Skip to main content
SpringerLink
Log in

Detoxification of Heavy Metals Using Earthworms

  • Chapter
  • First Online:
Detoxification of Heavy Metals

Part of the book series: Soil Biology ((SOILBIOL,volume 30))

Abstract

The number of different earthworm species living in a certain soil environment can be three or five and occasionally more than ten. Earthworms substantially enhance physical, chemical, and biological characteristics of soil through their feeding, casting, and burrowing activities. The factors affecting earthworm populations and activities in soil are climate, soil characteristics, plant vegetation, and biological relationships. The influences of earthworms on soil characteristics are mainly driven by their feeding, casting, and burrowing activities. Earthworms can affect either available or total metal concentrations in soil in that they have capability to accumulate heavy metals in their tissues and hence reduce their involvement in soil food chain. During their feeding activities, earthworms can change either available or total metal concentrations in soil in that they are capable to accumulate heavy metals in their tissues. The accumulation of heavy metals by earthworms is mainly associated with the factors such as type of mineral soil, organic matter content, and metal concentrations of their living environment and it should be kept in mind that earthworm–heavy metal relationships are mostly driven by soil characteristics and their ecological category.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ash CPJ, Lee DL (1980) Lead, cadmium, copper and iron in earthworms from roadside sites. Environ Pollut 22:59–67

    Article  CAS  Google Scholar 

  • Baker GH, Barrett VJ, Carter PJ, Williams PML, Buckerfield JC (1993) Seasonal changes in the abundance of earthworms (Annelida: Lumbricidae and Acanthodrilidae) in soils used for cereal and lucerne production in South Australia. Aust J Agric Res 44:1291–1301

    Article  Google Scholar 

  • Barois I, Lavelle P, Brossand M, Tondal L, Martinez M, Rossi JP, Senapati BK, Angeles A, Fragoso C, Jimienez JJ, Decaens T, Lattand C, Kamyono J, Chapius L, Brown GE, Monerno A (1999) Ecology of earthworms with large environmental tolerance and extended distribution. In: Lavelle P, Brussaard L, Hendrix P (eds) Earthworm management in tropical ecosystems. CABI, Wallingford, Oxford, UK, pp 57–86

    Google Scholar 

  • Bengtsson G, Nordstrom S, Rundgren S (1983) Population density and tissue metal concentration of lumbricids in forest soils near a brass mill. Environ Pollut 30:87–108

    Article  CAS  Google Scholar 

  • Bernier N, Ponge JF (1994) Humus form dynamics during the sylvogenetic cycle in a mountain spruce forest. Soil Biol Biochem 26:183–220

    Article  Google Scholar 

  • Beyer WN, Pattee OH, Sileo L, Hoffman DJ, Mulhern BM (1985) Metal contamination in wildlife living near two zinc smelters. Environ Pollut 38:63–86

    Article  CAS  Google Scholar 

  • Beyer WN, Hensler G, Moore I (1987) Relation of pH and other soil variables to concentrations of Pb, Cu, Zn, Cd and Se in earthworms. Pedobiologia 30:167–172

    CAS  Google Scholar 

  • Blanchart E, Lavelle P, Braudeau E, Le Bissonnais Y, Valentin C (1997) Regulation of soil structure by geophagous earthworm activities in humid savannas of Côte d.Ivoire. Soil Biol Biochem 29:431–439

    Article  CAS  Google Scholar 

  • Blanchart E, Albrecht A, Alegre J, Duboisset A, Gilot C, Pashanasi B, Lavelle P, Brussaard L (1999) Effects of earthworms on soil structure and physical properties. In: Lavelle P, Brussaard L, Hendrix P (eds) Earthworm management in tropical ecosystems. CABI, Wallingford, Oxford, UK, pp 149–172

    Google Scholar 

  • Cemek B, Kizilkaya R (2006) Spatial variability and monitoring of Pb contamination of farming soils affected by industry. Environ Monit Assess 117:357–375

    Article  PubMed  CAS  Google Scholar 

  • Chan KY, Heenan DP (1995) Occurrence of enchytraeid worms and some properties of their casts in an Australian soil under cropping. Aust J Soil Res 33:651–657

    Article  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 Contam Toxicol 32:166–171

    Article  PubMed  CAS  Google Scholar 

  • Curry JP, Cotton DCF (1983) Earthworms and land reclamation. In: Satchell JE (ed) Earthworm ecology from Darwin to vermiculture. Chapman and Hall, London, pp 215–228

