| Endocrine-Disrupting Effects of Cattle Feedlot Effluent on an Aquatic Sentinel Species, the Fathead Minnow Edward F. Orlando,1,2 Alan S. Kolok,3 Gerry A. Binzcik,1 Jennifer L. Gates,1 Megan K. Horton,3 Christy S. Lambright,4 L. Earl Gray, Jr.,4 Ana M. Soto,5 and Louis J. Guillette, Jr.1 1Department of Zoology, University of Florida, Gainesville, Florida, USA; 2Biology Department, St. Mary's College of Maryland, St. Mary's City, Maryland, USA; 3Department of Biology, University of Nebraska at Omaha, Omaha, Nebraska, USA; 4U.S. Environmental Protection Agency, Research Triangle Park, North Carolina, USA; 5Department of Anatomy and Cell Biology, Tufts University School of Medicine, Boston, Massachusetts, USA Abstract
Over the last decade, research has examined the endocrine-disrupting action of various environmental pollutants, including hormones, pharmaceuticals, and surfactants, in sewage treatment plant effluent. Responding to the growth of concentrated animal feeding operations (CAFOs) and the pollutants present in their wastewater (e.g., nutrients, pharmaceuticals, and hormones) , the U.S. Environmental Protection Agency developed a new rule that tightens the regulation of CAFOs. In this study, we collected wild fathead minnows (Pimephales promelas) exposed to feedlot effluent (FLE) and observed significant alterations in their reproductive biology. Male fish were demasculinized (having lower testicular testosterone synthesis, altered head morphometrics, and smaller testis size) . Defeminization of females, as evidenced by a decreased estrogen:androgen ratio of in vitro steroid hormone synthesis, was also documented. We did not observe characteristics in either male or female fish indicative of exposure to environmental estrogens. Using cells transfected with the human androgen receptor, we detected potent androgenic responses from the FLE. Taken together, our morphologic, endocrinologic, and in vitro gene activation assay data suggest two hypotheses: a) there are potent androgenic substance(s) in the FLE, and/or b) there is a complex mixture of androgenic and estrogenic substances that alter the hypothalamic-pituitary-gonadal axis, inhibiting the release of gonadotropin-releasing hormone or gonadotropins. This is the first study demonstrating that the endocrine and reproductive systems of wild fish can be adversely affected by FLE. Future studies are needed to further investigate the effects of agricultural runoff and to identify the biologically active agents, whether natural or pharmaceutical in origin. Key words: anabolic steroid hormones, aquatic ecosystem health, concentrated animal feeding operation (CAFO) , environmental androgens and estrogens, gene expression, HPG axis, hypothalamic-pituitary-gonadal axis, pharmaceuticals and personal care products (PPCPs) , Pimephales promelas. Environ Health Perspect 112:353-358 (2004) . doi:10.1289/ehp.6591 available via http://dx.doi.org/ [Online 1 December 2003]
Address correspondence to E.F. Orlando, Biology Department, 18952 E. Fisher Road, St. Mary's College of Maryland, St. Mary's City, MD 20686-3001 USA. Telephone: (240) 895-4376. Fax: (240) 895-4996. E-mail: eforlando@smcm.edu We thank G. Ankley, M. Chow, W. Hessler, M. Mann, K. Selcer, C. Tyler, and R. Stasiak for their assistance during this study. This research was supported by a grant to E.F.O. and L.J.G. from the European Commission (contract DG XII-E2/98/AF/2) . The research described in this article has been reviewed by the National Health Environmental Effects Research Laboratory, U.S. EPA, and approved for publication. Approval does not signify that the contents necessarily reflect the views and policies of the agency, nor does mention of trade names or commercial products constitute endorsement or recommendation for use. The authors declare they have no competing financial interests. Received 14 July 2003 ; accepted 1 December 2003. Table 3 was corrected on 10 March 2004.
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