Advertisement

Plant and Soil

, Volume 406, Issue 1–2, pp 55–69 | Cite as

Current status and challenges in developing nickel phytomining: an agronomic perspective

  • Philip Nti NkrumahEmail author
  • Alan J. M. Baker
  • Rufus L. Chaney
  • Peter D. Erskine
  • Guillaume Echevarria
  • Jean Louis Morel
  • Antony van der Ent
Regular Article

Abstract

Background

Nickel (Ni) phytomining operations cultivate hyperaccumulator plants (‘metal crops’) on Ni-rich (ultramafic) soils, followed by harvesting and incineration of the biomass to produce a high-grade ‘bio-ore’ from which Ni metal or pure Ni salts are recovered.

Scope

This review examines the current status, progress and challenges in the development of Ni phytomining agronomy since the first field trial over two decades ago. To date, the agronomy of less than 10 species has been tested, while most research focussed on Alyssum murale and A. corsicum. Nickel phytomining trials have so far been undertaken in Albania, Canada, France, Italy, New Zealand, Spain and USA using ultramafic or Ni-contaminated soils with 0.05–1 % total Ni.

Conclusions

N, P and K fertilisation significantly increases the biomass of Ni hyperaccumulator plants, and causes negligible dilution in shoot Ni concentration. Organic matter additions have pronounced positive effects on the biomass of Ni hyperaccumulator plants, but may reduce shoot Ni concentration. Soil pH adjustments, S additions, N fertilisation, and bacterial inoculation generally increase Ni phytoavailability, and consequently, Ni yield in ‘metal crops’. Calcium soil amendments are necessary because substantial amounts of Ca are removed through the harvesting of ‘bio-ore’. Organic amendments generally improve the physical properties of ultramafic soil, and soil moisture has a pronounced positive effect on Ni yield. Repeated ‘metal crop’ harvesting depletes soil phytoavailable Ni, but also promotes transfer of non-labile soil Ni to phytoavailable forms. Traditional chemical soil extractants used to estimate phytoavailability of trace elements are of limited use to predict Ni phytoavailability to ‘metal crop’ species and hence Ni uptake.

Keywords

Agronomy Annual Ni yield Biomass production Economic Ni phytomining Ni hyperaccumulator plants Ultramafic soils 

Notes

Acknowledgments

The authors acknowledge the French National Research Agency through the national “Investissements d’avenir” program (ANR-10-LABX-21 - LABEX RESSOURCES21) for funding Dr. van der Ent's postdoctoral position and for supporting Mr. Nkrumah's PhD research. Mr. Nkrumah is the recipient of an International Postgraduate Research Scholarship (IPRS) and a UQ Centennial Scholarship at The University of Queensland, Australia. The Nickel Producers Environmental Research Association (NiPERA) supported Dr. Chaney’s work on this evaluation, and findings of research undertaken in cooperation with J.S. Angle, Y.-M Li, R.D. Reeves, R.J. Roseberg, E. Brewer and U. Kukier included herein. We would like to thank the editor and two anonymous reviewers for their constructive comments on an earlier version of this manuscript.

