Skip to main content
SpringerLink
Log in

Screening effects of metsulfuron-methyl to collembolans and earthworms: the role of adjuvant addition on ecotoxicity

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Metsulfuron-methyl is a common active ingredient recommended for use in pre- and post-emergence control of annual grasses and broadleaf weeds in crops, usually applied with mineral oil as adjuvant to enhance its efficiency. Despite the increasing use of this herbicide, there are no information on its ecotoxicity effects to soil fauna. Avoidance and lethality tests were performed with earthworms and collembolans using tropical artificial soil contaminated with formulated products Ally® (600 g L−1 metsulfuron-methyl) and Assist® (756 g L−1 mineral oil) as adjuvant. Lethality test with earthworms showed no difference when tested with or without adjuvant. When Ally® was tested alone, it caused avoidance behavior only at high concentrations (5000 and 10,000 times field predicted dose). However, Assist® addition changed the response of soil invertebrates increasing the avoidance even at field predicted doses. The toxicity of the adjuvant was confirmed in tests exposing collembolans and earthworms to Assist® alone resulting in avoidance behavior. The results clearly show that the addition of mineral oil enhanced the ecotoxicity of metsulfuron-methyl. This study provides an important contribution to the knowledge on the toxicity of metsulfuron-methyl and indicates that adjuvants should be considered in risk assessment of pesticides, considering that under field conditions, these products are applied together.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Amorim MJB, Pereira C, Menezes-Oliveira VB, Campos B, Soares AMVM, Loureiro S (2012) Assessing single and joint effects of chemicals on the survival and reproduction of Folsomia candida (Collembola) in soil. Environ Pollut 160:145–152

    Article  CAS  Google Scholar 

  • Brami C, Glover AR, Butt KR, Lowe CN (2017) Effects of silver nanoparticles on survival, biomass change and avoidance behaviour of the endogeic earthworm Allolobophora chlorotica. Ecotoxicol Environ Saf 141:64–69. dx.doi.org. https://doi.org/10.1016/j.ecoenv.2017.03.015

    Article  CAS  Google Scholar 

  • Bretaud S, Toutant J-P, Saglio P (2000) Effects of carbofuran,diuron and nicosulfuron on acetylcholinesterase activity in goldfish (Carassius auratus). Ecotoxicol Environ Safe 47:117–124

    Article  CAS  Google Scholar 

  • Buch AC, Brown GG, Niva CC, Sautter KD, Sousa JP (2013) Toxicity of three pesticides commonly used in Brazil to Pontoscolex corethrurus (Müller, 1857) and Eisenia andrei (Bouché 1972). Appl Soil Ecol 69:32–38. dx.doi.org. https://doi.org/10.1016/j.apsoil.2012.12.011

    Article  Google Scholar 

  • Caquet T, Deydier-Stephan L, Lacroix G, Rouzic BL, Lescher-Moutoué F (2005) Effects of fomesafen, alone and in combination with an adjuvant, on plankton communities in freshwater outdoor pond mesocosms. Environ Toxicol Chem 24:1116–1124

    Article  CAS  Google Scholar 

  • Caselli F, Gastaldi L, Gambi N, Fabbri E (2006) In vitro characterization of cholinesterases in the earthworm Eisenia andrei. Comp Biochem Physiol 143:416–421

    Google Scholar 

  • Castro MC, Bedmar MG, Monterubbianesi MG, Peretti A, Barassi CA (2002) Determination of chlorimuron and metsulfuron residues in two soils of Argentina using a rapid seed-bioassay. J Environ Biol 23:353–358

    CAS  Google Scholar 

  • Chelinho S, Domene X, Andrés P, Natal Da Luz T, Norte C, Rufino C, Lopes I, Cachada A, Espindola E, Riberiro R, Duarte AC, Sousa JP (2014) Soil microarthropod community testing: a new approach to increase the ecological relevance of effect data for pesticide risk assessment. Appl Soil Ecol 83:200–209

    Article  Google Scholar 

  • Coutellec MA, Delous G, Cravedi JP, Lagadic L (2008) Effects of the mixture of diquat and a nonylphenol polyethoxylate adjuvant on fecundity and progeny early performances of the pond snail Lymnaea stagnalis in laboratory bio-assays and microcosms. Chemosphere 73(3):326–336. https://doi.org/10.1016/j.chemosphere.2008.05.068

