Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Endosulfan (ES), a persistent organochlorine pesticide, is widely used despite its toxicity to non-target animals. Upon reaching water bodies, ES can cause negative effects on aquatic animals, including disruption of hormonal systems. However, the action of ES on fish reproductive axis has been hardly studied thus far. The aim of the present work was to assess the endocrine disruptive potential of endosulfan on the pituitary gonadotropins levels and on the testes function due to ES in the South American freshwater fish Cichlasoma dimerus, using in vitro and in vivo approaches. In vitro experiments showed that ES inhibited the LH-stimulated steroidogenesis in gonads; no change was observed in gonadotropins release from pituitaries in culture. Laboratory waterborne ES (0.1, 0.3 and 1 μg/L) exposure for two months caused decrease in βFSH pituitary content and γGT activity in the testes (Sertoli cell function marker). Testicular histology revealed pathologies such as scarce intermediate stages of spermatogenesis, release of immature germ cells into the lobular lumen, presence of foam cells and interstitial fibrosis. As FSH and FSH-mediated steroidogenesis regulate spermatogenesis and Sertoli cell function, the effect of ES on FSH could be responsible for the morphological alterations observed in testes. In vitro, ES disrupted steroidogenesis in gonads, therefore similar effects in vivo cannot be ruled out. Based on this evidence, ES exhibits an endocrine disruptive action on the reproductive axis of C. dimerus, causing disruption at the pituitary and/or at the gonad level. These effects could acquire ecological significance under prolonged exposure to the pesticide in nature. © 2012 Elsevier B.V.

Registro:

Documento: Artículo
Título:Endocrine disruptive potential of endosulfan on the reproductive axis of Cichlasoma dimerus (Perciformes, Cichlidae)
Autor:Da Cuña, R.H.; Pandolfi, M.; Genovese, G.; Piazza, Y.; Ansaldo, M.; Lo Nostro, F.L.
Filiación:Laboratorio de Ecotoxicología Acuática DBBE, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, C1428EHA, Argentina
Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Ciudad Autónoma de Buenos Aires, C1033AAJ, Argentina
Laboratorio de Neuroendocrinología y Comportamiento DBBE, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, C1428EHA, Argentina
Instituto Antártico Argentino, Dirección Nacional del Antártico, Ciudad Autónoma de Buenos Aires, C1010AAZ, Argentina
Palabras clave:Cichlid fish; Endocrine disruption; Endosulfan; Gonadotropins; Sex steroids; Testes pathology; endosulfan; follitropin beta subunit; gamma glutamyltransferase; gonadotropin; luteinizing hormone; endocrine disruptor; endosulfan; morphology; organochlorine; perciform; pesticide; reproductive effort; toxicity; animal cell; animal experiment; animal tissue; article; brain function; brain region; cell function; Cichlasoma dimerus; cichlid; controlled study; ecotoxicology; endocrine disease; environmental exposure; enzyme activity; foam cell; germ cell; gonadotropin release; histopathology; hormone action; hypophysis; in vitro study; in vivo study; morphological trait; nonhuman; priority journal; regulatory mechanism; reproductive toxicity; Sertoli cell; spermatogenesis; steroidogenesis; testis function; tissue culture; Animals; Cells, Cultured; Cichlids; Endosulfan; Female; Gonadotropins, Pituitary; Male; Ovary; Pituitary Gland; Testis; Water Pollutants, Chemical; South America; Animalia; Cichlasoma; Cichlidae; Perciformes
Año:2013
Volumen:126
Página de inicio:299
Página de fin:305
DOI: http://dx.doi.org/10.1016/j.aquatox.2012.09.015
Título revista:Aquatic Toxicology
Título revista abreviado:Aquat. Toxicol.
