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Toxicity of imidacloprid to the earthworm Eisenia andrei and collembolan Folsomia candida in three contrasting tropical soils

  • Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article
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Abstract

Purpose

Imidacloprid is a widely used seed dressing insecticide in Brazil. However, the effects of this pesticide on non-target organisms such as soil fauna still present some knowledge gaps in tropical soils. This study aimed to assess the toxicity and risk of imidacloprid to earthworms Eisenia andrei and collembolans Folsomia candida in three contrasting Brazilian tropical soils.

Materials and methods

Acute and chronic toxicity assays were performed in the laboratory with both species in a tropical artificial soil (TAS) and in two natural soils (Oxisol and Entisol), at room temperature of 25 °C. The ecological risk was calculated for each species and soil by using the toxicity exposure ratio (TER) and hazard quotient (HQ) approaches.

Results and discussion

Acute toxicity for collembolans and earthworms was higher in Entisol (LC50 = 4.68 and 0.55 mg kg−1, respectively) when compared with TAS (LC50 = 10.8 and 9.18 mg kg−1, respectively) and Oxisol (LC50collembolans = 25.1 mg kg−1). Chronic toxicity for collembolans was similar in TAS and Oxisol (EC50 TAS = 0.80 mg kg−1; EC50 OXISOL = 0.83 mg kg−1), whereas higher toxicity was observed in Entisol (EC50 = 0.09 mg kg−1). In chronic assays with earthworms, imidacloprid was also more toxic in Entisol (EC50 = 0.21 mg kg−1) when compared to TAS (EC50 = 1.89 mg kg−1). TER and HQ values indicated a significant risk of exposure of the species to imidacloprid in all soils tested, and the risk in Entisol was at least six times higher than in Oxisol or TAS.

Conclusions

The toxicity and risk of imidacloprid varied significantly between tropical soils, being the species exposure to this pesticide particularly hazardous in very sandy natural soils such as Entisol.

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References

  • Akeju TO (2014) Assessment of the effects of the neonicotinoids thiacloprid and acetamiprid on soil fauna. Master’s thesis, University of Coimbra

  • Alves PRL, Cardoso EJBN, Martines AM, Sousa JP, Pasini A (2013) Earthworm ecotoxicological assessments of pesticides used to treat seeds under tropical conditions. Chemosphere 90:2674–2682

    Article  CAS  Google Scholar 

  • Alves PRL, Cardoso EJBN, Martines AM, Sousa JP, Pasini A (2014) Seed dressing pesticides on springtails in two ecotoxicological laboratory tests. Ecotoxicol Environ Saf 105:65–71

    Article  CAS  Google Scholar 

  • Alves PRL, Niemeyer JC, Cardoso EJBN (2017) Section I: terrestrial invertebrates as experimental models chapter 1. The use of non-standardized invertebrates in soil ecotoxicology. Issues in toxicology, 1-30, Royal Society of Chemistry

  • Amorim MJB, Römbke J, Scheffczyk A, Soares AMVM (2005) Effect of different soil types on the enchytraeids Enchytraeus albidus and Enchytraeus luxuriosus using the herbicide Phenmedipham. Chemosphere 61:1102–1114

    Article  CAS  Google Scholar 

  • Belfroid A, Meiling J, Sijm D, Hermens J, Seinen W, van Gestel K (1994) Uptake of hydrophobic halogenated aromatic hydrocarbons from food by earthworms (Eisenia andrei). Arch Environ Contam Toxicol 27:260–265

  • Bonmatin J-M, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Long E, Marzaro M, Mitchell EAD, Noome DA, Simon-Delso N, Tapparo A (2014) Environmental fate and exposure; neonicotinoids and fipronil. Environ Sci Pollut Res 22:35–67

    Article  CAS  Google Scholar 

  • Brazil (1996) IBAMA Normative Ordinance No. 84, October 15th, 1996. Establish procedures to be adopted in the Brazilian Institute of Environment and Renewable Natural Resources – IBAMA, for registration purposes and for assessment of the potential environmental hazard (PPA) of pesticides. DOU No. 203, Section 1, p. 21358 (in Portuguese)

  • Catae AF, Roat TC, Pratavieira M, Menegasso AR, Palma MS, Malaspina O (2018) Exposure to a sublethal concentration of imidacloprid and the side effects on target and nontarget organs of Apis mellifera (Hymenoptera, Apidae). Ecotoxicology 27:109–121

    Article  CAS  Google Scholar 

  • Chelinho S, Domene X, Campana P, Natal-da-Luz T, Scheffczyk A, Römbke J, Andrés P, Sousa JP (2011) Improving ecological risk assessment in the Mediterranean area: selection of reference soils and evaluating the influence of soil properties on avoidance and reproduction of two oligochaete species. Environ Toxicol Chem 30:1050–1058

