Effects of glyphosate and a commercial formulation Roundup® exposures on maturation of Xenopus laevis oocytes

  • Sylvain Slaby
  • Pauline Titran
  • Guillaume Marchand
  • Julie Hanotel
  • Arlette Lescuyer
  • Alain Leprêtre
  • Jean-François Bodart
  • Matthieu Marin
  • Sébastien LemiereEmail author
Multi-Stressors in Freshwater and Transitional Environments: from Legacy Pollutants to Emerging Ones


Pesticides are often found at high concentrations in small ponds near agricultural field where amphibians are used to live and reproduce. Even if there are many studies on the impacts of phytopharmaceutical active ingredients in amphibian toxicology, only a few are interested in the earlier steps of their life cycle. While their populations are highly threatened with extinction. The aim of this work is to characterize the effects of glyphosate and its commercial formulation Roundup® GT Max on the Xenopus laevis oocyte maturation which is an essential preparation for the laying and the fertilization. Glyphosate is an extensively used herbicide, not only known for its effectiveness but also for its indirect impacts on non-target organisms. Our results showed that exposures to both forms of glyphosate delayed this hormone-dependent process and were responsible for spontaneous maturation. Severe and particular morphogenesis abnormalities of the meiotic spindle were also observed. The MAPK pathway and the MPF did not seem to be affected by exposures. The xenopus oocyte is particularly affected by the exposures and appears as a relevant model for assessing the effects of environmental contamination.


Amphibian toxicology Glyphosate Roundup Pesticide Oocyte Maturation Xenopus 



Sylvain Slaby is a recipient for a doctoral fellowship from French Minister of Higher Education, Research and Innovation. We are indebted to the Research Federation FRABio (Univ. Lille, CNRS, FR 3688, FRABio, Biochimie Structurale et Fonctionnelle des Assemblages Biomoléculaires) for providing the scientific and technical environment conducive to the achievement of this work.


