Skip to main content

Low Concentrations of Glyphosate-Based Herbicide Affects the Development of Chironomus xanthus

Abstract

Glyphosate is an herbicide commonly used worldwide for weed control and generally applied as part of a formulated product, such as Roundup. Contamination of surface water by glyphosate-based herbicides can cause deleterious effects in organisms, mainly in aquatic systems near to intensive agricultural areas (e.g., transgenic soybean crops). Given the lack of toxicological information concerning effects of glyphosate-based herbicides on tropical aquatic ecosystems, we aimed to evaluate the lethal and sub-lethal effects of Roundup Original® on the dipteran Chironomus xanthus. The endpoints evaluated included survival, growth, and emergence. The results showed that the 48 h LC50 for glyphosate to C. xanthus was 251.5 mg a.e./L. Larval growth of C. xanthus was reduced under glyphosate exposure (LOEC for body length = 12.06 mg/L; LOEC for head capsule width = 0.49 mg/L). No effects were observed in terms of cumulative percentage of imagoes emergence. However, low concentrations of glyphosate caused delayed emergence of females (at 1.53 mg/L) and induced fast emergence of males (at 0.49 mg/L), compared to control treatment. The deleterious effects of environmental relevant concentrations of glyphosate (0.7 mg/L) observed in terms of C. xanthus growth and development suggest that glyphosate-based herbicides can have negative consequences for aquatic non-target invertebrates such as Chironomus. Multigerational assays are needed to assess the long term effects of glyphosate on C. xanthus populations. Finally, our study adds ecotoxicological data on the effects of glyphosate-based herbicides on tropical freshwater invertebrates.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Annett, R., Habibi, H. R., & Hontela, A. (2014). Impact of glyphosate and glyphosate-based herbicides on the freshwater environment. Journal of Applied Toxicology, 34(5), 458–479.

    CAS  Article  Google Scholar 

  • ASTM. (1980). Standard Practice for Conducting Acute Toxicity Tests with Fishes, Macroinvertebrates and Amphibians. Philadelphia: American Standards for Testing and Materials.

  • Baker, L. F., Mudge, J. F., Houlahan, J. E., Thompson, D. G., & Kidd, K. A. (2014). The direct and indirect effects of a glyphosate-based herbicide and nutrients on Chironomidae (Diptera) emerging from small wetlands. Environmental Toxicology and Chemistry, 33(9), 2076–2085.

    CAS  Article  Google Scholar 

  • Bretaud, S., Toutant, J. P., & Saglio, P. (2000). Effects of carbofuran, diuron, and nicosulfuron on acetylcholinesterase activity in goldfish (Carassius auratus). Ecotoxicology and Environmental Safety, 47(2), 117–124.

    CAS  Article  Google Scholar 

  • Brito, I. P., Tropaldi, L., Carbonari, C. A., & Velini, E. D. (2017). Hormetic effects of glyphosate on plants. Pest Management Science. Accepted article.:https://doi.org/10.1002/ps.4523.

  • Buhl, K. J., & Faerber, N. L. (1989). Acute toxicity of selected herbicides and surfactants to larvae of the midge Chironomus riparius. Archives of Environmental Contamination and Toxicology, 18(4), 530–536.

    CAS  Article  Google Scholar 

  • Cattani, D., Cavalli, V. L. D. L. O., Rieg, C. E. H., Domingues, J. T., Dal-Cim, T., Tasca, C. I., et al. (2014). Mechanisms underlying the neurotoxicity induced by glyphosate-based herbicide in immature rat hippocampus: involvement of glutamate excitotoxicity. Toxicology, 320, 34–45.

    CAS  Article  Google Scholar 

  • Cavalli, V. L. D. L. O., Cattani, D., Rieg, C. E. H., Pierozan, P., Zanatta, L., Parisotto, E. B., et al. (2013). Roundup disrupts male reproductive functions by triggering calcium-mediated cell death in rat testis and Sertoli cells. Free Radical Biology and Medicine, 65, 335–346.

