Abstract
Many water systems worldwide are affected by pollutants, including potential endocrine disruptors (EDs). Most studies on the effects of EDs on fish reproduction have focused on oviparous species. However, some important groups of fishes are not oviparous and there is scarce information about how EDs affect species with alternative reproductive modes. Goodeinae is a viviparous matrotrophic subfamily with intraluminal gestation (IG), where transfer of nutrients occurs and embryos develop inside the ovarian cavity. Goodeinae is endemic to the Mexican Central Plateau, an area affected by potential EDs, including 2,4-dichlorophenoxyacetic acid (2,4-D). This review synthesizes the available information about EDs in viviparous teleosts with IG and performs a case study on the effects of 2,4-D on gonadal structure of two Goodeinae species. We hypothesized that individuals exposed to 2,4-D might show altered gonadal structure. The available information included effects on gene expression, sexual differentiation, gametogenesis, secondary sexual characteristics, and sexual behavior. Knowledge gaps persisted on the effects of EDs on viviparous teleosts with IG. Holistic approaches are needed to understand the mechanisms underlying endocrine disruption effects. Field studies are needed to evaluate the consequences of EDs on wild populations. The case study revealed histological alterations in oocytes, spermatogonia, and sperm cysts in fishes exposed to 2,4-D. Ultrastructurally, gonads exhibited alterations in oocyte mitochondrial and nuclear membranes, and in spermatid mitochondria. The observed changes could be related to 2,4-D exposure, which may affect species reproduction in their natural environment. Matrotrophic viviparous teleosts with IG may serve as models to explore endocrine disruption.
Similar content being viewed by others
References
Andreassen TK, Skjoedt K, Korsgaard B (2005) Upregulation of estrogen receptor alpha and vitellogenin in eelpout (Zoarces viviparus) by waterborne exposure to 4-tert-octylphenol and 17beta-estradiol. Comp Biochem Physiol C Toxicol Pharmacol 140:340–346. doi:10.1016/j.cca.2005.03.003
APHA, AWWA, WPCF (2005) Standard methods for the examination of water and wastewater, 21st edn. APHA, Washington
Arellano-Aguilar O, Macías-García C (2008) Exposure to pesticides impairs the expression of fish ornaments reducing the availability of attractive males. Proc Biol Sci 275:1343–1350. doi:10.1098/rspb.2008.0163
Arévalo-Hernández A, Reynoso-Silva M, Álvarez-Moya C (2011) Compuestos órgano-persistentes y daño genético en núcleos hepáticos de Goodea atripinnis del Lago de Chapala. Sci CUCBA 13:1–8
Ateeq B, Farah MA, Ahmad W (2006) Evidence of apoptotic effects of 2,4-D and butachlor on walking catfish, Clarias batrachus, by transmission electron microscopy and DNA degradation studies. Life Sci 78:977–986. doi:10.1016/j.lfs.2005.06.008
Barbieri E (2009) Effect of 2,4-D herbicide (2,4-dichlorophenoxyacetic acid) on oxygen consumption and ammonium excretion of juveniles of Geophagus brasiliensis (Quoy & Gaimard, 1824) (Osteichthyes, Cichlidae). Ecotoxicology 18:55–60. doi:10.1007/s10646-008-0256-3
Barni MF, Gonzalez M, Miglioranza KS (2014) Assessment of persistent organic pollutants accumulation and lipid peroxidation in two reproductive stages of wild silverside (Odontesthes bonariensis). Ecotoxicol Environ Saf 99:45–53. doi:10.1016/j.ecoenv.2013.10.012
Behbahani M, Najafi F, Bagheri S, Bojdi MK, Hassanlou PG, Bagheri A (2014) Coupling of solvent-based de-emulsification dispersive liquid-liquid microextraction with high performance liquid chromatography for simultaneous simple and rapid trace monitoring of 2,4-dichlorophenoxyacetic acid and 2-methyl-4-chlorophenoxyacetic acid. Environ Monit Assess 186:2609–2618. doi:10.1007/s10661-013-3564-x
