Skip to main content

Advertisement

SpringerLink
Log in

Toxic effects of benzovindiflupyr, a new SDHI-type fungicide on earthworms (Eisenia fetida)

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

Abstract

Benzovindiflupyr has received increasing attention as a new novel succinate dehydrogenase inhibitor (SDHI)-type fungicide. Nonetheless, its traces remaining in soil potentially trigger an ecotoxicological threat to soil organisms including earthworms. This paper evaluates the eco-toxicity of different benzovindiflupyr doses (0.1, 1, 5, and 10 mg kg−1) on earthworms (Eisenia fetida) after long-term exposure. Consequently, benzovindiflupyr at higher doses significantly inhibited the activities of respiratory chain complex II and succinate dehydrogenase (SDH) in E. fetida. Besides, the reactive oxygen species (ROS) and lipid peroxidation (LPO) were significantly induced in earthworms when treated with this fungicide. After benzovindiflupyr exposure, activities of antioxidant enzymes including catalase, peroxidase, and superoxide dismutase were activated. However, glutathione S-transferase activity in E. fetida was initially induced then inhibited in earthworms after treatment. Furthermore, benzovindiflupyr exposure induced the protein carbonylation (PCO) level in cells indicating oxidative damage to the cellular protein. Due to the destruction of the normal function in the coelomocytes, the phagocytic activity was initially activated, then inhibited when earthworms were treated at 5 and 10 mg kg−1 concentrations. Additionally, DNA damage was induced (larger olive tail moment (OTM) values) with the increase of benzovindiflupyr doses and exposure time. The weight was significantly decreased after benzovindiflupyr exposure on days 21 and 28. Benzovindiflupyr at higher doses significantly decreased the reproduction (number of cocoons and juveniles) of E. fetida. These findings reveal that benzovindiflupyr potentially induces a potential toxicological risk to earthworms when applied in the mentioned above dosages.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

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

References

  • Avenot HF, Michailides TJ (2010) Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi. Crop Prot 29:643–651

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Bulavina L, Szulzewsky F, Rocha A, Krabbe G, Robson SC, Matyash V, Kettenmann H (2013) NTPDase1 activity attenuates microglial phagocytosis. Purinergic Signal 9:199–205

    Article  CAS  Google Scholar 

  • Chen X, Wang X, Gu X, Jiang Y, Ji R (2017) Oxidative stress responses and insights into the sensitivity of the earthworms Metaphire guillelmi and Eisenia fetida to soil cadmium. Sci Total Environ 574:300–306

    Article  CAS  Google Scholar 

  • Cheng Y, Zhu L, Song W, Jiang C, Li B, Du Z, Wang J, Wang J, Li D, Zhang K (2020) Combined effects of mulch film-derived microplastics and atrazine on oxidative stress and gene expression in earthworm (Eisenia fetida). Sci Total Environ 746:141280

    Article  CAS  Google Scholar 

  • Cheng Y, Song W, Tian H, Zhang K, Li B, Du Z, Zhang W, Wang J, Wang J, Zhu L (2021) The effects of high-density polyethylene and polypropylene microplastics on the soil and earthworm Metaphire guillelmi gut microbiota. Chemosphere 267:129219

    Article  CAS  Google Scholar 

  • Dang M, Liu M (2017) A novel fungicide-benzovindiflupyr. Fine Chem Intermed 47:7–10

  • Di Marzio WD, Saenz ME, Lemière S, Vasseur P (2005) Improved single-cell gel electrophoresis assay for detecting DNA damage in Eisenia foetida. Environ Mol Mutagen 46:246–252

    Article  Google Scholar 

  • Dong X, Zhu L, Wang J, Wang J, Xie H, Hou X, Jia W (2009) Effects of atrazine on cytochrome P450 enzymes of zebrafish (Danio rerio). Chemosphere 77:404–412

    Article  CAS  Google Scholar 

  • Edwards C (2004) The importance of earthworms as key representatives of the soil fauna. In: Edwards CA (ed) Earthworm Ecology, second edn. CRC Press, Boca Raton, pp 3–11

    Chapter  Google Scholar 

  • Fantke P, Jolliet O (2016) Life cycle human health impacts of 875 pesticides. Int J Life Cycle Assess 21:722–733

    Article  CAS  Google Scholar 

  • Fazeli F, Ghorbanli M, Niknam V (2007) Effect of drought on biomass, protein content, lipid peroxidation and antioxidant enzymes in two sesame cultivars. Biol Plant 51:98–103

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  Google Scholar 

  • Givaudan N, Binet F, Le Bot B, Wiegand C (2014) Earthworm tolerance to residual agricultural pesticide contamination: field and experimental assessment of detoxification capabilities. Environ Pollut 192:9–18

