Skip to main content

Advertisement

SpringerLink
Log in

Ecotoxicity of imidacloprid to soil invertebrates in two tropical soils with contrasting texture

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

Abstract

Imidacloprid is one of the most commercialized insecticides in agriculture in the world, with a broad spectrum of action. However, little is known about the effects of commercial formulations containing this active ingredient (a.i.) on non-target organisms in tropical soils. Our objective was to assess the toxicity based on the predicted environmental concentration (PEC) of imidacloprid, in the avoidance behaviour of earthworms and collembolans as well as in the reproduction of collembolans, in two representative soils of the Brazilian Cerrado with contrasting texture (clayey Oxisol and sandy Entisol). Ecotoxicity tests were carried out according to ISO protocols to assess the avoidance behaviour of earthworms (Eisenia andrei) and avoidance and reproduction of collembolans (Folsomia candida). In the earthworm’s avoidance test, more than 80% of the individuals were found in the control, in all tested concentrations, indicating a possible habitat function loss in both soils. The avoidance behaviour of collembolans was observed in both soils, being more expressive (up to 75% of escape) in Oxisol. In Entisol, only the two highest concentrations were avoided (up to 63%). There was a negative effect on the reproduction of collembolans in both soils, with a higher EC50 value (0.255 mg kg−1) in Oxisol than in Entisol (0.177 mg kg−1), demonstrating higher toxicity in the sandy soil. These differences were attributed to the contrasting texture of the studied soils, probably due to lower retention of the a.i. in the sandy soil, causing an increased bioavailability. This study demonstrated that imidacloprid can be highly toxic to soil invertebrates, even in soil concentrations lower than those expected from recommended dose, causing an impact on the edaphic organisms and, consequently, compromising its functions in the soil ecosystem.

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

Similar content being viewed by others

Data availability

Data, associated metadata, and calculation tools may be requested to the correspondent author (julia.carina@ufsc.br).

References

  • AGROFIT Sistema de Agrotóxicos Fitossanitários (2020) http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed 30 Nov 2019. (in Portuguese)

  • Albuquerque AF, Ribeiro JS, Kummrow F, Nogueira AJ, Montagner CC, Umbuzeiro GA (2016) Pesticides in Brazilian freshwaters: a critical review. Environ Sci Process Impacts 13;18(7):779-87. https://doi.org/10.1039/c6em00268d

  • 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. https://doi.org/10.1016/j.chemosphere.2012.11.046

    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. https://doi.org/10.1016/j.ecoenv.2014.04.010

    Article  CAS  Google Scholar 

  • Alves PRL, Silva EB, Cardoso EJBN, Alleoni LRF (2016) Ecotoxicological impact of arsenic on earthworms and collembolans as affected by attributes of a highly weathered tropical soil. Environ Sci Pollut R 25:13217–13225. https://doi.org/10.1007/s11356-016-6839-2

    Article  CAS  Google Scholar 

  • Alves PRL, Bandeira FO, Giraldi M, Presotto R, Segat JC, Cardoso EJBN, Baretta D (2019) Ecotoxicological assessment of Fluazuron: effects on Folsomia candida and Eisenia andrei. Environ Sci Pollut R 26:5842–5850. https://doi.org/10.1007/s11356-018-4022-7

    Article  CAS  Google Scholar 

  • Bandeira FO, Alves PRL, Hennig T, Schiehl A, Cardoso EJBN, Baretta D (2020) Toxicity of imidacloprid to the earthworm Eisenia andrei and collembolan Folsomia candida in three contrasting tropical soils. J Soils Sediments 20:1997–2007. https://doi.org/10.1007/s11368-019-02538-6

    Article  CAS  Google Scholar 

  • Bedos C, Cellier P, Calvet R, Barriuso E, Gabrielle B (2002) Mass transfer of pesticides into the atmosphere by volatilization from soils and plants: overview. Agronomie 22:21–33. https://doi.org/10.1051/agro:2001003

