Environmental Science and Pollution Research

, Volume 21, Issue 11, pp 6859–6876 | Cite as

Effects of arbuscular mycorrhizal fungi on Agrostis capillaris grown on amended mine tailing substrate at pot, lysimeter, and field plot scales

  • Aurora NeagoeEmail author
  • Paula Stancu
  • Andrei Nicoară
  • Marilena Onete
  • Florian Bodescu
  • Roxana Gheorghe
  • Virgil Iordache
Using microbes for the regulation of heavy metal mobility at ecosystem and landscape scale


Applied research programs in the remediation of contaminated areas can be used also for gaining insights in the physiological and ecological mechanisms supporting the resistance of plant communities in stress conditions due to toxic elements. The research hypothesis of this study was that in the heavily contaminated but nutrient-poor substrate of mine tailing dams, the beneficial effect of inoculation with arbuscular mychorrizal fungi (AMF) is due to an improvement of phosphorus nutrition rather than to a reduction of toxic element transfer to plants. A concept model assuming a causal chain from root colonization to element uptake, oxidative stress variables, and overall plant development was used. The methodological novelty lies in coupling in a single research program experiments conducted at three scales: pot, lysimeter, and field plot, with different ages of plants at the sampling moment (six subsets of samples in all). The inoculation with AMF in expanded clay carrier had a beneficial effect on the development of plants in the amended tailing substrate heavily contaminated with toxic elements. The effect of inoculation was stronger when the quantity of expanded carrier was smaller (1 % vs. 7 % inoculum), probably because of changes in substrate features. The improvement of plant growth was due mainly to an improvement in phosphorus nutrition leading to an increase of protein concentration and decrease of oxidative stress enzyme activity (superoxide dismutase and peroxidase). In a single data subset, an effect of inoculation on the uptake of several toxic elements could be proved (decrease of As concentration in plant roots correlated with a decrease of oxidative stress independent from the effect of P concentration increase). The multi-scale approach allowed us to find differences between the patterns characterising the data subsets. These subset-specific patterns point out the existence of physiological differences between plants in different development states (as a result of sampling at different plant ages). From an applied perspective, conclusions are drawn with respect to the use of plants in the monitoring programs of contaminated areas and the use of inoculation with AMF in the remediation of tailing dams.


Agrostis capillaris Arbuscular mycorrhizal fungi Phosphorus Heavy metals Oxidative stress Multiple scales Mine tailings Remediation 



This work was performed within the FP7 project UMBRELLA, grant agreement 226870/2009, and Partnership PN2 projects: 31-012/2007 FITORISC and 50/2012 ASPABIR funded by Executive Agency for Higher Education, Research, Development and Innovation Funding, Romania. The authors acknowledge Roxana Donciu, who was a technician in our lab. They also thank Prof. Dr. Katarzyna Turnau for the analysis of the mine tailing substrate with respect to mycorrhizal fungi content. They specially thank the anonymous reviewers for the constructive criticism that greatly improved the manuscript.

Supplementary material

11356_2013_1908_MOESM1_ESM.doc (1.6 mb)
ESM 1 (DOC 1676 kb)


  1. Adriano DC (2001) Trace elements in terrestrial environments. Biogeochemistry, bioavailability, and risk of metals (2nd edn). Springer, New YorkCrossRefGoogle Scholar
  2. Benhammou A, Yaacoubi A, Nibou L, Tanoutu B (2005) Adsorption of metal ions onto Moroccan stevensite: kinetic and isotherm studies. J Colloid Interf Sci 282:320–326Google Scholar
