Lifestyle and Environment · Environmental Exposures

Collapse of a fish population after exposure to a synthetic estrogen

Kidd KA, Blanchfield PJ, Mills KH, Palace VP, Evans RE, Lazorchak JM, Flick RW

Proceedings of the National Academy of Sciences of the United States of America, 2007
DOI 10.1073/pnas.0609568104 PMID 17517636 PMC PMC1874224

RRM Academy Synopsis

Synthetic estrogen nearly wiped out a lake's fathead minnows

A whole-lake experiment found that synthetic estrogen led to near extinction of fathead minnows. Researchers in Ontario added 17α-ethynylestradiol, the estrogen used in birth-control pills, to one lake for 3 years and compared it with two untreated lakes. Males in the treated lake were feminized, and the population collapsed in fall 2002 as young minnows disappeared.

Key Findings

  • Seven weeks into the additions, males in the treated lake produced vitellogenin, a protein females normally make, and the response held in each of the 3 years of additions.
  • All males collected in the first spring after additions had delayed sperm development, widespread fibrosis, and malformed tubules in the testes.
  • In spring 2003, four of nine males had testes holding primary-stage oocytes, a condition called intersex.
  • Catch per unit effort in trap nets fell steadily, from 180 ± 48 and 50 ± 43 in the pre-addition years to 0.1 ± 0.01 by the fifth year.
  • The population collapsed in fall 2002 through a loss of young-of-the-year. Reproductive failure continued 2 more years after additions stopped, though a few small fish were caught each year.

Interpretation

The Experimental Lakes Area study is a whole-lake field experiment. One lake received synthetic estrogen for 3 years. Two nearby lakes served as references, and fish were sampled for 2 years before and 2 years after the additions. The study examined fish in one treated lake. Fathead minnow live about 4 years in these lakes and few pass age 2, so the authors report that failed breeding in 2 straight years causes catastrophic drops in numbers. Longer-lived pearl dace in the same lake had not yet shown reproductive failure, and the authors suggest lifespan shapes a species' risk.

RRM Context

The authors call the estrogen in birth-control pills one of the more potent estrogens in city wastewater. Restorative reproductive medicine looks for root causes, and this experiment found one in the environment. A synthetic estrogen changed fish breeding at every level measured, from the cell to the whole population.

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.

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Lifestyle and Environment › Environmental Exposures › Endocrine Disrupting Chemicals
Karen A Kidd, Paul J Blanchfield, Kenneth H Mills, Vince P Palace, Robert E Evans, James M Lazorchak, Robert W Flick
K Kidd, P Blanchfield, Ken Mills, K Mills, V Palace, Bob Evans, Rob Evans, Bobby Evans, R Evans, Jim Lazorchak, Jimmy Lazorchak, J Lazorchak, Bob Flick, Rob Flick, Bobby Flick, R Flick
PMID 17517636 17517636 DOI 10.1073/pnas.0609568104 10.1073/pnas.0609568104 Kidd et al. 2007, Kidd 2007