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Gold phytomining. A review of the relevance of this


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Journal of Environmental Management 111 (2012) 249e257

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Journal of Environmental Management


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Review

Gold phytomining. A review of the relevance of this technology to mineral


extraction in the 21st century
Victor Wilson-Corral a, *, Christopher W.N. Anderson b, Mayra Rodriguez-Lopez c
a
Facultad de Ingenieria, Universidad Autonoma de Sinaloa, Culiacan 80013, Mexico
b
Institute of Natural Resources, Massey University, Palmerston North 4442, New Zealand
c
Centro de Estudios Justo Sierra, Surutato 80600, Mexico

a r t i c l e i n f o a b s t r a c t

Article history: The precious metal gold can be found at high concentration in tailings dumps and waste rock piles at
Received 10 January 2012 many mining locations around the world. Conventional technology is generally unable to economically
Received in revised form recover this residual gold, and, as a result, the potential resource is wasted, presenting environmental
27 June 2012
risk to the wider ecosystem through particulate and dissolved metal leaching and erosion. For the past 14
Accepted 31 July 2012
Available online
years, the idea of gold phytomining to recover this gold resource has been researched by various
scientific groups worldwide. A number of plant species have been tested under laboratory, greenhouse,
and field conditions to determine their potential for use in the phytoextraction of gold. This paper
Keywords:
Induced hyperaccumulation
presents a review of reported gold phytomining trials developed in the laboratory, the greenhouse under
Hyperaccumulator plants soil and hydroponic conditions, as well as in the field, between 1998 and 2011. A summary economic
Mine tailings assessment for gold phytomining in Mexico is also presented. Mexico is an example of a developing
Waste rock country with a long history of gold mining that has a large resource of sites that might be suitable to gold
Mineralized soils phytomining. The technology remains limited by certain environmental and plant physiology factors.
Economic assessment However, the increase in the market price for gold during the first decade of the 21st century and into
2011, and advances recorded for the gold concentration and biomass yield of a range of plant species,
suggest that gold phytomining might be an economically viable technology.
Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction causes environmental problems due to concentration of heavy


metals such as arsenic (Armienta et al., 2008), lead (Mendez et al.,
Despite advances in mining technologies, conventional tech- 2008), copper (Martínez-Pagán et al., 2009) and mercury (Melamed
nology cannot remove 100% of the gold hosted in minerals. and Villas-Bôas, 1998) in the tailings. Environmental risk that is
Therefore, mine waste or tailings areas usually contain residual apparent for tailings is a powerful driver for cost-effective remedial
gold at low concentration, but this can increase to relatively high solutions.
concentration in some heap leach pads and waste dumps (Sheoran The enormous costs associated with the removal of pollutants
et al., 2009; Wilson-Corral et al., 2006). Generally speaking, the from soil by means of traditional physicochemical technology have
older the mining operation, the higher the residual gold concen- stimulated the development of innovative biological technologies
tration in mine wastes. Past mining operations have generated to extract or to stabilize soil pollutants (Hernandez-Allica et al.,
large volumes of waste that is of the order of billons of tons and is 2006). One such technology that is widely recognized is phytor-
distributed around the world. These wastes are deposited in emediation (Salt et al., 1995), and the application of this technology
established locations and can remain at these locations for many to remove heavy metals from soil (phytoextraction) has been
decades in a non-rehabilitated state. Wastes generated by the demonstrated to be a cost-effective technology for soil remediation
mining industry are often subject to secondary movement that is if hyperaccumulator plants are used (Chaney et al., 2007). Gold is
facilitated by air and water (erosion). The transport of this material one of the metals for which phytoextraction has been described.
The recovery of residual gold left in mine tailings as well as
mineralized soils using several species of plants has been proposed
* Corresponding author. Facultad de Ingenieria Culiacan, Universidad Autonoma
de Sinaloa, Av. Universitarios s/n, Ciudad Universitaria, Culiacan 80013, Mexico. as a viable alternative for precious metals recovery from tailings,
E-mail addresses: vimawc@uas.edu.mx, vimawc@gmail.com (V. Wilson-Corral). waste rock and ore (Anderson et al., 1998).

0301-4797/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jenvman.2012.07.037
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250 V. Wilson-Corral et al. / Journal of Environmental Management 111 (2012) 249e257

