Interspecies differences in biochemical, histopathological, and population responses in four wild fish species exposed to ethynylestradiol added to a whole lake

Efforts to understand the effects of environmental estrogens on fish have shifted away from biochemical indica- tors towards population-level impacts. Ethynylestradiol (EE2) was added to a whole lake at environmentally relevant con- centrations for 3 consecutive years to examine links between vitellogenin (VTG) induction, histopathological impacts, and population decline in four species of fish. VTG induction and histopathological effects in tissues were most severe in fat- head minnow (Pimephales promelas) and pearl dace (Margariscus margarita). VTG was induced to a similar extent in lake trout (Salvelinus namaycush) but less so in white sucker (Catostomus commersonii). There were no histopathological effects in tissues of the two latter species. Population decline occurred in fathead minnows in the second year of EE2 addi- tions and there were some indications of population decline in pearl dace during the third year. White suckers were not af- fected but lake trout declined in year 3. Habitat selection probably altered EE2 exposure and the different effects in each species likely also reflect differing sensitivities. It appears that VTG induction is not sufficient to predict effects of xenoes- trogens on fish populations. However, stronger predictions can be made when VTG induction is assessed in conjunction with histopathological evidence of liver, kidney, and gonad tissue damage. Resume´ : Les efforts pour comprendre les effets des estrogenes de l'environnement sur les poissons se concentrent main- tenant sur les impacts au niveau des populations plutot que sur les indicateurs biochimiques. Nous avons ajoutede l'ethy- nylestradiol (EE2) aun lac entier ades concentrations pertinentes au niveau de l'environnement durant 3 annees consecutives afin d'examiner les liens entre l'induction de la vitellogenine (VTG), les impacts histopathologiques et le de ´- clin de la population chez quatre especes de poissons. L'induction de la VTG et les effets histopathologiques dans les tis- sus sont les plus importants chez la tete-de-boule (Pimephales promelas) et le mulet perle ´ (Margariscus margarita). L'induction de VTG est de niveau semblable chez le touladi (Salvelinus namaycush), mais moindre chez le meunier noir (Catastomus commersonii). Il n'y a pas d'effets histopathologiques dans les tissus de ces deux dernieres especes. Un declin demographique s'est produit chez la tete-de-boule durant la seconde annee des additions de EE2 et il y avait des signes de declin demographique chez le mulet perledurant la troisieme annee. Les meuniers noirs n'ont pas eteaffectes, mais les touladis ont diminuela troisieme annee. La selection des habitats modifie probablement l'exposition aEE2 et les effets distincts chez chaque espece refletent aussi vraisemblablement des sensibilites differentes. Il semble que l'induction de VTG ne suffise pas pour predire les effets des xenoestrogenes sur les populations de poissons. Il est, cependant, possible de faire de meilleures predictions lorsque l'induction de VTG est evaluee conjointement avec les signes histopathologiques de dommages dans les tissus du foie, des reins et des gonades. (Traduit par la Redaction)

[1]  J. Parrott,et al.  Life‐cycle exposure of fathead minnows (Pimephales promelas) to an ethinylestradiol concentration below 1 ng/L reduces egg fertilization success and demasculinizes males , 2005, Environmental toxicology.

[2]  H. Komen,et al.  Feminization of male carp , 1996, Nature.

[3]  Daniel L Villeneuve,et al.  Reproductive responses of common carp (Cyprinus carpio) exposed in cages to influent of the Las Vegas Wash in Lake Mead, Nevada, from late winter to early spring. , 2004, Environmental science & technology.

[4]  R. Devlin,et al.  Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences , 2002 .

[5]  G. Ankley,et al.  Screening and Testing for Endocrine Disruption in Fish—Biomarkers As “Signposts,” Not “Traffic Lights,” in Risk Assessment , 2005, Environmental health perspectives.

[6]  K. Zimmer,et al.  Population ecology and prey consumption by fathead minnows in prairie wetlands: importance of detritus and larval fish , 2007 .

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

[8]  Demetrio Raldúa,et al.  First evidence of endocrine disruption in feral carp from the Ebro River. , 2004, Toxicology and applied pharmacology.

