Xenopus laevis as a Bioindicator of Endocrine Disruptors in the Region of Central Chile

  • Sylvia Rojas-HucksEmail author
  • Arno C. Gutleb
  • Carlos M. González
  • Servane Contal
  • Kahina Mehennaoui
  • An Jacobs
  • Hilda E. Witters
  • José Pulgar


One of the direct causes of biodiversity loss is environmental pollution resulting from the use of chemicals. Different kinds of chemicals, such as persistent organic pollutants and some heavy metals, can be endocrine disruptors, which act at low doses over a long period of time and have a negative effect on the reproductive and thyroid system in vertebrates worldwide. Research on the effects of endocrine disruptors and the use of bioindicators in neotropical ecosystems where pressure on biodiversity is high is scarce. In Chile, although endocrine disruptors have been detected at different concentrations in the environments of some ecosystems, few studies have been performed on their biological effects in the field. In this work, Xenopus laevis (African clawed frog), an introduced species, is used as a bioindicator for the presence of endocrine disruptors in aquatic systems with different degrees of contamination in a Mediterranean zone in central Chile. For the first time for Chile, alterations are described that can be linked to exposure to endocrine disruptors, such as vitellogenin induction, decreased testosterone in male frogs, and histological changes in gonads. Dioxin-like and oestrogenic activity was detected in sediments at locations where it seem to be related to alterations found in the frogs. In addition, an analysis of land use/cover use revealed that urban soil was the best model to explain the variations in frog health indicators. This study points to the usefulness of an invasive species as a bioindicator for the presence of endocrine-disruptive chemicals.



The authors acknowledge the support of Boris Unterreiner for his help with sediment extraction. Mauricio Montaño is acknowledged for his assistance with the Luc-Assay calculations, and Caroll Stoore and Christian Hidalgo for their help in performing the ELISA tests. The authors acknowledge Dr. P. Balaguer (INSERM) who kindly provided the MELN cells and Dra. Angela Hernandez for her help with the coverage and land use analysis. The authors thank Lindsey Auguin for the language corrections. This research was conducted according to the Chilean wildlife regulations pertaining to permits 1545/2014, 7545/2014, and 8550/2014 of the Livestock and Agriculture Service (SAG) and permit 005/2014 of the Corporación Nacional Forestal de Chile (CONAF). This research was funded by the Fellowship Programme and the Dirección General de Investigación y Doctorados, Universidad Andres Bello, Number DI-592-14.

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  1. Abdel-Moneim AM, Al-Kahtani MA, Elmenshawy OM (2012) Histopathological biomarkers in gills and liver of Oreochromis niloticus from polluted wetland environments, Saudi Arabia. Chemosphere 88:1028–1035. Google Scholar
  2. Agbohessi PT, Toko II, Atchou V et al (2015) Pesticides used in cotton production affect reproductive development, endocrine regulation, liver status and offspring fitness in African catfish Clarias gariepinus (Burchell, 1822). Comp Biochem Physiol Part C Toxicol Pharmacol 167:157–172. Google Scholar
  3. Agius C, Roberts RJ (2003) Melanomacrophage centres and their role in fish pathology. J Fish Dis 26:499–509. Google Scholar
  4. Allinson G, Zhang P, Bui AD et al (2015) Pesticide and trace metal occurrence and aquatic benchmark exceedances in surface waters and sediments of urban wetlands and retention ponds in Melbourne, Australia. Environ Sci Pollut Res 22:10214–10226. Google Scholar
