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Fractionation and bioavailability of Cu in soil remediated by EDTA leaching and processed by earthworms (Lumbricus terrestris L.)

  • AREA 5 • REMEDIATION AND ECOSYSTEM RESTORATION • RESEARCH ARTICLE
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Abstract

Background, aim, and scope

Soil remediation with ethylenediamine tetraacetic acid (EDTA) leaching is capable of removing only part of the total metal concentration in the soil, mostly the labile, bioavailable metal species (metal bioavailability stripping). However, reintroduction of remediated soil in the environment exposes the soil to various environmental factors, which could potentially shift nonlabile residual metals back to labile bioavailable forms. We studied the effect of autochthonous earthworm species as model biotic environmental factor on the fractionation and bioavailability of Cu residual in soil after remediation.

Materials and methods

We used soil from a 50-year-old vineyard regularly managed and treated with CuSO4•5H2O (Bordeaux mixture) as fungicide. Soil containing 400 mg kg−1 of Cu was leached with total 15 mmol kg−1 EDTA. Remediated and nonremediated soil was processed by fully clitellated adult specimens of Lumbricus terrestris L., a prevailing autochthonous soil earthworm species. Cu fractionation, phytoavailability, and oral-bioavailability in processed and nonprocessed soil were determined using six-step sequential extraction, extraction with diethylenediamine pentaacetic acid, and in vitro physiologically based extraction test, respectively.

Results

EDTA leaching removed 41% of the pseudototal Cu, mostly from the soil Fe- and Mn-oxides, carbonates, and organic matter. A 2.7-fold decrease in Cu phytoavailability and a 4.4- and 2.8-fold decrease in Cu oral-bioavailability in the stomach and small intestine fractions, respectively, were achieved after remediation. In nonremediated soil, earthworms increased the share of nonlabile Cu in residual soil fraction, while in remediated soil they increased the share of Cu bound to carbonates. A statistically significant 1.1- and 1.7-fold increase in Cu phytoavailability and intestinal oral-bioavailability, respectively, was observed in earthworm processed remediated soil.

Discussion

Cu occurs in various soil “pools” of different solubilities with different chemical characteristics and consequently different functions. By removing the labile part of the metals from the soil during remediation, we disrupt the chemical equilibrium; the nonlabile residual metals left in soil after remediation might become more labile in time in tendency to re-establish that equilibrium. Earthworms alter the physical and chemical properties of soil affecting consequently the fractionation of metals. The increase in earthworm’s gut pH due to the excretion of ammonia and/or calcium carbonate into the intestine could lead to the transbounding of metals into the carbonate fraction. However, their activity in remediated soil increased Cu phytoavailability and intestinal oral-bioavailability, and it would, therefore, be improper to generalize the influence of earthworms on metal availability in soil.

Conclusions

The results presented here show that residual Cu in remediated soil is affected by environmental factors such as earthworms, which should be considered in evaluating the effect of Cu polluted soil remediation.

Recommendations and perspectives

Information on the behavior of residual metals in soil after its remediation is surprisingly scarce. The development of new effective remediation techniques should imply also the evaluation of postremediation effects on remediated soil. The results presented in this work indicate a possible tool for assessing the effect of biotic environmental factors on residual metals left in soil after its remediation.

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References

  • Abollino O, Giacomino A, Malandrino M, Mentasti E, Aceto M, Barberis R (2006) Assessment of metal availability in a contaminated soil by sequential extraction. Water Air Soil Poll 137:315–338

    Article  CAS  Google Scholar 

  • Adriano DC (2001) Trace elements in terrestrial environments. Springer-Verlag Inc, New York

    Google Scholar 

  • Arnold RE, Hodson ME, Black S, Davies NA (2003) The influence of mineral solubility and soil solution concentration on the toxicity of copper to Eisenia fetida Savigny. Pedobiologia 47:622–632

    CAS  Google Scholar 

  • Baker DE, Senft JP (1997) Copper. In: Alloway BJ (ed) Heavy metals in soils, 2nd edn. Chapman and Hall, Suffolk, Great Britain, pp 179–205

    Google Scholar 

  • Bohlen PJ (2002) Earthworms. In: Lal R (ed) Encyclopedia of soil science. Marcel Dekker, New York, pp 370–373

    Google Scholar 

  • Bouché MB (1977) Stratégies lombriciennes. In: Lohm U, Persson T (eds) Soil organisms as components of ecosystems. Ecol Bull 25:122–132

  • Boyle KE, Curry JP, Farrell EP (1997) Influence of earthworms on soil properties and grass in reclaimed cutover peat. Biol Fert Soils 25:20–26

