Advertisement

Developmental and lethal effects of glyphosate and a glyphosate-based product on Xenopus laevis embryos and tadpoles

  • Duygu Özhan Turhan
  • Abbas GüngördüEmail author
  • Murat Ozmen
Article

Abstract

Effects of pure glyphosate and a glyphosate-based product were evaluated comparatively using two embryonic development stages of Xenopus laevis as model system. When pure glyphosate was applied in pH adjusted media, lethal or developmental effects were not observed at concentrations up to 500 mg L−1. The 96 h LC50 values for the commercial herbicide, in contrast, were 32.1 and 35.1 mg active ingredient L−1 for embryos and tadpoles, respectively. Since pure glyphosate has no effect on the selected biomarkers, it is thought that developmental toxic effects caused by glyphosate-based products are increased mainly due to formulation additives.

Keywords

Xenopus laevis Glyphosate Roundup Toxicity 

Notes

References

  1. ASTM (2003) American Society for Testing and Materials, Standard guide for conducting the Frog Embryo Teragonesis Assay-Xenopus (FETAX), E1439-98. In: ASTM standards on biological effects and environmental fate, Vol. 11.05. Philadelphia, PA, pp 447–457Google Scholar
  2. Babalola OO, Truter JC, van Wyk JH (2019) Mortality, teratogenicity and growth inhibition of three glyphosate formulations using frog embryo teratogenesis Assay-Xenopus. J Appl Toxicol.  https://doi.org/10.1002/jat.3811 CrossRefGoogle Scholar
  3. Bach NC, Marino DJG, Natale GS, Somoza GM (2018) Effects of glyphosate and its commercial formulation, Roundup((R)) Ultramax, on liver histology of tadpoles of the neotropical frog, Leptodactylus latrans (amphibia: Anura). Chemosphere 202:289–297Google Scholar
  4. Bantle JA (1995) FETAX-A developmental toxicity assay using frog embryos. In: Rand GM (ed) Fundamental aquatic toxicology. Taylor and Francis, Washington, DC, pp 207–230Google Scholar
  5. Benbrook CM (2016) Trends in glyphosate herbicide use in the United States and globally. Environ Sci Eur 28:3.  https://doi.org/10.1186/s12302-016-0070-0 CrossRefGoogle Scholar
  6. Benbrook CM (2019) How did the US EPA and IARC reach diametrically opposed conclusions on the genotoxicity of glyphosate-based herbicides? Environ Sci Eur 31:2.  https://doi.org/10.1186/s12302-018-0184-7 CrossRefGoogle Scholar
  7. Bonfanti P, Saibene M, Bacchetta R, Mantecca P, Colombo A (2018) A glyphosate micro-emulsion formulation displays teratogenicity in Xenopus laevis. Aquat Toxicol 195:103–113Google Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254Google Scholar
  9. Brausch JM, Smith PN (2007) Toxicity of three polyethoxylated tallowamine surfactant formulations to laboratory and field collected fairy shrimp, Thamnocephalus platyurus. Arch Environ Contam Toxicol 52:217–221Google Scholar
  10. Cattani D, de Liz Oliveira Cavalli VL, Heinz Rieg CE, Domingues JT, Dal-Cim T, Tasca CI, Mena Barreto Silva FR, Zamoner A, (2014) Mechanisms underlying the neurotoxicity induced by glyphosate-based herbicide in immature rat hippocampus: involvement of glutamate excitotoxicity. Toxicology 320:34–45Google Scholar
  11. Carvalho WF, Ruiz de Arcaute C, Pérez-Iglesias JM, Laborde MRR, Soloneski S, Larramendy ML (2019) DNA damage exerted by mixtures of commercial formulations of glyphosate and imazethapyr herbicides in Rhinella arenarum (Anura, Bufonidae) tadpoles. Ecotoxicology 28(3):367–377Google Scholar
  12. Edge C, Gahl M, Thompson D, Hao C, Houlahan J (2014) Variation in amphibian response to two formulations of glyphosate-based herbicides. Environ Toxicol Chem 33:2628–2632Google Scholar
  13. Edginton AN, Sheridan PM, Stephenson GR, Thompson DG, Boermans HJ (2004) Comparative effects of pH and Vision (R) herbicide on two life stages of four anuran amphibian species. Environ Toxicol Chem 23:815–822Google Scholar
  14. Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95Google Scholar
  15. Fort DJ, Guiney PD, Weeks JA, Thomas JH, Rogers RL, Noll AM, Spaulding CD (2004) Effect of methoxychlor on various life stages of Xenopus laevis. Toxicol Sci 81:413–454Google Scholar