Bergek S, Ma Q, Vetemaa M, Franzén F, Appelberg M (2012) From individuals to populations: impacts of environmental pollution on natural eelpout populations. Ecotoxicol Environ Saf 79:1–12. doi:10.1016/j.ecoenv.2012.01.019
Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34. doi:10.1046/j.1365-2761.1999.00134.x
Blackburn DG (2015) Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. J Morphol 276(8):961–990. doi:10.1002/jmor.20272
Borg B (1994) Androgens in teleost fishes. Comp Biochem Physiol C 109(3):219–245. doi:10.1016/0742-8413(94)00063-G
Brande-Lavridsen N, Korsgaard B, Dahllöf I, Strand J, Tairova Z, Bjerregaard P (2013) Abnormalities in eelpout Zoarces viviparus upon chemical exposure. Mar Environ Res 92:87–94. doi:10.1016/j.marenvres.2013.09.004
Braunbeck T, Johnson R, Wolf J (2010) Guidance document on the diagnosis of endocrine-related histopathology in fish gonads. In: OECD (ed) Series on testing and assessment, vol 123. Organisation for Economic Cooperation and Development, Paris, pp 1–114
Coady K, Marino T, Thomas J, Sosinski L, Neal B, Hammond L (2013) An evaluation of 2,4-dichlorophenoxyacetic acid in the amphibian metamorphosis assay and the fish short-term reproduction assay. Ecotox Environ Saf 90:143–150. doi:10.1016/j.ecoenv.2012.12.025
Coady KK, Kan HL, Schisler MR, Gollapudi BB, Neal B, Williams A, LeBaron MJ (2014) Evaluation of potential endocrine activity of 2,4-dichlorophenoxyacetic acid using in vitro assays. Toxicol In Vitro 28(5):1018–1025. doi:10.1016/j.marenvres.2013.09.004
Dang Z (2014) Fish biomarkers for regulatory identification of endocrine disrupting chemicals. Environ Pollut 185:266–270. doi:10.1016/j.envpol.2013.11.006
De la Vega-Salazar MY, Macías-García C (2005) Principal factors in the decline of the Mexican endemic livebearing fishes (Goodeinae: Goodeidae). In: Uribe MC, Grier HJ (eds) Viviparous fishes. New Life Publications, Florida, pp 505–513
Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364. doi:10.1016/S0044-8486(02)00057-1
Domínguez-Domínguez O, Mercado-Silva N, Lyons J (2005) Conservation status of Mexican Goodeids: problems, perspectives and solutions. In: Uribe MC, Grier HJ (eds) Viviparous fishes. New Life Publications, Florida, pp 515–523
Downing-Meisner A (2005) Male modifications associated with insemination in teleosts. In: Uribe MC, Grier HJ (eds) Viviparous fishes. New Life Publications, Florida, pp 165–190
Dreze V, Monod G, Cravedi JP, Biagianti-Risbourg S, Le Gac F (2000) Effects of 4-nonylphenol on sex differentiation and puberty in mosquitofish (Gambusia holbrooki). Ecotoxicology 9:93–103. doi:10.1023/A:1008976431227
Edwards TM, Iguchi T, Guillette LJ Jr (2010) Genes to ecosystems: viviparous fishes and endocrine disruption. In: Uribe MC, Grier HJ (eds) Viviparous fishes, vol 2. New Life Publications, Florida, pp 375–386
Ensminger MP, Budd R, Kelley KC, Goh KS (2013) Pesticide occurrence and aquatic benchmark exceedances in urban surface waters and sediments in three urban areas of California, USA, 2008–2011. Environ Monit Assess 185:3697–3710. doi:10.1007/s10661-012-2821-8
Fairchild JF, Feltz KP, Allert AL, Sappington LC, Nelson KJ, Valle JA (2009) An ecological risk assessment of the exposure and effects of 2,4-D acid to rainbow trout (Oncorhynchus mykiss). Arch Environ Contam Toxicol 56:754–760. doi:10.1007/s00244-008-9281-8
Favari L, López E, Martínez-Tabche L, Díaz-Pardo E (2002) Effect of insecticides on plankton and fish of Ignacio Ramirez Reservoir (Mexico): a biochemical and biomagnification study. Ecotoxicol Environ Saf 51:177–186. doi:10.1006/eesa.2002.2142
Genovese G, Regueira M, Da Cuña RH, Ferreira MF, Varela ML, Lo Nostro FL (2014) Nonmonotonic response of vitellogenin and estrogen receptor α gene expression after octylphenol exposure of Cichlasoma dimerus (Perciformes, Cichlidae). Aquat Toxicol 156:30–40. doi:10.1016/j.aquatox.2014.07.019