    CAS  Article  Google Scholar 

  • Costa, J. B. (2007). Avaliação ecotoxicológica de efluente de tratamento secundário de esgoto sanitário após desinfecção com ácido peracético, cloro, ozônio e radiação ultravioleta. São Carlos, Brazil, 180 p (Doctoral dissertation, Tese de Doutorado. Escola de Engenharia de São Carlos. Universidade de São Paulo).

  • Coupe, R. H., Kalkhoff, S. J., Capel, P. D., & Gregoire, C. (2012). Fate and transport of glyphosate and aminomethylphosphonic acid in surface waters of agricultural basins. Pest Management Science, 68(1), 16–30.

    CAS  Article  Google Scholar 

  • Cuhra, M., Traavik, T., & Bøhn, T. (2013). Clone-and age-dependent toxicity of a glyphosate commercial formulation and its active ingredient in Daphnia magna. Ecotoxicology, 22(2), 251–262.

    CAS  Article  Google Scholar 

  • Devine, J. A., & Vanni, M. J. (2002). Spatial and seasonal variation in nutrient excretion by benthic invertebrates in a eutrophic reservoir. Freshwater Biology, 47(6), 1107–1121.

    Article  Google Scholar 

  • Dinehart, S. K., Smith, L. M., McMurry, S. T., Smith, P. N., Anderson, T. A., & Haukos, D. A. (2010). Acute and chronic toxicity of Roundup Weathermax® and Ignite® 280 SL to larval Spea multiplicata and S. bombifrons from the Southern High Plains, USA. Environmental Pollution, 158(8), 2610–2617.

    CAS  Article  Google Scholar 

  • Domingues, I., Guilhermino, L., Soares, A. M., & Nogueira, A. J. (2007). Assessing dimethoate contamination in temperate and tropical climates: Potential use of biomarkers in bioassays with two chironomid species. Chemosphere, 69(1), 145–154.

    CAS  Article  Google Scholar 

  • Duke, S. O., & Powles, S. B. (2008). Glyphosate: a once-in-a-century herbicide. Pest Management Science, 64(4), 319–325.

    CAS  Article  Google Scholar 

  • Folmar, L. C., Sanders, H. O., & Julin, A. M. (1979). Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrates. Archives of Environmental Contamination and Toxicology, 8(3), 269–278.

    CAS  Article  Google Scholar 

  • Frontera, J. L., Vatnick, I., Chaulet, A., & Rodríguez, E. M. (2011). Effects of glyphosate and polyoxyethylenamine on growth and energetic reserves in the freshwater crayfish Cherax quadricarinatus (Decapoda, Parastacidae). Archives of Environmental Contamination and Toxicology, 61(4), 590–598.

    CAS  Article  Google Scholar 

  • Giesy, J. P., Dobson, S., & Solomon, K. R. (2000). Ecotoxicological risk assessment for Roundup® herbicide. In Reviews of environmental contamination and toxicology (pp. 35–120). New York: Springer.

    Chapter  Google Scholar 

  • Glusczak, L., dos Santos Miron, D., Crestani, M., da Fonseca, M. B., de Araújo Pedron, F., Duarte, M. F., & Vieira, V. L. P. (2006). Effect of glyphosate herbicide on acetylcholinesterase activity and metabolic and hematological parameters in piava (Leporinus obtusidens). Ecotoxicology and Environmental Safety, 65(2), 237–241.

    CAS  Article  Google Scholar 

  • Glusczak, L., dos Santos Miron, D., Moraes, B. S., Simões, R. R., Schetinger, M. R. C., Morsch, V. M., & Loro, V. L. (2007). Acute effects of glyphosate herbicide on metabolic and enzymatic parameters of silver catfish (Rhamdia quelen). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 146(4), 519–524.

