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Effects of a Synthetic Estrogen on Aquatic Populations: a Whole Ecosystem Study

Principle Investigator: Karen Kidd
Freshwater Institute, Fisheries and Oceans Canada

Contributing Partner(s):
Scott Brown, Environment Canada
Mark McMaster, Environment Canada
David Findlay, Department of Fisheries and Oceans
Jack Klaverkamp, Department of Fisheries and Oceans
Vince Palace, Department of Fisheries and Oceans
Michael Paterson, Department of Fisheries and Oceans
David Graham, University of Kansas
Karsten Liber, University of Saskatchewan
Glen Van Der Kraak, University of Guelph

Why Project Was Undertaken: Alterations in sexual development, growth and reproduction occurs in fish exposed to estrogens and other hormone-acting substances in municipal sewage waste water. Male fish exposed to estrogens become feminized, produce egg proteins, have smaller reproductive tissues and in severe cases develop eggs. Estrogens used in hormone replacement therapy or birth control are not removed from treated waste water and are released into the environment. Long-term impacts of estrogens on fish reproduction and aquatic ecosystem health is unknown.

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How Project Was Conducted: The overall objective of TSRI Project # 94 was to conduct a whole-lake study the effects of synthetic 17 -ethynylestradiol, used in birth control pills, on aquatic organisms and populations. The synthetic estrogen was continually added to one lake at the Fisheries and Oceans Canada research station, the Experimental Lakes Area, Ontario to maintain an average concentration of 6.1 ppt (parts per trillion) estrogen in the surface water. Responses to estrogen exposure were studied in individual fish (lake trout, sucker and minnows) and their populations, as well as in tadpoles, bacteria, algae, leeches, zooplankton and sediment invertebrates.

What Was Found and Conclusions: Effects observed in fish were similar in type and severity to those seen in wild fish downstream of municipal waste water treatment plants. Male fish produced high levels of egg protein precursors, had delays in development of reproductive tissues, and in one species of minnow produced eggs. Female fish had delays in reproductive development and changes in the amount and timing of egg protein production. Kidneys and livers were also affected in fish. After about 6 months, there were no apparent changes in size of fish populations, fish growth rates, male to female ratios, or survival of offspring. There were no apparent affects on tadpole growth, development and sex ratios but a low number of males had eggs. Affects on sex ratio and egg production were observed in zooplankton populations. No effects were found on the numbers of bacteria, algae and leeches. Monitoring of the lake ecosystem will continue for three years following estrogen exposure to determine the long-term impacts on populations of fish and aquatic organisms.

Executive Summary

Municipal wastewater treatment plants (MWTP) discharge numerous contaminants into aquatic systems, and some of these chemicals are known or believed to act like hormones and interfere with the growth, reproduction and development of aquatic organisms. It is becoming increasingly apparent that male fish exposed to these effluents are becoming feminized due to the presence of natural and synthetic estrogens in the water. The potent synthetic estrogens excreted by women taking hormone replacement therapy or birth control pills are not completely broken down in the sewage treatment process and are discharged into waterways. The male fish exposed to these estrogens produce egg proteins, have smaller gonads and, in the more severe cases, develop eggs. Despite the growing evidence that fish are being impacted by chemicals that mimic estrogen, it is not known whether they can continue to successfully reproduce and maintain their population sizes. Also little is known about the effects of hormone mimics on the other components of the aquatic food web.

A whole-lake experiment was conducted at a Fisheries and Oceans Canada research station, the Experimental Lakes Area, in northwestern Ontario to examine the effects of a potent estrogen mimic on aquatic organisms and populations. In 1999 and 2000, background data on the fish, invertebrates, amphibians, bacteria and algae were collected from several lakes. During the summer of 2001, the synthetic estrogen used in birth control pills, 17 -ethynylestradiol, was added continuously to one lake to maintain low and environmentally-relevant concentrations in the water. Laboratory and field studies had previously demonstrated that this estrogen does not persist in the water, and can be degraded by bacteria naturally present in the sediments of the lake. The additions were done from the end of May until the end of October, and mean concentrations of the estrogen were 6.1 ng/L in the surface waters of the lake. We monitored the lake for responses of the individual fish (lake trout, sucker and minnows) and their populations, as well as changes in the tadpoles, bacteria, algae, leeches, zooplankton and benthic invertebrates as a result of the estrogen additions.

This study was successful at reproducing some of the impacts seen in fish downstream of MWTPs. Male fish from the estrogen-addition lake produced high concentrations of egg protein precursors, had developmental delays in their gonads and, in one species of minnow, produced eggs. Female fish exposed to the estrogen also showed delays in reproductive development and changes in the amount and timing of the egg protein production. The kidneys and livers were also impacted likely due to the atypical and high production of egg proteins in these fish. In the fall of 2001, we did not see any changes in the sizes of the fish populations, fish growth rates, the numbers of males versus females, and the survival of the offspring. It is likely that population- level responses of long-lived organisms will take longer to appear, and for this reason we are continuing to monitor the fish populations in this lake for 3 years following the estrogen additions.

Some impacts of estrogen additions were observed on the lower-trophic-level organisms. While there were no effects of the synthetic estrogen on tadpole growth, development and sex ratios, we did see a low incidence of males with eggs in the treated lake. After estrogen additions, one of the more predominant species of zooplankton had lower proportions of males, and females from several species of zooplankton produced fewer eggs. We did not see any impacts of the synthetic estrogen on bacteria and algae abundance. Growth rates and catches of leeches in the study lake were also similar during the estrogen additions to background and reference lake data.

In summary, results from this TSRI-funded study are being used as part of a longer-term experiment to determine the impacts of potent estrogen mimics on populations of fish and other aquatic organisms. To date, our results indicate that the experiment has been successful at reproducing the types and severity of impacts that estrogen mimics are having on fish downstream of MWTPs, and at demonstrating that synthetic estrogens do impact lower-trophic-level biota. These results will be linked to long-term monitoring of the fish populations in order to assess the ecosystem risks associated with discharges of estrogens into the aquatic environment. These results will be valuable to regulators in assessing the impacts of estrogen mimics released by MWTPs on aquatic populations and in determining whether emissions of these compounds need to be reduced.

PublicationsPublications in Scientific Journals Palace V.P., Wautier, K., Evans, R.E., Baron, C.L., Ranson, C., Klaverkamp, J.F., Kidd, K. 2001. Effects of 17~-estradiol exposure on metallothionein and fat soluble antioxidant vitamins in juvenile lake trout (Salvelinus namaycush). Bull. Environ Contam Toxicol. 66:591-596.

Palace, V.P., Dick, T.A., Evans, R.E., Wautier, K. Baron, C.L., Werner, J., Klaverkamp, J.F., Kidd, K.A. 2001. Altered metabolism of lipid soluble antioxidant vit amins in juvenile sturgeon expo sed to water borne ethynylestradiol. Environ. Toxicol. Chem. 20(10):2370-2376.

Palace, P., Evans, R.E., Wautier, K., Vandenbyllardt, L., Vandersteen, W., Kidd, K. 2002. Biochemical and physiological effects in wild fathead minnows from a lake experimentally treated with the synthetic estrogen, ethynylestradiol. Can. Jour. Water Quality. 37(3): 637-650.

Thesis Werner, J. Effects on environmental estrogens and metal exposure on metallothionein expression in tissues of wild lake trout and white sucker. University of Manitoba, Ph.D.