Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Phytoextraction of Pb and Cd by the Mediterranean saltbush (Atriplex halimus L.): metal uptake in relation to salinity

  • 1538 Accesses

  • 86 Citations


Background, aim, and scope

The success of phytoextraction depends upon the identification of suitable plant species that hyperaccumulate heavy metals and produce large amounts of biomass using established agricultural techniques. In this study, the Mediterranean saltbush Atriplex halimus L., which is a C4 perennial native shrub of Mediterranean basin with an excellent tolerance to drought and salinity, is investigated with the main aim to assess its phytoremediation potential for Pb and Cd removal from contaminated soils. In particular, the influence of soil salinity in metal accumulation has been studied as there is notable evidence that salinity changes the bioavailability of metals in soil and is a key factor in the translocation of metals from roots to the aerial parts of the plant.

Materials and methods

Three pot experiments were conducted under greenhouse conditions for a 10-week period with A. halimus grown in soil artificially polluted with 20 ppm of Cd and/or 800 ppm of Pb and irrigated with three different salt solutions (0.0%, 0.5%, and 3.0% NaCl). Soil measurements for soil characterization were performed with the expiration of the first week of plant exposure to metals and NaCl, and at the end of the experimental period, chlorophyll content, leaf protein content, leaf specific activity of guaiacol peroxidase (EC, shoot water content, biomass, and Cd and Pb content in the plant tissues were determined. Additionally, any symptoms of metal or salt toxicity exhibited by the plants were visually noted during the whole experimental period.


The experimental data suggest that increasing salinity increases cadmium uptake by A. halimus L. while in the case of lead there was not a clear effect of the presence of salt on lead accumulation in plant tissues. A. halimus developed no visible signs of metal toxicity; only salt toxicity symptoms were observed in plants irrigated with 3% NaCl solutions. Chlorophyll content, leaf protein content, shoot water content, and biomass were not negatively affected by the metals; instead, there was even an increase in the amount of photosynthetic pigments in plants treated with both metals and salinity. The specific activity of guaiacol peroxidase seems to have a general tendency for increase in plants treated with the metals in comparison with the respective controls but a statistically significant difference exists only in plants treated with the metal mixture and saline conditions.


The data revealed that lead and cadmium accumulation in plant tissues was kept generally at low levels. Salinity was found to have a positive effect on cadmium uptake by the plant and this may be related to a higher bioavailability of the metal in soil due to decreased Cd sorption on soil particles. On the other hand, salinity did not influence in a clear way the uptake of Pb by the plant probably because of lead’s limited mobility in soils and plant tissues. Cd and Pd usually decrease the chlorophyll content and biomass and change water relations in plants; however, A. halimus was found not to be affected indicating that it is a Cd- and Pb-tolerant plant. Guaiacol peroxidase activity as one of the parameters expressing oxidative damage and extent of stress in plants was not generally found to be significantly affected under the presence of metals in most plants suggesting that the extent of stress in plants was minimal, while only for plants treated with the metal mixture and low salinity the enzyme activity was elevated confirming that this enzyme serves as an antioxidative tool against the reactive oxygen species produced by the metals.


Atriplex halimus L. is a Pb- and Cd-tolerant plant but metal concentrations achieved in plant tissues were kept generally at low levels; however, metal accumulation in shoots, especially for Cd, considered together with its high biomass production, rapid growth, and deep root system able to cope with poor structure and xeric characteristics of several polluted soils suggest that this plant deserves further investigation.

Recommendations and perspectives

Phytoextraction by halophytes is a promising alternative for the remediation of heavy metal contaminated sites affected by salinity since saline depressions often indicate sites of industrial effluents accumulation, contaminated by heavy metals, including Pb and Cd. Halophytes are also promising candidates for the removal of heavy metals from non-saline soils. Furthermore, the use of such plants can be potentially viewed as an alternative method for soil desalination where salt is removed from the soil instead of being washed downwards by water or other solutions.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8


  1. Bajji M, Kinet J-M, Lutts S (1998) Salt effects on roots and leaves of Atriplex halimus L. and their corresponding callus cultures. Plant Sci 137:131–142

  2. Balsberg Påhlsson A-M (1989) Toxicity of heavy metals (Zn, Cu, Cd, Pb) to vascular plants. Water Air Soil Pollut 47:287–319

  3. Bingham FT, Strong JE, Sposito G (1983) Influence of chloride salinity on cadmium uptake by Swiss chard. Soil Sci 135:160–165

  4. Blumenthal-Goldschmidt S, Poljakoff-Mayber A (1968) Effects of substrate salinity on growth and on submicroscopic structure of leaf cells of Atriplex halimus L. Aust J Bot 16:469–478

  5. Boominathan R, Doran PM (2003) Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator Thlaspi caerulescens. Biotechnol Bioeng 83:158–167