  5. Aris AZ, Shamsuddin AS, Praveena SM (2014) Occurrence of 17α-ethynylestradiol (EE2) in the environment and effect on exposed biota: a review. Environ Int 69:104–119. Google Scholar
  6. Avberšek M, Žegura B, Filipič M et al (2013) Determination of estrogenic potential in waste water without sample extraction. J Hazard Mater 260:527–533. Google Scholar
  7. Bartell S (2006) Biomarkers, bioindicators, and ecological risk assessment—a brief review and evaluation. Environ Bioindic 1:60–73. Google Scholar
  8. Barton K (2014) MuMIn: multi-model inference. R package version 1.10.5. Accessed 8 Aug 2014
  9. Bates D, Maechler M, Bolker B et al (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. Google Scholar
  10. Berckmans P, Leppens H, Vangenechten C, Witters H (2007) Screening of endocrine disrupting chemicals with MELN cells, an ER-transactivation assay combined with cytotoxicity assessment. Toxicol Vitro 21:1262–1267. Google Scholar
  11. Berg V, Lyche JL, Karlsson C et al (2011) Accumulation and effects of natural mixtures of persistent organic pollutants (POP) in Zebrafish after two generations of exposure. J Toxicol Environ Health Part A 74:407–423. Google Scholar
  12. Bergman Å, Heindel JJ, Kasten T et al (2013) The impact of endocrine disruption: a consensus statement on the state of the science. Environ Health Perspect 121:104–106. Google Scholar
  13. Bernet D, Schmidt H, Meier W et al (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34. Google Scholar
  14. Besselink HT, Schipper C, Klamer H et al (2004) Intra- and interlaboratory calibration of the DR CALUX bioassay for the analysis of dioxins and dioxin-like chemicals in sediments. Environ Toxicol Chem 23:2781–2789. Google Scholar
  15. Bicho RC, Amaral MJ, Faustino AMR et al (2013) Thyroid disruption in the lizard Podarcis bocagei exposed to a mixture of herbicides: a field study. Ecotoxicology 22:156–165. Google Scholar
  16. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  17. Calle P, Alvarado O, Monserrate L et al (2015) Mercury accumulation in sediments and seabird feathers from the Antarctic Peninsula. Mar Pollut Bull 91:410–417. Google Scholar
  18. Campos I, Abrantes N, Keizer JJ et al (2016) Major and trace elements in soils and ashes of eucalypt and pine forest plantations in Portugal following a wildfire. Sci Total Environ 572:1363–1376. Google Scholar
  19. Carpenter DO (2011) Health effects of persistent organic pollutants: the challenge for the Pacific Basin and for the world. Rev Environ Health 26:61–69. Google Scholar
  20. Casals-Casas C, Desvergne B (2011) Endocrine disruptors: from endocrine to metabolic disruption. Annu Rev Physiol 73:135–162. Google Scholar
  21. Cevasco A, Urbatzka R, Bottero S et al (2008) Endocrine disrupting chemicals (EDC) with (anti)estrogenic and (anti)androgenic modes of action affecting reproductive biology of Xenopus laevis: II. Effects on gonad histomorphology. Comp Biochem Physiol C: Toxicol Pharmacol 147:241–251. Google Scholar
  22. Chuvieco E (2002) Teledeteccion ambiental: La observacion de la Tierra Desde el Espacio. Ariel Ciencia, BarcelonaGoogle Scholar
  23. Coady KK, Murphy MB, Villeneuve DL et al (2005) Effects of atrazine on metamorphosis, growth, laryngeal and gonadal development, aromatase activity, and sex steroid concentrations in Xenopus laevis. Ecotoxicol Environ Saf 62:160–173. Google Scholar
  24. Cong L, Qin Z-F, Jing X-N et al (2006) Xenopus laevis is a potential alternative model animal species to study reproductive toxicity of phytoestrogens. Aquat Toxicol 77:250–260. Google Scholar