    Article  CAS  Google Scholar 

  • Gong P, Perkins EJ (2016) Earthworm toxicogenomics: a renewed genome-wide quest for novel biomarkers and mechanistic insights. Appl Soil Ecol 104:12–24

    Article  Google Scholar 

  • Gordon S (2016) Phagocytosis: an immunobiologic process. Immunity 44:463–475

    Article  CAS  Google Scholar 

  • Gurunathan S, Jeyaraj M, Kang M-H, Kim J-H (2019) The effects of Apigenin-biosynthesized ultra-small platinum nanoparticles on the human monocytic THP-1 cell line. Cells 8:444

    Article  CAS  Google Scholar 

  • Han Y, Zhu L, Wang J, Wang J, Xie H, Zhang S (2014) Integrated assessment of oxidative stress and DNA damage in earthworms (Eisenia fetida) exposed to azoxystrobin. Ecotoxicol Environ Safe 107:214–219

    Article  CAS  Google Scholar 

  • He L, Cui K, Song Y, Mu W, Liu F (2018) High-efficiency control of gray mold by the novel SDHI fungicide benzovindiflupyr combined with a reasonable application approach of dipping flower. J Agric Food Chem 66:6692–6698

    Article  CAS  Google Scholar 

  • He L, Li X, Gao Y, Li B, Mu W, Liu F (2019) Oil adjuvants enhance the efficacy of pyraclostrobin in managing cucumber powdery mildew (Podosphaera xanthii) by modifying the affinity of fungicide droplets on diseased leaves. Plant Dis 103:1657–1664

  • Hirano T, Tamae K (2011) Earthworms and soil pollutants. Sensors (Basel) 11:11157–11167

    Article  Google Scholar 

  • Hou Y-P, Chen Y-L, Wu L-Y, Wang J-X, Chen C-J, Zhou M-G (2018) Baseline sensitivity of Bipolaris maydis to the novel succinate dehydrogenase inhibitor benzovindiflupyr and its efficacy. Pestic Biochem Physiol 149:81–88

    Article  CAS  Google Scholar 

  • Hu S, Zhang W, Li J, Lin K, Ji R (2016) Antioxidant and gene expression responses of Eisenia fetida following repeated exposure to BDE209 and Pb in a soil-earthworm system. Sci Total Environ 556:163–168

    Article  CAS  Google Scholar 

  • Ishii H, Zhen F, Hu M, Li X, Schnabel G (2016) Efficacy of SDHI fungicides, including benzovindiflupyr, against Colletotrichum species. Pest Manag Sci 72:1844–1853

    Article  CAS  Google Scholar 

  • IUPAC (International Union of Pure and Applied Chemistry) (2013) Environmental Fate–Ecotoxicology–Human Health–A to Z Index–Home: general information for benzovindiflupyr. http://sitem.herts.ac.uk/aeru/iupac/Reports/2621.htm. Accessed 8 Jan 2019

  • Końca K, Lankoff A, Banasik A, Lisowska H, Kuszewski T, Góźdź S, Koza Z, Wojcik A (2003) A cross-platform public domain PC image-analysis program for the comet assay. Mutat Res 534:15–20

    Article  Google Scholar 

  • Kuznetsov D, Cazenave AB, Rambach O, Camblin P, Nina M, Leipner J (2018) Foliar application of benzovindiflupyr shows non-fungicidal effects in wheat plants. Pest Manag Sci 74:665–671

    Article  CAS  Google Scholar 

  • Lawler JM, Song W, Demaree SR (2003) Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic Biol Med 35:9–16

    Article  CAS  Google Scholar 

  • Leist M, Single B, Naumann H, Fava E, Simon B, Kühnle S, Nicotera P (1999) Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. Exp Cell Res 249:396–403

    Article  CAS  Google Scholar 

  • Li X-Y, Luo Y-R, Yun M-X, Wang J, Wang J-J (2010) Effects of 1-methyl-3-octylimidazolium bromide on the anti-oxidant system of earthworm. Chemosphere 78:853–858

    Article  CAS  Google Scholar 

  • Li L, Yang D, Song Y, Shi Y, Huang B, Bitsch A, Yan J (2017) The potential acute and chronic toxicity of cyfluthrin on the soil model organism, Eisenia fetida. Ecotox Environ Safe 144:456–463

    Article  CAS  Google Scholar 

  • Li M, Ma X, Saleem M, Wang X, Sun L, Yang Y, Zhang Q (2020) Biochemical response, histopathological change and DNA damage in earthworm (Eisenia fetida) exposed to sulfentrazone herbicide. Ecol Indic 115:106465