1.1. Gold accumulation in plants induced hyperaccumulation, and has been achieved for gold using
a range of chemicals (Table 1).
Since the early years of the 20th century, there have been The geochemistry of the soil environment hosting the gold will
reports about the accumulation of gold by plants, particularly trees determine the chemical needed to promote gold solubility. While
(Warren and Delavault, 1950). These studies have shown that the form of gold present in the soil will dictate the concentration of
coniferous trees, in particular, can accumulate quantities of gold gold that will be introduced into the soil solution after the addition
that are in the order of parts per billion in their tissues. Some of appropriate chemicals (Anderson et al., 1999b). Gold hyper-
studies have reported several plant species as quick, inexpensive, accumulation has been defined as accumulation greater that 1 mg/
and effective tools for gold exploration in arid and semiarid kg, with this limit being based upon a normal gold concentration in
environments (Busche, 1989). And, as a result, some mining plants of only 0.01 mg/kg (Anderson et al., 2003).
companies use plant species as bioindicators of the presence of
gold in soil (biogeochemical exploration) (McInnes et al., 1996). 2. Gold phytomining
However, the hyperaccumulation of gold is not a natural trait of
plant species (Anderson et al., 1999a). Although gold can be highly The reuse of waste allows for beneficial secondary application,
mobile (Reith and McPhail, 2007), under surface environmental whereas recycling extracts resource ingredients or converts wastes
conditions it is insoluble and this reduces its bioavailability and into valuable products (Lottermoser, 2011). Lottermoser has sug-
limits the potential for phytoextraction; bioavailability is one of gested that as of yet, many of the proposed reuse and recycling
the most critical factors for plant uptake of metals (Gardea- concepts for mine wastes are not economic, and consequently, the
Torresdey et al., 2005). great majority of mine wastes are still being placed into waste
Gold may be solubilised from minerals and soils by microbial storage facilities. Phytoextraction technology (Salt et al., 1995), if
activity (Korobushkina et al., 1983), by cyanogenic plants (Girling successfully used to recover gold from tailings or another waste-
and Peterson, 1980; Lakin et al., 1974) and through the action of rock body, would, however, represent a technology paradigm
naturally-occurring soil chemicals (Bowell et al., 1993). Relatively shift in the context of Lottermoser’s discussion. Gold phytoex-
high gold solubility is known to occur in geological domains called traction, where the aim of the operation is to yield an economic
weathering terrains. Examples of these can be found in Western profit, is better known as gold phytomining. Phytomining (Nicks
Australia, West Africa and South America, but the geochemical and Chambers, 1994) has also been suggested as a possible alter-
characteristics of the associated weathering fluids are poorly native to recover nickel (Bhatia et al., 2005; Reeves et al., 1999;
understood. The existence of a low concentration of gold in soil Robinson et al., 1999), and thallium (Leblanc et al., 1999) from
solution at certain locations around the world as a result of these mineralized soils or waste rock.
biological and chemical processes explains the reported records of Effective systems for environmental protection are a key
gold in plants. component in modern mining operations. Mining in all countries
must today show environmental sustainability during the planning,
1.2. Metal hyperaccumulation by plants operation and rehabilitation stages of mining. It is in response to
this call for greater environmental sustainability that researchers
It is known that hyperaccumulator plants absorb metals, even around the world have sought to develop gold phytomining as an
those that are not essential, in concentrations similar to the macro effective and economically viable technology (Anderson et al.,
nutrients. Brooks and colleagues introduced the term hyper- 2000; Harris et al., 2009; Mohan, 2005; Sheoran et al., 2009;
accumulation to describe plants that absorb nickel concentrations, Wilson-Corral et al., 2011). Key researchers in the subject area are
exceeding 1000 mg/kg dry matter grown on serpentine soils (Jaffre based at the Institute of Natural Resources, Massey University in
et al., 1976). This report describes how areas of nickel-rich rock New Zealand; the Department of Chemistry, University of Texas El
around the world could be identified by analyzing small pieces of Paso in the United States of America; the Universidad Autonoma de
plant material. Later, the term hyperaccumulator was used to refer Sinaloa in Culiacan, Mexico; The School of Botany, University of
to any plant species in which metal accumulation is unusually high, Melbourne, and the School of Chemical and Biomolecular Engi-
irrespective of the metal concentration in the substrate (Brooks neering at the University of Sydney in Australia.
et al., 1977). Most recently, hyperaccumulator plants have been
Table 1
defined as those that accumulate metal to concentrations that are Chemicals used to solubilize gold in soil or soil-like media during gold phytoex-
10e100 times the concentrations found in “normal” plants (Chaney, traction studies.
1983). These concentrations are an order of magnitude higher than
Chemical name Formula Reference
that found in other plants growing in the same environment. Today,
Ammonium NH4SCN Anderson et al., 1998;
440 hyperaccumulator plant species are known, of which 75% are
thiocyanate Gardea-Torresdey et al., 2005;
nickel hyperaccumulator (Reeves, 2006). The remaining plant Msuya et al., 2000;
species hyperaccumulate metals such arsenic, cadmium, manga- Rodriguez-Lopez et al., 2009;
nese, sodium, thallium, and zinc. Rodriguez et al., 2006
Ammonium (NH4)2S2O3 Anderson et al., 1998; Lamb et al., 2001;
thiosulphate Msuya et al., 2000; Rodriguez-
1.3. Induced hyperaccumulation of gold in plants Lopez et al., 2009
Thiourea CH4N2S de la Rosa et al., 2009; Gardea-
The initial discovery (October 1997) that plants could be Torresdey et al., 1999; Rodriguez-
induced to accumulate gold from ‘soil’ was serendipitous Lopez et al., 2009; Rodriguez et al., 2006
Sodium thiocyanate NaSCN Lamb et al., 2001
(Anderson et al., 1998). From this initial finding, works have
Potassium iodide KI Lamb et al., 2001
intensified with an aim to increase the level of gold accumulation in Potassium cyanide KCN Lamb et al., 2001
plants. To overcome the apparent lack of gold solubility in soil, Potassium bromide KBr Lamb et al., 2001
scientists since 1998 have experimented with a range of chemicals Sodium cyanide NaCN Anderson et al., 1998;
that when applied to soil will increase gold solubility, and effec- Anderson et al., 2005; Piccinin et al., 2007;
Rodriguez-Lopez et al., 2009; Wilson-
tively force gold uptake into plants. This technique is described in Corral et al., 2011
the literature as chelant or chelate-enhanced phytoextraction, or
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V. Wilson-Corral et al. / Journal of Environmental Management 111 (2012) 249e257 251