    Chapter  Google Scholar 

  • Edwards CA (1983) Earthworm ecology in cultivated soils. In: Satchell JE (ed) Earthworm ecology from Darwin to vermiculture. Chapman and Hall, London, pp 123–137

    Chapter  Google Scholar 

  • Edwards CA, Bohlen PJ (1996) Biology of and ecology earthworms, 3rd edn. Chapman and Hall, London

    Google Scholar 

  • Edwards CA, Lofty JR (1982a) The effect of direct drilling and minimal cultivation on earthworm populations. J Appl Ecol 19:723–724

    Article  Google Scholar 

  • Edwards CA, Lofty JR (1982b) Nitrogenous fertilizers and earthworm populations in agricultural soils. Soil Biol Biochem 14:515–521

    Article  Google Scholar 

  • Edwards WM, Shipitalo MJ (2004) Consequences of earthworms in agricultural soils: aggregation and porosity. In: Edwards CA (ed) Earthworm ecology. Lewis Publishers, Boca Raton, pp 147–161

    Chapter  Google Scholar 

  • Fitzpatrick LC, Muratti-Ortiz JF, Venables BJ, Goven AJ (1996) Comparative toxicity in earthworms Eisenia fetida and Lumbricus terrestris exposed to cadmium nitrate using artificial soil and filter paper protocols. Bull Environ Contam Toxicol 57:63–68

    Article  PubMed  CAS  Google Scholar 

  • Fragoso C, Lavelle P (1992) Earthworm communities of tropical rain forests. Soil Biol Biochem 24:1397–1408

    Article  Google Scholar 

  • Fragoso C, Lavelle P, Blanchart E, Senapati BK, Jimenez JJ, Martinez M, Decaens T, Tondoh J (1999) Earthworm communities of tropical agroecosystems: origin, structure and influence of management practices. In: Lavelle P, Brussaard L, Hendrix P (eds) Earthworm management in tropical agroecosystems. CAB International, Wallingford

    Google Scholar 

  • Gerard BM (1967) Factors affecting earthworms in pastures. J Anim Ecol 36:235–252

    Article  Google Scholar 

  • Gish CD, Christensen RE (1973) Cadmium, nickel, lead and zinc in earthworms from roadside soil. Environ Sci Technol 7:1060–1062

    Article  PubMed  CAS  Google Scholar 

  • Green RN, Trowbridge RL, Klinka K (1993) Towards a taxonomic classification of humus forms. Forest Sci Monogr 29:1–49

    Google Scholar 

  • Guild WJMcL (1948) Studies on the relationship between earthworms and soil fertility. III. The effect of soil type on the structure of earthworm populations. Ann Appl Biol 35:181–192

    Article  Google Scholar 

  • Gullvag BM (1979) Subcellular localization of polluting metals in roadside earthworms exposed to traffic exhaust gases. Cytobios 22:141–153

    Google Scholar 

  • Haynes R, Fraser P (1998) A comparison of aggregate stability and biological activity of the earthworms Lumbricus terrestris and Aporrectodea giardi and consequences on C transfer in soil. Eur J Soil Biol 36:27–34

    Google Scholar 

  • Hendrix PF, Mueller BR, Bruce RR, Langdale GW, Parmelee RW (1992) Abundance and distribution of earthworms in relation to landscape factors on the Georgia Piedmont, USA. Soil Biol Biochem 24:1357–1361

    Article  Google Scholar 

  • Hepsen FS, Kizilkaya R (2007) Determination of sewage sludge soil treatments effect on Cu bioaccumulation by earthworms and Cu contents of casts and surrounding soil. 14th International conference of students, PhD students and young scientists, Lomosonov-2007, Moscow State University, Moscow, Russia, 10–14 April 2007

    Google Scholar 

  • Hepsen TFS, Kizilkaya R (2010) Effects of different application doses of sewage sludge on microbial biomass C and basal respiration in soil and in earthworm L. terrestris L. cast. In: Kizilkaya R, Gulser C, Dengiz O (eds) Proceedings of the international soil science congress on management of natural resources to sustain soil health and quality. Ondokuz Mayis University, Samsun, Turkey, pp 1111–1117, 26–28 May 2010

    Google Scholar 

  • Herms U, Brümner G (1984) Solubility and retention of heavy metals in soils. J Plant Nutr Soil Sci 147:400–424

    Article  CAS  Google Scholar 

  • International Standard Organization (1993) Standard number No.11268-1. Soil quality-effects of pollutants on earthworms (Eisenia fetida) – part I: determination of acute toxicity using artificial soil substrate. ISO, Geneva