  6. Butcher DJ (2009) Phytoremediation of lead in soil: recent applications and future prospects. Appl Spectrosc Rev 44:123–139

  7. Cheng S (2003) Effects of heavy metals on plants and resistance mechanisms. Environ Sci Pollut Res 10(4):256–264

  8. Council of the European Communities (1986) Council directive of 12 June 1986 on the protection of the environment and in particular of the soil, when sewage sludge is used in agriculture. Official J European Communities no. L181, pp 6–12

  9. Das P, Samantaray S, Rout GR (1997) Studies of cadmium toxicity in plants: a review. Environ Pollut 98:29–36

  10. Erdelský K, Frič F (1979) Praktikum a analytické metódy vo fyziológii rastlín (Prakticum and analytical methods in plant physiology), SPN Bratislava

  11. Fitzgerald E, Caffrey J, Nesaratnam S, McLoughlin P (2003) Copper and lead concentrations in salt marsh plants on the Suir Estuary, Ireland. Environ Pollut 123:67–74

  12. Ghnaya T, Nouairi I, Slama I, Messedi D, Grignon C, Adbelly C, Ghorbel MH (2005) Cadmium effects on growth and mineral nutrition of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum. J Plant Physiol 162:1133–1140

  13. Ghnaya T, Slama I, Messedi D, Grignon C, Ghorbel MH, Adbelly C (2007) Effects of Cd+2 on K+, Ca2+ and N uptake in two halophytes Sesuvium portulacastrum and Mesembryanthemum crystallinum: consequences on growth. Chemosphere 67:72–79

  14. Harborne JB (1984) Chlorophylls. In: Phytochemical methods, 2nd edn. Chapman and Hall, London, pp 214–221

  15. Jordan FL, Robin-Abbott M, Maier RM, Glenn EP (2002) A comparison of chelator-facilitated metal uptake by a halophyte and a glycophyte. Environ Toxicol Chem 21:2698–2704

  16. Kadukova J, Papadontonakis N, Naxakis G, Kalogerakis N (2004) Lead accumulation by the salt-tolerant plant Atriplex halimus. In: Moutzouris C, Christodoulatos C, Dermatas D, Koutsospyros A, Skanavis C, Stamou A (eds) e-Proceedings of the International Conference on Protection and Restoration of the Environment VII, June 28–July 1, Mykonos, Greece

  17. Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Environ Qual 31:109–120

  18. Le Houérou HN (1992) The role of saltbushes (Atriplex spp.) in arid land rehabilitation in the Mediterranean Basin: a review. Agroforest Syst 18:107–148

  19. Lindsay WL, Norvell WA (1978) Development of a DTPA test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–428

  20. Liu D, Jiand W, Liu C, Xin C, Hou W (2000) Uptake and accumulation of lead by roots, hypocotyls and shoots of Indian mustard [Brassica juncea (L.)]. Bioresour Technol 71:273–277

  21. Lutts S, Lefèvre I, Delpèrèe C, Kivits S, Dechamps C, Robledo A, Correal E (2004) Heavy metal accumulation by halophyte species Mediterranean saltbush. J Environ Qual 33:1271–1279

  22. Manousaki E, Kadukova J, Papadantonakis N, Kalogerakis N (2008) Phytoextraction and phyto-excretion of Cd by Tamarix smyrnensis growing on contaminated non saline and saline soils. Environ Res 106:326–332

  23. Martin HW, Kaplan DI (1998) Temporal changes in cadmium, thallium and vanadium mobility in soil and phytoavailability under field conditions. Water Air Soil Pollut 101:399–410

  24. Martin TA, Ruby MV (2004) Review of in situ remediation technologies for lead, zinc and cadmium in soil. Remed J 14:35–53

  25. Memon AR, Schröder P (2009) Implications of metal accumulation mechanisms to phytoremediation. Environ Sci Pollut Res 16:162–175

  26. Naidu R, Gupta VVSR, Rogers S, Kookana RS, Bolan NS, Adriano DC (2003) Bioavailability of metals in the soil plant environment and its potential role in risk assessment. In: Naidu R, Gupta VVSR, Kookana RS, Rogers S, Adriano D (eds) Bioavailability, toxicity and risk relationships in ecosystems. Science Publishers, Enfield, pp 21–57

  27. Nedelkoska TV, Doran PM (2000) Hyperaccumulation of cadmium by hairy roots of Thlaspi caerulescens. Biotechnol Bioeng 67:607–615

  28. Nelson DW, Sommers LE (1996) Total carbon, organic carbon and organic matter. In: Sparks DL (ed) Methods of soil analysis, Part 3, chemical methods—SSSA book series no. 5. Soil Science Society of America and American Society of Agronomy, Madison, pp 995–1007