ISSN:0166445X
CODEN:AQTOD
CAS:endosulfan, 115-29-7; gamma glutamyltransferase, 85876-02-4; gonadotropin, 63231-54-9; luteinizing hormone, 39341-83-8, 9002-67-9; Endosulfan, 115-29-7; Gonadotropins, Pituitary; Water Pollutants, Chemical
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0166445X_v126_n_p299_DaCuna

Referencias:

  • Abel, M.H., Baker, P.J., Charlton, H.M., Monteiro, A., Verhoeven, G., De Gendt, K., Guillou, F., O'Shaughnessy, P.J., Spermatogenesis and Sertoli cell activity in mice lacking Sertoli cell receptors for follicle-stimulating hormone and androgen (2008) Endocrinology, 149, pp. 3279-3285
  • Armenti, A.E., Zama, A.M., Passantino, L., Uzumcu, M., Developmental methoxychlor exposure affects multiple reproductive parameters and ovarian folliculogenesis and gene expression in adult rats (2008) Toxicology and Applied Pharmacology, 233, pp. 286-296
  • Balasubramani, A., Pandian, T.J., Endosulfan suppresses growth and reproduction in zebrafish (2008) Current Science India, 94, pp. 883-890
  • Ballesteros, M.L., Wunderlin, D.A., Bistoni, M.A., Oxidative stress responses in different organs of Jenynsia multidentata exposed to endosulfan (2009) Ecotoxicology and Environment Safety, 72, pp. 199-205
  • Beard, A.P., Rawlings, N.C., Thyroid function and effects on reproduction in ewes exposed to the organochlorine pesticides lindane or pentachlorophenol (PCP) from conception (1999) Journal of Toxicology and Environmental Health, Part A, 58, pp. 509-530
  • Bisson, M., Hontela, A., Cytotoxic and endocrine-disrupting potential of atrazine, diazinon, endosulfan, and mancozeb in adrenocortical steroidogenic cells of rainbow trout exposed in vitro (2002) Toxicology and Applied Pharmacology, 180, pp. 110-117
  • (2005) Canadian Council on Animal Care, p. 94. , http://www.ccac.ca/Documents/Standards/Guidelines/Fish.pdf, Guidelines on the Care and the Use of Fish in Research, Teaching and Testing. CCAC, ISBN: 0-919087-43-4
  • Canepa, M., Pozzi, A., Astola, A., Maggese, M.C., Vissio, P., Effect of salmon melanin-concentrating hormone and mammalian gonadotrophin-releasing hormone on somatolactin release in pituitary culture of Cichlasoma dimerus (2008) Cell and Tissue Research, 333, pp. 49-59
  • Capkin, E., Altinok, I., Karahan, S., Water quality and fish size affect toxicity of endosulfan, an organochlorine pesticide, to rainbow trout (2006) Chemosphere, 64, pp. 1793-1800
  • Caride, A., Lafuente, A., Cabaleiro, T., Endosulfan effects on pituitary hormone and both nitrosative and oxidative stress in pubertal male rats (2010) Toxicology Letters, 197, pp. 106-112
  • Carreau, S., Drosdowsky, M.A., Foucault, P., Enzymatic properties of adult human Sertoli cells in vitro (1996) Andrologia, 28, pp. 89-95
  • Caston, L.A., Sanborn, B.M., Regulation of testicular and Sertoli cell gamma-glutamyl transpeptidase by follicle-stimulating hormone (1988) Biology of Reproduction, 38, pp. 109-113
  • Chakrabarty, S., Rajakumar, A., Raqhuveer, K., Sridevi, P., Mohanachary, A., Prathibha, Y., Bashyam, L., Senthilkumaran, B., Endosulfan and flutamide, alone and in combination, target ovarian growth in juvenile catfish, Clarias batrachus (2012) Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology, 155, pp. 491-497
  • Chakravorty, S., Lal, B., Singh, T.P., Effect of endosulfan (thiodan) on vitellogenesis and its modulation by different hormones in the vitellogenic catfish Clarias batrachus (1992) Toxicology, 75, pp. 191-198
  • Choudhary, N., Joshi, S.C., Reproductive toxicity of endosulfan in male albino rats (2003) Bulletin of Environment Contamination and Toxicology, 70, pp. 285-289
  • Christiansen, T., Korsgaard, B., Jespersem, Å., Effects of nonylphenol and 17β-oestradiol on vitellogenin synthesis, testicular structure and cytology in male eelpout Zoarces viviparus (1998) Journal of Experimental Biology, 201, pp. 179-192
  • Christiansen, T., Kinnberg, K., Bjerregaard, P., Korsgaard, B., γ-Glutamyl transpeptidase as a possible marker of Sertoli cells in fish testes for studies of xenoestrogens (2000) Marine Environment Research, 50, pp. 213-216