    Article  CAS  Google Scholar 

  • Liu J (2008) The effects and mechanisms of mitochondrial nutrient alpha-lipoic acid on improving age-associated mitochondrial and cognitive dysfunction: an overview. Neurochem Res 33:194–203

    Article  CAS  Google Scholar 

  • Liu X, Sun Z, Chong W, Sun Z, He C (2009) Growth and stress responses of the earthworm Eisenia fetida to Escherichia coli O157:H7 in an artificial soil. Microb Pathog 46:266–272

    Article  Google Scholar 

  • Liu T, Wang X, Chen D, Li Y, Wang F (2018) Growth, reproduction and biochemical toxicity of chlorantraniliprole in soil on earthworms (Eisenia fetida). Ecotox Environ Safe 150:18–25

    Article  CAS  Google Scholar 

  • Luo S, Wehr NB (2009) Protein carbonylation: avoiding pitfalls in the 2,4-dinitrophenylhydrazine assay. Redox Rep 14:159–166

    Article  CAS  Google Scholar 

  • Ma J, Cheng C, Du Z, Li B, Wang J, Wang J, Wang Z, Zhu L (2019) Toxicological effects of pyraclostrobin on the antioxidant defense system and DNA damage in earthworms (Eisenia fetida). Ecol Indic 101:111–116

    Article  CAS  Google Scholar 

  • Martinez-Fernandez E, Gil-Peralta A, Garcia-Lozano R, Chinchon I, Aguilera I, Fernandez-Lopez O, Arenas J, Campos Y, Bautista J (2001) Mitochondrial disease and stroke. Stroke 32:2507–2510

    Article  CAS  Google Scholar 

  • OECD (2004) Guidelines for testing of chemicals No. 222: earthworm reproduction tests (Eisenia Fetida/Eisenia Andrei). Organisation for Economic Co-operation and Development (OECD), Paris

    Google Scholar 

  • Pirinccioglu AG, Gökalp D, Pirinccioglu M, Kizil G, Kizil M (2010) Malondialdehyde (MDA) and protein carbonyl (PCO) levels as biomarkers of oxidative stress in subjects with familial hypercholesterolemia. Clin Biochem 43:1220–1224

    Article  CAS  Google Scholar 

  • Qiao Z, Zhang F, Yao X, Yu H, Sun S, Li X, Zhang J, Jiang X (2019) Growth, DNA damage and biochemical toxicity of cyantraniliprole in earthworms (Eisenia fetida). Chemosphere 236:124328

    Article  CAS  Google Scholar 

  • Qiao Z, Yao X, Liu X, Zhang J, Du Q, Zhang W, Li X, Jiang X (2021) Transcriptomics and enzymology combined five gene expressions to reveal the responses of earthworms (Eisenia fetida) to the long-term exposure of cyantraniliprole in soil. Ecotox Environ Safe 209:111824

  • Qu B, Zhao H, Zhou J (2010) Toxic effects of perfluorooctane sulfonate (PFOS) on wheat (Triticum aestivum L.) plant. Chemosphere 79:555–560

    Article  CAS  Google Scholar 

  • Shao Y, Hou K, Du Z, Li B, Wang J, Juhasz A, Wang J, Zhu L (2019) Evaluation of the toxicity of 1-butyl-3-methyl imidazolium tetrafluoroborate using earthworms (Eisenia fetida) in two soils. Sci Total Environ 686:946–958

    Article  CAS  Google Scholar 

  • Shi Y-j, Xu X-b, Zheng X-q, Lu Y-l (2015) Responses of growth inhibition and antioxidant gene expression in earthworms (Eisenia fetida) exposed to tetrabromobisphenol A, hexabromocyclododecane and decabromodiphenyl ether. Comp Biochem Physiol C Toxicol Pharmacol 174-175:32–38

    Article  CAS  Google Scholar 

  • Sierotzki H, Scalliet G (2013) A review of current knowledge of resistance aspects for the next-generation succinate dehydrogenase inhibitor fungicides. Phytopathology 103:880–887

    Article  CAS  Google Scholar 

  • Singh S, Eapen S, D’Souza SF (2006) Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62:233–246

    Article  CAS  Google Scholar 

  • Song Y, Zhu LS, Wang J, Wang JH, Liu W, Xie H (2009) DNA damage and effects on antioxidative enzymes in earthworm (Eisenia foetida) induced by atrazine. Soil Biol Biochem 41:905–909

    Article  CAS  Google Scholar 

  • Su G, Zhang X, Raine JC, Xing L, Higley E, Hecker M, Giesy JP, Yu H (2013) Mechanisms of toxicity of triphenyltin chloride (TPTC) determined by a live cell reporter array. Environ Sci Pollut Res Int 20:803–811

