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Combined toxicity of chlorpyrifos, abamectin, imidacloprid, and acetamiprid on earthworms (Eisenia fetida)

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Abstract

Mixed pesticides have been broadly used in agriculture. However, assessing the combined effects of pesticides in the environment is essential for potential risk assessment, though the task is far from complete. Median lethal concentrations of pesticides as well as acetylcholinesterase (AChE) levels and cellulose activities were measured in earthworms (Eisenia fetida) individually and jointly exposed to pesticides imidacloprid (IMI), acetamiprid (ACE), chlorpyrifos (CRF), and abamectin (ABM)). A 3:1 mixture of CRF and IMI had additive effects, while a 3:1 mixture of CRF and ACE had synergic effects. The joint effects of ABM with IMI or with ACE were synergistic. As CRF concentration increased, AChE activities were significantly decreased. For high concentrations of IMI, AChE activities under combined CRF and IMI applications were significantly inhibited following increased exposure time. Moreover, the cellulase activities under combined applications of CRF with IMI or with ACE had similar effects. This study provides basic data for scientifically evaluating the environmental risk and safety of combined uses of pesticides.

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Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • 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 

  • Bart S, Pelosi C, Barraud A, Pery ARR, Cheviron N, Grondin V, Mougin C, Crouzet O (2019) Earthworms mitigate pesticide effects on soil microbial activities. Front Microbiol 10:11

    Article  Google Scholar 

  • Belden JB, Brain RA (2017) Incorporating the joint toxicity of co-applied pesticides into the ecological risk assessment process. Integr Environ Assess Manag 14(1):79–91

    Article  CAS  Google Scholar 

  • Bishop CA, Woundneh MB, Maisonneuve F, Common J, Elliott JE, Moran AJ (2020) Determination of neonicotinoids and butenolide residues in avian and insect pollinators and their ambient environment in Western Canada (2017,2018). Sci Total Environ 737:139386

    Article  CAS  Google Scholar 

  • Blouin M, Hodson ME, Delgado EA, Baker G, Brussaard L, Butt KR, Dai J, Dendooven L, Peres G, Tondoh JE, Cluzeau D, Brun JJ (2013) A review of earthworm impact on soil function and ecosystem services. Eur J Soil Sci 64:161–182

    Article  Google Scholar 

  • Campbell WC (2012): Ivermectin and abamectin. Springer Science & Business Media

  • Castillo Diaz JM, Martin-Laurent F, Beguet J, Nogales R, Romero E (2016) Fate and effect of imidacloprid on vermicompost-amended soils under dissimilar conditions: risk for soil functions, structure, and bacterial abundance. ence of the Total. Environment 579:1111–1119

    Google Scholar 

  • Cedergreen N (2014) Quantifying synergy: a systematic review of mixture toxicity studies within environmental toxicology. PLoS One 9:e96580

    Article  CAS  Google Scholar 

  • Chagnon M, Kreutzweiser D, Mitchell EA, Mitchell EA, Morrissey CA, Noome DA, Noome DA, Van der Sluijs JP, Van der Sluijs JP (2015) Risks of large-scale use of systemic insecticides to ecosystem functioning and services. Environ Sci Pollut Res 22:119–134

    Article  CAS  Google Scholar 

  • Chan KY (2001) An overview of some tillage impacts on earthworm population abundance and diversity - implications for functioning in soils. Soil Tillage Res 57:179–191

    Article  Google Scholar 

  • Cimino AM, Boyles AL, Thayer KA, Perry MJ (2017) Effects of neonicotinoid pesticide exposure on human health: a systematic review. Environ Health Perspect 125:155–162

    Article  CAS  Google Scholar 

  • Colovic MB, Krstic DZ, Lazarevic-Pasti TD, Bondzic AM, Vasic VM (2013) Acetylcholinesterase Inhibitors: pharmacology and toxicology. Curr Neuropharmacol 11(3):315–335

    Article  CAS  Google Scholar 

  • Dong-Mei XU, Yan-Hua W, Nan W, Gui-Wei R (2015) Effects of Single and Co-Exposure of Cu and Chlorpyrifos on the Toxicity of Earthworm. Environ Sci 36:280–285

