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) Environmental Health Program (Toxic Substances Hydrology and Contaminant Biology) of the Ecosystems Mission Area, 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.
See below for related science.
Immunomodulation Science Team
Fishing and Hunting Integrated Science Team
Synthetic Progestin Affects Fish Reproductive Development and Behavior in Laboratory Exposure Study
Contaminants of Emerging Concern in the Environment
Complex Mixtures, Complex Responses—Using Comprehensive Approaches to Assess Pharmaceutical Effects on Fish
- Overview
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.
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. 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) Environmental Health Program (Toxic Substances Hydrology and Contaminant Biology) of the Ecosystems Mission Area, 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.
- Science
See below for related science.
Immunomodulation Science Team
The Immunomodulation Integrated Science Team focuses on contaminant and pathogen exposures in the environment that might influence the immune systems of wildlife and the connection to their shared environment with humans. In collaboration with public-health officials, the Team also addresses potential human-health risks stemming from similar exposures. If actual risks are identified, this Team...Fishing and Hunting Integrated Science Team
The Fishing and Hunting integrated science team focuses on contaminant and pathogen exposures in the environment that could impact the presence and vitality of fish and wildlife populations that drive commercial, recreational and subsistence activities such as hunting and fishing. If actual risks are identified this project will inform how to economically and effectively minimize risk by providing...Synthetic Progestin Affects Fish Reproductive Development and Behavior in Laboratory Exposure Study
Scientists conducted laboratory experiments on levonorgestrel (a synthetic progestin) and observed differential effects to males (reproductive behavior) and females (masculinization) of eastern mosquitofish (Gambusia holbrooki).Contaminants of Emerging Concern in the Environment
The USGS is conducting source-to-receptor research on a broad range of chemical and microbial contaminants including pharmaceuticals, personal care products, pathogens, antibiotic resistant genes, and natural toxins that are not commonly considered in environmental research but have the potential to impact environmental health.Complex Mixtures, Complex Responses—Using Comprehensive Approaches to Assess Pharmaceutical Effects on Fish
The occurrence of complex mixtures of prescription pharmaceuticals in streams and rivers around the globe has raised concerns about potential unintended adverse effects on aquatic organisms. The deleterious effects (for example, alteration of fish behavior) observed in this study confirm that effluents containing pharmaceuticals can adversely affect fish in ways that are central to sustaining... - Publications