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Combined toxicity of imidacloprid and three insecticides to the earthworm, Eisenia fetida (Annelida, Oligochaeta)

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Abstract

Although the earthworm Eisenia fetida has been used in many ecotoxicological studies in recent years, most of these studies have only focused on assessing the effects of individual insecticides. In the present study, we aimed to compare the individual and combined toxic effects of imidacloprid and three insecticides (phoxim, chlorpyrifos, and lambda-cyhalothrin) on E. fetida. We showed that imidacloprid had the highest intrinsic toxicity to the worms in filter paper contact test, followed by phoxim and lambda-cyhalothrin, while the least toxicity was found from chlorpyrifos. Moreover, 14-day soil toxicity test revealed that the highest toxicity was still detected for imidacloprid with an LC50 value of 2.82 (2.61∼3.17) mg a.i. kg−1 dry weight (DW), followed by chlorpyrifos with an LC50 value of 384.9 (353.5∼440.3) mg a.i. kg−1 DW. Meanwhile, a relatively less toxicity was found for lambda-cyhalothrin with an LC50 value of 560.3 (475.9∼718.5) mg a.i. kg−1 DW, while the lowest toxicity to E. fetida was observed for phoxim with an LC50 value of 901.5 (821.3∼1017) mg a.i. kg−1 DW. In addition, significant synergistic responses were found from the ternary mixture of imidacloprid-phoxim-lambda-cyhalothrin and quaternary mixture of imidacloprid-phoxim-chlorpyrifos-lambda-cyhalothrin in both bioassay systems. Therefore, our findings highlighted that the simultaneous presence of several insecticides in the soil environment might lead to increased toxicity, resulting in serious damage to the nontarget organisms compared with individual insecticides.

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References

  • Ahmad M (2004) Potentiation/antagonism of deltamethrin and cypermethrin with organophosphate insecticides in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Pestic Biochem Phys 80:31–42

    Article  CAS  Google Scholar 

  • Bednarska AJ, Choczyński M, Laskowski R, Walczak M (2017) Combined effects of chlorpyriphos, copper and temperature on acetylcholinesterase activity and toxicokinetics of the chemicals in the earthworm Eisenia fetida. Environ Pollut 220(Part A):567–576

    Article  CAS  Google Scholar 

  • Calisi A, Lionetto MG, Schettino T (2011) Biomarker response in the earthworm Lumbricus terrestris exposed to chemical pollutants. Sci Total Environ 409:4456–4464

    Article  CAS  Google Scholar 

  • Chen C, Wang YH, Qian YZ, Zhao XP, Wang Q (2015) The synergistic toxicity of the multiple chemical mixtures: implications for risk assessment in the terrestrial environment. Environ Int 77:95–105

    Article  CAS  Google Scholar 

  • Chi H (1997) Computer program for the probit analysis. National Chung Hsing University, Taichung

    Google Scholar 

  • Elhalwagy MEA, Zaki NI (2009) Comparative study on pesticide mixture of organophosphorus and pyrethroid in commercial formulation. Environ Toxicol Phar 28:219–224

    Article  CAS  Google Scholar 

  • Ellis SR, Hodson ME, Wege P (2010) The soil-dwelling earthworm Allolobophora chlorotica modifies its burrowing behaviour in response to carbendazim applications. Ecotoxicol Environ Saf 73:1424–1428

    Article  CAS  Google Scholar 

  • Environmental Protection Agency (EPA), U.S (1994) ECO update: catalogue of standard toxicity tests for ecological risk assessment. Intermittent Bull 2:1–4

    Google Scholar 

  • Furlan L, Kreutzweiser D (2015) Alternatives to neonicotinoid insecticides for pest control: case studies in agriculture and forestry. Environ Sci Pollut R 22:135–147

    Article  CAS  Google Scholar 

  • Garcia M, Scheffczyk A, Garcia T, Römbke J (2011) The effects of the insecticide lambda-cyhalothrin on the earthworm Eisenia fetida under experimental conditions of tropical and temperate regions. Environ Pollut 159:398–400