The current state of gold phytomining technology is reviewed in treatments 5 mg/kg gold þ ammonium thiocyanate, 5 mg/kg
this work, and options for the implementation of the technology in gold þ thiourea, 10 mg/kg gold þ ammonium thiocyanate and
Mexico are proposed. 10 mg/kg gold þ thiourea was about 197, 296, 206 and 210 mg/kg of
dry mass, respectively (Rodriguez et al., 2006).
2.1. Evidence for gold phytoextraction Also during 2006, studies were conducted in Mexico where
plants were tested for their ability to extract gold from silica sand.
The key variable necessary for the uptake of gold by plants is In this work the following species were used: Amaranthus spp.
formation of a stable, soluble, goldeligand complex within the soil (amaranth), Sorghum halepense (L.) Pers. (johnson grass), Helianthus
solution. If such a complex is formed, it seems likely that a plant annuus L. (sunflower), Sesamum indicum L. (sesame), Gossypium
will have little choice but to act as a pump and accumulate the hirsutum L. (upland cotton), Brassica campestris L. (field mustard),
metal during transpiration, to a concentration that is proportional and Amoreuxia palmatifida Moc. & Sessé ex DC. (mexican yellow-
to the total gold concentration in the soil. Problematic is the fact show) (Wilson-Corral, 2008). Results showed that it is possible to
that gold will only form soluble and stable complexes for a narrow induce gold concentrations above 304 mg/kg of dry matter in
range of pH and redox (Eh) parameters that change as a function of B. campestris growing at gold-enriched silica sand and using
the specific ligand used (Anderson, 2005). No plants of high ammonium thiocyanate in a dose of 1.0 g/kg of substrate.
biomass will grow well at low pH and thus it would not be practical In 2007, a study on gold phytoextraction conducted in Australia
to phytoextract gold from an area of auriferous material with a pH was reported. Material was collected from the Davis stockpile at
of less than 4. As a result, studies have been developed during the Stawell Gold Mine, Victoria, Australia. The oxide ore collected for
last years to determine the optimal conditions for gold phytoex- this study had a mean gold grade of 1.75 mg/kg and a pH of 5.0. The
traction from mine wastes under laboratory conditions. following plants were tested: Eucalyptus polybractea R. T. Baker
Generally the chemicals used to induce gold uptake are effective (blue mallee), Acacia decurrens (Wendl. f.) Willd. (black wattle),
at alkaline pH (cyanide and thiocyanate). Thiocyanate is, however, Sorghum bicolor (L.) Moench (sorghum), Trifolium repens L. (white
an exception, and can form a stable complex with gold under acid clover cvs. Tribute and Prestige), Bothriochloa macra (Steud.) S.T.
conditions (Shacklette et al., 1970). The pH levels in a substrate may Blake (red grass), Austrodanthonia caespitosa (Gaudich.) H.P. Linder
be modified by applying soil amendments that will either raise (wallaby grass), and Microlaena stipoides (Labill.) R. Br. (weeping
(lime) or lower pH such as ammonia-containing fertilizers, organic grass). All plants were grown in pots with 500 g of ore for three to
and inorganic acids, and elemental sulphur (S) (Sheoran et al., five months prior to treatment with sodium cyanide at a treatment
2009). rate of 0.1 g or 1 g cyanide per kg ore. Biomass was harvested after
treatment and analyzed by ICP-OES for gold and other metals. The
2.2. Laboratory and greenhouse studies for gold phytoextraction results of this study showed that gold hyperaccumulation was
induced in all plant species tested. Mean gold concentrations of up
The first report of induced hyperaccumulation of gold in plants to 27 mg/kg dry weight were found in the plant tissue of T. repens
was made for a greenhouse study (Anderson et al., 1998). In this cv. Prestige. Higher gold concentrations were generally found in the
work, Brassica juncea (L.) Czern. (Indian mustard) was induced to stems and older leaves with the lowest gold concentrations in the
