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Ovarian growth impairment after chronic exposure to Roundup Ultramax® in the estuarine crab Neohelice granulata

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Abstract

Adult females of the estuarine crab Neohelice granulata were exposed to the glyphosate formulation Roundup Ultramax® during the entire 3-month pre-reproductive period. At the end of the assay, a significant higher increment of glycemia was noted at both glyphosate concentrations assayed (0.01 and 0.2 mg/L, acid equivalent). Although no differences were observed in the gonadosomatic index, a significantly higher proportion of reabsorbed vitellogenic oocyte was observed at the highest glyphosate concentration, together with a significant decrease of vitellogenin content in the ovary. In addition, some in vitro assays were carried out by co-incubating small pieces of ovary with or without the addition of Roundup; at both concentrations tested (same as those used in vivo), a decrease in the ovarian vitellogenin content was observed, whereas the ovarian protein synthesis was significantly inhibited by glyphosate at 0.2 mg/L in the Roundup formulation used.

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References

  • American Public Health Association, American Water Works Association, Water Pollution Control Federation (2005) Standard methods for the examination of water and wastewaters, 21st edn. American Public Health Association, Washington DC

    Google Scholar 

  • Aparicio VC, De Gerónimo E, Marino D, Primost J, Carriquiriborde P, Costa JL (2013) Environmental fate of glyphosate and aminomethylphosphonic acid in surface waters and soil of agricultural basins. Chemosphere 93:1866–1873

    Article  CAS  Google Scholar 

  • Arancibia F (2013) Challenging the bioeconomy: the dynamics of collective action in Argentina. Technol Soc 35:79–22

    Article  Google Scholar 

  • Avigliano L, Álvarez NB, Mac Loughlin C, Rodríguez EM (2014a) Effects of glyphosate on egg incubation, larvae hatching and ovarian re-maturation, in the estuarine crab Neohelice granulata. Environ Toxicol Chem 33:1879–1884

    Article  CAS  Google Scholar 

  • Avigliano L, Fassiano AV, Medesani DA, Ríos de Molina MC, Rodríguez EM (2014b) Effects of glyphosate on growth rate, metabolic rate and energy reserves of early juvenile crayfish, Cherax quadricarinatus M. B Environ ContamToxicol 92:631–635

    Article  CAS  Google Scholar 

  • BenckSoso A, Gil Barcello LJ, Ranzani-Paiva MJ, Kreutz LC, Mezzalira Quevedo R, Anziliero D, Lima M, Bolognesi da Silva L, Ritter F, Calliari Bedin A, Finco JA (2007) Chronic exposure to sub-lethal concentration of a glyphosate-based herbicide alters hormone profiles and affects reproduction of female Jundiá (Rhamdiaquelen). Environ Toxicol Phar 23:308–313

    Article  Google Scholar 

  • Cahansky AV, Medesani DA, Chaulet A, Rodríguez EM (2011) In vitro effects of both dopaminergic and enkephalinergic antagonists on the ovarian growth of Cherax quadricarinatus (Decapoda, Parastacidae), at different periods of the reproductive cycle. Comp Biochem Physiol 158A:126–131

    Article  CAS  Google Scholar 

  • Chang ES, Chang SA, Keller R, Reddy PS, Snyder MJ, Spees JL (1999) Quantification of stress in lobsters: crustacean hyperglycemic hormone, stress protein and gene expression. Am Zool 39:487–495

    Article  CAS  Google Scholar 

  • Charmantier G, Charmantier-Daures M, Van Herp F (1997) Hormonal regulation of growth and reproduction in crustaceans. In: Fingerman M, Nagabhushanam R, Thompson MF (eds) Recent advances in marine biotechnology. Oxford & IBH Publishing Co, New Delhi, pp 109–161

    Google Scholar 

  • Chaulet A, Medesani DA, Freitas J, Cervino A, Cervino N, Rodríguez EM (2012) Induction of somatic growth in juvenile crayfish Cherax quadricarinatus (Decapoda, Parastacidae), by ecdysone and insulin growth factor. Aquaculture 370–371:1–6

    Article  Google Scholar 

  • Comisión Administradora del Río de la Plata (1990) Estudio para la evaluación de la contaminación en el Río de la Plata. Argentine Hydrographic Service Navy, Buenos Aires

