Skip to main content

Advertisement

SpringerLink
Log in

Effects of perfluorooctanoic acid and perfluorooctane sulfonate on acute toxicity, superoxide dismutase, and cellulase activity in the earthworm Eisenia fetida

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

Abstract

Perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) are the two best-known perfluorinated chemicals and have received much attention due to their ubiquity in the environment. In the present study, we evaluated the effects of PFOS and PFOA on acute toxicity, superoxide dismutase (SOD), and cellulase activities in Eisenia fetida. The results of acute toxicity testing using a filter paper contact test and a natural field soil test showed that PFOA and PFOS exhibited acute toxicity in earthworms, and the toxic effect of PFOS was greater than that of PFOA. The results also showed that avoidance behavior is a more sensitive and easy operation biomarker than acute toxicity and will give us information for early diagnosis of soil pollution, well before the lethal effect becomes apparent. Subchronic exposure to PFOA or PFOS resulted in changes in SOD and cellulase activities in E. fetida, and SOD activity was more sensitive than cellulase activity during early exposure. Based on these findings, we suggest that avoidance behavior and SOD activity in earthworms are suitable biomarkers for evaluating the toxicity of PFOA- and PFOS-contaminated soils. These results indicate that exposure to PFOA and PFOS has a potential impact on soil animals and their environment.

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

References

  • Amorim MJ, Römbke J, Soares AM (2005) Avoidance behaviour of Enchytraeus albidus: effects of benomyl, carbendazim, phenmedipham and different soil types. Chemosphere 59:501–510

    Article  CAS  Google Scholar 

  • Arias EVA, Mallavarapu M, Naidu R (2015) Identification of the source of PFOS and PFOA contamination at a military air base site. Environ Monit Assess 187:4111

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Butenhoff JL, Gaylor DW, Moore JA, Olsen GO, Rodricks J, Mande JH, Zobel LR (2004) Characterization of risk for general population exposure to perfluorooctaneoate. Regul Toxicol Pharmacol 39:363–380

    Article  CAS  Google Scholar 

  • Butenhoff JL, Chang SC, Olsen GW, Thomford PJ (2012) Chronic dietary toxicity and carcinogenicity study with potassium perfluorooctanesulfonate in Sprague Dawley rats. Toxicology 293:1–15

    Article  CAS  Google Scholar 

  • Cao H, Shi CL, Jia XY (2012) Cadmium exposure to shading frog testis induced and its effect on the protein oxidative damage mechanism of ROS. Acta Ecol Sin 32:4199–4206

    Article  CAS  Google Scholar 

  • Edwards CA (2004) Earthworm ecology. CRC Press, Boca Raton

    Book  Google Scholar 

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

    CAS  Google Scholar 

  • Grandjean P, Andersen EW, Budtz-Jorgensen E, Nielsen F, Molbak K, Weihe P, Heilmann C (2012) Serum vaccine antibody concentrations in children exposed to perfluorinated compounds. JAMA 307:391–397

    Article  CAS  Google Scholar 

  • Hayashi Y, Engelmann P, Foldbjerg R, Szabo M, Somogyi I, Pollak E, Molnar L, Autrup H, Sutherland DS, Scott-Fordsmand J, Heckmann LH (2012) Earthworms and humans in vitro: characterizing evolutionarily conserved stress and immune responses to silver nanoparticles. Environ Sci Technol 46:4166–4173

    Article  CAS  Google Scholar 

  • He W, Megharaj M, Naidu R (2016) Toxicity of perfluorooctanoic acid towards earthworm and enzymatic activities in soil. Environ Monit Assess 188(7):424

    Article  Google Scholar 

  • ISO (2004) Draft: soil quality–avoidance test for evaluating the quality of soils and the toxicity of chemicals. Test with earthworms (Eisenia fetida/andrei). International Organization for Standardization, Geneva

    Google Scholar 

  • Johansson N, Fredriksson A, Eriksson P (2008) Neonatal exposure to perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) causes neurobehavioural defects in adult mice. Neurotoxicology 29(1):160–169