    Google Scholar 

  • International Standard Organization (1998) Standard number No.11268-2. Soil quality-effects of pollutants on earthworms (Eisenia fetida) – part II: method for the determination of effects on reproduction. ISO, Geneva

    Google Scholar 

  • Ireland MP, Richars KS (1977) The occurrence and localization of heavy metals and glycogen in the earthworms Lumbricus rubellus and Dendrobaena rubida from a heavy metal site. Histochemistry 51:153–166

    Article  PubMed  CAS  Google Scholar 

  • Karaca A, Naseby D, Lynch J (2002) Effect of cadmium-contamination with sewage sludge and phosphate fertiliser amendments on soil enzyme activities, microbial structure and available cadmium. Biol Fertil Soils 35:435–440

    Article  Google Scholar 

  • Karaca A, Kizilkaya R, Turgay OC, Cetin SC (2010a) Effects of earthworms on the availability and removal of heavy metals in soils. In: Sherameti I, Varma A (eds) Soil heavy metals, soil biology, vol 19. Springer, Berlin, pp 369–388

    Chapter  Google Scholar 

  • Karaca A, Cetin SC, Turgay OC, Kizilkaya R (2010b) Effects of heavy metals on soil enzyme activities. In: Sherameti I, Varma A (eds) Soil heavy metals, soil biology, vol 19. Springer, Berlin, pp 237–262

    Chapter  Google Scholar 

  • Khalil MA, Abdel-Lateif HM, Bayoumi BM, van Straalen NM (1996) Analysis of separate and combined effects of heavy metals on the growth of Aporrectodea caliginosa (Oligochaeta; Annelida), using the toxic approach. Appl Soil Ecol 4:213–219

    Article  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 

  • Kizilkaya R (2005) The role of different organic wastes on zinc bioaccumulation by earthworm Lumbricus terrestris L. (Oligochaeta) in successive Zn added soil. Ecol Eng 25:322–331

    Article  Google Scholar 

  • Kizilkaya R (2008) Dehydrogenase activity in Lumbricus terrestris casts and surrounding soil affected by addition of different organic wastes and Zn. Bioresour Technol 99:946–953

    Article  PubMed  CAS  Google Scholar 

  • Kizilkaya R, Askin T (2002) Influence of cadmium fractions on microbiological properties in Bafra plain soils. Arch Agro Soil Sci 48:263–272

    Article  CAS  Google Scholar 

  • Kizilkaya R, Bayraklı B (2005) Effects of N-enriched sewage sludge on soil enzyme activities. Appl Soil Ecol 30:192–202

    Article  Google Scholar 

  • Kizilkaya R, Hepsen S (2004) Effect of biosolid amendment on enzyme activities in earthworm (Lumbricus terrestris) casts. J Plant Nutr Soil Sci 167:202–208

    Article  CAS  Google Scholar 

  • Kizilkaya R, Hepsen S (2007) Microbiological properties in earthworm Lumbricus terrestris L. cast and surrounding soil amended with various organic wastes. Commun Soil Sci Plant Anal 38:2861–2876

    Article  CAS  Google Scholar 

  • Kizilkaya R, Askin T, Bayraklı B, SaÄŸlam M (2004) Microbiological characteristics of soils contaminated with heavy metals. Eur J Soil Biol 40:95–102

    Article  CAS  Google Scholar 

  • Kizilkaya R, Hepsen S, Akca I, Bayrakli B, Askin T, Turkmen C (2009) Determination of total and mobile Pb fractions during vermicomposting in sewage sludge. International symposium on environment, Kyrgyzstan – Turkey Manas University, Faculty of Engineering, Bishkek, Kyrgyzstan, 20–23 May 2009

    Google Scholar 

  • Kizilkaya R, Hepsen Turkay FS, Turkmen C, Durmus M (2010a) Vermicompost effects on the wheat yield and nutrient contents in soil and plant. International conference on soil fertility and soil productivity, Berlin, Germany, 17–20 March 2010

    Google Scholar 

  • Kizilkaya R, Hepsen Turkay FS, Bayrakli B, Askin T, Turkmen C, Akca I, Ceyhan V (2010b) Enzyme and earthworm activities during vermicomposting in sewage sludge, In: Kizilkaya R, Gulser C, Dengiz O (eds) Proceedings of the international soil science congress on management of natural resources to sustain soil health and quality. Ondokuz Mayis University, Samsun, Turkey, pp 1047–1054, 26–28 May 2010

    Google Scholar 

  • Kizilkaya R, Karaca A, Turgay OC, Cetin SC (2011) Earthworm interactions with soil enzymes. In: Karaca A (ed) Biology of earthworms, soil biology, vol 24. Springer, Berlin, pp 141–158

