Welcome to International Network for Natural Sciences | INNSpub

Paper Details

Review Paper | January 1, 2015

| Download 2

Role of earthworms against metal contamination: a review

Zeba Usmani, Vipin Kumar

Key Words:

J. Bio. Env. Sci.6(1), 414-427, January 2015


JBES 2015 [Generate Certificate]


Heavy metal contamination, occurring due to both natural and anthropogenic activities, is a subject of major concern throughout the globe. Increase in heavy metal content can have an adverse impact on functioning of the soil ecosystem by hampering the activities of soil fauna. Earthworms play an important role in metal pollution monitoring and are widely recognized in terrestrial ecosystems. They have an inherent potential for bioaccumulation of metals in their chloragogenous tissues and can be used as an ecological indicator of soil contamination. The present review is focused on: biology and ecology of earthworms, their role as ecosystem engineers and the mechanism involved in uptake, accumulation and excretion of metals by different species of earthworm under varieties of soil. A brief discussion about kinetics of metal accumulation was also laid importance. The review brings these studies together in order to highlight the ability of earthworms to affect metal mobility and its availability in various contaminated sites and elaborates the potential of various species of earthworm to remediate metal dominant substrates.


Copyright © 2015
By Authors and International Network for
Natural Sciences (INNSPUB)
This article is published under the terms of the Creative
Commons Attribution Liscense 4.0

Role of earthworms against metal contamination: a review

Abdul Rida AMM, Bouche MB. 1994 A method to assess chemical biorisks in terrestrial ecosystems. In: Donker MH, Eijackers H, Heimbach F, eds. Ecotoxicology of soil organisms, Lewis, Boca Raton, FL: CRC Press, 383-394.

Atkins GL. 1969. Multicompartment models for biological systems. 153 Seiten. Methuen Co. Ltd., London. Geb. 35s. Food/Nahrung. 15(2), 225. DOI: 10.1002/food.19710150248

Becquer T, Dai J, Quantin C, Lavelle P. 2005. Sources of bioavailable trace metals for earthworms from a Zn, Pb, and Cd-contaminated soil. Soil Biology and Biochemistry 37(8), 1564-1568.

Benitez E, Romero M, Gomez M, Gallardolaro F, Nogales R. 2001. Biosolid and biosolid ash as sources of heavy metals in plant-soil system. Water Air and Soil Pollution 132(1-2), 75-87.

Bhattacharya SS, Iftikar W, Sahariah B, Chattopadhyay GN. 2012. Vermicomposting converts fly ash to enrich soil fertility and sustain crop growth in red and lateritic soils. Resources Conservation and Recycling 65, 100-106.

Brown GG. 1995. How do earthworms affect microfloral and faunal community diversity? The Significance and Regulation of Soil Biodiversity 63, 247-269.

Brown GG, Barois I, Lavelle P. 2000. Regulation of soil organic matter dynamics and microbial activity in the drilosphere and role of interactions with other edaphic functional domains. Eurasian Journal of Soil Biology 36(3-4), 177-198.

Butenschoen O, Ji R, Schaffer A, Scheu S. 2009. The fate of catechol in soil as affected by earthworms and clay. Soil Biology and Biochemistry 41(2), 330-339.

Cheng J, Wong MH. 2002. Effects of earthworms on Zn fractionation in soils. Biology and Fertility of Soils 36(1), 72-78.

Conder JM, Lanno RP. 2000. Evaluation of surrogate measures of cadmium, lead, and zinc bioavailability to Eisenia fetida. Chemosphere 41, 1659-1668.

Conder JM, Seals LD, Lanno RP. 2002. Method for determining toxicologically relevant cadmium residues in the earthworm Eisenia fetida. Chemosphere 49(1), 1-7.

Dai J, Becquer T, Rouiller JH, Reversat G, Bernhard-Reversat F, Nahmani J, Lavelle P. 2004. Heavy metal accumulation by two earthworm species and its relationship to total and DTPA extractable metals in soil. Soil Biology and Biochemistry 36(1), 91-98.

Devliegher W, Verstraete W. 1996. Lumbricus terrestris in a soil core experiment: effects of nutrient-enrichment processes (NEP) and gut-associated processes (GAP) on the availability of plant nutrients and heavy metals. Soil Biology and Biochemistry 28(4-5), 489-496.

Dickinson NM. 2000. Strategies for sustainable woodland on contaminated soils. Chemosphere 41(1-2), 259-263.