References

  1. Abou-Shanab RAI, Angle JS, Delorme TA, Chaney RL, Van Berkum P, Moawad H, Ghanem K, Ghozlan HA (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224CrossRefGoogle Scholar
  2. Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 38:2882–2889CrossRefGoogle Scholar
  3. Alexander EB (2004) Serpentine soil redness, differences among peridotite and serpentinite materials, Klamath Mountains, California. Int Geol Rev 46:754–764CrossRefGoogle Scholar
  4. Álvarez-López V, Prieto-Fernández Á, Cabello-Conejo MI, Kidd PS (2016) Organic amendments for improving biomass production and metal yield of Ni-hyperaccumulating plants. Sci Tot Environ 548–549:370–379CrossRefGoogle Scholar
  5. Anderson CWN, Brooks RR, Chiarucci A, LaCoste CJ, Leblanc M, Robinson BH, Simcock R, Stewart RB (1999) Phytomining for nickel, thallium and gold. J Geochem Explor 67:407–415CrossRefGoogle Scholar
  6. Angle JS, Baker AJM, Whiting SN, Chaney RL (2003) Soil moisture effects on uptake of metals by Thlaspi, Alyssum, and Berkheya. Plant Soil 256:325–332CrossRefGoogle Scholar
  7. Antić-Mladenović S, Rinklebe J, Frohne T, Stärk H-J, Wennrich R, Tomić Z, Ličina V (2011) Impact of controlled redox conditions on nickel in a serpentine soil. J Soils Sediments 11:406–415CrossRefGoogle Scholar
  8. Baillie IC, Evangelista PM, Inciong NB (2000) Differentiation of upland soils on the Palawan ophiolitic complex, Philippines. Catena 39:283–299CrossRefGoogle Scholar
  9. Baker AJM (1999) Revegetation of asbestos mine wastes. Princeton Architectural Press, New YorkGoogle Scholar
  10. Baker AJM, Brooks R (1989) Terrestrial higher plants which hyperaccumulate metallic elements: a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126Google Scholar
  11. Baker AJM, Walker PL (1989) Physiological responses of plants to heavy metals and the quantification of tolerance and toxicity. Chem Spec Bioavailab 1:7–17Google Scholar
  12. Baker AJM, Proctor J, Van Balgooy M, Reeves R (1992) Hyperaccumulation of nickel by the flora of the ultramafics of Palawan, Republic of the Philippines. Intercept Ltd, AndoverGoogle Scholar
  13. Bani A (2007) In-situ phytoextraction of Ni by a native population of Alyssum murale on an ultramafic site (Albania). Plant Soil 293:79–89CrossRefGoogle Scholar
  14. Bani A, Imeri A, Echevarria G, Pavlova D, Reeves RD, Morel JL, Sulçe S (2013) Nickel hyperaccumulation in the serpentine flora of Albania. Fresen Environ Bull 22:1792–1801Google Scholar
  15. Bani A, Echevarria G, Montargès-Pelletier E, Gjoka F, Sulçe S, Morel JL (2014) Pedogenesis and nickel biogeochemistry in a typical Albanian ultramafic toposequence. Environ Monit Assess 186:4431–4442CrossRefPubMedGoogle Scholar
  16. Bani A, Echevarria G, Sulçe S, Morel JL (2015a) Improving the agronomy of Alyssum murale for extensive phytomining: a five-year field study. Int J Phytoremediat 17:117–127CrossRefGoogle Scholar
  17. Bani A, Echevarria G, Zhang X, Benizri E, Laubie B, Morel JL, Simonnot M-O (2015b) The effect of plant density in nickel-phytomining field experiments with Alyssum murale in Albania. Aust J Bot 63:72–77Google Scholar
  18. Becquer T, Pétard J, Duwig C, Bourdon E, Moreau R, Herbillon AJ (2001) Mineralogical, chemical and charge properties of Geric Ferralsols from New Caledonia. Geoderma 103:291–306CrossRefGoogle Scholar
  19. Bennett F, Tyler E, Brooks R, Gregg P, Stewart R (1998) Fertilisation of hyperaccumulators to enhance their potential for phytoremediation and phytomining. CAB International, WallingfordGoogle Scholar
  20. Booth EJ, Batchelor SE, Walker KC (1995) The effect of foliar-applied sulfur on individual glucosinolates in oilseed rape seed. Z Pflanz Bodenkunde 158:87–88CrossRefGoogle Scholar
