Skip to main content
SpringerLink
Log in

Combined toxicity of imidacloprid, acetochlor, and tebuconazole to zebrafish (Danio rerio): acute toxicity and hepatotoxicity assessment

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

Abstract

Compound pollution refers to two or more kinds of pollutants with different properties, a pollutant from different sources, or the simultaneous existence of two or more different types of pollutants in the same environment. In this study, we aimed to investigate the individual and combined toxicity of the insecticide imidacloprid (IMI), the herbicide acetochlor (ACT), and the fungicide tebuconazole (TBZ) to zebrafish. The acute toxicity test results showed that the 96-h LC50 values of IMI, ACT, and TBZ were 276.84 (259.62–294.35) mg active ingredient (a.i.) L−1, 1.52 (1.34–1.74) mg a.i. L−1, and 8.16 (7.7–8.6) mg a.i. L−1, respectively. The combinations of IMI, ACT, and TBZ with toxicity ratios of 1:2:2, 1:4:4, 2:4:1, and 4:1:4 displayed synergistic toxic effects on zebrafish, while the toxicity ratios of 1:1:1, 1:1:2, 2:1:2, 2:2:1, and 4:2:1 of IMI, ACT, and TBZ, respectively, exhibited antagonistic toxic effects on zebrafish. The following experiments were performed with a toxicity ratio of 1:4:4 (IMI:ACT:TBZ). The activities of four enzyme biomarkers related to oxidative stress in the liver, catalase (CAT), superoxide dismutase (SOD), glutathione S-transferase (GST), and malondialdehyde (MDA) content were evaluated in each exposure group on days 7, 14, 21, and 28. Compared with those of the control group, the activities of CAT, SOD, and GST and the MDA content were significantly altered at different time points in the individual and combined exposure groups. Additionally, the activities of CAT, SOD, and GST and the MDA content were significantly altered in the combined group compared with those of the individual group after 14 days or 21 days of exposure. Therefore, it was confirmed that combined toxicity studies are indispensable in risk assessment.

.

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

Similar content being viewed by others

References

  • Anderson J, Dubetz C, Palace V (2015) Neonicotinoids in the Canadian aquatic environment: a literature review on current use products with a focus on fate, exposure, and biological effects. Sci Total Environ 505:409–422

    CAS  Google Scholar 

  • Bernabò I, Guardia A, Macirella R, Sesti S, Crescente A, Brunelli E (2016) Effects of long-term exposure to two fungicides, pyrimethanil and tebuconazole, on survival and life history traits of Italian tree frog (Hyla intermedia). Aquat Toxicol 172:56–66

    Google Scholar 

  • Castro T, Souza J, Carvalho A, Assis I, Palmieri M, Vieira L, Marcussi S, Machado M, Murgas L (2018) Anxiety- associated behavior and genotoxicity found in adult, Danio rerio, exposed to tebuconazole-based commercial product. Environ Toxicol Phar 62:140–146

    CAS  Google Scholar 

  • Cohen Y, Levy Y (1990) Joint action of fungicides in mixtures: theory and practice. Phytoparasitica 18:159–169

    CAS  Google Scholar 

  • Cui N, Xu H, Yao S, He Y, Zhang H, Yu Y (2018) Chiral triazole fungicide tebuconazole: enantioselective bioaccumulation, bioactivity, acute toxicity, and dissipation in soils. Environ Sci Pollut Res 25:25468–25475

    CAS  Google Scholar 

  • Ding Z, Yang Y, Jin H, Shan Z, Yu H, Feng J, Zhang X, Zhou J (2004) Acute toxicity and bio-concentration factor of three pesticides on Brachydanio rerio. Chin J Appl Ecol 15(5):888–890 (in Chinese)

    CAS  Google Scholar 

  • Foley M, Sigler V, Gruden C (2008) A multiphasic characterization of the impact of the herbicide acetochlor on freshwater bacterial communities. ISME J 2:56–66

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ge W, Yan S, Wang J, Zhu L, Chen A, Wang J (2015) Oxidative stress and DNA damage induced by imidacloprid in zebrafish (Danio rerio). J Agr Food Chem 63:1856–1862

    CAS  Google Scholar 

  • Grung M, Lin Y, Zhang H, Steen A, Huang J, Zhang G, Larssen T (2015) Pesticide levels and environmental risk in aquatic environments in China—a review. Environ Int 81:87–97

    CAS  Google Scholar 

  • Guo D, Wang Y, Qian Y, Chen C, Jiao B, Cai L, Wang Q (2017) Joint acute and endocrine disruptive toxicities of malathion, cypermethrin and prochloraz to embryo-larval zebrafish, Danio rerio. Chemosphere 166:63–71