  3. Bernal MP, Clemente R, Walker DJ (2007) The role of organic amendments in the bioremediation polluted soil. In: Environmental research at the leading edge, Alfred G (ed). Nova Science Publishers Inc. Chapter 1, pp 1–57Google Scholar
  4. Bes C, Mench M (2008) Remediation of copper-contaminated topsoils from a wood treatment facility using in situ stabilisation. Environ Pollut 156:1128–1138CrossRefGoogle Scholar
  5. Bucher M (2006) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173(1):11–26CrossRefGoogle Scholar
  6. Cao X, Dermatas D, Xu X, Shen G (2008) Immobilization of lead in shooting range soils by means of cement, quicklime, and phosphate amendments. Env Sci Pollut Res 15(2):120–12CrossRefGoogle Scholar
  7. Cárcamo V, Bustamante E, Trangolao E, de la Fuente LM, Mench M, Neaman A, Ginocchio R (2012) Simultaneous immobilization of metals and arsenic in acidic polluted soils near a copper smelter in central Chile. Environ Sci Pollut Res 19:1131–1143. doi: 10.1007/s11356-011-0673-3 CrossRefGoogle Scholar
  8. Carrasco L, Gattinger A, Flieβbach A, Roldán A, Schloter M, Caravaca F (2009) Estimation by PLFA of microbial community structure associated with the rhizosphere of Lygeum spartum and Piptatherum miliaceum growing in semiarid mine tailings. Microb Ecol 60:265–271CrossRefGoogle Scholar
  9. Carrasco L, Barata C, Garçia-Berthou E, Tobias A, Bayona JM, Diez S (2011) Patterns of mercury and methylmercury bioaccumulation in fish species downstream of a long-term mercury-contaminated site in the lower Ebro River (NE Spain). Chemosphere 84:1642–1649CrossRefGoogle Scholar
  10. Chen X, Chunhua W, Tang J, Hu S (2005) Arbuscular mycorrhizae enhance metal uptake and growth of host plants under a sand culture experiment. Chemosphere 60:665–671CrossRefGoogle Scholar
  11. Chen BD, Zhu YG, Duan J, Xiao XY, Smith SE (2007) Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environ Pollut 147:374–380CrossRefGoogle Scholar
  12. Chen B, Roos P, Zhu YG, Jakobsen I (2008) Arbuscular mycorrhizas contribute to phytostabilization of uranium in uranium mining tailings. Environ Radioactiv J 99:801–810CrossRefGoogle Scholar
  13. Chen MM, Yin HB, O’Connor P, Wang YS, Zhu YG (2010) C: N: P stoichiometry and specific growth rate of clover colonized by arbuscular mycorrhizal fungi. Plant Soil 326:21–29CrossRefGoogle Scholar
  14. Chen Q, Hu C, Tan Q, Sun X (2011) Effect of different phosphate sources on availability of cadmium in soil. Huanjing Kexue Xuebao/Acta Sci Circumstantiae 31(10):2254–2259Google Scholar
  15. Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2012) Arbuscular mycorrhizal fungi modulate the leaf transcriptome of a Populus alba L. clone grown on a zinc and copper-contaminated soil. Environ Experim Botany 75:25–35CrossRefGoogle Scholar
  16. Claassen VP, Zasoski RJ (2006) Enhancement of revegetation on construction fill by fertilizer and topsoil application: effect on mycorrhizal infection. Land Degrad Dev 4(1):45–57CrossRefGoogle Scholar
  17. Damian F, Damian G (2007) Detoxification of heavy metal contaminated soils. Am J Environ Sci 3:193–198CrossRefGoogle Scholar
  18. Dazy M, Béraud E, Cotelle S, Grévilliot F, Férard JF, Masfaraud JF (2009) Changes in plant communities along soil pollution gradients: responses of leaf antioxidant enzyme activities and phytochelatin contents. Chemosphere 77:376–383CrossRefGoogle Scholar
  19. de Souza LA, Lopez de Andrade SA, Ribeiro de Souza SC, Schiavinato MA (2012) Arbuscular mycorrhiza confers Pb tolerance in Calopogonium mucunoides. Acta Physiologiae Plantarum 34(2):523–531CrossRefGoogle Scholar
  20. de Souza LA, Lopez de Andrade SA, Ribeiro de Souza SC, Schiavinato MA (2013) Evaluation of mycorrhizal influence on the development and phytoremediation potential of Canavalia gladiata in Pb-contaminated soils. Int J Phytoremediat 15:465–476CrossRefGoogle Scholar
  21. DIN ISO 11260 1997–05 (1997) Soil quality—determination of effective cation exchange capacity and base saturation level using barium chloride solution. Deutsches Institut für Normung, Beuth Verlag GmbH, Berlin, D (in German)Google Scholar
