Selection of native plants with phytoremediation potential for highly contaminated Mediterranean soil restoration: Tools for a non-destructive and integrative approach

Journal of Environmental Management

Volumn 183, Issue , 2016, Pages 850-863

  Heckenroth, Alma ^a,b   Rabier, Jacques ^a   Dutoit, Thierry ^a   Torre, Franck ^a   Prudent, Pascale ^c   Laffont Schwob, Isabelle ^a  

^a AVIGNON UNIVERSITÉ   (France)

^b Parc de Pichaury   (France)

^c CNRS   (France)

Author keywords

Ecological restoration; Metal(loid)s; Phytostabilization; Plant community; Plant successions; Protected area

Indexed keywords

CONCENTRATION (COMPOSITION); CONTAMINATED LAND; GEOCHEMICAL SURVEY; INTEGRATED APPROACH; MEDITERRANEAN SOIL; NATIVE SPECIES; PHYTOREMEDIATION; PLANT COMMUNITY; PROTECTED AREA; RESTORATION ECOLOGY; SMELTING; SUCCESSION; TOPSOIL;

FRANCE; GEOGRAPHIC INFORMATION SYSTEM; MONITORING; MULTIVARIATE ANALYSIS; NATIONAL PARK; PHYTOREMEDIATION; PLANT COMMUNITY; PLANT ECOLOGY; SOIL POLLUTION; SOIL TREATMENT; SPECIES; STRESS; VEGETATION; ANALYSIS; BIOREMEDIATION; CHEMISTRY; ECOSYSTEM; FABACEAE; METABOLISM; PLANT; PLANTAGINACEAE; POLLUTION; SOIL; SOIL POLLUTANT;

BOUCHES DU RHONE; CALANQUES NATIONAL PARK; FRANCE; PROVENCE-ALPES-COTE D'AZUR;

CORONILLA JUNCEA; GLOBULARIA ALYPUM;

METAL; SOIL; SOIL POLLUTANT;

BIODEGRADATION, ENVIRONMENTAL; ECOSYSTEM; ENVIRONMENTAL POLLUTION; FABACEAE; FRANCE; METALS; PLANTAGINACEAE; PLANTS; SOIL; SOIL POLLUTANTS;

EID: 84992327348     PISSN: 03014797     EISSN: 10958630     Source Type: Journal    
DOI: 10.1016/j.jenvman.2016.09.029     Document Type: Article

References (85)