[9]  Francesc Piferrer,et al.  Endocrine sex control strategies for the feminization of teleost fish , 2001 .

[10]  D. Chapman,et al.  Reproductive condition and occurrence of intersex in bighead carp and silver carp in the Missouri River , 2006, Hydrobiologia.

[11]  F. Gagné,et al.  Estrogenic properties of municipal and industrial wastewaters evaluated with a rapid and sensitive chemoluminescent in situ hybridization assay (CISH) in rainbow trout hepatocytes , 1998 .

[12]  Henrik Holbech,et al.  Gonad development and vitellogenin production in zebrafish (Danio rerio) exposed to ethinylestradiol and methyltestosterone. , 2003, Aquatic toxicology.

[13]  J. Sumpter,et al.  Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. , 1995, Environmental health perspectives.

[14]  K. Kidd,et al.  Induction of Vitellogenin and Histological Effects in Wild Fathead Minnows from a Lake Experimentally Treated with the Synthetic Estrogen, Ethynylestradiol , 2002 .

[15]  D. Schindler,et al.  Pelagic distribution of lake trout (Salvelinus namaycush) in small Canadian Shield lakes with respect to temperature, dissolved oxygen, and light , 1998 .

[16]  M. Pettersson,et al.  ETHINYLOESTRADIOL - AN UNDESIRED FISH CONTRACEPTIVE , 1999 .

[17]  H. Komen,et al.  Feminisation of young males of the common carp, Cyprinus carpio, exposed to 4-tert-pentylphenol during sexual differentiation , 1998 .

[18]  Yong Chen,et al.  Growth, Abundance, and Food Supply of White Sucker , 1995 .

[19]  R. Verheyen,et al.  Comparison of vitellogenin responses in zebrafish and rainbow trout following exposure to environmental estrogens. , 2003, Ecotoxicology and environmental safety.

[20]  Edwin J. Routledge,et al.  Identification of Estrogenic Chemicals in STW Effluent. 2. In Vivo Responses in Trout and Roach , 1998 .

[21]  C. Tyler,et al.  Effects of 17alpha-ethinylestradiol in a fathead minnow (Pimephales promelas) gonadal recrudescence assay. , 2004, Ecotoxicology and environmental safety.

[22]  K. Kidd,et al.  Waterborne ethynylestradiol induces vitellogenin and alters metallothionein expression in lake trout (Salvelinus namaycush). , 2003, Aquatic toxicology.

[23]  P. White,et al.  Plasma vitellogenin in male teleost fish from 43 rivers worldwide is correlated with upstream human population size. , 2010, Environmental pollution.

[24]  C. Tyler,et al.  Associations between altered vitellogenin concentrations and adverse health effects in fathead minnow (Pimephales promelas). , 2007, Aquatic toxicology.

[25]  Wayne A. Hubert,et al.  Relations of Physical Habitat to Abundance of Four Nongame Fishes in High-Plains Streams: A Test of Habitat Suitability Index Models , 1989 .

[26]  R. Hill,et al.  Developmental estrogenic exposure in zebrafish (Danio rerio): II. Histological evaluation of gametogenesis and organ toxicity. , 2003, Aquatic toxicology.

[27]  M. Mac Effects of ration size on preferred temperature of lake charr Salvelinus namaycush , 1985, Environmental Biology of Fishes.

[28]  L. Barber,et al.  Anthropogenic tracers, endocrine disrupting chemicals, and endocrine disruption in Minnesota lakes. , 2010, The Science of the total environment.

[29]  J. Gunn,et al.  Coping with a Warm Environment: Behavioral Thermoregulation by Lake Trout , 1995 .

[30]  J N Lester,et al.  The Effects of Natural and Synthetic Steroid Estrogens in Relation to their Environmental Occurrence , 2002, Critical reviews in toxicology.

[31]  F. Pakdel,et al.  In vivo estrogen induction of hepatic estrogen receptor mRNA and correlation with vitellogenin mRNA in rainbow trout , 1991, Molecular and Cellular Endocrinology.