  • Coimbra, A.M., Reis-Henriques, M.A., Darras, V.M., Circulating thyroid hormone levels and iodothyronine deiodinase activities in Nile tilapia (Oreochromis niloticus) following dietary exposure to Endosulfan and Aroclor 1254 (2005) Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology, 141, pp. 8-14
  • Da Cuña, R.H., Rey Vázquez, G., Piol, M.N., Verrengia Guerrero, N., Maggese, M.C., Lo Nostro, F.L., Assessment of the acute toxicity of the organochlorine pesticide endosulfan in Cichlasoma dimerus (Teleostei, Perciformes) (2011) Ecotoxicology and Environmental Safety, 74, pp. 1065-1073
  • Dalvie, M.A., Cairncross, E., Solomon, A., London, L., Contamination of rural surface and ground water by endosulfan in farming areas of the Western Cape, South Africa (2003) Environmental Health, 2, p. 1
  • Dorval, J., Leblond, V.S., Hontela, A., Oxidative stress and loss of cortisol secretion in adrenocortical cells of rainbow trout (Oncorhynchus mykiss) exposed in vitro to endosulfan, an organochlorine pesticide (2003) Aquatic Toxicology, 63, pp. 229-241
  • Dutta, H.M., Misquitta, D., Khan, S., The effects of endosulfán on the testes of bluegill fish. Lepomis macrochirus: a histopathological study (2006) Archives of Environment Contamination and Toxicology, 51, pp. 149-156
  • Genovese, G., Da Cuña, R., Towle, D.W., Maggese, M.C., Lo Nostro, F., Early expression of zona pellucida proteins under octylphenol exposure in Cichlasoma dimerus (Perciformes, Cichlidae) (2011) Aquatic Toxicology, 101, pp. 175-185
  • Genovese, G., Regueira, M., Piazza, Y., Towle, D.W., Maggese, M.C., Lo Nostro, F.L., Time-course recovery of estrogen-responsive genes of a cichlid fish exposed to waterborne octylphenol (2012) Aquatic Toxicology, pp. 1-13
  • Gormley, K.L., Teather, K.L., Developmental, behavioral, and reproductive effects experienced by Japanese medaka (Oryzias latipes) in response to short-term exposure to endosulfán (2003) Ecotoxicology and Environment Safety, 54, pp. 330-338
  • Grier, H., Comparative organization of Sertoli cells including the Sertoli cell barrier (1993) The Sertoli Cell Book, , Cache River Press, USA, pp. 703-739, L.D. Rusell, M.D. Griswold (Eds.)
  • Han, Z., Jiao, S., Kong, D., Shan, Z., Zhang, X., Effects of B-endosulfan on the growth and reproduction of zebrafish (Danio rerio) (2011) Environmental Toxicology and Chemistry, 30, pp. 2525-2531
  • Highleyman, L., Franciscus, A., (2011), http://www.hcvadvocate.org/, Disease progression: What is fibrosis? HcspFACTsheet, accessed May 2012; IRAM (2008) Calidad ambiental, Calidad del agua, , Determinación de la toxicidad letal aguda de sustancias en peces de agua dulce. Método semiestático. IRAM 29112:2008
  • Je, K.H., Kim, K.N., Nam, K.W., Cho, M.H., Mar, W., TERT mRNA expression is up-regulated in MCF-7 cells and a mouse mammary organ culture (MMOC) system by endosulfan treatment (2005) Archives of Pharmacal Research, 28, pp. 351-357
  • Kagawa, H., Tanaka, H., Okuzawa, K., Kobayashi, M., GTH II but not GTH I induces final oocyte maturation and the development of maturational competence of oocytes of red seabream in vitro (1998) General and Comparative Endocrinology, 112, pp. 80-88
  • Kamei, H., Kawazoe, I., Kaneko, T., Aida, K., Purification of follicle-stimulating hormone from immature Japanese eel, Anguilla japonica, and its biochemical properties and steroidogenic activities (2005) General and Comparative Endocrinology, 143, pp. 257-266
  • Kegley, S.E., Hill, B.R., Orme, S., Choi, A.H., (2011), http://www.pesticideinfo.org/, PAN Pesticide Database, Pesticide Action Network, North America, San Francisco, CA; Kisilevsky, R., Tam, S.P., The mobilization of cholesterol released at sites of tissue injury (2003) Cell Growth and Cholesterol Esters. Molecular Biology Intelligence Unit, pp. 50-64. , Eureka.com/Kluwer Academic/Plenum Publishers, New York, A. Pani, S. Dessì (Eds.)
