Journal of Soils and Sediments

, Volume 19, Issue 1, pp 296–309 | Cite as

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

  • Iteb BoughattasEmail author
  • Sabrine Hattab
  • Vanessa Alphonse
  • Alexandre Livet
  • Stéphanie Giusti-Miller
  • Hamadi Boussetta
  • Mohamed Banni
  • Noureddine Bousserrhine
Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article



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.


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.


Bioindicator Bioremediation Earthworm Heavy metal speciation Soil Soil enzymes 



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.”


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Iteb Boughattas
    • 1
    Email author
  • Sabrine Hattab
    • 2
  • Vanessa Alphonse
    • 3
  • Alexandre Livet
    • 3
  • Stéphanie Giusti-Miller
    • 4
  • Hamadi Boussetta
    • 1
  • Mohamed Banni
    • 1
  • Noureddine Bousserrhine
    • 3
  1. 1.Laboratory of Biochemistry and Environnemental ToxicologyHigher Institute of AgronomySousseTunisia
  2. 2.Regional Research Centre in Horticulture and Organic AgricultureSousseTunisia
  3. 3.Leesu (Laboratoire Eau, Environnement et Systèmes Urbains)Université Paris-Est CréteilParisFrance
  4. 4.Institut d’Ecologie et des Sciences de l’EnvironnementUniversité Paris-Est CréteilParisFrance

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