  25. Costa PM, Caeiro S, Lobo J et al (2011) Estuarine ecological risk based on hepatic histopathological indices from laboratory and in situ tested fish. Mar Pollut Bull 62:55–65. Google Scholar
  26. Cuevas N, Zorita I, Costa PM et al (2015) Development of histopathological indices in the digestive gland and gonad of mussels: integration with contamination levels and effects of confounding factors. Aquat Toxicol 162:152–164. Google Scholar
  27. Daly GL, Lei YD, Teixeira C et al (2007) Accumulation of current-use pesticides in neotropical montane forests. Environ Sci Technol 41:1118–1123. Google Scholar
  28. Diamanti-Kandarakis E, Bourguignon J-P, Giudice LC et al (2009) Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 30:293–342. Google Scholar
  29. Dislich C, Keyel AC, Salecker J et al (2017) A review of the ecosystem functions in oil palm plantations, using forests as a reference system. Biol Rev 92:1539–1569. Google Scholar
  30. Douglas A, Bolker B, Walker S et al (2017) Linear mixed-effects models using “Eigen” and S4. Accessed 27 Sept 2017
  31. Ellis EA, Baerenklau KA, Marcos-Martínez R, Chávez E (2010) Land use/land cover change dynamics and drivers in a low-grade marginal coffee growing region of Veracruz, Mexico. Agrofor Syst 80:61–84. Google Scholar
  32. Fenoglio C, Boncompagni E, Fasola M et al (2005) Effects of environmental pollution on the liver parenchymal cells and Kupffer-melanomacrophagic cells of the frog Rana esculenta. Ecotoxicol Environ Saf 60:259–268. Google Scholar
  33. Folmar LC, Gardner GR, Schreibman MP et al (2001) Vitellogenin-induced pathology in male summer flounder (Paralichthys dentatus). Aquat Toxicol 51:431–441. Google Scholar
  34. Fuzzen MLM, Bragg LM, Tetreault GR et al (2016) An assessment of the spatial and temporal variability of biological responses to municipal wastewater effluent in rainbow darter (Etheostoma caeruleum) collected along an urban gradient. PLoS ONE 11:1–31. Google Scholar
  35. Gadzala-Kopciuch R, Berecka B, Bartoszewicz J, Buszewski B (2004) Some considerations about bioindicators in environmental monitoring. Pol J Environ Stud 13:453–462Google Scholar
  36. Ge J, Liu M, Yun X et al (2014) Occurrence, distribution and seasonal variations of polychlorinated biphenyls and polybrominated diphenyl ethers in surface waters of the East Lake, China. Chemosphere 103:256–262. Google Scholar
  37. Gibson L, Lynam AJ, Bradshaw CJA et al (2013) Near-complete extinction of native small mammal fauna 25 years after forest fragmentation. Science 341:1508–1510. Google Scholar
  38. Green CD, Tata JR (1976) Direct induction by estradiol on vitellogenin synthesis in organ cultures of male Xenopus laevis liver. Cell 7:131–139. Google Scholar
  39. Hamers T, Leonards PEG, Legler J et al (2010) Toxicity profiling: an integrated effect-based tool for site-specific sediment quality assessment. Integr Environ Assess Manag 6:761–773. Google Scholar
  40. Hamlin HJ, Guillette LJ (2010) Birth defects in wildlife: the role of environmental contaminants as inducers of reproductive and developmental dysfunction. Syst Biol Reprod Med 56:113–121. Google Scholar
  41. Hamlin HJ, Guillette LJ (2011) Embryos as targets of endocrine disrupting contaminants in wildlife. Birth Defects Res Part C Embryo Today Rev 93:19–33. Google Scholar
  42. Hayes TB, Collins A, Lee M et al (2002) Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci U S A 99:5476–5480. Google Scholar
  43. Hayes TB, Case P, Chui S et al (2006) Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact? Environ Health Perspect 114:40–50. Google Scholar