accumulate gold in leaf tissues to a concentration as high as 57 mg/ young leaves. Plants grown in substrate treated with 1 g/kg cyanide
kg of dry matter from silica sand containing finely disseminated generally had a higher concentration of gold in their plant tissue
gold at a concentration of 5 mg/kg of susbstrate. Subsequent to the than plants grown in the 0.1 g/kg cyanide treatment. This study
1998 findings, laboratory tests using the crop plants Raphanus highlighted the potential use of plants to extract and concentrate
sativus L. (radish), Allium cepa L. (onion), Beta vulgaris L. (beet) and gold from ‘real life’ low-grade ore and waste products (Piccinin
Daucus carota L. (carrot) cultivated in a silica sand containing et al., 2007).
3.8 mg/kg gold at a pH of 6.4, showed that gold concentrations During 2009, to evaluate the gold extraction potential of
greater than 200 mg/kg of plant tissue in R. sativus could be ach- S. halepense cultivated on mine tailings with a gold concentration of
ieved (Msuya et al., 2000). 2.35 mg/kg and a value of pH of 7.3, a greenhouse trial using this
During 2001, scientists developed a trial in which artificial gold- species was developed in Mexico. In this study, sodium cyanide,
bearing soil was prepared to contain a gold concentration of 5 mg/ thiourea, ammonium thiocyanate, and ammonium thiosulphate
kg. The chemicals used as an amendment in this work were NaCN were used to induce gold hyperaccumulation. These trials revealed
(sodium cyanide), KCN (potassium cyanide), KI (potassium iodide), that cyanide at a dose of 1.0 mg/kg of susbstrate could induce gold
KBr (potassium bromide), and (NH4)2S2O3 (ammonium thio- concentrations up to 31 mg/kg of dry matter (Rodriguez-Lopez
sulphate). B. juncea, Berkheya coddii Roessler and Cichorium intybus et al., 2009). A similar test using the same mine tailings was con-
L. (chicory) were grown in the artificial ore and treated with each of ducted using Kalanchoe serrata (magic tower), a plant species that
the stated chemicals. The results of this study showed that gold can grow under high temperature and scarce water conditions that
concentrations in B. juncea plants could reach as high as 326 mg/kg can prevail in deserts. The results of this study showed that
(dry weight) in the leaves and 46e88 mg/kg for stems and roots K. serrata could accumulate an average gold concentration of
(dry weight) after treatment of the soil with cyanide (Lamb et al., 21 mg/kg using cyanide to promote gold solubility (Wilson-Corral
2001). et al., 2011).
During 2006, a greenhouse trial using the desert plant Chilopsis A summary of the highest gold concentrations reported for
linearis (Cav.) Sweet (desert willow) cultivated in soil was carried greenhouse studies is presented as Table 2.
out. The substrate was amended with a gold concentration of 5 or A recent laboratory study described the collateral effects on
10 mg/kg soil. The chelating agents used in this experiment to plants of the amendments used for gold phytomining. Ammonium
induce gold uptake were thiourea or ammonium thiocyanate at thiosulphate, ammonium thiocyanate and sodium cyanide were
a treatment rate of 0.76 g/kg of substrate. A representative sample used to test the degree of solubilization and leaching of non-target
of plants was harvested at 5 h, 24 h, 2 days and 4 days after the metals of potential regulatory interest in an oxide ore under
application of the chelating agents. Plants grown in soil with 5 and varying levels of pH (Ebbs et al., 2010). The results of this work
10 mg/kg gold accumulated similar amounts of gold in their stems. showed that metals such as copper and iron will leach when
The average gold concentration accumulated in stems for the cyanide or thiosulphate (respectively) is added to ore and to a lesser
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252 V. Wilson-Corral et al. / Journal of Environmental Management 111 (2012) 249e257