Gercken J, Sordyl H (2002) Intersex in feral marine and freshwater fish from northeastern Germany. Mar Environ Res 54:651–655. doi:10.1016/S0141-1136(02)00156-3
Glasauer SM, Neuhauss SC (2014) Whole-genome duplication in teleost fishes and its evolutionary consequences. Mol Genet Genom 289:1045–1060. doi:10.1007/s00438-014-0889-2
Grier HJ, Fitzsimons JM, Linton JR (1978) Structure and ultrastructure of the testis and sperm formation in goodeid teleosts. J Morphol 156:419–437. doi:10.1002/jmor.1051560306
Guerrero-Estévez S, Moreno-Mendoza N (2010) Sexual determination and differentiation in teleost fish. Rev Fish Biol Fish 20:101–121. doi:10.1007/s11160-009-9123-4
Guerrero-Estévez S, Moreno-Mendoza N (2012) Gonadal morphogenesis and sex differentiation in the viviparous fish Chapalichthys encaustus (Teleostei, Cyprinodontiformes, Goodeidae). J Fish Biol 80:572–594. doi:10.1111/j.1095-8649.2011.03196.x
Hanson N, Aberg P, Sundelöf A (2005) Population-level effects of male-biased broods in eelpout (Zoarces viviparus). Environ Toxicol Chem 24:1235–1241. doi:10.1897/04-185R.1
Hedman JE, Rüdel H, Gercken J, Bergek S, Strand J, Quack M, Appelberg M, Förlin L, Tuvikene A, Bignert A (2011) Eelpout (Zoarces viviparus) in marine environmental monitoring. Mar Pollut Bull 62:2015–2029. doi:10.1016/j.marpolbul.2011.06.028
Hutchinson TH, Brown R, Brugger KE, Campbell PM, Holt M, Länge R, McCahon P, Tattersfield LJ, van Egmond R (2000) Ecological risk assessment of endocrine disruptors. Environ Health Perspect 08:1007–1014. doi:10.1289/ehp.001081007
Kaufman MH, Chang HH (2000) Studies of the mechanism of amniotic sac puncture-induced limb abnormalities in mice. Int J Dev Biol 44:161–175
Korsgaard B, Andreassen TK, Rasmussen TH (2002) Effects of an environmental estrogen, 17alpha-ethinyl-estradiol, on the maternal-fetal trophic relationship in the eelpout Zoarces viviparus (L). Mar Environ Res 54:735–739. doi:10.1016/S0141-1136(02)00112-5
LaChapelle AM, Ruygrok ML, Toomer M, Oost JJ, Monnie ML, Swenson JA, Compton AA, Stebbins-Boaz B (2007) The hormonal herbicide, 2,4-dichlorophenoxyacetic acid, inhibits Xenopus oocyte maturation by targeting translational and post-translational mechanisms. Reprod Toxicol 23:20–31. doi:10.1016/j.reprotox.2006.08.013
Lambert JGD (1970) The ovary of the guppy Poecilia reticulata. The atretic follicle, a corpus atreticum or a corpus luteum praeovulationis. Z Zellforsch Mikrosk Anat 107:54–67. doi:10.1007/BF00338958
Larsson DG, Förlin L (2002) Male-biased sex ratios of fish embryos near a pulp mill: temporary recovery after a short-term shutdown. Environ Health Perspect 110:739–742
Larsson DG, Hällman H, Förlin L (2000) More male fish embryos near a pulp mill. Environ Toxicol Chem 19:2911–2917. doi:10.1002/etc.5620191210
Leet JK, Gall HE, Sepúlveda MS (2011) A review of studies on androgen and estrogen exposure in fish early life stages: effects on gene and hormonal control of sexual differentiation. J Appl Toxicol 31(5):379–398. doi:10.1002/jat.1682
Macías-Garcia C, Saborío E, Berea C (1998) Does male-biased predation lead to male scarcity in viviparous fish? J Fish Biol 53(Supplement A):104–117. doi:10.1111/j.1095-8649.1998.tb01021.x
Mills LJ, Chichester C (2005) Review of evidence: are endocrine-disrupting chemicals in the aquatic environment impacting fish populations? Sci Total Environ 343:1–34. doi:10.1016/j.scitotenv.2004.12.070
Mnif W, Hassine AI, Bouaziz A, Bartegi A, Thomas O, Roig B (2011) Effect of endocrine disruptor pesticides: a review. Int J Environ Res Public Health 8:2265–2303. doi:10.3390/ijerph8062265
Morthorst JE, Brande-Lavridsen N, Korsgaard B, Bjerregaard P (2014) 17β-estradiol causes abnormal development in embryos of the viviparous eelpout. Environ Sci Technol 48:14668–14676. doi:10.1021/es5046698
