Skip to main content
Log in

Use of earthworms Eisenia andrei on the bioremediation of contaminated area in north of Tunisia and microbial soil enzymes as bioindicator of change on heavy metals speciation

  • Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

A better understanding is required of the potential of soil biota in controlling the availability and mobility of heavy metals and ascertaining their toxicity. The objectives of this work are to assess, first, the modification of heavy metal speciation induced by earthworms Eisenia andrei and, second, the consequence of this metal speciation change on soil enzyme activities as an easy bioindicator of stress.

Materials and methods

The experiment was conducted on six sites from Jebel Ressas Mines, which are characterized by a gradient heavy metal contamination (Pb, Zn, and Cd). Earthworms E. andrei were introduced in these six soils for 60 days. We had performed heavy metal speciation both in the presence and absence of worms. Modifications of activities of seven enzymes implicated in C, N, and P biochemical cycles were used as a bioindicator of metal stress. We had used the co-inertia statistical method to evaluate the correlation between change in heavy metal speciation induced by earthworms and the enzyme activities in soils.

Results and discussion

Our results suggested that earthworms modified the heavy metal dynamic and speciation. They decrease the amount of metal associated with the most available fraction, such as exchangeable one, and increase the amount of metal bound to the more stable fraction, like Mn and Fe oxide ones. On the same hand, enzyme activities increased in majority of the soils, following earthworm activity, but this effect is dependent on the amount of soil contamination. Moreover, the co-inertia results denote that change in heavy metal speciation significantly influences the soil enzyme activities in Jebel Ressas soils, especially β-glucosidase, urease, deshydrogenase, and fluorescein diacetate hydrolysis (FDA), and can be considered as bioindicators of metal toxicity and biological quality in the contaminated area.

Conclusions

By reducing the availability of heavy metals, the earthworms are useful in the bioremediation of heavy metal contaminated soils. Soil enzymes β- glucosidase, urease, deshydrogenase, and FDA can be used to assess the changes in metal speciation and can let us, therefore, predict if the soils are bioremediated.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Bahadir T, Bakan G, Altaş L, Buyukgungor H (2007) The investigation of lead by biosorption: An application at storage battery industry wastewaters. Enzym Microb Technol 41:98–102

    Article  CAS  Google Scholar 

  • Bohlen JP (2002) Earthworms. Encyclopedia of Soil Science, 370–373

  • Borowik A, Wyszkowska J, Kucharski J, Baćmaga M, Tomkiel M (2017) Response of microorganisms and enzymes to soil contamination with a mixture of terbuthylazine, mesotrione, and S-metolachlor. Environ Sci Pollut Res Int 24(2):1910–1925

    Article  CAS  Google Scholar 

  • Boughattas I, Hattab S, Boussetta H, Sappin-Didier V, Viarengo A, Banni M, Sforzini S (2016) Biomarker responses of Eisenia andrei to a polymetallic gradient near a lead mining site in North Tunisia. Environ Pollut 218:530–541

    Article  CAS  Google Scholar 

  • Boughattas I, Hattab S, Boussetta H, Banni M, Navarro E (2017) Impact of heavy metal contamination on oxidative stress of Eisenia andrei and bacterial community structure in Tunisian mine soil. Environ Sci Pollut Res 24(22):18083–18095

    Article  CAS  Google Scholar 

  • Casida L, Klein D, Santoro T (1964) Soil Dehydrogenase Activity. Soil Sci 98:371–376

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ciarkowska K, Sołek-Podwika K, Wieczorek J (2014) Enzyme activity as an indicator of soilrehabilitation processes at a zinc and Lead ore mining and processing area. J Environ Manag 132:250–256

    Article  CAS  Google Scholar 

  • Coyle C, Duggan P, Godinho M, McGrath D (1999) The development of a phytoremediation technique for the detoxification of soils contaminated with phenolic compounds using horseradish peroxidase (Armoracia rusticana): preliminary results. Int J Phytoremediat 1(2):189–202

    Article  CAS  Google Scholar 

  • D’Ascoli R, Rao MA, Adamo P, Renella G, Landi L, Rutigliano FA, Terribile F, Gianfreda L (2006) Impact of river overflowing on trace element contamination of volcanic soils in south Italy: Part II. Soil biological and biochemical properties in relation to trace element speciation. Environ Pollut 144:317–326

