Heavy metal transport and fate in soil-plant system: study case of industrial cement vicinity, Tunisia

  • Ines Terwayet BayouliEmail author
  • Beatriz Gómez-Gómez
  • Houssem Terwayet Bayouli
  • Teresa Pérez-Corona
  • Erik Meers
  • Emna Ammar
  • Ali Ferchichi
  • Yolanda Madrid Albarrán
Original Paper


During the last decades, Southeastern Tunisia has suffered from an industrial expansion leading to a serious pollution problem. In this work, heavy metal contamination near Gabes cement plant (Southeastern Tunisia) was assessed in the soils and statistically compared with a control site located 12 km away. Soil samples were collected from 5 to 15 cm below the surface layer. Concentrations of Cr, Mn, Co, Ni, Cu, Zn, Cd, Pb, and Fe and chemical parameters (conductivity, pH, CaCO3, OM) were measured. The variance analysis exhibited a significant difference (p < 0.05) in metal content between the two sites reflecting the cement plant contamination effect on the surrounding area. Eleven plant species widely distributed in the study area were collected together with the soil in which they were rooted, to assess their phytoextraction potential. Principal component analysis (PCA) was applied to understand the complex connection between soil, plants, and heavy metal contents. Lygeum spartum with respective total bioaccumulation factor (MBF = 1.48 ˃ 1 and Echiochilon fruticosum with a total translocation factor (MTF = 7.06) ˃ 1 were revealed as pertinent candidates for phytoremediation applications.


Topsoils Cement plant pollution Heavy metals Plant species Bioaccumulation factor Phytoremediation 



We thank the University Complutense de Madrid especially the Laboratory team of analytical chemistry. Special thanks to Pr. Houcine Khatelli the director of Arid Regions Institute, Tunisia, for all the facilities he offered for the realization of this study.

Funding information

This study was supported by the Spanish Commission of Science and Technology (CTQ2014-54801-C2-1-R) and the Community of Madrid FEDER programme S2013/ABI-3028, AVANSECAL-CM.


