Abstract
Although the effects of estrogens on model laboratory species are well documented, their utility as surrogates for other species, including those listed as endangered, are less clear. Traditionally, conservation policies are evaluated based on model organism responses but are intended to protect all species in an environment. We tested the hypothesis that the endangered Rio Grande silvery minnow (Hybognathus amarus) is more vulnerable to endocrine disruption—as assessed through its larval predator-escape performance, survival, juvenile sex ratios, and whole-body vitellogenin concentration—than the commonly used toxicological model species fathead minnow (Pimephales promelas) and the bluegill sunfish (Lepomis macrochirus). Fish were exposed concurrently for 21 days to the model endocrine active compound (EAC) 17ß-estradiol (E2) at 10 ng E2/L and 30 ng E2/L in a flow-through system using reconstituted water that simulated the physicochemical conditions of the Middle Rio Grande in New Mexico, USA. No significant differences were observed between the fathead and silvery minnow in larval predator-escape response or juvenile sex ratio. Rio Grande silvery minnow survival decreased significantly at day 14 compared with the other two species; by day 21, both cyprinid species (silvery minnow and fathead minnow) exhibited a significant decrease in survival compared with bluegill sunfish, a member of the family Centrarchidae. Male Rio Grande silvery minnow showed a significant increase in whole-body vitellogenin concentration in the 10 ng/L treatment, whereas fathead minnow and bluegill sunfish showed no significant increases in vitellogenin concentrations across treatments. Our study showed response differences to estrogen exposures between the two cyprinid species and further divergence in responses between the families Cyprinidae and Centrarchidae. These results suggest that commonly used laboratory model organisms may be less sensitive to EACs than the endangered Rio Grande silvery minnow. However, this study supports the continued use of surrogate species for the beneficial implementation of water-quality regulations for the protection of threatened and endangered species if phylogenetic relationships are taken into consideration.
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References
American Public Health Association, American Water Works Association, Water Environment Federation (1995) Standard methods for the examination of water and wastewater, 19th ed. APHA, Washington, DC
Ankley GT, Johnson RD (2004) Small fish models for identifying and assessing the effects of endocrine-disrupting chemicals. Lab Anim Res J 45:469–483
Ankley GT, Villeneuve DL (2006) The fathead minnow in aquatic toxicology: past, present and future. Aquat Toxicol 78:91–102
Barber LB, Lee KE, Swackhamer D, Schoenfuss HL (2007) Response of male fathead minnows exposed to wastewater treatment plant effluent, effluent treated with XAD8 resin, and an environmentally relevant mixture of alkylphenol compounds. Aquat Toxicol 82:36–46
Barber LB, Brown GK, Nettesheim TG, Murphy EW, Bartell SE, Schoenfuss HL (2011) Effects of organic contaminant mixtures on fish in a wastewater dominated urban stream. Sci Tot Environ 409:4720–4728
Beresford N, Brian JV, Runnalls TJ, Sumpter JP, Jobling S (2011) Estrogenic activity of tropical fish food can alter baseline vitellogenin concentrations in male fathead minnow (Pimephales promelas). Environ Toxicol Chem 30:1139–1145
Bistodeau TJ, Barber LB, Bartell SE, Cediel RA, Grove KJ, Klaustermeier J et al (2006) Larval exposure to environmentally relevant mixtures of alkylphenolethoxylates reduces reproductive competence in male fathead minnows. Aquat Toxicol 79:268–277
Bjorkblom C, Hogfors E, Salste L, Bergelin E, Olsson P, Katsiadaki I et al (2009) Estrogenic and androgenic effects of municipal wastewater effluent on reproductive endpoint biomarkers in three-spined stickleback (Gasterosteus aculeatus). Environ Toxicol Chem 28:1063–1071
Buhl KJ (2002) The relative toxicity of inorganic contaminants to the Rio Grande silvery minnow (Hybognathus amarus) and fathead minnow (Pimephales promelas) in a water quality simulating that in the Rio Grande, New Mexico. Final Report to the U.S. Fish and Wildlife Service, Albuquerque, NM