  29. Norvell WA, Wu J, Hopkins DG, Welch RM (2000) Association of cadmium in durum wheat grain with soil chloride and chelate-extractable soil cadmium. Soil Sci Soc Am J 64:2162–2168

  30. Orcutt DM, Nilsen ET (2000) Phytotoxicity and soil pollution: heavy metals and xenobiotics. In: The physiology of plants under stress, soil and biotic factors. Wiley, New York, pp 481–517

  31. Ortíz-Dorda J, Martínez-Mora C, Correal E, Simón B, Cenis JL (2005) Genetic structure of Atriplex halimus populations in the Mediterranean Basin. Ann Bot—London 95:827–834

  32. Osman AE, Bahhady F, Hassan N, Ghassali F, Al Ibrahim T (2006) Livestock production and economic implications from augmenting degraded rangeland with Atriplex halimus and Salsola vermiculata in northwest Syria. J Arid Environ 65:474–490

  33. Otte ML (1991) Contamination of coastal wetlands with heavy metals: factors affecting uptake of heavy metals by salt marsh plants. In: Rozema J, Verkleij JAC (eds) Ecological responses to environmental stresses. Kluwer Academic, Netherlands, pp 126–133

  34. Palmer CE, Warwick S, Keller W (2001) Brassicaceae (Cruciferae) family, plant biotechnology, and phytoremediation. Int J Phytorem 3:245–287

  35. Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29:529–540

  36. Qadir M, Schubert S, Steffens D (2005) Phytotoxic substances in soils. In: Hillel D (ed) Encyclopedia of soils in the environment. Elsevier, Oxford, pp 216–222

  37. Radotic K, Ducic T, Mutavdzic D (2000) Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentration of cadmium. Environ Exp Bot 44:105–113

  38. Raskin I, Smith RD, Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8:221–226

  39. Rauret G (1998) Extraction procedures for the determination of heavy metals in contaminated soil and sediment. Talanta 46:449–455

  40. Rieuwerts JS, Ashmore MR, Farago ME, Thornton I (2006) The influence of soil characteristics on the extract ability of Cd, Pb and Zn in upland and moorland soils. Sci Total Environ 366:864–875

  41. Saifullah ME, Qadir M, de Caritat P, Tack FMG, Du Laing G, Zia MH (2009) EDTA-assisted Pb phytoextraction. Chemosphere 74:1279–1291

  42. Smolders E, McLaughlin ML (1996) Effect of Cl on Cd uptake by Swiss Chard in nutrient solutions. Plant Soil 179:57–64

  43. Smolders E, Lambregts RM, McLaughlin MJ, Tiller KG (1998) Effect of soil solution chloride on cadmium availability to Swiss chard. J Environ Qual 27:426–431

  44. Soon YK (1998) Determination of cadmium, chromium, cobalt, lead and nickel in plant tissue. In: Kaltra P (ed) Handbook of reference methods for plant analysis. CRC, London, pp 193–198

  45. Thomas GW (1996) Soil pH and soil acidity. In: Sparks DL (ed) Methods of soil analysis, part 3, chemical methods—SSSA book series no. 5. Soil Science Society of America and American Society of Agronomy, Madison, pp 475–489

  46. Thomas JC, Malick FK, Endreszl C, Davies EC, Murray KS (1998) Distinct responses to copper stress in the halophyte Mesembryanthemum crystallinum. Physiol Plant 102:360–368

  47. US Environmental Protection Agency (1994) Test methods for evaluating soils and wastes. SW 846.

  48. US Environmental Protection Agency (2001) Phytoremediation of contaminated soil and ground water at hazardous waste sites. EPA/540/S-01/500.

  49. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655

  50. Wahla IH, Kirkham MB (2008) Heavy metal displacement in salt-water-irrigated soil during phytoremediation. Environ Pollut 155:271–283

  51. Weggler K, McLaughlin MJ, Graham RD (2004) Effects of chloride in soil solution on the plant availability of biosolid-borne cadmium. J Environ Qual 33:496–504

  52. Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533

Download references


The project was funded by the European Social Fund and National Resources—EPEAEK II—IRAKLITOS.

Author information

Correspondence to Nicolas Kalogerakis.

Additional information

Responsible editor: Peter Schröder and Jean-Paul Schwitzguébel

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Manousaki, E., Kalogerakis, N. Phytoextraction of Pb and Cd by the Mediterranean saltbush (Atriplex halimus L.): metal uptake in relation to salinity. Environ Sci Pollut Res 16, 844–854 (2009).

Download citation


  • Atriplex halimus L.
  • Cadmium
  • COST—phytoremediation of contaminated soils
  • Halophytes
  • Heavy metal tolerance
  • Lead
  • Phytoextraction
  • Pot experiment
  • Salinity
  • Stress