    Article  CAS  Google Scholar 

  • D'Annibale A, Sechi V, Larsen T, Christensen S, Krogh PH, Eriksen J (2017) Does introduction of clover in an agricultural grassland affect the food base and functional diversity of Collembola? Soil Biol Biochem 112:165–176. https://doi.org/10.1016/j.soilbio.2017.05.010

    Article  CAS  Google Scholar 

  • Dignac MF, Derrien D, Barré P, Barot S, Cécillon L, Chenu C, Chevallier T, Freschet GT, Garnier P, Guenet B, Hedde M, Klumpp K, Lashermes G, Maron PA, Nunan N, Roumet C, Basiledoelsch I (2017) Increasing soil carbon storage: mechanisms, effects of agricultural practices and proxies. A review. Agron Sustain Dev 37:14

    Article  CAS  Google Scholar 

  • Domene X, Colón J, Uras MV, Izquierdo R, Avila A, Alcaniz JM (2010) Role of soil properties in sewage sludge toxicity to soil collembolans. Soil Biol Biochem 42:1982–1990

    Article  CAS  Google Scholar 

  • EFSA – European Food Safety Authority (2007) Opinion of the scientific panel on Plant Prot products and their residues on a request from the commission related to the revision of annexes II and III to council Directive 91/414/EEC concerning the placing of Plant Prot products on the market – ecotoxicological studies. EFSA J 461:1–44

    Google Scholar 

  • EFSA – European Food Safety Authority (2017) Scientific Opinion on the state of the science on pesticide risk assessment for amphibians and reptiles. https://www.efsa.europa.eu/sites/default/files/consultation/170410.pdf. Assessed 12 Nov 2017

  • EPPO European Plant Protection Organization (2003) EPPO Standars. Environmental Risk Assessment scheme for plant protection produtcts. EPPO Bull 33:195–208

    Article  Google Scholar 

  • Fernandez-Vega C, Sancho E, Ferrando MD, Andreu E (2002) Thiobencarb-induced changes in acetylcholinesterase activity of the fish Anguilla anguilla. Pestic Biochem Physiol 72:55–63

    Article  CAS  Google Scholar 

  • Fountain MT, Hopkin SP (2001) Continuous monitoring of Folsomia candida (Insecta: Collembola) in a metal exposure test. Ecotox Environ Safe 48:275–286

    Article  CAS  Google Scholar 

  • García M (2004) Effects of pesticides on soil fauna: development of ecotoxicological test methods for tropical regions. Ecol Dev Ser 19:291

    Google Scholar 

  • Ghobadi M, Yamini Y, Ebrahimpour B (2015) Extraction and determination of sulfonylurea herbicides in water and soil samples by using ultrasound-assisted surfactant-enhanced emulsification microextraction and analysis by high-performance liquid chromatography. Ecotoxicol Environ Safe 112:68–73

    Article  CAS  Google Scholar 

  • He Y, Shen D, Fang C, He R, Zhu Y (2006) Effects of metsulfuron-methyl on the microbial population and enzyme activities in wheat rhizosphere soil. J Environ Sci Health 41:269–284

    Article  CAS  Google Scholar 

  • Hopkin SP (1997) Biology of the springtails (Insecta: Collembola). Oxford University Press, Oxford

    Google Scholar 

  • IBAMA (1996) Portaria Normativa IBAMA No 84, de 15 de outubro de 1996 https://servicosibamagovbr/ctf/manual/html/Portaria_84pdf Assessed 12 Nov 2017

  • IBAMA (2016) Agrochemicals and similars statistical consumption (2000-2014). http://ibamagovbr/phocadownload/qualidadeambiental/relatorios/2014/grafico_historico_comercializacao_2000_2014pdf Assessed 12 Nov 2017

  • ISO - International Organization For Standardization (2008) ISO 17512–1: Soil quality – Avoidance test for determinig the quality of soils and effects on behaviour – Part 1: Test with earthworms (Eisenia fetida and Eisenia andrei). ISO, Geneva

  • ISO - International Organization For Standardization (2011) ISO 17512–2: Soil quality - Avoidance test for determining the qualite of soils and effects of chemicals on behavior - Part 2: Test with collembolans (Folsomia candida). ISO, Geneva