1. Aillaud, G.J., Crouzet, A., Un milieu difficile, des plantes adaptées: la végétation littorale du Sud du golfe de Marseille. 1988, Centre Régional de Documentation Pédagogique, Marseille, 50.
2. Affholder, M.C., Approche des mécanismes de tolérance du romarin aux éléments traces métalliques et métalloïdes: perspectives pour une phytostabilisation des sols méditerranéens pollués. PhD thesis, 2013, Aix-Marseille University, 288.
3. Affholder, M.C., Prudent, P., Masotti, V., Coulomb, B., Rabier, J., Nguyen-The, B., Laffont-Schwob, I., Transfer of metals and metalloids from soil to shoots in wild rosemary (Rosmarinus officinalis L.) growing on a former lead smelter site: human exposure risk. Sci. Total Environ. 454–455 (2013), 219–229.
4. Affholder, M.C., Pricop, A.D., Laffont-Schwob, I., Coulomb, B., Rabier, J., Borla, A., Demelas, C., Prudent, P., As, Pb, Sb, and Zn transfer from soil to root of wild rosemary: do native symbionts matter?. Plant Soil 382 (2014), 219–236.
5. Affre, L., Dumas, P.J., Dumas, E., Laffont-Schwob, I., Tatoni, T., Regard écologique sur le recul stratégique: atouts et risques pour la diversité végétale péri-urbaine marseillaise. Vertigo, Hors-série 21, avril 2015, Droit des risques littoraux et changement climatique: connaissance, anticipation et innovation, 2015, 13.
6. Akaike, H., Information theory and the maximum likelihood principle. Petrov, B.N., Csaki, F., (eds.) 2nd International Symposium on Information Theory, 1973, Akademiai Kiado, Budapest, 267–281.
7. Alguacil, M.M., Torrecillas, E., Caravaca, F., Fernandez, D.A., Azcon, R., Roldan, A., The application of an organic amendment modifies the arbuscular mycorrhizal fungal communities colonizing native seedlings grown in a heavy-metal-polluted soil. Soil Biol. Biochem. 43 (2011), 1498–1508.
8. Ali, H., Khan, E., Sajad, M.A., Phytoremediation of heavy metals – concepts and applications. Chemosphere 91 (2013), 869–881.
9. Alkorta, I., Hernandez-Allica, J., Becerril, J.M., Amezaga, I., Albizu, I., Garbisu, C., Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Rev. Environ. Sci. Biotechnol. 3 (2004), 71–90.
10. Anderson, C.W.N., Brooks, R.R., Chiarucci, A., La Coste, C.J., Leblanc, M., Robinson, B.H., Simcock, R., Stewart, R.B., Phytomining for nickel, thallium and gold. J. Geochem. Explor. 67 (1999), 407–415.
11. Baker, A.J.M., Ernst, W.H.O., Van Der Ent, A., Malaisse, F., Ginocchio, R., Metallophytes: the unique biological resource, its ecology and conservational status in Europe, central Africa and Latin America. Batty, L.C., Hallberg, K.B., (eds.) Ecology of Industrial Pollution, 2010, Cambridge University Press, Cambridge, UK, 21–40 British Ecological Society 2010.
12. Barea, J.M., Palenzuela, J., Cornejo, P., Sánchez-Castro, I., Navarro-Fernández, C., Lopéz-García, A., Estrada, B., Azcón, R., Ferrol, N., Azcón-Aguilar, C., Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. J. Arid. Environ. 75 (2011), 1292–1301.
13. Blanchet, F.G., Legendre, P., Borcard, D., Forward selection of explanatory variables. Ecology 89:9 (2008), 2623–2632.
14. Borcard, D., Gillet, F., Legendre, P., Numerical Ecology with R. 2011, Springer, New York, Dordrecht, London, Heidelberg, 10.1007/978-1-4419-7976-6.
15. Boukhris, A., Laffont-Schwob, I., Mezghani, I., El Kadri, L., Prudent, P., Pricop, A., Tatoni, T., Chaieb, M., 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 (2015), 217–223.
16. Brewer, S., Guiot, J., Torre, F., Mid-Holocene climate change in Europe: a data-model comparison. Clim. Past. 3:3 (2007), 499–512.
17. Bringezu, K., Lichtenberger, O., Leopold, I., Neumann, D., Heavy metal tolerance of Silene vulgaris. J. Plant. Physiol. 154 (1999), 536–546.
18. Cain, S.A., The species-area curve. Am. Midl. Nat. 19:3 (1938), 573–581.
19. Carrasco, L., Azcón, R., Kohler, J., Roldán, A., Caravaca, F., Comparative effects of native filamentous and arbuscular mycorrhizal fungi in the establishment of an autochthonous, leguminous shrub growing in a metal-contaminated soil. Sci. Total Environ. 409 (2011), 1205–1209.
20. Clewell, A.F., Aronson, J., Ecological Restoration: Principles, Values, and Structure of an Emerging Profession. 2013, Island Press, Washington, 339.
