Collapse of a fish population after exposure to a synthetic estrogen

Abstract

Municipal wastewaters are a complex mixture containing estrogens and estrogen mimics that are known to affect the reproductive health of wild fishes. Male fishes downstream of some wastewater outfalls produce vitellogenin (VTG) (a protein normally synthesized by females during oocyte maturation) and early-stage eggs in their testes, and this feminization has been attributed to the presence of estrogenic substances such as natural estrogens [estrone or 17beta-estradiol (E2)], the synthetic estrogen used in birth-control pills [17 alpha-ethynylestradiol (EE2)], or weaker estrogen mimics such as nonylphenol in the water. Despite widespread evidence that male fishes are being feminized, it is not known whether these low-level, chronic exposures adversely impact the sustainability of wild populations. We conducted a 7-year, whole-lake experiment at the Experimental Lakes Area (ELA) in northwestern Ontario, Canada, and showed that chronic exposure of fathead minnow (Pimephales promelas) to low concentrations (5-6 ng x L(-1)) of the potent 17 alpha-ethynylestradiol led to feminization of males through the production of vitellogenin mRNA and protein, impacts on gonadal development as evidenced by intersex in males and altered oogenesis in females, and, ultimately, a near extinction of this species from the lake. Our observations demonstrate that the concentrations of estrogens and their mimics observed in freshwaters can impact the sustainability of wild fish populations.

Fig. 1.

Mean ± SE (n = 4–7) VTG concentrations in whole-body homogenates of male (Lower) and female (Upper) fathead minnow captured in 1999–2003 from reference Lakes 114 and 442 and from Lake 260 before and during additions of 5–6 ng·L⁻¹ of EE2 (low catches of fish in Lake 260 in 2004 and 2005 did not allow for these analyses in the latter 2 years of the study).

Fig. 2.

Gonadal tissue sections from fathead minnow sampled in early May 2003. (A) Ovary from reference Lake 442 with small, dark, primary-stage oocytes situated between cortical alveolar-stage oocytes and large vitellogenic oocytes. (B) Ovary from EE2-amended Lake 260 demonstrating an atretic follicle (arrow). (C) Testis from reference Lake 442. (D) Testis from EE2-amended Lake 260 demonstrating intersex; arrows indicate primary-stage oocytes among the remnants of testicular tissue. (Scale bars: A, B, 300 μm; C, D, 80 μm.)

Fig. 3.

Length frequency distributions of fathead minnow captured in trap nets in reference Lake 442 (A) and Lake 260 (B) (amended with 5–6 ng·L⁻¹ of EE2 in 2001–2003) during the fall of 1999–2005. Distributions for each fall have been standardized to 100 trap-net days. Mean ± SE daily trap-net CPUE data for adults and juveniles for the fall catches are shown in the panels.