  • ISO - International Organization For Standardization (2012) ISO 11268–1: Effects of pollutants on earthworms - Part 1: Determination of acute toxicity to Eisenia fetida/Eisenia andrei. ISO, Geneva

  • Jansch S, Frampton GK, Rombke J, Van den Brink PJ, Scott-Fordsmand JJ (2006) Effects of pesticides on soil invertebrates in model ecosystem and field studies: a review and comparison with laboratory toxicity data. Environ Toxicol Chem 25:2490–2501

    Article  Google Scholar 

  • Lavelle P (2014) Earthworms as ecosystem engineers. Encyclopedia of Agrophysics pp 233–235. DOI: https://doi.org/10.1007/978-90-481-3585-1_45

  • Lowe CN, Butt KR, Cheynier KY-M (2016) Assessment of avoidance behaviour by earthworms (Lumbricus rubellus and Octolasion cyaneum) in linear pollution gradients. Ecotoxicol Environ Saf 124:324–328. dx.doi.org. https://doi.org/10.1016/j.ecoenv.2015.11.015

    Article  CAS  Google Scholar 

  • Ma JY, Lin FC, Zhang RZ, Yu WW, Lu NH (2004) Differential sensitivity of two green algae, Scenedesmus quadricauda and Chlorella vulgaris, to 14 pesti-cide adjuvants. Ecotox Environ Saf 58:61–67. https://doi.org/10.1016/j.ecoenv.2003.08.023

    Article  CAS  Google Scholar 

  • Ma J, Qin W, Lu N, Wang P, Huang C, Xu R (2005) Differential sensitivity of three cyanobacteria (Anabaena flos-aquae, Microcystis flos-aquae and Mirocystis aeruginosa) to 10 pesticide adjuvants. Bull Environ Contam Toxicol 75(5):873–881. https://doi.org/10.1007/s00128-005-0831-8

    Article  CAS  Google Scholar 

  • Marques C, Pereira R, Gonçalves F (2009) Using earthworm avoidance behaviour to assess the toxicity of formulated herbicides and their active ingredients on natural soils. J Soils Sediments 9:137–147

    Article  CAS  Google Scholar 

  • Martins C, Natal-da-Luz T, Sousa JP, Goncalves MJ, Salgueiro L, Canhoto C (2013) Effects of essential oils from Eucalyptus globulus leaves on soil organisms involved in leaf degradation. PLoS One 8(4):e61233. https://doi.org/10.1371/journal.pone.0061233

    Article  CAS  Google Scholar 

  • Miron D, Crestani M, Schetinger RM, Morsch MV, Baldisserotto B, Tierno AM, Moraes G, Vieira PLV (2005) Effects of the herbicides clomazone, quinclorac, and metsulfuron methyl on acetylcholinesterase activity in the silver catfish (Rhamdia quelen) (Heptapteridae). Ecotoxicol Environ Safe 61:398–403

    Article  CAS  Google Scholar 

  • Natal da Luz T, Ribeiro R, Sousa JP (2004) Avoidance tests with collembola and earthworms as early screening tools for site-specific assessment of polluted soils. Environ Toxicol Chem 23:2188–2193

    Article  Google Scholar 

  • Nelemans B, Wijngaarden RV, Roessink I, Arts GH (2017) Effects of the herbicide metsulfuron-methyl on a plant community, including seed germination success in the F1 generation. Front Environ Sci, 5:10. https://doi.org/10.3389/fenvs.2017.00010

  • Niva CC, Niemeyer JC, Júnior FMRDS, Nunes MET, De Sousa DL, Aragão CWS, Sautter KD, Espindola EG, Sousa JP, Römbke J (2016) Soil ecotoxicology in Brazil is taking its course. Environ Sci Pollut Res 23:11363–11378. https://doi.org/10.1007/s11356-016-6597-1

    Article  CAS  Google Scholar 

  • Nobels I, Spanoghe P, Haesaert G, Robbens J, Blust R (2011) Toxicity ranking and toxic mode of action evaluation of commonly used agricultural adjuvants on the basis of bacterial gene expression profiles. PLoS One 6(11):e24139. https://doi.org/10.1371/journal.pone.0024139

    Article  CAS  Google Scholar 

  • OECD - The Organisation for Economic Co-Operation and Development (2016) Test No. 226: Predatory mite (Hypoaspis (Geolaelaps) aculeifer) reproduction test in soil. OECD Guidelines for Testing of Chemicals. OECD, Paris