    Article  CAS  Google Scholar 

  • Chelinho S, Domene X, Campana P, Andrés P, Römbke J, Sousa JP (2014) Toxicity of phenmedipham and carbendazim to Enchytraeus crypticus and Eisenia andrei (Oligochaeta) in Mediterranean soils. J Soils Sediments 14:584–599

    Article  CAS  Google Scholar 

  • Chevillot F, Convert Y, Desrosiers M, Cadoret N, Veilleux É, Cabana H, Bellenger J (2017) Selective bioaccumulation of neonicotinoids and sub-lethal effects in the earthworm Eisenia andrei exposed to environmental concentrations in an artificial soil. Chemosphere 186:839–847

    Article  CAS  Google Scholar 

  • Dankyi E, Gordon C, Carboo D, Fomsgaard IS (2014) Quantification of neonicotinoid insecticide residues in soils from cocoa plantations using a QuEChERS extraction procedure and LC-MS/MS. Sci Total Environ 499:276–283

    Article  CAS  Google Scholar 

  • de Lima ESC, Brennan N, Brouwer JM, Commandeur D, Verweij RA, van Gestel CAM (2017) Comparative toxicity of imidacloprid and thiacloprid to different species of soil invertebrates. Ecotoxicology 26:555–564

  • De Silva PMCS, van Gestel CAM (2009) Development of an alternative artificial soil for earthworm toxicity testing in tropical countries. Appl Soil Ecol 43:170–174

    Article  Google Scholar 

  • De Silva PMCS, Pathiratne A, van Gestel CAM (2009) Influence of temperature and soil type on the toxicity of three pesticides to Eisenia andrei. Chemosphere 76:1410–1415

    Article  CAS  Google Scholar 

  • Domene X, Chelinho S, Campana P, Natal-da-Luz T, Alcañiz JM, Andrés P, Römbke J, Sousa JP (2011) Influence of soil properties on the performance of Folsomia candida: implications for its use in soil ecotoxicology testing. Environ Toxicol Chem 30:1497–1505

    Article  CAS  Google Scholar 

  • Donnarumma L, Pulcini P, Pochi D, Rosati S, Lusco L, Conte E (2011) Preliminary study on persistence in soil and residues in maize of imidacloprid. J Environ Sci Health B 46:469–472

    CAS  Google Scholar 

  • Douglas MR, Tooker JF (2015) Large-scale deployment of seed treatments has driven rapid increase in use of neonicotinoid insecticides and preemptive pest management in U.S. field crops. Environ Sci Technol 49:5088–5097

    Article  CAS  Google Scholar 

  • EC (2002) SANCO/10329/2002 - Final Guidance Document on Terrestrial Ecotoxicology under Council Directive 91/414/EEC. European Commission Health & Consumer Protection Directorate-General. E1-Plant Health

  • EC (2003) Technical Guidance Document on Risk Assessment. In Support of Commission Directive 93/67/EEC. Commission Regulation (EC) No 1488/94 and Directive 98/8/EC. European Commission Joint Research Center

  • EFSA (2018) European food safety authority. Conclusion on the peer review of the pesticide risk assessment for bees for the active substance imidacloprid considering the uses as seed treatments and granules. EFSA J 16(2):5178–5113

    Google Scholar 

  • EMBRAPA (2006) Centro Nacional de Pesquisa de Solos (Rio de Janeiro, RJ). Sistema brasileiro de classificação de solos, 2nd edn. EMBRAPA-SPI, Rio de Janeiro

    Google Scholar 

  • Environmental Canada (2007) Guidance Document on Statistical Methods for Environmental Toxicity Test. Environmental Protection Series, EPS 1/RM/46, 2005 with 2007 updates. Environmental Canada, Ottawa

  • EPPO (2003) Environmental risk assessment scheme for plant protection products. Chapter 4: Soil. OEPP EPP0 Bull 33:151–162

    Article  Google Scholar 

  • EU (2013) COMMISSION REGULATION (EU) No 283/2013 of 1 March 2013 setting out the data requirements for active substances, in accordance with Regulation (EC) No 1107/2009 of the European Parliament and of the Council concerning the placing of plant protection products on the market. Off J Eur Union L 93:1–84

  • Fountain MT, Hopkin SP (2005) Folsomia candida (COLLEMBOLA): a “standard” soil arthropod. Annu Rev Entomol 50:201–222

    Article  CAS  Google Scholar 

  • Garcia MVB (2004) Effects of pesticides on soil fauna: development of ecotoxicological test methods for tropical regions. Ecology and development series, vol 19. Doctoral thesis, University of Bonn