  21. Broadhurst CL, Chaney RL, Angle JS, Maugel TK, Erbe EF, Murphy CA (2004a) Simultaneous hyperaccumulation of nickel, manganese, and calcium in Alyssum leaf trichomes. Environ Sci Technol 38:5797–5802CrossRefPubMedGoogle Scholar
  22. Broadhurst CL, Chaney RL, Angle JA, Erbe EF, Maugel TK (2004b) Nickel localization and response to increasing Ni soil levels in leaves of the Ni hyperaccumulator Alyssum murale. Plant Soil 265:225–242CrossRefGoogle Scholar
  23. Broadhurst CL, Tappero RV, Maugel TK, Erbe EF, Sparks DL, Chaney RL (2009) Interaction of nickel and manganese in accumulation and localization in leaves of the Ni hyperaccumulators Alyssum murale and Alyssum corsicum. Plant Soil 314:35–48CrossRefGoogle Scholar
  24. Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides Press, Oregon, USAGoogle Scholar
  25. Brooks RR (1998) Plants that hyperaccumulate heavy metals: their role in phytoremediation, microbiology, archaeology, mineral exploration, and phytomining. CAB International, WallingfordGoogle Scholar
  26. Brooks RR, Wither ED (1977) Nickel accumulation by Rinorea bengalensis (Wall.) O.K. J Geochem Explor 7:295–300CrossRefGoogle Scholar
  27. Brooks R, Chiarucci A, Jaffré T (1998) Revegetation and stabilisation of mine dumps and other degraded terrain. CAB International, WallingfordGoogle Scholar
  28. Cabello-Conejo MI, Prieto-Fernández Á, Kidd PS (2014) Exogenous treatments with phytohormones can improve growth and nickel yield of hyperaccumulating plants. Sci Total Environ 494–495:1–8CrossRefPubMedGoogle Scholar
  29. Cassina L, Tassi E, Morelli E, Giorgetti L, Remorini D, Chaney RL, Barbafieri M (2011) Exogenous cytokinin treatments of an ni hyper-accumulator, Alyssum murale, grown in a serpentine soil: implications for phytoextraction. Int J Phytoremediat 13:90–101CrossRefGoogle Scholar
  30. Centofanti T, Siebecker MG, Chaney RL, Davis AP, Sparks DL (2012) Hyperaccumulation of nickel by Alyssum corsicum is related to solubility of Ni mineral species. Plant Soil 359:71–83CrossRefGoogle Scholar
  31. Chaney RL, Angle JS, Baker AJM, Li YM (1998) Method for phytomining of nickel, cobalt and other metals from soil. US Patent 5:711–784, 27 January 1998Google Scholar
  32. Chaney RL, Li YM, Brown SL, Homer FA, Malik M, Angle JS, Baker AJM, Reeves RD, Chin M (2000) Improving metal hyperaccumulator wild plants to develop commercial phytoextraction systems: approaches and progress. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. CRC Press, Boca Raton, FL, pp 129–158Google Scholar
  33. Chaney RL, Angle JS, Li YM et al. (2007) Recovering metals from soil. US Patent 7268273 B2, 11 September 2007Google Scholar
  34. Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL (2007b) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1433CrossRefPubMedGoogle Scholar
  35. Chaney RL, Chen KY, Li YM, Angle JS, Baker AJM (2008) Effects of calcium on nickel tolerance and accumulation in Alyssum species and cabbage grown in nutrient solution. Plant Soil 311:131–140CrossRefGoogle Scholar
  36. Chardot V, Massoura ST, Echevarria G, Reeves RD, Morel JL (2005) Phytoextraction potential of the nickel hyperaccumulators Leptoplax emarginata and Bornmuellera tymphaea. Int J Phytoremediat 7:323–335CrossRefGoogle Scholar
  37. Chardot V, Echevarria G, Gury M, Massoura S, Morel JL (2007) Nickel bioavailability in an ultramafic toposequence in the Vosges Mountains (France). Plant Soil 293:7–21CrossRefGoogle Scholar
  38. Cheng C-H, Jien S-H, Iizuka Y, Tsai H, Chang Y-H, Hseu Z-Y (2011) Pedogenic chromium and nickel partitioning in serpentine soils along a toposequence. Soil Sci Soc Am J 75:659–668CrossRefGoogle Scholar
  39. Das SK, Sahoo RK, Muralidhar J, Nayak BK (1999) Mineralogy and geochemistry of profiles through lateritic nickel deposits at Kansa, Sukinda, Orissa. J Geol Soc India 53:649–668Google Scholar
