Abstract
Roundup® (glyphosate formulation) is a nonselective and posts emergent herbicide used for controlling aquatic weeds and different concentrations are used in cultures around the world. The objective of this investigation was to examine the effects of Roundup® (glyphosate formulation) on the biochemical composition, levels of lipoperoxidation, Na+/K+ATPase activity and reproductive traits in the Hyalella castroi. Amphipods were collected in summer 2009, in the southern Brazilian highlands. In the laboratory, the animals were kept in aquariums under controlled conditions for 7 days, and after this period they were exposed to 0.36, 0.52, 1.08 and 2.16 mg/l of glyphosate for 7 days. After the period of exposure, the animals were immediately frozen for determination of glycogen, proteins, lipids, triglycerides, cholesterol, levels of lipoperoxidation, and Na+/K+ATPase activity. During each day of the cultivation reproductive traits (number of reproductive pairs, ovigerous females and eggs in the marsupium) were observed. All concentrations of Roundup® induced significant decreases in all biochemical parameters and Na+/K+ATPase activity, and significant increase in lipoperoxidation levels. Showing this form a potentially toxic effect at very low concentrations, this pattern of results can lead to significant changes in trophic structure of limnic environments because these amphipods are important links in food chain in these habitats.
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References
Achiorno L, Villalobos C, Ferrari L (2008) Toxicity of the herbicide glyphosate to Chordodes nobilii (Gordiida, Nematomorpha). Chemosphere 71:1816–1822
Amarante OP, Santos TCR (2002) Glifosato: propriedades, toxicidade, usos e legislação. Quím Nova 25:589–593
Amrhein N, Deus B, Gehrke P, Steinrucken HC (1980) The site of the inhibition of the shikimate pathway by glyphosate. II. Interference of glyphosate with chorismate formation in vivo and in vitro. Plant Physiol 66:830–834
Barnes JM, Murphy PA, Kirkham D, Henley JM (1993) Interaction of guanine nucleotides with [3H] kainate and 6-[3H] cyano-7-nitroquinoxaline-2,3-dione binding in goldfish brain. J Neurochem 61:1685–1691
Buege JA, Aust SD (1978) Microsomal lipids peroxidation. Methods Enzymol 52:302–310
Calow P, Sibly RM (1990) A physiological basis of populations processes: ecotoxicological implications. Funct Ecol 4:283–288
Castiglioni DS, Bond-Buckup G (2008) Ecological traits of two sympatric species of Hyalella Smith, 1874 (Crustacea, Amphipoda, Dogielinotidae) from southern Brazil. Acta Oecol 33:36–48
Chan LPE, Swaminathan R (1986) Adenosine-triphosphate interferes with phosphate determination. Clin Chem 32:1981
da Silva MD, Peralba MDR, Mattos MLT (2003) Determinação de glifosato e ácido aminometilfosfônico em águas superficiais do arroio passo do pilão. Pesticidas: R. Ecotoxicol. Meio Ambiente 13:19–28
Donker MH (1992) Energy reserves and distribution of metals in populations of the isopod Porcellio caber from metal contaminated sites. Funct Ecol 6:445–454
Dutra BK (2007) Estudo do Metabolismo Intermediário e da Lipoperoxidação de Hyalella curvispina e Hyalella pleoacuta (Crustacea, Amphipoda, Dogielinotidae) e Padronização destas Espécies como Bioindicadores Ambientais. Programa de Pós-graduação em Zoologia. Pontifícia Universidade Católica do Rio Grande do Sul, PUC RS, Brasil, 180pp
Dutra BK, Santos RB, Castiglioni DS, Bueno AAP, Bond-Buckup G, Oliveira GT (2007) Seasonal variations of the energy metabolism of two sympatric species of Hyalella (Crustacea, Amphipoda, Dogielinotidae) in the southern Brazilian highlands. Comp Biochem Physiol A 148:239–247
Dutra BK, Fernandes FA, Oliveira GT (2008) Carbofuran-induced alterations in biochemical composition, lipoperoxidation, and Na+/K+ATPase activity of Hyalella pleoacuta and Hyalella curvispina in bioassays. Comp Biochem Physiol C 147:179–188