    Article  CAS  Google Scholar 

  • Doledec S, Chessel D (1994) Co-inertia analysis: an alternative method for studying species-environment relationships. Freshw Biol 31:277–294

    Article  Google Scholar 

  • Dray S, Chessel D, Thioulouse J (2003) Co-inertia analysis and the linking of ecological data tables. J Ecol 84(11):3078–3089

    Article  Google Scholar 

  • Ghorbel M, Munoz M, Solmon F (2014) Health hazard prospecting by modeling wind transfer of metal-bearing dust from mining waste dumps: application to Jebel RessasPb–Zn–Cd abandoned mining site (Tunisia). Environ Geochem Health 36:935–951

    Article  CAS  Google Scholar 

  • Gianfreda L, Bollag JM (1996) Influence of natural and anthropogenic factors on enzyme activity in soil. In: Stotzky G, Bollag JM (eds) Soil biochemistry, vol 9. Marcel Dekker, New York, pp 123–194

  • Haberern J (1992) Viewpoint: A Soil health index. J Soil Water Conserv 47:6

    Google Scholar 

  • Han Y, Ni Z, Li S, Qu M, Tang F, Mo R, Ye C, Liu Y (2018) Distribution, relationship, and risk assessment of toxic heavy metals in walnuts and growth soil. Environ Sci Pollut Res Int. https://doi.org/10.1007/s11356-018-1896-3

  • Harmsen J (2007) Measuring bioavailability: from a scientific approach to standard methods. J Environ Qual 36:1420–1428

    Article  CAS  Google Scholar 

  • He MM, Tian GM, Liang XQ (2009) Phytotoxicity and speciation of copper, zinc and lead during the aerobic composting of sewage sludge. J Hazard Mater 163:671–677

    Article  CAS  Google Scholar 

  • Hinojosa MB, Carreira JA, Garcia-Ruiz R, Dick RP (2004) Soil moisture pretreatment effects on enzyme activities as indicators of heavy metal-contaminated and reclaimed soils. Soil Biol Biochem 36:1559–1568

    Article  CAS  Google Scholar 

  • 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. Environ Pollut 144:639–646

    Article  CAS  Google Scholar 

  • Hu W, Jiao Z, Wu F, Liu Y, Dong M, Ma X, Fan T, An L, Feng H (2014) Long-term effects of fertilizer on soil enzymatic activity of wheat field soil in Loess Plateau, China. Ecotoxicology 23(10):2069–2080. https://doi.org/10.1007/s10646-014-1329-0

    Article  CAS  Google Scholar 

  • Jenny H (1980) The soil resource - origin and behavior. Springer, New York, p 377

    Book  Google Scholar 

  • Jusselme MD, Poly F, Miambi E, Mora P, Blouin M, Pando A (2012) Effect of earthworms on plant Lantana camara Pb-uptake and on bacterial communities in root-adhering soil. Sci Total Environ 416:200–207

    Article  CAS  Google Scholar 

  • Kandeler E, Kampichler C, Horak O (1996) Influence of heavy metals on the functional diversity of soil microbial communities. Boil Fertil Soils 23:299–309

    Article  CAS  Google Scholar 

  • Kaur P, Bali S, Sharma A, Pal Vig A, Bhardwaj R (2017) Effect of earthworms on growth, photosynthetic efficiency and metal uptake in Brassica juncea L. plants grown in cadmium-polluted soils. Environ Sci Pollut Res Int 24:13452–13465

    Article  CAS  Google Scholar 

  • Klose S, Tabatabai MA (2000) Urease activity of microbial biomass in soils as affected by cropping systems. Biol Fertil Soils 31:191–199

    Article  CAS  Google Scholar 

  • Lee YB, Lorenz N, Dick LK, Dick RP (2007) Cold storage and pretreatment incubation effects on soil microbial properties. Soil Sci Soc Am 71:1299–1305

    Article  CAS  Google Scholar 

  • Lemtiri A, Liénard A, Alabi T, Brostaux Y, Cluzeau D, Francis F, Colinet G (2016) Earthworms Eisenia fetida affect the uptake of heavy metals by plants Vicia faba and Zea mays in metal-contaminated soils. Appl Soil Ecol 104:67–78. https://doi.org/10.1016/j.apsoil.2015.11.021

  • Li L, Wu J, Tian G, Xu Z (2009) Effect of the transit through the gut of earthworm (Eisenia fetida) on fractionation of Cu and Zn in pig manure. J Hazard Mat 167:634–640

