Content uploaded by Antony Van der Ent
Author content
All content in this area was uploaded by Antony Van der Ent on Mar 24, 2016
Content may be subject to copyright.
REGULAR ARTICLE
Current status and challenges in developing nickel
phytomining: an agronomic perspective
Philip Nti Nkrumah & Alan J. M. Baker & Rufus L. Chaney & Peter D. Erskine &
Guillaume Echevarria & Jean Louis Morel & Antony van der Ent
Received: 5 October 2015 /Accepted: 10 March 2016
#
Springer International Publishing Switzerland 2016
Abstract
Background Nickel (Ni) phytomining operations
cultivate hyperaccumulator plants ( ‘metal crops ’ )
on Ni-rich (ultramafic) soils, followed by harvest-
ing and incineration of the biomass to produce a
high-grade ‘bio-ore’ from which Ni metal or pure
Ni salts are recovered.
Scope This r eview examines th e current st atus,
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, Ca nada, France,
Italy, New Zealand, Spain and USA us ing ultra-
mafic or Ni-contaminated soils with 0.05–1%
total Ni.
Conclusions N, P and K fertilisation significantly in-
creases the biomass of Ni hyperaccumulator plants, and
causes negligible dilution in shoot Ni concentration.
Organic matter additions have pronounced positive ef-
fects on the biomass of Ni hyperaccumulator plants, but
may reduce shoot Ni concentration. Soil pH adjust-
ments, S additions, N fertilisation, and bacterial inocu-
lation generally increase Ni phytoavailability, and con-
sequently, 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
Plant Soil
DOI 10.1007/s11104-016-2859-4
Responsible Editor: Fangjie Zhao.
P. N. Nkrumah (*)
:
A. J. M. Baker
:
P. D. Erskine
:
A. van der Ent
Centre for Mined Land Rehabilitation, Sustainable Minerals
Institute, The University of Queensland, Brisbane, QLD 4072,
Australia
e-mail: p.nkrumah@uq.edu.au
A. J. M. Baker
School of BioSciences, The University of Melbourne, Melbourne,
Australia
R. L. Chaney
USDA-Agricultural Research Service, Crop Systems and Global
Change Laboratory, Beltsville, MD, USA
A. J. M. Baker
:
G. Echevarria
:
J. L. Morel
:
A. van der Ent
Université de Lorraine, Laboratoire Sols et Environnement, UMR
1120, Vandœuvre-lès-Nancy, France
G. Echevarria
:
J. L. Morel
:
A. van der Ent
INRA, Laboratoire Sols et Environnement, UMR 1120,
Vandœuvre-lès-Nancy, France
Introduction
Phytomining operat ions cultivate hyperaccumulator
plants on low-grade ore bodies or superficially
mineralised (ultramafic) soils, followed by harvesting
and a series of post-harvest processing operations to
recover target elements such as nickel (Ni) for profit
(Anderson et al. 1999;Chaneyetal.1998;Hunt2014;
Robinson et al. 1999a; van der Ent et al. 2015). Appro-
priate agronomic practises are a critical pre-requisite in
the development of commercially viable phytomining
technology (Li et al. 2003a; Rascio and Navari-Izzo
2011). Numerous agronomic experiments have been
undertaken since the first phytomining field trial
in 1995 and these studies have substantially ad-
vanced our understanding on phytomining agrono-
my(Banietal.2015a; Chaney et al. 2007b;Li
et al. 2003a; Nicks and Chambers 1995;Robinson
et a l. 1997a). This review examines the current
status of knowledge on N i phytomining agronomy
since the first field trial, and identifies future chal-
lenges and research priorities.