    Google Scholar 

  • Goedkoop, W., Spann, N., & Åkerblom, N. (2010). Sublethal and sex-specific cypermethrin effects in toxicity tests with the midge Chironomus riparius Meigen. Ecotoxicology, 19(7), 1201–1208.

    CAS  Article  Google Scholar 

  • Herbert, L. T., Vásquez, D. E., Arenas, A., & Farina, W. M. (2014). Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour. Journal of Experimental Biology, 217, 3457–3464.

    Article  Google Scholar 

  • Howe, C. M., Berrill, M., Pauli, B. D., Helbing, C. C., Werry, K., & Veldhoen, N. (2004). Toxicity of glyphosate-based pesticides to four North American frog species. Environmental Toxicology and Chemistry, 23(8), 1928–1938.

    CAS  Article  Google Scholar 

  • Kumar, M., Gupta, G. P., & Rajam, M. V. (2009). Silencing of acetylcholinesterase gene of Helicoverpa armigera by siRNA affects larval growth and its life cycle. Journal of Insect Physiology, 55(3), 273–278.

    CAS  Article  Google Scholar 

  • Moreira, S. S., & Zuanon, J. (2002). Dieta de Retroculus lapidifer (Perciformes: Cichlidae), um peixe reofílico do rio Araguaia, estado do Tocantins, Brasil. Acta Amazonica, 32(4), 691–705.

    Google Scholar 

  • Novelli, A., Vieira, B. H., Cordeiro, D., Cappelini, L. T. D., Vieira, E. M., & Espíndola, E. L. G. (2012). Lethal effects of abamectin on the aquatic organisms Daphnia similis, Chironomus xanthus and Danio rerio. Chemosphere, 86(1), 36–40.

    CAS  Article  Google Scholar 

  • OECD (2004). Test no. 219: sediment–water chironomid toxicity using spiked water. OECD Guidel Test Chem. OECD Publishing.

  • OECD (2011). Test no. 235: Chironomus sp., acute immobilisation test. OECD Guidel Test Chem. OECD Publishing.

  • Peruzzo, P. J., Porta, A. A., & Ronco, A. E. (2008). Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environmental Pollution, 156(1), 61–66.

    CAS  Article  Google Scholar 

  • Pestana, J. L., Loureiro, S., Baird, D. J., & Soares, A. M. (2009). Fear and loathing in the benthos: responses of aquatic insect larvae to the pesticide imidacloprid in the presence of chemical signals of predation risk. Aquatic Toxicology, 93(2), 138–149.

    CAS  Article  Google Scholar 

  • Relyea, R. A. (2012). New effects of Roundup on amphibians: Predators reduce herbicide mortality; herbicides induce antipredator morphology. Ecological Applications, 22(2), 634–647.

    Article  Google Scholar 

  • Rodrigues, A. C., Gravato, C., Quintaneiro, C., Golovko, O., Žlábek, V., Barata, C., et al. (2015). Life history and biochemical effects of chlorantraniliprole on Chironomus riparius. Science of the Total Environment, 508, 506–513.

    CAS  Article  Google Scholar 

  • Rodrigues, L. B., de Oliveira, R., Abe, F. R., Brito, L. B., Moura, D. S., Valadares, M. C., et al. (2017). Ecotoxicological assessment of glyphosate-based herbicides: effects on different organisms. Environmental Toxicology and Chemistry, 36(7), 1755–1763.

  • Roy, N. M., Carneiro, B., & Ochs, J. (2016). Glyphosate induces neurotoxicity in zebrafish. Environmental Toxicology and Pharmacology, 42, 45–54.

    CAS  Article  Google Scholar 

  • Sandahl, J. F., Baldwin, D. H., Jenkins, J. J., & Scholz, N. L. (2005). Comparative thresholds for acetylcholinesterase inhibition and behavioral impairment in coho salmon exposed to chlorpyrifos. Environmental Toxicology and Chemistry, 24(1), 136–145.