  • Li LXY, Xu ZL, Wu JY, Tian GM (2010) Bioaccumulation of heavy metals in the earthworm Eisenia fetida in relation to bioavailable metal concentrations in pig manure. Bioresour Technol 101:3430–3436

    Article  CAS  Google Scholar 

  • Lipiec J, Frąc M, Brzezińska M, Turski M, Oszust K (2016) Linking microbial enzymatic activities and functional diversity of soil around earthworm burrows and casts. Front Microbiol 7:1361

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Liu X, Li X, Guo R, Kuzyakov Y, Li F (2015) The effect of plastic mulch on the fate of urea-N in rainfed maize production in a semiarid environment as assessed by N-15-labeling. Eur J Agron 70:71–77

    Article  CAS  Google Scholar 

  • Lock K, Janssen CR (2003) Influence of aging on metal availability in soils. In: Reviews of environmental contamination and toxicology (pp. 1–21). Springer, New York

  • 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

  • Lv B, Xing M, Yang J (2016) Speciation and transformation of heavy metals during vermicomposting of animal manure. Bioresour Technol 209:397–401

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ma SC, Zhang HB, Ma ST, Wang R, Wang GX, Shao Y, Li CX (2015) Effects of mine wastewater irrigation on activities of soil enzymes and physiological properties, heavy metal uptake and grain yield in winter wheat. Ecotoxicol Environ Saf 113:483–490

    Article  CAS  Google Scholar 

  • Ma X, Xing M, Wang Y, Xu Z, Yang J (2016) Microbial enzyme and biomass responses: deciphering the effects of earthworms and seasonal variation on treating excess sludge. J Environ Manag 170:207–214

    Article  CAS  Google Scholar 

  • Meng J, Tao M, Wang L, Liu X, Xu (2018) Changes in heavy metal bioavailability and speciation from a Pb-Zn mining soil amended with biochars from co-pyrolysis of rice straw and swine manure. Sci Total Environ 633:300–307

    Article  CAS  Google Scholar 

  • Minkina T, Nevidomskaya D, Bauer T, Shuvaeva V, Soldatov A, Mandzhieva S, Zubavichus Y, Trigub A (2018) Determining the speciation of Zn in soils around the sediment ponds of chemical plants by XRD and XAFS spectroscopy and sequential extraction. Sci Total Environ 12(634):1165–1173

    Article  CAS  Google Scholar 

  • Norvell WA (1984) Comparison of Chelating Agents for metals in diverse soil materials. Soil Sci Soc Am J 48:1285–1292

    Article  CAS  Google Scholar 

  • OECD (2004) Guideline for the Testing of Chemicals No. 222. Earthworm Reproduction Test (Eisenia fetida/Eisenia Andrei). Organization for Economic Cooperation and Development, Paris

    Google Scholar 

  • Pankhurst CE, Doube BM, Gupta VVSR (1997) Biological indicators of soil health: synthesis. In: Pankhurst CE, Doube BM, Gupta VVSR (eds) Biological indicators of soil health. CABI, Wallingford, pp 419–435

    Google Scholar 

  • Pérez-Marín AB, Zapata VM, Ortuño JF, Aguilar M, Sáez J, Lloréns M (2007) Removal of cadmium from aqueous solutions by adsorption onto orange waste. Hazard Mater 136(1):122–131

    Article  CAS  Google Scholar 

  • Ruiz E, Alonso-Azcarate J, Rodriguez L (2011) Lumbricus terrestris L. activity increases the availability of metals and their accumulation in maize and barley. Environ Pollut 159:722–728

    Article  CAS  Google Scholar 

  • Saif S, Khan MS (2018) Assessment of toxic impact of metals on proline, antioxidant enzymes, and biological characteristics of Pseudomonas aeruginosa inoculated Cicer arietinum grown in chromium and nickel-stressed sandy clay loam soils. Environ Monit Assess 190(5):290

    Article  CAS  Google Scholar 

  • Sanchez-Hernandez JC, Notario Del Pino J, Capowiez Y, Mazzia C, Rault M (2018) Soil enzyme dynamics in chlorpyrifos-treated soils under the influence of earthworms. Sci Total Environ 15:1407–1416

    Article  CAS  Google Scholar 

  • Schnürer J, Rosswall T (1982) Fluorescein diacetate hydrolysis as a measure of total microbial activity in soil and litter. Appl Environ Microbiol 43(6):1256–1261