Dominguez J. 2004. State of the art and new perspectives on vermicomposting research. In: Edwards CA, ed. Earthworm ecology, Vol. II. Boca Raton, FL: CRC Press, 401-424.

Edwards CA, Bohlen PJ. 1996. Biology and Ecology of Earthworms. Springer science and business media, Vol. III. Chapman and Hall, London, 426.

Edwards CA, Lofty JR. 1972. Biology of Earthworms. Vol. II. Chapman and Hall, London: New York, 283-300.

Frouz J, Pizl V, Tajovsky K. 2007. The effect of earthworms and other saprophagous macrofauna on soil microstructure in reclaimed and un-reclaimed postmining sites in Central Europe. European Journal of Soil Biology 43, S184-S189.

Gomez-Brandon M, Lores M, Dominguez J. 2013. Changes in chemical and microbiological properties of rabbit manure in a continuous-feeding vermicomposting system. Bioresource technology 128, 310-316.

Hobbelen PHF, Koolhaas JE, van Gestel CAM. 2006. Bioaccumulation of heavy metals in the earthworms Lumbricus rubellus and Aporrectodea caliginosa in relation to total and available metal concentrations in field soils. Environmental Pollution 144(2), 639-646.

Ireland MP. 1979. Metal accumulation by the earthworms Lumbricus rubellus, Dendrobaena veneta and Eiseniella tetraeda living in heavy metal polluted sites. Environmental Pollution 19(3), 201-206.

Janssen HH. 1989. Heavy metal analysis in earthworms from an abandoned mining area. Zoologica Anz 222(5/6), 306-321.

Janssen RPT, Posthuma L, Baerselman R, Den Hollander HA, Van Veen RPM, Peijnenburg W.J.G.M. 1997. Equilibrium partitioning of heavy metals in Dutch field soils. II. Prediction of metal accumulation in earthworms. Environmental Toxicology. and Chemistry 16(12), 2479-2488.

Jones TH, Thompson LJ, Lawton JH, Bezemer TM, Bardgett RD, Blackburn TM, Bruce KD, Cannon PF, Hall GS, Hartley SE, Howson G, Jones CG, Kampichler C, Kandeler E, Ritchie DA. 1998. Impacts of rising atmospheric carbon dioxide on model terrestrial ecosystems. Science 280(5362), 441-443.

Kruse EA, Barrett GW. 1985. Effects of municipal sludge and fertilizer on heavy metal accumulation in earthworms. Environmental Pollution Series A, Ecological and Biological 38(3), 235-244.

Langdon CJ, Piearce TG, Meharg AA, Semple KT. 2001. Survival and behaviour of the earthworms Lumbricus rubellus and Dendrodrilus rubidus from arsenate-contaminated and non-contaminated sites. Soil Biology and Biochemistry 33(9), 1239-1244.

Lanno R, Wells J, Conder J, Bradham K, Basta N. 2004. The bioavailability of chemical in soil for earthworms. Ecotoxicology and Environmental Safety 57(1), 39-47.

Laskowski R, Bednarska AJ, Spurgeon D, Svendsen C, van Gestel AM. 2010. Three phase metal kinetics in terrestrial invertebrates exposed to high metal concentrations. Science of the Total Environment 408(18), 3794-3802.

Lavelle P. 1997. Faunal activities and soil processes: adaptive strategies that determine ecosystem function. Advances in Ecological Research, Academic Press, 27, 93-122.

Lazcano C, Gomez-Brandon M, Domınguez J. 2008.Comparison of the effectiveness of composting and vermicomposting for the biological stabilization of cattle manure. Chemosphere 72(7), 1013-1019.

Lee KE. 1985. Earthworms: their ecology and relationship with Soils and land Use. Australia, Academic Press, 56-57.

Lores M, Gomez-Brandon M, Perez D, Dominguez J. 2006. Using FAME profiles for the characterization of animal wastes and vermicomposts. Soil Biology and Biochemistry 38(9), 2993-2996.

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. Biology and Fertility of Soils 36(1), 79-86.

Maboeta MS, Reinecke SA, Reinecke AJ. 2004. The relationship between lysosomal biomarker and organismal responses in an acute toxicity test with Eisenia fetida (Oligochaeta) exposed to the fungicide copper oxychloride. Environmental Research 96(1), 95-101.

