ELSEVIER Journal of Geochemical Exploration 67 (1999) 407±415 www.elsevier.com/locate/jgeoexp Phytomining for nickel, thallium and gold C.W.N. Anderson a, R.R. Brooks a,Ł, A. Chiarucci b, C.J. LaCoste a,M.Leblancc, B.H. Robinson d,R.Simcocke,R.B.Stewarta a Soil and Earth Sciences, Institute of Natural Resources, Massey University, Palmerston North, New Zealand b Dipartimento di Biologia Ambientale, UniversitaÁ di Siena, Siena, Italy c GeÂo¯uides-Bassins-Eau, CNRS, Universite de Montpellier II, Montpellier 34095, France d Horticulture and Food Research Institute, Palmerston North, New Zealand e Landcare Research Ltd., Massey University, Palmerston North, New Zealand Accepted 22 July 1999 Abstract The technique of phytomining involves growing a crop of a metal-hyperaccumulating plant species, harvesting the biomass and burning it to produce a bio-ore. The ®rst phytomining experiments were carried out in California using the Ni-hyperaccumulator Streptanthus polygaloides and it was found that a yield of 100 kg=ha of sulphur-free Ni could be produced. We have used the same technique to test the phytomining potential of the Ni-hyperaccumulators Alyssum bertolonii from Italy and Berkheya coddii from South Africa. The effect of different fertiliser treatments on growth of Alyssum bertolonii was established in situ in Tuscany and showed that the biomass of the plant could be increased by a factor of nearly 3 (4.5 t=ha to 12 t=ha) without signi®cant loss of the Ni concentration (7600 mg=kg) in the plant. Analogous experiments have been carried out on Berkheya coddii where a biomass yield of over 20 t=ha can readily be achieved though the Ni concentration is not as high as in A. bertolonii. The total yield is, however, much greater. We have also been able to induce plants to hyperaccumulate Au by adding ammonium thiocyanate to the substrate. Up to 57 mg=kg Au (dry mass) could be accumulated by Indian mustard (Brassica juncea). Unusual hyperaccumulation (>500 mg=kg dry mass) of Tl has been determined in Iberis intermedia and Biscutella laevigata (Brassicaceae) from southern France. The Iberis contained up to 0.4% Tl (4000 mg=kg) in the whole-plant dry matter and the Biscutella over 1.5%. This unusually high accumulation of Tl has signi®cance for animal and human health, phytoremediation of contaminated soils, and phytomining for Tl. We calculate that using Iberis, a net return of $ US 1200=ha (twice the return from a crop of wheat) would be possible with a biomass yield of 10 t=ha containing 0.08% Tl in dry matter. The break-even point (net yield of $ US 500=ha) would require 170 mg=kg (0.017%) Tl in dry matter. A model of a phytomining operation and its economics is presented and its advantages and disadvantages discussed. 1999 Elsevier Science B.V. All rights reserved. Keywords: Alyssum bertolonii; Berkheya coddi; phytomining; phytoremediation; gold; nickel; thallium 1. Introduction metal. Subsequently, the crop is harvested and the metal extracted. Hyperaccumulator plants were orig- The technique of phytomining involves the use of inally de®ned by Brooks et al. (1977) as taxa con- hyperaccumulator plants to grow and concentrate a taining >1000 mg=kg (ppm) Ni in their dry biomass. This concentration was selected on the basis of being Ł Corresponding author. E-mail: [email protected] 100 times the Ni concentration of non-accumulator 0375-6742/99/$ ± see front matter 1999 Elsevier Science B.V. All rights reserved. PII: S0375-6742(99)00055-2 408 C.W.N. Anderson et al. / Journal of Geochemical Exploration 67 (1999) 407±415 plants, even when growing over Ni-rich ultrama®c (`serpentine') soils. The term hyperaccumulator was later rede®ned to include uptake by plants of most other heavy metals except for Cd (at a threshold of 100 mg=kg Ð Reeves et al., 1995), Mn and Zn (at 10,000 mg=kg Ð Reeves and Brooks, 1983), and Au (at 1 mg=kg Ð Anderson et al., 1998). There are about 300 Ni-hyperaccumulator species, 26 of Co, 24 of Cu, 19 of Se, 16 of Zn, 11 of Mn, 2 of Tl (including new data in this present paper) and one of Cd (Table 1). Most of these plants were initially regarded as scienti®c curiosities until it was proposed by Chaney (1983) and Baker and Brooks (1989) that they might be used to remove pollutants from soils (phytoremediation). Their use for phyto- mining was ®rst suggested by Chaney (1983). A phy- tomining operation would entail planting a hyperac- cumulator crop over a low-grade ore body or mineral- ized soil, followed by harvesting and incineration of the biomass to produce a commercial bio-ore. A U.S. Patent has since been taken out on phytomining for various metals including Ni (Chaney et al., 1998). 