    Article  Google Scholar 

  • Bonmatin JM, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Long E, Marzaro M, Mitchell EA, Noome DA, Simon-Delso N, Tapparo A (2015) Environmental fate and exposure; neonicotinoids and fipronil. Environ Sci Pollut R 22:35–67. https://doi.org/10.1007/s11356-014-3332-7

    Article  CAS  Google Scholar 

  • Bonmatin JM, Noome DA, Moreno H, Mitchell EAD, Glauser G, Soumana OS, van Lexmond MB, Sánchez-Bayo F (2019) A survey and risk assessment of neonicotinoids in water, soil and sediments of Belize. Environ Pollut 249:949–958. https://doi.org/10.1016/j.envpol.2019.03.099

    Article  CAS  Google Scholar 

  • Bortoluzzi EC, Rheinheimer DS, Gonçalves CS, Pellegrini JBR, Zanella R, Copetti ACC (2006) Contaminação de águas superficiais por agrotóxicos em função do uso do solo numa microbacia hidrográfica de Agudo, RS. Revista Brasileira de Engenharia Agrícola e Ambiental 10(4):881–887. (in Portuguese). https://doi.org/10.1590/S1415-43662006000400015

    Article  Google Scholar 

  • Brandt A, Gorenflo A, Siede R, Meixner M, Buchler R (2016) The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). J Insect Physiol 86:40–47. https://doi.org/10.1016/j.jinsphys.2016.01.001

    Article  CAS  Google Scholar 

  • Bünemann EK, Bongiorno G, Bai Z, Creamer RE, De Deyn G, De Goede R, Fleskens L, Geissen V, Kuyper TW, Mäder P, Pulleman M, Sukkel W, Willem J, Groenigen V, Brussaard L (2018) Soil quality – a critical review. Soil Biol Biochem 120:105–125. https://doi.org/10.1016/j.soilbio.2018.01.030

    Article  CAS  Google Scholar 

  • Carniel LSC, Niemeyer JC, Oliveira Filho LCI, Alexandre D, Gebler L, Klauberg-Filho O (2019) The fungicide mancozeb affects soil invertebrates in two subtropical Brazilian soils. Chemosphere 232:180–185. https://doi.org/10.1016/j.chemosphere.2019.05.179

    Article  CAS  Google Scholar 

  • Cox L, Koskinen WC, Celis R, Hermosin MC, Cornejo J, Yen PY (1998) Sorption of imidacloprid on soil clay mineral and organic components. Soil Sci Soc Am J 62(4):911–915. https://doi.org/10.2136/sssaj1998.03615995006200040009x

    Article  CAS  Google Scholar 

  • Daam MA, Chelinho S, Niemeyer JC, Owojori OJ, De Silva PMCS, Sousa JP, van Gestel CAM, Rombke J (2019) Environmental risk assessment of pesticides in tropical terrestrial ecosystems: test procedures, current status and future perspectives. Ecotoxicol Environ Saf 181:534–547. https://doi.org/10.1016/j.ecoenv.2019.06.038

    Article  CAS  Google Scholar 

  • De Lima e Silva C, 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. https://doi.org/10.1007/s10646-017-1790-7

    Article  CAS  Google Scholar 

  • De Lima e Silva C, van Haren C, Mainardi G, Rooij W, Ligtelijn M, van Straalen N, van Gestel CAM (2021) Bringing ecology into toxicology: life-cycle toxicity of two neonicotinoids to four different species of springtails in LUFA 2.2 natural soil. Chemosphere 263: 128245. https://doi.org/10.1016/j.chemosphere.2020.128245

  • Dell Inc., 2015. Dell Statistica (Data Analysis Software System), Version 13. software.dell.com

  • Domene X, Chelinho S, Campana P, Alcañiz JP, Rombke J, Sousa JP (2012) Applying a GLM-based approach to model the influence of soil properties on the toxicity of phenmedipham to Folsomia candida. J Soils Sediments 12:888–899. https://doi.org/10.1007/s11368-012-0502-4

    Article  CAS  Google Scholar 

  • EC European Commission (2002) Draft working document. Guidance Document on Terrestrial Ecotoxicology under Council Directive 91/414/EEC. DOC Sanco/10329/2002 rev.2 (final) Brussels, 17 October