    CAS  Article  Google Scholar 

  • Saraiva, A. S., Sarmento, R. A., Pedro-Neto, M., Teodoro, A. V., Erasmo, E. A. L., Belchior, D. C. V., & de Azevedo, E. B. (2016). Glyphosate sub-lethal toxicity to non-target organisms occurring in Jatropha curcas plantations in Brazil. Experimental and Applied Acarology, 70(2), 179–187.

    Article  Google Scholar 

  • Saraiva, A. S., Sarmento, R. A., Rodrigues, A. C., Campos, D., Fedorova, G., Žlábek, V., et al. (2017). Assessment of thiamethoxam toxicity to Chironomus riparius. Ecotoxicology and Environmental Safety, 137, 240–246.

    CAS  Article  Google Scholar 

  • Sildanchandra, W., & Crane, M. (2000). Influence of sexual dimorphism in Chironomus riparius Meigen on toxic effects of cadmium. Environmental Toxicology and Chemistry, 19(9), 2309–2313.

    CAS  Article  Google Scholar 

  • Solomon, K. R., & Thompson, D. G. (2003). Ecological risk assessment for aquatic organisms from over-water uses of glyphosate. Journal of Toxicology and Environmental Health - Part B-Crit. Rev., 6(3), 289–324.

    CAS  Article  Google Scholar 

  • Sprague, J. B., & Fogels, A. (1977) Watch the Y in bioassay. Proceedings of the 3rd aquatic toxicity workshop, Halifax, Nova Scotia Nov. 2–3, 1976 Environment Canada, Tech. Report No. EPS-5AR-77-1, p. 107–18.

  • Taenzler, V., Bruns, E., Dorgerloh, M., Pfeifle, V., & Weltje, L. (2007). Chironomids: suitable test organisms for risk assessment investigations on the potential endocrine disrupting properties of pesticides. Ecotoxicology, 16(1), 221–230.

    CAS  Article  Google Scholar 

  • Tomlin, C. D. S. (2006). The pesticides manual: a world compendium. British Crop Protection Council, 14, 351.

    Google Scholar 

  • Tsui, M. T., & Chu, L. M. (2004). Comparative toxicity of glyphosate-based herbicides: aqueous and sediment porewater exposures. Archives of Environmental Contamination and Toxicology, 46(3), 316–323.

    CAS  Article  Google Scholar 

  • Vencill, W. K. (2002). Herbicide Handbook. 8th ed. W. K. Vencill, ed. Lawrence, KS: Weed Science Society of America. 493p.

  • Wagner, N., Reichenbecher, W., Teichmann, H., Tappeser, B., & Lötters, S. (2013). Questions concerning the potential impact of glyphosate-based herbicides on amphibians. Environmental Toxicology and Chemistry, 32(8), 1688–1700.

    CAS  Article  Google Scholar 

Download references

Funding Information

This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil (Projects: A058_2013; PROCAD 2013—88881.068483/2014-01). We also thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brazil—Projects: 401201/2014-7 and 304178/2015-2; and young Talent Fellowship (314907/2014-9) and the Universidade Federal do Tocantins for financial support. Renato A. Sarmento received scholarship from CNPq (Produtividade em Pesquisa—Project: 304178/2015-2). João Pestana aknowledges the Portuguese Foundation for Science and Technology (FCT) for the research contracts under the program “Investigador FCT” (IF/01420/2015 ). The authors thank the Instituto Federal de Educação, Ciência e Tecnologia Goiano - campus Campos Belos for support and partnership.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Renato Almeida Sarmento.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ferreira-Junior, D.F., Sarmento, R.A., Saraiva, A.d.S. et al. Low Concentrations of Glyphosate-Based Herbicide Affects the Development of Chironomus xanthus . Water Air Soil Pollut 228, 390 (2017). https://doi.org/10.1007/s11270-017-3536-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-017-3536-9

Keywords

  • Roundup
  • Non-target organisms
  • Chironomidae
  • Survival
  • Life history