Abstract
Roundup is the most popular commercial glyphosate formulation applied in the cultivation of genetically modified glyphosate-resistant crops. The aim of this study was to evaluate the histological lesions of the neotropical native fish, Jenynsia multidentata, in response to acute and subchronic exposure to Roundup and to determine if subchronic exposure to the herbicide causes changes in male sexual activity of individuals exposed to a sublethal concentration (0.5 mg/l) for 7 and 28 days. The estimated 96-h LC50 was 19.02 mg/l for both male and female fish. Gill and liver histological lesions were evaluated through histopathological indices allowing quantification of the histological damages in fish exposed to different concentrations of the herbicide. Roundup induced different histological alterations in a concentration-dependent manner. In subchronic-exposure tests, Roundup also altered normal histology of the studied organs and caused a significant decrease in the number of copulations and mating success in male fish exposed to the herbicide. It is expected that in natural environments contaminated with Roundup, both general health condition and reproductive success of J. multidenatata could be seriously affected.
Similar content being viewed by others
References
Abdelghani AA, Tchounwou PB, Anderson AC, Sujono H, Heyer LR, Monkiedje A (1997) Toxicity evaluation of single and chemical mixtures of Roundup, Gardon-3A, 2,4-D and syndets surfactant to channel catfish (Ictalurus punctatus), bluegill sunfish (Lepomis microchirus), and crayfish (Procambarus spp). Environ Toxicol Water Qual 12:237–243
Alazemi BM, Lewis JW, Andrews EB (1996) Gill damage in the freshwater fish Gnathonemus petersii (family: Mormyridae) exposed to selected pollutants: an ultrastructural study. Environ Technol 17(3):225–238
Albinati ACL, Moreira ELT, Albinati RCB, Carvalho JV, Santos GB, Lira AD (2007) Toxicidade aguda do herbicida Roundup® para piauçu (Leporinus macrocephalus). Rev Bras Saúde Prod Anim 8:184–192
Albinati ACL, Moreira ELT, Albinati JRCB, Carvalho V, De Lira AD, Santos GB et al (2009) Biomarcadores histológicos―Toxicidade crônica pelo Roundup em piauçu (Leporinus macrocephalus). Arq Bras Med Vet Zootec 61(3):621–627
Amarante OP Jr, Santos TCR, Brito NM, Ribeiro ML (2002) Glifosato: propiedades, toxicidade, uso e legislação. Quím Nova 25:589–593
Amé MV, Baroni MV, Galanti LN, Bocco JL, Wunderlin DA (2009) Effects of microcystin-LR on the expression of P-glycoprotein in Jenynsia multidentata. Chemosphere 74:1179–1186
Ayoola SO (2008) Toxicity of glyphosate herbicides on Nile tilapia (Oreochromis niloticus) juvenile. Afr J Agric Res 3(12):825–834
Ballesteros ML, Bianchi G, Carranza M, Bistoni M (2007) Endosulfan acute toxicity and histomorphological alterations in Jenynsia multidentata (Anablepidae, Cyprinodontiformes). J Environ Sci Health B 42:351–357
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
Bernet D, Schmidt-Posthaus H, Wahli T, Burkhardt-Holm P (2004) Evaluation of two monitoring approaches to assess effects of waste water disposal on histological alterations in fish. Hydrobiologia 524:53–66
Bisazza A, Manfredi S, Pilastro A (2000) Sexual competition, Coercive mating and mate assessment in the one-sided livebearer, Jenynsia multidentata: are they predictive of sexual dimorphism? Ethology 106:961–978
Bols NC, Brubacher JL, Ganassin RC, Lee LE (2001) Ecotoxicology and innate immunity in fish. Dev Comp Immunol 25:853–873
Brausch MJ, Smith NP (2007) Toxicity of three polyethoxylated tallowamine surfactant formulations to laboratory and field collected fairy shrimp, Thamnocephalus platyurus. Arch Environ Contam Toxicol 52:217–221