    Google Scholar 

  • Cooke IM, Haylett BA, Weatherby TM (1977) Electrically elicited neurosecretory and electrical responses of the isolated crab sinus gland in normal and reduced calcium salines. J Exp Biol 101:125–149

    Google Scholar 

  • De Kleijn DPV, Van Herp F (1998) Involvement of the hyperglycaemic neurohormone family in the control of reproduction in decapod crustaceans. Invertebr Rep Dev 33:263–272

    Article  Google Scholar 

  • Dreon MS, Heras H, Pollero RJ (2003) Metabolism of ovorubin, the major egg lipoprotein from the apple snail. Mol Cell Biochem 243:9–14

    Article  CAS  Google Scholar 

  • Eastman-Reks SB, Fingerman M (1985) In vitro synthesis of vitellin by the ovary of the fiddler crab Uca pugilator. J Exp Zool 233:111–116

    Article  CAS  Google Scholar 

  • Elwood RW, Barr S, Patterson L (2009) Pain and stress in crustaceans? App Anim Behav Sci 118:128–136

    Article  Google Scholar 

  • Fanjul-Moles ML (2006) Biochemical and functional aspects of crustacean hyperglycemic hormone in decapod crustaceans: review and update. Comp Biochem Physiol 142C:390–400

    CAS  Google Scholar 

  • Folch J, Lees M, Stanley GHS (1957) A simple method for isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  Google Scholar 

  • Fring CS, Dunn RT (1970) A colorimetric method for determination of total serum lipids based on the sulfo-phospho-vanillin reaction. Am J Clin Pathol 53:89–91

    Article  Google Scholar 

  • Frontera JL, Vatnick I, Chaulet A, Rodríguez EM (2011) Effects of glyphosate and polyoxyethylenamine on growth and energetic reserves in the freshwater crayfish Cherax quadricarinatus (Decapoda, Parastacidae). Arch Environ Con Toxicology 61:590–598

    Article  CAS  Google Scholar 

  • García F, Cunningham ML, Garda H, Heras H (2008) Embryo lipoproteins and yolk lipovitellin consumption during embryogenesis in Macrobrachium borellii (Crustacea: Palaemonidae). J Comp Physiol 151B:317–322

    Google Scholar 

  • Gasnier C, Dumont C, Benachour N, Clair E, Chagnon MC, Séralini GE (2009) Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines. Toxicology 262:184–191

    Article  CAS  Google Scholar 

  • Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for roundup herbicide. Rev Environ Contam 167:35–120

    CAS  Google Scholar 

  • Gu PL, KL Y, Chan SM (2000) Molecular characterization of an additional shrimp hyperglycemic hormone: cDNA cloning, gene organization, expression and biological assay of recombinant proteins. FEBS Lett 472:122–128

    Article  CAS  Google Scholar 

  • Howe CM, Berrill M, Pauli BD, Helbing CC, Werry K, Veldhoen N (2004) Toxicity of glyphosate-based pesticides to four North American frog species. Environ Toxicol Chem 23:1928–1938

    Article  CAS  Google Scholar 

  • Kogan M, López Greco LS, Romano LA, Rodríguez EM (2000) Effects of cadmium on somatic and gonadal growth of juvenile females of the estuarine crab Chasmagnathus granulata (Brachyura, Grapsidae). Zool Stud 39:344–350

    CAS  Google Scholar 

  • López Greco LS, Rodríguez EM (1999) Annual reproduction and growth of adult crabs, Chasmagnathus granulata (Crustacea, Brachyura, Grapsidae). Cah Biol Mar 40:155–164

    Google Scholar 

  • Lowry OH, Rosenbrough NJ, Randal RJ (1951) Protein measurements with the Folin phenol reagent. J Biol Chem 183:265–275

    Google Scholar 

  • Lydon J, Duke SO (1989) Pesticide effects on secondary metabolism of greater plants. Pestic Sci 25:361–373

    Article  CAS  Google Scholar 

  • Mann RM, Bidwell JR (1999) The toxicity of glyphosate and several glyphosate formulations to four species of southwestern Australian frogs. Arch Environ Con Toxicology 36:193–199

