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Annual Review of Animal Biosciences

Volume 6, 2018

Reproductive Impacts of Endocrine-Disrupting Chemicals on Wildlife Species: Implications for Conservation of Endangered Species

Abstract

Wildlife have proven valuable to our understanding of the potential effects of endocrine-disrupting chemicals (EDCs) on human health by contributing considerably to our understanding of the mechanisms and consequences of EDC exposure. But the threats EDCs present to populations of wildlife species themselves are significant, particularly for endangered species whose existence is vulnerable to any reproductive perturbation. However, few studies address the threats EDCs pose to endangered species owing to challenges associated with their study. Here, we highlight those barriers and review the available literature concerning EDC effects on endangered species. Drawing from other investigations into nonthreatened wildlife species, we highlight opportunities for new approaches to advance our understanding and potentially mitigate the effects of EDCs on endangered species to enhance their fertility.

Keyword(s): endangered species, endocrine-disrupting chemicals, wildlife
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2018-02-15
2024-04-26
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Literature Cited

  1. Carson R. 1.  1962. Silent Spring Greenwich, CT: Fawcett
  2. Christie DA, Tassey EM. 2. , eds. 2004. Environmental toxicology: the legacy of Silent Spring. . Wellcome Witn. 20th Cent. Med19 http://www.histmodbiomed.org/sites/default/files/44841.pdf
  3. Colborn T, Dumanoski D, Myers JP. 3.  1997. Our Stolen Future: Are We Threatening Our Fertility, Intelligence, and Survival? A Scientific Detective Story New York: Plume
  4. Colborn T, Clement C. 4.  1992. Chemically-Induced Alterations in Sexual and Functional Development: The Wildlife/Human Connection Princeton, NJ: Princeton Sci.
  5. 5. US Environ. Prot. Agency. 2015. Endocrine Disruptor Screening Program (EDSP) Estrogen Receptor Bioactivity Washington, DC: US Environ. Prot. Agency. https://www.epa.gov/endocrine-disruption/endocrine-disruptor-screening-program-edsp-estrogen-receptor-bioactivity
  6. 6. US Environ. Prot. Agency. 2015. Endocrine Disruptor Screening Program Tier 1 Screening Determinations and Associated Data Evaluation Records Washington, DC: US Environ. Prot. Agency https://www.epa.gov/endocrine-disruption/endocrine-disruptor-screening-program-tier-1-screening-determinations-and
  7. Diamanti-Kandarakis E, Bourguignon J-P, Giudice LC, Hauser R, Prins GS. 7.  et al. 2009. Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocr. Rev. 30:293–342 [Google Scholar]
  8. Bergman A, Heindel JJ, Jobling S, Kidd KA, Zoeller RT. 8. , eds. 2013. State of the Science of Endocrine Disrupting Chemicals 2012: Summary for Decision-Makers Geneva: UN Environ. Progr. World Health Organ296
  9. Gore AC, Chappell VA, Fenton SE, Flaws JA, Nadal A. 9.  et al. 2015. EDC-2: the endocrine society's second scientific statement on endocrine-disrupting chemicals. Endocr. Rev. 36:E1–E150 [Google Scholar]
  10. Hotchkiss AK, Rider CV, Blystone CR, Wilson VS, Hartig PC. 10.  et al. 2008. Fifteen years after “Wingspread”—environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go. Toxicol. Sci. 105:235–59 [Google Scholar]
  11. McLachlan JA. 11.  2016. Environmental signaling: from environmental estrogens to endocrine-disrupting chemicals and beyond. Andrology 4:684–94 [Google Scholar]
  12. Colborn T, vom Saal FS, Soto AM. 12.  1993. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health Perspect. 101:378–84 [Google Scholar]
  13. Oberdörster E, Cheek AO. 13.  2001. Gender benders at the beach: endocrine disruption in marine and estuarine organisms. Environ. Toxicol. Chem. 20:23–36 [Google Scholar]
  14. León-Olea M, Martyniuk CJ, Orlando EF, Ottinger MA, Rosenfeld CS. 14.  et al. 2014. Current concepts in neuroendocrine disruption. Gen. Comp. Endocrinol. 203:158–73 [Google Scholar]