  16. Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup (R) Herbicide. Rev Environ Contam Toxicol 167(167):35–120Google Scholar
  17. Gill JPK, Sethi N, Mohan A, Datta S, Girdhar M (2018) Glyphosate toxicity for animals. Environ Chem Lett 16:401–426Google Scholar
  18. Güngördü A (2013) Comparative toxicity of methidathion and glyphosate on early life stages of three amphibian species: Pelophylax ridibundus, Pseudepidalea viridis, and Xenopus laevis. Aquat Toxicol 140–141:220–228Google Scholar
  19. Güngördü A, Uckun M, Yologlu E (2016) Integrated assessment of biochemical markers in premetamorphic tadpoles of three amphibian species exposed to glyphosate- and methidathion-based pesticides in single and combination forms. Chemosphere 144:2024–2035Google Scholar
  20. Guyton KZ, Loomis D, Grosse Y, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Scoccianti C, Mattock H, Straif K (2015) Carcinogenicity of tetrachlorvinphos, parathion, malathion, diazinon, and glyphosate. Lancet Oncol 16:490–491Google Scholar
  21. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  22. Hansen LR, Roslev P (2016) Behavioral responses of juvenile Daphnia magna after exposure to glyphosate and glyphosate-copper complexes. Aquat Toxicol 179:36–43Google Scholar
  23. Hong YH, Yang XZ, Huang Y, Yan GW, Cheng YX (2018) Assessment of the oxidative and genotoxic effects of the glyphosate-based herbicide roundup on the freshwater shrimp, Macrobrachium nipponensis. Chemosphere 210:896–906Google Scholar
  24. 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 23:1928–1938Google Scholar
  25. IUCN (2019) www.iucnredlist.org. Accessed Nov 4, 2019
  26. Iummato MM, Sabatini SE, Cacciatore LC, Cochón AC, Cataldo D, de Molina MDCR, Juárez ÁB (2018) Biochemical responses of the golden mussel Limnoperna fortunei under dietary glyphosate exposure. Ecotoxicol Environ Saf 15:69–75Google Scholar
  27. Jacques MT, Bornhorst J, Soares MV, Schwerdtle T, Garcia S, Avila DS (2019) Reprotoxicity of glyphosate-based formulation in Caenorhabditis elegans is not due to the active ingredient only. Environ Pollut 252(Pt B):1854–1862Google Scholar
  28. Lanzarin GAB, Felix LM, Santos D, Venancio CAS, Monteiro SM (2019) Dose-dependent effects of a glyphosate commercial formulation - Roundup® UltraMax - on the early zebrafish embryogenesis. Chemosphere 223:514–522Google Scholar
  29. 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 60:681–689Google Scholar
  30. Lajmanovich RC, Junges CM, Attademo AM, Peltzer PM, Cabagna-Zenklusen MC, Basso A (2013) Individual and Mixture Toxicity of Commercial Formulations Containing Glyphosate, Metsulfuron-Methyl, Bispyribac-Sodium, and Picloram on Rhinella arenarum Tadpoles. Water Air Soil Pollut 224:1404Google Scholar
  31. Li J, Smeda RJ, Sellers BA, Johnson WG (2005) Influence of formulation and glyphosate salt on absorption and translocation in three annual weeds. Weed Sci 53:153–159Google Scholar
  32. Mann RM, Bidwell JR (1999) The toxicity of glyphosate and several glyphosate formulations to four species of southwestern Australian frogs. Arch Environ Contam Toxicol 36:193–199Google Scholar
  33. Miko Z, Ujszegi J, Gal Z, Hettyey A (2017) Effects of a glyphosate-based herbicide and predation threat on the behaviour of agile frog tadpoles. Ecotoxicol Environ Saf 140:96–102Google Scholar
  34. Monsanto (2019) Monsanto product safety assistance website. https://www.sdslibrary.monsanto.com/Pages/Default.aspx. Accessed Dec 4, 2019
  35. Moore LJ, Fuentes L, Rodgers JH Jr, Bowerman WW, Yarrow GK, Chao WY, Bridges WC Jr (2012) Relative toxicity of the components of the original formulation of Roundup to five North American anurans. Ecotoxicol Environ Saf 78:128–133Google Scholar
  36. Navarro-Martin L, Lanctot C, Jackman P, Park BJ, Doe K, Pauli BD, Trudeau VL (2014) Effects of glyphosate-based herbicides on survival, development, growth and sex ratios of wood frogs (Lithobates sylvaticus) tadpoles. I: Chronic laboratory exposures to VisionMax (R). Aquat Toxicol 154:278–290Google Scholar