    Article  CAS  Google Scholar 

  • Gaughan LC, Engel JL, Casida JE (1980) Pesticide interactions: effects of organophosphorus pesticides on the metabolism, toxicity, and persistence of selected pyrethroid insecticides. Pestic Biochem Phys 14:81–85

    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 

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

    Article  Google Scholar 

  • Hernández AF, Parrón T, Tsatsakis AM, Requena M, Alarcón R, López-Guarnido O (2013) Toxic effects of pesticide mixtures at a molecular level: their relevance to human health. Toxicology 307:136–145

    Article  Google Scholar 

  • Jovana M, Tanja M, Mirjana S (2014) Effects of three pesticides on the earthworm Eisenia fetida (Savigny 1826) under laboratory conditions: assessment of mortality, biomass and growth inhibition. Eur J Soil Biol 62:127–131

    Article  CAS  Google Scholar 

  • Koutsaftis A, Aoyama I (2007) Toxicity of four antifouling biocides and their mixtures on the brine shrimp Artemia salina. Sci Total Environ 387:166–174

    Article  CAS  Google Scholar 

  • Levi PE, Hollingworth RM, Hodgson E (1988) Differences in oxidative dearylation and desulfuration of fenitrothion by cytochrome P-450 isozymes and in the subsequent inhibition of monooxygenase activity. Pestic Biochem Phys 32:224–231

    Article  CAS  Google Scholar 

  • Lister LJ, Svendsen C, Wright J, Hooper HL, Spurgeon DJ (2011) Modelling the joint effects of a metal and a pesticide on reproduction and toxicokinetics in Lumbricid earthworms. Environ Int 37:663–670

    Article  CAS  Google Scholar 

  • Lydy M, Belden J, Wheelock C, Hammock B, Denton D (2004) Challenges in regulating pesticide mixtures. Ecol Soc 9:1

    Article  Google Scholar 

  • Marking LL (1985) Toxicity of chemical mixtures. In: Rand G, Petroceli S (eds) Fundamentals of aquatic toxicology. Hemisphere Publishing Corporation, Washington, DC, pp 164–176

    Google Scholar 

  • Mayer FL, Ellersieck MR, Slaughter AR (2011) Accuracy assessment of time concentration-effect models in predicting chronic lethality from acute toxicity data. Environ Toxicol Chem 30:757–762

    Article  CAS  Google Scholar 

  • Morcillo SM, Yela JL, Capowiez Y, Mazzia C, Rault M, Sanchez-Hernandez JC (2013) Avoidance behaviour response and esterase inhibition in the earthworm, Lumbricus terrestris, after exposure to chlorpyrifos. Ecotoxicology 22:597–607

    Article  Google Scholar 

  • Mostert MA, Schoeman AS, van der Merwe M (2002) The relative toxicities of insecticides to earthworms of the Pheretima group (Oligochaeta). Pest Manag Sci 58:446–450

    Article  CAS  Google Scholar 

  • OECD Guideline for Testing of Chemicals No. 207 (1984) Earthworm acute toxicity. OECD, Paris

    Google Scholar 

  • Piola L, Fuchs J, Oneto ML, Basack S, Kesten E, Casabé N (2013) Comparative toxicity of two glyphosate-based formulations to Eisenia andrei under laboratory conditions. Chemosphere 91:545–551

    Article  CAS  Google Scholar 

  • Qv XY, Jiang JG (2013) Toxicity evaluation of two typical surfactants to Dunaliella bardawil, an environmentally tolerant alga. Environ Toxicol Chem 32:426–433

    Article  CAS  Google Scholar 

  • Rich CD, Blaine AC, Hundal L, Higgins CP (2015) Bioaccumulation of perfluoroalkyl acids by earthworms (Eisenia fetida) exposed to contaminated soils. Environ Sci Technol 49:881–888

    Article  CAS  Google Scholar 

  • Rico A, Sabater C, Castillo MÁ (2016) Lethal and sub-lethal effects of five pesticides used in rice farming on the earthworm Eisenia fetida. Ecotoxicol Environ Saf 127:222–229