  40. Deng THB, Coquet C, Tang YT, Sterckeman T, Echevarria G, Estrade N, Morel JL, Qiu RL (2014) Nickel and zinc isotope fractionation in hyperaccumulating and nonaccumulating plants. Environ Sci Technol 48:11926–11933CrossRefPubMedGoogle Scholar
  41. Durand A, Piutti S, Rue M et al. (2015) Improving nickel phytoextraction by co-cropping hyperaccumulator plants inoculated by plant growth promoting rhizobacteria. Plant Soil:1–14Google Scholar
  42. Echevarria G, Morel JL, Fardeau JC, Leclerc-Cessac E (1998) Assessment of phytoavailability of nickel in soils. J Environ Qual 27:1064–1070CrossRefGoogle Scholar
  43. Echevarria G, Stamatia Tina M, Thibault S, Becquer T, Schwartz C, Morel JL (2006) Assessment and control of the bioavailability of nickel in soils. Environ Toxicol Chem 25:643–651CrossRefPubMedGoogle Scholar
  44. Ernst WHO (1996) Bioavailability of heavy metals and decontamination of soils by plants. Appl Geochem 11:163–167CrossRefGoogle Scholar
  45. Estrade N, Cloquet C, Echevarria G, Sterckeman T, Deng T, Tang Y, Morel J-L (2015) Weathering and vegetation controls on nickel isotope fractionation in surface ultramafic environments (Albania). Earth Planet Sci Lett 423:24–35CrossRefGoogle Scholar
  46. Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191CrossRefPubMedPubMedCentralGoogle Scholar
  47. Golightly J (1979) Nickeliferous laterites: a general description. In: International Laterite Symposium, New Orleans. Soc Mining Eng, Am Instit Mining, Metallurgical, Petroleum Eng 38–56Google Scholar
  48. Hseu Z-Y (2006) Concentration and distribution of chromium and nickel fractions along a serpentinitic toposequence. Soil Sci 171:341–353CrossRefGoogle Scholar
  49. Hunt AJ (2014) Phytoextraction as a tool for green chemistry. Green Process Synthesis 3:3–22CrossRefGoogle Scholar
  50. Jenny H (1980) The soil resource: origin and behaviourGoogle Scholar
  51. Jopony M, Tongkul F (2011) Heavy metal hyperaccumulating plants in Malaysia and its potential applications. In: Kuhn K (ed) New perspectives in sustainable management in different woods. Schriftenreihe der SRH Hochschule Heidelberg, Verlag Berlin GmbH. Logos Verlag Berlin GmbH, Verlag, pp 129–142Google Scholar
  52. Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534CrossRefPubMedGoogle Scholar
  53. Kruckeberg AR (1985) California serpentines: Flora, vegetation, geology, soils, and management problems. vol 78. University of California Press, USAGoogle Scholar
  54. Kruckeberg AR (1991) Plant life of western North American ultramafics. Springer, NetherlandsGoogle Scholar
  55. Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ (2004) The effect of pH on metal accumulation in two Alyssum species. J Environ Qual 33:2090–2102CrossRefPubMedGoogle Scholar
  56. Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Environ Qual 31:109–120CrossRefPubMedGoogle Scholar
  57. Li YM, Chaney R, Brewer E, Roseberg R, Angle JS, Baker AJM, Reeves R, Nelkin J (2003a) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115CrossRefGoogle Scholar
  58. Li YM, Chaney RL, Brewer EP, Angle JS, Nelkin J (2003b) Phytoextraction of nickel and cobalt by hyperaccumulator Alyssum species grown on nickel-contaminated soils. Environ Sci Technol 37:1463–1468CrossRefGoogle Scholar
  59. Massoura ST, Echevarria G, Leclerc-Cessac E, Morel JL (2004) Response of excluder, indicator, and hyperaccumulator plants to nickel availability in soils. Aust J Soil Res 42:933–938CrossRefGoogle Scholar
  60. Massoura ST, Echevarria G, Becquer T, Ghanbaja J, Leclerc-Cessac E, Morel J-L (2006) Control of nickel availability by nickel bearing minerals in natural and anthropogenic soils. Geoderma 136:28–37CrossRefGoogle Scholar