Burger M, Fernández S (2004) Exposición al herbicida glifosato: aspectos clínicos toxicológicos. Rev Med Uruguay 20:202–207
Cazenave J, Wunderlin DA, Bistoni MA, Amé MV, Krause E, Pflugmacher S et al (2005) Uptake, tissue distribution and accumulation of microcystin-RR in Corydoras paleatus, Jenynsia multidentata and Odontesthes bonariensis: a field and laboratory study. Aquat Toxicol 15:178–190
Cengiz EI, Ünlü E (2003) Histopathology of gills in mosquitofish, Gambusia affinis after long-term exposure to sublethal concentrations of malathion. J Environ Sci Health B 38:581–589
Cox C (2004) Glyphosate herbicide factsheet. J Pesticide Reform 24(4):10–15
Crawford JM (2000) El hígado y las vías biliares. In: Cotram RS, Kumar V, Collins T (eds) Patología estructural y funcional. Editorial McGraw-Hill Interamericana, Madrid, Spain, pp 881–940
Doyle CJ, Lim RP (2005) Sexual behavior and impregnation success of adult male mosquitofish following exposure to 17β-estradiol. Ecotox Environ Safe 61(3):392–397
Folmar LC, Sanders HO, Julin AM (1979) Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrates. Arch Environ Contam Toxicol 8:269–278
Ghedotti MJ (2000) Phylogenetic analysis and taxonomy of Poecillioid fishes (Teleostei: Cyprinidontifomes). Zool J Linn Soc 130:1–53
Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup herbicide. Rev Environ Contam Toxicol 167:35–120
Hinton DE, Segner H, Braunbeck T (2001) Toxic responses of the liver. In: Schlenk D, Benson WH (eds) Target organ toxicity in marine and freshwater teleosts, vol 1. Taylor & Francis, London, pp 224–268
Hued AC, Bistoni MA (2005) Development and validation of a biotic index for evaluation of environmental quality in the central region of Argentina. Hydrobiologia 543:279–298
Hued AC, Caruso MN, Wunderlin DA, Bistoni MA (2006) A Field and in vitro evaluation of ammonia toxicity on native fish species of the central region of Argentina. B Environ Contam Tox 76:984–991
Infostat (2002) Grupo infostat. Facultad de Ciencias Agropecuarias, Universidad Nacional de Córdoba, Argentina
Jamieson BGM (1991) Fish evolution and systematics: evidence from Spermatozoa. Cambridge University Press, Cambridge, 319 pp
Jiraungkoorskul W, Upatham ES, Kruatrachue M, Sahaphong S, Vichasri-Grams S, Pokethitiyook P (2002) Acute toxicity of Roundup, a glyphosate herbicide, to Nile tilapia (Oreochromis niloticus). Sci Asia 28:119–125
Jiraungkoorskul W, Upatham ES, Kruatrachue M, Sahaphong S, Vichasri-Grams S, Pokethitiyook P (2003) Biochemical and histopathological effects of glyphosate herbicide on Nile tilapia (Oreochromis niloticus). Environ Toxicol 18:260–267
Langiano VC, Martinez CBR (2008) Toxicity and effects of a glyphosate-based herbicide on the Neotropical fish Prochilodus lineatus. Comp Biochem Physiol 147:222–231
Malabarba L, Reis R, Vari R, Lucena Z, Lucena C (1998) Phylogeny and classification of neotropical fishes. EDIPUCRS, Porto Alegre
Martínez CBR, Cólus IMS (2002) Biomarcadores em peixes neotropicais para monitoramento da poluição acuática na bacia do río Tibagi. In: Moacyr E, Bianchini E, Shibat OA, Pimenta JA (eds) A bacia do río Tibagi. MC Gráfica, Londrina, pp 551–577
Meisner AD (2005) Male modifications associated with insemination in Teleosts. In: Uribe MC, Grier HJ (eds) Viviparous Fishes. New Life Publications, Homestead, FL, pp 167–192
Mitchell DG, Chapman PM, Long TL (1987) Acute toxicity of Roundup and Rodeo herbicides to rainbow trout, chinook and coho salmon. Bull Environ Contam Toxicol 39:1028–1035
Nakayama K, Oshima Y, Yamaguchi T, Tsuruda Y, Kang IJ, Kobayashi M et al (2004) Fertilization success and sexual behavior in male medaka, Oryzias latipes, exposed to tributyltin. Chemosphere 55(10):1331–1337
