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Toxicological responses of earthworm (Eisenia fetida) exposed to metal-contaminated soils

  • Contaminated Land, Ecological Assessment and Remediation Conference Series (CLEAR 2012) : Environmental Pollution and Risk Assessments
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Abstract

The aim of this study was to evaluate the toxicological responses of earthworm (Eisenia fetida) induced by field-contaminated, metal-polluted soils. Biochemical responses and DNA damage of earthworm exposed to two multi-metal-contaminated soils in a steel industry park and a natural reference soil in Zijin Mountain for 2, 7, 14, and 28 days were studied. Results showed that three enzyme activities, including superoxide dismutase (SOD), acetylcholinesterase (AChE), and cellulase, in earthworm in metal-contaminated soils were significantly different from those of the reference soil. Cellulase and AChE were more sensitive than SOD to soil contamination. The Olive tail moment of the comet assay after 2-day exposure increased 56.5 and 552.0 % in two contaminated soils, respectively, compared to the reference soil. Our findings show that cellulase and DNA damage levels can be used as potential biomarkers for exposure of earthworm to metal-polluted soils.

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References

  • Alvarenga P, Palma P, Gonçalves AP, Fernandes RM, Varennes A, Vallini G, Duarte E, Cunha-Queda AC (2008) Evaluation of tests to assess the quality of mine-contaminated soils. Environ Geochem Hlth 30(2):95–99. doi:10.1007/s10653-008-9147-z

    Article  CAS  Google Scholar 

  • Barillet S, Buet A, Adam C, Devaux A (2005) Does uranium exposure induce genotoxicity in the teleostean Danio rerio? First experimental results. Radioprotection 40:175–181. doi:10.1051/radiopro:2005s1-028

    Article  Google Scholar 

  • Basta NT, Ryan JA, Chaney RL (2005) Trace element chemistry in residual-treated soil: key concepts and metal bioavailability. J Environ Qual 34(1):49–63

    CAS  Google Scholar 

  • Beauvais SL, Jones SB, Parris JT, Brewer SK, Little EE (2001) Cholinergic and behavioral neurotoxicity of carbaryl and cadmium to larval rainbow trout (Oncorhynchus mykiss). Ecotox Environ Safe 49(1):84–90. doi:10.1006/eesa.2000.2032

    Article  CAS  Google Scholar 

  • Berthelot Y, Valton É, Auroy A, Trottier B, Robidoux PY (2008) Integration of toxicological and chemical tools to assess the bioavailability of metals and energetic compounds in contaminated soils. Chemosphere 74(1):166–177. doi:10.1016/j.chemosphere.2008.07.056

    Article  CAS  Google Scholar 

  • Bigorgne E, Cossu-Leguille C, Bonnard M, Nahmani J (2010) Genotoxic effects of nickel, trivalent and hexavalent chromium on the Eisenia fetida earthworm. Chemosphere 80(9):1109–1112. doi:10.1016/j.chemosphere.2010.05.039

    Article  CAS  Google Scholar 

  • Bonnard M, Devin S, Leyval C, Morel JL, Vasseur P (2010) The influence of thermal desorption on genotoxicity of multipolluted soil. Ecotox Environ Safe 73(5):955–960. doi:10.1016/j.ecoenv.2010.02.023

    Article  CAS  Google Scholar 

  • Bonnard M, Eom I-C, Morel J-L, Vasseur P (2009) Genotoxic and reproductive effects of an industrially contaminated soil on the earthworm Eisenia fetida. Environ Mol Mutagen 50(1):60–67. doi:10.1002/em.20436

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Anal Biochem 72(1–2):248–254. doi:10.1006/abio.1976.9999

    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(20):4456–4464. doi:10.1016/j.scitotenv.2011.06.058

    Article  CAS  Google Scholar 

  • Capowiez Y, Rault M, Mazzia C, Belzunces L (2003) Earthworm behaviour as a biomarker—a case study using imidacloprid. Pedobiologia 47(5–6):542–547. doi:10.1078/0031-4056-00226

    Google Scholar 

  • Chakra Reddy N, Venkateswara Rao J (2008) Biological response of earthworm, Eisenia foetida (Savigny) to an organophosphorous pesticide, profenofos. Ecotox Environ Safe 71(2):574–582. doi:10.1016/j.ecoenv.2008.01.003