Nickel phytomining operations
Nickel phytomining operations consist of growing se-
lected hyperaccumulator plant species (‘metal crops’)
on Ni-rich (ultramafic) soils, followed by harvesting and
incineration of the biomass to produce a ‘bio-ore’ from
which Ni salts or Ni metal may be recovered (Anderson
et al. 1999; Chaney et al. 1998;Hunt2014;Robinson
et al. 1999b). These operations may be undertaken on:
(i) large ultramafic areas with suitable topography,
where soils are unsuitable for food production; or (ii)
degraded Ni-rich land which includes Ni laterite mine
sites, smelter contaminated areas and ore beneficiation
tailings (van der Ent et al. 2015a). The criteria for
selection of ‘metal crops’ include high biomass yield
combined with high Ni concentrations (>1 %) in the
above-ground biomass (Chaney et al. 2007a). Local
plant species are recommended because of their adapta-
tion to local climatic and edaphic conditions (Baker
1999). Suitable species must be relatively easy to collect
as bulk seed accessions and have high success rates of
germination, establishment and growth (O'Dell and
Claassen 2009). The selected species may be propagated
via direct seeding, transplantation, or by using cuttings
(Brooks et al. 1998;Lietal.2003a). Appropriate soil
and plant management practices, based on insights from
laboratory and field tests, are required to maximise the
yields of the selected ‘metal crop’. Annual Ni yields
ranging from 67.5 to 168 kg ha
-1
have been demonstrat-
ed in phytomining field trials (Bani et al. 2015a;Bani
et al. 2015b;Robinsonetal.1997a;Robinsonetal.
1997b). In principle, Ni phytomining has similar costs
of production as food crops such as corn (Chaney et al.
2007a); and this potentially makes Ni phytomining a
viable business opportunity for ‘metal farmers’ especial-
ly in developing countries such as Indonesia (van der
Ent et al. 2013b).
Economics of Ni phytomining
Here we present the economic potential of Ni
phytomining under two generalised production systems:
an intensive system such as demonstrated in the USA
(e.g. Li et al. 2003a) and an extensive system as dem-
onstrated in Albania (e.g. Bani et al. 2015a). In the
intensive system, the cost of production is high, includ-
ing costs for seed stock, fertilisers, labor and equipment,
whereas the production costs in the extensive system are
relatively low because it mainly involves the use of
fertilisers, herbicides and complementary agricultural
management practices. On the basis of: (i) an average
commercial value of Ni over a period of 5 years (2010–
2015) at the London Metal Exchange of $18 per kg, (ii)
an annual crop Ni yield of 200 kg ha
-1
for an intensive
system and 110 kg ha
-1
for an extensive system, (iii) a
cost of production in 2016 of $1074 ha
-1
yr
-1
and $600
ha
-1
yr
-1
for the intensive and extensive systems, respec-
tively, (iv) an estimated 20 % of Ni value for the cost of
metal r ecove ry, then th e gross values of an annual
phytomining crop per ha for intensive and an extensive
system are $3600 and $1980, respectively, with
corresponding net values of $1806 and $984. It
is henc e clear that Ni ph ytomining is a highly
profitable agricultural technology for the respective
systems. Other potential sources that may further
increase the profitability of Ni phytomining in-
clude: i) recovery of energy of combustion a nd
ii) sale of carbon credits. Although a Ni metal
product is in itself profitable, other higher value
Ni products, including pure Ni salts, may further
increase the profitability of N i phytomini ng, but
the current market for pure Ni sal ts is limited.
Plant Soil
Soil Ni availability for ‘metal crops’
Ultramafic soils develop from the weathering of ultra-
mafic bedrock (Baillie et al. 2000; Brooks 1987;Lietal.
2003a; Tappero et al. 2007) and are characterised by
relatively high concentrations of Mg, Fe, Cr, Co, Mn
and Ni, usually low concentrations of Ca, low to defi-
cient levels of macronutrients (N, P and K), and defi-
cient levels of Mo and B (Baker and Brooks 1989;
Brooks 1987;Jenny1980; Kruckeberg 1985; Proctor
and Woodell 1975). The soil pH of many ultramafic
soils, especially those derived from strongly
serpentinised bedrock, is often relatively high due to
the buffering of Mg-silicates (Alexander 2004;
Chardot et al. 2007). The soil pH can range from neutral
to alkaline with a pH ranging from 6–8 in Mediterranean
climates and in young soils (Cambisols) (Massoura et al.
2006), whereas in tropica l regions with intensiv e
leaching, th e soil pH may be acidic (pH 5. 5) on
Ferralsols (‘laterites’)(vanderEntetal.2013b). Total
Ni concentrations in ultramafic surface soils typically
range from 0.1 to 0.3 % but is often strongly enriched in
the underlying saprolite (0.8–1.5 %), especially under
intense leaching under tropical conditions (Estrade et al.
2015;Golightly1979; Proctor and Nagy 1992;Quantin
et al. 2002). Ultramafic soils that have total Ni concen-
trations greater than 0.1 % with high phytoavailable Ni
pools are potentially suitable for Ni phytomining (van
der Ent et al. 2015b).
