Detoxification of Heavy Metals Using Earthworms

  • Oguz Can Turgay
  • Ridvan Kizilkaya
  • Ayten KaracaEmail author
  • Sema Camci Cetin
Part of the Soil Biology book series (SOILBIOL, volume 30)


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.


Heavy Metal Mineral Soil Total Metal Concentration Earthworm Species Ecological Category 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Ash CPJ, Lee DL (1980) Lead, cadmium, copper and iron in earthworms from roadside sites. Environ Pollut 22:59–67CrossRefGoogle Scholar
  2. 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 44:1291–1301CrossRefGoogle Scholar
  3. 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 57–86Google Scholar
  4. Bengtsson G, Nordstrom S, Rundgren S (1983) Population density and tissue metal concentration of lumbricids in forest soils near a brass mill. Environ Pollut 30:87–108CrossRefGoogle Scholar
  5. Bernier N, Ponge JF (1994) Humus form dynamics during the sylvogenetic cycle in a mountain spruce forest. Soil Biol Biochem 26:183–220CrossRefGoogle Scholar
  6. Beyer WN, Pattee OH, Sileo L, Hoffman DJ, Mulhern BM (1985) Metal contamination in wildlife living near two zinc smelters. Environ Pollut 38:63–86CrossRefGoogle Scholar
  7. 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 30:167–172Google Scholar
  8. 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 29:431–439CrossRefGoogle Scholar
  9. 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 149–172Google Scholar
  10. Cemek B, Kizilkaya R (2006) Spatial variability and monitoring of Pb contamination of farming soils affected by industry. Environ Monit Assess 117:357–375PubMedCrossRefGoogle Scholar
  11. 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 33:651–657CrossRefGoogle Scholar
  12. 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 32:166–171PubMedCrossRefGoogle Scholar
  13. Curry JP, Cotton DCF (1983) Earthworms and land reclamation. In: Satchell JE (ed) Earthworm ecology from Darwin to vermiculture. Chapman and Hall, London, pp 215–228CrossRefGoogle Scholar
  14. Edwards CA (1983) Earthworm ecology in cultivated soils. In: Satchell JE (ed) Earthworm ecology from Darwin to vermiculture. Chapman and Hall, London, pp 123–137CrossRefGoogle Scholar
  15. Edwards CA, Bohlen PJ (1996) Biology of and ecology earthworms, 3rd edn. Chapman and Hall, LondonGoogle Scholar
  16. Edwards CA, Lofty JR (1982a) The effect of direct drilling and minimal cultivation on earthworm populations. J Appl Ecol 19:723–724CrossRefGoogle Scholar
  17. Edwards CA, Lofty JR (1982b) Nitrogenous fertilizers and earthworm populations in agricultural soils. Soil Biol Biochem 14:515–521CrossRefGoogle Scholar
  18. 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 147–161CrossRefGoogle Scholar
  19. 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 57:63–68PubMedCrossRefGoogle Scholar
  20. Fragoso C, Lavelle P (1992) Earthworm communities of tropical rain forests. Soil Biol Biochem 24:1397–1408CrossRefGoogle Scholar
  21. 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, WallingfordGoogle Scholar
  22. Gerard BM (1967) Factors affecting earthworms in pastures. J Anim Ecol 36:235–252CrossRefGoogle Scholar
  23. Gish CD, Christensen RE (1973) Cadmium, nickel, lead and zinc in earthworms from roadside soil. Environ Sci Technol 7:1060–1062PubMedCrossRefGoogle Scholar
  24. Green RN, Trowbridge RL, Klinka K (1993) Towards a taxonomic classification of humus forms. Forest Sci Monogr 29:1–49Google Scholar
  25. 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 35:181–192CrossRefGoogle Scholar
  26. Gullvag BM (1979) Subcellular localization of polluting metals in roadside earthworms exposed to traffic exhaust gases. Cytobios 22:141–153Google Scholar
  27. 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 36:27–34Google Scholar
  28. 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 24:1357–1361CrossRefGoogle Scholar
  29. 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 2007Google Scholar
  30. 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 2010Google Scholar
  31. Herms U, Brümner G (1984) Solubility and retention of heavy metals in soils. J Plant Nutr Soil Sci 147:400–424CrossRefGoogle Scholar
  32. 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, GenevaGoogle Scholar
  33. 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, GenevaGoogle Scholar
  34. 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 51:153–166PubMedCrossRefGoogle Scholar
  35. 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 35:435–440CrossRefGoogle Scholar
  36. 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 369–388CrossRefGoogle Scholar
  37. 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 237–262CrossRefGoogle Scholar
  38. 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 4:213–219CrossRefGoogle Scholar
  39. 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 22:141–151CrossRefGoogle Scholar
  40. 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 25:322–331CrossRefGoogle Scholar
  41. Kizilkaya R (2008) Dehydrogenase activity in Lumbricus terrestris casts and surrounding soil affected by addition of different organic wastes and Zn. Bioresour Technol 99:946–953PubMedCrossRefGoogle Scholar
  42. Kizilkaya R, Askin T (2002) Influence of cadmium fractions on microbiological properties in Bafra plain soils. Arch Agro Soil Sci 48:263–272CrossRefGoogle Scholar
  43. Kizilkaya R, Bayraklı B (2005) Effects of N-enriched sewage sludge on soil enzyme activities. Appl Soil Ecol 30:192–202CrossRefGoogle Scholar
  44. Kizilkaya R, Hepsen S (2004) Effect of biosolid amendment on enzyme activities in earthworm (Lumbricus terrestris) casts. J Plant Nutr Soil Sci 167:202–208CrossRefGoogle Scholar