    Article  CAS  Google Scholar 

  • Chang LW, Meier JR, Smith MK (1997) Application of plant and earthworm bioassays to evaluate remediation of a lead-contaminated soil. Arch Environ Con Tox 32(2):166–171. doi:10.1007/s002449900170

    Article  CAS  Google Scholar 

  • Ching EWK, Siu WHL, Lam PKS, Xu LH, Zhang YY, Richardson BJ, Wu RSS (2001) DNA adduct formation and DNA strand breaks in green-lipped mussels (Perna viridis) exposed to benzo[a]pyrene: dose- and time-dependent relationships. Mar Pollut Bull 42(7):603–610. doi:10.1016/s0025-326x(00)00209-5

    Article  CAS  Google Scholar 

  • Collins AR (2004) The comet assay for DNA damage and repair principles, applications, and limitations. Mol Biotechnol 26:249–261. doi:10.1385/MB:26:3:249

    Article  CAS  Google Scholar 

  • Collins AR, Ma AG, Duthie SJ (1995) The kinetics of repair of oxidative DNA-damage (strand breaks and oxidized pyrimidines) in human-cells. Mutat Res-dna Repair 336(1):69–77. doi:10.1016/0921-8777(94)00043-6

    Article  CAS  Google Scholar 

  • Dayton EA, Basta NT, Payton ME, Bradham KD, Schroder JL, Lanno RP (2006) Evaluating the contribution of soil properties to modifying lead phytoavailability and phytotoxicity. Environ Toxicol Chem 25(3):719–725. doi:10.1897/05-307r.1

    Article  CAS  Google Scholar 

  • Dhindsa RS, Plumbdhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane-permeability and lipid-peroxidation, and decreased levels of superoxide-dismutase and catalase. J Exp Bot 32(126):93–101. doi:10.1093/jxb/32.1.93

    Article  CAS  Google Scholar 

  • 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(4):246–252. doi:10.1002/em.20153

    Article  Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7((2):88. doi:10.1016/0006-2952(61)90145-9

    Article  CAS  Google Scholar 

  • Eyambe GS, Goven AJ, Fitzpatrick LC, Venables BJ, Cooper EL (1991) A noninvasive technique for sequential collection of earthworm (Lumbricus terrestris) leukocytes during subchronic immunotoxicity studies. Lab Anim-uk 25(1):61–67. doi:10.1258/002367791780808095

    Article  CAS  Google Scholar 

  • Faust F (2004) The use of the alkaline comet assay with lymphocytes in human biomonitoring studies. Mutat Res-rev Mutat 566(3):209–229. doi:10.1016/j.mrrev.2003.09.007

    Article  CAS  Google Scholar 

  • Frasco MF, Fournier D, Carvalho F, Guilhermino L (2005) Do metals inhibit acetylcholinesterase (AChE)? Implementation of assay conditions for the use of AChE activity as a biomarker of metal toxicity. Biomarkers 10(5):360–375. doi:10.1080/13547500500264660

    Article  CAS  Google Scholar 

  • Gastaldi L, Ranzato E, Caprì F, Hankard P, Pérès G, Canesi L, Viarengo A, Pons G (2007) Application of a biomarker battery for the evaluation of the sublethal effects of pollutants in the earthworm Eisenia andrei. Comp Biochem Phys C 146(3):398–405. doi:10.1016/j.cbpc.2007.04.014

    Google Scholar 

  • Hankard PK, Svendsen C, Wright J, Wienberg C, Fishwick SK, Spurgeon DJ, Weeks JM (2004) Biological assessment of contaminated land using earthworm biomarkers in support of chemical analysis. Sci Total Environ 330(1–3):9–20. doi:10.1016/j.scitotenv.2003.08.023

    Article  CAS  Google Scholar 

  • Honsi TG, Hoel L, Stenersen JV (1999) Non-inducibility of antioxidant enzymes in the earthworms Eisenia veneta and E. fetida after exposure to heavy metals and paraquat. Pedobiologia 43(6):652–657