  15. Jefferson WN, Patisaul HB, Williams CJ. 15.  2012. Reproductive consequences of developmental phytoestrogen exposure. Reproduction 143:247–60 [Google Scholar]
  16. Piazza YG, Pandolfi M, Lo Nostro FL. 16.  2011. Effect of the organochlorine pesticide endosulfan on GnRH and gonadotrope cell populations in fish larvae. Arch. Environ. Contam. Toxicol. 61:300–10 [Google Scholar]
  17. Qin F, Wang L, Wang X, Liu S, Xu P. 17.  et al. 2013. Bisphenol A affects gene expression of gonadotropin-releasing hormones and type I GnRH receptors in brains of adult rare minnow Gobiocypris rarus. . Comp. Biochem. Physiol. C Toxicol. Pharmacol. 157:192–202 [Google Scholar]
  18. Patisaul HB, Whitten PL, Young LJ. 18.  1999. Regulation of estrogen receptor beta mRNA in the brain: opposite effects of 17β-estradiol and the phytoestrogen, coumestrol. Mol. Brain Res. 67:165–71 [Google Scholar]
  19. DeLeon S, Halitschke R, Hames RS, Kessler A, DeVoogd TJ, Dhondt AA. 19.  2013. The effect of polychlorinated biphenyls on the song of two passerine species. PLOS ONE 8:e73471 [Google Scholar]
  20. Jasarevic E, Sieli PT, Twellman EE, Welsh TH Jr., Schachtman TR. 20.  et al. 2011. Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A. PNAS 108:11715–20 [Google Scholar]
  21. Blum MJ, Walters DM, Burkhead NM, Freeman BJ, Porter BA. 21.  2010. Reproductive isolation and the expansion of an invasive hybrid swarm. Biol. Invasions 12:2825–36 [Google Scholar]
  22. Ward JL, Blum MJ. 22.  2012. Exposure to an environmental estrogen breaks down sexual isolation between native and invasive species. Evol. Appl. 5:901–12 [Google Scholar]
  23. Jobling S, Sumpter JP, Sheahan D, Osborne JA, Matthiessen P. 23.  1996. Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ. Toxicol. Chem. 15:194–202 [Google Scholar]
  24. Parks LG, Lambright CS, Orlando EF, Guillette JLJ, Ankley GT, Gray JLE. 24.  2001. Masculinization of female mosquitofish in Kraft mill effluent-contaminated Fenholloway River water is associated with androgen receptor agonist activity. Toxicol. Sci. 62:257–67 [Google Scholar]
  25. Purdom C, Hardiman P, Bye V, Eno N, Tyler CR, Sumpter JP. 25.  1994. Estrogenic effects of effluents from sewage treatment works. Chem. Ecol. 8:275–85 [Google Scholar]
  26. Carr JA, Gentles A, Smith EE, Goleman WL, Urquidi LJ. 26.  et al. 2003. Response of larval Xenopus laevis to atrazine: assessment of growth, metamorphosis, and gonadal and laryngeal morphology. Environ. Toxicol. Chem. 22:396–405 [Google Scholar]
  27. Hayes TB, Collins A, Lee M, Mendoza M, Noriega N. 27.  et al. 2002. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. PNAS 99:5476–80 [Google Scholar]
  28. Guillette LJ, Gross TS, Masson GR, Matter JM, Percival HF, Woodward AR. 28.  1994. Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ. Health Perspect. 102:680–88 [Google Scholar]
  29. Willingham E, Crews D. 29.  1999. Sex reversal effects of environmentally relevant xenobiotic concentrations on the red-eared slider turtle, a species with temperature-dependent sex determination. Gen. Comp. Endocrinol. 113:429–35 [Google Scholar]
  30. Fry DM, Toone CK. 30.  1981. DDT-induced feminization of gull embryos. Science 213:922–24 [Google Scholar]
  31. Schreiber RW, Risebrough RW. 31.  1972. Studies of the brown pelican. Wilson Bull 84:119–35 [Google Scholar]
  32. Gress F, Risebrough R, Anderson DW, Kiff LF, Jehl JRJ. 32.  1973. Reproductive failure of double-crested cormorants in southern California and Baja California. Wilson Bull 85:197–208 [Google Scholar]
  33. Helle E, Olsson M. 33.  1976. PCB levels correlated with pathological changes in seal uteri. Ambio 5:261–63 [Google Scholar]
  34. Kohno S, Katsu Y, Iguchi T, Guillette LJ Jr.. 34.  2008. Novel approaches for the study of vertebrate steroid hormone receptors. Integr. Comp. Biol. 48:527–34 [Google Scholar]
  35. Guillette LJ. 35.  2006. Endocrine disrupting contaminants—beyond the dogma. Environ. Health Perspect. 114:9–12 [Google Scholar]