  44. Hayes TB, Falso P, Gallipeau S, Stice M (2010a) The cause of global amphibian declines: a developmental endocrinologist’s perspective. J Exp Biol 213:921–933. Google Scholar
  45. Hayes TB, Khoury V, Narayan A et al (2010b) Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). Proc Natl Acad Sci 107:4612–4617. Google Scholar
  46. Hecker M, Giesy JP, Jones PD et al (2004) Plasma sex steroid concentrations and gonadal aromatase activities in African clawed frogs (Xenopus laevis) from South Africa. Environ Toxicol Chem 23:1996–2007. Google Scholar
  47. Hecker M, Kim WJ, Park J-W et al (2005) Plasma concentrations of estradiol and testosterone, gonadal aromatase activity and ultrastructure of the testis in Xenopus laevis exposed to estradiol or atrazine. Aquat Toxicol 72:383–396. Google Scholar
  48. Hernández A, Miranda M, Arellano EC et al (2015) Landscape dynamics and their effect on the functional connectivity of a Mediterranean landscape in Chile. Ecol Indic 48:198–206. Google Scholar
  49. Hilty J, Merenlender A (2000) Faunal indicator taxa selection for monitoring ecosystem health. Biol Conserv 92:185–197. Google Scholar
  50. Holt EA, Miller SW (2010) Bioindicators: using organisms to measure environmental impacts. Nat Educ Knowl 3:8Google Scholar
  51. Houtman CJ, Cenijn PH, Hamers T et al (2004) Toxicological profiling of sediments using in vitro bioassays, with emphasis on endocrine disruption. Environ Toxicol Chem 23:32–40. Google Scholar
  52. Iglesias-Carrasco M, Martín J, Cabido C (2017) Urban habitats can affect body size and body condition but not immune response in amphibians. Urban Ecosyst. Google Scholar
  53. Islam MS, Ahmed MK, Raknuzzaman M et al (2015) Heavy metal pollution in surface water and sediment: a preliminary assessment of an urban river in a developing country. Ecol Indic 48:282–291. Google Scholar
  54. Jantawongsri K, Thammachoti P, Kitana J et al (2015) Altered immune response of the rice frog Fejervarya limnocharis living in agricultural area with intensive herbicide utilization at Nan Province, Thailand. EnvironmentAsia 8:68–74. Google Scholar
  55. King-Heiden TC, Mehta V, Xiong KM et al (2012) Reproductive and developmental toxicity of dioxin in fish. Mol Cell Endocrinol 354:121–138. Google Scholar
  56. Legler J, Dennekamp M, Vethaak AD et al (2002) Detection of estrogenic activity in sediment-associated compounds using in vitro reporter gene assays. Sci Total Environ 293:69–83. Google Scholar
  57. Li S, Li M, Gui W et al (2017) Disrupting effects of azocyclotin to the hypothalamo–pituitary–gonadal axis and reproduction of Xenopus laevis. Aquat Toxicol 185:121–128. Google Scholar
  58. Liebel S, Tomotake MEM, Oliveira-ribeiro CA (2013) Fish histopathology as biomarker to evaluate water quality. Ecotoxicol Environ Contam 8:9–15. Google Scholar
  59. Linde-Arias AR, Inácio AF, de Alburquerque C et al (2008) Biomarkers in an invasive fish species, Oreochromis niloticus, to assess the effects of pollution in a highly degraded Brazilian River. Sci Total Environ 399:186–192. Google Scholar
  60. Lobos G, Jaksic FM (2005) The ongoing invasion of African clawed frogs (Xenopus laevis) in Chile: causes of concern. Biodivers Conserv 14:429–439. Google Scholar
  61. López-Doval JC, Montagner CC, de Alburquerque AF et al (2017) Nutrients, emerging pollutants and pesticides in a tropical urban reservoir: spatial distributions and risk assessment. Sci Total Environ 575:1307–1324. Google Scholar
  62. Louiz I, Ben-Attia M, Ben-Hassine OK (2009) Gonadosomatic index and gonad histopathology of Gobius niger (Gobiidea, Teleost) from Bizerta lagoon (Tunisia): evidence of reproduction disturbance. Fish Res 100:266–273. Google Scholar