  • EC European Commission (2013) Commission Implementing Regulation (EU) 485/2013 of 24 May 2013 amending Implementing Regulation (EU) No 540/2011, as regards the conditions of approval of the active substances clothianidin, thiamethoxam and imidacloprid, and prohibiting the use and sale of seeds treated with plant protection products containing those active substances. Off J Eur Union 139:12–26

    Google Scholar 

  • EC European Commission (2018) Commission Implementing Regulation (EU) 2018/783 of 29 May 2018 amending Implementing Regulation (EU) No 540/2011 as regards the conditions of approval of the active substance imidacloprid. Official J Eur Union L 132:31–34

    Google Scholar 

  • EFSA European Food Safety Authority (2017) Scientific opinion addressing the state of the science on risk assessment of plant protection products for in-soil organisms. EFSA J 15:e04690. https://doi.org/10.2903/j.efsa.2017.4690

    Article  Google Scholar 

  • EMBRAPA (2004). Reunião de correlação, classificação e aplicação de levantamentos de solos da região Centro-Oeste – RCC-GO/MT. Rio de Janeiro: Embrapa Solos, 2004. 104p. (Boletim de Pesquisa e Desenvolvimento, 55). (in Portuguese)

  • EMBRAPA (2011) Manual de Métodos de Análise de Solo, 2nd edn. Embrapa Solos, Rio de Janeiro, RJ, Brazil (in Portuguese)

    Google Scholar 

  • Environment Canada (2007) Biological test method: test for measuring survival and reproduction of springtails exposed to contaminants in soil. Environmental Technology Center, Ottawa, Ontario, Canada

    Google Scholar 

  • Fox J, Weisberg S (2011) An {R} Companion to Applied Regression, 2nd edn. Sage, Thousand Oaks, CA

    Google Scholar 

  • Franco IO, Scopel I, Assunção HF (2015) Unidades de mapeamento de solos sob cultivo de cana-de-açúcar em 2011: análise da expansão da cultura no sudoeste de goiás (Brasil). Revista do Departamento de Geografia 30:1–18 (in Portuguese)

    Google Scholar 

  • Fu C, Liu T, Li L, Liu H, Chen D, Tang F (2013) The absorption, distribution, excretion and toxicity of mesoporous silica nanoparticles in mice following different exposure routes. Biomaterials 34:2565–2575. https://doi.org/10.1016/j.biomaterials.2012.12.043

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • 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. https://doi.org/10.1016/j.ecoenv.2018.06.064

    Article  CAS  Google Scholar 

  • Gomes L, Simões SJC, Dalla Nora EL, de Sousa-Neto ER, Forti MC, Ometto JPHB (2019) Agricultural expansion in the Brazilian Cerrado: increased soil and nutrient losses and decreased agricultural productivity. Land 8:12

    Article  Google Scholar 

  • Hayasaka D, Kobashi K, Hashimoto K (2019) Community responses of aquatic insects in paddy mesocosms to repeated exposures of the neonicotinoids imidacloprid and dinotefuran. Ecotoxicol Environ Saf 175:272–281. https://doi.org/10.1016/j.ecoenv.2019.03.051

    Article  CAS  Google Scholar 

  • Heupel K (2002) Avoidance response of different collembolan species to Betanal. Eur J Soil Biol 38:273–276. https://doi.org/10.1016/S1164-5563(02)01158-5

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346e363–346e363. https://doi.org/10.1002/bimj.200810425

    Article  Google Scholar 

  • IBAMA (2020) Relatório de Comercialização de Agrotóxicos. http://ibama.gov.br/agrotoxicos/relatorios-de-comercializacao-de-agrotoxicos. Accessed 30 nov 2019. (in Portuguese)

  • ISO International Organization for Standardization (2011a) Soil quality: avoidance test for determining the quality of soils and effects of chemicals on behaviour - Part 1: Test with earthworms (Eisenia fetida and Eisenia andrei). ISO 17512-1. Geneva.