    Article  CAS  Google Scholar 

  • Mayer FL, Versteeg DJ, McKee MJ, Folmar LC, Graney RL, McCume DC, Rattner BA (1992) Physiological and nonspecific biomarkers. In: Huggett RJ, Kimerle RA, Mehrle Jr PM, Bergman HL (eds) Biomarkers: biochemical, physiological and histological markers of anthropogenic stress. Society of Environmental Toxicology and Chemistry special publications series, Lewis publishers, Boca Raton, pp 5–85

  • Nagaraju GPC (2011) Reproductive regulators in decapod crustaceans: an overview. J Exp Biol 214:3–16

    Article  CAS  Google Scholar 

  • Peruzzo PJ, Porta AA, Ronco AE (2008) Levels of glyphosate in surface waters, sediments and soil associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environ Pollut 156:61–66

    Article  CAS  Google Scholar 

  • Reddy Buchi S, Vaadala S, Hosamani N, Reddy Pamuru R, Reddy Pamanji S (2016) Regulation of vitellogenesis by selected endocrine modulators in crab Oziothelphusa senex senex, with special reference to methyl farnesoate. Aquacult Rep 3:24–30

    Article  Google Scholar 

  • Richard S, Moslemi S, Sipahutar H, Benachour N, Seralini GE (2005) Differential effects of glyphosate and roundup on human placental cells and aromatase. Environ Health Persp 113:716–720

    Article  CAS  Google Scholar 

  • Rodríguez EM, Schuldt M, Romano L (1994) Chronic histopathological effects of parathion and 2,4-D on female gonads of Chasmagnathus granulata (Decapoda, Brachyura). Food Chem Toxicol 32:811–818

    Article  Google Scholar 

  • Rodríguez EM, López Greco LS, Fingerman M (2000) Inhibition of ovarian growth by cadmium, in the fiddler crab Uca pugilator (Decapoda, Ocypodidae). Ecotox Environ Saf 46:202–206

    Article  Google Scholar 

  • Rodríguez EM, López Greco LS, Medesani DA, Laufer H, Fingerman M (2002) Effect of methyl farnesoate, alone and in combination with other hormones, on ovarian growth of the red swamp crayfish, Procambarus clarkii, during vitellogenesis. Gen Comp Endocrinol 125:34–40

    Article  Google Scholar 

  • Sánchez F, Mari N, Lasta C, Giangioble A (1991) Alimentación de la corvina rubia (Micropogonias furnieri) en la Bahía de Samborombón. Frente Marítimo 8:43–50

    Google Scholar 

  • Sarojini R, Nagabhushanam R, Fingerman M (1997) An in vitro study of the inhibitory action of methionine enkephaline on ovarian maturation in the red swamp crayfish, Procambarus clarkii. Comp Biochem Physiol 117C:207–210

    CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, New York

    Google Scholar 

  • Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance n aquatic invertebrates. Mar Environ Res 79:1–15

    Article  CAS  Google Scholar 

  • Solomon KR, Thompson DG (2003) Ecological risks assessment for aquatic organisms from overwater uses of glyphosate. J Toxicol Environ Health 6B:289–324

    Article  Google Scholar 

  • Sook Chung J, Zmora N, Katayama H, Tsutsui N (2010) Crustacean hyperglycemic hormone (CHH) neuropeptides family: functions, titer, and binding to target tissues. Gen Comp Endocrinol 166:447–454

    Article  Google Scholar 

  • Van Handel E (1965) Estimation of glycogen in small amount soft tissue. Anal Biochem 1:256–265

    Article  Google Scholar 

  • Zapata V, López Greco LS, Rodríguez EM (2001) Effect of copper on hatching and development of larvae of the estuarine crab Chasmagnathus granulata (Decapoda, Brachyura). Environ Toxicol Chem 20:1579–1583

    Article  CAS  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgements

This study was supported by grants from the University of Buenos Aires (UBACYT 2016–2018, code 20020150100060BA) and CONICET (PIP 2015, code 11220150100100CO).

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Correspondence to Enrique M. Rodríguez.

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Responsible editor: Philippe Garrigues

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Canosa, I.S., Silveyra, G.R., Avigliano, L. et al. Ovarian growth impairment after chronic exposure to Roundup Ultramax® in the estuarine crab Neohelice granulata . Environ Sci Pollut Res 25, 1568–1575 (2018). https://doi.org/10.1007/s11356-017-0581-2

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