  36. Sanderson JT, Seinen W, Giesy JP, van den Berg M. 36.  2000. 2-Chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: A novel mechanism for estrogenicity?. Toxicol. Sci. 54:121–27 [Google Scholar]
  37. Connor K, Howell J, Chen I, Liu H, Berhane K. 37.  et al. 1996. Failure of chloro-s-triazine-derived compounds to induce estrogen receptor-mediated responses in vivo and in vitro. Fundam. Appl. Toxicol. 30:93–101 [Google Scholar]
  38. Fan W, Yanase T, Morinaga H, Gondo S, Okabe T. 38.  et al. 2007. Atrazine-induced aromatase expression is SF-1 dependent: implications for endocrine disruption in wildlife and reproductive cancers in humans. Environ. Health Perspect. 115:720–27 [Google Scholar]
  39. Hamlin HJ, Edwards TM, McCoy J, Cruze L, Guillette LJ Jr.. 39.  2016. Environmentally relevant concentrations of nitrate increase plasma testosterone concentrations in female American alligators (Alligator mississippiensis). Gen. Comp. Endocrinol. 238:55–60 [Google Scholar]
  40. Letcher RJ, Bustnes JO, Dietz R, Jenssen BM, Jørgensen EH. 40.  et al. 2010. Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci. Total Environ. 408:2995–3043 [Google Scholar]
  41. Mathieu-Denoncourt J, Wallace SJ, de Solla SR, Langlois VS. 41.  2015. Plasticizer endocrine disruption: highlighting developmental and reproductive effects in mammals and non-mammalian aquatic species. Gen. Comp. Endocrinol. 219:74–88 [Google Scholar]
  42. Baker M. 42.  2014. The microbiome as a target for endocrine disruptors: Novel chemicals may disrupt androgen and microbiome-mediated autoimmunity. Endocr. Disrupt. 2:e964539 [Google Scholar]
  43. Ankley GT, Jensen KM, Makynen EA, Kahl MD, Korte JJ. 43.  et al. 2003. Effects of the androgenic growth promoter 17-β-trenbolone on fecundity and reproductive endocrinology of the fathead minnow. Environ. Toxicol. Chem. 22:1350–60 [Google Scholar]
  44. Orlando EF, Kolok AS, Binzcik GA, Gates JL, Horton MK. 44.  et al. 2004. Endocrine-disrupting effects of cattle feedlot effluent on an aquatic sentinel species, the fathead minnow. Environ. Health Perspect. 112:353–58 [Google Scholar]
  45. Kersey DC, Dehnhard M. 45.  2014. The use of noninvasive and minimally invasive methods in endocrinology for threatened mammalian species conservation. Gen. Comp. Endocrinol. 203:296–306 [Google Scholar]
  46. McCormick SD, Romero LM. 46.  2017. Conservation endocrinology. BioScience 67:429–42 [Google Scholar]
  47. Tubbs C, McDonough CE, Felton R, Milnes MR. 47.  2014. Advances in conservation endocrinology: the application of molecular approaches to the conservation of endangered species. Gen. Comp. Endocrinol. 203:29–34 [Google Scholar]
  48. Czekala NM, Lasley BL. 48.  1977. A technical note on sex determination in monomorphic birds using faecal steroid analysis. Int. Zoo Yearb. 17:209–11 [Google Scholar]
  49. Ganswindt A, Brown JL, Freeman EW, Kouba AJ, Penfold LM. 49.  et al. 2012. International Society for Wildlife Endocrinology: the future of endocrine measures for reproductive science, animal welfare and conservation biology. Biol. Lett. 8:695–97 [Google Scholar]
  50. Adams EM, Frederick PC, Larkin ILV, Guillette LJ. 50.  2009. Sublethal effects of methylmercury on fecal metabolites of testosterone, estradiol, and corticosterone in captive juvenile white ibises (Eudocimus albus). Environ. Toxicol. Chem. 28:982–89 [Google Scholar]
  51. Jayasena N, Frederick PC, Larkin ILV. 51.  2011. Endocrine disruption in white ibises (Eudocimus albus) caused by exposure to environmentally relevant levels of methylmercury. Aquatic Toxicol 105:321–27 [Google Scholar]
  52. Felton RG, Steiner CC, Durrant BS, Keisler DH, Milnes MR, Tubbs CW. 52.  2015. Identification of California condor estrogen receptors 1 and 2 and their activation by endocrine disrupting chemicals. Endocrinology 156:4448–57 [Google Scholar]
  53. Tubbs C, Hartig P, Cardon M, Varga N, Milnes M. 53.  2012. Activation of southern white rhinoceros (Ceratotherium simum simum) estrogen receptors by phytoestrogens: Potential role in the reproductive failure of captive-born females?. Endocrinology 153:1444–52 [Google Scholar]