  1. Akcha F, Spagnol C, Rouxel J (2012) Genotoxicity of diuron and glyphosate in oyster spermatozoa and embryos. Aquat Toxicol 106–107:104–113. CrossRefGoogle Scholar
  2. Alford RA (2010) Declines and the global status of amphibians. In: Sparling DW, Linder G, Bishop CA, Krest SK (eds) Ecotoxicology of amphibians and reptiles, 2nd edn. CRC Press, Boca Raton, USA, pp 13–45CrossRefGoogle Scholar
  3. Alford RA, Richards SJ (1999) Global amphibian declines: a problem in applied ecology. Annu Rev Ecol Syst 30:133–165. CrossRefGoogle Scholar
  4. Battaglin WA, Kolpin DW, Scribner EA, Kuivila KM, Sandstrom MW (2005) Glyphosate, other herbicides, and transformation products in midwestern stream, 2002. J Am Water Resour Assoc 41:323–332. CrossRefGoogle Scholar
  5. Blaustein AR, Romansic JM, Kiesecker JM, Hatch AC (2003) Ultraviolet radiation, toxic chemicals and amphibian population declines. Divers Distrib 9:123–140. CrossRefGoogle Scholar
  6. Blaustein AR, Wake DB (1990) Declining amphibian populations: a global phenomenon? Trends Ecol Evol 5:203–204. CrossRefGoogle Scholar
  7. Blaustein AR, Wake DB (1995) The puzzle of declining amphibian populations. Sci Am 272:52–57CrossRefGoogle Scholar
  8. Bonfanti P, Saibene M, Bacchetta R, Mantecca P, Colombo A (2018) A glyphosate micro-emulsion formulation displays teratogenicity in Xenopus laevis. Aquat Toxicol 195:103–113. CrossRefGoogle Scholar
  9. Botta F, Lavison G, Couturier G, Alliot F, Moreau-Guigon E, Fauchon N, Guery B, Chevreuil M, Blanchoud H (2009) Transfer of glyphosate and its degradate AMPA to surface waters through urban sewerage systems. Chemosphere 77:133–139. CrossRefGoogle Scholar
  10. Brachet J, Hanocq F, Van Gansen P (1970) A cytochemical and ultrastructural analysis of in vitro maturation in amphibian oocytes. Dev Biol 21:157–195. CrossRefGoogle Scholar
  11. Bridges CM, Boone MD (2003) The interactive effects of UV-B and insecticide exposure on tadpole survival, growth and development. Biol Conserv 113:49–54. CrossRefGoogle Scholar
  12. Duke SO, Powles SB (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 64:319–325. CrossRefGoogle Scholar
  13. Dumont JN (1972) Oogenesis in Xenopus laevis (Daudin) I Stages of oocyte development in laboratory maintained animals. J Morphol 136:153–179. CrossRefGoogle Scholar
  14. Ferrell JE (1999) Xenopus oocyte maturation: new lessons from a good egg. BioEssays 21:833–842.<833::AID-BIES5>3.0.CO;2-P CrossRefGoogle Scholar
  15. Frödin M, Gammeltoft S (1999) Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol Cell Endocrinol 151:65–77. CrossRefGoogle Scholar
  16. Gelaude A, Marin M, Cailliau K, Jeseta M, Lescuyer-Rousseau A, Vandame P, Nevoral J, Sedmikova M, Martoriati A, Bodart JF (2015) Nitric oxide sonor s-nitroso-n-acetyl penicillamine (SNAP) alters meiotic spindle morphogenesis in Xenopus oocytes. J Cell Biochem 116:2445–2454. CrossRefGoogle Scholar
  17. Guilherme S, Gaivão I, Santos MA, Pacheco M (2010) European eel (Anguilla anguilla) genotoxic and pro-oxidant responses following short-term exposure to Roundup®—a glyphosate-based herbicide. Mutagenesis 25:523–530. CrossRefGoogle Scholar
  18. Hans F, Dimitrov S (2001) Histone H3 phosphorylation and cell division. Oncogene 20:3021–3027. CrossRefGoogle Scholar
  19. Hendzel MJ, Wei Y, Mancini MA, van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360. CrossRefGoogle Scholar
  20. 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. CrossRefGoogle Scholar
  21. IARC (2017) Some organophosphate insecticides and herbicides - IARC monographs on the evaluation of carcinogenic risks to humans, vol 112. WHO Press, Lyon, FranceGoogle Scholar
  22. INERIS (2014) INERIS-Valeur Guide Environnementale : GlyphosateGoogle Scholar
  23. Ji Q, Lee J, Lin Y-H, Jing G, Tsai LJ, Chen A, Hetrick L, Jocoy D, Liu J (2016) Atrazine and malathion shorten the maturation process of Xenopus laevis oocytes and have an adverse effect on early embryo development. Toxicol in Vitro 32:63–69. CrossRefGoogle Scholar
  24. Lajmanovich RC, Attademo AM, Peltzer PM, Junges CM, Cabagna MC (2011) Toxicity of four herbicide formulations with glyphosate on Rhinella arenarum (Anura: Bufonidae) tadpoles: B-esterases and glutathione S-transferase inhibitors. Arch Environ Contam Toxicol 60:681–689. CrossRefGoogle Scholar