    Chapter  Google Scholar 

  • Lavelle P (1983) The structure of earthworm communities. In: Satchell JE (ed) Earthworm ecology from Darwin to vermiculture. Chapman and Hall, London, pp 449–466

    Chapter  Google Scholar 

  • Lavelle P (1988) Earthworms and the soil system. Biol Fertil Soils 6:237–251

    Article  Google Scholar 

  • Lavelle P, Spain AV (2001) Soil ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Lavelle P, Barois I, Martin A, Zaidi Z, Schaefer R (1989) Management of earthworm populations in agroecosystems: a possible way to maintain soil quality? In: Clarholm M, Bergström L (eds) Ecology of arable land. perspectives and challenges. Kluwer Academic Publishers, Dordrecht, pp 109–122

    Chapter  Google Scholar 

  • Lavelle P, Pashanasi B, Charpentier F, Gilot C, Rossi J, Derouard L, Andre J, Ponge J, Bernier N (1998) Influence of earthworms on soil organic matter dynamics, nutrient dynamics and microbiological ecology. In: Edwards CA (ed) Earthworm ecology. Lewis Publishers, Boca Raton, FL, pp 103–122

    Google Scholar 

  • Lavelle P, Brussaard L, Hendrix P (1999) Earthworm management in tropical agroecosystems. CABI Publishing, Wallingford, Oxford, UK

    Google Scholar 

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

    Google Scholar 

  • Lopez-Hernandez D, Lavelle P, Fardeau JC, Nino M (1993) Phosphorous transformations in two P-sorption contrasting tropical soils during transit through Pontoscolex corethrurus (Glossoscolecidae: Oligochaeta). Soil Biol Biochem 25:789–792

    Article  CAS  Google Scholar 

  • Ma WC (1982) The influence of soil properties and worm-related factors on the concentrations of heavy metals in earthworms. Pedobiologia 24:109–119

    CAS  Google Scholar 

  • Ma WC (1988) Toxicity of copper to lumbricid earthworms in sandy agricultural soils amended with Cu-enriched organic waste materials. Ecol Bull 39:53–56

    CAS  Google Scholar 

  • Ma WC, Edelman Th, van Beersum I, Jans Th (1983) Uptake of cadmium, zinc, lead and copper by earthworms near a zinc-smelting complex: influence of soil pH and organic matter. Bull Environ Contam Toxicol 30:424–427

    Article  PubMed  CAS  Google Scholar 

  • Mackay AD, Springgett JA, Syers JK, Gregg PEH (1983) Origin of the effect of earthworms on the availability of phosphorus in a phosphate rock. Soil Biol Biochem 15:63–73

    Article  Google Scholar 

  • Marinussen MPJC, van der Zee SEATM (1997) Cu accumulation by Lumbricus rubellus as affected by total amount of Cu in soil, soil moisture and soil heterogeneity. Soil Biol Biochem 29:641–647

    Article  CAS  Google Scholar 

  • Masciandaro G, Ceccanti D, Garcia C (2002) In situ vermicomposting of biological sludges and impacts on soil quality. Soil Biol Biochem 32:1015–1024

    Article  Google Scholar 

  • Morgan JE (1985) The interactions of exogenous and endogenous factors on the uptake of heavy metals by the earthworm Lumbricus rubellus. In: Lekkas TD (ed) Proceedings of the International conference of heavy metals in the environment, vol 1. CEP Consultants Ltd, Edinburg, pp 736–738

    Google Scholar 

  • Morgan JE, Morgan AJ (1988) Calcium-lead interactions involving earthworms. Part 2. The effects of accumulated lead on endogenous calcium in Lumbricus rubellus. Environ Pollut 55:41–54

    Article  PubMed  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 ecotoxicological testing. Appl Soil Ecol 13:9–20

    Article  Google Scholar 

  • Nahmani J, Hodson ME, Black S (2007) A review of studies performed to assess metal uptake by earthworms. Environ Pollut 145:402–424

    Article  PubMed  CAS  Google Scholar 

  • Neuhauser EF, Loehr RC, Milligan DL, Malecki MR (1985) Toxicity of metals to the earthworm Eisenia fetida. Biol Fertil Soils 1:149–152

    Article  CAS  Google Scholar 

  • Nordström S (1975) Seasonal activity of lumbricids in southern Sweden. Oikos 26:307–315

    Article  Google Scholar 

  • Nordström S, Rundgren S (1974) Environmental factors and lumbricid associations in southern Sweden. Pedobiologia 14:1–27

