Windows of Susceptibility and Consequences of Early Life Exposures to 17β-estradiol on Medaka (Oryzias latipes) Reproductive Success.

Estrogens and estrogen mimics are commonly found in surface waters and are associated with deleterious effects in fish populations. Impaired fertility and fecundity in fish following chronic exposures to estrogens and estrogen mimics during critical windows in development are well documented. However, information regarding differential reproductive effects of exposure within defined developmental stages remains sparse. In this study, reproductive capacity was assessed in Japanese medaka (Oryzias latipes) after exposure to two concentrations of 17β-estradiol (E2β; 2 ng/L and 50 ng/L) during four distinct stages of development: gonad development, gonad differentiation, development of secondary sex characteristics (SSC) and gametogenesis. Exposure to E2β did not adversely impact survival, hatch success, growth, or genotypic ratios. In contrast, exposure to 50 ng/L E2β during SSC development altered phenotypic ratios and SSC. Exposure to both E2β treatments reduced reproductive capacity (fertility, fecundity) by 7.3-57.4% in adult medaka breeding pairs, with hindrance of SSC development resulting in the largest disruption in breeding capacity (51.6-57.4% decrease) in the high concentration. This study documents differential effects among four critical stages of development and provides insight into factors (window of exposure, exposure concentration and duration of exposure period) contributing to reproductive disruption in fish.

[1]  R. Klaper,et al.  Emerging wastewater contaminant metformin causes intersex and reduced fecundity in fish. , 2015, Chemosphere.

[2]  Nathan T. Fleischhacker,et al.  Phytoestrogens in the environment, I: Occurrence and exposure effects on fathead minnows , 2014, Environmental toxicology and chemistry.

[3]  Zijian Wang,et al.  Long-term exposure investigating the estrogenic potency of estriol in Japanese medaka (Oryzias latipes). , 2014, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[4]  A. Whitehead,et al.  Anchoring Ethinylestradiol Induced Gene Expression Changes with Testicular Morphology and Reproductive Function in the Medaka , 2012, PloS one.

[5]  B. Faircloth,et al.  Primer3—new capabilities and interfaces , 2012, Nucleic acids research.

[6]  G. Genovese,et al.  Time-course recovery of estrogen-responsive genes of a cichlid fish exposed to waterborne octylphenol. , 2012, Aquatic toxicology.

[7]  M. Kinoshita,et al.  Reproduction of Medaka , 2012 .

[8]  M. Servos,et al.  Reproductive and histopathological effects in wild fish inhabiting an effluent-dominated stream, Wascana Creek, SK, Canada. , 2012, Aquatic toxicology.

[9]  Laura N. Vandenberg,et al.  Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. , 2012, Endocrine reviews.

[10]  Marlo K. Sellin Jeffries,et al.  Occurrence and endocrine effects of agrichemicals in a small Nebraska, USA, watershed , 2011, Environmental toxicology and chemistry.

[11]  M. Servos,et al.  Intersex and reproductive impairment of wild fish exposed to multiple municipal wastewater discharges. , 2011, Aquatic toxicology.

[12]  L. Barber,et al.  Demasculinization of male fish by wastewater treatment plant effluent. , 2011, Aquatic toxicology.

[13]  T. Iguchi,et al.  Differential expression of three estrogen receptor subtype mRNAs in gonads and liver from embryos to adults of the medaka, Oryzias latipes , 2011, Molecular and Cellular Endocrinology.

[14]  Nancy D Denslow,et al.  Behavioral and genomic impacts of a wastewater effluent on the fathead minnow. , 2011, Aquatic toxicology.

[15]  C. Tyler,et al.  Implications of persistent exposure to treated wastewater effluent for breeding in wild roach (Rutilus rutilus) populations. , 2011, Environmental science & technology.

[16]  Veronica Vinciotti,et al.  The Consequences of Feminization in Breeding Groups of Wild Fish , 2010, Environmental health perspectives.

[17]  O. Kah,et al.  17alpha-ethinylestradiol disrupts the ontogeny of the forebrain GnRH system and the expression of brain aromatase during early development of zebrafish. , 2010, Aquatic toxicology.

[18]  S. Zaugg,et al.  Mortality of centrarchid fishes in the Potomac drainage: survey results and overview of potential contributing factors. , 2010, Journal of aquatic animal health.

[19]  J. Mank,et al.  Evolutionary Perspectives on Hermaphroditism in Fishes , 2009, Sexual Development.

[20]  Masato Kinoshita,et al.  Medaka: Biology, Management, and Experimental Protocols , 2009 .

[21]  W. Cranor,et al.  Reproductive health of bass in the Potomac, USA, drainage: Part 2. Seasonal occurrence of persistent and emerging organic contaminants , 2009, Environmental toxicology and chemistry.