  • Ge J, Xiao Y, Chai Y, Yan H, Wu R, Xin X, Wang D, Yu X (2018) Sub-lethal effects of six neonicotinoids on avoidance behavior and reproduction of earthworms (Eisenia fetida). Ecotoxicol Environ Saf 162:423–429

    Article  CAS  Google Scholar 

  • Goulson D (2013) REVIEW: an overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50:977–987

    Article  Google Scholar 

  • Ihara M, Matsuda K (2018) Neonicotinoids: molecular mechanisms of action, insights into resistance and impact on pollinators. Curr Opin Insect Sci 30:1–7

    Article  Google Scholar 

  • ISO (1993) International organization for standardization - 11268-1. Soil quality - effects of pollutants on earthworms (Eisenia fetida) - Part 1: Determination of acute toxicity using soil substrate. Genève, pp 26

  • ISO (2012) International Standardization Organization - 11268-2. Soil quality - effects of pollutants on earthworms - Part 2: Determination of effects on reproduction of Eisenia fetida/Eisenia andrei. Genève, Switzerland

  • ISO (2014) International Standardization Organization – 11267. Soil quality - Inhibition of reproduction of Collembola (Folsomia candida) by soil contaminants. Genève, Switzerland

  • Jeschke P, Nauen R, Schindler M, Elbert A (2011) Overview of the status and global strategy for neonicotinoids. J Agric Food Chem 59:2897–2908

    Article  CAS  Google Scholar 

  • Laycock I, Lenthall KM, Barratt AT, Cresswell JE (2012) Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21:1937–1945

    Article  CAS  Google Scholar 

  • Mabubu JI, Nawaz M, Cai W, Zhao J, He Y, Hua H (2017) Ecotoxicity of the neonicotinoid insecticides imidacloprid and thiacloprid to the soil-dwelling arthropod Folsomia candida (Collembola). J Kansas Entomol Soc 90:323–333

    Article  Google Scholar 

  • Maccari AP, Baretta D, Paiano D, Leston S, Freitas A, Ramos F, Sousa JP, Klauberg-Filho O (2016) Ecotoxicological effects of pig manure on Folsomia candida in subtropical Brazilian soils. J Hazard Mater 314:113–120

    Article  CAS  Google Scholar 

  • Niemeyer JC, Chelinho S, Sousa JP (2017) Soil ecotoxicology in Latin America: current research and perspectives. Environ Toxicol Chem 36:1795–1810

    Article  CAS  Google Scholar 

  • Niva CC, Niemeyer JC, Júnior FM, Nunes ME, De Sousa DL, Aragão CW, Sautter KD, Espindola EG, Sousa JP, Römbke J (2016) Soil ecotoxicology in Brazil is taking its course. Environ Sci Pollut Res 23:11363–11378

    Article  CAS  Google Scholar 

  • Ogungbemi AO, van Gestel CAM (2018) Extrapolation of imidacloprid toxicity between soils by exposing Folsomia candida in soil pore water. Ecotoxicology 27:1107–1115

  • Peijnenburg W, Capri E, Kula C, Liess M, Luttik R, Montforts M, Nienstedt K, Römbke J, Sousa JP, Jensen J (2012) Evaluation of exposure metrics for effect assessment of soil invertebrates. Crit Rev Environ Sci Technol 42:1862–1893

    Article  CAS  Google Scholar 

  • Ping L, Zhang C, Zhu Y, Wu M, Dai F, Hu X, Zhao H, Li Z (2010) Imidacloprid adsorption by soils treated with humic substances under different pH and temperature conditions. J Biotechnol 9:1935–1940

    CAS  Google Scholar 

  • Pisa LW, Amaral-Rogers LP, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, Kreutzweiserm DP, Krupke C, Liess M, McField M, Morrissey CA, Noome DA, Settele J, Simon-Delso N, Stark JD, Van der Sluijs JP, Van Dyck H, Wiemers M (2015) Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res 22:68–102

    Article  CAS  Google Scholar 

  • Renaud M, Akeju T, Natal-da-Luz T, Leston S, Rosa J, Ramos F, Sousa JP, Azevedo-Pereira HMVS (2018) Effects of the neonicotinoids acetamiprid and thiacloprid in their commercial formulations on soil fauna. Chemosphere 194:85–93

    Article  CAS  Google Scholar 

  • Rutherford DW, Chiou CT, Kile DE (1992) Influence of soil organic matter composition on the partition of organic compounds. Environ Sci Technol 26:336–340

    Article  CAS  Google Scholar 

  • Segat JC, Alves PRL, Baretta D, Cardoso EJBN (2015) Ecotoxicological evaluation of swine manure disposal on tropical soils in Brazil. Ecotoxicol Environ Saf 122:91–97

    Article  CAS  Google Scholar 

  • Sharma S, Singh B (2014) Persistence behaviour of imidacloprid and its metabolites in soil under sugarcane. Environ Monit Assess 186:2281–2288

