Ecotoxicology

, Volume 21, Issue 7, pp 1805–1816 | Cite as

Direct and indirect effects of the glyphosate formulation Glifosato Atanor® on freshwater microbial communities

  • María Solange Vera
  • Eugenia Di Fiori
  • Leonardo Lagomarsino
  • Rodrigo Sinistro
  • Roberto Escaray
  • María Mercedes Iummato
  • Angela Juárez
  • María del Carmen Ríos de Molina
  • Guillermo Tell
  • Haydée Pizarro
Article

Abstract

Glyphosate-based formulations are among the most widely used herbicides in the world. The effect of the formulation Glifosato Atanor® on freshwater microbial communities (phytoplankton, bacterioplankton, periphyton and zooplankton) was assessed through a manipulative experiment using six small outdoor microcosms of small volume. Three of the microcosms were added with 3.5 mg l−1 of glyphosate whereas the other three were left as controls without the herbicide. The treated microcosms showed a significant increase in total phosphorus, not fully explained by the glyphosate present in the Glifosato Atanor®. Therefore, part of the phosphorus should have come from the surfactants of the formulation. The results showed significant direct and indirect effects of Glifosato Atanor® on the microbial communities. A single application of the herbicide caused a fast increase both in the abundance of bacterioplankton and planktonic picocyanobacteria and in chlorophyll a concentration in the water column. Although metabolic alterations related to oxidative stress were induced in the periphyton community, the herbicide favored its development, with a large contribution of filamentous algae typical of nutrient-rich systems, with shallow and calm waters. An indirect effect of the herbicide on the zooplankton was observed due to the increase in the abundance of the rotifer Lecane spp. as a consequence of the improved food availability given by picocyanobacteria and bacteria. The formulation affected directly a fraction of copepods as a target. It was concluded that the Glifosato Atanor® accelerates the deterioration of the water quality, especially when considering small-volume water systems.