    CAS  Google Scholar 

  • Hu CW, Li M, Cui YB, Li DS, Chen J, Yang LY (2010) Toxicological effects of TiO2 and ZnO nanoparticles in soil on earthworm Eisenia fetida. Soil Biol Biochem 42:586–591. doi:10.1016/j.soilbio.2009.12.007

    Article  CAS  Google Scholar 

  • Key PB, Fulton MH (2002) Characterization of cholinesterase activity in tissues of the grass shrimp (Palaemonetes pugio). Pestic Biochem Phys 72(3):186–192. doi:10.1016/s0048-3575(02)00006-8

    Article  CAS  Google Scholar 

  • Khalil MA, AbdelLateif HM, Bayoumi BM, vanStraalen NM, vanGestel CAM (1996) Effects of metals and metal mixtures on survival and cocoon production of the earthworm Aporrectodea caliginosa. Pedobiologia 40(6):548–556

    CAS  Google Scholar 

  • Łaszczyca P, Augustyniak M, Babczyńska A, Bednarska K, Kafel A, Migula P, Wilczek G, Witas I (2004) Profiles of enzymatic activity in earthworms from zinc, lead and cadmium polluted areas near Olkusz (Poland). Environ Int 30(7):901–910. doi:10.1016/j.envint.2004.02.006

    Article  Google Scholar 

  • Li M, Liu Z, Xu Y, Cui Y, Li D, Kong Z (2009) Comparative effects of Cd and Pb on biochemical response and DNA damage in the earthworm Eisenia fetida (Annelida, Oligochaeta). Chemosphere 74(5):621–625. doi:10.1016/j.chemosphere.2008.10.048

    Article  CAS  Google Scholar 

  • Lourenço JI, Pereira RO, Silva AC, Morgado JM, Carvalho FP, Oliveira JM, Malta MP, Paiva AA, Mendo SA, Gonçalves FJ (2011) Genotoxic endpoints in the earthworms sub-lethal assay to evaluate natural soils contaminated by metals and radionuclides. J Hazard Mater 186(1):788–795. doi:10.1016/j.jhazmat.2010.11.073

    Article  Google Scholar 

  • Luo Y-R, Wang S-H, Yun M-X, Li X-Y, Wang J-J, Sun Z-J (2009) The toxic effects of ionic liquids on the activities of acetylcholinesterase and cellulase in earthworms. Chemosphere 77:313–318. doi:10.1016/j.chemosphere.2009.07.026

    Article  CAS  Google Scholar 

  • Luo Y, Zang Y, Zhong YA, Kong ZM (1999) Toxicological study of two novel pesticides on earthworm Eisenia foetida. Chemosphere 39(13):2347–2356. doi:10.1016/s0045-6535(99)00142-3

    Article  CAS  Google Scholar 

  • Lutz WK (1998) Dose–response relationships in chemical carcinogenesis: superposition of different mechanisms of action, resulting in linear–nonlinear curves, practical thresholds, J-shapes. Mutat Res-fund Mol M 405(2):117–124. doi:10.1016/s0027-5107(98)00128-6

    Article  CAS  Google Scholar 

  • Maity S, Roy S, Chaudhury S, Bhattacharya S (2008) Antioxidant responses of the earthworm Lampito mauritii exposed to Pb and Zn contaminated soil. Environ Pollut 151(1):1–7. doi:10.1016/j.envpol.2007.03.005

    Article  CAS  Google Scholar 

  • Manerikar RS, Apte AA, Ghole VS (2008) In vitro and in vivo genotoxicity assessment of Cr(VI) using comet assay in earthworm coelomocytes. Environ Toxicol Phar 25(1):63–68. doi:10.1016/j.etap.2007.08.009

    Article  CAS  Google Scholar 

  • Nahmani J, Hodson ME, Black S (2007a) Effects of metals on life cycle parameters of the earthworm Eisenia fetida exposed to field-contaminated, metal-polluted soils. Environ Pollut 149(1):44–58. doi:10.1016/j.envpol.2006.12.018

    Article  CAS  Google Scholar 

  • Nahmani J, Hodson ME, Black S (2007b) A review of studies performed to assess metal uptake by earthworms. Environ Pollut 145(2):402–424. doi:10.1016/j.envpol.2006.04.009