    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. Environl Sci Technol 49:5088–5097

    Article  CAS  Google Scholar 

  • Fang W, Peng Y, Muir D, Lin J, Zhang X (2019) A critical review of synthetic chemicals in surface waters of the US, the EU and China. Environ Int 131:104994

    Article  CAS  Google Scholar 

  • FAO (2021) Food and agriculture organization of the United Nations. http://www.fao.org/faostat/en.#data/RP

  • EFSA (2019): European votes against renew chlorpyrifos approval. https://www.foodsafetynews.com/2019/12/eu-votes-against-renewing-chlorpyrifos-approval/

  • Ghose TK (1987) Measurement of cellulase activities. Pure Appl Chem 59(2):257–268

    Article  CAS  Google Scholar 

  • Gomez-Eyles JL, Svendsen C, Lister L, Martin H, Hodson ME, Spurgeon DJ (2009) Measuring and modelling mixture toxicity of imidacloprid and thiacloprid on Caenorhabditis elegans and Eisenia fetida. Ecotoxicol Environ Saf 72:71–79

    Article  CAS  Google Scholar 

  • Hallmann CA, Foppen RPB, Turnhout CAMV, Kroon HD, Jongejans E (2014) Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511:341–343

    Article  CAS  Google Scholar 

  • Hasenbein S, Lawler SP, Geist J, Connon RE (2015) The use of growth and behavioral endpoints to assess the effects of pesticide mixtures upon aquatic organisms. Ecotoxicology 24:746–759

    Article  CAS  Google Scholar 

  • Ikarashi Y, Yarimizu J, Yokoyama K, Kobayashi T, Nakazawa H (2016) Characterization of two endoglucanases for the classification of the earthworm, Eisenia fetida Waki. Biosci Biotechnol Biochem 80(1):55–66

    Article  CAS  Google Scholar 

  • John EM, Shaike JM (2015) Chlorpyrifos: pollution and remediation. Environ Chem Lett 13:269–291

    Article  CAS  Google Scholar 

  • Kaizer RR, Spanevello RM, Costa E, Morsch VM, Schetinger MRC (2017): Effect of high fat diets on 5′-nucleotidase and acetylcholinesterase activities in the central nervous system. Int J Dev Neuroence Off J Int Soc Dev Neuroence S0736574817300096

  • Karanjkar AS, Naik RL (2009) Acute toxicity: novel mode of pesticides on earthworm. Int J Plant Protect 2:182–185

    Google Scholar 

  • Kousba AA, Sultatos LG, Poet TS, Timchalk C (2004) Comparison of chlorpyrifos-oxon and paraoxon acetylcholinesterase inhibition dynamics: potential role of a peripheral binding site. Toxicol Sci 80:239–248

    Article  CAS  Google Scholar 

  • Kwak JI, An Y-J (2021) Microplastic digestion generates fragmented nanoplastics in soils and damages earthworm spermatogenesis and coelomocyte viability. J Hazard Mater 402:124034

    Article  CAS  Google Scholar 

  • Liang Y, Dong B, Pang N, Hu J (2019) ROS generation and DNA damage contribute to abamectin-induced cytotoxicity in mouse macrophage cells. Chemosphere 234:328–337

    Article  CAS  Google Scholar 

  • Loureiro S, Svendsen C, Ferreira ALG, Pinheiro C, Ribeiro F, Soares AMVM (2010) Toxicity of three binary mixtures to Daphnia magna: comparing chemical modes of action and deviations from conceptual models. Environ Toxicol Chem 29:1716–1726

    Article  CAS  Google Scholar 

  • Mattsson K, Johnson EV, Malmendal A, Linse S, Hansson LA, Cedervall T (2017) Brain damage and behavioural disorders in fish induced by plastic nanoparticles delivered through the food chain. Sci Rep 7:11452

    Article  CAS  Google Scholar 

  • Nozaki M, Miura C, Tozawa Y, Miura T (2009) The contribution of endogenous cellulase to the cellulose digestion in the gut of earthworm (Pheretima hilgendorfi: Megascolecidae). Soil Biol Biochem 41:762–769

    Article  CAS  Google Scholar 

  • OECD (1984): Earthworm acute toxicity. OECD Giideline for Testig of Chemicals No. 207.