    Article  CAS  Google Scholar 

  • Roberts BL, Dorough HW (1984) Relative toxicities of chemicals to the earthworm Eisenia foetida. Environ Toxicol Chem 3:67–78

    Article  CAS  Google Scholar 

  • Santos MJG, Ferreira V, Soares AMVM, Loureiro S (2011) Evaluation of the combined effects of dimethoate and spirodiclofen on plants and earthworms in a designed microcosm experiment. Appl Soil Ecol 48:294–300

    Article  Google Scholar 

  • Santos MJG, Soares AMVM, Loureiro S (2010) Joint effects of three plant protection products to the terrestrial isopod Porcellionides pruinosus and the collembolan Folsomia candida. Chemosphere 80:1021–1030

    Article  CAS  Google Scholar 

  • Schnug L, Ergon T, Jakob L, Scott-Fordsmand JJ, Joner EJ, Leinaas HP (2015) Responses of earthworms to repeated exposure to three biocides applied singly and as a mixture in an agricultural field. Sci Total Environ 505:223–235

    Article  CAS  Google Scholar 

  • Schnug L, Jakob L, Hartnik T (2013) The toxicity of a ternary biocide mixture to two consecutive earthworm (Eisenia fetida) generations. Environ Toxicol Chem 32:937–947

    Article  CAS  Google Scholar 

  • Schnug L, Leinaas HP, Jensen J (2014) Synergistic sub-lethal effects of a biocide mixture on the springtail Folsomia fimetaria. Environ Pollut 186:158–164

    Article  CAS  Google Scholar 

  • Slaughter AR, Palmer CG, Muller WJ (2007) An assessment of two-step linear regression and multifactor probit analysis as alternatives to acute to chronic ratios in the estimation of chronic response from acute toxicity data to derive water quality guidelines. Integr Environ Assess Manag 3:193–202

    Article  CAS  Google Scholar 

  • Stepić S, Hackenberger BK, Velki M, Lončarić Ž, Hackenberger DK (2013) Effects of individual and binary-combined commercial insecticides endosulfan, temephos, malathion and pirimiphos-methyl on biomarker responses in earthworm Eisenia andrei. Environ Toxicol Phar 36:715–723

    Article  Google Scholar 

  • Su L, Zhang X, Yuan X, Zhao Y, Zhang D, Qin W (2012) Evaluation of joint toxicity of nitroaromatic compounds and copper to Photobacterium phosphoreum and QSAR analysis. J Hazard Mater 241-242:450–455

    Article  CAS  Google Scholar 

  • Svartz GV, Aronzon CM, Coll CSP (2016) Combined endosulfan and cypermethrin-induced toxicity to embryo-larval development of Rhinell arenarum. J Toxicol Environ Heal Part A 79:197–209

    Article  CAS  Google Scholar 

  • Svendsen C, Siang P, Lister LJ, Rice A, Spurgeon DJ (2010) Similarity, independence, or interaction for binary mixture effects of nerve toxicants for the nematode Caenorhabditis elegans. Environ Toxicol Chem 29:1182–1191

    CAS  Google Scholar 

  • Thompson HM (1996) Interactions between pesticides: a review of reported effects and their implications for wildlife risk assessment. Ecotoxicology 5:59–81

    Article  CAS  Google Scholar 

  • Velki M, Hackenberger BK (2012) Species-specific differences in biomarker responses in two ecologically different earthworms exposed to the insecticide dimethoate. Comp Biochem Phys Part C 156:104–112

    CAS  Google Scholar 

  • Velki M, Hackenberger BK (2013) Biomarker responses in earthworm Eisenia andrei exposed to pirimiphos-methyl and deltamethrin using different toxicity tests. Chemosphere 90:1216–1226

    Article  CAS  Google Scholar 

  • Velki M, Hackenberger BK, Lončarić Ž, Hackenberger DK (2014) Application of microcosmic system for assessment of insecticide effects on biomarker responses in ecologically different earthworm species. Ecotoxicol Environl Saf 104:110–119

