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RESEARCH ARTICLE

Response of excluder, indicator, and hyperaccumulator plants to nickel availability in soils

Stamatia Tina Massoura A B , Guillaume Echevarria B C , Elisabeth Leclerc-Cessac A and Jean Louis Morel B
+ Author Affiliations
- Author Affiliations

A Andra, Agence pour la gestion des déchets radioactifs, Parc de la Croix Blanche, 1/7, rue Jean Monnet, F-92298, Châtenay-Malabry cedex, France.

B Laboratoire Sols et Environnement, ENSAIA-INRA/INPL-UMR 1120, BP: 172, 2, avenue de la Forêt de Haye, F-54505, Vandoeuvre-lès-Nancy cedex, France.

C Corresponding author. Email: guillaume.echevarria@ensaia.inpl-nancy.fr

Australian Journal of Soil Research 42(8) 933-938 https://doi.org/10.1071/SR03157
Submitted: 14 November 2003  Accepted: 21 June 2004   Published: 14 December 2004

Abstract

Availability is a key property for the assessment of soil-to-plant transfer of heavy metals. This work was conducted to determine whether the available pool of Ni differs according to the ability of plants to take up and accumulate the metal. An excluder plant species (Triticum aestivum L.), an indicator (Trifolium pratense L.), and 3 populations of the Ni-hyperaccumulator Alyssum murale (Waldst. & Kit.) were grown for 90 days on 4 soils with a gradient of concentrations of total and available Ni. Isotopic exchange methods with 63Ni ions were used to measure the exchangeable soil Ni (E-value, intensity, and capacity factors), to monitor its uptake by plants and to determine the size of the available pool (L-value). Results showed that, for a given soil, the L-values were similar for all plant species, showing that they all access the same Ni exchangeable pool regardless of their Ni uptake capacity. Also, L-values for a given soil were equal to the E-value calculated for a 90-day period, demonstrating that plant Ni originated from the isotopically exchangeable soil Ni. This pool can be accurately and simply determined with the isotopic exchange kinetic methods run on soil–solution batch systems without plants. Moreover, the results indicate that the plant species take up Ni as a response to ‘intensity’, ‘capacity’, and ‘quantity’ soil factors and that E-value alone is not enough to predict plant uptake. This work suggests a uniform behaviour of the plants tested towards soil Ni and may have practical applications in phytoextraction and phytomining, as the plants removed Ni exclusively from the exchangeable pool.

Additional keywords: Ni, E-value, L-value, phytoavailability, hyperaccumulator, indicator, excluder.


Acknowledgments

This project, was funded by Andra (Agence nationale pour la gestion des déchets radioactifs), as part of the doctoral thesis of S.T. Massoura. Funds were also provided by the Ministère de l’Aménagement du Territoire et de l’Environnement, France. The authors are debtfull to Dr JC Fardeau and Dr A Jacobson useful suggestions and to Dr S Shallari who kindly supplied the Alyssum seeds. Special thanks are due to S. Colin for invaluable help in the sampling of soils.


References


AFNOR (1994). ‘Qualité des sols.’ (AFNOR: Paris, France)

Baker AJM (1981) Accumulators and excluders-strategies in the reponse of plants to heavy metals. Journal of Plant Nutrition 3( ), 643–654. open url image1

Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements-A review of their distribution, ecology and phytochemistry. Biorecovery 1, 81–126. open url image1

Baker AJM, Walker PL (1989) Physiological responses of plants to heavy metals and the quantification of tolerance and toxicity. Chemistry and Speciation Bioavailability 1, 7–17. open url image1

Brooks, RR (1992). ‘Serpentine and its vegetation: a multidisciplinary approach.’ (Croom Helm: London)

Brooks RR, Lee J, Reeves RD, Jaffré T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. Journal of Geochemical Exploration 7, 49–57.
Crossref | GoogleScholarGoogle Scholar | open url image1

Echevarria G, Klein S, Morel JL, Fardeau JC (1997) Mesure de la fraction assimilable des éléments en traces du sol par la méthode des cinétiques d'échange isotopique: cas du nickel. C.R.A.S. Paris 324, 221–227. open url image1