  • OECD (2004): Earthworm reproduction test (Eisenia fetida/Eisenia andrei). OECD Giideline for Testig of Chemicals No. 222.

  • Pandey S, Singh DK (2004) Total bacterial and fungal population after chlorpyrifos and quinalphos treatments in groundnut (Arachis hypogaea L.) soil. Chemosphere 55:197–205

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pitam S, Mukherjee I, Kumar A (2013) Evaluation of environmental fate of acetamiprid in the laboratory. Environ Monit Assess 185:2807–2816

    Article  CAS  Google Scholar 

  • Rao JV, Pavan YS, Madhavendra SS (2003) Toxic effects of chlorpyrifos on morphology and acetylcholinesterase activity in the earthworm, Eisenia foetida. Ecotoxicol Environ Saf 54:296–301

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ren X, Zeng G, Tang L, Wang J, Wan J, Feng H, Song B, Huang C, Tang X (2018) Effect of exogenous carbonaceous materials on the bioavailability of organic pollutants and their ecological risks. Soil Biol Biochem 116:70–81

    Article  CAS  Google Scholar 

  • Rizzati V, Briand O, Guillou H, Gamet-Payrastre L (2016) Effects of pesticide mixtures in human and animal models: an update of the recent literature. Chem Biol Interact 254:231–246

    Article  CAS  Google Scholar 

  • Rundlof M, Andersson GKS, Bommarco R, Fries I, Hederstrom V, Herbertsson L, Jonsson O, Klatt BK, Pedersen TR, Yourstone J, Smith HG (2015) Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521:77–U162

    Article  CAS  Google Scholar 

  • Sakthiselvi T, Paramasivam M, Vasanthi D, Bhuvaneswari K (2020) Persistence, dietary and ecological risk assessment of indoxacarb residue in/on tomato and soil using GC-MS. Food Chem 328:127134

    Article  CAS  Google Scholar 

  • Sarkar M, Roy S, Kole R, Chowdhury A (2001) Persistence and metabolism of imidacloprid in different soils of West Bengal. Pest Manag Sci 57:598–602

    Article  CAS  Google Scholar 

  • Shao X, Xia S, Durkin KA, Casida JE (2013) Insect nicotinic receptor interactions in vivo with neonicotinoid, organophosphorus, and methylcarbamate insecticides and a synergist. Proc Natl Acad Sci U S A 110(43):17273–17277

    Article  Google Scholar 

  • Singh S, Gupta R, Sharma S (2015) Effects of chemical and biological pesticides on plant growth parameters and rhizospheric bacterial community structure in Vigna radiata. J Hazard Mater 291:102–110

    Article  CAS  Google Scholar 

  • Soreq H, Seidman S (2001) Acetylcholinesterase - new roles for an old actor. Nat Rev Neurosci 2:294–302

    Article  CAS  Google Scholar 

  • Stanley DA, Garratt MPD, Wickens JB, Wickens VJ, Potts SG, Raine NE (2015) Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528:548-+

    Article  CAS  Google Scholar 

  • Sun Y, Johnson ER (1960) Analysis of joint action of insecticides against house flies. J Econ Entomol 53:887–892

    Article  CAS  Google Scholar 

  • Sun Y, Diao X, Zhang Q, Shen J (2005) Bioaccumulation and elimination of avermectin B1a in the earthworms (Eisenia fetida). Chemosphere 60:699–704

    Article  CAS  Google Scholar 

  • Tenorio Nunes ME, Gaeta Espindola EL (2012) Sensitivity of Eisenia andrei (Annelida, Oligochaeta) to a commercial formulation of abamectin in avoidance tests with artificial substrate and natural soil under tropical conditions. Ecotoxicology 21:1063–1071

    Article  CAS  Google Scholar 

  • Tomalski M, Leimkuehler W, Schal C, Vargo EL (2010) Metabolism of Imidacloprid in Workers of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 103:84–95