  54. Koepfli K-P, Paten B, O'Brien SJ. 54.  2015. The Genome 10K Project: a way forward. Annu. Rev. Anim. Biosci. 3:57–111 [Google Scholar]
  55. Tubbs CW, Durrant BS, Milnes MR. 55.  2017. Reconsidering the use of soy and alfalfa in southern white rhinoceros diets. Pachyderm 58:135–39 [Google Scholar]
  56. Tubbs C. 56.  2016. California condors and DDT: Examining the effects of endocrine disrupting chemicals in a critically endangered species. Endocr. Disrupt. 4:e1173766 [Google Scholar]
  57. Reed CE, Fenton SE. 57.  2013. Exposure to diethylstilbestrol during sensitive life stages: a legacy of heritable health effects. Birth Defects Res. C Embryo Today Rev. 99:134–46 [Google Scholar]
  58. Adams NR. 58.  1995. Organizational and activational effects of phytoestrogens on the reproductive tract of the ewe. Proc. Soc. Exp. Biol. Med. 208:87–91 [Google Scholar]
  59. Guillette LJ, Crain DA, Rooney AA, Pickford DB. 59.  1995. Organization versus activation: the role of endocrine-disrupting contaminants (EDCs) during embryonic development in wildlife. Environ. Health Perspect. 103:157–64 [Google Scholar]
  60. Skinner MK. 60.  2014. Endocrine disruptor induction of epigenetic transgenerational inheritance of disease. Mol. Cell. Endocrinol. 398:4–12 [Google Scholar]
  61. Emslie R, Brooks M. 61.  1999. African Rhino: Status Survey and Conservation Action Plan Gland, Switz.: Int. Union Conserv. Nat.
  62. Swaisgood RR, Dickman DM, White AM. 62.  2006. A captive population in crisis: testing hypotheses for reproductive failure in captive-born southern white rhinoceros females. Biol. Conserv. 129:468–76 [Google Scholar]
  63. Tubbs CW, Moley LA, Ivy JA, Metrione LC, LaClaire S. 63.  et al. 2016. Estrogenicity of captive southern white rhinoceros diets and their association with fertility. Gen. Comp. Endocrinol. 238:32–38 [Google Scholar]
  64. Skinner MK, Guerrero-Bosagna C. 64.  2009. Environmental signals and transgenerational epigenetics. Epigenomics 1:111–17 [Google Scholar]
  65. Head JA. 65.  2014. Patterns of DNA methylation in animals: an ecotoxicological perspective. Integr. Comp. Biol. 54:77–86 [Google Scholar]
  66. Matsumoto Y, Buemio A, Chu R, Vafaee M, Crews D. 66.  2013. Epigenetic control of gonadal aromatase (cyp19a1) in temperature-dependent sex determination of red-eared slider turtles. PLOS ONE 8:e63599 [Google Scholar]
  67. Parrott BB, Kohno S, Cloy-McCoy JA, Guillette JLJ. 67.  2014. Differential incubation temperatures result in dimorphic DNA methylation patterning of the SOX9 and aromatase promoters in gonads of alligator (Alligator mississippiensis) embryos. Biol. Reprod. 90:21–11 [Google Scholar]
  68. Kucharski R, Maleszka J, Foret S, Maleszka R. 68.  2008. Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827 [Google Scholar]
  69. Anway MD, Cupp AS, Uzumcu M, Skinner MK. 69.  2005. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466 [Google Scholar]
  70. Skinner MK, Haque CG-BM, Nilsson E, Bhandari R, McCarrey JR. 70.  2013. Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line. PLOS ONE 8:e66318 [Google Scholar]
  71. Wolstenholme JT, Edwards M, Shetty SRJ, Gatewood JD, Taylor JA. 71.  et al. 2012. Gestational exposure to bisphenol A produces transgenerational changes in behaviors and gene expression. Endocrinology 153:3828–38 [Google Scholar]
  72. Head JA, Dolinoy DC, Basu N. 72.  2012. Epigenetics for ecotoxicologists. Environ. Toxicol. Chem. 31:221–27 [Google Scholar]
  73. Vandegehuchte MB, Janssen CR. 73.  2011. Epigenetics and its implications for ecotoxicology. Ecotoxicology 20:607–24 [Google Scholar]
  74. Schwindt AR. 74.  2015. Parental effects of endocrine disrupting compounds in aquatic wildlife: Is there evidence of transgenerational inheritance?. Gen. Comp. Endocrinol. 219:152–64 [Google Scholar]
  75. Kortenkamp A. 75.  2007. Ten years of mixing cocktails: a review of combination effects of endocrine-disrupting chemicals. Environ. Health Perspect. 115:98–105 [Google Scholar]