  63. Loumbourdis NS, Vogiatzis AK (2002) Impact of cadmium on liver pigmentary system of the frog Rana ridibunda. Ecotoxicol Environ Saf 53:52–58. Google Scholar
  64. MacCracken JG, Stebbings JL (2012) Test of a body condition index with amphibians. J Herpetol 46:346–350. Google Scholar
  65. Mace GM, Norris K, Fitter AH (2012) Biodiversity and ecosystem services: a multilayered relationship. Trends Ecol Evol 27:19–25. Google Scholar
  66. Marchand MJ, van Dyk JC, Pieterse GM et al (2009) Histopathological alterations in the liver of the sharptooth catfish Clarias gariepinus from polluted aquatic systems in South Africa. Environ Toxicol 24:133–147. Google Scholar
  67. Marchand MJ, Pieterse GM, Barnhoorn IEJ (2010) Sperm motility and testicular histology as reproductive indicators of fish health of two feral fish species from a currently DDT sprayed area, South Africa. J Appl Ichthyol 26:707–714. Google Scholar
  68. Matsumura N, Ishibashi H, Hirano M et al (2005) Effects of nonylphenol and triclosan on production of plasma vitellogenin and testosterone in male South African clawed frogs (Xenopus laevis). Biol Pharm Bull 28:1748–1751. Google Scholar
  69. McCoy KA, Hoang LK, Guillette LJ Jr, St. Mary CM (2008) Renal pathologies in giant toads (Bufo marinus) vary with land use. Sci Total Environ 407:348–357. Google Scholar
  70. McDaniel TV, Martin PA, Struger J et al (2008) Potential endocrine disruption of sexual development in free ranging male northern leopard frogs (Rana pipiens) and green frogs (Rana clamitans) from areas of intensive row crop agriculture. Aquat Toxicol 88:230–242. Google Scholar
  71. Mcgeoch MA (1998) The selection, testing, and application of terrestrial insects as bioindicators. Biol Rev 73:181–201. Google Scholar
  72. McGeoch MA, Butchart SHM, Spear D et al (2010) Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Divers Distrib 16:95–108. Google Scholar
  73. Mela M, Randi MAF, Ventura DF et al (2007) Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias malabaricus. Ecotoxicol Environ Saf 68:426–435. Google Scholar
  74. Mercer EV, Mercer TG, Sayok AK (2014) Effects of forest conversions to oil palm plantations on freshwater macroinvertebrates: a case study from Sarawak, Malaysia. J Land Use Sci 9:260–277. Google Scholar
  75. Millennium Ecosystem Assessment (2005) Ecosystems and human well-being: biodiversity synthesis. World Resources Institute, Washington, DCGoogle Scholar
  76. Mitsui N, Tooi O, Kawahara A (2003) Sandwich ELISAs for quantification of Xenopus laevis vitellogenin and albumin and their application to measurement of estradiol-17 beta effects on whole animals and primary-cultured hepatocytes. Comp Biochem Physiol C: Toxicol Pharmacol 135C:305–313. Google Scholar
  77. Montaño M, Zimmer KE, Dahl E et al (2011) Effects of mixtures of persistent organic pollutants (POPs) derived from cod liver oil on H295R steroidogenesis. Food Chem Toxicol 49:2328–2335. Google Scholar
  78. Montaño M, Gutleb AC, Murk AJ (2013) Persistent toxic burdens of halogenated phenolic compounds in humans and wildlife. Environ Sci Technol 47:6071–6081. Google Scholar
  79. Montaño M, Murk AJ, Gutleb AC (2014) Impact of sediment sample stock concentration on bioassay based toxicological risk characterization. J Soils Sediments 14:1200–1212. Google Scholar
  80. Morrissey CA, Stanton DWG, Pereira MG et al (2013) Eurasian dipper eggs indicate elevated organohalogenated contaminants in urban rivers. Environ Sci Technol 47:8931–8939. Google Scholar