    Article  CAS  Google Scholar 

  • Sheng GY, Yang YN, Huang MS, Yang K (2005) Influence of pH on pesticide sorption by soil containing wheat residue-derived char. Environ Pollut 134:457–463

    Article  CAS  Google Scholar 

  • Sillapawattana P, Schäffer A (2017) Effects of imidacloprid on detoxifying enzyme glutathione S-transferase on Folsomia candida (Collembola). Environ Sci Pollut Res 24:11111–11119

    Article  CAS  Google Scholar 

  • Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke CH, Liess M, Long E, McField M, Mineau P, Mitchell EAD, Morrissey CA, Noome DA, Pisa L, Settele J, Stark JD, Tapparo A, Van Dyck H, Van Praagh J, Van der Sluijs JP, Whitehorn PR, Wiemers M (2015) Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res 22:5–34

    Article  CAS  Google Scholar 

  • Tedesco MJ, Gianello C, Bissani CA, Bohnen H, Volkweiss SJ (1995) Análise de solo, plantas e outros materiais, 2nd edn. Universidade Federal do Rio Grande do Sul, Porto Alegre, p 147 (Boletim Técnico, 5)

    Google Scholar 

  • Van der Sluijs JP, Amaral-Rogers V, Belzunces LP, Bijleveld van Lexmond MFIJ, Bonmatin J, Chagnon M, Downs CA, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Long E, McField M, Mineau P, Mitchell EAD, Morrissey CA, Noome DA, Pisa L, Settele J, Simon-Delso N, Stark JD, Tapparo A, Van Dyck H, Van Praagh J, Whitehorn PR, Wiemers M (2015) Conclusions of the worldwide integrated assessment on the risks of neonicotinoids and fipronil to biodiversity and ecosystem functioning. Environ Sci Pollut Res 22:148–154

    Article  CAS  Google Scholar 

  • van Gestel CAM (2012) Soil ecotoxicology: state of the art and future directions. ZooKeys 176:275–296

  • van Gestel CAM, de Lima ESC, Lam T, Koekkoek JC, Lamoree MH, Verweij RA (2017) Multigeneration toxicity of imidacloprid and thiacloprid to Folsomia candida. Ecotoxicology 26(3):1–9

  • Wang J, Wang J, Wang G, Zhu L, Wang J (2016) DNA damage and oxidative stress induced by imidacloprid exposure in the earthworm Eisenia fetida. Chemosphere 144:510–517

    Article  CAS  Google Scholar 

  • Wang X, Zhu X, Peng Q, Wang Y, Ge J, Yang G, Wang X, Cai L, Shen W (2019) Multi-level ecotoxicological effects of imidacloprid on earthworm (Eisenia fetida). Chemosphere 219:923–932

    Article  CAS  Google Scholar 

  • Wood TJ, Goulson D (2017) The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environ Sci Pollut Res 24:17285–17325

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the reviewers who provided thoughtful and constructive feedback on this manuscript and also thank the National Research Coucil (CNPq) for the research grant (Project 407170/2016-2). D.B. and E.J.B.N.C thank CNPq for their research productivity grants (Processes number 307162/2015-0 and 305193/2016-3, respectively). T.B.H. thanks CNPq for a Grant of Scientific Initiation (Process number 167664/2017-4). A.S. thanks Federal University of Fronteira Sul for a Grant of Scientific Initiation (Process code PES-2018-0959). F.O.B. thanks the Coordination for the Improvement of Higher Education Personnel (CAPES) for a master grant.

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Authors and Affiliations

  1. Department of Soil Science, Santa Catarina State University, Av. Luis de Camões, 2090, Lages, SC, 88520-000, Brazil

    Felipe Ogliari Bandeira & Thuanne Bráulio Hennig

  2. Federal University of Fronteira Sul, Av. Fernando Machado 108 E, Chapecó, SC, 89802112, Brazil

    Paulo Roger Lopes Alves & Aline Schiehl

  3. Department of Soil Science, University of São Paulo, Avenida Pádua Dias, 11, Piracicaba, 13416-900, Brazil

    Elke Jurandy Bran Nogueira Cardoso

  4. Centro de Educação Superior do Oeste, Santa Catarina State University, Beloni Trombeta Zanin, 680-E, Chapecó, SC, 89815-630, Brazil

    Dilmar Baretta

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  1. Felipe Ogliari Bandeira
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Correspondence to Paulo Roger Lopes Alves.

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Bandeira, F.O., Alves, P.R.L., Hennig, T.B. et al. Toxicity of imidacloprid to the earthworm Eisenia andrei and collembolan Folsomia candida in three contrasting tropical soils. J Soils Sediments 20, 1997–2007 (2020). https://doi.org/10.1007/s11368-019-02538-6

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