Echevarria G, Morel JL, Fardeau JC, Leclerc-Cessac E (1998) Assessment of phytoavailability of nickel in soils. Journal of Environmental Quality 27, 1064–1070. open url image1

Ernst WHO (1996) Bioavailability of heavy metals and decontamination of soils by plants. Applied Geochemistry 11, 163–167.
Crossref | GoogleScholarGoogle Scholar | open url image1

Eskew DL, Welch RM, Norwell WA (1984) Nickel in higher plants: further evidence for an essential role. Plant Physiology 76, 691–693. open url image1

Fardeau JC, Morel C, Jappé J (1985) Cinétique d'échange des ions phosphate dans les systèmes sol-solution. Vérification expérimentale de l'équation théorique. C.R.A.S. Paris 300, 371–376. open url image1

Gérard E, Echevarria G, Sterckeman T, Morel JL (2000) Cadmium availability to three species varying cadmium accumulation pattern. Journal of Environmental Quality 29, 1117–1123. open url image1

Hamon R, Wundke J, McLaughlin M, Naidu R (1997) Availability of zinc and cadmium to different plant species. Australian Journal of Soil Research 35, 1267–1275. open url image1

Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminata: A hyperaccumulator of nickel from New Caledonia. Science 193, 579–580. open url image1

Hutchinson JJ, Young SD, McGrath SP, West HM, Black CR, Baker AJ (2000) Determining uptake of ‘non-labile’ soil cadmium by Thlaspi caerulescens using isotopic dilution techniques. New Phytologist 146, 453–460.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kabata-Pendias A (1993) Behavioural properties of traces metals in soils. Applied Geochemistry 2, 3–9. open url image1

McGrath SP (1995) Chromium and nickel. ‘Heavy metals in soils’. (Ed. BJ Alloway) pp. 152–174. (Blackie Academic and Professional: London)

Mench M, Martin E (1991) Mobization of cadmium and other metals from two soils by root exudates of Zea mays L., Nicotiana tabacum L. and Nicotiana rustica L. Plant and Soil 132, 187–196. open url image1

Nyamangara J, Mzezewa J (1999) The effect of long-term sewage sludge application on Zn, Cu, Ni and Pb levels in a clay loam soil under pasture grass in Zimbabwe. Environmental and Experimental Botany 73, 199–204.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reeves RD, Brooks RR, Dudley TR (1983) Uptake of nickel by species of Alyssum, Bornmuellera and other genera of old world tribus Alysseae. Taxon 32, 184–192. open url image1

Reeves RD, Brooks RR, Press JR (1980) Nickel accumulation by species of Peltaria Jacq. (Cruciferae). Taxon 29, 629–633. open url image1

Salt DE, Kato N, Krämer U, Smith RD, Raskin I (2000) The role of root exudates in nickel hyperaccumulation and tolerance in accumulator and nonhyperaccumulator species of Thaspi. ‘Phytoremediation of contaminated soil and water’. pp. 189–200., (CRC Press: Boca Raton, FL)

Shallari S, Schwartz C, Hasko A, Morel JL (1998) Heavy metals in soils and plants of serpentine and industrial sites of Albania. Science of the Total Environment 209, 133–142.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shallari S, Echevarria G, Schwartz C, Morel JL (2001) Availability of nickel in soil for the hyperaccumulator Alyssum murale (Waldst. & Kit.). South African Journal of Soil Science 97, 568–570. open url image1

Tiller KG, Honeysett JL, de Vries MPC (1972) Soil zinc and its uptake by plants. I. Isotopic exchange equilibria and the application of tracer techniques. Soil Research 10, 151–164. open url image1

Voegelin A, Vulava VM, Kretzschman R (2001) Reaction-based model describing competitive sorption and transport of Cd, Zn, and Ni in an acidic soil. Environmental Science and Technology 35, 1651–1657.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yang X, Baligar VC, Marthens DC, Clarks RB (1996) Plant tolerance to nickel toxicity: II. Nickel effects of influx and transport of mineral nutriments in four species. Journal of Plant Nutrition 19, 265–279. open url image1

Zhao FJ, Hamon RE, McLaughlin MJ (2001) Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytologist 151, 613–620.
Crossref | GoogleScholarGoogle Scholar | open url image1