Table 2 (dry weight) from a hydroponic solution treated with thiourea


A summary of the maximum reported gold concentrations obtained for a range of (0.2 M). Accumulation was reported across a pH range of 2.0e6.0.
plant species grown under greenhouse conditions.
C. linearis has been extensively studied for gold phytomining in
Plant specie Substrate Gold in Chelating Rateb MGCPc Reference hydroponic solutions using thiourea as an agent to induce uptake
substratea agent (Rodríguez et al., 2007a) as well as in agar-based growing media
Brassica Silica sand NRd NH4 SCN 0.64 57 Anderson (Rodriguez et al., 2007b). Gold concentrations as high as 179 mg/kg
juncea et al., 1998
(dry weight) have been reported from solution with a gold
Raphanus Silica sand 3.8 NH4 SCN 1.0 220 Msuya
sativus et al., 2000 concentration of 160 mg of gold/L. The capacity of Zea mays L. (corn)
Brassica Silica sand 5 KCN 1.0 326 Lamb to uptake gold in the presence of thiourea and ammonium thio-
juncea et al., 2001 cyanate has been investigated in hydroponic media. Results have
Chilopsis Soil 5 CH4N2S 0.76 296 Rodriguez showed that a gold concentration in solution of up to 160 mg/L does
linearis et al., 2006
Brassica Silica sand 3.8 NH4 SCN 1.0 304 Wilson-
not reduce corn seed germination or plant growth. Both thiourea
campestris Corral, 2008 and ammonium thiocyanate have been shown to induce a 6-fold
Trifolium Mineral 1.75 NaCN 1.0 27 Piccinin increase of the gold concentration in roots, while thiourea will
repens et al., 2007 induce a 10-fold increase of the gold concentration in shoots (de la
cv. Prestige
Rosa et al., 2009).
Sorghum Mine tailings 2.35 NaCN 1.0 31 Rodriguez-
halepense Lopez et al., A study published in 2010 showed that M. sativa roots could
2009 obtain a gold concentration as high as 287 mg/g (287,000 mg/kg)
Kalanchoe Mine tailings 2.35 NaCN 1.0 21 Wilson- when exposed for 72 h to solution containing 10 g/L (10,000 mg/L)
serrata Corral et al., gold at a pH of 3. B. juncea recorded a maximum root gold
2011
concentration of 227 mg/g when exposed to the same solution for
a
The units of gold concentration are g/t or mg/kg. 48 h (Bali et al., 2010).
b
Treatment rate is expressed as g of chemical per kg of substrate. Molar
concentrations (where originally reported) have been converted to mass
concentrations. 2.3. Field trials for gold phytoextraction
c
MGCP ¼ Maximum Gold Concentration in Plants; expressed in mg/kg dry
matter. During 2003, the first field trial for gold phytoextraction from
d
NR ¼ Not reported. mine tailings was conducted using sodium cyanide and ammonium
thiocyanate as chemicals to induce gold hyperaccumulation
extent nickel or zinc when cyanide or thiocyanate (respectively) is (Anderson et al., 2005). In this work B. juncea and Z. mays were used
used. The interactions between soil, metals and the root system to recover gold from rock with a gold concentration of 0.6 mg/kg.
represent key factors controlling the success of plant production The pH range in soils was 8.9e9.5. The results showed that from
(Epstein, 1965), and increased solubility of these non-target metals this gold concentration in soil it is possible to achieve an average
is likely to detrimentally affect plant health. Some studies have gold concentration of up to 39 mg/kg of dry matter in Indian
therefore been developed to evaluate the practical effect of the mustard under field conditions. This trial suggested that potentially
enhanced mobility of these non-target metals also present in mine between 10 and 20% of the total gold present in the plant root zone
tailings. For example, the effect of the presence of copper in mine can be removed in any one crop.
tailings on growth and element uptake by mesquite plants (Prosopis Towards the end of 2006, researchers at the Centro de Innova-
sp.) was recently reported (Haque et al., 2009). Although some cion y Desarrollo Educativo (CIDE A.C.) conducted field trials in
plants species have developed tolerance to certain copper levels Mexico where plants of B. juncea were cultivated in mine tailings
(Stewart and Anderson, 2005), this is a toxic metal for other plant with a gold concentration of 2.47 mg/kg and a pH of 7.6. The results
species (Deo and Nayak, 2011; Michaud et al., 2008). Research has showed that it was possible to obtain commercial-scale biomass
specifically investigated the interactive effect of copper and gold in yields in excess of 8 ton/ha under field conditions (Wilson-Corral,
soil solution after treatment of soil to induce gold uptake (Wilson- 2008). Then, in 2009, a field trial was conducted to establish the
Corral et al., 2011). The results of this study confirmed that there is potential of the species H. annuus to recover gold from mine tail-
an associated increase in copper uptake by some plants when ings. A plot of 50 m2 was constructed. The average gold concen-
treatment is applied to soil to induce gold uptake and indicate that trations for leaves, stems, and roots, were 16, 21, and 15 mg/kg of
increased copper uptake causes necrosis of the plants after treat- dry mater, respectively after cyanide treatment of the mature
ment. However, this response does not appear to be equivalent for biomass (Wilson-Corral et al., 2011).
all species. Some trials have shown that H. annuus has the potential
ability to accumulate copper without being overly sensitive to 2.4. What is the best plant species for gold phytomining?
copper toxicity (Lin et al., 2003) and this may lead to increased
potential for gold uptake in this species. A review of the literature shows that a large number of plant
Gold phytoextraction processes have also been studied under species have been used for gold phytomining research. These plants
hydroponic conditions. A hydroponic experimental growth media have generally been crop species, presumably due to the ready
presents an advantage over soil media in that the solubility of gold, availability of seed and well established systems for propagation
nutrient and other heavy metals can be more tightly controlled. and growth. For a gold phytomining operation the desirable traits
This allows for the testing of isolated or specific variables. For of a plant species include fast growth and high biomass yield as
example the effects of gold and mercury on the growth, nutrient well as drought, salinity and high temperature resistance. But, no
uptake and anatomical changes of C. linearis have been studied single crop of plants is likely to remove all of the gold in the soil.
(Rodríguez et al., 2009). Literature evidence indicates that plants may remove 10e20% of
The first report on gold phytoextraction from hydroponic solu- the total amount of gold in the root zone during any single cropping
tions was published by scientists from the University of Texas, El cycle (Anderson et al., 2003). This necessitates a system of
Paso (UTEP) (Gardea-Torresdey et al., 1999) using the plant species successive cropping to maximize gold recovery from soil. Therefore,
Medicago sativa L. (alfalfa). Results from this study showed that species that can be cultivated across a range of climatic conditions
M. sativa could accumulate gold to a concentration of 40.9 mg/kg throughout a year could lead to greater efficiencies in phytomining.
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V. Wilson-Corral et al. / Journal of Environmental Management 111 (2012) 249e257 253