  81. Murk AJ, Leonards PEG, van Hattum B et al (1998) Application of biomarkers for exposure and effect of polyhydrogenated aromatic hydrocarbons in naturally exposed European otter (Lutra lutra). Environ Toxicol Pharmacol 6:91–102. Google Scholar
  82. Murphy MO, Agha M, Maigret TA et al (2016) The effects of urbanization on body size of larval stream salamanders. Urban Ecosyst 19:275–286. Google Scholar
  83. Nomen R, Sempere J, Chávez F et al (2012) Measurement of pollution levels of organochlorine and organophosphorus pesticides in water, soil, sediment, and shrimp to identify possible impacts on shrimp production at Jiquilisco Bay. Environ Sci Pollut Res Int 19:3547–3555. Google Scholar
  84. Oka T, Tooi O, Mitsui N et al (2008) Effect of atrazine on metamorphosis and sexual differentiation in Xenopus laevis. Aquat Toxicol 87:215–226. Google Scholar
  85. Oliveira Ribeiro CA, Vollaire Y, Sanchez-Chardi A, Roche H (2005) Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the Eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquat Toxicol 74:53–69. Google Scholar
  86. Ortiz JB, de González Canales ML, Sarasquete C (2003) Histopathological changes induced by lindane (γ-HCH) in various organs of fishes. Sci Mar 67:53–61. Google Scholar
  87. Orton F, Baynes A, Clare F et al (2014) Body size, nuptial pad size and hormone levels: potential non-destructive biomarkers of reproductive health in wild toads (Bufo bufo). Ecotoxicology 23:1359–1365Google Scholar
  88. Osman AGM (2010) Enzymatic and histopathologic biomarkers as indicators of aquatic pollution in fishes. Nat Sci 02:1302–1311. Google Scholar
  89. Palmer B, Palmer S (1995) Vitellogenin induction by xenobiotic estrogens in the red-eared turtle and African clawed frog. Environ Health Perspect 103:19–25. Google Scholar
  90. Păunescu A, Ponepal CM, Drăghici O, Marinescu AG (2010) Liver histopathologic alterations in the frog rana (Pelophylax ridibunda) induce by the action of Reldan 40EC insecticide. Analele Univ din Oradea Fasc Biol 17:166–169Google Scholar
  91. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891. Google Scholar
  92. Peig J, Green AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol 24:1323–1332. Google Scholar
  93. Pimm SL, Jenkins CN, Abell R et al (2014) The biodiversity of species and their rates of extinction, distribution, and protection. Science 344:1246752. Google Scholar
  94. Prado PS, Souza CC, Bazzoli N, Rizzo E (2011) Reproductive disruption in lambari Astyanax fasciatus from a Southeastern Brazilian reservoir. Ecotoxicol Environ Saf 74:1879–1887. Google Scholar
  95. Pysek P, Richardson DM (2010) Invasive species, environmental change and management, and health. Annu Rev Environ Resour 35:25–55. Google Scholar
  96. Qin Z-F, Qin X-F, Yang L et al (2007) Feminizing/demasculinizing effects of polychlorinated biphenyls on the secondary sexual development of Xenopus laevis. Aquat Toxicol 84:321–327. Google Scholar
  97. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  98. Rasar MA, Hammes SR (2006) The physiology of the Xenopus laevis ovary. In: Liu XJ (ed) Xenopus protocols: cell biology and signal transduction. Humana Press Inc., Totowa, pp 17–30Google Scholar
  99. Rey Vázquez G, Meijide FJ, Da Cuña RH et al (2009) Exposure to waterborne 4-tert-octylphenol induces vitellogenin synthesis and disrupts testis morphology in the South American freshwater fish Cichlasoma dimerus (Teleostei, Perciformes). Comp Biochem Physiol C: Toxicol Pharmacol 150:298–306. Google Scholar
  100. Ribeiro CADO, Katsumiti A, França P et al (2013) Biomarkers responses in fish (Atherinella brasiliensis) of paranaguá bay, southern Brazil, for assessment of pollutant effects. Braz J Oceanogr 61:1–11. Google Scholar