  25. Lopes FM, Junior ASV, Corcini CD et al (2014) Effect of glyphosate on the sperm quality of zebrafish Danio rerio. Aquat Toxicol 155:322–326. CrossRefGoogle Scholar
  26. Marin M, Slaby S, Marchand G, Demuynck S, Friscourt N, Gelaude A, Lemière S, Bodart JF (2015) Xenopus laevis oocyte maturation is affected by metal chlorides. Toxicol in Vitro 29:1124–1131. CrossRefGoogle Scholar
  27. Martinez DA, Loening UE, Graham MC (2018) Impacts of glyphosate-based herbicides on disease resistance and health of crops: a review. Environ Sci Eur 30:2. CrossRefGoogle Scholar
  28. Mesnage R, Defarge N, de Vendômois JS, Séralini GE (2015) Potential toxic effects of glyphosate and its commercial formulations below regulatory limits. Food Chem Toxicol 84:133–153. CrossRefGoogle Scholar
  29. Ministère de la Transition écologique et solidaire (2017) Les pesticides les plus rencontrés dans les eaux continentales. In: Les Pestic. dans les eaux. Accessed 26 Jun 2018
  30. Monastersky R (2014) Life—a status report. Nature 516:158–161. CrossRefGoogle Scholar
  31. Moore LJ, Fuentes L, Rodgers JH et al (2012) Relative toxicity of the components of the original formulation of Roundup® to five north American anurans. Ecotoxicol Environ Saf 78:128–133. CrossRefGoogle Scholar
  32. Nieuwkoop PD, Faber J (1967) Normal table of Xenopus laevis (Daudin): a systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis, 2nd edn. Garland Science, Amsterdam, NetherlandsGoogle Scholar
  33. Norbury C, Nurse P (1990) Controls of cell proliferation in yeast and animals. In: Bock G, Marsh J (eds) Ciba Foundation Symposium 150-proto-oncogenes in cell development. John Wiley & Sons, Ltd., Chichester, pp 168–183Google Scholar
  34. Peruzzo 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. CrossRefGoogle Scholar
  35. Rissoli RZ, Abdalla FC, Costa MJ, Rantin FT, McKenzie DJ, Kalinin AL (2016) Effects of glyphosate and the glyphosate based herbicides Roundup Original® and Roundup Transorb® on respiratory morphophysiology of bullfrog tadpoles. Chemosphere 156:37–44. CrossRefGoogle Scholar
  36. Slaby S, Hanotel J, Marchand G, Lescuyer A, Bodart JF, Leprêtre A, Lemière S, Marin M (2017) Maturation of Xenopus laevis oocytes under cadmium and lead exposures: cell biology investigations. Aquat Toxicol 193:105–110. CrossRefGoogle Scholar
  37. Sparling DW, Linder G, Bishop CA, Krest SK (2010) Recent advancements in amphibian and reptile ecotoxicology. In: Sparling DW, Linder G, Bishop CA, Krest SK (eds) Ecotoxicology of amphibians and reptiles, 2nd edn. CRC Press, Boca Raton, USA, pp 1–11CrossRefGoogle Scholar
  38. 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. CrossRefGoogle Scholar
  39. Struger J, Thompson D, Staznik B, Martin P, McDaniel T, Marvin C (2008) Occurrence of glyphosate in surface waters of southern Ontario. Bull Environ Contam Toxicol 80:378–384. CrossRefGoogle Scholar
  40. Székács A, Darvas B (2012) Forty years with glyphosate. In: Hasaneen MN (ed) Herbicides-properties, Synthesis and Control of Weeds. InTech, Rijeka, HR, pp 247–284Google Scholar
  41. Van Hooser A, Goodrich DW, Allis CD et al (1998) Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. J Cell Sci 111:3497 LP–3493506Google Scholar
  42. Yadav SS, Giri S, Singha U, Boro F, Giri A (2013) Toxic and genotoxic effects of Roundup on tadpoles of the Indian skittering frog (Euflictis cyanophlyctis) in the presence and absence of predator stress. Aquat Toxicol 132–133:1–8. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Sylvain Slaby
    • 1
    • 2
    • 3
  • Pauline Titran
    • 1
  • Guillaume Marchand
    • 1
  • Julie Hanotel
    • 1
  • Arlette Lescuyer
    • 1
  • Alain Leprêtre
    • 3
  • Jean-François Bodart
    • 1
  • Matthieu Marin
    • 1
  • Sébastien Lemiere
    • 3
    Email author
  1. 1.CNRS, INRA, UMR 8576-UGSF-Unité de Glycobiologie Structurale et FonctionnelleUniversity LilleLilleFrance
  2. 2.URAFPA, Unité de Recherche Animal et Fonctionnalités des Produits AnimauxUniversity de LorraineNancyFrance
  3. 3.EA 4515-LGCgE-Laboratoire Génie Civil et géo-Environnement, Cité scientifique, SN3University LilleVilleneuve d’AscqFrance

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