  • ISO International Organization for Standardization (2011b) Soil quality: avoidance test for determining the quality of soils and effects of chemicals on behaviour - Part 2: Test with Collembolans (Folsomia candida). ISO 17512-2. Geneva.

  • ISO International Organization for Standardization (2012) Soil quality: effects of pollutants on earthworms – Part 2: determination of effects on reproduction of Eisenia fetida/Eisenia andrei. ISO 11268-2. Geneva.

  • ISO International Organization for Standardization (2014) Soil quality e inhibition of reproduction of Collembola (Folsomia candida) by soil contaminants. ISO 11267. Geneva.

  • IUPAC International Union of Pure and Applied Chemistry (2020) Organic Chemistry. https://iupac.org. Accessed 15 Jan 2020

  • Jactel H, Verheggen F, Thiéry D, Escobar-Gutiérrez AJ, Gachet E, Desneux N (2019) Alternatives to neonicotinoids. Environ Int 129:423–429. https://doi.org/10.1016/j.envint.2019.04.045

    Article  CAS  Google Scholar 

  • Kandil MM, El-Aswad AF, Koskinen WC (2015) Sorption–desorption of imidacloprid onto a lacustrine Egyptian soil and its clay and humic acid fractions. Journal of Environmental Science and Health. Part B 50(7):473–483. https://doi.org/10.1080/03601234.2015.1018758

    Article  CAS  Google Scholar 

  • Karahan A, Çakmak I, Hranitz JM, Karaca I, Wells H (2015) Sublethal imidacloprid effects on honey bee flower choices when foraging. Ecotoxicology 24:2017–2025. https://doi.org/10.1007/s10646-015-1537-2

    Article  CAS  Google Scholar 

  • Klink CA, Machado RB (2005) A conservação do Cerrado brasileiro. Megadiversidade 1(1):147–155 (in Portuguese)

    Google Scholar 

  • Kobashi K, Harada T, Adachi Y, Mori M, Ihara M (2017) Comparative ecotoxicity of imidacloprid and dinotefuran to aquatic insects in rice mesocosms. Ecotoxicol Environ Saf 138:122–129. https://doi.org/10.1016/j.ecoenv.2016.12.025

    Article  CAS  Google Scholar 

  • Komsta L, Novomestky F (2015) Moments, cumulants, skewness, kurtosis and related tests. R package version 0.14.

  • Lee YS, Lee SE, Son J, Kim Y, Wee J, Cho K (2018) Toxicity effects and biomarkers of tebufenozide exposure in Yuukianura szeptyckii (Collembola: Neanuridae). Environ Geochem Health 40:2773–2784. https://doi.org/10.1007/s10653-018-0143-7

    Article  CAS  Google Scholar 

  • Liu W, Zheng W, Ma Y, Liu KK (2006) Sorption and degradation of imidacloprid in soil and water. J Environ Sci Health B 41:623–634. https://doi.org/10.1080/03601230600701775

    Article  CAS  Google Scholar 

  • Maliszewska-Kordybach B, Klimkowicz-Pawlas A, Smreczak B (2008) Soil reference materials in ecotoxicity testing – application of the concept of EURO-soils to soils from Poland. Pol J Environ Stud 17:257–266

    CAS  Google Scholar 

  • Menezes-Oliveira VB, Bianchi MO, Espindola ELG (2018) Hazard assessment of the pesticides kraft 36 EC and score in a tropical natural soil using an ecotoxicological test battery. Environ Toxicol Chem 37:2919–2924. https://doi.org/10.1002/etc.4056

    Article  CAS  Google Scholar 

  • Moscardini VF, Gontijo PC, Michaud JP, Carvalho GA (2015) Sublethal effects of insecticide seed treatments on two nearctic lady beetles (Coleoptera: Coccinellidae). Ecotoxicology 24:1152–1161. https://doi.org/10.1007/s10646-015-1462-4

    Article  CAS  Google Scholar 

  • Motaung TE (2020) Chloronicotinyl insecticide imidacloprid: agricultural relevance, pitfalls and emerging opportunities. Crop Prot 131:105097. https://doi.org/10.1016/j.cropro.2020.105097