21. Conesa, H.M., Faz, A., Arnaldos, R., Initial studies for the phytostabilization of a mine tailing from the Cartagena-La Union Mining District (SE Spain). Chemosphere 66 (2007), 38–44.
22. Cortina, J., Amat, B., Castillo, V., Fuentes, D., Maestre, F.T., Padilla, F.M., Rojo, L., The restoration of vegetation cover in the semi-arid Iberian southeast. J. Arid. Environ. 75 (2011), 1377–1384.
23. Darmendrail, D., Baize, D., Barbier, J., Freyssinet, P., Mouvet, C., Salpéteur, I., Wavrer, P., Fonds géochimique naturel: Etat des connaissances à l'échelle nationale. 2000, 93 BRGM/RP-50158-FR.
24. Dassot, M., Constant, T., Fournier, M., The use of terrestrial LiDAR technology in forest science: application fields, benefits and challenges. Ann. For. Sci. 68:5 (2011), 959–974.
25. De Baets, S., Poesen, J., Knapen, A., Barberá, G.G., Navarro, J.A., Root characteristics of representative Mediterranean plant species and their erosion-reducing potential during concentrated runoff. Plant Soil 294 (2007), 169–183.
26. Disante, K.B., Fuentes, D., Cortina, J., Sensitivity to zinc of Mediterranean woody species important for restoration. Sci. Total Environ. 408 (2010), 2216–2225.
27. Dray, S., Dufour, A.B., Chessel, D., The ade4 package-II: two-table and K-table methods. R. News 7:2 (2007), 47–52.
28. Durán-Zuazo, V.H., Francia-Martínez, J.R., Martínez Raya, A., Impact of vegetative cover on runoff and soil erosion at hillslope scale in Lanjaron, Spain. Environmentalist 24 (2004), 39–48.
29. Ernst, W.H.O., Evolution of metal tolerance in higher plants. For. Snow Landsc. Res. 80:3 (2006), 251–274.
30. Favas, P.J.C., Pratas, J., Varun, M., D'Souza, R., Paul, M.S., Phytoremediation of soils contaminated with metals and metalloids at mining areas: potential of native flora. Hernandez-Soriano, M.C., (eds.) Environmental Risk Assessment of Soil Contamination, 2014, InTech, Rijeka, Croatia, 485–517.
31. Fournier, P., (eds.) Les quatre flores de France Corse comprise: Générale, Alpine, Méditerranéenne, Littorale, 1961, Lechevalier, Paris, France.
32. Freitas, H., Prasad, M.N.V., Pratas, J., Analysis of serpentinophytes from north-east of Portugal for trace metal accumulation – relevance to the management of mine environment. Chemosphere 54 (2004), 1625–1642.
33. Frérot, H., Lefèbvre, C., Gruber, W., Collin, C., Dos Santos, A., Escarré, J., Specific interactions between local metallicolous plants improve the phytostabilization of mine soils. Plant Soil 282 (2006), 53–65.
34. Gachet, S., Véla, E., Tatoni, T., BASECO: a floristic and ecological database of Mediterranean French flora. Biodivers. Conserv. 14 (2005), 1023–1034.
35. Grime, J.P., Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111 (1977), 1169–1194.
36. Guillamot, F., Calvert, V., Millot, M.V., Criquet, S., Does antimony affect microbial respiration in Mediterranean soils? A microcosm experiment. Pedobiologia 57 (2014), 119–121.
37. Hartigan, J.A., Wong, M.A., A K-means clustering algorithm. Appl. Stat. 28 (1979), 100–108.
38. Horta, A., Malone, B., Stockmann, U., Minasny, B., Bishop, T.F.A., McBratney, A.B., Pallaser, R., Pozza, L., Potential of integrated field spectroscopy and spatial analysis for enhanced assessment of soil contamination: a prospective review. Geoderma 241–242 (2015), 180–209.
39. Jones, C.G., Lawton, J.H., Shachak, M., Organisms as ecosystem engineers. Oikos 69 (1994), 373–386.
40. Kabata-Pendias, A., Pendias, H., Trace Elements in Soils and Plants. third ed., 2001, CRC Press LCC, Boca Raton, London, New York, Washington D.C., 403.
41. Kalnicky, D.J., Singhvi, R., Field portable XRF analysis of environmental samples. J. Hazard. Mater 83 (2001), 93–122.
42. Khan, A.G., Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J. Trace Elem. Med. Bio 18 (2005), 355–364.
43. Khan, S., Cao, Q., Zheng, Y.M., Huang, Y.Z., Zhu, Y.G., Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ. Pollut. 152 (2008), 686–692.
44. Kholer, J., Caravaca, F., Azcón, R., Díaz, G., Roldán, A., Selection of plant species-organic amendment combinations to assure plant establishment and soil microbial function recovery in the phytostabilization of a metal-contaminated soil. Water Air Soil Pollut., 225(5), 2014, 13.