  • Oliveira RS Jr,. Mecanismos de Ação de Herbicidas (2011) In Oliveira Jr, RS, Biologia e Manejo de Plantas Daninhas, 1ed, Omnipax, Curitiba. http://omnipax.com.br/livros/2011/BMPD/BMPDcap7.pdf. Assessed in 12 Nov 2017

  • Pelosi C, Barot S, Capowiez Y, Hedde M, Van den Bulcke F (2014) Pesticides and earthworms: a review. Agron Sustain Dev 34:199–228

    Article  CAS  Google Scholar 

  • Potapov AA, Semenina EE, Korotkevich AY, Kuznetsova NA, Tiunov AV (2016) Connecting taxonomy and ecology: trophic niches of collembolans as related to taxonomic identity and life forms. Soil Biol Biochem 101:20–31. https://doi.org/10.1016/j.soilbio.2016.07.002

    Article  CAS  Google Scholar 

  • Rastetter N, Gerhardt A (2018) Continuous monitoring of avoidance behaviour with the earthworm Eisenia fetida. J Soils Sediments 18: 957. https://doi.org/10.1007/s11368-017-1791-4

  • Rebelo RM, Vasconcelos RA, Buys BDMC, Rezende JA, Moraes KOC, Oliveira RP (2010) Pesticides and related products marketed in 2009 in Brazil: an environmental approach. Technical Report. IBAMA, Brasília, DF

  • Reinecke SA, Reinecke AJ (2007) The impact of organophosphate pesticides in orchards on earthworms in the Western Cape, South Africa. Ecotoxicol Environ Safe 66:244–251

    Article  CAS  Google Scholar 

  • Römbke J, Schmelz RM, Pélosi C (2017) Effects of organic pesticides on Enchytraeids (Oligochaeta) in agroecosystems: laboratory and higher-tier tests. Front Environ Sci 5:1–20

    Article  Google Scholar 

  • Singh C, Singh K (2015) Toxic effect of herbicide 2,4-D on the earthworm Eutyphoeus waltoni Michaelsen. Environ Process 2:251–260

    Article  CAS  Google Scholar 

  • Surgan M, Condon M, Cox C (2010) Pesticide risk indicators: unidentified inert ingredients compromise their integrity and utility. Environ Manag 45:834–841

    Article  Google Scholar 

  • Wang Y, An X, Shen W, Chen L, Jiang J, Wang Q, Cai L (2016) Individual and combined toxic effects of herbicide atrazine and three insecticides on the earthworm, Eisenia fetida. Ecotoxicol 25:991–999

    Article  CAS  Google Scholar 

  • Xie HQ, Xu T, Chen Y, Li Y, Xia Y, Xu SL, Wang L, Tsim KWK, Zhao B (2016) New perspectives for multi-level regulations of neuronal acetylcholinesterase by dioxins. Chem Biol Interact 259:286–290

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Fernanda Benedet de Santo and Júlia Carina Niemeyer contributed equally to this work.

Authors and Affiliations

  1. Programa de Pós-Graduação em Ecossistemas Agrícolas e Naturais (PPGEAN), Federal University of Santa Catarina, Rodovia Ulysses Gaboardi, Km 3, Campus of Curitibanos, Curitibanos, 89520-000, Brazil

    Fernanda Benedet de Santo, Cesar Augusto Marchioro & Júlia Carina Niemeyer

  2. Federal University of Santa Catarina, Campus of Curitibanos, Curitibanos, 89520-000, Brazil

    Guilherme Alves Ramos, Altair Maçaneiro Ricardo Filho, Cesar Augusto Marchioro & Júlia Carina Niemeyer

Authors
  1. Fernanda Benedet de Santo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guilherme Alves Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Altair Maçaneiro Ricardo Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cesar Augusto Marchioro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Júlia Carina Niemeyer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernanda Benedet de Santo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights and informed consent

This article does not contain any studies with human participants or animals (vertebrates) performed by any of the authors.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Santo, F.B., Ramos, G.A., Ricardo Filho, A.M. et al. Screening effects of metsulfuron-methyl to collembolans and earthworms: the role of adjuvant addition on ecotoxicity. Environ Sci Pollut Res 25, 24143–24149 (2018). https://doi.org/10.1007/s11356-018-2481-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-2481-5

Keywords

Search

Navigation