    Article  Google Scholar 

  • Brun LA, Maillet J, Hinsinger P, Pépin M (2001) Evaluation of copper availability to plants in copper-contaminated vineyard soils. Environ Pollut 111:293–302

    Article  CAS  Google Scholar 

  • Carlon C (ed) (2007) Derivation methods of soil screening values in Europe. A review and evaluation of national procedures towards harmonization EUR 22805-EN. European Commision, Joint Research Centre, Ispra

  • Cheng J, Wong MH (2002) Effects of earthworms on Zn fractionation in soils. Biol Fert Soils 36:72–78

    Article  CAS  Google Scholar 

  • Conder JM, Lanno RP, Basta NT (2001) Assessment of metal availability in smelter soil using earthworms and chemical extractions. J Environ Qual 30:1231–1237

    CAS  Google Scholar 

  • Davis S, Mirick DK (2006) Soil ingestion in children and adults in the same family. J Expo Sci Env Epid 16:63–75

    Article  CAS  Google Scholar 

  • Dermont G, Bergeron M, Mercier G, Richer-Lafléche M (2008) Soil washing for metal removal: a review of physical/chemical technologies and field applications. J Hazard Mater 152:1–31

    Article  CAS  Google Scholar 

  • Devliegher W, Verstraete W (1996) Lumbricus terrestris in a soil sore experiment: effects of nutrient-enrichment processes (NEP) and gut-associated processes (GAP) on the availability of plant nutrients and heavy metals. Soil Biol Biochem 28:489–496

    Article  CAS  Google Scholar 

  • Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms. Chapman & Hall, London

    Google Scholar 

  • Eisler R (2000) Handbook of chemical risk assessment. CRC Press LLC

  • El Gharmali A, Rada A, El Meray M, Nejmeddine A (2002) Study of the effect of earthworm Lumbricus terrestris on the speciation of heavy metals in soils. Environ Technol 23:775–780

    Article  CAS  Google Scholar 

  • Feroci G, Fina A, Fazio G, Zuman P (1995) Interaction between dihydroxy bile-salts and divalent heavy-metal ions studied by polarography. Anal Chem 67:4077–4085

    Article  CAS  Google Scholar 

  • Fiedler HJ, Hoffmann F, Schmiedel H (1964) Die Untersuchung der Boden, Band 1, 1st edn. Theodor Steinkopff, Dresden und Leipzig

    Google Scholar 

  • Finzgar N, Lestan D (2006) Heap leaching of Pb and Zn contaminated soil using ozone/UV treatment od EDTA extractants. Chemosphere 63:1736–1743

    Article  CAS  Google Scholar 

  • Finzgar N, Lestan D (2007) Multi-step leaching of Pb and Zn contaminated soils with EDTA. Chemosphere 66:824–832

    Article  CAS  Google Scholar 

  • Flemming CA, Trevors JT (1989) Copper toxicity and chemistry in the environment: a review. Water Air Soil Poll 44:143–158

    Article  CAS  Google Scholar 

  • Ginocchio R, Sánchez P, de la Fuente LM, Camus I, Bustamante E, Silva Y, Urrestarazu P, Torres JC, Rodriguez PH (2006) Agricultural soils spiked with copper mine wastes and copper concentrate: implications for copper bioavailability and bioaccumulation. Environ Toxicol Chem 25:712–718

    Article  CAS  Google Scholar 

  • Griffiths RA (1995) Soil washing technology and practice. J Hazard Mater 40:175–189

    Article  CAS  Google Scholar 

  • Hopkin SP (1989) Ecophysiology of metals in terrestrial invertebrates. Elsevier, London, New York

    Google Scholar 

  • ISO 10693 (1995) Soil quality—determination of carbonate content—volumetric method. International organization for standardization. Genève, Switzerland

    Google Scholar 

  • ISO 14235 (1998) Soil quality—determination of organic carbon by sulfochromic oxidation. International organization for standardization. Genève, Switzerland

    Google Scholar 

  • Kabata-Pendias A, Pendias H (1984) Trace elements in soils and plants. CRC Press, Inc., Boca Raton, Florida

    Google Scholar 

  • Kalra YP, Maynard DG (1991) Methods manual for forest soil and plant analysis. Canadian Forest Service, Northern Forestry Centre, Edmonton

    Google Scholar 

  • Kamnev AA, van der Lelie D (2000) Chemical and biological parameters as tools to evaluate and improve heavy metal phytoremediation. Bioscience Rep 20:239–258