Mossman HW (1937) Comparative morphogenesis of the fetal membranes and accessory uterine structures. Carnegie Inst Contr Embryol 26:129–246
Nicholson MDO, Lindsay LA, Murphy CR (2010) Ovarian hormones control the changing expression of claudins and occludin rat uterine epithelial cells during early pregnancy. Acta Histochem 112:42–52. doi:10.1016/j.acthis.2008.07.003
Olivares-Rubio HF, Dzul-Caamal R, Gallegos-Rangel ME, Madera-Sandoval RL, Domínguez-López ML, García-Latorre E, Vega-López A (2015) Relationship between biomarkers and endocrine-disrupting compounds in wild Girardinichthys viviparus from two lakes with different degrees of pollution. Ecotoxicology 24(3):664–685. doi:10.1007/s10646-014-1414-4
Payne J, Rajapakse N, Wilkins M, Kortenkamp A (2000) Prediction and assessment of the effects of mixtures of four xenoestrogens. Environ Health Perspect 108(10):983–987. doi:10.1289/ehp.00108983
Rasmussen TH, Korsgaard B (2004) Estrogenic octylphenol affects seminal fluid production and its biochemical composition of eelpout (Zoarces viviparus). Comp Biochem Physiol C Toxicol Pharmacol 139:1–10. doi:10.1016/j.cca.2004.08.016
Rasmussen TH, Andreassen TK, Pedersen SN, Van der Ven LT, Bjerregaard P, Korsgaard BJ (2002) Effects of waterborne exposure of octylphenol and oestrogen on pregnant viviparous eelpout (Zoarces viviparus) and her embryos in ovario. J Exp Biol 205:3857–3876
Rasmussen TH, Teh SJ, Bjerregaard P, Korsgaard B (2005) Anti-estrogen prevents xenoestrogen-induced testicular pathology of eelpout (Zoarces viviparus). Aquat Toxicol 72:177–194. doi:10.1016/j.aquatox.2004.12.003
Rehwoldt RE, Kelley E, Mahoney M (1977) Investigations into the acute toxicity and some chronic effects of selected herbicides and pesticides on several fresh water fish species. Bull Environ Contam Toxicol 18:361–365
Rotchel JM, Ostrander GK (2003) Molecular markers of endocrine disruption in aquatic organisms. J Toxicol Environ Health B Crit Rev 6:453–496. doi:10.1080/10937400306476
Ruggeri B, Ubaldi M, Lourdusamy A, Soverchia L, Ciccocioppo R, Hardiman G et al (2008) Variation of the genetic expression pattern after exposure to estradiol-17beta and 4-nonylphenol in male zebrafish (Danio rerio). Gen Comp Endocrinol 158:138–144. doi:10.1016/j.ygcen.2008.05.012
SAGARPA (2001) Norma oficial mexicana NOM-062-ZOO-1999. Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio. http://www.senasica.gob.mx/?doc=743. Accessed 15 Nov 2015
Sánchez-Guerra M, Pérez-Herrera N, Quintanilla-Vega B (2011) Organophosphorous pesticides research in Mexico: epidemiological and experimental approaches. Toxicol Mech Methods 21:681–691. doi:10.3109/15376516.2011.602130
Schiedek D, Broeg K, Barsiene J, Lehtonen KK, Gercken J, Pfeifer S, Vuontisjärvi H et al (2006) Biomarker responses as indication of contaminant effects in blue mussel (Mytilus edulis) and female eelpout (Zoarces viviparus) from the southwestern Baltic Sea. Mar Pollut Bull 53:387–405. doi:10.1016/j.marpolbul.2005.11.013
Schindler JF (2015) Structure and function of placental exchange surfaces in goodeid fishes (Teleostei: Atheriniformes). J Morphol 276(8):991–1003. doi:10.1002/jmor.20292
Schindler JF, Hamlett WC (1993) Maternal-embryonic relations in viviparous teleosts. J Exp Zool 266:378–393. doi:10.1002/jez.1402660506
Scholz S, Klüver N (2009) Effects of endocrine disrupters on sexual, gonadal development in fish. Sex Dev 3:136–151. doi:10.1159/000223078
Selman K, Wallace RA (1983) Oogenesis in Fundulus heteroclitus. III. Vitellogenesis. J Exp Zool 226:441–457. doi:10.1002/jez.1402260315
Sharpe RL, Benskin JP, Laarman AH, MacLeod SL, Martin JW, Wong CS, Goss GG (2010) Perfluorooctane sulfonate toxicity, isomer-specific accumulation, and maternal transfer in zebrafish (Danio rerio) and rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 29(9):1957–1966. doi:10.1002/etc.257