    CAS  Google Scholar 

  • Hladik M, Bouwer E, Roberts A (2008) Neutral chloroacetamide herbicide degradates and related compounds in Midwestern United States drinking water sources. Sci Total Environ 390:155–165

    CAS  Google Scholar 

  • Hladik M, Kolpin D, Kuivila K (2014) Widespread occurrence of neonicotinoid insecticides in streams in a high corn and soybean producing region, USA. Environ Pollut 193:189–196

    CAS  Google Scholar 

  • Jiang J, Wu S, Liu X, Wang Y, An X, Cai L, Zhao X (2015) Effect of acetochlor on transcription of genes associated with oxidative stress, apoptosis, immunotoxicity and endocrine disruption in the early life stage of zebrafish. Environ Toxicol Phar 40:516–523

    CAS  Google Scholar 

  • Jiang J, Chen Y, Yu R, Zhao X, Wang Q, Cai L (2016) Pretilachlor has the potential to induce endocrine disruption, oxidative stress, apoptosis and immunotoxicity during zebrafish embryo development. Environ Toxicol Phar 42:125–134

    CAS  Google Scholar 

  • Ken C, Hsiung T, Huang Z, Juang R, Lin C (2005) Characterization of Fe/Mn-superoxide dismutase from diatom Thallassiosira weissflogii: cloning, expression, and property. J Agr Food Chem 53:1470–1474

    CAS  Google Scholar 

  • Kolpin D, Nations B, Goolsby D, Thurman E (1996) Acetochlor in the hydrologic system in the Midwestern United States, 1994. Environ Sci Technol 30:1459–1464

    CAS  Google Scholar 

  • Konda L, Pásztor Z (2001) Environmental distribution of acetochlor, atrazine, chlorpyrifos, and propisochlor under field conditions. J Agr Food Chem 49:3859–3863

    CAS  Google Scholar 

  • Kunce W, Josefsson S, Örberg J, Johansson F (2015) Combination effects of pyrethroids and neonicotinoids on development and survival of Chironomus riparius. Ecotox Environ Saf 122:426–431

    CAS  Google Scholar 

  • Li H, Feng Y, Li X, Zeng D (2018) Analytical confirmation of various herbicides in drinking water resources in sugarcane production regions of Guangxi, China. B Environ Contam Tox 100:815–820

    CAS  Google Scholar 

  • Liu N, Dong F, Xu J, Liu X, Zheng Y (2016) Chiral bioaccumulation behavior of tebuconazole in the zebrafish (Danio rerio). Ecotox Environ Saf 126:78–84

    CAS  Google Scholar 

  • Livingstone D (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666

    CAS  Google Scholar 

  • Main A, Headley J, Peru K, Michel N, Cessna A, Morrissey C (2014) Widespread use and frequent detection of neonicotinoid insecticides in wetlands of Canada’s Prairie Pothole Region. PLoS One 9:e92821

    Google Scholar 

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

    Google Scholar 

  • Morrissey C, Mineau P, Devries J, Sanchez-Bayo F, Liess M, Cavallaro M, Liber K (2015) Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: a review. Environ Int 74:291–303

    CAS  Google Scholar 

  • Mu X, Chai T, Wang K, Zhang J, Zhu L, Li X, Wang C (2015) Occurrence and origin of sensitivity toward difenoconazole in zebrafish (Danio reio) during different life stages. Aquat Toxicol 160:57–68

    CAS  Google Scholar 

  • OECD (1992) OECD guidelines for the testing of chemicals no. 203, fish acute toxicity. OECD, Paris

    Google Scholar 

  • Rabiet M, Margoum C, Gouy V, Carluer N, Coquery M (2010) Assessing pesticide concentrations and fluxes in the stream of a small vineyard catchment—effect of sampling frequency. Environ Pollut 158:737–748

    CAS  Google Scholar 

  • Samoucha Y, Gisi U (1987) Possible explanations of synergism in fungicide mixtures against Phytophthora infestans. Ann appl biol 110:303–311

    CAS  Google Scholar 

  • Sancho E, Villarroel M, Ferrando M (2016) Assessment of chronic effects of tebuconazole on survival, reproduction and growth of Daphnia magna after different exposure times. Ecotox Environ Saf 124:10–17

    CAS  Google Scholar 

  • Svensson R, Rinaldi R, Swedmark S, Morgenstern R (2000) Reactivity of cysteine-49 and its influence on the activation of microsomal glutathione transferase 1: evidence for subunit interaction. Biochemistry-US 39:15144–15149