  22. Doula MK, Elaiopoulos K, Kavvadias VA, Mavraganis V (2012) Use of clinoptilolite to improve and protect soil quality from disposal of oil mills wastes. J Hazard Mater 207–208:103–110CrossRefGoogle Scholar
  23. Eapen S, Singh S, D’Souza SF (2007) Phytoremediation of metals and radionuclides, Chapter 8. In: Environmental bioremediation technologies. Springer, Heidelberg, pp 189–209CrossRefGoogle Scholar
  24. Farrag K, Senesi N, Nigro F, Petrozza A, Palma A, Shaarawi S, Brunetti G (2012) Growth responses of crop and weed species to heavy metals in pot and field experiments. Environ Sci Pollut Res 19:3636–3644CrossRefGoogle Scholar
  25. Fenglian F, Wan Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manage 92(3):407–418CrossRefGoogle Scholar
  26. Fenn ME, Perea-Estrada VM, De Bauer LI, Perez-Suarez M, Parker DR, Centina-Alcala VM (2006) Nutrient status and plant growth effects of forest soils in the basin of Mexico. Environ Pollut 140:187–199CrossRefGoogle Scholar
  27. Garau G, Castaldi P, Santona L, Deiana P, Melis P (2007) Influence of red mud, zeolite and lime on heavy metal immobilization, culturable heterotrophic microbial populations and enzyme activities in a contaminated soil. Geoderma 142:47–57CrossRefGoogle Scholar
  28. Garg N, Kaur H (2012) Influence of zinc on cadmium-induced toxicity in nodules of pigeonpea (Cajanus cajan L. Mill sp.) inoculated with arbuscular mycorrhizal (AM) fungi. Acta Physiol Plant 34:1363–1380CrossRefGoogle Scholar
  29. Ginocchio R, Baker AJM (2004) Metallophytes in Latin America: a remarkable biological and genetic resource scarcely known and studied in the region. Rev Chil Hist Nat 77:185–194CrossRefGoogle Scholar
  30. Gómez-Sagasti MT, Alkorta I, Becerril JM, Epelde L, Anza M, Garbisu C (2012) Microbial monitoring of the recovery of soil quality during heavy metal phytoremediation. Water Air Soil Pollut. doi: 10.1007/s11270-012-1106-8 Google Scholar
  31. González-Guerrero M, Oger E, Benabdellah K, Azcón-Aguilar C, Lanfranco L, Ferrol N (2010) Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices. Curr Genet 56:265–274CrossRefGoogle Scholar
  32. Hanauer T, Henningsen PF, Steffens D, Kalandadze B, Navrozashvili L, Urushadze T (2011) In situ stabilization of metals (Cu, Cd, and Zn) in contaminated soils in the region of Bolnisi, Georgia. Plant Soil 341:193–208CrossRefGoogle Scholar
  33. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  34. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146CrossRefGoogle Scholar
  35. Hoffmann G (1991) Methodenbuch, Band 1. In: Die Untersuchung von Böden (ed). VDLUFA-Verlag, DarmstadtGoogle Scholar
  36. Hong CO, Lee DK, Kim PJ (2008) Feasibility of phosphate fertilizer to immobilize cadmium in a field. Chemosphere 70(11):2009–2015CrossRefGoogle Scholar
  37. Iordache V, Ion S, Pohoaţă A (2009a) Integrated modeling of metals biogeochemistry: potential and limits. Chem Erde-Geochem 69:125–169CrossRefGoogle Scholar
  38. Iordache V, Gherghel F, Kothe E (2009b) Assessing the effect of disturbances on ectomycorrhiza diversity, review. Int J Environ Res Public Health 6:414–432CrossRefGoogle Scholar
  39. IordacheV, Onete M, Paucă M, Oromulu L, Honciuc V, Purice D, Cobzaru I, Gomoiu I, Neagoe A (2010) Biological communities in mining areas: scale dependent patterns, organisms’ potential as bioindicators, and naive plants for remediation, Proceedings 7th European Conference on Ecological Restoration Avignon, France, 23-27/08/2010,
  40. Iordache V, Lăcătusu R, Scrădeanu D, Onete M, Jianu D, Bodescu F, Neagoe A, Purice D, Cobzaru I (2012) Scale specific mechanisms of metals mobility in contaminated areas. In: Kothe E, Varma A (eds) Bio-geo-interactions in contaminated soils. Springer, Heidelberg, pp 385–416CrossRefGoogle Scholar
