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Human Contraceptive Gestodene Affects Fish Reproductive Behavior

Four photos depecting effects of exposure of fathead minnows to gestodene
Control fathead minnows (Pimephales promelas) depicted on top row with male under the breeding tile (left) and fertilized eggs deposited on tile (on right, shown standing so eggs are visible). On bottom row, gestodene exposed fish behavior was altered and egg deposition arrested.
Adapted with permission from Frankel, T.E., Meyer, M.T., Kolpin, D.W., Gillis, A.B., Alvarez, D.A., and Orlando, E.F., 2016, Exposure to the contraceptive progestin, gestodene, alters reproductive behavior, arrests egg deposition, and masculinizes development in the fathead minnow (Pimephales promelas): Environmental Science and Technology, v. 50, no. 11, p. 5991-5999, doi:10.1021/acs.est.6b00799. Copyright 2016 American Chemical Society, Photos taken by Edward F. Orlando, University of Maryland.

Short-term laboratory exposure of adult fathead minnows to the human contraceptive progestin, gestodene (GES), at environmentally relevant concentrations induced rapid and negative effects on reproductive health and suggests that wild fish may be similarly affected.

There is a continuing concern regarding the effects of endocrine disrupting chemicals (EDCs) that enter aquatic ecosystems from a variety of sources, including wastewater treatment plants, agricultural runoff, and paper mill plants, and their potential effect on the reproductive health of aquatic organisms. Synthetic hormones are one class of chemicals that are designed to alter endocrine function as in the case of GES, which is used as a human contraceptive. Thus far, research on the exposure and effects of synthetic hormones has mainly focused on the reproduction of aquatic vertebrates including changes to circulating hormone concentrations, egg deposition or sperm characteristics, changes in ovarian or testicular tissues, and development of secondary sexual characteristics in fishes. Although behavior has been recognized as a sensitive endpoint that is critical for successful reproduction, comparatively few studies have examined EDC exposure effects on behavior in fish.

In this study, scientists investigated the exposure effects of GES on reproductive behaviors of fathead minnows (Pimephales promelas) while also retaining the more traditional measures of biological endpoints (for example, the number of eggs deposited and the development of secondary sex characteristics). Scientists intentionally selected an 8-day exposure period due to their interest in examining the potential short-term effects of GES exposure on behavior. Fish were exposed to two levels of GES to bracket environmental concentrations of similar synthetic hormones (10 and 100 nanograms per liter [ng/L] and controls) using a flow-through system in the laboratory.

This research documents that short-term exposure of adult fathead minnows to GES at environmentally relevant concentrations induced rapid and negative effects on reproductive behavior, egg deposition, and sexual development. Exposure to GES caused rapid changes in normal reproductive behavior of both male and female fathead minnows. After only 1 day, males exposed to GES were more aggressive and less interested in courtship and mating, and exposed females displayed less female courtship behavior. In contrast to behavioral changes, GES exposure only affected the development of secondary sex characteristics in female fathead minnows (females developed characteristics typical in males). Consistent with previous research, GES exposure negatively affected the number of eggs deposited by fathead minnows (63- and 95-percent declines in the number for eggs in the 10- and 100-ng/L treatment groups, respectively). No changes in ovarian or testicular tissue histology were observed. The study results suggest that effects on egg deposition measured in this short-term study are primarily due to altered reproductive behavior. The rapid changes in behavior and decreased egg production from GES exposure suggest that exposed populations of wild fish may be similarly influenced.

The study was funded by the U.S. Geological Survey (USGS) Toxic Substances Hydrology Program, as well as the National Institutes of Water Resources Grant (2014MD321G, to EFO), the Morris Animal Foundation Grant (D14ZO-010 to EFO), and the University of Maryland.

Reference

Frankel, T.E., Meyer, M.T., Kolpin, D.W., Gillis, A.B., Alvarez, D.A., and Orlando, E.F., 2016, Exposure to the contraceptive progestin, gestodene, alters reproductive behavior, arrests egg deposition, and masculinizes development in the fathead minnow (Pimephales promelas): Environmental Science and Technology, v. 50, no. 11, p. 5991-5999, doi:10.1021/acs.est.6b00799.

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