[22]  Alfred E Pinkney,et al.  Reproductive health of bass in the Potomac, USA, drainage: Part 1. Exploring the effects of proximity to wastewater treatment plant discharge , 2009, Environmental toxicology and chemistry.

[23]  C. Tyler,et al.  Estrogenic wastewater treatment works effluents reduce egg production in fish. , 2009, Environmental science & technology.

[24]  Gerald T. Ankley,et al.  Direct Effects, Compensation, and Recovery in Female Fathead Minnows Exposed to a Model Aromatase Inhibitor , 2008, Environmental health perspectives.

[25]  G. Ankley,et al.  Investigating compensation and recovery of fathead minnow (Pimephales promelas) exposed to 17alpha-ethynylestradiol with metabolite profiling. , 2008, Environmental science & technology.

[26]  L. Barber,et al.  Reproductive disruption in fish downstream from an estrogenic wastewater effluent. , 2008, Environmental science & technology.

[27]  A. L. Filby,et al.  Health Impacts of Estrogens in the Environment, Considering Complex Mixture Effects , 2007, Environmental health perspectives.

[28]  Daniel L Villeneuve,et al.  Ketoconazole in the fathead minnow (Pimephales promelas): Reproductive toxicity and biological compensation , 2007, Environmental toxicology and chemistry.

[29]  Karen A Kidd,et al.  Collapse of a fish population after exposure to a synthetic estrogen , 2007, Proceedings of the National Academy of Sciences.

[30]  Maido Remm,et al.  Enhancements and modifications of primer design program Primer3 , 2007, Bioinform..

[31]  Dalma Martinović,et al.  Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows , 2007, Environmental toxicology and chemistry.

[32]  M. Morita,et al.  Feminization of Japanese medaka (Oryzias latipes) exposed to 17beta-estradiol: effect of exposure period on spawning performance in sex-transformed females. , 2006, Aquatic toxicology.

[33]  D. O. Norris,et al.  Intersex and other reproductive disruption of fish in wastewater effluent dominated Colorado streams. , 2006, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[34]  V. Braithwaite,et al.  Endocrine disrupting effects on the nesting behaviour of male three-spined stickleback Gasterosteus aculeatus L , 2006 .

[35]  Daniel L Villeneuve,et al.  Relationship between brain and ovary aromatase activity and isoform-specific aromatase mRNA expression in the fathead minnow (Pimephales promelas). , 2006, Aquatic toxicology.

[36]  M. Matsuda.  [Sex determination in the teleost medaka, Oryzias latipes]. , 2005, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[37]  A. L. Filby,et al.  Molecular Characterization of Estrogen Receptors 1, 2a, and 2b and Their Tissue and Ontogenic Expression Profiles in Fathead Minnow (Pimephales promelas)1 , 2005, Biology of reproduction.

[38]  C. Tyler,et al.  Assessing the Sensitivity of Different Life Stages for Sexual Disruption in Roach (Rutilus rutilus) Exposed to Effluents from Wastewater Treatment Works , 2005, Environmental health perspectives.

[39]  Masanori Seki,et al.  Fish full life‐cycle testing for 17β‐estradiol on medaka (Oryzias latipes) , 2005, Environmental toxicology and chemistry.

[40]  S. Tilton,et al.  Relationship between ethinylestradiol‐mediated changes in endocrine function and reproductive impairment in Japanese medaka (Oryzias latipes) , 2005, Environmental toxicology and chemistry.

[41]  Charles R. Tyler,et al.  Long-Term Exposure to Environmental Concentrations of the Pharmaceutical Ethynylestradiol Causes Reproductive Failure in Fish , 2004, Environmental health perspectives.

[42]  Tohru Kobayashi,et al.  Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[43]  M. Sakaizumi,et al.  Field Survey of Sex-Reversals in the Medaka, Oryzias latipes: Genotypic Sexing of Wild Populations , 2004, Zoological science.

[44]  C. Metcalfe,et al.  Alterations to gonadal development and reproductive success in japanese medaka (Oryzias latipes) exposed to 17α‐ethinylestradiol , 2004, Environmental toxicology and chemistry.

[45]  Walter Giger,et al.  Combined biological and chemical assessment of estrogenic activities in wastewater treatment plant effluents , 2004, Analytical and bioanalytical chemistry.

[46]  Masanori Seki,et al.  Fish full life‐cycle testing for the weak estrogen 4‐tert‐pentylphenol on medaka (Oryzias latipes) , 2003, Environmental toxicology and chemistry.

[47]  N. Denslow,et al.  Relationship between reproductive success and male plasma vitellogenin concentrations in cunner, Tautogolabrus adspersus. , 2002, Environmental health perspectives.