  45. 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 38:2861–2876CrossRefGoogle Scholar
  46. Kizilkaya R, Askin T, Bayraklı B, Sağlam M (2004) Microbiological characteristics of soils contaminated with heavy metals. Eur J Soil Biol 40:95–102CrossRefGoogle Scholar
  47. 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 2009Google Scholar
  48. 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 2010Google Scholar
  49. 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 2010Google Scholar
  50. 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 141–158CrossRefGoogle Scholar
  51. Lavelle P (1983) The structure of earthworm communities. In: Satchell JE (ed) Earthworm ecology from Darwin to vermiculture. Chapman and Hall, London, pp 449–466CrossRefGoogle Scholar
  52. Lavelle P (1988) Earthworms and the soil system. Biol Fertil Soils 6:237–251CrossRefGoogle Scholar
  53. Lavelle P, Spain AV (2001) Soil ecology. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  54. 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 109–122CrossRefGoogle Scholar
  55. 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 103–122Google Scholar
  56. Lavelle P, Brussaard L, Hendrix P (1999) Earthworm management in tropical agroecosystems. CABI Publishing, Wallingford, Oxford, UKGoogle Scholar
  57. Lee KE (1985) Earthworms: their ecology and relationships with soils and land use. Academic, Sydney, AustraliaGoogle Scholar
  58. 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 25:789–792CrossRefGoogle Scholar
  59. Ma WC (1982) The influence of soil properties and worm-related factors on the concentrations of heavy metals in earthworms. Pedobiologia 24:109–119Google Scholar
  60. Ma WC (1988) Toxicity of copper to lumbricid earthworms in sandy agricultural soils amended with Cu-enriched organic waste materials. Ecol Bull 39:53–56Google Scholar
  61. 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 30:424–427PubMedCrossRefGoogle Scholar
  62. 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 15:63–73CrossRefGoogle Scholar
  63. 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 29:641–647CrossRefGoogle Scholar
  64. Masciandaro G, Ceccanti D, Garcia C (2002) In situ vermicomposting of biological sludges and impacts on soil quality. Soil Biol Biochem 32:1015–1024CrossRefGoogle Scholar
  65. 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 736–738Google Scholar
  66. 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 55:41–54PubMedCrossRefGoogle Scholar
  67. 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 13:9–20CrossRefGoogle Scholar
  68. Nahmani J, Hodson ME, Black S (2007) A review of studies performed to assess metal uptake by earthworms. Environ Pollut 145:402–424PubMedCrossRefGoogle Scholar
  69. Neuhauser EF, Loehr RC, Milligan DL, Malecki MR (1985) Toxicity of metals to the earthworm Eisenia fetida. Biol Fertil Soils 1:149–152CrossRefGoogle Scholar
  70. Nordström S (1975) Seasonal activity of lumbricids in southern Sweden. Oikos 26:307–315CrossRefGoogle Scholar
  71. Nordström S, Rundgren S (1974) Environmental factors and lumbricid associations in southern Sweden. Pedobiologia 14:1–27Google Scholar
  72. Paoletti MG (1999) The role of earthworms for assessment of sustainability and as bioindicators. Agric Ecosyst Environ 74:137–155CrossRefGoogle Scholar
  73. Parkin TB, Berry EC (1994) Nitrogen transformations associated with earthworm casts. Soil Biol Biochem 26:1233–1238CrossRefGoogle Scholar
  74. 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 29:105–111Google Scholar
  75. Phillipson J, Abel R, Steel J, Woodell SRJ (1976) Earthworms and the factors governing their distribution in an English Beachwood. Pedobiologia 16:258–285Google Scholar
  76. Rozen A, Mazur L (1997) Influence of different levels of traffic pollution on haemoglobin content in the earthworm Lumbricus terrestris. Soil Biol Biochem 29:709–711CrossRefGoogle Scholar
  77. Satchell JE (1967) Lumbricidae. In: Burges A, Raw F (eds) Soil biology. Academic, London, pp 259–322Google Scholar
  78. Siekierska E, Urbanska-Jasik D (2002) Cadmium effect on the ovarian structure in earthworm Dendrobaena veneta (Rosa). Environ Pollut 120:289–297PubMedCrossRefGoogle Scholar
  79. Spurgeon DJ, Hopkin SP (1995) Extrapolation of the laboratory based OECD earthworm toxicity test to metal-contaminated field sites. Ecotoxicology 4:190–205CrossRefGoogle Scholar
  80. 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 35:86–95PubMedCrossRefGoogle Scholar
  81. 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 32:99–107CrossRefGoogle Scholar
  82. 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 159–183Google Scholar
  83. 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 12:117–121CrossRefGoogle Scholar
  84. Wang Z, Zhang Y, Guo Y, Xia W, Li Z (1998) Monitoring of soil heavy metal pollution by earthworm. J Environ Sci 10:437–444Google Scholar
  85. Wright MA, Stringer A (1980) Lead, zinc and cadmium content of earthworms from pasture in the vicinity of an industrial smelting complex. Environ Pollut 23:313–321CrossRefGoogle Scholar
  86. 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 32:2055–2062CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Oguz Can Turgay
    • 1
  • Ridvan Kizilkaya
    • 2
  • Ayten Karaca
    • 1
    Email author
  • Sema Camci Cetin
    • 3
  1. 1.Faculty of Agriculture, Department of Soil Science and Plant NutritionAnkara UniversityAnkaraTurkey
  2. 2.Faculty of Agriculture, Department of Soil Science and Plant NutritionOndokuz Mayis UniversitySamsunTurkey
  3. 3.Faculty of ForestryCankiri Karatekin UniversityCankiriTurkey

Personalised recommendations