Keywords

Glyphosate formulation Microcosms Microbial communities Water quality 

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefGoogle Scholar
  2. Amorós I, Alonso JL, Romaguera S, Carrasco JM (2007) Assessment of toxicity of a glyphosate-based formulation using bacterial systems in lake water. Chemosphere 67:2221–2228CrossRefGoogle Scholar
  3. Amrhein N, Deus B, Gehrke P, Steinrücken HC (1980) The site of inhibition of the shikimate pathway by glyphosate. II. Interference of glyphosate with chorismate formation in vivo and in vitro. Plant Physiol 66:830–834CrossRefGoogle Scholar
  4. APHA (American Publication Health Association) (2005) Standard methods for the examination of water and wastewater, 21st edition Centennial Edition edn. APHA, American Water Works Association, Water Environmental Federation, Washington, DCGoogle Scholar
  5. Bagchi D, Bagchi M, Hassoun EA, Stohs SJ (1995) In vitro and in vivo generation of reactive oxygen species, DNA damage and lactate dehydrogenase leakage by selected pesticides. Toxicology 104:129–140CrossRefGoogle Scholar
  6. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–286CrossRefGoogle Scholar
  7. Bonnet JL, Bonnemoy F, Dusser M, Bohatier J (2007) Assessment of the potential toxicity of herbicides and their degradation products to nontarget cells using two microorganisms, the bacteria Vibrio fischeri and the ciliate Tetrahymena pyriformis. Environ Toxicol 22:78–91CrossRefGoogle Scholar
  8. Bonnineau C, Bonet B, Corcoll N, Guasch H (2011) Catalase in fluvial biofilms: a comparison between different extraction methods and example of application in a metal-polluted river. Ecotoxicology 20:293–303CrossRefGoogle Scholar
  9. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310CrossRefGoogle Scholar
  10. CASAFE (2010) Mercado Argentino de Productos Fitosanitarios 2009. Cámara de Sanidad Agropecuaria y Fertilizantes, Buenos AiresGoogle Scholar
  11. Chan K, Leung SC (1986) Effects of paraquat and glyphosate on growth, respiration, and enzyme activity of aquatic bacteria. Bull Environ Contam Toxicol 36:52–59CrossRefGoogle Scholar
  12. Contardo-Jara V, Klingelmann E, Wiegand C (2009) Bioaccumulation of glyphosate and its formulation roundup ultra in Lumbricus variegatus and its effects on biotransformation and antioxidant enzymes. Environ Pollut 157:57–63CrossRefGoogle Scholar
  13. Costa MJ, Monteiro DA, Oliveira-Neto AL, Rantin FT, Kalinin AL (2008) Oxidative stress biomarkers and heart function in bullfrog tadpoles exposed to Roundup originals. Ecotoxicology 17:153–163CrossRefGoogle Scholar
  14. Duke SO (1988) Glyphosate. In: Kearney PC, Kaufman DD (eds) Herbicides: chemistry degradation and mode of action. Marcel Dekker, New York, pp 1–58Google Scholar
  15. Feng JC, Thompson DG, Reynolds P (1990) Fate of glyphosate in a Canadian forest watershed. 1. Aquatic residues and off-target deposit assessment. J Agric Food Chem 38:1110–1118CrossRefGoogle Scholar
  16. Forlani G, Pavan M, Gramek M, Kafarski P, Lipok J (2008) Biochemical bases for a widespread tolerance of cyanobacteria to the phosphonate herbicide glyphosate. Plant Cell Physiol 49:443–456CrossRefGoogle Scholar
  17. Franz JE, Mao MK, Sikorski JA (1997) Glyphosate. A unique global herbicide. ACS monographs 189. American Chemical Society, Washington, DCGoogle Scholar
  18. Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup® herbicide. Rev Environ Contam Toxicol 167:35–120CrossRefGoogle Scholar
  19. Goldsborough LG, Brown DJ (1988) Effect of glyphosate (Roundup® formulation) on periphytic algal photosynthesis. Bull Environ Contam Toxicol 41:253–260CrossRefGoogle Scholar
  20. Goldsborough LG, Robinson GGC (1996) Periphyton patterns in wetlands. In: Stevenson RJ, Bothwell ML, Lowe RJ (eds) Algal ecology: freshwater benthic ecosystems. Academic Press, San Diego, pp 77–117Google Scholar
  21. Guasch H, Atli G, Bonet B, Corcoll N, Leira M, Serra A (2010) Discharge and the response of biofilms to metal exposure in Mediterranean rivers. Hydrobiologia 657:143–157CrossRefGoogle Scholar
  22. Källqvist T, Abdel-Hamid MI, Berge D (1994) Effects of agricultural pesticides on freshwater plankton communities in enclosures. Nor J Agric Sci 13(Supplement):133–152Google Scholar
  23. Lichtenthaler HK (1987) Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:349–382Google Scholar
  24. Lipok J, Studnik H, Gruyaert S (2010) The toxicity of Roundup® 360 SL formulation and its main constituents: glyphosate and isopropylamine towards non-target water photoautotrophs. Ecotoxicol Environ Saf 73:1681–1688CrossRefGoogle Scholar
  25. Lopretto EC, Tell G (1995) Ecosistemas de aguas continentales. Ediciones Sur, La PlataGoogle Scholar