    Google Scholar 

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

    Article  Google Scholar 

  • Parkin TB, Berry EC (1994) Nitrogen transformations associated with earthworm casts. Soil Biol Biochem 26:1233–1238

    Article  Google Scholar 

  • Peramaki P, Itamies J, Karttunen V, Lajunen LHJ, And PE (1992) Influence of pH on the accumulation of cadmium and lead in earthworms (Aporrectodea caliginosa) under controlled conditions. Ann Zool Fenn 29:105–111

    Google Scholar 

  • Phillipson J, Abel R, Steel J, Woodell SRJ (1976) Earthworms and the factors governing their distribution in an English Beachwood. Pedobiologia 16:258–285

    Google Scholar 

  • Rozen A, Mazur L (1997) Influence of different levels of traffic pollution on haemoglobin content in the earthworm Lumbricus terrestris. Soil Biol Biochem 29:709–711

    Article  CAS  Google Scholar 

  • Satchell JE (1967) Lumbricidae. In: Burges A, Raw F (eds) Soil biology. Academic, London, pp 259–322

    Google Scholar 

  • Siekierska E, Urbanska-Jasik D (2002) Cadmium effect on the ovarian structure in earthworm Dendrobaena veneta (Rosa). Environ Pollut 120:289–297

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Spurgeon DJ, Hopkin SP (1996) Effects of metal-contaminated soils on the growth, sexual development, and early cocoon production of the earthworm Eisenia fetida, with particular reference to zinc. Ecotoxicol Environ Saf 35:86–95

    Article  PubMed  CAS  Google Scholar 

  • Suthar S, Singh S, Dhawan S (2008) Earthworms as bioindicator of metals (Zn, Fe, Mn, Cu, Pb and Cd) in soils: is metal bioaccumulation affected by their ecological category? Ecol Eng 32:99–107

    Article  Google Scholar 

  • Tomlin AD, Shipitalo MJ, Edwards WM, Protz R (1995) Earthworms and their influence on soil structure and infiltration. In: Hendrix PF (ed) Earthworm ecology and biogeography in North America. Lewis Publishers, Boca Raton, FL, pp 159–183

    Google Scholar 

  • Van Gestel M, van Dis WA, Dirven-van Breemen EM, Sparenburg PM, Baerselman R (1991) Influence of cadmium copper and pentachlorophenol on growth and sexual development of Eisenia andrei (Oligochaeta, Annelida). Biol Fertil Soils 12:117–121

    Article  Google Scholar 

  • Wang Z, Zhang Y, Guo Y, Xia W, Li Z (1998) Monitoring of soil heavy metal pollution by earthworm. J Environ Sci 10:437–444

    CAS  Google Scholar 

  • Wright MA, Stringer A (1980) Lead, zinc and cadmium content of earthworms from pasture in the vicinity of an industrial smelting complex. Environ Pollut 23:313–321

    Article  CAS  Google Scholar 

  • Zhang B, Li G, Shen T, Wang J, Sun Z (2000) Changes in microbial biomass C, N and P and enzyme activities in soil incubated with the earthworms Metaphire guilelmi or Eisenia fetida. Soil Biol Biochem 32:2055–2062

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Agriculture, Department of Soil Science and Plant Nutrition, Ankara University, Diskapi, Ankara, Turkey

    Oguz Can Turgay & Ayten Karaca

  2. Faculty of Agriculture, Department of Soil Science and Plant Nutrition, Ondokuz Mayis University, Samsun, Turkey

    Ridvan Kizilkaya

  3. Faculty of Forestry, Cankiri Karatekin University, Cankiri, Turkey

    Sema Camci Cetin

Authors
  1. Oguz Can Turgay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ridvan Kizilkaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ayten Karaca
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sema Camci Cetin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ayten Karaca .

Editor information

Editors and Affiliations

  1. , Inst. Allgemeine Botanik u. Pflanzenphys, Universität Jena, Dornburger Str. 159, Jena, 07743, Germany

    Irena Sherameti

  2. Amity Institute of Microbial Sciences, Amity University Uttar Pradesh, Noida, 201303, Uttar Pradesh, India

    Ajit Varma

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Turgay, O.C., Kizilkaya, R., Karaca, A., Cetin, S.C. (2011). Detoxification of Heavy Metals Using Earthworms. In: Sherameti, I., Varma, A. (eds) Detoxification of Heavy Metals. Soil Biology, vol 30. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-21408-0_21

Download citation

Publish with us

Policies and ethics

Search

Navigation