    Article  CAS  Google Scholar 

  • Neuhauser EF, Loehr RC, Milligan DL, Maleck MR (1985) Toxicity of metals to the earthworm Eisenia fetida. Biol and Fert Soils 1(3):149–152. doi:10.1007/BF00301782

    Article  CAS  Google Scholar 

  • Novais SC, Gomes SIL, Gravato C, Guilhermino L, De Coen W, Soares AMVM, Amorim MJB (2011) Reproduction and biochemical responses in Enchytraeus albidus (Oligochaeta) to zinc or cadmium exposures. Environ Pollut 159(7):1836–1843. doi:10.1016/j.envpol.2011.03.031

    Article  CAS  Google Scholar 

  • Peijnenburg W, Jager T (2003) Monitoring approaches to assess bioaccessibility and bioavailability of metals: matrix issues. Ecotox Environ Safe 56(1):63–77. doi:10.1016/s0147-6513(03)0051-4

    Article  CAS  Google Scholar 

  • Qiao M, Chen Y, Wang C-X, Wang Z, Zhu Y-G (2007) DNA damage and repair process in earthworm after in-vivo and in vitro exposure to soils irrigated by wastewaters. Environ Pollut 148(1):141–147. doi:10.1016/j.envpol.2006.10.033

    Article  CAS  Google Scholar 

  • Rao JV, Kavitha P (2004) Toxicity of azodrin on the morphology and acetylcholinesterase activity of the earthworm Eisenia foetida. Environ Res 96(3):323–327. doi:10.1016/j.envres.2004.02.014

    Article  CAS  Google Scholar 

  • Ribera D, Narbonne JF, Arnaud C, Saint-Denis M (2001) Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil, effects of carbaryl. Soil Biol Biochem 33(7–8):1123–1130. doi:10.1016/s0038-0717(01)00035-9

    Article  CAS  Google Scholar 

  • Romani R, Antognelli C, Baldracchini F, De Santis A, Isani G, Giovannini E, Rosi G (2003) Increased acetylcholinesterase activities in specimens of Sparus auratus exposed to sublethal copper concentrations. Chem-biol Interact 145(3):321–329. doi:10.1016/s0009-2797(03)00058-9

    Article  CAS  Google Scholar 

  • Reinecke SA, Reinecke AJ (2004) The comet assay as biomarker of heavy metal genotoxicity in earthworms. Arch Environ Con Tox 46:208–215. doi:10.1007/s00244-003-2253-0

    CAS  Google Scholar 

  • Saint-Denis M, Narbonne JF, Arnaud C, Ribera D (2001) Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil: effects of lead acetate. Soil Biol Biochem 33(3):395–404. doi:10.1016/s0038-0717(00)00177-2

    Article  CAS  Google Scholar 

  • Saint-Denis M, Narbonne JF, Arnaud C, Thybaud E, Ribera D (1999) Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil: effects of benzo[a]pyrene. Soil Biol Biochem 31(13):1837–1846. doi:10.1016/s0038-0717(99)00106-6

    Article  CAS  Google Scholar 

  • Sarkarati B, Cokugras AN, Tezcan EF (1999) Inhibition kinetics of human serum butyrylcholinesterase by Cd2+, Zn2+ and Al3+: comparison of the effects of metal ions on cholinesterases. Comp Biochem Physiol C-Pharmacol Toxicol Endocrinol 122(2):181–190. doi:10.1016/s0742-8413(98)10102-0

    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. doi:10.1016/j.pestbp.2007.02.005

    Article  CAS  Google Scholar 

  • Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low-levels of DNA damage in individual cells. Exp Cell Res 175(1):184–191. doi:10.1016/0014-4827(88)90265-0

    Article  CAS  Google Scholar 

  • Spurgeon DJ, Hopkin SP (1995) Extrapolation of the laboratory-based OECD earthworm toxicity test to metal-contaminated field sites. Ecotoxicology 4(3):190–205. doi:10.1007/bf00116481

    Article  CAS  Google Scholar 

  • Spurgeon DJ, Hopkin SP (1996) Effects of variations of the organic matter content and pH of soils on the availability and toxicity of zinc to the earthworm Eisenia fetida. Pedobiologia 40(1):80–96