    Article  CAS  Google Scholar 

  • Wang K, Mu X, Qi S, Chai T, Pang S, Yang Y, Wang C, Jiang J (2015) Toxicity of a neonicotinoid insecticide, guadipyr, in earthworm (Eisenia fetida). Ecotox Environ Safe 114:17–22

    Article  CAS  Google Scholar 

  • 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 

  • Wiglesworth M, Tally A (2015) SolatenolTM fungicide—a new SDHI fungicide from Syngenta (abstract). Phytopathology 105(Suppl. 2):S2.11–S2.12

    Google Scholar 

  • Xia B, Chen B, Sun X, Qu K, Ma F, Du M (2015) Interaction of TiO2 nanoparticles with the marine microalga Nitzschia closterium: growth inhibition, oxidative stress and internalization. Sci Total Environ 508:525–533

    Article  CAS  Google Scholar 

  • Yan X, Wang J, Zhu L, Wang J, Li S, Kim YM (2021) Oxidative stress, growth inhibition, and DNA damage in earthworms induced by the combined pollution of typical neonicotinoid insecticides and heavy metals. Sci Total Environ 754:141873

    Article  CAS  Google Scholar 

  • Yang Y, Qi S, Wang D, Wang K, Zhu L, Chai T, Wang C (2016) Toxic effects of thifluzamide on zebrafish (Danio rerio). J Hazard Mater 307:127–136

    Article  CAS  Google Scholar 

  • Yang Y, Xiao Y, Chang Y, Cui Y, Klobučar G, Li M (2018) Intestinal damage, neurotoxicity and biochemical responses caused by tris (2-chloroethyl) phosphate and tricresyl phosphate on earthworm. Ecotox Environ Safe 158:78–86

    Article  CAS  Google Scholar 

  • Yao X, Zhang F, Qiao Z, Yu H, Sun S, Li X, Zhang J, Jiang X (2020) Toxicity of thifluzamide in earthworm (Eisenia fetida). Ecotox Environ Safe 188:109880

    Article  CAS  Google Scholar 

  • Ye X, 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 

  • Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B, Kroemer G (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182:367–377

    Article  CAS  Google Scholar 

  • Zhang Q, Zhu L, Wang J, Xie H, Wang J, Han Y, Yang J (2013) Oxidative stress and lipid peroxidation in the earthworm Eisenia fetida induced by low doses of fomesafen. Environ Sci Pollut Res Int 20:201–208

    Article  CAS  Google Scholar 

  • Zhang Q, Zhang G, Yin P, Lv Y, Yuan S, Chen J, Wei B, Wang C (2015) Toxicological effects of soil contaminated with spirotetramat to the earthworm Eisenia fetida. Chemosphere 139:138–145

    Article  CAS  Google Scholar 

  • Zhang C, Zhu L, Wang J, Wang J, Du Z, Li B, Zhou T, Cheng C, Wang Z (2018) Evaluating subchronic toxicity of fluoxastrobin using earthworms (Eisenia fetida). Sci Total Environ 642:567–573

    Article  CAS  Google Scholar 

  • Zhou Y, Liu X, Wang J (2020) Ecotoxicological effects of microplastics and cadmium on the earthworm Eisenia foetida. J Hazard Mater 392:122273

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Jerry from the Home for researcher editorial team (https://www.home-for-researchers.com) for linguistic assistance during manuscript preparation. We sincerely thank the reviewers for their help in improving the quality of the manuscript.

Funding

This study was funded by the National Key R & D Program of China (2018YFD0200604).

Author information

Authors and Affiliations

  1. School of Environmental Science and Engineering, America CRC for Environment & Health, Shandong University, 72# Jimo Binhai Road, Qingdao, Shandong, 266237, People’s Republic of China

    Falin He, Jingqiang Wan, Xiangxiang Li, Shanshan Chu, Ning Sun & Rutao Liu

Authors
  1. Falin He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jingqiang Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiangxiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shanshan Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ning Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rutao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Falin He: conceptualization, methodology, validation, formal analysis, investigation, writing-original draft. Jingqiang Wan: data curation, supervision, writing-review, and editing. Xiangxiang Li, Shanshan Chu, and Ning Sun: formal analysis, review, and editing. Rutao Liu: supervision, conceptualization, writing-review, and editing.

Corresponding author

Correspondence to Falin He.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Chris Lowe

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, F., Wan, J., Li, X. et al. Toxic effects of benzovindiflupyr, a new SDHI-type fungicide on earthworms (Eisenia fetida). Environ Sci Pollut Res 28, 62782–62795 (2021). https://doi.org/10.1007/s11356-021-15207-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-15207-4

Keywords

Search

Navigation