  41. Iverson SL, Maier RM (2009) Effects of compost on colonization of roots of plants grown in metalliferous mine tailings, as examined by fluorescence in situ hybridization. Appl Environ Microb 75:842–847CrossRefGoogle Scholar
  42. Javot H, Pumplin N, Harrison J (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322CrossRefGoogle Scholar
  43. Jianu D, Iordache V, Soare B, Petrescu L, Neagoe A, Iacob CR, Orza R (2012) The role of mineralogy and geochemistry in hazard potential assessment of mining areas. In: Kothe E, Varma A (eds) Bio-geo interactions in metal-contaminated soils. Springer, Heidelberg, pp 35–79CrossRefGoogle Scholar
  44. Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca RatonGoogle Scholar
  45. Khalvati M, Bartha B, Dupigny A, Schröder P (2010) Arbuscular mycorrhizal association is beneficial for growth and detoxification of xenobiotics of barley under drought stress. J Soils Sediments 10:54–64CrossRefGoogle Scholar
  46. Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364CrossRefGoogle Scholar
  47. Kumpiene J, Lagerkvist A, Maurice C (2008) Stabilization of As, Cr, Cu, Pb and Zn in soils using amendments. A review. Waste Manag 28:215–225CrossRefGoogle Scholar
  48. Lagrimini LM (1991) Wound induced deposition of polyphenols in transgenic plants overexpressing peroxidase. Plant Physiol 96:577–583CrossRefGoogle Scholar
  49. Lasat MM (2000) Phytoextraction of metals from contaminated soil: a review of plant/soil/metal interaction and assessment of pertinent agronomic issues. J Hazard Subst Res 2:1–25Google Scholar
  50. Lefévre I, Marchal G, Corréal E, Zanuzzi A, Lutts S (2009) Variation in response to heavy metals during vegetative growth in Dorycnium pentaphyllum Scop. Plant Growth Regul 59:1–11CrossRefGoogle Scholar
  51. Liu LZ, Gong ZQ, Zhang YL, Li PJ (2011) Growth, cadmium accumulation and physiology of marigold (Tageteserecta L.) as affected by arbuscular mycorrhizal fungi. Pedosphere 21(3):319–327CrossRefGoogle Scholar
  52. Lopareva-Pohu A, Verdin A, Garçon G, Lounes-Hadj Sahraoui A, Pourrut B, Debiane D, Waterlot C, Laruelle F, Bidar G, Douay F, Shirali P (2011) Influence of fly ash aided phytostabilization of Pb, Cd and Zn highly contaminated soils on Lolium perenne and Trifolium repens metal transfer and physiological stress. Environ Pollut 159:1721–1729CrossRefGoogle Scholar
  53. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  54. Luster J, Menon M, Hermle S, Schulin R, Günthard-Goerg MS, Nowack B (2008) Initial changes in refilled lysimeters built with metal polluted topsoil and acidic or calcareous subsoils as indicated by changes in drainage water composition. Water Air Soil Pollut Focus 8:163–176CrossRefGoogle Scholar
  55. Madejón E, Doronila AI, Madejón P, Baker AJM, Woodrow IE (2012) Biosolids, mycorrhizal fungi and eucalypts for phytostabilization of arsenical sulphidic mine tailings. Agroforest Syst 84:389–399CrossRefGoogle Scholar
  56. Madrid F, Diaz-Barrientos E, Florido MC (2008) Inorganic amendments to decrease metal availability in soil of recreational urban areas: limitations to their efficiency and possible drawbacks. Water Air Soil Pollut 192:117–125CrossRefGoogle Scholar
  57. Malizia D, Giuliano A, Ortaggi G, Masotti A (2012) Common plants as alternative analytical tools to monitor heavy metals in soil. Chem Cent J 6(Suppl 2):S6. doi: 10.1186/1752-153X-6-S2-S6 CrossRefGoogle Scholar
  58. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, LondonGoogle Scholar
  59. Mascher R, Fischer S, Scheiding W, Neagoe A, Bergmann H (2005) Exogenous 2-aminoethanol can diminish paraquat induced oxidative stress in barley (Hordeum vulgare L.). Plant Growth Regul 45:103–112CrossRefGoogle Scholar
  60. McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymatic function for erythrocuprein. J Biol Chem 244:6049–6055Google Scholar
  61. Meier S, Borie F, Bolan N, Cornejo P (2012) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci and Technol 42:741–775CrossRefGoogle Scholar