    Google Scholar 

  • Shankar T, Mariappan V, Isaiarasu L (2011) Screening cellulolytic bacteria from the mid-gut of the popular composting earthworm, Eudrilus eugeniae (Kinberg). World J Zool 6(2):142–148

    Google Scholar 

  • Shen G, Lu Y, Zhou Q, Hang J (2005) Interaction of polycyclic aromatic hydrocarbons and heavy metals on soil enzyme. Chemosphere 61:1175–1182

    Article  CAS  Google Scholar 

  • Silveira RSA, Megreiros DH, Lozinski R, Almeida FA, Wajmsztazn GM, Oliveira LCK (1979) Estudo da Bacia Rio Paraiba do Sul. Trecho Funil-Stalecilia Guandu, Cadernos FEEMA, Ser. Tec. 9/79

  • Silveira ML, Alleoni LRF, O’Connor GA, Chang AC (2006) Heavy metal sequential extraction methods - a modification for tropical soils. Chemosphere 64:1929–1938

    Article  CAS  Google Scholar 

  • Sivakumar S, Subbhuraam CV (2005) Toxicity of chromium (III) and chromium (VI) to the earthworm Eisenia fetida. Ecotoxicol Environ Saf 62(1):93–98

    Article  CAS  Google Scholar 

  • Sivakumar S, Nityanandi D, Barathi S, Prabha D, Rajeshwari S, Son HK, Subbhuraam CV (2012) Selected enzyme activities of urban heavy metal-polluted soils in the presence and absence of an oligochaete, Lampito mauritii (Kinberg). J Hazard Mater 227–228

  • Sivakumar S, Prabha S, Barathi D, Nityanandi C, Subbhuraam T, Seralathan S, Kamala-Kannan, Jang P, Yi I (2015) The influence of the earthworm Lampito mauritii (Kinberg) on the activity of selected soil enzymes in cadmium-amended soil. Environ Monit Assess 187:174–178

    Article  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 

  • Sizmur T, Palumbo-Roe B, Watts MJ, Hodson ME (2011) Impact of the earthworm Lumbricus terrestris (L.) on As, Cu, Pb and Zn mobility and speciation in contaminated soils. Environ Pollut 159:742–748

    Article  CAS  Google Scholar 

  • Souissi R, Souissi F, Chakroun HK, Bouchardon JL (2013) Mineralogical and geochemical characterization of mine tailings and Pb, Zn, and cd mobility in a carbonate setting (northern Tunisia). Mine Water Environ 32:16–27

    Article  CAS  Google Scholar 

  • Spurgeon DJ, Weeks JM, Van Gestel CAM (2003) A summary of eleven years progress in earthworm ecotoxicology: the 7th international symposium on earthworm ecology, Cardiff, Wales. Pedobiologia 47:588–606

    Google Scholar 

  • Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA (2005) Principles and applications of soil microbiology, 2nd edn. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Tabatabai MA (1994) Soil enzymes. In: Methods of soil analysis: microbiological and biochemical properties. Part 2. SSSA Book Ser, Madison, pp 775–833

  • Tejada L, Abellán A, Cayuela JM, Martínez Cacha A, Fernández-Salguero J (2008) Proteolysis in goats’ milk cheese made with calf rennet and plant coagulant. Int Dairy J 18:139–146

    Article  CAS  Google Scholar 

  • Tessier A, Campbell P, Bisson M (1979) Sequential Extraction Procedure for the Speciation of Particulate Trace Metals. Anal Chem 51:844–851

    Article  CAS  Google Scholar 

  • Thioulouse J, Dray S (2007) Interactive multivariate data analysis in R with the ade4 and ade4TkGUI packages. J Stat Softw 22(5):1–14

    Article  Google Scholar 

  • Turgay OC, Görmez A, Bilen S (2012) Isolation and characterization of metal resistant-tolerant rhizosphere bacteria from the serpentine soils in Turkey. Environ Monit Assess 184(1):515–526

    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 

  • Uwizeyimana H, Wang M, Chen W, Khan K (2017) The eco-toxic effects of pesticide and heavy metal mixtures towards earthworms in soil. Environ Toxicol Pharmacol 55:20–29

    Article  CAS  Google Scholar 

  • Wang D, Li H, Wei Z, Wang X, Hu F (2006) Effect of earthworms on the phytoremediation of zincpolluted soil by ryegrass and Indian mustard. Biol Ferti Soils 43:120–123