Dutra BK, Fernandes FA, Laufer AL, Oliveira GT (2009) Carbofuran-induced alterations in biochemical composition, lipoperoxidation, and Na+/K+ATPase activity of Hyalella castroi in bioassays. Comp Biochem Physiol C 149:640–646
Esmann M (1988) ATPase and phosphatase activity of Na+K+-ATPase: molar and specific activity, protein determination. Meth Enzymol 156:105–115
Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
Geary N, Langhans W, Scharrer E (1981) Metabolic concomitants of glucagon-induced suppression of feeding in the rat. Am J Physiol 241:330–335
Gerhardt SD, Brune A, Schink B (2005) Dynamics of redox changes of iron caused by light–dark variations in littoral sediment of a freshwater lake. Biogeochemistry 74:323–339
Gering FS, de Oliveira LF, Dutra BK, Oliveira GT (2009) Biochemical composition, lipoperoxidation, Na+/K+ATPase activity and reproduction of Hyalella castroi (Amphipoda, Dogielinotidae) fed with different diets. J Exp Zool 311:408–421
Glusczak L, Miron DS, Moraes BS, Simões RR, Schetinger MRC, Morsch VM, Loro VL (2007) Acute effects of glyphosate herbicide on metabolic and enzymatic parameters of silver catfish (Rhamdia quelen). Comp Biochem Physiol C 146:519–524
Goldsborough L, Brown D (1989) Rapid dissipation of glyphosate in small forest ponds. Arch Environ Contam Toxicol 18:537–544
Irving EC, Baird DJ, Culp JM (2003) Ecotoxicological responses of the mayfly Baetis tricauadatus to dietary and waterborne cadmium: implications for toxicity testing. Environ Toxicol Chem 22:1058–1064
Langiano VC, Martinez CBR (2008) Toxicity and effects of a glyphosate-based herbicide on the neotropical fish Prochilodus lineatus. Comp Biochem Physiol C 147:222–231
Llesuy SF, Milei J, Molina H, Boveris A, Milei S (1985) Comparison of lipid peroxidation and myocardial damage induced by adriamycin and 4′-epiadrimicin in mice. Tumor 71:241–249
Lowry OH, Rosenbrough NJ, Fau AL, Randal RJ (1951) Protein measurements with the Folin phenol reagent. J Biol Chem. 193:265–275
Maltby L (1994) Stress, shredders and streams: using Gammarus energetics to assess water quality. In: Sutcliffe DW (ed) Water quality and stress indicator in marine and freshwater ecosystems. Linking levels organizations individuals, populations and communities. Freshwater Biological Association, Windermere, pp 98–110
Maltby L, Naylor C (1990) Preliminary observations on the ecological relevance of the Gammarus ‘scope of growth’ assay: Effect of zinc on reproduction. Funct Ecol 4:393–397
Maltby L, Kedwards TJ, Forbes VE, Grasman K, Kammenga JE, Munns WR Jr, Ringwood AH, Weis JS, Wood SN (2001) Linking individual-level response and population-level consequences. In: Baird DJ, Burton GA Jr (eds) Ecological variability: separating natural and anthropogenic causes of ecosystem impairment. SETAC, Pensacola, pp 27–82
Matthiessen P, Sheahan D, Harrison R, Kirby M, Rycroft R, Turnbull A, Volkner C, Williams R (1995) Use of a Gammarus pulex bioassay to measure the effects of transient carbofuran runoff from farmland. Ecotoxicol Environ Saf 30:111–119
Mecocci P, Beal MF, Cecchetti R, Polidori MC, Cherubini A, Chionne F, Avellini L, Romano G, Senin U (1997) Mitochondrial membrane fluidity and oxidative damage to mitochondrial DNA in aged and AD human brain. Mol Chem Neuropathol 31:53–64
Meyer E, Walter A (1980) Methods for the estimation of protein, lipid, carbohydrate and chitin levels in fresh water invertebrates. Arch Hydrobiol 113:161–177
Milatovic D, Gupta RC, Dekundy A, Montine TJ, Dettbarn WD (2005) Carbofuran-induced oxidative stress in slow and fast skeletal muscles: prevention by memantine and atropine. Toxicology 208:13–24
Naqvi SM, Vaishnavi C (1993) Bioaccumulative potential and toxicity of endosulfan insecticide to non-target animals. Comp Biochem Physiol C 105:347–361
Naylor C, Malby L, Callow P (1989) Scope for growth in Gammarus pulex, a freshwater detritivore. Hydrobiologia 188(189):517–523
Peixoto F (2005) Comparative effects of the Roundup and glyphosate on mitochondrial oxidative phosphorylation. Chemosphere 61:1115–1122