[48]  J. Sumpter,et al.  Wild Intersex Roach (Rutilus rutilus) Have Reduced Fertility1 , 2002, Biology of reproduction.

[49]  Shuichi Asakawa,et al.  DMY is a Y-specific DM-domain gene required for male development in the medaka fish , 2002, Nature.

[50]  E. Thurman,et al.  Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. , 2002, Environmental science & technology.

[51]  J. Sumpter,et al.  Altered Sexual Maturation and Gamete Production in Wild Roach (Rutilus rutilus) Living in Rivers That Receive Treated Sewage Effluents1 , 2002, Biology of reproduction.

[52]  T. Croley,et al.  Estrogenic potency of chemicals detected in sewage treatment plant effluents as determined by in vivo assays with Japanese medaka (Oryzias latipes) , 2001, Environmental toxicology and chemistry.

[53]  Roberta Curini,et al.  Monitoring Natural and Synthetic Estrogens at Activated Sludge Sewage Treatment Plants and in a Receiving River Water , 2000 .

[54]  H. Gutzeit,et al.  17-α-ethinylestradiol affects reproduction, sexual differentiation and aromatase gene expression of the medaka (Oryzias latipes) , 2000 .

[55]  J. Nagler,et al.  Induction of gonadal intersex in genotypic male rainbow trout (Oncorhynchus mykiss) embryos following immersion in estradiol‐17ß , 2000, Molecular reproduction and development.

[56]  S. Teh,et al.  Determining the sensitive developmental stages of intersex induction in medaka (Oryzias latipes) exposed to 17 beta-estradiol or testosterone. , 2000, Marine environmental research.

[57]  J. Edmunds,et al.  Permanent and functional male-to-female sex reversal in d-rR strain medaka (Oryzias latipes) following egg microinjection of o,p'-DDT. , 2000, Environmental health perspectives.

[58]  D. Tillitt,et al.  An in vivo model fish system to test chemical effects on sexual differentiation and development: exposure to ethinyl estradiol , 2000 .

[59]  S. Adams,et al.  Evaluating Effects of Contaminants on Fish Health at Multiple Levels of Biological Organization: Extrapolating from Lower to Higher Levels , 2000 .

[60]  W. Benson,et al.  Reproduction and development of Japanese medaka following an early life stage exposure to xenoestrogens , 1998 .

[61]  John P. Sumpter,et al.  Widespread Sexual Disruption in Wild Fish , 1998 .

[62]  W. Hartley,et al.  Gonadal development in Japanese medaka (Oryzias latipes) exposed to 17 β-estradiol , 1998 .

[63]  Andrew A. Rooney,et al.  Organization versus activation: the role of endocrine-disrupting contaminants (EDCs) during embryonic development in wildlife. , 1995, Environmental health perspectives.

[64]  T. Iwamatsu.  Stages of normal development in the medaka Oryzias latipes , 1994, Mechanisms of Development.

[65]  A. Arnold,et al.  Organizational and activational effects of sex steroids on brain and behavior: A reanalysis , 1985, Hormones and Behavior.

[66]  Masaru Nakamura,et al.  Gonadal Sex Differentiation in Tilapia mossambica, with Special Regard to the Time of Estrogen Treatment Effective in Inducing Complete Feminization of Genetic Males , 1973 .

[67]  Toki-O Yamamoto,et al.  Artificially induced sex‐reversal in genotypic males of the medaka (Oryzias latipes) , 1953 .

[68]  J. Tarazona,et al.  An artificial fertilization method with the Japanese medaka: implications in early life stage bioassays and solvent toxicity. , 2008, Ecotoxicology and environmental safety.

[69]  Gerald T Ankley,et al.  Small fish models for identifying and assessing the effects of endocrine-disrupting chemicals. , 2004, ILAR journal.

[70]  Kei Nakayama,et al.  Suppression of sexual behavior in male Japanese medaka (Oryzias latipes) exposed to 17beta-estradiol. , 2003, Chemosphere.

[71]  M. Schartl,et al.  Common spontaneous sex-reversed XX males of the medaka Oryzias latipes. , 2003, Genetics.

[72]  M. I C H A E,et al.  Pharmaceuticals, Hormones, and Other Organic Wastewater Contaminants in U.S. Streams, 1999-2000: A National Reconnaissance , 2002 .

[73]  L. Carruth.  Freshwater Cichlid Crenicara punctulata Is a Protogynous Sequential Hermaphrodite , 2000, Copeia.

[74]  Scholz,et al.  17-alpha-ethinylestradiol affects reproduction, sexual differentiation and aromatase gene expression of the medaka (Oryzias latipes). , 2000, Aquatic toxicology.