    Article  CAS  Google Scholar 

  • Kizilkaya R (2004) Cu and Zn accumulation in earthworm Lumbricus terrestris L. in sewage sludge amended soil and fractions of Cu and Zn in casts and surrounding soil. Ecol Eng 22:141–151

    Article  Google Scholar 

  • Kumpiene J, Lagerkvist A, Maurice C (2007) Stabilization of Pb- and Cu-contaminated soil using coal fly ash and peat. Environ Pollut 145:365–373

    Article  CAS  Google Scholar 

  • Langdon CJ, Piearce TG, Meharg AA, Semple KT (2001) Survival and behavior of the earthworms Lumbricus rubellus and Dendrodrilus rubidus from arsenate-contaminated and non-contaminated sites. Soil Biol Biochem 33:1239–1244

    Article  CAS  Google Scholar 

  • Lee KL (1985) Earthworms: their ecology and relationships with soils and land use. Academic, Sydney

    Google Scholar 

  • Lestan D, Grcman H, Zupan M, Bacac N (2003) Relationship of soil properties to fractionation of Pb and Zn in soil and their uptake into Plantago lanceolata. Soil Sediment Contam 12:507–522

    Article  CAS  Google Scholar 

  • Lestan D, Luo C, Li X (2008) The use of chelating agents in the remediation of metal-contaminated soils: a review. Environ Pollut 153:3–13

    Article  CAS  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of a DTPA test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–428

    Article  CAS  Google Scholar 

  • Liu X, Hu C, Zhang S (2005) Effects of earthworm activity on fertility and heavy metal bioavailability in sewage sludge. Environ Int 31:874–879

    Article  CAS  Google Scholar 

  • Lukkari T, Teno S, Väisänen A, Haimi J (2006) Effects of earthworms on decomposition and metal availability in contaminated soil: microcosm studies of populations with different exposure histories. Soil Biol Biochem 38:359–370

    CAS  Google Scholar 

  • Ma Y, Dickinson NM, Wong MH (2002) Toxicity of Pb/Zn mine tailings to the earthworm Pheretima and the effects of burrowing on metal availability. Biol Fert Soils 36:79–86

    Article  CAS  Google Scholar 

  • Ma Y, Dickinson NM, Wong MH (2003) Interactions between earthworms, trees, soil nutrition and metal mobility in amended Pb/Zn mine tailings from Guangdong, China. Soil Biol Biochem 35:1369–1379

    Article  CAS  Google Scholar 

  • Maiz I, Arambarri I, Garcia R, Millán E (2000) Evaluation of heavy metal availability in polluted soil by two sequential extraction procedures using factor analysis. Environ Pollut 110:3–9

    Article  CAS  Google Scholar 

  • McLaren RG, Swift RS, Williams JG (1981) The adsorption of copper by soil materials at low equilibrium solution concentrations. J Soil Sci 32:247–256

    Article  CAS  Google Scholar 

  • Morgan JE, Morgan AJ (1988) Earthworms as biological monitors of cadmium, copper, lead and zinc in metalliferous soils. Environ Pollut 54:123–138

    Article  CAS  Google Scholar 

  • Morgan JE, Morgan AJ (1999) The accumulation of metals (Cd, Cu, Pb, Zn and Ca) by two ecologically contrasting earthworm species (Lumbricus rubellus and Aporrectodea caliginosa): implications for ecotoxicoogical testing. Appl Soil Ecol 13:9–20

    Article  Google Scholar 

  • Mršić N (1997) Animals in our soil. (in Slovenian.). Tehniška založba Slovenije, Ljubljana

    Google Scholar 

  • Mulligan CN, Yong RN, Gibbs BF (2001) Remediation technologies for metal contaminated soils and groundwater: an evaluation. Eng Geol 60:193–207

    Article  Google Scholar 

  • Nowack B, Schulin R, Robinson BH (2006) Critical asessment of chelant metal phytoextraction. Environ Sci Technol 40:5225–5232

    Article  CAS  Google Scholar 

  • Paoletti MG (1999) The role of earthworms for assessment of sustainability and as bioindicators. Agr Ecosyst Environ 74:137–155

    Article  Google Scholar 

  • Paoletti MG, Iovane E, Cortese M (1988) Pedofauna bioindicators as heavy metals in five agroecosystems in north-east Italy. Rev Ecol Biol Sol 25:33–58

    CAS  Google Scholar 

  • Peters RW (1999) Chelant extraction of heavy metals from contaminated soils. J Hazard Mater 66:151–210