45. Knoerr, A., Le milieu, la flore, la végétation, la biologie des halophytes, dans l'archipel de Riou et sur la côte Sud de Marseille. PhD thesis, 1959, Aix-Marseille University, France, 420.
46. Krumins, J.A., Goodey, N.M., Gallagher, F., Plant-soil interactions in metal contaminated soils. Soil Biol. Biochem. 80 (2015), 224–231.
47. Laffont-Schwob, I., Dumas, P.J., Pricop, A.D., Rabier, J., Miché, L., Affre, L., Masotti, V., Prudent, P., Tatoni, T., Insights on metal tolerance and symbionts of the rare species Astragalus tragacantha aiming at phytostabilization of polluted soils and plant conservation. Ecol. Mediterr. 37 (2011), 57–62.
48. Laffont-Schwob, I., Heckenroth, A., Rabier, J., Masotti, V., Oursel, B., Prudent, P., Diffuse and widespread present-day pollution. Daumalin, X., Laffont-Schwob, I., (eds.) Pollution of Marseille's Industrial Calanques, REF2C, France, 2016, 206–249.
49. Legendre, P., Gallagher, E.D., Ecologically meaningful transformations for ordination of species data. Oecologia 129 (2001), 271–280.
50. Legendre, P., Oksanem, J., Ter Braak, C.J.F., Testing the significance of canonical axes in redundancy analysis. Methods Ecol. Evol. 2 (2011), 269–277.
51. Li, M.S., Ecological restoration of mineland with particular reference to the metalliferous mine wasteland in China: a review of research and practice. Sci. Total Environ. 357 (2006), 38–53.
52. Maestre, F.T., Cortina, J., Are Pinus halepensis plantations useful as a restoration tool in semiarid Mediterranean areas. For. Ecol. Manag 198 (2004), 303–317.
53. Marchiol, L., Fellet, G., Boscutti, F., Montella, C., Mozzi, R., Guarino, C., Gentle remediation at the former “Pertusola Sud” zinc smelter: evaluation of native species for phytoremediation purposes. Ecol. Eng. 53 (2013), 343–353.
54. Markham, J., Young, I., Renault, S., Plant facilitation on a mine tailings dump. Restor. Ecol. 19 (2011), 569–571.
55. Martin-Peinado, F., Morales-Ruano, S., Bagur-Gonzales, M.G., Estepa-Molina, C., A rapid field procedure for screening trace elements in polluted soil using portable X-ray fluorescence (PXRF). Geoderma 159 (2010), 76–82.
56. Mench, M., Schwitzguébel, J.P., Schroeder, P., Bert, V., Gawronski, S., Gupta, S., Assessment of successful experiments and limitations of phytotechnologies: contaminant uptake, detoxification and sequestration, and consequence for food safety. Environ. Sci. Pollut. Res. 16 (2009), 876–900.
57. Mendez, M.O., Maier, R., Phytoremediation of mine tailings in temperate and arid environments. Rev. Environ. Sci. Biotechnol. 7 (2008), 47–59.
58. Moreno-Jiménez, E., Vazquez, S., Carpena-Ruiz, R.O., Esteban, E., Penalosa, J.M., Using Mediterranean shrubs for the phytoremediation of a soil impacted by pyritic wastes in Southern Spain: a field experiment. J. Environ. Manage 92 (2011), 1584–1590.
59. Nsanganwimana, F., Pourrut, B., Mench, M., Douay, F., Suitability of Miscanthus species for managing inorganic and organic contaminated land and restoring ecosystem services. A review. J. Environ. Manage 143 (2014), 123–134.
60. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, Henry, P.M., Stevens, H., Wagner, H., Vegan: Community Ecology Package. R Package Version 2.2-0. 2014 URL http://CRAN.R-project.org/package=vegan.
61. Ottenhof, C.J.M., Faz Cano, A., Arocena, J.M., Nierop, K.G.J., Verstraten, J.M., Van Mourik, J.M., Soil organic matter from pioneer species and its implications to phytostabilization of mined sites in the Sierra de Cartagena (Spain). Chemosphere 69 (2007), 1341–1350.
62. Padilla, F.M., Ortega, R., Sanchez, J., Pugaire, F.I., Rethinking species selection for restoration of arid shrublands. Basic Appl. Ecol. 10 (2009), 640–647.
63. Párraga-Aguado, I., Gonzalez-Alcaraz, M.N., Alvarez-Rogel, J., Jimenez-Carceles, F.J., Conesa, H.M., The importance of edaphic niches and pioneer plant species succession for the phytomanagement of mine tailings. Environ. Pollut. 176 (2013), 134–143.
64. Párraga-Aguado, I., Querejeta, J.I., Gonzalez-Alcaraz, M.N., Jimenez-Carceles, F.J., Conesa, H.M., Usefulness of pioneer vegetation for the phytomanagement of metal(loid)s enriched tailings: grasses vs. shrubs vs. trees. J. Environ. Manage 133 (2014), 51–58.
65. Paulette, L., Man, T., Weindorf, D.C., Person, T., Rapid assessment of soil and contaminant variability via portable x-ray fluorescence spectroscopy: Copsa Micà, Romania. Geoderma 243–244 (2015), 130–140.
