Collapse of a fish population after exposure to a synthetic estrogen

Karen A. Kidd; Paul J. Blanchfield; Kenneth H. Mills; Vince P. Palace; Robert E. Evans; James M. Lazorchak; Robert W. Flick

doi:10.1073/pnas.0609568104

New Research In

Edited by Deborah Swackhamer, University of Minnesota, Minneapolis, MN, and accepted by the Editorial Board March 29, 2007 (received for review October 27, 2006)

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 17β-estradiol (E2)], the synthetic estrogen used in birth-control pills [17α-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·L⁻¹) of the potent 17α-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.

Footnotes

^†To whom correspondence should be sent at the present address:
Canadian Rivers Institute and Biology Department, University of New Brunswick, Saint John, New Brunswick, Canada E2E 4P1.
E-mail: kiddk{at}unbsj.ca
Author contributions: K.A.K., P.J.B., K.H.M., and V.P.P. designed research; K.A.K., P.J.B., K.H.M., V.P.P., R.E.E., and J.M.L. performed research; P.J.B., K.H.M., V.P.P., R.E.E., J.M.L., and R.W.F. analyzed data; and K.A.K., P.J.B., K.H.M., V.P.P., R.E.E., J.M.L., and R.W.F. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. D.S. is a guest editor invited by the Editorial Board.
Abbreviations:
CPUE,
catch-per-unit-effort;
E2,
17β-estradiol;
EE2,
17α-ethynylestradiol;
VTG,
vitellogenin.
Freely available online through the PNAS open access option.
© 2007 by The National Academy of Sciences of the USA