Maenpaa KA, Kukkonen JVK, Lydyn MJ. 2002. Remediation of heavy metal-contaminated soils using phosphorus: evaluation of bioavailability using an earthworm bioassay. Archives of Environmental Contamination and Toxicology 43(4), 389-398.

Marino F, Morgan AJ. 1999a. The time-course of metal (Ca, Cd, Cu, Pb, Zn) accumulation from a contaminated soil by three populations of the earthworm, Lumbricus rubellus. Applied Soil Ecology 12(2), 169-177.

Marino F, Morgan AJ. 1999b. Equilibrated body metal concentrations in laboratory exposed earthworms: Can they be used to screen candidate metal-adapted populations? Applied Soil Ecology 12(2), 179-189.

Marinussen MPJC, vander Zee SEATM. 1997. Cu accumulation by Lumbricus rubellus as affected by total amount of Cu in soil, soil moisture and soil heterogeneity. Soil Biology and Biochemistry 29(3-4), 641-647.

Morgan JE, Morgan AJ. 1988. Earthworms as biological monitors of cadmium, copper, lead and zinc in metalliferous soils. Environmental Pollution 54(2), 123-138.

Morgan JE, Morgan AJ. 1989a. Zinc sequestration by earthworm (Annelida: Oligochaeta) chloragocytes. An in vivo investigation using fully quantitative electron probe X-ray microanalysis. Histochemistry 90(5), 405-411.

Morgan JE, Morgan AJ. 1989b. The effect of lead incorporation on the elemental composition of earthworm (Annelida: Oligochaeta) chloragosome granules. Histochemistry 92(3), 237-241.

Morgan JE, Morgan AJ. 1992. Heavy metal concentrations in the tissues, ingesta and faeces of ecophysiologically different earthworm species. Soil Biology and Biochemistry 24(12), 1691-1697.

Morgan JE, Morgan AJ. 1998. The distribution and intracellular compartmentation of metals in the endogeic earthworm Aporrectodea caliginosa sampled from an unpolluted and a metal-contaminated site. Environmental Pollution 99(2), 167-175.

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. Applied Soil Ecology 13(1), 9-20.

Morgan JE, Norey CG, Morgan AJ, Key J. 1989. A comparison of the cadmium-binding proteins isolated from the posterior alimentary canal of the earthworms Dendrodrilus rubida and Lumbricus rubellus. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology 92(1), 15-21.

Nahmani J, Lavelle P. 2002. Effects of heavy metal pollution on soil macrofauna in a grassland of Northern France. Eurasian Journal of Soil Biology 38(3-4), 297-300.

Nannoni F, Protano G, Riccobono F. 2011. Uptake and bioaccumulation of heavy elements by two earthworm species from a smelter contaminated area in northern Kosovo. Soil Biology and Biochemistry 43(12), 2359-2367.

Nei L, Kruusma J, Ivask M, Kuu A. 2009. Novel approaches to bioindication of heavy metals in soils contaminated by oil shale wastes. Oil Shale 26(3), 424-431.

Neuhauser EF, Cukic ZV, Malecki MR, Loehr RC, Durkin PR. 1995. Bioconcentration and biokinetics of heavy metals in the earthworm. Environmental Pollution 89(3), 293-301.

OECD 2004. Guideline for testing of chemical n 222. Earthworm reproduction test (Eisenia fetida/Eisenia andrei), acute toxicity tests, adopted 13 April 2004.

Pattnaik S, Reddy MV. 2009. Assessment of municipal solid waste management in Puducherry (Pondicherry), India. Resources Conservation and Recycling 54(8), 512-520.

Peijnenberg WJGM, Baerselman R, de Groot AC, Jager T, Posthuma L, Van Veen RPM. 1999. Relating environmental availability to bioavailability: Soil type dependent metal accumulation in the oligochaete Eisenia andrei. Ecotoxicology and Environmental Safety 44(3), 294-310.

Pokarzhevskii AD, Zaboyev DP, Ganin GN, Gordienko SA. 1997. Amino acids in earthworms: Are earthworms ecosystemivorous? Soil Biology and Biochemistry 29(3-4), 559-567.

Rada A, El Gharmali A, Elmeray M, Morel JL. 1996. Bioavailability of cadmium and copper in two soils from the sewage farm of Marrakech city (Morocco): effect of earthworms. Agricoltura Mediterranea 126, 364-368.