Carter LF (1995) Water-quality assessment of the Rio Grande Valley, Colorado, New Mexico, and Texas—Fish communities at selected sites 1993–95. United States Geological Survey Water-Resources Investigations Report 97-4017
Columbia Environmental Research Center (2008) Animal welfare plan. Columbia Environmental Research Center, US Geological Survey, Columbia, MO
Dammann AA, Shappell NW, Bartell SE, Schoenfuss HL (2011) Comparing biological effects and potencies of estrone and 17β-estradiol in mature fathead minnows, Pimephales promelas. Aquat Toxicol 105:559–568
Dwyer FJ, Mayer FL, Sappington LC, Buckler DR, Bridges CM, Greer IE et al (2005a) Assessing contaminant sensitivity of endangered and threatened aquatic species: part I. Acute toxicity of five chemicals. Arch Environ Contam Toxicol 48:143–154
Dwyer FJ, Hardesty DK, Henke CE, Ingersoll CG, Whites DW, Augspurger T et al (2005b) Assessing contaminant sensitivity of endangered and threatened aquatic species: part III. Effluent toxicity test. Arch Environ Contam Toxicol 48:174–183
Endangered Species Act of 1973. Public Law 93-205, 87 Stat. 884 16 U.S.C. 1531–1544. Section 3:6 20
Ferreira F, Santos MM, Castro LFC, Reis-Henriques MA, Lima D, Vieira MN et al (2009) Vitellogenin gene expression in the intertidal blenny Lipophrys pholis: a new sentinel species for estrogenic chemical pollution monitoring in the European Atlantic coast? Compd Biochem Physiol C 149:58–64
Fulton TW (1904) The rate of growth of fishes. Fisheries Board of Scotland, Annual Report 22 (part 3), pp 141–241
Gabe M (1976) Histological techniques. Springer-Verlag, New York
Hach Company (1997) Water quality handbook, 3rd edn. Hach Company, Loveland, CO
Helfman GS, Collette BB, Facey DE (1997) The diversity of fishes. Blackwell Science, Malden, MA, pp 62, 123, 143, 301, 308
Hyndman KM, Biales A, Bartell SE, Schoenfuss HL (2010) Assessing the effects of exposure timing on biomarker expression using 17β-estradiol. Aquat Toxicol 96:264–272
Kohn M, Melnick R (2002) Biochemical origins of the nonmonotonic receptor-mediated dose-response. J Mol Endocrinol 29:113–123
Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Saugg SD, Barber LB et al (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams 1999–2000: a national reconnaissance. Environ Sci Technol 36:1202–1211
Korner O, Vermeirssen ELM, Burkhardt-Holm P (2005) Intersex in feral brown trout from Swiss midland rivers. J Fish Biol 67:1734–1740
Martinović D, Denny JS, Schmieder PK, Ankley GT, Sorensen PW (2008) Temporal variation in the estrogenicity of a sewage treatment plant effluent and its biological significance. Environ Sci Technol 42:3421–3427
McGee MR, Julius ML, Vajda AM, Norris DO, Barber LB, Schoenfuss HL (2009) Predator avoidance performance of larval fathead minnows (Pimephales promelas) following short-term exposure to estrogen mixtures. Aquat Toxicol 91:355–361
Nielsen L, Baatrup E (2006) Quantitative studies on the effects of environmental estrogens on the testis of the guppy, Poecilia reticulate. Aquat Toxicol 80:140–148
Orn S, Yamani S, Norrgren L (2006) Comparison of vitellogenin induction, sex ratio, and gonad morphology between zebrafish and Japanese medaka after exposure to 17α-ethinylestradiol and 17β-trenbolone. Arch Environ Contam Toxicol 51:237–243
Painter MM, Buerkley MA, Julius ML, Vajda AM, Norris DO, Barber LB et al (2009) Antidepressants at environmentally relevant concentrations affect predator avoidance behavior of larval fathead minnows (Pimephales promelas). Environ Toxicol Chem 28:2677–2684
Palace VP, Evans RE, Wautier KG, Mills KH, Blanchfield PJ, Park BJ et al (2009) Interspecies differences in biochemical, histopathological, and population responses in four wild fish species exposed to ethynylestradiol added to a whole lake. Can J Fish Aquat Sci 66:1920–1935
Panter GH, Thompson RS, Sumpter JP (1998) Adverse reproductive effects in male fathead minnows (Pimephales promelas) exposed to environmentally relevant concentration of the natural oestrogens, oestradiol and oestrone. Aquat Toxicol 42:243–253
Pawlowski S, van Aerle R, Tyler CR, Braunbeck T (2004) Effects of 17α-ethynylestradiol in a fathead minnow (Pimephales promelas) gonadal recrudescence assay. Ecotoxicol Environ Safe 57:330–345
Sappington LC, Mayer FL, Dwyer FJ, Buckler DR, Jones JR, Ellersieck MR (2001) Contaminant sensitivity of threatened and endangered fishes compared to standard surrogate species. Environ Toxicol Chem 20:2869–2876
