Water, Air, & Soil Pollution

, 225:2207 | Cite as

Glyphosate Sublethal Effects on the Population Dynamics of the Earthworm Eisenia fetida (Savigny, 1826)



Pesticides’ sublethal effects are not regularly taken into account when assessing agrochemical’s toxicity. With the objective of detecting chronic, sublethal effects of the widely used herbicide glyphosate, an experiment was performed using the earthworm Eisenia fetida as model organism. Earthworm adults were randomly assigned to three glyphosate treatments: control (no glyphosate), regular dose for perennial weeds, and double dose. Six E. fetida individuals were placed in each pot. Two random pots were taken weekly from each treatment and the number of adults, individual weight, number of cocoons, and presence and number of young earthworms were recorded. A matrix analysis was performed with the data. The matrix population model built showed that while the control population had a positive growth rate, both glyphosate treatments showed negative growth rates. The results suggest that under these sublethal effects, non-target populations are at risk of local extinction, underscoring the importance of this type of studies in agrochemical environmental risk assessment.


Ecotoxicology Chronic effects Earthworms Pesticides Agrochemicals 


  1. Abdullah, M., Singh, J., & Sohal, B. (2006). Behavioral hormoligosis in oviposition preference of Bemisia tabaci on cotton. Pesticide Biochemistry and Physiology, 84, 10–16.CrossRefGoogle Scholar
  2. Antón, F. A., Laborda, E., Laborda, P., & Ramos, E. (1993). Carbofuran acute toxicity to Eisenia foetida Savigny. Earthworms. Bulletin of Environmental Contamination and Toxicology, 50, 407–412.Google Scholar
  3. Billoir, E., Péry, A. R. R., & Charles, S. (2007). Integrating the lethal and sublethal effects of toxic compounds into the population dynamics of Daphnia magna: a combination of the DEBtox and matrix population models. Ecological Modelling, 203, 204–214.CrossRefGoogle Scholar
  4. Casabé, N., Piola, L., Fuchs, J., Oneto, M. L., Pamparato, L., Basack, S., Giménez, R., Massaro, R., Papa, J., & Kesten, E. (2007). Ecotoxicological assessment of the effects of glyphosate and chlorpyrifos in an Argentine soya field. Journal of Soils and Sediments, 7, 232–239.CrossRefGoogle Scholar
  5. Caswell, H. (2001). Matrix population models—construction, analysis, and interpretation. Sunderland: Sinauer Associates Inc.Google Scholar
  6. Charles, S., Billoir, E., Lopes, C., & Chaumot, A. (2009). Matrix population models as relevant modeling tools in ecotoxicology. Ecotoxicology Modeling 2, 261–298.Google Scholar
  7. Cox, C. (1995). Glyphosate, part 2: human exposure and ecological effects. Journal of Pesticide Reform, 15, 14–20.Google Scholar
  8. Edwards, C. A., & Bohlen, P. J. (1996). Biology of earthworms (3rd ed.). London: Chapman & Hall.Google Scholar
  9. Emlen, J. M., & Springman, K. R. (2007). Developing methods to assess and predict the population level effects of environmental contaminants. Integrated Environmental Assessment and Management 3, 157–165.Google Scholar
  10. FAO (2012). Internet resource URL: http://www.fao.org/agronoticias/agro-noticias/detalle/en/c/161730/ Last accessed: February 21, 2013.
  11. Farji-Brenner, A. G., de Torres Curth, M. I., Casanovas, P. V., & Naim, P. N. (2003). Consecuencias demográficas del sitio de nidificación en la hormiga cortadora de hojas Acromyrmex lobicornis: un enfoque utilizando modelos matriciales. Ecología Austral, 13, 183–194.Google Scholar
  12. Gimsing, A. L., Borggaard, O. K., Jacobsen, O. S., Aamand, J., & Sørensen, J. (2004). Chemical and microbiological soil characteristics controlling glyphosate mineralisation in Danish surface soils. Applied Soil Ecology, 27, 233–242.CrossRefGoogle Scholar
  13. Harper, E., Rittenhouse, T., & Semlitsch, R. (2008). Demographic consequences of terrestrial habitat loss for pool-breeding amphibians: predicting extinction risks associated with inadequate size of buffer zones. Conservation Biology, 22, 1205–1215.CrossRefGoogle Scholar
  14. ISO (International Organization for Standardization) (1993). 11268–1: Soil quality—effects of pollutants on earthworms (Eisenia fetida)—part 1: determination of acute toxicity using artificial soil substrate. Google Scholar
  15. ISO. (International Organization for Standardization) (1998). 11268–2. Soil quality—effects of pollutants on earthworms (Eisenia fetida)—part 2: determination of effects on reproduction. Google Scholar
  16. James, C. (2011). Global status of commercialized biotech/GM crops: 2011. ISAAA brief no. 43. Ithaca: ISAAA.Google Scholar
  17. Judas, M. (1988). The species. Oecologia, 76, 579.Google Scholar
  18. Lavelle, P., & Spain, A. (2001). Soil ecology. Dordrecht: Kluwer Academic Publishers.CrossRefGoogle Scholar
  19. Lavelle, P., Barois, J., Martin, A., Zaidi, Z., Schaefer, R. (1989). Management of earthworm populations in Agro-ecosystem. A possible way to maintain soil quality?. In M. Charholm & K. Bergstrom (eds.), Ecology of arable lands. Perspectives and Challenges Proceedings of an International Symposium, June 9-12, 1987, Swedish University of Agricultural Sciences, Uppsala, Sweden. Series: Developments in Plant and Soil Sciences, Vol. 39. Springer.(pp. 109–122)Google Scholar