  26. Lushchak OV, Kubrak OI, Storey JM, Storey KB, Lushchak VI (2009) Low toxic herbicide Roundup induces mild oxidative stress in goldfish tissues. Chemosphere 76:932–937CrossRefGoogle Scholar
  27. Mudge SM, Seguel CG (1999) Organic contamination of San Vicente Bay, Chile. Mar Pollut Bull 38:1011–1021CrossRefGoogle Scholar
  28. Paganelli A, Gnazzo V, Acosta H, López SL, Carrasco AE (2010) Glyphosate-based herbicides produce teratogenic effects on vertebrates by impairing retinoic acid signaling. Chem Res Toxicol 23:1586–1595CrossRefGoogle Scholar
  29. Pérez GL, Torremorell A, Mugni H, Rodríguez P, Vera MS, do Nascimento M, 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 17:2310–2322CrossRefGoogle Scholar
  30. Pesce S, Batisson I, Bardot C, Fajon C, Portelli C, Montuelle B, Bohatier J (2009) Response of spring and summer riverine microbial communities following glyphosate exposure. Ecotoxicol Environ Saf 72:1905–1912CrossRefGoogle Scholar
  31. Pessagno RC, Torres Sanchez RM, dos Santos AfonsoM (2008) Glyphosate behavior at soil and mineral-water interfaces. Environ Pollut 153:53–59CrossRefGoogle Scholar
  32. Peterson HG, Boutin C, Martin PA, Freemark KE, Ruecker NJ, Moody MJ (1994) Aquatic phytotoxicity of 23 pesticides applied at expected environmental concentrations. Aquat Toxicol 28:275–292CrossRefGoogle Scholar
  33. Porter KC, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948CrossRefGoogle Scholar
  34. Qian H, Chen W, Sun L, Jin Y, Liu W, Fu Z (2009) Inhibitory effects of paraquat on photosynthesis and the response to oxidative stress in Chlorella vulgaris. Ecotoxicology 18:537–543CrossRefGoogle Scholar
  35. Relyea RA (2005) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 15:618–627CrossRefGoogle Scholar
  36. Relyea R, Hoverman J (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1157–1171CrossRefGoogle Scholar
  37. Relyea RA, Schoeppner NM, Hoverman JT (2005) Pesticides and amphibians: the importance of assemblage context. Ecol Appl 5:1125–1134CrossRefGoogle Scholar
  38. Robertson EB, Bunting DL (1976) The acute toxicity of four herbicides to 0–4 hour nauplii of Cyclops vernalis Fisher (Copepoda, Cyclopoida). Bull Environ Contam Toxicol 16:682–688CrossRefGoogle Scholar
  39. Romero DM, Ríos de Molina MC, Juárez AB (2011) Oxidative stress induced by a commercial glyphosate formulation in a tolerant strain of Chlorella kessleri. Ecotoxicol Environ Saf 74:741–747CrossRefGoogle Scholar
  40. Ross C, Santiago-Vázquez L, Paul V (2006) Toxin release in response to oxidative stress and programmed cell death in the cyanobacterium Microcystis aeruginosa. Aquat Toxicol 78:66–73CrossRefGoogle Scholar
  41. Salisbury FB, Ross CW (1994) Fisiología vegetal. Grupo Editorial Iberoamérica, MéxicoGoogle Scholar
  42. Tsui MTK, Chu LM (2003) Aquatic toxicity of glyphosate-based formulations: comparison between different organisms and the effects of environmental factors. Chemosphere 52:1189–1197CrossRefGoogle Scholar
  43. Utermöhl H (1958) Zur vervollkommnung der quantitativen Phytoplankton Methodik. Mitt Int Ver Limnol 9:1–38Google Scholar
  44. Venrick EL (1978) How many cells to count? In: Sournia A (ed) Phytoplankton manual. UNESCO, Paris, pp 167–180Google Scholar
  45. Vera MS, Lagomarsino L, Sylvester M, Pérez G, Rodríguez P, Mugni H, Sinistro R, Ferraro M, Bonetto C, Zagarese H, Pizarro H (2010) New evidences of Roundup® (glyphosate formulation) impact on the periphyton and the water quality of freshwater ecosystems. Ecotoxicology 19:710–721CrossRefGoogle Scholar
  46. Walsh LP, McCormick C, Martin C, Stocco DM (2000) Roundup inhibits steroidogenesis by disrupting steroidogenic acute regulatory (StAR) protein expression. Environ Health Perspect 108:769–776CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • María Solange Vera
    • 1
    • 5
  • Eugenia Di Fiori
    • 1
    • 5
  • Leonardo Lagomarsino
    • 2
    • 5
  • Rodrigo Sinistro
    • 1
    • 5
  • Roberto Escaray
    • 2
    • 5
  • María Mercedes Iummato
    • 3
    • 5
  • Angela Juárez
    • 3
    • 4
  • María del Carmen Ríos de Molina
    • 3
    • 5
  • Guillermo Tell
    • 1
    • 5
  • Haydée Pizarro
    • 1
    • 5
  1. 1.Laboratorio de Limnología, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresCiudad de Buenos AiresArgentina
  2. 2.Instituto de Investigaciones Biotecnológicas, Instituto Tecnológico de Chascomús (IIB-INTECH)Chascomús, Buenos AiresArgentina
  3. 3.Laboratorio de Enzimología, Estrés Oxidativo y Metabolismo, Departamento de Química Biológica, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresCiudad de Buenos AiresArgentina
  4. 4.Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresCiudad de Buenos AiresArgentina
  5. 5.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Buenos AiresArgentina

Personalised recommendations