  1. Addinsoft. XLSTAT (2016). Data analysis and statistical solution for Microsoft excel. Paris, FranceGoogle Scholar
  2. Adriano A, Wenzel W, Vangrosveld C, Boland NS (2004) Role of assisted natural remediation in environmental cleanup. Geoderma 122:121–142CrossRefGoogle Scholar
  3. Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability and risks of metals 2nd. ed. New York; SpringerGoogle Scholar
  4. Ahemad M, Khan MS (2012) Effect of fungicides on plant growth promoting activities of phosphate solubilizing Pseudomonas putida isolated from mustard (Brassica compestris) rhizosphere. Chemosphere 86:945–950CrossRefGoogle Scholar
  5. Ahluwalia S, Goyal D (2007) Microbial and plant derived biomass for removal of heavy metals from wastewater. Bioresour Technol 98:2243–2257CrossRefGoogle Scholar
  6. Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals–concepts and applications. Chemosphere 91:869–881CrossRefGoogle Scholar
  7. Al-Kashman O and Shawabkeh RA, (2006). Metal distribution in soils around cement factory in southern Jordan. Editions Elsevier. J Environ Pollut (140):387–394Google Scholar
  8. Anjum NA, Pereira ME, Ahmad I, Duarte AC, Umar S, Kahar N (2013) Phytotechnologies: remediation of environmental contaminants. CRC Press Taylor and Françis Group editions, Floride 579pGoogle Scholar
  9. Arrivabenes H, Campos C, Souza L, Wunderlin D, Milanez C, Machado S, (2016). Differential bioaccumulation and translocation patterns in 3 mangrove plants experimentally exposed to iron. Consequences for environmental sensing. Environ Pollut (215) 302-313CrossRefGoogle Scholar
  10. Bermudez GMA, Moreno M, Invernizzi R, Plà R, Pignata ML (2010) Heavy metal pollution in topsoils near a cement plant: the role of organic matter and distance to the source to predict total and HCl-extracted heavy metal concentrations. Chemosphere 78:375–381CrossRefGoogle Scholar
  11. Boeken B, Ariza C, Gutterman Y, & Zaady E (2004) Environmental factors affecting dispersal, germination and distribution of Stipa capensis in the Negev Desert, Israel. Ecol Res 19(5):533–540Google Scholar
  12. Botuga P, D’orazio V, Sokolowska Z, Senesi N, 2016. Effect of selected chemical and physicochemical properties of humic acids from peat soils on their interaction mechanisms with copper ions at various pHs. Geochem explor (168)119–126Google Scholar
  13. Boukhris A, Laffont Schwob I, Mezghany I, El Kadri L, Prudent P, Pricop A, Tatoni T, Chaeib M (2015) Screening biological traits and fluoride contents of native vegetations in arid environments to select efficiently fluoride tolerant native plant species for in situ phytoremediation. Chemosphere 119:217–223CrossRefGoogle Scholar
  14. Campo J, Marti G (2004) Comparison of floristic changes on vegetation affected by different levels of soils erosion in Miocene clays and Eocene marls from Northeast Spain. Plant Ecol 173:83–93CrossRefGoogle Scholar
  15. Commissariat Regional de Développement Agricole (CRDA), (2005). Le gouvernorat de Gabès en chiffres en 2005. Ministère de Développement économique. Office de Développement du Sud. Editions CRDA. 32 pGoogle Scholar
  16. Conesa HM, Robinson BH, Schulin R, & Nowack B (2007) Growth of Lygeum spartum in acid mine tailings: response of plants developed from seedlings, rhizomes and at field conditions. Environ Pollut 145(3):700–707Google Scholar
  17. Conesa M, Faz A (2011) Metal uptake by spontaneous vegetation in acidic mine tailings from semi-arid area in South Spain: implications for revegetation and land management. Wat Soil Pollut 215:221–227CrossRefGoogle Scholar
  18. De Santiago-Martin A, Valverde-Asenjo I, Quintana JR, Vasquez A, Lafuente AL, Huecas CG, (2014). Carbonates, organic and clay fractions determine metal bioavailability in periurban calcareous agricultural soils in the Mediterranean area. Geoderma (221–222)103–112Google Scholar
  19. Deng H, Ye Z, Wong M (2004) Accumulation of lead, zinc, copper and cadmium by 12 wetland plant species thriving in metal contaminated sites in China. Environ Pollut 132:29–40CrossRefGoogle Scholar
  20. Dewald U, Achternbosch M, (2016). Why did more sustainable cements failed so far? Disruptive innovations and their barriers in a basic industry. Environ Innovat Soci trans (19)15-30Google Scholar
  21. Dhiman S, Selvaraj C, Li J, Singh R, Zhao X, Kim D, Kim J Y, Kang Y C, Lee J K, (2016). Phytoremediation of metal-contaminated soils by the hypperaccumulator canola (Brassica napus L.) and the use of its biomass for ethanol production. Fuel (183)107-114Google Scholar
  22. Esmaeli A, Moore F, Keshavarzi B, Jaafarzadeh N, Kermani M (2014) A geochemical survey of heavy metals in agricultural and background soils of the Isfahan industrial zone, Iran. Catena 121:88–98CrossRefGoogle Scholar
  23. Fuentes A, Salazar C, Torres J, Cano E, Valle F, (2001). Review of communities of Lygeum spartum L. in the Southeastern Iberian Peninsula (Western Mediterranean). J. Arid Environ (48) 323–339Google Scholar