    Article  CAS  Google Scholar 

  • Kula C (1998) Endpoints in laboratory testing with earthworms: experience with regard to regulatory decisions for plant protection products. In: Sheppard S, Bembridge J, Holmstrup M, Posthuma L (eds) Advances in earthworm ecotoxicology. SETAC Press, Pensacola, pp 3–14

    Google Scholar 

  • Li MH (2009) Toxicity of perfluorooctane sulfonate and perfluorooctanoic acid to plants and aquatic invertebrates. Environ Toxicol 24:95–101

    Article  Google Scholar 

  • Lin AY, Panchangam SC, Tsai YT, Yu TH (2014) Occurrence of perfluorinated compounds in the aquatic environment as found in science park effluent, river water, rainwater, sediments, and biotissues. Environ Monit Assess 186:3265–3275

    Article  CAS  Google Scholar 

  • Luebker DJ, York RG, Hansen KJ, Moore JA, Butenhoff JL (2005) Neonatal mortality from in utero exposure to perfluorooctanesulfonate (PFOS) in Sprague-Dawley rats: dose-response, and biochemical and pharmacokinetic parameters. Toxicology 215:149–169

    Article  CAS  Google Scholar 

  • Ma L, Liu H, Qu H, Xu Y, Wang P, Sun M, Zhou Z, Liu D (2016) Chiral quizalofop-ethyl and its metabolite quizalofop-acid in soils: enantioselective degradation, enzymes interaction and toxicity to Eisenia foetida. Chemosphere 152:173–180

    Article  CAS  Google Scholar 

  • Malinverno G, Colombo I, Visca M (2005) Toxicological profile of hydrofluoropolyethers. Regul Toxicol Pharmacol 41:228–239

    Article  CAS  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474

    Article  CAS  Google Scholar 

  • Mayilswami S, Krishnan K, Megharaj M, Naidu R (2014) Chronic PFOS exposure alters the expression of neuronal development-related human homologues in Eisenia fetida. Ecotoxicol Environ Saf 110:288–297

    Article  CAS  Google Scholar 

  • Mayilswami S, Krishnan K, Megharaj M, Naidu R (2016) Gene expression profile changes in Eisenia fetida chronically exposed to PFOA. Ecotoxicology 25(4):759–769

    Article  CAS  Google Scholar 

  • OECD (1984) Earthworm acute toxicity tests, guidelines for the testing of chemicals. No.207. OECD, Paris

    Book  Google Scholar 

  • OECD (2006) Results of the 2006 survey on production and use of PFOS, PFAS, PFOA, PFCA, their related substances and products/mixtures containing these substances. In: Environment Directorate Joint Meeting of the Chemicals Committee and the Working Party on Chemicals, P.a.B. (Ed.)

  • Routti H, Krafft BA, Herzke D, Eisert R, Oftedal O (2015) Perfluoroalkyl substances detected in the world’s southernmost marine mammal, the Weddell seal (Leptonychotes weddellii). Environ Pollut 197:62–67

    Article  CAS  Google Scholar 

  • Schaefer R, Achazi R (2004) Toxicity of hexyl to F. candida and E. crypticus. J Soils Sediments 4:157–162

    Article  CAS  Google Scholar 

  • Schuetze A, Heberer T, Effkemann S, Juergensen S (2010) Occurrence and assessment of perfluorinated chemicals in wild fish from Northern Germany. Chemosphere 78:647–652

    Article  CAS  Google Scholar 

  • Shi Y, Shi Y, Wang X, Lu Y, Yan S (2007) Comparative effects of lindane and deltamethrin on mortality, growth, and cellulase activity in earthworms (Eisenia fetida). Pestic Biochem Phys 89:31–38

    Article  CAS  Google Scholar 

  • Spurgeon DJ, Weeks JM, Van Gestel CAM (2003) A summary of eleven years progress in earthworm ecotoxicology. Pedobiologia 47:588–606