Shen ZG, Wang HP (2014) Molecular players involved in temperature-dependent sex determination and sex differentiation in Teleost fish. Genet Sel Evol 46:26. doi:10.1186/1297-9686-46-26
Stebbins-Boaz B, Fortner K, Frazier J, Piluso S, Pullen S, Rasar M, Reid W, Sinclair K, Winger E (2004) Oocyte maturation in Xenopus laevis is blocked by the hormonal herbicide, 2,4-dichlorophenoxy acetic acid. Mol Reprod Dev 67:233–242. doi:10.1002/mrd.10396
Storz JF, Opazo JC, Hoffmann FG (2013) Gene duplication, genome duplication, and the functional diversification of vertebrate globins. Mol Phylogenet Evol 66(2):469–478. doi:10.1016/j.ympev.2012.07.013
Sumpter JP, Jobling S (1995) Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ Health Perspect 103(Suppl 7):173–178. doi:10.2307/3432529
Uribe MC, De la Rosa-Cruz G, García-Alarcón A (2005) The ovary of viviparous teleosts. Morphological differences between the ovaries of Goodea atripinnis and Ilyodon whitei (Goodeidae). In: Uribe MC, Grier HJ (eds) Viviparous fishes. New Life Publications, Florida, pp 217–235
Valdez Salas B, Garcia Duran EI, Wiener MS (2000) Impact of pesticides use on human health in Mexico: a review. Rev Environ Health 15:399–412. doi:10.1515/REVEH.2000.15.4.399
Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13(2):57–149. doi:10.1016/S1382-6689(02)00126-6
Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, Shioda T et al (2012) Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 33:378–455. doi:10.1210/er.2011-1050
Vega-López A, Martínez-Tabche L, Domínguez-López ML, García-Latorre E, Ramón-Gallegos E, García-Gasca A (2006) Vitellogenin induction in the endangered goodeid fish Girardinichthys viviparus: vitellogenin characterization and estrogenic effects of polychlorinated biphenyls. Comp Biochem Physiol C Toxicol Pharmacol 142:356–364. doi:10.1016/j.cbpc.2005.11.009
Velasco-Santamaría YM, Bjerregaard P, Korsgaard B (2010) Gonadal alterations in male eelpout (Zoarces viviparus) exposed to ethinylestradiol and trenbolone separately or in combination. Mar Environ Res 69:S67–S69. doi:10.1016/j.marenvres.2009.09.009
Velasco-Santamaría YM, Bjerregaard P, Korsgaard B (2013) Evidence of small modulation of ethinylestradiol induced effects by concurrent exposure to trenbolone in male eelpout Zoarces viviparus. Environ Pollut 178:189–196. doi:10.1016/j.envpol.2013.03.011
Wourms JP (1981) Viviparity: the maternal-fetal relationships in fishes. Am Zool 21:473–515. doi:10.1093/icb/21.2.473
Wourms JP (2005) Functional morphology, development and evolution of trophotaeniae. In: Uribe MC, Grier HJ (eds) Viviparous fishes. New Life Publications, Florida, pp 219–244
Wourms JP, Grove BD, Lombardi J (1988) The maternal-embryonic relationships in viviparous fishes. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol 11. Academic Press, New York, pp 1–134
Xie L, Thrippleton K, Irwin MA, Siemering GS, Mekebri A, Crane D, Berry K, Schlenk D (2005) Evaluation of estrogenic activities of aquatic herbicides and surfactants using a rainbow trout vitellogenin assay. Toxicol Sci 87:391–398. doi:10.1093/toxsci/kfi249
Acknowledgments
The authors thank the National Science and Technology Council (CONACyT), the Government of the State of Morelos (FOMIX 2011-173996), and the Ministry of Research and Post-graduate, Instituto Politécnico Nacional (IPN) (SIP 20140853) for financial support of this research, as well as the Chemical-Biological Sciences Posgrade, IPN.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Guerrero-Estévez, S.M., López-López, E. Effects of endocrine disruptors on reproduction in viviparous teleosts with intraluminal gestation. Rev Fish Biol Fisheries 26, 563–587 (2016). https://doi.org/10.1007/s11160-016-9443-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11160-016-9443-0