    Article  CAS  Google Scholar 

  • Rhoades JD (1982) Cation exchange capacity. In: Page AL, Miller RH, Keeney DR (eds) Methods of soils analysis. part 2: chemical and microbiological properties. Serie Agronomy N°9, ASA – SSSA, Madison, pp 149–157

    Google Scholar 

  • Rida AMMA (1996) Trace element concentrations and growth of earthworms and plants in soils with and without cadmium, copper, iron, lead and zinc contamination: interaction of plants, soil and earthworms. Soil Biol Biochem 28:1037–1044

    Article  Google Scholar 

  • Ruby MV, Davis A, Schoof R, Eberle S, Sellstone CM (1996) Estimation of lead and arsenic bioavailability using a physiologically based extraction test. Environ Sci Technol 30:422–430

    Article  CAS  Google Scholar 

  • Ruiz E, Rodriguez L, Alonso-Azcárate J (2009) Effects of earthworms on metal uptake of heavy metals from polluted mine soils by different crop plants. Chemosphere 75:1035–1041

    Article  CAS  Google Scholar 

  • Sizmur T, Hodson ME (2009) Do earthworms impact metal mobility and availability in soil? A review. Environ Pollut 157:1981–1989

    Article  CAS  Google Scholar 

  • Spurgeon DJ, Hopkin SP (1999) Tolerance to zinc in populations of the earthworm Lumbricus rubellus from uncontaminated and metal-contaminated ecosystems. Arch Environ Con Tox 37:332–337

    Article  CAS  Google Scholar 

  • Sun B, Zhao FJ, Lombi E, McGrath SP (2001) Leaching of heavy metals from contaminated soils using EDTA. Environ Pollut 113:111–120

    Article  CAS  Google Scholar 

  • Tiunov AV, Scheu S (2000) Microbial biomass, biovolume and respiration in Lumbricus terrestris L. cast material of different age. Soil Biol Biochem 32:265–275

    Article  CAS  Google Scholar 

  • Turner A, Ip KH (2007) Bioaccessibility of metals in dust from the indoor environment: application of a physiologically based extraction test. Environ Sci Technol 41:7851–7856

    Article  CAS  Google Scholar 

  • Udovic M, Lestan D (2007) EDTA leaching of Cu contaminated soils using ozone/UV for treatment and reuse of washing solution in a closed loop. Water Air Soil Poll 181:319–327

    Article  CAS  Google Scholar 

  • Udovic M, Plavc Z, Lestan D (2007) The effect of earthworms on the fractionation, mobility and bioavailability of Pb, Zn and Cd before and after soil leaching with EDTA. Chemosphere 70:126–134

    Article  CAS  Google Scholar 

  • Ur. L. RS No 68, 29. XI (1996) Uredba o mejnih, opozorilnih in kritičnih imisijskih vrednostih nevarnih snovi v tleh. Uradni List Republike Slovenije, Ljubljana

    Google Scholar 

  • Ure AM (1996) Single extraction schemes for soil analysis and related applications. Sci Total Environ 178:3–10

    Article  CAS  Google Scholar 

  • Wen JHC, Wong MH (2004) Effects of earthworm activity and P-solubilizing bacteria on P availability in soil. J Plant Nutr Soil Sc 167:209–213

    Article  Google Scholar 

  • Wen B, Hu X, Liu Y, Wang W, Feng M, Shan X (2004) The role of earthworms (Eisenia fetida) in influencing bioavailability of heavy metals in soils. Biol Fertil Soils 40:181–187

    Article  CAS  Google Scholar 

  • Wright DA, Welbourn P (2002) Environmental toxicology. Cambridge University Press, Cambridge

    Google Scholar 

  • Zorn MI, Van Gestel CAM, Eijsackers H (2005) The effect of two endogeic earthworm species on zinc distribution and availability in artificial soil columns. Soil Biol Biochem 37:917–925

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Slovenian Ministry for Education, Science and Sport, grant J4 9277.

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  1. Biotechnical Faculty, Agronomy Department, Centre for Soil and Environmental Science, University of Ljubljana, Jamnikarjeva 101, 1000, Ljubljana, Slovenia

    Metka Udovic & Domen Lestan

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  1. Metka Udovic
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  2. Domen Lestan
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Correspondence to Domen Lestan.

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Responsible editor: Henner Hollert

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Udovic, M., Lestan, D. Fractionation and bioavailability of Cu in soil remediated by EDTA leaching and processed by earthworms (Lumbricus terrestris L.). Environ Sci Pollut Res 17, 561–570 (2010). https://doi.org/10.1007/s11356-009-0262-x

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