    CAS  Google Scholar 

  • Thuyet D, Watanabe H, Ok J (2013) Effect of pH on the degradation of imidadoprid and fipronil in paddy water. J Pestic Sci 38:223e227

    Google Scholar 

  • Tisler T, Jemec A, Mozetic B, Trebse P (2009) Hazard identification of imidacloprid to aquatic environment. Chemosphere 76:0–914

    CAS  Google Scholar 

  • Toni C, Ferreira D, Kreutz L, Loro V, Barcellos L (2011) Assessment of oxidative stress and metabolic changes in common carp (Cyprinus carpio) acutely exposed to different concentrations of the fungicide tebuconazole. Chemosphere 83:579–584

    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 Phar 55:20–29

    CAS  Google Scholar 

  • Vieira C, Pérez M, Acayaba R, Raimundo C, Martinez C (2018) DNA damage and oxidative stress induced by imidacloprid exposure in different tissues of the Neotropical fish Prochilodus lineatus. Chemosphere 195:125–134

    CAS  Google Scholar 

  • Wang Y, Lv L, Yu Y, Yang G, Xu Z, Wang Q, Cai L (2017) Single and joint toxic effects of five selected pesticides on the early life stages of zebrafish (Denio rerio). Chemosphere 170:61–67

    CAS  Google Scholar 

  • Wang H, Meng Z, Zhou L, Cao Z, Liao X, Ye R, Lu H (2019) Effects of acetochlor on neurogenesis and behaviour in zebrafish at early developmental stages. Chemosphere 220:954–964

    CAS  Google Scholar 

  • Wu Y, Wang C, Wang Y, Zhao Y, Chen Y, Zuo Z (2007) Antioxidant responses to benzo[a]pyrene, tributyltin and their mixture in the spleen of Sebasticus marmoratus. J Environ Sci China 19:1129–1135

    CAS  Google Scholar 

  • Wu C, Liu X-G, He M-Y, Dong F-S, Xu J, Wu X-H, Zheng Y-Q (2017) Acute toxicity and bio-concentration of tebuconazole in Brachydanio rerio. Asian J Ecotoxicol 12:302–309 (in Chinese)

    Google Scholar 

  • Xia X, Xia X, Huo W, Dong H, Zhang L, Chang Z (2016) Toxic effects of imidacloprid on adult loach (Misgurnus anguillicaudatus). Environ Toxicol Phar 45:132–139

    CAS  Google Scholar 

  • Yang M, Hu J, Li S, Ma Y, Gui W, Zhu G (2015) Thyroid endocrine disruption of acetochlor on zebrafish (Danio rerio) larvae. J Appl Toxicol 36:844–852

    Google Scholar 

  • Zhang Q, Hua X, Yang Y, Yin W, Tian M, Shi H, Wang M (2015) Stereoselective degradation of flutriafol and tebuconazole in grape. Environ Sci Pollut Res 22:4350–4358

    CAS  Google Scholar 

  • Zhao L, Zhu X, Wang Y, Jin H, Wang J, Wang C, Lao Y, Jiang Y, Tao Y, Zhou J, Cai Z (2015) The combined toxic effect of nanoscale titanium dioxide (nTiO2) and bisphenol A (BPA) on Scenedesmus obliquus. Asian J Ecotoxicol 10(6):110–120 (in Chinese)

    Google Scholar 

  • Zhou Q, Cheng Y, Zhang Q, Liang J (2004) Quantitative analyses of relationships between ecotoxicological effects and combined pollution. Sci China Ser C 47(4):332–339

    CAS  Google Scholar 

Download references

Acknowledgments

We thank the American Journal Experts (AJE) for the English language editing.

Funding

This work was supported by the National Key Research Development Program of China (No. 2016YFD0200500) and the National Natural Science Foundation of China (31801769).

Author information

Author notes

  1. Yiming Chang and Liangang Mao contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Control of Biological Hazard Factors (Plant Origin) for Agri-product Quality and Safety, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, People’s Republic of China

    Yiming Chang, Liangang Mao, Lan Zhang, Yanning Zhang & Hongyun Jiang

Authors
  1. Yiming Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liangang Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanning Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hongyun Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hongyun Jiang.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chang, Y., Mao, L., Zhang, L. et al. Combined toxicity of imidacloprid, acetochlor, and tebuconazole to zebrafish (Danio rerio): acute toxicity and hepatotoxicity assessment. Environ Sci Pollut Res 27, 10286–10295 (2020). https://doi.org/10.1007/s11356-020-07653-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-07653-3

Keywords

Search

Navigation