Some plant species tested under both laboratory and field condi- 4. Detailed economic consideration of gold phytomining
tions may not be suitable for commercial-scale cultivation, while
some plant species tested under greenhouse conditions may not be A mathematical relationship between the concentration of gold
suitable for field use where extreme drought and temperatures in the soil, and the gold concentration that might be expected in
(both cold and hot) might be expected. Although more than 20 a plant [Y ¼ 51.314 ln (x) þ 62.882], was proposed by Anderson et al.
species have been tested, in this review six species are selected that (2005) based on the combined results from laboratory and green-
could be suitable for commercial-scale field use (Table 3). house studies. In this mathematical model, Y is the gold concen-
tration in the plant, and x is that in the soil. This relationship was
3. Procedure for a gold phytomining operation proposed using cyanide as the agent to induce gold uptake in
B. juncea. The levels of gold concentration in the soil used in this
The potential for gold phytomining has been clearly shown by work are realistic values for the total gold concentration that might
the extensive record of published laboratory and greenhouse be expected in some tailings or waste rock bodies, and yielded gold
studies; and reports of field trials to date suggest the promise of an concentrations in the plant of potential economic significance.
economic return. What are needed are further demonstration trials The first economic assessment of the returns that might be
to better prove the viability of the technology. A gold phytomining realized from gold phytomining was published by scientists from
operation could be done with a well defined general sequence of Massey University (Anderson et al., 1998). In 2003, an economic
steps. Step one: find a site with mining waste rock containing some model for gold phytomining was proposed by Anderson and
small amount of gold. Stage two: plant a fast growing hardy species colleagues. Costs were broken into three categories: a) the costs of
with a large biomass that is tolerant to dry conditions, acid and/or growing the biomass, b) the costs of chemical used to induce
salt that are often present in waste rock from the mine. Step three: uptake of gold and c) the costs of recovery of gold from the biomass.
when the plants near maturity or reach their maximum biomass, The modelled costs showed that the final economic yield (gross
treat the waste rock substrate with a chosen chemical agent. This profit) could be $USD 6437/ha if the gold recovery from plant
introduces a pulse of metal into the soil for plants to accumulate. tissues is based on the use of conventional solvent extraction,
Stage Four: Once the plants show signs of ill health as a result of considered as the most viable processing technology.
metal uptake and any inherent toxicity of the chemicals used to Scientists at the University of Sydney have evaluated the tech-
induce solubility, the plants are harvested. At this point transpira- nical feasibility and the economic viability of nickel and gold phy-
tion will have ceased with no further extraction of metal from the tomining in Australia. In this work possible sites were identified
soil. Stage Five: Incinerate the harvested biomass to produce a bio- and plant species most suited to these regions and methods of
mineral from which metal can be melted and finally recovered recovering the metals from the plants were suggested. The indic-
(Anderson et al., 2000). ative profitability for a Ni phytomining operation in Australia was
A well-planned gold phytomining operation might consider predicted to be 11,500 AU$/ha/harvest, using the hyperaccumulator
factors such as: a) the gold concentration in mineralized soil or waste B. coddii on nickel-rich serpentine soils and with energy generation
mining; b) the way in which gold is present in the substrate from harvested biomass. For gold, a profit of 26,000 AU$/ha/harvest
(geochemistry); c) heavy metal and chemical contaminants in the was predicted using induced accumulation (with thiocyanate) with
substrate that may be toxic for plants; d) plant species that might be a crop of B. juncea coupled with energy generation from the har-
suited to the climatic conditions of the site; e) water availability for vested biomass (Harris et al., 2009).
irrigation of the operation; f) the concentration of plant nutrients
present in substrate as well as the availability of these nutrients to 4.1. Gold phytomining in Mexico
the plant species selected; g) the pH level in the substrate; h) the
chemical agent necessary to form a stable gold complex for uptake; i) Mexico is a country with a long history of open pit and under-
the dose and time for application of the chelating agent; j) a system ground gold mining. Although the main producer of gold in recent
to protect plants against herbivore and/or pathogen attack; k) the years has been China (with an annual production close to 300 tons),
time for plant harvest; l) an adequate system for incineration of gold production in Mexico over the last four years has allowed
biomass; m) an adequate system for ash processing in a laboratory or Mexico to become one of the top 12 gold producing countries
engineering facility (Wilson-Corral et al., 2011). Failure to worldwide. The annual gold production in Mexico in recent years
adequately address any one of these factors may lead to a poor or has reached 75 tons annually. As a result of such historic and
sub-economic return from the gold phytomining operation. modern mining activity, waste volumes in the order of millions of
The economic goal of current research that is being conducted tons have been generated, and this waste material contains
around the world is to induce into plants a gold concentration of a residual gold concentration. This is material that could potentially
100 mg/kg dry matter harvested. If it is also possible to harvest be exploited through the application of gold phytomining making
10 tones of dry matter per hectare, then the final gold yield would Mexico a country with great potential for the application of this
be equivalent to 1 kg of gold per hectare of cultivation. This level of innovative technique. Greenhouse and field research into gold
gold recovery is considered to represent sufficient revenue to cover phytomining that has been conducted in Mexico over the past eight
the associated costs of the operation. years has allowed for the development of calculations regarding the
likely economic viability of gold phytomining based on the current
Table 3 costs of materials and processes that would be required for a large-
Selected plant species for possible gold phytomining use under commercial-scale scale gold phytomining operation (Table 4). This economic model
field conditions. may be applicable to other parts of South America and Africa with
Plant specie Reported by Comments a similar developing economy and cost structure for labour and
Kalanchoe serrata Rodríguez-Lopez et al., 2009 Not tested at field infrastructure.
Brassica juncea Anderson et al., 1998 Tested at field The analysis in Table 4, which is based on previously published
Chilopsis linearis Rodriguez et al., 2006 Not tested at field work (Anderson et al., 2003), shows that a biomass yield of 8.3 t/ha
Brassica campestris Wilson-Corral, 2008 Tested at field reported for a Mexican field trial developed by Wilson-Corral
Helianthus annuus Wilson-Corral, 2008 Tested at field
Bothriochloa macra Piccinin et al., 2007 Not tested at field
(2008), with a gold concentration of 55.6 mg/kg reported for
a field trial by Wilson-Corral et al. (2011) will yield a gold return of
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254 V. Wilson-Corral et al. / Journal of Environmental Management 111 (2012) 249e257