[32]  H. Holbech,et al.  Effects of exposure to 17α-ethinylestradiol during early development on sexual differentiation and induction of vitellogenin in zebrafish (Danio rerio) , 2003 .

[33]  D R Dietrich,et al.  Determination of vitellogenin kinetics in male fathead minnows (Pimephales promelas). , 2002, Toxicology letters.

[34]  R. Hecky,et al.  Effects of lake size, water clarity, and climatic variability on mixing depths in Canadian Shield lakes , 1996 .

[35]  I. C. Johnson,et al.  The sheepshead minnow as an in vivo model for endocrine disruption in marine teleosts: A partial life‐cycle test with 17α‐ethynylestradiol , 2001, Environmental toxicology and chemistry.

[36]  J. Gee,et al.  Intraspecific resource partitioning in a headwaters stream fish, the pearl dace Semotilus margarita (Cyprinidae) , 1982, Environmental Biology of Fishes.

[37]  J. Magnuson,et al.  Temperature as an Ecological Resource , 1979 .

[38]  J. Magnuson,et al.  Potential Changes in the Thermal Habitat of Great Lakes Fish after Global Climate Warming , 1990 .

[39]  D. Barceló,et al.  Feminization of wild carp, Cyprinus carpio, in a polluted environment: plasma steroid hormones, gonadal morphology and xenobiotic metabolizing system. , 2003, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

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

[41]  J. Raelson,et al.  Up-regulation of estrogen receptor mRNA and estrogen receptor activity by estradiol in liver of rainbow trout and other teleostean fish. , 1996, Comparative biochemistry and physiology. Part C, Pharmacology, toxicology & endocrinology.

[42]  K. Mills,et al.  Responses of Fish Populations in Lake 223 to 8 Years of Experimental Acidification , 1987 .

[43]  P. Blanchfield,et al.  Performance of temperature and dissolved oxygen criteria to predict habitat use by lake trout (Salvelinus namaycush)This paper is part of the series “Forty Years of Aquatic Research at the Experimental Lakes Area”. , 2009 .

[44]  K. Kidd,et al.  Reproductive fitness of lake trout ( Salvelinus namaycush ) exposed to environmentally relevant concentrations of the potent estrogen ethynylestradiol (EE2) in a whole lake exposure experiment , 2006 .

[45]  C. Tyler,et al.  An in vivo testing system for endocrine disruptors in fish early life stages using induction of vitellogenin , 1999 .

[46]  V. Palace,et al.  VARIATION OF HEPATIC ENZYMES IN THREE SPECIES OF FRESHWATER FISH FROM PRECAMBRIAN SHIELD LAKES AND THE EFFECT OF CADMIUM EXPOSURE , 1993 .

[47]  Charles R. Tyler,et al.  Endocrine disruption in wild freshwater fish , 2003 .

[48]  J. Sumpter,et al.  Effects of the synthetic estrogen 17α‐ethinylestradiol on the life‐cycle of the fathead minnow (Pimephales promelas) , 2001 .

[49]  James J. Nagler,et al.  Short‐term exposure to 17α‐ethynylestradiol decreases the fertility of sexually maturing male rainbow trout (Oncorhynchus mykiss) , 2003 .

[50]  D. Schindler,et al.  Johnson and Vallentyne's legacy: 40 years of aquatic research at the Experimental Lakes Area. , 2009 .

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

[52]  Irvin R. Schultz,et al.  Dose–response relationships and pharmacokinetics of vitellogenin in rainbow trout after intravascular administration of 17α-ethynylestradiol , 2001 .

[53]  Karen A Kidd,et al.  Biochemical and histopathological effects in pearl dace (Margariscus margarita) chronically exposed to a synthetic estrogen in a whole lake experiment , 2006, Environmental toxicology and chemistry.

[54]  J. Sumpter,et al.  Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom Freshwaters , 2001, Environmental toxicology and chemistry.

[55]  K. Kidd,et al.  Effects of the synthetic estrogen ethinylestradiol on early life stages of mink frogs and green frogs in the wild and in situ , 2005, Environmental toxicology and chemistry.