  20. Lee, K. (1985). Earthworms. Their ecology and relationships with soils and land use. North Ryde: Academic. 411 pp.Google Scholar
  21. Leslie, P. H. (1945). On the use of matrices in certain population mathematics. Biometrika, 33, 184–212.CrossRefGoogle Scholar
  22. Leslie, P. H. (1948). Some further notes on the use of matrices in population mathematics. Biometrika, 35, 213–245.CrossRefGoogle Scholar
  23. Momo, F. & Falco, L. (2009). Biología y ecología del suelo.142-143. Imago Mundis (ed). Universidad Nacional de General Sarmiento, Buenos Aires, ArgentinaGoogle Scholar
  24. Morse, J. G. (1998). Agricultural implications of pesticide-induced hormesis of insects and mites. Human and Experimental Toxicology, 17, 266–269.CrossRefGoogle Scholar
  25. Neuhauser, E., & Callahan, C. (1990). Growth and reproduction of the earthworm Eisenia fetida exposed to sublethal concentrations of organic chemicals. Soil Biology and Biochemistry, 22, 175–179.CrossRefGoogle Scholar
  26. OECD. Organization for Economic Co-Operation and Development, Paris, France (2004). Guideline for testing of chemicals. 222, Earthworm reproduction test (Eisenia fetida/andrei).Google Scholar
  27. Pengue, W. A. (2000). Cultivos transgénicos ¿Hacia dónde vamos? Buenos Aires: Lugar Editorial.Google Scholar
  28. Pérez-Jones, A., Park, K. W., Colquhoun, J., Mallory-Smith, C., & Shaner, D. (2005). Identification of glyphosate-resistant ryegrass (Lolium multiflorum) in Oregon. Weed Science, 53, 775–779.CrossRefGoogle Scholar
  29. Piccolo, A., & Celano, G. (1994). Hydrogen bonding interactions between the herbicide glyphosate and water-soluble humic substances. Environmental Toxicology and Chemistry, 13, 1737–1741.CrossRefGoogle Scholar
  30. Qaim, M. (2005). Agricultural biotechnology adoption in developing countries. American Journal of Agricultural Economics, 87, 1317–1324.CrossRefGoogle Scholar
  31. Reinecke, A. J., & Venter, J. M. (1987). Moisture preferences, growth and reproduction of the compost worm Eisenia fetida (Oligochaeta). Biology and Fertility of Soils, 3, 135–141.Google Scholar
  32. Reynolds, J. W. (1996). Earthworms biology and ecology (Course manual. Pp 40–139. U.N. Córdoba, Facultad de Cs). Córdoba Argentina: Exactas.Google Scholar
  33. Sprankle, P., Meggitt, W., & Penner, D. (1975). Rapid inactivation of glyphosate in the soil. Weed Science, 23, 224–228.Google Scholar
  34. Spurgeon, D., Svendsen, C., Kille, P., Morgan, A., & Weeks, J. (2004). Responses of earthworms (Lumbricus rubellus) to copper and cadmium as determined by measurement of juvenile traits in a specially designed test system. Ecotoxicology and Environmental Safety, 57, 54–64.CrossRefGoogle Scholar
  35. Trigo, E., & Cap, E. (2003). The impact of the introduction of transgenic crops in Argentinean agriculture. AgBioforum, 6, 87–94.Google Scholar
  36. USDA. (2010). Keys to soil taxonomy. United States Department of Agriculture. Natural Resources Conservation Center. Eleventh Edition, 338 pp.Google Scholar
  37. U S Environmental Protection Agency (1999). Technical fact sheets on: glyphosate. National primary drinking water regulations. Google Scholar
  38. Venkateswara Roa, J., Sutya Pavan, Y., & Madhavendra, S. (2003). Toxic effects of chlorpyrifos on morphology and acetylcholinesterase activity in the earthworm, Eisenia foetida. Ecotoxicology and Environmental Safety, 54, 296–301.CrossRefGoogle Scholar
  39. Venter, J. M., & Reinecke, A. J. (1988). The life-cycle of the compost worm Eisenia fetida (Oligochaeta). South African Journal of Zoology, 23, 161–165.Google Scholar
  40. Viswanathan, R. (1992). Study of pesticides impact on earthworms using closed laboratory model ecosystem. Greig-Smith, Becker, Edwards y Heinnbach (Eds.). Ecotoxicology of earthworms.Andover, Hampshire: Intercept. pp 269 Google Scholar
  41. Wakelin, A. M., Lorraine-Colwill, D. F., & Preston, C. (2004). Glyphosate resistance in four different populations of Lolium rigidum is associated with reduced translocation of glyphosate to meristematic zones. Weed Research, 44, 453–459.CrossRefGoogle Scholar
  42. Welten, R. (2000). Ecotoxicity of contaminated suspended solids for filter feeders (Daphnia magna). Archives of Environmental Contamination and Toxicology, 39, 315–323.CrossRefGoogle Scholar
  43. Zang, Y., Zhong, Y., Luo, Y., & Kong, Z. (2000). Genotoxicity of two novel pesticides for the earthworm, Eisenia fetida. Environmental Pollution, 108, 271–278.CrossRefGoogle Scholar
  44. Zoran, M. J., Heppner, T. J., & Drewes, C. D. (1986). Teratogenic effect of the fungicide Benomyl on posterior segmental regeneration in the earthworms Eisenia fetida. Pesticide Science, 17, 641–652.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Marina Santadino
    • 1
  • Carlos Coviella
    • 1
  • Fernando Momo
    • 1
    • 2
  1. 1.Programa de Ecología Terrestre, Departamento de Ciencias Básicas e Instituto de Ecología y Desarrollo SustentableUniversidad Nacional de LujánLujánArgentina
  2. 2.Instituto de CienciasUniversidad Nacional de General SarmientoBuenos AiresArgentina

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