66. Pavon, D., Mémento pour l'aide à la détermination de la flore vasculaire du département des Bouches-du-Rhône. Bull. la Société linnéenne Provence, Numéro Spéc., 18, 2014, 248.
67. Pielou, E.C., An Introduction to Mathematical Ecology. 1969, Wiley-Interscience, New York.
68. Quézel, P., Médail, F., (eds.) Ecologie et biogéographie des forêts du bassin méditerranéen, 2003, Elsevier, Paris.
69. R Core Team, R: A Language and Environment for Statistical Computing. 2014, R Foundation for Statistical Computing, Vienna, Austria URL http://www.R-project.org/.
70. Rabier, J., Laffont-Schwob, I., Pricop, A., Ellili, A., D'enjoy-Weinkammerer, G., Salducci, M.D., Prudent, P., Lotmani, B., Tonetto, A., Masotti, V., Heavy metal and arsenic resistance of the halophyte Atriplex halimus L. along a gradient of contamination in a French Mediterranean spray-zone. Water Air Soil Pollut. 225:7 (2014), 54–69.
71. Rameau, J.C., Mansion, D., Dumé, G., Flore forestière française: guide écologique illustré. Tome 3: Région méditerranéenne. Ministère de l'Agriculture Institut Pour le Développement For., 2008, 2421.
72. Rashed, M.N., Monitoring of contaminated toxic and heavy metals, from mine tailings through age accumulation, in soil and some wild plants at Southeast Egypt. J. Hazard. Mater. 178 (2010), 739–746.
73. Raunkier, C., The Life-forms of Plants and Statistical Plant Geography. 1934, Oxford University Press, Oxford, 632.
74. Regvar, M., Likar, M., Piltaver, A., Kugonic, N., Smith, J.E., Fungal community structure under goat willows (Salix caprea L.) growing at metal polluted site: the potential of screening in a model phytostabilisation study. Plant Soil 330 (2010), 345–356.
75. Schaeffer, A., Amelung, W., Hollert, H., Kaestner, M., Kandeler, E., Kruse, J., Miltner, A., Ottermanns, R., Pagel, H., Peth, S., Poll, C., Rambold, G., Schloter, M., Schulz, S., Streck, T., Roß-Nickoll, M., The impact of chemical pollution on the resilience of soils under multiple stresses: a conceptual framework for future research. Sci. Total. Environ., 2016, 10, 10.1016/j.scitotenv.2016.06.161 in press.
76. Suchkova, N., Tsiripidis, I., Alifragkis, D., Ganoulis, J., Darakas, E., Sawidis, Th, Assessment of phytoremediation potential of native plants during the reclamation of an area affected by sewage sludge. Ecol. Eng. 69 (2014), 160–169.
77. Testiati, E., Parinet, J., Massiani, C., Laffont-Schwob, I., Rabier, J., Pfeifer, H.R., Lenoble, V., Masotti, V., Prudent, P., Trace metal and metalloid contamination levels in soils and in two native plant species of a former industrial site: evaluation of the phytostabilization potential. J. Hazard. Mater. 248–249 (2013), 131–141.
78. Tordoff, G.M., Baker, A.J.M., Willis, A.J., Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41 (2000), 219–228.
79. Vangronsveld, J., Herzig, R., Weyens, N., Boulet, J., Adriaensen, K., Ruttens, A., Thewys, T., Vassilev, A., Meers, E., Nehnevajova, N., Van Der Lelie, D., Mench, M., Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ. Sci. Pollut. Res. 16 (2009), 765–794.
80. Weindorf, D.C., Paulette, L., Man, T., In-situ assessment of metal contamination via portable x-ray fluorescence spectroscopy: Zlatna, Romania. Environ. Pollut. 182 (2013), 92–100.
81. Wenzel, W.W., Jockwer, F., Accumulation of heavy metals in plants grown on mineralised soils of the Austrian Alps. Environ. Poll. 104 (1999), 145–155.
82. Wenzel, W.W., Lombi, E., Adriano, D.C., Biogeochemical processes in the rhizosphere: role in phytoremediation of metal-polluted soils. Prasad, M.N.V., Hagemeyer, J., (eds.) Heavy Metal Stress in Plants - from Molecules to Ecosystems, 1999, Springer-Verlag, Berlin, 271–303.
83. Wierzbicka, M., Pielichowska, M., Adaptation of Biscutella leavigata L., a metal hyperaccumulator, to growth on a zinc-lead waste heap in southern Poland. I: difference between waste-heap and mountain populations. Chemosphere 54 (2004), 1663–1674.
84. Wong, M.H., Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50 (2003), 775–800.
85. Wuana, R.A., Okieimen, F.E., Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. IRSN Ecol., 2011, 2011, 20, 10.5402/2011/402647.