  • Kullander, S.O., (1983) A Revision of the South American Cichlid Genus Cichlasoma (Teleostei: Cichlidae), , Swedish Museum of Natural History, Stockholm
  • Kullander, S.O., Cichlidae (Cichlids) (2003) Checklist of the Freshwater Fishes of South and Central America, pp. 605-654. , EDIPUCRS, Porto Alegre, R.E. Reis, S.O. Kullander, C.J. Ferraris (Eds.)
  • Kumar, R.S., Ijiri, S., Trant, J.M., Molecular biology of the channel catfish gonadotropin receptors: 1. Cloning of a functional luteinizing hormone receptor and preovulatory induction of gene expression (2001) Biology of Reproduction, 64, pp. 1010-1018
  • Kwok, H.F., So, W.K., Wang, Y., Ge, W., Zebrafish gonadotropins and their receptors. I. Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone receptors: evidence for their distinct functions in follicle development (2005) Biology of Reproduction, 72, pp. 1370-1381
  • Laemmli, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4 (1970) Nature, 227, pp. 680-685
  • Lanfranchi, A.L., Menone, M.L., Miglioranza, K.S.B., Janiot, L.J., Aizpún, J.E., Moreno, V.J., Striped weakfish (Cynoscion guatucupa): a biomonitor of organochlorine pesticides in estuarine and near-coastal zones (2006) Marine Pollutution Bulletin, 52, pp. 74-80
  • Leong, K.H., Tan, L.L., Mustafa, A.M., Contamination levels of selected organochlorine and organophosphate pesticides in the Selangor River, Malaysia between 2002 and 2003 (2007) Chemosphere, 66, pp. 1153-1159
  • Meijide, F.J., Guerrero, G.A., Embryonic and larval development of a substrate-brooding cichlid, Cichlasoma dimerus (Heckel, 1840), under laboratory conditions (2000) Journal of Zoology, 252, pp. 481-493
  • Menone, M.L., Aizpún de Moreno, J.E., Moreno, V.J., Lafranchi, A.L., Metcalfe, T.L., Metcalfe, C.D., PCBs and organochlorines in tissues of silverside (Odontesthes bonaerensis) from a coastal lagoon in Argentina (2000) Archives of Environment Contamination and Toxicology, 38, pp. 202-208
  • Miglioranza, K.S.B., González Sagrario, M.A., Aizpún de Moreno, J.E., Moreno, V.J., Escalante, A.H., Osterrieth, M.L., Agricultural soil as a potencial source of organochlorine pesticides into nearby pond (2002) Environmental Science and Pollution Research International, 9, pp. 250-256
  • Mills, L.J., Chichester, C., Review of evidence: are endocrine-disrupting chemicals in the aquatic environment impacting fish populations? (2005) Science of the Total Environment, 343, pp. 1-34
  • Moncaut, N., Lo Nostro, F., Maggese, M.C., Vitellogenin detection in surface mucus of the South American cichlid fish Cichlasoma dimerus (Heckel, 1840) induced by estradiol-17β. Effects on liver and gonads (2003) Aquatic Toxicology, 63, pp. 127-137
  • Neuparth, T., Bickham, J.W., Theodorakis, C.W., Costa, F.O., Costa, M.H., Endosulfan-induced genotoxicity detected in the Gilthead seabream, Sparus aurata L., by means of flow cytometry and micronuclei assays (2006) Bulletin of Environment Contamination and Toxicology, 76, pp. 242-248
  • Ohta, T., Miyake, H., Miura, C., Kamei, H., Aida, K., Miura, T., Follicle-stimulating hormone induces spermatogenesis mediated by androgen production in Japanese eel, Anguilla japonica (2007) Biology of Reproduction, 77, pp. 970-977
  • Pandolfi, M., Lo Nostro, F.L., Shimizu, A., Pozzi, A.G., Meijide, F.J., Rey Vázquez, G., Maggese, M.C., Identification of immunoreactive FSH and LH cells in the cichlid fish Cichlasoma dimerus during the ontogeny and sexual differentiation (2006) Anatomy and Embryology, 211, pp. 355-365