    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 

  • Niemeyer JC, Chelinho S, Sousa JP (2017) Soil ecotoxicology in Latin America: current research and perspectives. Environ Toxicol Chem 36:1795–1810. https://doi.org/10.1002/etc.3792

    Article  CAS  Google Scholar 

  • Nilsson E, Bengtsson G (2004) Death odour changes movement pattern of a Collembola. Oikos 104:509–517. https://doi.org/10.1111/j.0030-1299.2004.12921.x

    Article  Google Scholar 

  • 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 

  • OECD (2016) The Organization for Economic Cooperation and Development (2016) Predatory mite (Hypoaspis (Geolaelaps) aculeifer) reproduction test in soil. Test No. 226. OECD Guidelines for the Testing of Chemicals, Section 2, OECD Publishing. Paris. https://doi.org/10.1787/9789264264557-en

  • Ogungbemi AO, van Gestel CAM (2018) Extrapolation of imidacloprid toxicity between soils by exposing Folsomia candida in soil pore water. Ecotoxicology 27:1107–1115. https://doi.org/10.1007/s10646-018-1965-x

    Article  CAS  Google Scholar 

  • Oliveira RS, Koskinen WC, Werdin NR, Yen PY (2000) Sorption of imidacloprid and its metabolites on tropical soils. J Environ Sci Health B 35(1):39–49. https://doi.org/10.1080/03601230009373252

    Article  Google Scholar 

  • Oliveira VA, Jacomine PKT, Couto EG (2017) Solos do Bioma Cerrado. In: Curi N (ed) Pedologia – solos dos biomas brasileiros, 1st edn. Sociedade Brasileira de Ciência do Solo, Viçosa, MG, pp 177–226 (in Portuguese)

    Google Scholar 

  • Pereira CMS, Novais SC, Soares AMVM, Amorim MJB (2013) Dimethoate affects cholinesterases in Folsomia candida and their locomotion - false negative results of an avoidance behaviour test. Sci Total Environ 443(15):821–827. https://doi.org/10.1016/j.scitotenv.2012.11.044

    Article  CAS  Google Scholar 

  • Pietrzak D, Kania J, Kmiecik E, Malina G, Wątor K (2020) Fate of selected neonicotinoid insecticides in soil–water systems: current state of the art and knowledge gaps. Chemosphere 255:126981. https://doi.org/10.1016/j.chemosphere.2020.126981

    Article  CAS  Google Scholar 

  • Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, Kreutzweiser 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 R 22:68–102. https://doi.org/10.1007/s11356-014-3471-x

    Article  CAS  Google Scholar 

  • R Core Team, 2017. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2013 http://wwwR-projectorg/ Assessed 01 Oct 2018.

  • Sánchez-Bayo F, Goka K, Hayasaka D (2016) Contamination of the aquatic environment with neonicotinoids and its implication for ecosystems. Front Environ Sci 4:71. https://doi.org/10.3389/fenvs.2016.00071

    Article  Google Scholar 

  • Sánchez-Bayo F, Belzunces L, Bonmatin JM (2017) Lethal and sublethal effects, and incomplete clearance of ingested imidacloprid in honey bees (Apis mellifera). Ecotoxicology 26:1199–1206. https://doi.org/10.1007/s10646-017-1845-9

    Article  CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089

    Article  CAS  Google Scholar 

  • Souza LFCB, Montagner CC, Almeida MB, Kuroda EK, Vidal C, Freire RL (2019) Determination of pesticides in the source and drinking waters in Londrina, Paraná, Brazil. Semina:Ciencias Agrarias 40(3):1153-1163. 10.5433/1679-0359.2019v40n3p1153

  • van Gestel CAM, Lima e Silva C, Lam T, Koekkoek JC, Lamoree MH, Verweij RA (2017) Multigeneration toxicity of imidacloprid and thiacloprid to Folsomia candida. Ecotoxicology 26:320-328. https://doi.org/10.1007/s10646-017-1765-8