    Article  Google Scholar 

  • Wang YP, Shi J, Wang H, Lin Q, Chen X, Chen Y (2007) The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotoxicol Environ Saf 67:75–81

    Article  CAS  Google Scholar 

  • Wang Y, Han W, Wang X, Chen H, Zhu F, Wang X, Lei C (2017) Speciation of heavy metals and bacteria in cow dung after vermicomposting by the earthworm, Eisenia fetida. Bioresour Technol 245:411.418

    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 Ferti Soils 40:181–187

    Article  CAS  Google Scholar 

  • Wyszkowska J, Kurcharski J, Lajszner W (2006) The effects of copper on soil biochemical properties and its interaction with other heavy metals. Pol J Environ Stud 15:927–934

    CAS  Google Scholar 

  • Xia X, Lin S, Zhao J, Zhang W, Lin K, Lu Q, Zhou B (2018) Toxic responses of microorganisms to nickel exposure in farmland soil in the presence of earthworm (Eisenia fetida). Chemosphere 192:43–50

    Article  CAS  Google Scholar 

  • Yadav A, Suthar S, Garg VK (2015) Dynamics of microbiological parameters, enzymatic activities and worm biomass production during vermicomposting of effluent treatment plant sludge of bakery industry. Environ Sci Pollut Res Int 22(19):14702–14709

    Article  CAS  Google Scholar 

  • Yang J, Zhao C, Xing M, Lin Y (2013) Enhancement stabilization of heavy metals (Zn, Pb, Cr and Cu) during vermifiltration of liquid-state sludge. Bioresour Technol 146:649–655

    Article  CAS  Google Scholar 

  • Yeardley JR, Lazorchak RB, Cast LC (1996) The potential of an earthworm avoidance test for evaluation of hazardous waste sites. Environ Toxicol Chem 15:1532–1537

    CAS  Google Scholar 

  • Yin SU, Xinzhong Y, Guangming Z (2008) Study on Influence Factors of Transport and Transformation of Pb in Soil-plant System [J]. J Anhui Agric Sci 16:145

    Google Scholar 

  • Yu X, Cheng J, Wong MH (2005) Earthworm–mycorrhiza interaction on Cd uptake and growth of ryegrass. Soil Biol Biochem 37:195–201

    Article  CAS  Google Scholar 

  • Zeng LS, Liao M, Chen CL, Huang CY (2007) Effects of lead contamination on soil enzymatic activities, microbial biomass, and rice physiological indices in soil-lead-rice (Oryza sativa L.) system. Ecotoxicol Environ Saf 67:67–74

    Article  CAS  Google Scholar 

  • Zhang YL, Chen LJ, Sun CX, Wu ZJ, Chen ZH, Dong GH (2010) Soil hydrolase activities and kinetic properties as affected by wheat cropping systems of northeastern China. Plant Soil Environ 56(11):526–532

    Article  CAS  Google Scholar 

  • Zhao K, Liu J Xu X, Selim HM (2010) Heavy metals contaminations in a soil-rice system: Identification of spatial dependence in relation to soil properties of paddy fields. J Hard Mater 181(1-3):778–787. https://doi.org/10.1016/j.jhazmat.2010.05.081

    Article  CAS  Google Scholar 

  • Zhao L, Sun YL, Cui SX, Chen M, Yang HM, Liu HM (2011) Cd-induced changes in leaf proteome of the hyperaccumulator plant Phytolacca americana. Chemosphere 85:56–66

    Article  CAS  Google Scholar 

  • Zorn MI, Van Gestel CAM, Eijsackers H (2005a) The effect of Lumbricus rubellus and Lumbricus terrestris on zinc distribution and availability in artificial soil columns. Biol Fert Soils 41:212–215

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was also supported by funds from the “Ministère de l’Enseignement Supérieur et de la Recherche Scientifique; UR04A6R05.Biochimie et Toxicologie Environnementale” and by the Mistral Project “Them SICMED.”

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Iteb Boughattas.

Additional information

Responsible editor: Daniel C.W. Tsang

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boughattas, I., Hattab, S., Alphonse, V. et al. Use of earthworms Eisenia andrei on the bioremediation of contaminated area in north of Tunisia and microbial soil enzymes as bioindicator of change on heavy metals speciation. J Soils Sediments 19, 296–309 (2019). https://doi.org/10.1007/s11368-018-2038-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-018-2038-8

Keywords

Navigation