  • Pandolfi, M., Pozzi, A.G., Cánepa, M., Vissio, P.G., Shimizu, A., Maggese, M.C., Lobo, G., Presence of beta-follicle-stimulating hormone and beta-luteinizing hormone transcripts in the brain of Cichlasoma dimerus (Perciformes: Cichlidae): effect of brain-derived gonadotropins on pituitary hormone release (2009) Neuroendocrinology, 89, pp. 27-37
  • Piazza, Y.G., Pandolfi, M., Lo Nostro, F.L., Effect of the organochlorine pesticide endosulfan on GnRH and gonadotrope cell populations in fish larvae (2011) Archives of Environment Contamination and Toxicology, 61, pp. 300-310
  • Planas, J.V., Swanson, P., Maturation-associated changes in the response of the salmon testis to the steroidogenic actions of gonadotropins (GTH I and GTH II) in vitro (1995) Biology of Reproduction, 52, pp. 697-704
  • (2010), http://chm.pops.int/, POPRC (Persistent Organic Pollutants Review Committee). Recommendation of the POPRC on Endosulfan. (accessed 05. 2012); Rajakumar, A., Singh, R., Chakrabarty, S., Murugananthkumar, R., Laldinsangi, C., Prathibha, Y., Sudhakumari, C.C., Senthilkumaran, B., Endosulfan and flutamide impair testicular development in the juvenile Asian catfish, Clarias batrachus (2012) Aquatic Toxicology, pp. 123-132
  • Rasmussen, T.H., Teh, S.J., Bjerregaard, P., Korsgaard, B., Anti-estrogen prevents xenoestrogen-induced testicular pathology of eelpout (Zoarces viviparus) (2005) Aquatic Toxicology, 72, pp. 177-194
  • Rey Vázquez, G., Meijide, F., Da Cuña, R., Lo Nostro, F., Piazza, Y., Babay, P., Trudeau, V., Guerrero, G., Exposure to waterborne 4-tert-octylphenol induces vitellogenin synthesis and disrupts testis morphology in the South American freshwater fish Cichlasoma dimerus (Teleostei, Perciformes) (2009) Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology, 150, pp. 298-306
  • Schteingart, H.F., Cigorraga, S.B., Calandra, R.S., Gonzalez-Calvar, S.I., Modulation by polyamines of gamma-glutamyl transpeptidase activity and lactate production in cultured Sertoli cells from immature and adult regressed golden hamster (2002) Endocrine Research, 28, pp. 239-255
  • Shimizu, A., Yamashita, M., Purification of mummichog (Fundulus heteroclitus) gonadotropins and their subunits, using an immunochemical assay with antisera raised against synthetic peptides (2002) General and Comparative Endocrinology, 125, pp. 79-91
  • Shimizu, A., Tanaka, H., Kagawa, H., Immunocytochemical applications of specific antisera raised against synthetic fragment peptides of mummichog GtH subunits: examining seasonal variations of gonadotrophs (FSH cells and LH cells) in the mummichog and applications to other acanthopterygians fishes (2003) General and Comparative Endocrinology, 132, pp. 35-45
  • Singh, S.K., Pandey, R.S., Effect of sub-chronic endosulfan exposures on plasma gonadotrophins, testosterone, testicular testosterone and enzymes of androgen biosynthesis in rat (1990) Indian Journal of Experimental Biology, 28, pp. 953-956
  • Singh, H., Singh, T.P., Effect of parathion and aldrin on survival, ovarian 32P-uptake and gonadotrophic potency in a freshwater catfish, Heteropneustes fossilis (Bloch) (1981) Endokrinologie, 77, pp. 173-178
  • Singh, S., Dureja, P., Kumar, S., Biodegradation of α and β isomers of endosulphan and endosulphan sulfate in Indian soils (2000) Journal of Environmental Science and Health, 35, pp. 337-346
  • Singh, P.B., Singh, V., Nayak, P.K., Pesticide residues and reproductive dysfunction in different vertebrates from north India (2008) Food and Chemical Toxicology, 46, pp. 2533-2539
