before and after remediation of the WWTW effluent. The results show for the first time in a UK field study a clear seasonality of blood VTG concentrations in wild male fish, following closely the VTG profile in female fish from both rivers. VTG levels in male fish from the R. Ray were significantly reduced after the GAC installation. However, VTG levels in males from the control sites also varied significantly across the same period, reducing the significance of this finding. A laboratory exposure to oestradiol (using site-specific lower and upper levels of oestrogenic activity) failed to elevate VTG concentrations in male sticklebacks suggesting that concentrations in the effluent, even prior to remediation, may not have exceeded a critical sensitivity threshold. Most importantly, a significant increase in female kidney spiggin content (a highly specific biomarker of xeno-androgen exposure) occurred in fish in the R. Ray after the GAC installation to levels comparable with those in fish from the control river. The significance of this finding is strengthened by the fact that during the pre-remediation period in the R. Ray, female spiggin levels increased with increasing distance from the WWTW. Our results provide the first in vivo evidence of the presence of anti-androgens in a U.K. WWTW effluent. To our knowledge this is the first U.K.-based comprehensive field study on the effects of a WWTW upgrade on biomarkers of EDC exposure using a sentinel fish species and our findings confirm the value of the stickleback as a model species for studying EDCs both in the laboratory and in the wild.