  61. Morrey DR, Balkwill K, Balkwill MJ (1989) Studies on serpentine flora - preliminary analyses of soils and vegetation associated with serpentinite rock formations in the Southeastern Transvaal. S Afr J Bot 55:171–177CrossRefGoogle Scholar
  62. Na G, Salt DE (2011) Differential regulation of serine acetyltransferase is involved in nickel hyperaccumulation in Thlaspi goesingense. J Biol Chem 286:40423–40432CrossRefPubMedPubMedCentralGoogle Scholar
  63. Nicks L, Chambers M (1995) Farming for metals. Min Environ Manag 3:15–18Google Scholar
  64. O’Dell RE, Claassen VP (2009) Serpentine revegetation: a review. Northeast Nat 16:253–271CrossRefGoogle Scholar
  65. Orłowska E, Przybyłowicz W, Orlowski D, Turnau K, Mesjasz-Przybyłowicz J (2011) The effect of mycorrhiza on the growth and elemental composition of Ni-hyperaccumulating plant Berkheya coddii Roessler. Environ Pollut 159:3730–3738CrossRefPubMedGoogle Scholar
  66. Pollard AJ (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566CrossRefGoogle Scholar
  67. Proctor J, Nagy L (1992) Ultramafic rocks and their vegetation: an overview. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, pp 469–494Google Scholar
  68. Proctor J, Woodell SR (1975) The ecology of serpentine soils. Adv Ecol Res 9:255–366CrossRefGoogle Scholar
  69. Quantin C, Becquer T, Rouiller JH, Berthelin J (2001) Oxide weathering and trace metal release by bacterial reduction in a New Caledonia ferrasol. Biogeochemistry 53:323–340CrossRefGoogle Scholar
  70. Quantin C, Becquer T, Rouiller JH, Berthelin J (2002) Redistribution of metals in a New Caledonia Ferralsol after microbial weathering. Soil Sci Soc Am J 66:1797–1804CrossRefGoogle Scholar
  71. Raous S, Becquer T, Garnier J, Martins ED, Echevarria G, Sterckeman T (2010) Mobility of metals in nickel mine spoil materials. Appl Geochem 25:1746–1755CrossRefGoogle Scholar
  72. Raous S, Echevarria G, Sterckeman T, Hanna K, Thomas F, Martins ES, Becquer T (2013) Potentially toxic metals in ultramafic mining materials: identification of the main bearing and reactive phases. Geoderma 192:111–119CrossRefGoogle Scholar
  73. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181CrossRefPubMedGoogle Scholar
  74. Reeves RD, Brooks RR, Press JR (1980) Nickel accumulation by species of Peltaria Jacq. (Cruciferae). Taxon 29:629–633CrossRefGoogle Scholar
  75. Reeves RD, Brooks RR, Dudley TR (1983) Uptake of nickel by species of Alyssum, Bornmuellera, and other genera of Old World Tribus Alysseae. Taxon 32:184–192CrossRefGoogle Scholar
  76. Reeves RD, Baker AJM, Borhidi A, Berazaín R (1996) Nickel-accumulating plants from the ancient serpentine soils of Cuba. New Phytol 133:217–224CrossRefGoogle Scholar
  77. Reeves RD, Baker AJM, Borhidi A, BerazaÍN R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot-London 83:29–38CrossRefGoogle Scholar
  78. Robinson BH, Brooks RR, Kirkman JH, Gregg PEH, Gremigni P (1996) Plant‐available elements in soils and their influence on the vegetation over ultramafic (“serpentine”) rocks in New Zealand. J Roy Soc New Zeal 26:457–468CrossRefGoogle Scholar
  79. Robinson BH, Brooks RR, Howes AW, Kirkman JH, Gregg PEH (1997a) The potential of the high-biomass nickel hyperaccumulator Berkheya coddii for phytoremediation and phytomining. J Geochem Explor 60:115–126CrossRefGoogle Scholar
  80. Robinson BH, Chiarucci A, Brooks RR, Petit D, Kirkman JH, Gregg PEH, De Dominicis V (1997b) The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel. J Geochem Explor 59:75–86CrossRefGoogle Scholar
  81. Robinson BH, Brooks RR, Clothier BE (1999a) Soil amendments affecting nickel and cobalt uptake by Berkheya coddii: potential use for phytomining and phytoremediation. Ann Bot-London 84:689–694CrossRefGoogle Scholar