    Google Scholar 

  • Van Asselt ED, Kowalczyk J, van Eijkeren JCH, Zeilmaker MJ, Ehlers S, Fürst P, Lahrssen-Wiederholt M, van der Fels-Klerx HJ (2013) Transfer of perfluorooctane sulfonic acid (PFOS) from contaminated feed to dairy milk. Food Chem 141:1489–1495

    Article  Google Scholar 

  • Wang XF, Chen WH, Zhang Z, Chen HG, Jia XP (2013) Effects of water-borne mercury and cadmium exposure on lipid peroxidation and antioxidant enzymes in mangrove red snapper Lutjanus argentimaculatus. Res J Appl Sci Eng Technol 6:2395–2401

    CAS  Google Scholar 

  • Wen B, Zhang H, Li L, Hu X, Liu Y, Shan XQ, Zhang S (2015) Bioavailability of perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) in biosolids-amended soils to earthworms (Eisenia fetida). Chemosphere 118:361–366

    Article  CAS  Google Scholar 

  • Xiao N, Jing B, Ge F, Liu X (2006) The fate of herbicide acetochlor and its toxicity to Eisenia fetida under laboratory conditions. Chemosphere 62:1366–1373

    Article  CAS  Google Scholar 

  • Xu D, Li C, Wen Y, Liu W (2013) Antioxidant defense system responses and DNA damage of earthworms exposed to perfluorooctane sulfonate (PFOS). Environ Pollut 174:121–127

    Article  CAS  Google Scholar 

  • Yuan ZQ, Zhang JY, Meng W, Zhou Y (2014) Effects of perfluorooctane sulfonate on behavioral activity, regeneration and antioxidant enzymes in planarian Dugesia japonica. Chem Ecol 30:187–195

    Article  CAS  Google Scholar 

  • Yuan ZQ, Zhang JY, Zhang YL, Zhen H, Sun YQ (2015) The effect of perfluorooctanoic acid on the planarian Dugesia japonica. Pol J Environ Stud 24:801–807

    Article  CAS  Google Scholar 

  • Zhang H, Pan LQ, Tao YX (2014) Antioxidant responses in clam Venerupis philippinarum exposed to environmental pollutant hexabromocyclododecane. Environ Sci Pollut Res 21:8206–8215

    Article  CAS  Google Scholar 

  • Zheng XM, Liu HL, Shi W, Wei S, Giesy JP, Yu HX (2011) Effects of perfluorinated compounds on development of zebrafish embryos. Environ Sci Pollut Res Int 19:2498–2505

    Article  Google Scholar 

  • Zheng K, Liu Z, Li Y, Cui Y, Li M (2013) Toxicological responses of earthworm (Eisenia fetida) exposed to metal-contaminated soils. Environ Sci Pollut Res Int 20:8382–8390

    Article  CAS  Google Scholar 

  • Zheng XQ, Shi YJ, Lu YL, Xu XB (2016) Growth inhibition and DNA damage in the earthworm (Eisenia fetida) exposed to perfluorooctane sulphonate and perfluorooctanoic acid. Chem Ecol 32(2):103–116

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the members of our laboratory for the suggestions and encouragement. Research was supported by the National Nature Science Foundation of China (grant no. 41201518, 31100377) and a Project of Shandong Province Higher Educational Science and Technology Program (grant no. J16LE02).

Author information

Authors and Affiliations

  1. School of Life Sciences, Shandong University of Technology, 12 Zhangzhou Road, Zibo, People’s Republic of China

    Zuoqing Yuan, Jianyong Zhang, Lili Zhao, Jing Li & Hongbin Liu

Authors
  1. Zuoqing Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianyong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lili Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hongbin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jianyong Zhang.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yuan, Z., Zhang, J., Zhao, L. et al. Effects of perfluorooctanoic acid and perfluorooctane sulfonate on acute toxicity, superoxide dismutase, and cellulase activity in the earthworm Eisenia fetida . Environ Sci Pollut Res 24, 18188–18194 (2017). https://doi.org/10.1007/s11356-017-9477-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-9477-4

Keywords

Search

Navigation