  37. Pereira AG et al (2018) Low-concentration exposure to glyphosate-based herbicide modulates the complexes of the mitochondrial respiratory chain and induces mitochondrial hyperpolarization in the Danio rerio brain. Chemosphere 209:353–362Google Scholar
  38. Perez GL, Vera MS, Miranda L (2011) Effects of herbicide glyphosate and glyphosate-based formulations on aquatic ecosystems. In: Kortekamp A (ed) Herbicides and environment. IntechOpen, Rijeka.Google Scholar
  39. Perkins PJ, Boermans HJ, Stephenson GR (2000) Toxicity of glyphosate and triclopyr using the frog embryo teratogenesis assay–Xenopus. Environ Toxicol Chem 19:940–945Google Scholar
  40. Relyea RA, Jones DK (2009) The toxicity of Roundup Original Max to 13 species of larval amphibians. Environ Toxicol Chem 28:2004–2008Google Scholar
  41. Relyea RA (2011) Amphibians Are Not Ready for Roundup®. In: Elliott JE, Bishop CA, Morrissey CA (eds) Wildlife ecotoxicology: forensic approaches. Springer, New York, pp 267–300Google Scholar
  42. Samanta P, Pal S, Mukherjee AK, Ghosh AR (2014) Biochemical effects of glyphosate based herbicide, Excel Mera 71 on enzyme activities of acetylcholinesterase (AChE), lipid peroxidation (LPO), catalase (CAT), glutathione-S-transferase (GST) and protein content on teleostean fishes. Ecotoxicol Environ Saf 107:120–125Google Scholar
  43. SERA (2011) Glyphosate—human health and ecological risk assessment—final Report. USDA, Forest Service, Forest Health Protection. SERA TR-052-22-03b. Atlanta, Georgia. https://www.fs.fed.us/foresthealth/pesticide/pdfs/Glyphosate_SERA_TR-052-22-03b.pdf
  44. Silveira T et al (2019) Roundup (R) Herbicide decreases quality parameters of spermatozoa of silversides odontesthes humensis. Bull Environ Contam Toxicol 102:1–6Google Scholar
  45. Smith GR (2001) Effects of acute exposure to a commercial formulation of glyphosate on the tadpoles of two species of anurans. Bull Environ Contam Toxicol 67:483–488Google Scholar
  46. Stephensen E, Svavarsson J, Sturve J, Ericson G, Adolfsson-Erici M, Forlin L (2000) Biochemical indicators of pollution exposure in shorthorn sculpin (Myoxocephalus scorpius), caught in four harbours on the southwest coast of Iceland. Aquat Toxicol 48:431–442Google Scholar
  47. Szekacs A, Darvas B (2018) Re-registration challenges of glyphosate in the European Union. Front Environ Sci 6:1–35Google Scholar
  48. Tush D, Loftin KA, Meyer MT (2013) Characterization of polyoxyethylene tallowamine surfactants in technical mixtures and glyphosate formulations using ultra-high performance liquid chromatography and triple quadrupole mass spectrometryle. J Chromatogr A 1319:80–87Google Scholar
  49. Tush D, Maksimowicz MM, Meyer MT (2018) Dissipation of polyoxyethylene tallowamine (POEA) and glyphosate in an agricultural field and their co-occurrence on streambed sediments. Sci Total Environ 636:212–219Google Scholar
  50. Walsh PT, Downie JR, Monaghan P (2008) Plasticity of the duration of metamorphosis in the African clawed toad. J Zool 274:143–149Google Scholar
  51. Wagner N, Reichenbecher W, Teichmann H, Tappeser B, Lotters S (2013) Questions concerning the potential impact of glyphosate-based herbicides on amphibians. Environ Toxicol Chem 32:1688–1700Google Scholar
  52. 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 Pharmacol 31:117–165Google Scholar
  53. Yanniccari M, Istilart C, Gimenez DO, Castro AM (2012) Effects of glyphosate on the movement of assimilates of two Lolium perenne L. populations with differential herbicide sensitivity. Environ Exp Bot 82:14–19Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2020

Authors and Affiliations

  • Duygu Özhan Turhan
    • 1
  • Abbas Güngördü
    • 1
    Email author
  • Murat Ozmen
    • 1
  1. 1.Laboratory of Environmental Toxicology, Department of Biology, Faculty of Arts and SciencesInonu UniversityMalatyaTurkey

Personalised recommendations