  24. Gianfagna A, (2014). Periodico di Mineralogia. Nuova Cultura, Rome Italy,Vol 83.5. 299pGoogle Scholar
  25. Gomes M A C, Hauser-Davis R A, De Souza AN, Vitorià AP, (2016). Metal phytoremediation: general strategies, genetically modified plants and applications in metal nanoparticle contamination. Ecotox Environ Saf (134)133–147CrossRefGoogle Scholar
  26. Guo G, Zhou Q, Ma L, (2006). Availability and assessment of fixing additives for the in-situ remediation of heavy metal contaminated soils: a review. Environ Monit Assess (116) 513-528CrossRefGoogle Scholar
  27. Haydar A, (1987). Industrialisation de gabes et ses conséquences. Etude géographie urbaine et économique. Édité par l’université de Tunis Faculté des Lettres et Sciences Humaines de Tunis.Volume XIX. 194pGoogle Scholar
  28. Houben D, Evrad L, Sonnet P, (2013). Mobility, bioavailability and pH-dependent leaching of cadmium, zinc, lead in a contaminated soil amended with biochar. Chemosphere (92)1450-1475Google Scholar
  29. Isikli B, Demir TA, Akar T, Berber A, Urer SM, Kalyonucu C, Canbek M (2006) Cadmium exposure from the cement dust emissions: a field study in a rural residence. Chemosphere 63:1546–1552CrossRefGoogle Scholar
  30. Kashem M, Singh B (2001) Metal availability in contaminated soil: effecting of flooding and organic matter on changes in eh, pH and solubility of cadmium, nickel and zinc. Nut Cycl Agroecos 61(3):247–255CrossRefGoogle Scholar
  31. Kowalska J, Mazurek R, Gasiorek M, Setlak M, Zaleski T, Waroszewski J, (2016). Soil pollution indices conditioned by medieval metallurgical activity- a case study from Krakow (Poland). Environ pollut(218)1023–1036Google Scholar
  32. Lange B, Van der Int A, Baker AJ, Echevarria G, Mahy G, Malaisse F, Meerts P, Pourret G, Verbruggen N, Faucon ML (2016) Copper and cobalt accumulation in plants: a critical assessment of the current state of knowledge. New Phytol 213:537–551CrossRefGoogle Scholar
  33. Leguizamo M A O, Gomez W D F, Sarmiento M C G, (2017). Native herbaceous plant species with potential use in phytoremediation of heavy metals, spotlights in wetlands. Chemosphere (168)1230-1247Google Scholar
  34. Leyton JM, Navarro-Ramos MJ, Munez-Vallès S, Fiqueroa E, Cambrollé J (2016) Evaluation of the potential of Atriplex halimus stem cuttings for phytoremediation of metal-polluted soils. Ecol Eng 97:553–557CrossRefGoogle Scholar
  35. Liang S, Jin Y, Liu W, Li X, Shen S, (2017). Feasibility of Pb phytoextraction using nano-materials assisted ryegrass: results of one year field scale. J. Environ Manage (190)170-175Google Scholar
  36. Lim J M, Salido A L, Butcher D J, (2004). Phytoremediation of lead using Indian mustard (Brassica Juncea) with EDTA and electrodics. J. Microchem (76) 3-9CrossRefGoogle Scholar
  37. Martin MH (2012) Biological of heavy metal pollution: land and air. Editions Applied Sciences Publishers, Bristol 391pGoogle Scholar
  38. Nguyen T,Amyot M, Labrecque M, (2017). Differential root systems on nickel, copper and silver bioavailability in contaminated soil. Chemosphere (168)131-138CrossRefGoogle Scholar
  39. Ogundiran M B et Osibango O, (2008). Heavy metals concentrations in soils and accumulation in plants growing in a deserted slag dumpsite in Nigeria. J. Afr Biotechno (17) 3053-3060Google Scholar
  40. Ogunkunle C O, Fatoba P O, (2014). Contamination and spatial distribution of heavy metals in topsoils surrounding a mega cement factory. Atm. Pol. Res (5) 270-282CrossRefGoogle Scholar
  41. Pignatteli S, Colzi I, Buccianti A, Cecchi L, Arnetoli M, Monani R, Gabrielli R, Gonneli C, (2012). Exploring element accumulation patterns of a metal excluder plant naturally colonizing a highly contaminated soil. J. Hazard. Mater. (222-228) 362-369Google Scholar
  42. Pilon Smits E, (2005). Phytoremediation. Annu. Rev.Plant Biol (56)15–39CrossRefGoogle Scholar
  43. Qureshi AS, Hussain MI, Ismail S, Khan QM (2016) Evaluating heavy metal accumulation and potential health risks in vegetables irrigated with treated waste water. Chemosphere 163:54–61CrossRefGoogle Scholar
  44. Read DS, Matzke M, Gweon HS, Newbold LK, Heggelund L, Ortiz MD, Lahive E, Spurgeon D, Svensen C (2015) Soil pH effects on the interactions between dissolved zinc, non nano and ZnO with soil bacterial communities. Environ Sci Pol Res 23(5):4120–4128CrossRefGoogle Scholar
  45. Reijonen I, Metzler M, Hartikainen H (2016) Impact of soil pH and organic matter on the chemical bioavailability of vanadium species, the underlying basis of risk assessment. Environ Pollut 210:371–379CrossRefGoogle Scholar
  46. Richardson W, (1997). Handbook of copper compounds and applications. Marcel dekker editions, New York United States.395pGoogle Scholar