  82. Robinson BH, Brooks RR, Gregg PEH, Kirkman JH (1999b) The nickel phytoextraction potential of some ultramafic soils as determined by sequential extraction. Geoderma 87:293–304CrossRefGoogle Scholar
  83. Robinson B, Fernández J-E, Madejón P, Marañón T, Murillo J, Green S, Clothier B (2003) Phytoextraction: an assessment of biogeochemical and economic viability. Plant Soil 249:117–125CrossRefGoogle Scholar
  84. Shallari S, Echevarria G, Schwartz C, Morel JL (2001) Availability of nickel in soils for the hyperaccumulator Alyssum murale Waldst. & Kit. S Afr J Sci 97:568–570Google Scholar
  85. Tappero R et al (2007) Hyperaccumulator Alyssum murale relies on a different metal storage mechanism for cobalt than for nickel. New Phytol 175:641–654CrossRefPubMedGoogle Scholar
  86. Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:844–851CrossRefGoogle Scholar
  87. van der Ent A, Mulligan D (2015) Multi-element concentrations in plant parts and fluids of Malaysian nickel hyperaccumulator plants and some economic and ecological considerations. J Chem Ecol 41:396–408CrossRefPubMedGoogle Scholar
  88. van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013a) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334CrossRefGoogle Scholar
  89. van der Ent A, Baker AJM, van Balgooy MMJ, Tjoa A (2013b) Ultramafic nickel laterites in Indonesia (Sulawesi, Halmahera): mining, nickel hyperaccumulators and opportunities for phytomining. J Geochem Explor 128:72–79CrossRefGoogle Scholar
  90. van der Ent A, Baker AJM, Reeves RD, Chaney RL (2015a) Agromining: farming for metals in the future? Environ Sci Technol 49:4773–4780CrossRefPubMedGoogle Scholar
  91. van der Ent A, Erskine P, Sumail S (2015b) Ecology of nickel hyperaccumulator plants from ultramafic soils in Sabah (Malaysia). Chemoecology 25:243–259CrossRefGoogle Scholar
  92. Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776CrossRefPubMedGoogle Scholar
  93. Viets FG (1962) Micronutrient availability, chemistry and availability of micronutrients in soils. J Agr Food Chem 10:174–178CrossRefGoogle Scholar
  94. Vithanage M, Rajapaksha AU, Oze C, Rajakaruna N, Dissanayake CB (2014) Metal release from serpentine soils in Sri Lanka. Environ Monit Assess 186:3415–3429CrossRefPubMedGoogle Scholar
  95. Vlamis J, Jenny H (1948) Calcium deficiency in serpentine soils as revealed by adsorbent technique. Science 107:549CrossRefPubMedGoogle Scholar
  96. Walker RB (1948) Molybdenum deficiency in serpentine barren soils. Science 108:473–475CrossRefPubMedGoogle Scholar
  97. Walker RB (2001) Low molybdenum status of serpentine soils of western North America. S Afr J Sci 97:565–568Google Scholar
  98. Walker RB, Walker HM, Ashworth PR (1955) Calcium-magnesium nutrition with special reference to serpentine soils. Plant Physiol 30:214–221CrossRefPubMedPubMedCentralGoogle Scholar
  99. Wild H (1974) Indigenous plants and chromium in Rhodesia. Kirkia:233–241Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Philip Nti Nkrumah
    • 1
    Email author
  • Alan J. M. Baker
    • 1
    • 2
    • 4
  • Rufus L. Chaney
    • 3
  • Peter D. Erskine
    • 1
  • Guillaume Echevarria
    • 4
    • 5
  • Jean Louis Morel
    • 4
    • 5
  • Antony van der Ent
    • 1
    • 4
    • 5
  1. 1.Centre for Mined Land Rehabilitation, Sustainable Minerals InstituteThe University of QueenslandBrisbaneAustralia
  2. 2.School of BioSciencesThe University of MelbourneMelbourneAustralia
  3. 3.USDA-Agricultural Research Service, Crop Systems and Global Change LaboratoryBeltsvilleUSA
  4. 4.Université de Lorraine, Laboratoire Sols et EnvironnementVandœuvre-lès-NancyFrance
  5. 5.INRA, Laboratoire Sols et EnvironnementVandœuvre-lès-NancyFrance

Personalised recommendations