Table 4 conducted in Brazil on waste rock with a total gold grade of only
An economic model for gold phytomining in Mexico based on incineration of har- 0.6 g/t. If processing costs can be lowered or a higher concentration
vested biomass and solvent extraction of the ash. After Anderson et al., 2003.
of gold reached in the plants, this would change the economic
Concept Note Cost US$ parameters.
Agricultural cost (per ha) 1630 Gold phytomining could be an excellent mechanism to develop
Price of chemical ($) $8/kg economic activity in metalliferous or historic mining areas. Such
Application rate @0.25 g Total volume
areas are often associated with poor socio-economic conditions,
chemical/kg soil needed: 180 kg
Cost of chemical 1440 and in Mexico, like many developing countries, people in such
Cost of chemical application 500 regions resort to the cultivation and processing of narcotics due to
Crop monitoring 2200 an absence of economic alternatives for daily subsistence living. In
Cost of producing 5770 such a scenario the agricultural skills and infrastructure exist. Could
biomass/ha
Biomass per ha 8 330a
these people be convinced to turn from the farming of illegal crops
(kg dry weight/year) to farming for gold?
Au concentration in 55.6b In a study initiated in 2006, four gold mines in Sinaloa State,
plant (mg/kg DW) Mexico that had been exploited and abandoned during the 20th
Incineration of DW @ $250/t 2075
century were selected and sampled to determine the residual gold
ASH Conversion DW to ash @ 10% 0.83 t
Operating cost (solvent extraction) $1000/tonne 830 concentration. These mines (Fig. 1) were 1) El Mineral de Nuestra
Capital cost $480/tonne 400 Señora de la Candelaria, 2) La Verde, 3) El Magistral 4) Palmarito
Cost of gold 3305 Mineral. The samples were prepared in the laboratory and analyzed
recovery/ha using atomic absorption spectrometry. The laboratory results show
Gold recovered (asume 100%) 463 g
Market price of gold $US/oz 1623.90
that only the tailings at the El Magistral mine contain significant
Market price of gold $US/g 52.21 quantities of gold, with an average concentration of gold of
Value of gold extracted US$ 24 173 2.35 mg/kg (Wilson-Corral et al., 2006). The volume of tailings in
Total value of crop/ha 24 173 this dump is approximately 100,000 tons, although erosion is
Gross profit/ha (value-cost) $15 098
steadily transporting this material to the coast of the Gulf of Cal-
Notes: These calculations do not consider the possible economic value of electricity ifornia. The levels of gold found in the El Magistral tailings are
generated through biomass incineration. The gold price was quoted on 12-16-2011. similar to that determined by other investigators at gold mines in
a
Wilson-Corral (2008).
b
Wilson-Corral et al. (2011).
Australia and South Africa. The tailings located in El Magistral mine
might be suitable for gold extraction using phytomining and
463 g per hectare. The gold price used for this calculation is the negotiations to access these tailings for a phytomining operation
average world market price for the period December 11e16, 2011 ($ are being actively pursued. The results from this survey highlight
USD 1623.90) (Kitko Inc., 2011). The gross profit in this model is US$ the importance of a well-planned exploration program to locate
14,537/ha. potential sites for operation. If the gold grade in the soil is too low, it
Further analysis of the data in this economic model indicates is unlikely that the operation will yield an economic return.
that a gold recovery of 179 g is sufficient to pay the costs of
production ($ 9636). This would be equivalent to a gold concen- 5. Environmental considerations of gold phytomining
tration of just under 21.56 mg/kg assuming a biomass yield of 8.3 t/
ha (DW) (Wilson-Corral et al., 2011). This concentration is lower The process of recovering gold from any geological media
than that reported by Anderson et al. (2005) for a field trial requires the use of chemicals. This is because of the limited solubility

Fig. 1. The location of four sites evaluated for gold phytomining by Wilson-Corral et al. (2006), in the Northwest portion of Mexico.
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V. Wilson-Corral et al. / Journal of Environmental Management 111 (2012) 249e257 255