  • Sinha, N., Adhikari, N., Saxena, D.K., Effect of endosulfan during fetal gonadal differentiation on spermatogenesis in rats (2001) Environmental Toxicology and Pharmacology, 10, pp. 29-32
  • Sun, L., Zhang, J., Zuo, Z., Chen, Y., Wang, X., Huang, X., Wang, C., Influence of triphenyltin exposure on the hypothalamus-pituitary-gonad axis in male Sebastiscus marmoratus (2011) Aquatic Toxicology, 104, pp. 263-269
  • Sutherland, T.D., Home, I., Weir, K.M., Russell, R.J., Oakeshott, J.G., Toxicity and residues of endosulfan isomers (2004) Reviews of Environment Contamination and Toxicology, 183, pp. 99-113
  • Swanson, P., Dickey, J.T., Campbell, B., Biochemistry and physiology of fish gonadotropins (2003) Fish Physiology and Biochemistry, 28, pp. 53-59
  • Szasz, G., Weimann, G., Stahler, F., Wahlefel, A.W., Persijn, J.P., New substrates for measuring gamma-glutamyl transpeptidase activity (1974) Zeitschrift für Klinische Chemie und Klinische Biochemie, 12, p. 228
  • Teather, K., Jardine, C., Gormley, K., Behavioral and sex ratio modification of Japanese medaka (Oryzias latipes) in response to environmentally relevant mixtures of three pesticides (2005) Environmental Toxicology, 20, pp. 110-117
  • (1996), US Environmental Protection Agency. Test Methods for Evaluation of Solid Waste, vol. 1B: Laboratory Manual, Physical/Chemical Methods (SW-846), Method 8081A, Organochlorine Pesticides and Polychlorinated Biphenyls by Gas Chromatography, Revision 1, Paragraph 5.6.2; Vischer, H.F., Bogerd, J., Cloning and functional characterization of a gonadal luteinizing hormone receptor complementary DNA from the African catfish (Clarias gariepinus) (2003) Biology of Reproduction, 68, pp. 262-271
  • Weber, J., Halsall, C.J., Muir, D., Teixeira, C., Small, J., Solomon, K., Hermanson, M., Bidleman, T., Endosulfan, a global pesticide: a review of its fate in the environment and occurrence in the Arctic (2010) Science of the Total Environment, 408, pp. 2966-2984
  • Wilcove, D.S., Rothstein, D., Dubow, J., Phillips, A., Losos, E., Quantifying threats to imperilled species in the United States: assessing the relative importance of habitat destruction, alien species, pollution, overexploitation and disease (1998) Bioscience, 48, pp. 607-615

Citas:

---------- APA ----------
Da Cuña, R.H., Pandolfi, M., Genovese, G., Piazza, Y., Ansaldo, M. & Lo Nostro, F.L. (2013) . Endocrine disruptive potential of endosulfan on the reproductive axis of Cichlasoma dimerus (Perciformes, Cichlidae). Aquatic Toxicology, 126, 299-305.
http://dx.doi.org/10.1016/j.aquatox.2012.09.015
---------- CHICAGO ----------
Da Cuña, R.H., Pandolfi, M., Genovese, G., Piazza, Y., Ansaldo, M., Lo Nostro, F.L. "Endocrine disruptive potential of endosulfan on the reproductive axis of Cichlasoma dimerus (Perciformes, Cichlidae)" . Aquatic Toxicology 126 (2013) : 299-305.
http://dx.doi.org/10.1016/j.aquatox.2012.09.015
---------- MLA ----------
Da Cuña, R.H., Pandolfi, M., Genovese, G., Piazza, Y., Ansaldo, M., Lo Nostro, F.L. "Endocrine disruptive potential of endosulfan on the reproductive axis of Cichlasoma dimerus (Perciformes, Cichlidae)" . Aquatic Toxicology, vol. 126, 2013, pp. 299-305.
http://dx.doi.org/10.1016/j.aquatox.2012.09.015
---------- VANCOUVER ----------
Da Cuña, R.H., Pandolfi, M., Genovese, G., Piazza, Y., Ansaldo, M., Lo Nostro, F.L. Endocrine disruptive potential of endosulfan on the reproductive axis of Cichlasoma dimerus (Perciformes, Cichlidae). Aquat. Toxicol. 2013;126:299-305.
http://dx.doi.org/10.1016/j.aquatox.2012.09.015