    CAS  Google Scholar 

  • Spurgeon DJ, Hopkin SP, Jones DT (1994) Effects of cadmium, copper, lead and zinc on growth, reproduction and survival of the earthworm Eisenia foetida (savigny)—assessing the environmental-impact of point-source metal contamination in terrestrial ecosystems. Environ Pollut 84(2):123–130. doi:10.1016/0269-7491(94)90094-9

    Article  CAS  Google Scholar 

  • Svendsen C, Spurgeon DJ, Hankard PK, Weeks JM (2004) A review of lysosomal membrane stability measured by neutral red retention: is it a workable earthworm biomarker? Ecotox Environ Safe 57(1):20–29. doi:10.1016/j.ecoenv.2003.08.009

    Article  CAS  Google Scholar 

  • Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35(3):206–221. doi:10.1002/(sici)1098-2280(2000)35:3<206::aid-em8>3.0.co;2-j

    Article  CAS  Google Scholar 

  • Venkateswara Rao J, Surya Pavan Y, Madhavendra SS (2003) Toxic effects of chlorpyrifos on morphology and acetylcholinesterase activity in the earthworm, Eisenia foetida. Ecotox Environ Safe 54(3):296–301. doi:10.1016/s0147-6513(02)00013-1

    Article  CAS  Google Scholar 

  • Wei B, Yang L (2010) A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchem J 94(2):99–107. doi:10.1016/j.microc.2009.09.014

    Article  CAS  Google Scholar 

  • Xia JC (1996) Detailed study of the soil environmental quality standards. China environmental science publisher, Beijing, China (in Chinese)

    Google Scholar 

  • Xiao N-W, Song Y, Ge F, Liu X-H, Ou-Yang Z-Y (2006a) Biomarkers responses of the earthworm Eisenia fetida to acetochlor exposure in OECD soil. Chemosphere 65(6):907–912. doi:10.1016/j.chemosphere.2006.03.060

    Article  CAS  Google Scholar 

  • Xiao NW, Jing B, Ge F, Liu XH (2006b) The fate of herbicide acetochlor and its toxicity to Eisenia fetida under laboratory conditions. Chemosphere 62(8):1366–1373. doi:10.1016/j.chemosphere.2006.07.043

    Article  CAS  Google Scholar 

  • Xiao RY, Wang ZJ, Wang CX, Yu G, Zhu YG (2006c) Genotoxic risk identification of soil contamination at a major industrialized city in northeast China by a combination of in vitro and in vivo bioassays. Environ Sci Technol 40(19):6170–6175. doi:10.1021/es0607335

    Article  CAS  Google Scholar 

  • Xie X, Wu Y, Zhu M, Y-k Z, Wang X (2011) Hydroxyl radical generation and oxidative stress in earthworms (Eisenia fetida) exposed to decabromodiphenyl ether (BDE-209). Ecotoxicology 20(5):993–999. doi:10.1007/s10646-011-0645-x

    Article  CAS  Google Scholar 

  • Zatta P, Ibn-Lkhayat-Idrissi M, Zambenedetti P, Kilyen M, Kiss T (2002) In vivo and in vitro effects of aluminum on the activity of mouse brain acetylcholinesterase. Brain Res Bull 59(1):41–45. doi:10.1016/s0361-9230(02)00836-5

    Article  CAS  Google Scholar 

  • Zhang DA (1991) The experimental handbook of biological macromolecule. The press of Jilin University. Changchun, China (in Chinese)

    Google Scholar 

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Acknowledgments

This work was supported by the Science and Technology Support Program of Jiangsu Province (No. BE2012737), Public Sector Special Scientific Research Program of the National Environmental Protection Ministry (No. 2011467054), and National Natural Science Foundation of China (No. 21077052). The authors are grateful to Richard A. Manderville for his assistance and helpful advice.

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Correspondence to Mei Li.

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Zheng, K., Liu, Z., Li, Y. et al. Toxicological responses of earthworm (Eisenia fetida) exposed to metal-contaminated soils. Environ Sci Pollut Res 20, 8382–8390 (2013). https://doi.org/10.1007/s11356-013-1689-7

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