Pérez GL, Torremorell A, Mugni H, Rodríguez P, Solange M, do Nascimento VM, Allende L, Bustingorry J, Escaray R, Ferraro M, Izaguirre I, Pizarro H, Bonetto C, Morris DP, Zagarese H (2007) Effects of the herbicide roundup on freshwater microbial communities: a mesocosm study. Ecol Appl 17:2310–2322
Rambabu JP, Rao MB (1994) Effect of an organochlorine and three organophosphate pesticides on glucose, glycogen, lipid, and protein contents in tissues of the freshwater snail Bellamya dissimillis (Müller). Bull Environ Contam Toxicol 53:142–148
Relyea RA (2005) The lethal impact of Roundup on aquatic and terrestrial amphibians. Ecol Appl 15:1118–1124
Ren NQ, Zhang XD, Zhou GH, Chen SJ (2008) Induced apoptosis and mechanism of endosulfan in mouse germ cells. Huan Jing Ke Xué 29:386–390
Ribeiro S, Sousa JP, Nogueira AJA, Soares AMVM (2001) Effect of endosulfan and parathion on energy reserves and physiological parameters of the terrestrial Isopod porcellio dilatatus. Ecotoxicol Environ Saf 49:131–138
Roddie BD, Redshaw CJ, Nixon S (1996) Sublethal biological effects of monitoring using the common mussel, Mytilus edulis. Comparison of laboratory and in situ effects of an industrial effluent discharge. In: Tapp JF, Hunt SM, Wharfe JR (eds) Toxic impacts of wastes on the aquatic environment. Royal Society of Chemistry, Cambridge, pp 125–137
Rodrigues BN, Almeida FS (1998). Guia de Herbicidas. Londrina, Paraná-Brazil, 648pp
Salisbury FB, Ross CW (1994) Fisiología vegetal. Grupo Editorial Iberoamérica, México
Sancho E, Ferrando MD, Fernandez C, Andreu E (1998) Liver energy metabolism of Anguilla anguilla after exposure to fenitrothion. Ecotoxicol Environ Saf 41:168–175
Sorensen FF, Weeks JM, Baatrup E (1997) Altered locomotory behavior in woodlice (Oniscus asellus (L.)) collected at a polluted site. Environ Toxicol Chem 16:685–690
Tellez-Bañuelos MC, Santerre A, Casas-Solis J, Bravo-Cuellar A, Zaitseva G (2009) Oxidative stress in macrophages from spleen of Nile tilapia (Oreochromis niloticus) exposed to sublethal concentration of endosulfan. Fish Shelf Immunol 27:105–111
Tsui MTK, Chu LM (2004) Comparative toxicity of glyphosate-based herbicides: aqueous and sediment porewater exposures. Arch Environ Contam Toxicol 46:316–323
Van Brummelen TC, Stuijfzand SC (1993) Effects of benzo(a)pyrene on survival, growth and energy reserves in the terrestrial isopods Oniscus asellus and Porcellio scaber. Sci Tot Environ Suppl 93:921–930
Van Brummelen TC, Van Gestel CAM, Verweij RA (1996) Long-term toxicity of polycyclic aromatic hydrocarbons for the terrestrial isopods Oniscus asellus and Porcellio scaber. Environ Toxicol Chem 15:1199–1210
Van Handel E (1965) Estimation of glycogen in small amounts of tissue. Anal Biochem 11:256–265
Wayland M, Boag DA (1990) Toxicity of carbofuran to selected macroinvertebrates in prairie ponds. Bull Environ Contam Toxicol 45:1685–1691
WHO (1994) Environmental heal criteria: glyphosate. World Health Organization, Geneva
Williams GM, Kroes R, Munro IC (2000) Safety evaluation and risk assessment of the herbicide Roundup and its active ingredient, glyphosate, for human. Regul Toxicol Pharmacol 31:117–165
Acknowledgments
The authors wish to express their gratitude to the reviewer for the valorous suggestion of change in this work. The current stuffy was supported by the CAPES/MINCYT (Brazil-Argentina) for the financial support to Dr. Guendalina Turcato Oliveira (Project 50/03) and by fellowship give by Conselho Nacional de Desenvolvimento Tecnológico (CNPq, Process no. 140283/2008-0) to the first author. This work was carried out according to state and federal laws concerning wild animal sampling.
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Dutra, B.K., Fernandes, F.A., Failace, D.M. et al. Effect of roundup® (glyphosate formulation) in the energy metabolism and reproductive traits of Hyalella castroi (Crustacea, Amphipoda, Dogielinotidae). Ecotoxicology 20, 255–263 (2011). https://doi.org/10.1007/s10646-010-0577-x
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DOI: https://doi.org/10.1007/s10646-010-0577-x