  • van Groenigen J, Lubbers I, Vos H et al (2015) Earthworms increase plant production: a meta-analysis. Sci Rep 4:6365. https://doi.org/10.1038/srep06365

    Article  CAS  Google Scholar 

  • Wang X, Zhu J, 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. https://doi.org/10.1016/j.chemosphere.2018.12.001

    Article  CAS  Google Scholar 

  • Wenke K, Kai M, Piechulla B (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231:499–506. https://doi.org/10.1007/s00425-009-1076-2

    Article  CAS  Google Scholar 

  • Xiao D, Zhao J, Guo X, Chen H, Qu M, Zhai W, Desneux N, Biondi A, Zhang F, Wang S (2016) Sublethal effects of imidacloprid on the predatory seven-spot ladybird beetle Coccinella septempunctata. Ecotoxicology 25:1782–1793. https://doi.org/10.1007/s10646-016-1721-z

    Article  CAS  Google Scholar 

  • Zhang P, Ren C, Sun H, Min L (2018) Sorption, desorption and degradation of neonicotinoids in four agricultural soils and their effects on soil microorganisms. Sci Total Environ 615:59–69. https://doi.org/10.1016/j.scitotenv.2017.09.097

    Article  CAS  Google Scholar 

  • Zortea T, Reis TR, Serafini S, Souza JP, Silva AS, Baretta D (2018) Ecotoxicological effect of fipronil and its metabolites on Folsomia candida in tropical soils. Environ Toxicol Pharmacol 62:203–209. https://doi.org/10.1016/j.etap.2018.07.011

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are thankful for the financial support of The Brazilian National Council for Scientific and Technological Development (CNPq) through the process 449731/2014-6. We also acknowledge the Coordination for the Improvement of Higher Education Personnel (CAPES) for the master’s scholarship of MM Bernardino, and the Foundation for Research and Innovation of the State of Santa Catarina (FAPESC) for the master’s scholarship of FB de Santo. The authors would like to thank the two anonymous reviewers for their constructive comments that greatly contributed to improving the final version of the paper.

Funding

Financial support received from The Brazilian National Council for Scientific and Technological Development (CNPq) under Grant Agreement 449731/2014-6; Master Scholarship of MMB supported by Coordination for the Improvement of Higher Education Personnel (CAPES), and of FBS by Foundation for Research and Innovation of the State of Santa Catarina (FAPESC).

Author information

Authors and Affiliations

  1. Postgraduate Program in Agrochemistry, Goiano Federal Institute of Education, Science and Technology, P.O Box 66, Campus Rio Verde, Rio Verde, Goiás, 75901-970, Brazil

    Murilo Martins Bernardino & Rafael Marques Pereira Leal

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

    Paulo Roger Lopes Alves

  3. Postgraduate Program in Agricultural and Natural Ecosystems (PPGEAN), Federal University of Santa Catarina (UFSC), Campus of Curitibanos, Curitibanos, Santa Catarina, 89520-000, Brazil

    Fernanda Benedet de Santo & Júlia Carina Niemeyer

Authors
  1. Murilo Martins Bernardino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paulo Roger Lopes Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernanda Benedet de Santo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Júlia Carina Niemeyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rafael Marques Pereira Leal
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MM Bernardino: data acquisition, writing; PRL Alves, FB de Santo: data analysis, writing, reviewing, editing; RP Leal, JC Niemeyer: conceptualization, funding acquisition, writing, reviewing, editing, supervision.

Corresponding author

Correspondence to Júlia Carina Niemeyer.

Ethics declarations

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

Consent to participate

Not applicable.

Consent to publish

Not applicable.

Additional information

Responsible Editor: Chris Lowe

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 83 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bernardino, M.M., Alves, P.R.L., de Santo, F.B. et al. Ecotoxicity of imidacloprid to soil invertebrates in two tropical soils with contrasting texture. Environ Sci Pollut Res 28, 27655–27665 (2021). https://doi.org/10.1007/s11356-021-12562-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-12562-0

Keywords

Search

Navigation