  47. Rieuwerts JS, Thornton ME, Ashmore FA (1998) Factors influencing metal bioavailability in soils: preliminary investigations for the development of a critical loads approach for metals. J Chem Spec Bioavailab 10(2)CrossRefGoogle Scholar
  48. Rodriguez N, Alonso M, Grasa G, Abandes J C, (2008). Process for capturing CO2 arising from the calcination of CaCO3 used in cement manufacture. J. Environ Sci. Technol (42) 6980-6984Google Scholar
  49. Rome C, Huang X, Danku J, Salt D, Sebestiani L, (2016). Expression of specific genes involved in Cd uptake, translocation, vacuolar compartementalization and recycling in Populus alba Villa France clone. J. plant physiol (202) 83-91CrossRefGoogle Scholar
  50. Roy M, McDonald LM (2015) Metal Uptake in Plants and Health Risk Assessments in Metal-Contaminated Smelter Soils. Land Degrad Dev 26(8):785–792CrossRefGoogle Scholar
  51. Sarwar N, Imran M, Shaheen MR, Ishaque W, Kamran MA, Matloob A, Rehim A, Hussain S (2017) Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171:710–721CrossRefGoogle Scholar
  52. Singh G, Bhati M, Rathod T, (2010). Use of tree seedlings for the phytoremediation of a municipal effluent used in dry areas of North-Western India: plant growth and nutrient uptake.J. Eco Eng (36)1299-1306CrossRefGoogle Scholar
  53. Song U, Park H (2017) Importance of biomass management acts and policies after phytoremediation. J EcolEnviron 41(13):1–6. CrossRefGoogle Scholar
  54. Tang LX, Hashemi M, Xu J, Brooks P (2015) Effect of organic and inorganic amendements on the uptake of lead and trace elements by Brassica chinenesis in acidic red soil. Chemosphere 119:177–183CrossRefGoogle Scholar
  55. Thakur S, Singh L, Wahid Z A, Siddiqui M F, Atnaw S M, Md Din M F, (2016). Plant-driven removal of heavy metals from soil: uptake, translocation, tolerance mechanism, challenges and future perspectives. J. Environ Monit Assess (4)188–206Google Scholar
  56. Tounsadi H, Khalidi A, Machrouhi A, Farnane M, Elmoubarki R, Elhalil A, Sadiq M, Barka N, (2016). Highly efficient activated carbon from Glebionis coronaria L. biomass: optimization of preparation conditions and heavy metals removal using experimental design approach. J. Environ Chem Eng (4) 4549-4564CrossRefGoogle Scholar
  57. Trasande L, Digangi J, Evers D C, Petrlik J, Buck D G, Samanek J, Beeler B, Turnquist M A, Regan K, (2016). Economic implications of mercury exposure in the context of the global mercury treaty: hair mercury levels and estimated lost economic productivity in selected developing countries. J. Environ Manage (183) 229-235CrossRefGoogle Scholar
  58. Viehweger K, (2014). How plants cope with heavy metals. Bot. Stud. J (1):55-35Google Scholar
  59. Wang J, & Jia H (2016) Metagenome-wide association studies: fine-mining the microbiome. Nat Rev Microbiol 14(8):508Google Scholar
  60. Wu Z, Zhang X, Wu M, 2016. Mitigating construction dust pollution: state of the art and the way forward. J. Clean. Prod. (112) 1658–1666CrossRefGoogle Scholar
  61. Yang W, Zhang T, Li S, & Ni W (2014) Metal removal from and microbial property improvement of a multiple heavy metals contaminated soil by phytoextraction with a cadmium hyperaccumulator Sedum alfredii H. J Soil Sediment 14(8);1385–1396Google Scholar
  62. Yanqun Z, Yuana L, Jianjunb C, Haiyanb C, Lib Q, Schvartzc C (2005) Hyperaccumulation of Pb, Zn and Cd in herbaceous grown on lead-zinc mining area in Yunnan, China. Environ Inter 31:755–762CrossRefGoogle Scholar
  63. Yaylali-Abanuz G (2011) Heavy metal accumulation of surface soil around Gebze industrial area, Turkey. Microchem J (99):82–92Google Scholar
  64. Zemba S, Ames M, Green L, Botelho MJ, Gossman D, Linkov I, Oliveira JP (2011) Emissions of metals and polychlorinated dibenzo (p) dioxins and furans (PCDD/Fs) from Portland cement manufacturing plants: inter-kiln variability and dependence on fuel-tyes. Sci Total Environ 409:4198–4205CrossRefGoogle Scholar
  65. Zha Q, Xiao Z, Zhang X, Han Z, Wang Y (2016) Cloning and functional analysis of MxNRAMP1 and MxNRAMP3, two genes related to high metal tolerance of Malus xiaojinensis. S Afr J Bot 102:75–80CrossRefGoogle Scholar

Copyright information

© Saudi Society for Geosciences 2020

Authors and Affiliations

  • Ines Terwayet Bayouli
    • 1
    Email author
  • Beatriz Gómez-Gómez
    • 2
  • Houssem Terwayet Bayouli
    • 3
  • Teresa Pérez-Corona
    • 2
  • Erik Meers
    • 4
  • Emna Ammar
    • 5
  • Ali Ferchichi
    • 3
  • Yolanda Madrid Albarrán
    • 2
  1. 1.Arid Regions Institute, TunisiaUniversity of GabesMedenineTunisia
  2. 2.Department of Analytical Chemistry, Faculty of Chemical SciencesComplutense University of MadridMadridSpain
  3. 3.National Agronomic Institute of TunisTunisTunisia
  4. 4.Department of Green Chemistry and TechnologyGhent UniversityGhentBelgium
  5. 5.RU Coastal and Urbans Environments, National Engineering School of Sfax, BP 1173University of SfaxSfaxTunisia

Personalised recommendations