  62. Mench M, Vangroensveld J, Lepp NM, Edwards R (1998) Physico-chemical aspects and efficiency of trace element immobilization by soil amendments. In: Vangroensveld J, Cummingham SD (eds) Metal-contaminated soils. Springer, Berlin, pp 151–182Google Scholar
  63. Mench M, Lepp N, Bert V, Schwitzguebel JP, Gawronski SW, Schröder P, Vangronsveld J (2010) Successes and limitations of phytotechnologies at field scale: outcomes, assessment and outlook from COST Action 859. J Soils Sediments 10:1039–1070CrossRefGoogle Scholar
  64. Mendez MO, Maier RM (2008) Phytoremediation of mine tailings in temperate and arid environments. Rev Environ Sci Biotechnol 7:47–59CrossRefGoogle Scholar
  65. Moirou A, Xenidi A, Paspaliaris A (2001) Stabilization of Pb, Zn, and Cd-contaminated soils by means of natural zeolite. Soil Sediment Contam 10:251–267CrossRefGoogle Scholar
  66. Mozgawa W, Bajda T (2005) Spectroscopic study of heavy metals sorption on clinoptilolite. Phys Chem Minerals 31:709–713CrossRefGoogle Scholar
  67. Neagoe A, Ebenå G, Carlsson E (2005) The effects of soil amendments on plant performance in an area affected by acid mine drainage. Chem Erde-Geochem 65(S1):115–130CrossRefGoogle Scholar
  68. Neagoe A, Merten D, Iordache V, Buechel G (2009) The effect of bioremediation methods involving different degrees of soil disturbance on the export of metals by leaching and by plant uptake. Chem Erde-Geochem 69:57–73CrossRefGoogle Scholar
  69. Neagoe A, Iordache V, Fărcăşanu I (2011) Remediation of polluted areas. Bucharest University Press, Bucharest, p 95 (in Romanian)Google Scholar
  70. Neagoe A, Iordache V, Bergmann H, Kothe E (2013) Patterns of effects of arbuscular mycorrhizal fungi on plants grown in contaminated soil. J Plant Nutr Soil Sci. doi: 10.1002/jpln.201200079 Google Scholar
  71. Pansou M, Gautheyrou F (2006) Handbook of soil analysis: Mineralogical, organic and inorganic methods. Springer, BerlinCrossRefGoogle Scholar
  72. Petkovšek SAS (2013) Forest biomonitoring of the largest Slovene thermal power plant with respect to reduction of air pollution. Environ Monit Assess 185:1809–1823CrossRefGoogle Scholar
  73. Powell J, Klironomos J (2007) The ecology of plant-mutualisms. In: Eldor AP (ed) Soil microbiology, ecology, and biochemistry (third edn.). Elsevier, Amsterdam, pp 257–281CrossRefGoogle Scholar
  74. Prasad MNV, Freitas H (2003) Metal hyperaccumulation in plants - biodiversity prospecting for phytoremediation technology. Electronic J Biotechnol 6:275–321CrossRefGoogle Scholar
  75. Rydlova J, Vosatka M (2003) Effect of Glomus intraradices isolated from Pb-contaminated soil on Pb uptake by Agrostis capillaris is changed by its cultivation in a metal-free substrate. Folia Geobot 38:155–165CrossRefGoogle Scholar
  76. Salt DE, Blaylock M, Kumar NPBA, Dusenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnol 13:468–474CrossRefGoogle Scholar
  77. Sand W, Jozsa PG, Kovacs ZM, Săsăran N, Schippers A (2007) Long-term evaluation of acid rock drainage mitigation measures in large lysimeters. J Geochem Explor 92:205–211CrossRefGoogle Scholar
  78. Schöpfer P (1989) Experimentelle Pflanzenphysiologie-Einführung in die Anwendung, vol 2. Springer, BerlinCrossRefGoogle Scholar
  79. Schmitz O, Danneberg G, Hundeshagen B, Klinger A, Bothe H (1991) Quantification of vesicular-arbuscular mycorrhiza by biochemical parameters. J Plant Physiol 139:106–114CrossRefGoogle Scholar
  80. Soares CRFS, Siqueira JO (2008) Mycorrhiza and phosphate protection of tropical grass species against heavy metal toxicity in multi-contaminated soil. Biol Fertil Soils 44:833–841CrossRefGoogle Scholar
  81. Stancu P, Nicoară A, Neagoe A, Grawunder W, Iordache V (2011) The effect of amendments on geochemical characterisation of tailing substrate in a field experiment. Proceedings of the 11th international symposium on “Metal elements in environment, medicine and biology”, Cluj-Napoca, RomaniaGoogle Scholar