of gold under environmental conditions (Anderson, 2005). There- regions of the world (Mendez and Maier, 2007). The locations of these
fore, any technology to recover gold, including phytomining, will areas include northern Mexico, western United States, the Pacific
require the use of chemicals. The environmental challenge in any coast of South America (Chile and Peru), the South of Spain, West
mining operation is to use chemicals in a way such that they pose no India, South Africa and Australia (Tordoff et al., 2000). Associated with
harm to the environment. A gold phytomining operation has simi- these legacy mining areas are large expanses of barren mine tailings;
larities with heap leaching. In both operations cyanide has been The United States alone has about half a million abandoned mines
shown to be the most effective chemical to make gold soluble. with about 45 billion tons of mine waste (USEPA, 2004). Many of these
However, a key difference lies in the amount of cyanide used, and the abandoned mines were gold mines, or mines where base metals were
timeframe over which this cyanide is used. Heap leaching requires targeted, but where gold was also present in the rock. In addition to
the constant use of chemical over a timeframe of years (Bowell et al., gold, the tailings often contain elevated concentrations of other
2009) where the purpose of cyanide use is to leach gold through the contaminants, such as arsenic, mercury and cyanide compounds
rock pile. Phytomining requires the use of cyanide once only, over which can present unwanted environmental risk.
a timeframe of minutes, where the purpose of the chemical is to Despite the high gold price in 2012, conventional mining tech-
promote sufficient solubility for uptake. During phytomining the niques are not generally suitable to exploit the gold left in the tailings,
irrigation of chemical is designed to mitigate the potential for and the material is often left idle. An option to exploit these areas of
leaching of the chemical and gold out of the root zone. tailings is phytomining. Application of this technology could poten-
Concerns have been raised over the persistence of these tially create the added benefits of employment of local communities
chemical amendments in the soil, the collateral effects of the in agricultural production, and the clean up or management of the
amendments on soil microbiota, and the possible mobilization of contaminated sites. Thus, phytomining for gold extraction could be
the contaminants to groundwater (Ebbs et al., 2010). Much considered as an economically viable and environmentally sustain-
discussion has been made on the environmental consequences of able technology that might operate alongside conventional tech-
using the chemical EDTA during phytoextraction (Nowack et al., nology at operating mining sites, or alone at legacy sites.
2006), and we agree with the concerns that have been expressed A case study for the phytomining of historic gold mine wastes in
in literature. However, in gold phytomining the soil being treated India was published during 2005. The subject of this report was the
with chemical (ore or tailings), is often contained within a lined development of phytomining at the Kolar Gold Fields (KGF) in Kar-
tailings facility that is designed to stop leachate from entering nataka, locally known as Bangarapet (city of gold). This area was
groundwater. Alternatively, the soil may be placed on top of a liner once considered to be the premier gold mining area in India and was
following the design of a heap leach pad (a phyto leach pad). The operated by the Bharath Gold Mines Limited (BGML). The mines
liner in these scenarios could mitigate concerns over the movement have a recorded history of nearly 200 years of operation. Studies
of metal complexes into groundwater. There would be a cost have shown that there are about 33 million tons of tailings that have
associated with this additional layer of operation design, but the been accumulated over the years which may be a source of 24 tons of
expected revenue from operating on a soil with in excess of 1 mg/kg gold (Mohan, 2005). According to the author of the Indian report,
could make the economics of such design sustainable. phytomining could prove to be a novel and cost-effective technology
The four main chemicals that have been used in gold phyto- to extract gold from these tailings and also from low-grade ore in the
mining (cyanide, thiocyanate, thiourea and thiosulphate) are all area (grade less than 3 g/t). Phytomining in this area would re-
naturally occurring chemicals that will degrade in the environment vitalize the mining sector, creating employment, revenue, and
(Anderson, 2005). The degradation of cyanide to thiocyanate, and opportunities for new technology development.
the pathways for further biodegradation of thiocyanate are well
studied (Gould et al., 2012). Twenty strains of bacteria have been 7. Recommendations for future work
isolated that can transform thiocyanate to sulphate, ammonia (or
nitrate) and carbon dioxide coming from genera such as Bacillus, Gold phytomining is a technique with great potential for appli-
Acinetobacter, Pseudomonas and Thiobacillus (Boucabeille et al., cation to mineralized soils and gold mining waste around the world.
1994; Hutchinson et al., 1965). The benchmark OECD ‘Closed However the conditions of water scarcity and extreme weather that
Bottle’ biodegradation test shows that ammonium thiocyanate is prevail at many potential phytomining locations will limit the plant
degraded 80% within 28 days (Garttener and van Ginkel, 1999), and species that can be used. Many regions of the world that host historic
in OECD countries thiocyanate is regarded as biodegradable. Ebbs mining wastes currently offer limited choices for economic activity.
et al. (2011) investigated the degradation of chemicals used in The economic estimates presented in Table 4 suggest that phyto-
a phytomining operation and concluded that these chemicals are not mining could provide for new activity that will generate employ-
inherently persistent and that natural attenuation may lead to their ment, revenue and infrastructure in phytomining areas. Research is
rapid degradation in soil. This work was conducted on milled gold ongoing in Mexico and elsewhere under both greenhouse and field
ore, with a very low level of organic carbon (less than 0.15%) which conditions to assess the economic returns that could be generated
was likely to have had low biological activity. The soil or ore in the by the implementation of phytomining. Considering the scientific
root zone of plants being used for phytomining, where the chemicals studies reported in this manuscript, the following objectives are
are placed, will have a higher level of biological activity due to root highlighted for active research: a) standardized systems to evaluate
exudation, and biodegradation may be much greater. The environ- the potential of ore, tailings or waste produced by mining activities
mental concerns regarding the use of chemicals in gold phytomining to gold phytomining; b) standardized tests to identify plant species
are real, and represent the greatest drawback in acceptance of the that can be used in these areas for gold phytomining; c) robust
technology. Further research is needed to establish more clearly the economic assessment to determine the potential profits that could
environmental risks involved in using chemical to promote gold be gained through application of the technology; and d) the
uptake by plants and to design strategies to mitigate these risks. implementation of commercial scale phytomining operations.

6. Global opportunities for gold phytomining Acknowledgements

The safe and effective management of abandoned mine sites is The authors acknowledge the license granted by Facultad de
a global issue which is especially prevalent in many arid and semiarid Ingenieria of the Universidad Autonoma de Sinaloa for the
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256 V. Wilson-Corral et al. / Journal of Environmental Management 111 (2012) 249e257

development of this work. The financial support of the Programa de Haque, N., Peralta-Videa, J.R., Duarte-Gardea, M., Gardea-Torresdey, J.L., 2009.
Differential effect of metals/metalloids on the growth and element uptake of
Fomento a la Investigacion, Desarrollo e Innovacion of Fundacion
mesquite plants obtained from plants grown at a copper mine tailing and
Educacion Superior-Empresa (FESE) from Mexico (project commercial seeds. Bioresour. Technol. 100, 6177e6182.
I þ D þ i  051) is acknowledged. Harris, A.T., Naidoo, K., Nokes, J., Walker, T., Orton, F., 2009. Indicative assessment
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