  101. Rowe CL (2008) “The calamity of so long life”: life histories, contaminants, and potential emerging threats to long-lived vertebrates. Bioscience 58:623. Google Scholar
  102. Safholm M, Norder A, Fick J, Berg C (2012) Disrupted oogenesis in the frog Xenopus tropicalis after exposure to environmental progestin concentrations. Biol Reprod 86:126. Google Scholar
  103. Scheffers BR, Paszkowski CA (2016) Large body size for metamorphic wood frogs in urban stormwater wetlands. Urban Ecosyst 19:347–359. Google Scholar
  104. Schipper CA, Rietjens IMCM, Burgess RM, Murk AJ (2010) Application of bioassays in toxicological hazard, risk and impact assessments of dredged sediments. Mar Pollut Bull 60:2026–2042. Google Scholar
  105. Shih SI, Lee WJ, Lin LF et al (2008) Significance of biomass open burning on the levels of polychlorinated dibenzo-p-dioxins and dibenzofurans in the ambient air. J Hazard Mater 153:276–284. Google Scholar
  106. Silva AG, Martinez CBR (2007) Morphological changes in the kidney of a fish living in an urban stream. Environ Toxicol Pharmacol 23:185–192. Google Scholar
  107. Soufy H, Soliman M, El-Manakhly E, Gaafa A (2007) Some biochemical and pathological investigations on monosex Tilapia following chronic exposure to carbofuran pesticides. Glob Vet 1:45–52Google Scholar
  108. Stronkhorst J, Leonards P, Murk AJ (2002) Using the dioxin receptor-CALUX in vitro bioassay to screen marine harbor sediments for compounds with a dioxin-like mode of action. Environ Toxicol Chem 21:2552–2561. Google Scholar
  109. Suzuki G, Someya M, Matsukami H, Minh N (2016) Comprehensive evaluation of dioxins and dioxin-like compounds in surface soils and river sediments from e-waste-processing sites in a village in northern Vietnam: heading towards the environmentally sound management of e-waste. Emerg Contam 2:98–108. Google Scholar
  110. Svartz GV, Herkovits J, Pérez-Coll CS (2012) Sublethal effects of atrazine on embryo-larval development of Rhinella arenarum (Anura: Bufonidae). Ecotoxicology 21:1251–1259. Google Scholar
  111. Tamschick S, Rozenblut-Koscisty B, Ogielska M et al (2016a) Sex reversal assessments reveal different vulnerability to endocrine disruption between deeply diverged anuran lineages. Sci Rep 6:1–8. Google Scholar
  112. Tamschick S, Rozenblut-Kościsty B, Ogielska M et al (2016b) Impaired gonadal and somatic development corroborate vulnerability differences to the synthetic estrogen ethinylestradiol among deeply diverged anuran lineages. Aquat Toxicol 177:503–514. Google Scholar
  113. Tamschick S, Rozenblut-Kościsty B, Ogielska M et al (2016c) The plasticizer bisphenol A affects somatic and sexual development, but differently in pipid, hylid and bufonid anurans. Environ Pollut 216:282–291Google Scholar
  114. Tijani JO, Fatoba OO, Petrik LF (2013) A review of pharmaceuticals and endocrine-disrupting compounds: sources, effects, removal, and detections. Water Air Soil Pollut 224:1770. Google Scholar
  115. Tompsett AR, Wiseman S, Higley E et al (2012) Effects of 17α-ethynylestradiol on sexual differentiation and development of the African clawed frog (Xenopus laevis). Comp Biochem Physiol Part C Toxicol Pharmacol 156:202–210. Google Scholar
  116. Torreilles S, McClure D, Green S (2009) Evaluation and refinement of euthanasia methods for Xenopus laevis. J Am Assoc Lab Anim Sci 48:512–516Google Scholar
  117. Troncoso IC, Cazenave J, Bacchetta C, de los Bistoni MA (2012) Histopathological changes in the gills and liver of Prochilodus lineatus from the Salado River basin (Santa Fe, Argentina). Fish Physiol Biochem 38:693–702. Google Scholar
  118. Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149Google Scholar