2. Phytomining for nickel 2.1. Pioneering studies with Streptanthus polygaloides Fig. 1. A crop of nickel in plants of Streptanthus polygaloides growing in California. Photo by Larry Nicks and Michael Cham- bers. The ®rst ®eld trials on Ni phytomining in 1994 were based at the US Bureau of Mines, Reno, Nevada (Nicks and Chambers, 1995, 1998) and other crops Ð for example, it is well in excess of the used a naturally occurring stand of Streptanthus average return of $ US 333=ha (including $ US 111 polygaloides (Fig. 1), a known Ni-hyperaccumula- for wheat straw) obtained by US wheat farmers in tor (Reeves et al., 1981). The soil contained about 1995. 0.35% Ni, well below the economic range for con- ventional mining. Nicks and Chambers (1995, 1998) 2.2. Studies with Alyssum bertolonii proposed that a net return to the grower of $ US 513=ha could be achieved, assuming that: (1) a mini- Alyssum bertolonii (Fig. 2), the ®rst plant species mum of selective breeding produced plants with 1% identi®ed as a hyperaccumulator of Ni (Minguzzi Ni in dry mass; (2) the world price of Ni was $ US and Vergnano, 1948) was used in the second phyto- 7.65=kg; (3) the biomass yield after moderate fertil- mining ®eld trials (Robinson et al., 1997a) in Italy at ization was 10 t=ha; (4) a quarter of the energy of Murlo, Tuscany. Plants were fertilized with N C P C combustion of the biomass could be turned into elec- K combinations over a two-year period. A threefold tricity for a yield of $ US 131=ha; (5) the return to increase of the biomass of dry matter to 9.0 t=ha the grower would be half of the gross yield of $ US was gained with N C P C K without dilution of the 765 for the metal plus the energy yield of $ US 131. unfertilized Ni concentration. A Ni level of 0.8% in This compares well with the average returns from dry matter (11% in ash), equated to a yield of 72 C.W.N. Anderson et al. / Journal of Geochemical Exploration 67 (1999) 407±415 409 Table 1 Speci®c hyperaccumulators (natural and induced) that could be used for phytomining Element Species Mean metal concn. Biomass (mg=kg d.w.) (t=ha) Cadmium Thlaspi caerulescens 3,000 (1) 4 Cobalt Haumaniastrum robertii 10,200 (1) 4 Copper Haumaniastrum katangense 8,356 (1) 5 Gold a Brassica juncea 10 (0.001) 20 Lead Thlaspi rotundifolium subsp. 8,200 (5) 4 Manganese Macadamia neurophylla 55,000 (400) 30 Nickel Alyssum bertolonii 13,400 (2) 9 Berkheya coddii 17,000 (2) 22 Selenium Astragalus pattersoni 6,000 (1) 5 Thallium Biscutella laevigata 13,768 (1) 4 Iberis intermedia 4,055 (1) 10 Uranium Atriplex confertifolia 100 (0.5) 10 Zinc Thlaspi calaminare 10,000 (100) 4 d.w. D dry weight. a Induced hyperaccumulation using ammonium thiocyanate. NB: values in parentheses are mean concentrations usually found in non-accumulator plants. kg of Ni=ha. There was no correlation between the concentration of 768 mg=kg. Thus, seven croppings age of a plant and its Ni content. The long-term would reduce the plant-available Ni pool by 30%. cropping sustainability of the soils was simulated A proposed model for phytomining (Robinson et al., by sequential extractions with potassium hydrogen 1997a) involved harvesting the crop after 12 months phthalate solutions at pH 2, 4 and 6 (Robinson et and burning the material to produce a sulphur-free al., 1999) that showed a limiting plant-available Ni bio-ore with about 11% Ni. Fig. 2. Alyssum bertolonii Ð a nickel hyperaccumulator from Tuscany, Italy. The dried leaves contain on average about 1% (10,000 mg=kg) nickel. 410 C.W.N. Anderson et al. / Journal of Geochemical Exploration 67 (1999) 407±415 2.3. Studies with Berkheya coddii intermedia,andMinuartia verna (a non-accumula- tor). The third recorded phytomining ®eld trials for Thallium is extremely toxic and is used both in Ni (Robinson et al., 1997b) used the South African rat poison and for the control of ants. It also has Ni-hyperaccumulator Berkheya coddii. Field trials uses in the electronics industry in semiconductors, in New Zealand showed that a dry biomass of 22 switches and fuses. Thallium minerals are quite rare t=ha could be achieved after moderate fertilisation (0.7 mg=kg in the Earth's crust Ð Green, 1972), and (N C P C K). Pot trials showed enhanced biomass are found almost exclusively in the realgar deposits and relatively higher uptake of Ni with increasing of Allchar (Alsar) in Macedonia near the Greek bor- nitrogen addition, but no increase with phosphorus. der. They occur as complex sulphides of As±Hg±Tl The Ni content of the plant was directly related (lorandite, picopaulite, raguinite, vrbaite) associated to the ammonium-acetate-extractable fraction of Ni with realgar and iron sulphides.