Nero V, Farwell A, Lister A, Van Der Kraak G, Lee LEJ, Van Meer T et al (2006) The effects of salinity on naphthenic acid toxicity to yellow perch: Gill and liver histopathology. Ecotox Environ Safe 65:252–264
Neskovic NK, Poleksic V, Elezovic I, Karan V, Budimir M (1996) Biochemical and histopathological effects of glyphosate on carp (Cyprinus carpio). Bull Environ Contam Toxicol 56:295–302
Newman MC, Unger MA (2003) Fundamentals of ecotoxicology, 2nd edn. Lewis, North Carolina
Oshima Y, Kang IJ, Kobayashi M, Nakayama K, Imada N, Honjo T (2003) Suppression of sexual behavior in male Japanese medaka (Oryzias latipes) exposed to 17β-estradiol. Chemosphere 50(3):429–436
Pengue W (2005) Transgenic crops in Argentina. Ecol Social Debt Bull Sci Technol Soc 25(4):314–322
Perusso PJ, Porta AA, Ronco AE (2008) Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environ Pollut 156:61–66
Ramírez-Duarte WF, Rondón-Barragán IS, Eslava-Mocha PR (2008) Acute toxicity and histopathological alterations of Roundup® herbicide on “cachama blanca” (Piaractus brachypomus). Pesq Vet Bras 28(11):547–554
Rasband WS (2005) Image J National Institutes of Health, Bethesda MD. http://rsb.info.nih.gov/ij/. Accessed March 2005
Rendón-von Osten J, Ortíz-Arana A, Guilhermino L, Soares AMVM (2005) In vivo evaluation of three biomarkers in the mosquitofish (Gambusia yucatana) exposed to pesticides. Chemosphere 58(5):627–636
Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: Integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68:369–392
Sokal RR, Rohlf FJ (1999) Introducción a la bioestadística. Editorial Reverté, Barcelona
Stentiford GD, Longshaw M, Lyons BP, Jones G, Green M, Feist SW (2003) Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants. Mar Environ Res 55(2):137–159
Szarek J, Siwicki A, Andrzejewska A, Terech-Majewska E, Banaszkiewicz T (2000) Effects of the herbicide Roundup on the ultraestructural pattern of hepatocytes in carp (Cyprinus carpio). Mar Environ Res 20:263–266
Toft G, Guillette LJ Jr (2005) Decreased sperm count and sexual behavior in mosquitofish exposed to water from a pesticide-contaminated lake. Ecotox Environ Safe 60(1):15–20
United States Environmental Protection Agency (2005) Probit analysis program used for calculating LC/EC values Version 1.5. Ecological Monitoring Research Division. Environmental Monitoring Systems Laboratory, Cincinnati, OH, 1992. http://www.epa.gov/nerleerd/stat2.html. Accessed March 2005
Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environ Toxicol Pharmacol 13:57–149
Williams GM, Kroes R, Munro IC (2000) Safety evaluation and risk assessment of the herbicide Roundup and its active ingredient, glyphosate, for humans. Regul Toxicol Pharm 31:117–165
World Health Organization (1994) Glyphosate. Environmental health criteria, publication no 159. WHO, Geneva
World Health Organization (2005) Glyphosate and AMPA in drinking-water. Background document for development of WHO guidelines for drinking-water quality. WHO, Geneva
Acknowledgments
This work was supported by grants from Consejo de Investigaciones Científicas y Técnicas and Secretaría de Ciencia y Técnica de la Universidad Nacional de Córdoba. The as wish thank to Ariel Lucero for field assistance.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hued, A.C., Oberhofer, S. & de los Ángeles Bistoni, M. Exposure to a Commercial Glyphosate Formulation (Roundup®) Alters Normal Gill and Liver Histology and Affects Male Sexual Activity of Jenynsia multidentata (Anablepidae, Cyprinodontiformes). Arch Environ Contam Toxicol 62, 107–117 (2012). https://doi.org/10.1007/s00244-011-9686-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-011-9686-7