USGS - Pesticide National Synthesis Project Pesticides Report

Reconnaissance of 17ß-Estradiol, 11-Ketotestosterone, Vitellogenin, and Gonad Histopathology in Common Carp of United States Streams: Potential for Contaminant-Induced Endocrine Disruption

By Steven L. Goodbred, Robert J. Gilliom, Timothy S. Gross, Nancy P. Denslow, Wade L. Bryant, and Trenton R. Schoeb

U.S. Geological Survey Open-File Report 96-627

Introduction

Interest in endocrine disruption---the effects of environmental contaminants on the endocrine system of animals---has increased markedly over the past 20 years. McLachlan (1980) initiated a debate on the effects of environmental contaminants on the endocrine system. Based on a recent symposium on endocrine disruption, Colborn and Clement (1992) concluded that "a large number of manmade chemicals that have been released into the environment * * * have the potential to disrupt the endocrine systems of animals including humans." At least 45 chemicals have been identified as potential endocrine-disrupting contaminants (Colborn and others, 1993), including industrial contaminants (such as dioxins and polychlorinated biphenyls [PCBs]), insecticides (such as DDT and carbaryl), and herbicides (such as dichlorophenoxy acetic acid [2,4D] and atrazine).

Injury to endocrine function by environmental contaminants is potentially debilitating to a variety of physiological systems. The endocrine system in animals consists of glands that produce hormones that enter the bloodstream to maintain physiological homeostasis. This is accomplished through regulation of immune, metabolic, morphogenic, neural, and reproductive functions. Previous studies have found correlations between specific impairments of reproductive activity and elevated tissue concentrations of xenobiotic agents (Hose and others, 1989 and Tillitt and others, 1992). The reproductive injuries reported to date include reduced fertility, hatchability, and viability of offspring; impaired reproductive hormone activity; and altered sexual development and behavior. There are also reports of slow growth, atrophy, and lower rates of metabolic activity (Colborn and Clement, 1992). Abnormalities of these types may be caused by disruption of normal endocrine function either before or after hormone interactions with specific cellular receptors. Though some cause and effect relations are known, the underlying mechanisms of endocrine disruption are poorly understood (Colborn and Clement, 1992; Bern, 1992; McLachlan and others, 1992). Reproductive impairment often is correlated with altered or decreased circulating con-centrations of sex steroid hormones or other critical reproductive factors (Colborn and Clement, 1992; Mayer and others, 1992). The cause-effect linkage between xenobiotic compounds and observed effects is, however, clouded by limited knowledge of the biochemical effects of these compounds in tissues, limited data on exposure to contaminants, and incon-sistent data for both contaminants and their effects in terms of analytical methodologies, sampling media, species, age, and sex (Swain and others, 1992).

Studies of aquatic wildlife that are directly exposed to contaminants in our waterways, and thus act as sentinels, often provide early indications of potential environmental problems. Recent studies have found evidence of endocrine disruption in fish from a variety of contaminated ecosystems. Fitzsimmons (1990) reported depressed steroid hormone concentrations in male lake trout (Salvelinus namaycush) from Lake Ontario as compared to those from less polluted sites. Systemic concentrations of 11-ketotestosterone, a sex steroid hormone, were inversely proportional to contaminant body burdens. A similar relation between 11-ketotestosterone and contaminant body burden also was reported for coho salmon (Oncorhynchus kisutch) by Leatherland (1992). In addition, Munkittrick and others (1992) reported depressed gonadal sex steroids, as well as delayed sexual maturity, reduced gonad size and altered secondary sex characteristics in white suckers (Catostomus commersoni) and lake whitefish (Coregonus clupeaformis) from Lake Superior in the vicinity of effluents from a bleach kraft pulp mill. Kraft mill effluents also have been reported in association with masculinization of female Poeciliid fish (Davis and Bortone, 1992).

These studies have used sex steroid concentra-tions as biomarkers of contaminant exposure. Monitoring of sex steroid hormones, such as 17ß-estradiol and 11-ketotestosterone in fish, may be useful for the assessment of biological effects and exposure to environmental contamination (Mayer and others, 1992). In addition to sex steroid hormones, vitellogenin, an estrogen-inducible phosphoprotein, also can be used as a biomarker of contaminant exposure in fish and in other oviparous vertebrates. Vitellogenin is normally synthesized by the liver of female oviparous vertebrates during oogenesis (Specker and Sullivan, 1994) and is a precursor of egg yolk. Recent reports have documented vitellogenin synthesis in both male common carp (Cyprinus carpio) and male rainbow trout (Oncorhynchus mykiss) in streams impacted by sewage effluent (Purdom and others, 1994; Folmar and others, 1996). The use and development of these and other biomarkers of potential endocrine disruption in fish are important for detecting and monitoring poten-tial adverse effects of environmental contaminants on aquatic organisms.

The purpose of this paper is to present results of a reconnaissance of selected biomarkers of potential endocrine disruption in fish from streams throughout the United States. The primary objectives of the study were: (1) to determine if endocrine disruption is potentially widespread in fish of United States streams; (2) to evaluate potential relations between endocrine disruption and contaminant levels; and (3) to aid in determining whether further study of this issue is needed and what type of investigations are likely to be most useful. The study was designed to sample and analyze common carp from streams with a wide range of environmental settings and contaminant levels throughout the United States. Most of the 23 streams and 2 impoundments sampled are established water-quality sites of the National Water Quality Assessment (NAWQA) Program (Gilliom and others, 1995), where levels of a variety of contaminants have been characterized. The study was a collaboration of the National Biological Service (now the Biological Resources Division of the U.S. Geological Survey), the U.S. Geological Survey, and the University of Florida's Biotechnologies for the Ecological, Evolutionary, and Conservation Sciences Program.

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