Reinecke SA, Prinsloo MW, Reinecke AJ. 1999. Resistance of Eisenia fetida (Oligochaeta) to Cadmium after Long-Term Exposure. Ecotoxicology and Environmental Safety 42(1), 75-80.

Richards KS, Ireland MP. 1978. Glycogen-Lead relationship in the earthworm Dendrobaena rubida from a heavy metal site. Histochemistry 56(1), 55-64.

Sary AA, Sari VK. 2014. Effects of ecological changes on the Iron levels and hazard quotient (HQ) on muscle of pelagic, demersal and neritic fish from Khuzestan, south west of Iran. Journal of Biodiversity and Environmental Sciences 5(5), 23-28.

Scaps P, Grelle C, Descamps M. 1997. Cadmium and lead accumulation in the earthworm Eisenia fetida (Savigny) and its impacts on cholinesterase and metabolic pathway enzyme activity. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 116(3), 233-238.

Senapati BK. 1992. Biotic interactions between soil nematodes and earthworms. Soil Biology and Biochemistry 24(12), 1441-1444.

Sheppard S, Evenden W, Cornwell T. 1997. Depuration and uptake kinetics of I, Cs, Mn, Zn, Cd, by the litter earthworm (Lumbricus terrestris) in radiotracer-spiked litter. Environmental Toxicology and Chemistry 16(10), 2106-2112.

Sims RW, Gerard BM. 1985. Earthworms: In Synopses of the British Fauna (New Series) 31 Kermac DM, Barnes RSK, eds. The Linnean Society of London, 171.

Sinha RK, Bharambe G, Chaudhari U. 2008. Sewage treatment by vermifiltration with synchronous treatment of sludge by earthworms: a low-cost sustainable technology over conventional systems with potential for decentralization. Environmentalist 28(4), 409-428.

Sizmur T, Hodson ME. 2009. Do earthworms impact metal mobility and availability in soil? A review. Environmental Pollution 157(7), 1981-1989.

Spurgeon DJ, Hopkin SP. 1996. Risk assessment of the threat of secondary poisoning by metals of predators of earthworms in the vicinity of a primary smelting works. Science of the Total Environment 187(3), 167-183.

Spurgeon DJ, Hopkin SP. 1999. Comparisons of metal accumulation and excretion kinetics in earthworms (Eisenia fetida) exposed to contaminated field and laboratory soils. Applied Soil Ecology 11(2-3), 227-243.

Spurgeon DJ, Hopkin SP, Jones DT. 1994. Effects of cadmium, copper, lead and zinc on growth, reproduction and survival of the earthworm Eisenia fetida (Savigny): Assessing the environmental impact of point-source metal contamination in terrestrial ecosystems. Environmental Pollution (Series A) Ecological and Biological 84(2), 123-130.

Talashikar SC, Powar AG. 1998. Vermibiotechnology for eco-friendly disposal of wastes. Ecotechnology for pollution control and environment management. Indian Journal of Environmental Ecoplanning 7, 535-538.

Terhivuo J, Pankakoski E, Hyvarinen H, Koivisto I. 1994. Lead uptake by ecologically dissimilar earthworm (Lumbricidae) species near a lead smelter in South Finland. Environmental pollution 85(1), 87-96.

Tiunov AV, Scheu S. 2000. Microbial biomass, biovolume and respiration in Lumbricus terrestris L. cast material of different age. Soil Biology and Biochemistry 32(2), 265-275.

Uzoma KO, Iroha AE, Chinyere CG, Sunday EA, Kelechukwu DM, Ahuwaraeze NL. 2013. Effects of mining effluent contaminated soil treated with fertilizers on growth parameters, chlorophyll and proximate composition of Cucurbita pepo vegetable. Journal of Biodiversity and Environmental Sciences 3(9), 1-8.

Weeks JM, Spurgeon DJ, Svendsen C, Hankard PK, Kammenga JK, Dallinger R, Kohler H-R, Simonsen V, Scott-Fordsmand N. 2004. Critical analysis of soil invertebrate biomarkers: a field case study in Avonmouth, UK. Ecotoxicology 13(8), 819-824.

Wen B, Hu X, Liu Y, Wang W, Feng M, Shan X. 2004. The role of earthworms (Eisenia fetida) on influencing bioavailability of heavy metals in soils. Biology and Fertility of Soil 40(3), 181-187.


Style Switcher

Select Layout
Chose Color
Chose Pattren
Chose Background