An environmental oestrogen disrupts fish population dynamics through direct and transgenerational effects on survival and fecundity

Abstract

Summary Increased need for water and projected declines in precipitation due to climate change could leave waterways increasingly dominated by wastewater effluent. Understanding how components of wastewater influence fish populations is necessary for effective conservation and management. Despite research demonstrating effects of oestrogens, such as 17α‐ethynylestradiol (EE2), on fish physiology and population failure, the generality of population responses is uncertain and the underlying mechanisms affecting population declines are unknown. EE2 is the steroid oestrogen in human contraceptive pills and has been measured up to 11 ng L−1 in the environment. We identify disrupted population dynamics due to direct and transgenerational effects on survival and fecundity. We conducted a year‐long study on three generations of fathead minnows Pimephales promelas Rafinesque in aquatic mesocosms and laboratory aquaria. We added environmentally relevant concentrations of EE2 daily using a static renewal, which approximates a pulsed exposure that fish experience in natural systems. EE2 (3·2 ng L−1) reduced F0 male survival to 17% (48% lower than controls) and juvenile production by 40% compared to controls. F1 fish continuously exposed to EE2 failed to reproduce, and reproduction of the F1 transferred to clean water was 70–99% less than controls. F2 larval survival, exposed only as germ cells in their parents, was reduced by 51–97% compared to controls. The indirect effect on F2 survival suggests the possibility of transgenerational effects of EE2. Synthesis and applications. Our results suggest that fish populations exposed to environmentally relevant 17α‐ethynylestradiol (EE2) concentrations may not recover from exposure. Management of short‐lived highly fecund fishes should be prioritized to protect fish from the embryo through gonadal differentiation. Reducing effluent will not be possible in many situations; hence, conservation of breeding and rearing habitat in unpolluted tributaries or reaches is needed. Additionally, resource managers could enhance habitat connectivity in rivers to facilitate immigration. Finally, investment in advanced wastewater processing technology should improve removal of bioactive chemicals such as EE2. Our results provide a baseline for regulatory agencies to consider when assessing the ecological effects of environmental oestrogens, and our approach to evaluating population‐level effects could be widely applied to other contaminants.