  76. Manikkam M, Guerrero-Bosagna C, Tracey R, Haque MM, Skinner MK. 76.  2012. Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures. PLOS ONE 7:e31901 [Google Scholar]
  77. Nilsen FM, Parrott BB, Bowden JA, Kassim BL, Somerville SE. 77.  et al. 2016. Global DNA methylation loss associated with mercury contamination and aging in the American alligator (Alligator mississippiensis). Sci. Total Environ. 545–46:389–97 [Google Scholar]
  78. Guillette LJ Jr., Parrott BB, Nilsson E, Haque MM, Skinner MK. 78.  2016. Epigenetic programming alterations in alligators from environmentally contaminated lakes. Gen. Comp. Endocrinol. 238:4–12 [Google Scholar]
  79. Martyniuk CJ, Simmons DB. 79.  2016. Spotlight on environmental omics and toxicology: a long way in a short time. Comp. Biochem. Physiol. D Genom. Proteom. 19:97–101 [Google Scholar]
  80. Simmons DBD, Benskin JP, Cosgrove JR, Duncker BP, Ekman DR. 80.  et al. 2015. Omics for aquatic ecotoxicology: control of extraneous variability to enhance the analysis of environmental effects. Environ. Toxicol. Chem. 34:1693–704 [Google Scholar]
  81. Baker ME, Hardiman G. 81.  2014. Transcriptional analysis of endocrine disruption using zebrafish and massively parallel sequencing. J. Mol. Endocrinol. 52:R241–R56 [Google Scholar]
  82. Martyniuk CJ, Doperalski NJ, Prucha MS, Zhang J-L, Kroll KJ. 82.  et al. 2016. High contaminant loads in Lake Apopka's riparian wetland disrupt gene networks involved in reproduction and immune function in largemouth bass. Comp. Biochem. Physiol. D Genom. Proteom. 19:140–50 [Google Scholar]
  83. Maier T, Güell M, Serrano L. 83.  2009. Correlation of mRNA and protein in complex biological samples. FEBS Lett 583:3966–73 [Google Scholar]
  84. Martyniuk CJ, Houlahan J. 84.  2013. Assessing gene network stability and individual variability in the fathead minnow (Pimephales promelas) transcriptome. Comp. Biochem. Physiol. D Genom. Proteom. 8:283–91 [Google Scholar]
  85. Bissegger S, Martyniuk CJ, Langlois VS. 85.  2014. Transcriptomic profiling in Silurana tropicalis testes exposed to finasteride. Gen. Comp. Endocrinol. 203:137–45 [Google Scholar]
  86. Veldhoen N, Skirrow RC, Brown LLY, van Aggelen G, Helbing CC. 86.  2014. Effects of acute exposure to the non-steroidal anti-inflammatory drug ibuprofen on the developing North American bullfrog (Rana catesbeiana) tadpole. Environ. Sci. Technol. 48:10439–47 [Google Scholar]
  87. Johnson SA, Spollen WG, Manshack LK, Bivens NJ, Givan SA, Rosenfeld CS. 87.  2017. Hypothalamic transcriptomic alterations in male and female California mice (Peromyscus californicus) developmentally exposed to bisphenol A or ethinyl estradiol. Physiol. Rep. 5:e13133 [Google Scholar]
  88. Manshack LK, Conard CM, Bryan SJ, Deem SL, Holliday DK. 88.  et al. 2017. Transcriptomic alterations in the brain of painted turtles (Chrysemys picta) developmentally exposed to bisphenol A or ethinyl estradiol. Physiol. Genom. 49:201–15 [Google Scholar]
  89. Collette TW, Skelton DM, Davis JM, Cavallin JE, Jensen KM. 89.  et al. 2016. Metabolite profiles of repeatedly sampled urine from male fathead minnows (Pimephales promelas) contain unique lipid signatures following exposure to anti-androgens. Comp. Biochem. Physiol. D Genom. Proteom. 19:190–98 [Google Scholar]
  90. Steiner CC, Putnam AS, Hoeck PEA, Ryder OA. 90.  2013. Conservation genomics of threatened animal species. Annu. Rev. Anim. Biosci. 1:261–81 [Google Scholar]
/content/journals/10.1146/annurev-animal-030117-014547
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Reproductive Impacts of Endocrine-Disrupting Chemicals on Wildlife Species: Implications for Conservation of Endangered Species
Annual Review of Animal Biosciences 6, 287 (2018); https://doi.org/10.1146/annurev-animal-030117-014547
/content/journals/10.1146/annurev-animal-030117-014547
/content/journals/10.1146/annurev-animal-030117-014547
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