    Article  CAS  Google Scholar 

  • Wang K, Mu XY, Qi SZ, Chai TT, Pang S, Yang Y, Wang CJ, Jiang JZ (2015b) Toxicity of a neonicotinoid insecticide, guadipyr, in earthworm (Eisenia fetida). Ecotoxicol Environ Saf 114:17–22

    Article  CAS  Google Scholar 

  • Wang K, Pang S, Mu XY, Qi SZ, Li DZ, Cui F, Wang CJ (2015a) Biological response of earthworm, Eisenia fetida, to five neonicotinoid insecticides. Chemosphere 132:120–126

    Article  CAS  Google Scholar 

  • Wang Y, Cang T, Yu R, Wu S, Liu X, Chen C, Wang Q, Cai L (2016) Joint acute toxicity of the herbicide butachlor and three insecticides to the terrestrial earthworm, Eisenia fetida. Environ Sci Pollut R 23:11766–11776

    Article  CAS  Google Scholar 

  • Wang Y, Cang T, Zhao X, Yu R, Chen L, Wu C, Wang Q (2012a) Comparative acute toxicity of twenty-four insecticides to earthworm, Eisenia fetida. Ecotoxicol Environ Saf 79:122–128

    Article  CAS  Google Scholar 

  • Wang Y, Chen C, Qian Y, Zhao X, Wang Q (2015a) Ternary toxicological interactions of insecticides, herbicides, and a heavy metal on the earthworm, Eisenia fetida. J Hazard Mater 284:233–240

    Article  CAS  Google Scholar 

  • Wang Y, Chen C, Qian Y, Zhao X, Wang Q, Kong X (2015b) Toxicity of mixtures of λ-cyhalothrin, imidacloprid and cadmium on the earthworm Eisenia fetida by combination index (CI)-isobologram method. Ecotoxicol Environ Saf 111:242–247

    Article  CAS  Google Scholar 

  • Wang Y, Wu S, Chen L, Wu C, Yu R, Wang Q, Zhao X (2012b) Toxicity assessment of 45 pesticides to the epigeic earthworm Eisenia fetida. Chemosphere 88:484–491

    Article  CAS  Google Scholar 

  • Ye XQ, Xiong K, Liu J (2016) Comparative toxicity and bioaccumulation of fenvalerate and esfenvalerate to earthworm Eisenia fetida. J Hazard Mater 310:82–88

    Article  CAS  Google Scholar 

  • Yu W, Du J, Hu Y, Shen R, Mu W (2012) Toxicity of six insecticides to black cutworm Agrotis ypsilon (Rottemberg) and safety evaluation to soil organisms. Acta Phytophylacica Sinica 39:277–282

    CAS  Google Scholar 

  • Zhang QM, Zhang BH, Wang CX (2014) Ecotoxicological effects on the earthworm Eisenia fetida following exposure to soil contaminated with imidacloprid. Environ Sci Pollut R 21:12345–12353

    Article  CAS  Google Scholar 

  • Zhou SP, Duan CQ, Michelle WHG, Yang FZ, Wang XH (2011) Individual and combined toxic effects of cypermethrin and chlorpyrifos on earthworm. J Environ Sci 23:676–680

    Article  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge the help provided by Weihua Yu and Lizhi Yang (Zhejiang Academy of Agricultural Sciences) in the laboratorial experiments. The study was funded by National Natural Science Foundation of China (Grant Nos. 31401767 and 31572028), Zhejiang Province Key Research and Development Project (Grant No. 2015C02043), and Zhejiang Province Major Bidding Project (Grant No. 2014C02002).

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Correspondence to Yanhua Wang.

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Cang, T., Dai, D., Yang, G. et al. Combined toxicity of imidacloprid and three insecticides to the earthworm, Eisenia fetida (Annelida, Oligochaeta). Environ Sci Pollut Res 24, 8722–8730 (2017). https://doi.org/10.1007/s11356-017-8627-z

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