    Article  CAS  Google Scholar 

  • Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247

    Article  CAS  Google Scholar 

  • Utami RR, Geerling GW, Salami IRS, Notodarmojo S, Ragas AMJ (2020) Environmental prioritization of pesticide in the Upper Citarum River Basin, Indonesia, using predicted and measured concentrations. Sci Total Environ 738:140130–140130

    Article  CAS  Google Scholar 

  • Uwizeyimana H, Wang M, Chen W, Khan K (2017) The eco-toxic effects of pesticide and heavy metal mixtures towards earthworms in soil. Environ Toxicol Pharmacol 55:20–29

    Article  CAS  Google Scholar 

  • Van Groenigen JW, Van Groenigen KJ, Koopmans GF, Stokkermans L, Vos HMJ, Lubbers IM (2019) How fertile are earthworm casts? A meta-analysis. Geoderma 338:525–535

    Article  CAS  Google Scholar 

  • Wang K, Pang S, Mu X, Qi S, Li D, Cui F, Wang C (2015) Biological response of earthworm, Eisenia fetida, to five neonicotinoid insecticides. Chemosphere 132:120–126

    Article  CAS  Google Scholar 

  • Woodcock BA, Bullock JM, Shore RF, Heard MS, Pereira MG, Redhead J, Ridding L, Dean H, Sleep D, Henrys P, Peyton J, Hulmes S, Hulmes L, Sarospataki M, Saure C, Edwards M, Genersch E, Knaebe S, Pywell RF (2017) Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356:1393

    Article  CAS  Google Scholar 

  • Worek F, Eyer P, Thiermann H (2012) Determination of acetylcholinesterase activity by the Ellman assay: a versatile tool for in vitro research on medical countermeasures against organophosphate poisoning. Drug Test Anal 4:282–291

    Article  CAS  Google Scholar 

  • Xu B, Xue R, Zhou J, Wen X, Shi Z, Chen M, Xin F, Zhang W, Dong W, Jiang M (2020) Characterization of acetamiprid biodegradation by the microbial consortium ACE-3 enriched from contaminated soil. Front Microbiol 11:1429

    Article  Google Scholar 

  • Xusheng S, Zewen L, Xiaoyong X, Zhong L, Xuhong Q (2013) Overall status of neonicotinoid insecticides in China: production, application and innovation. J Pestic Sci 38:1–9

    Google Scholar 

  • Yang G, Chen Y, Yijun Z, Huiyu W, Wen Y (2018) Combined effects of four pesticides and heavy metal chromium (VI) on the earthworm using avoidance behavior as an endpoint. Ecotoxicol Environ Saf 157:191–200

    Article  CAS  Google Scholar 

  • Zhou Y, Guo J, Wang Z, Zhang B, Sun Z, Yun X, Zhang J (2020) Levels and inhalation health risk of neonicotinoid insecticides in fine particulate matter (PM2.5) in urban and rural areas of China. Environ Int 142:105822

    Article  CAS  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China [grant number 41630645, 41521003].

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Authors and Affiliations

  1. State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Dayang Fang 8#, Beijing, 100012, Chaoyang District, China

    Miaomiao Teng, Xiaoli Zhao, Chen Wang, Lingfeng Zhou, Xiaowei Wu & Fengchang Wu

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  1. Miaomiao Teng
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  2. Xiaoli Zhao
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  3. Chen Wang
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  4. Lingfeng Zhou
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  5. Xiaowei Wu
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Contributions

Miaomiao Teng: investigation; formal analysis; validation; writing original draft. Xiaoli Zhao: conceptualization; investigation; supervision; resources; writing, review and editing. Chen Wang: conceptualization; writing, review and editing. Lingfeng Zhou: investigation; formal analysis. Xiaowei Wu: review and editing. Fengchang Wu: resources; writing—review and editing, project administration.

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Correspondence to Xiaoli Zhao.

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Teng, M., Zhao, X., Wang, C. et al. Combined toxicity of chlorpyrifos, abamectin, imidacloprid, and acetamiprid on earthworms (Eisenia fetida). Environ Sci Pollut Res 29, 54348–54358 (2022). https://doi.org/10.1007/s11356-021-18025-w

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