  119. van Dyk JC, Marchand MJ, Smit NJ, Pieterse GM (2009) A histology-based fish health assessment of four commercially and ecologically important species from the Okavango Delta panhandle, Botswana. Afr J Aquat Sci 34:273–282. Google Scholar
  120. Van Dyk JC, Cochrane MJ, Wagenaar GM (2012) Liver histopathology of the sharptooth catfish Clarias gariepinus as a biomarker of aquatic pollution. Chemosphere 87:301–311. Google Scholar
  121. van Wyk JH, Pool EJ, Leslie AJ (2003) The effects of anti-androgenic and estrogenic disrupting contaminants on breeding gland (nuptial pad) morphology, plasma testosterone levels, and plasma vitellogenin levels in male Xenopus laevis (African clawed frog). Arch Environ Contam Toxicol 44:247–256. Google Scholar
  122. Vrabie CM, Jonker MTO, Murk AJ (2009) Specific in vitro toxicity of crude and refined petroleum products. 1. Aryl hydrocarbon receptor-mediated responses. Environ Toxicol Chem 28:1995–2003. Google Scholar
  123. White SS, Birnbaum LS (2009) An overview of the effects of dioxins and dioxin-like compounds on vertebrates, as documented in human and ecological epidemiology. J Environ Sci Heal Part C Environ Carcinog Ecotoxicol Rev 27:197–211. Google Scholar
  124. Willis KJ, Bhagwat SA (2009) Biodiversity and climate change. Science 326:806–807. Google Scholar
  125. Witters H, Freyberger A, Smits K et al (2010) The assessment of estrogenic or anti-estrogenic activity of chemicals by the human stably transfected estrogen sensitive MELN cell line: results of test performance and transferability. Reprod Toxicol 30:60–72. Google Scholar
  126. Wright K, Whitaker B (2001) Amphibian medicine and captive husbandry. Krieger Publishing Company, MalabarGoogle Scholar
  127. Zava DT, Blen M, Duwel G (1997) Estrogenic activity of natural and synthetic estrogens in human breast cancer cells in culture. Environ Health Perspect 105:637–645. Google Scholar
  128. Zhang Q, Huang J, Yu G (2008) Polychlorinated dibenzo-p-dioxins and dibenzofurans emissions from open burning of crop residues in China between 1997 and 2004. Environ Pollut 151:39–46. Google Scholar
  129. Zillioux EJ, Johnson IC, Kiparissis Y et al (2001) The sheepshead minnow as an in vivo model for endocrine disruption in marine teleosts: a partial life-cycle test with 17α-ethynylestradiol. Environ Toxicol Chem 20:1968–1978. Google Scholar
  130. Zimmerli S, Bernet D, Burkhardt-Holm P et al (2007) Assessment of fish health status in four Swiss rivers showing a decline of brown trout catches. Aquat Sci 69:11–25. Google Scholar
  131. Zohar I, Bookman R, Levin N et al (2014) Contamination history of lead and other trace metals reconstructed from an urban winter pond in the Eastern Mediterranean Coast (Israel). Environ Sci Technol 48:13592–13600. Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Sylvia Rojas-Hucks
    • 1
    Email author
  • Arno C. Gutleb
    • 3
  • Carlos M. González
    • 2
  • Servane Contal
    • 3
  • Kahina Mehennaoui
    • 3
  • An Jacobs
    • 4
  • Hilda E. Witters
    • 4
  • José Pulgar
    • 1
  1. 1.Departamento de Ecología y Biodiversidad, Facultad Ciencias de la VidaUniversidad Andres BelloSantiagoChile
  2. 2.Escuela de Medicina Veterinaria, Facultad Ciencias de la VidaUniversidad Andres BelloSantiagoChile
  3. 3.Environmental Research and Innovation (ERIN) DepartmentLuxembourg Institute of Science and Technology (LIST)Esch-sur-AlzetteLuxembourg
  4. 4.Department Environmental Health and Risk, Team Applied Bio and Molecular Sciences (ABS)Flemish Institute for Technological Research (VITO)MolBelgium

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