Schoenfuss HL, Levitt JT, Van Der Kraak G, Sorensen PW (2002) Ten week exposure to treated sewage effluent discharge has small, variable effects on reproductive behavior and sperm production in goldfish. Environ Toxicol Chem 21:2185–2190
Schultz MM, Bartell SE, Schoenfuss HL (2012) Effects of triclosan and triclocarban, two ubiquitous environmental contaminants, on anatomy, physiology and behavior of the fathead minnow (Pimephales promelas). Arch Environ Contam Toxicol 63:114–124
Schultz MM, Minarik TA, Martinovic-Weigelt D, Curran EA, Bartell SE, Schoenfuss HL (2013) Environmental estrogens in an urban aquatic ecosystem: II. Biological effects. Environ Int 61:138–149
Shappell NW, Hyndman KM, Bartell SE, Schoenfuss HL (2010) Comparative biological effects and potency of 17a- and 17µ estradiol in fathead minnows. Aquat Toxicol 100:1–8
Stephan CE, Mount DI, Hansen DJ, Gentile JH, Chapman GA, Brungs WA (1985) Guidelines for deriving numerical national water quality criteria for the protection of aquatic organisms and their uses. PB 85-22-7049. National Technical Information Service, Springfield, VA
Teather K, Parrott J (2006) Assessing the chemical sensitivity of freshwater fish commonly used in toxicological studies. Water Qual Res J Can 41:100–105
Thorpe KL, Benstead R, Hutchinson TH, Tyler CR (2007) Associations between altered vitellogenin concentrations and adverse health effects in fathead minnow (Pimephales promelas). Aquat Toxicol 85:176–183
Tyler CR, van der Eerden B, Jobling S, Panter G, Sumpter JP (1996) Measurement of vitellogenin, a biomarker for exposure to oestrogenic chemicals, in a wide variety of cyprinid fish. J Compd Physiol B 166:418–426
Tyler CR, van Aerle R, Hutchinson TH, Maddix S, Trip H (1999) An in vivo testing system for endocrine disruptors in fish early life stages using induction of vitellogenin. Environ Toxicol Chem 18:337–347
United States Fish and Wildlife Service (1973) Endangered species act of 1973 as amended through the 108th Congress. USFWS, Washington, DC
United States Fish and Wildlife Service (2004) Endangered and threatened wildlife and plants; Final rule to list the Rio Grande silvery minnow as an endangered species. Federal Register 59:36988–37001
United States Fish and Wildlife Service (2007) Draft revised Rio Grande silvery minnow (Hybognathus amarus) recovery plan. USFWS, Albuquerque, NM
Vajda AM, Barber LB, Gray JL, Lopez EM, Woodling JD, Norris JD (2008) Reproductive disruption in fish downstream from an estrogenic wastewater effluent. Environ Sci Technol 42:3407–3414
Vajda AM, Barber LB, Gray JL, Lopez EM, Bolden AM, Schoenfuss HL et al (2011) Demasculinization of male fish by wastewater treatment plant effluent. Aquat Toxicol 103:213–221
Van den Belt K, Berckmans P, Vangenechten C, Verheyen R, Witters H (2004) Comparative study on the in vitro/in vivo estrogenic potencies of 17β-estradiol, estrone 17α-ethynylestradiol and nonylphenol. Aquat Toxicol 66:183–195
Writer JH, Barber LB, Brown GK, Taylor HE, Kiesling RL, Ferrey ML et al (2010) Anthropogenic tracers, endocrine disrupting chemicals, and endocrine disruption in Minnesota lakes. Sci Total Environ 409:100–111
Yokota H, Seki M, Maeda M, Oshima Y, Tadokora H, Honjo T et al (2001) Life-cycle toxicity of 4-nonylphenol to medaka (Oryzias latipes). Environ Toxicol Chem 20:2552–2560
Acknowledgments
We thank the staff at the USGS Yankton Field Research Station, specifically Ron Grandi, Travis Schaeffer, and Evie Sime, for their assistance in daily care and maintenance of the exposure system and fish. Andrew Meister and Jeffrey Miller at the St. Cloud State University Aquatic Toxicology Laboratory provided assistance with sample preparation. Partial funding for this project was provided by the Minnesota Environment and Natural Resources Trust Fund as recommended by the Legislative-Citizen Commission on Minnesota Resources. Any use of trade, product, or firm names is for descriptive puproses only and does not imply endorsement by the US Government.
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Jorgenson, Z.G., Buhl, K., Bartell, S.E. et al. Do Laboratory Species Protect Endangered Species? Interspecies Variation in Responses to 17β-Estradiol, a Model Endocrine Active Compound. Arch Environ Contam Toxicol 68, 204–215 (2015). https://doi.org/10.1007/s00244-014-0076-9
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DOI: https://doi.org/10.1007/s00244-014-0076-9