  82. Tordoff GM, Baker AJM, Willis AJ (2000) Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41:219–228CrossRefGoogle Scholar
  83. Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA Press, Paris, pp 217–221Google Scholar
  84. Turnau K, Orlowska E, Ryszka P, Zubek S, Anielska T, Gawronski S, Jurkiewicz A (2006) Role of mycorrhizal fungi in phytoremediation and toxicity monitoring of heavy metal rich industrial wastes in southern Poland. In: Twardowska I, Allen HE, Häggblom MH, Stefaniak S (eds) Soil and water pollution monitoring, protection and remediation. Springer, Berlin, pp 3–23Google Scholar
  85. Turnau K, Anielska T, Ryszka P, Gawroński S, Ostachowicz B, Jurkiewicz A (2008) Establishment of arbuscular mycorrhizal plants originating from xerothermic grasslands on heavy metal rich industrial wastes—new solution for waste revegetation. Plant Soil 305:267–280CrossRefGoogle Scholar
  86. Turnau K, Ryszka P, Wojtczak G (2010) Metal tolerant mycorrhizal plants: A review from the perspective on industrial waste in temperate region. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizal: Physiology and function. Springer, Dordrecht, pp 257–276CrossRefGoogle Scholar
  87. USEPA (2007) The use of soil amendments for remediation, revitalization, and reuse. EPA 542-R-07-013. Office of Superfund Remediation and Technology Innovation (OSRTI). EPA/ National Service Center for Environmental Publications, CincinnatiGoogle Scholar
  88. Vangronsveld J, Herzig R, Weynes N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794CrossRefGoogle Scholar
  89. Von Alten H, Blal B, Dodd JC, Feldmann F, Vosatka M (2002) Quality control of arbuscular mycorrhizal fungi inoculum in Europe. In: Gianinazzi H, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture. Birkhäuser Verlag, Switzerland, pp 281–296CrossRefGoogle Scholar
  90. Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321:385–408CrossRefGoogle Scholar
  91. Willscher S, Mirgorodsky D, Jablonski L, Ollivier D, Merten D, Büchel G, Wittig J, Werner P (2013) Field scale phytoremediation experiments on a heavy metal and uranium contaminated site, and further utilization of the plant residues. Hydrometallurgy 131–132:46–53CrossRefGoogle Scholar
  92. Wirtz S, Seeger M, Ries JB (2012) Field experiments for understanding and quantification of rill erosion processes. Catena 91:21–34CrossRefGoogle Scholar
  93. Wong MH (2003) Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50:775–780CrossRefGoogle Scholar
  94. Wu SC, Wong CC, Shu WS, Khan AG, Wong MH (2011) Mycorrhizo-remediation of lead/zinc mine tailings using vetiver: a field study. Int J Phytoremed 13:61–74CrossRefGoogle Scholar
  95. Xu W, Ly L, Grace JR (2010) Zinc removal from acid rock drainage by clinoptilolite in a slurry bubble column. Appl Clay Sci 50(1):158–163CrossRefGoogle Scholar
  96. Zaller JG, Saccani F, Frank T (2011) Effects of earthworms and mycorrhizal fungi on the growth of the medicinal herb Calendula officinalis (Asteraceae). Plant Soil Environ 57(11):499–504Google Scholar
  97. Zeien H, Brümmer GW (1989) Chemische Extraktionen zur Bestimmung von Schwermetall-bildungformen in Böden. Mitt Dtsch Bodenk Gesell 59:505–510Google Scholar
  98. Zhang HH, Tang M, Chen H, Zheng CL, Niu ZC (2010) Effect of inoculation with AM fungi on lead uptake, translocation and stress alleviation of Zea mays L. seedlings planting in soil with increasing lead concentrations. Eur J Soil Biol 46(5):306–311CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Aurora Neagoe
    • 1
    Email author
  • Paula Stancu
    • 1
  • Andrei Nicoară
    • 1
  • Marilena Onete
    • 2
  • Florian Bodescu
    • 1
  • Roxana Gheorghe
    • 1
  • Virgil Iordache
    • 1
  1. 1.Research Centre for Ecological Services (CESEC), Faculty of BiologyUniversity of BucharestBucharestRomania
  2. 2.Bucharest Institute of BiologyRomanian AcademyBucharestRomania

Personalised recommendations