Nickel in ultramafic soils is associated with three
main fractions: (i) short-term labile fraction (water-sol-
uble fraction, NH
4
-acetate-exchangeable fraction, ex-
changeable from Mn-oxides and amorphous Fe-oxides);
(ii) long-term labile fraction (bound to crystalline Fe-
oxides and adsorbed to organic matter); and (iii) non-
labile fraction (solid phase residual fraction including
Ni-Al layered double hydroxides, Ni-silicates and Ni
occluded in Fe and Mn oxides), the latter generally
constitutes >50 % of the soil total Ni content (Cheng
et al. 2011;Hseu2006; Quantin et al. 2002; Tessier et al.
1979;Viets1962; Vithanage et al. 2014). Soil Ni avail-
ability is mainly controlled by the mineralogy and Ni-
bearing mineral phases (Becquer et al. 2001;Chardot
et al. 2007; Quantin et al. 2001). In strongly leached
ultramafic soils, such as in Ferralsols, generally the Ni
phytoavailability is low (Bani et al. 2014; Cheng et al.
2011; Das et al. 1999; Echevarria et al. 2006; Massoura
et al. 2006; Raous et al. 2010; Raous et al. 2013).
However, in clay-mineral rich young soils (Cambisols)
and saprolite materials, the Ni phytoavailable fraction is
generally high (Raous et al. 2010). The main factors that
influence Ni phytoavailability include: (i) the original
parent material characteristics and its weathering histo-
ry; (ii) soil composition, such as organic matter and clay
content, thermodynamic conditions including pH and
redox potential, and (iii) rhizosphere effects including
root exudates (Antić-Mladenović et al. 2011; Baker and
Walker 1989; Chardot et al. 2007; Echevarria et al.
1998; Echevarria et al. 2006; Ernst 1996; Massoura
et al. 2006;Massouraetal.2004 ). High nickel
phytoavailability is essential for successful Ni
phytomining (Massoura et al. 2004), as Ni
hyperaccumulator plants take up Ni from the same soil
labile Ni pools as ‘normal’ plants (Echevarria et al.
2006; Shallari et al. 2001). Nickel hyperaccumulator
plants have efficient root absorption mechanisms that
deplete the phytoavailable Ni pools to the extent that the
soil Ni chemical equilibrium is changed (Centofanti
et al. 2012; Deng et al. 2014). As a result, Ni from
non-labile pools replenishes the labile pool over time
to maintain equilibration (Centofanti et al. 2012
), but
th
is is a slow process and depends on the local buffering
system (Massoura et al. 2004).
Several different chemical extraction methods permit
measuring soil Ni labile pools. These are illustrated in
Fig. 1a, b providing data for the DTPA- and NH
4
-
acetate-extractable Ni of 17 ultramafic soils from Ore-
gon and Maryland, USA, which have been acidified by
addition of HNO
3
and leaching of dissolved cations
before fertilisation with N, P, K, CaSO
4
, B and Mo
and cropped with Alyssum species (Chaney et al. un-
published). Figure 1c shows the accumulation of Ni in
shoots of A. murale and A. corsicum on 17 of the same
topsoils after growing Alyssum for 120 days from
transplanting. It is clear that the effect of pH on extract-
ability is not closely related to th e effect of pH on
accumulation of Ni in shoots of Alyssum species and
these usual soil extraction methods are not predictive of
Ni accumulation by Alyssum species. Traditional soil
extraction methods cannot be used for prediction of Ni
accumulation by hyperaccumulator plants, even though
several authors have previously used NH
4
-acetate ex-
traction to predict the depletion of Ni by
phytoextraction, or to compare varied soils as a
phytomining resource (e.g. Robinson et al. 2003;
Robinson et al. 1999b). The Isotopic Exchange Kinetics
(IEK) method allows for the description of the magni-
tude of the Ni labile pool (Echevarria et al. 1998)but
Plant Soil
may not describe the supply of Ni from the soil for
uptake in hyperaccumulator plants. Currently no chem-
ical extraction method can accurately predict Ni avail-
ability, and hence uptake to hyperaccumulator plants.
Nickel hyperaccumulator plants as ‘metal crops’
More than 400 Ni hyperaccumulator plants across over
40 families have been recorded worldwide (Krämer
2010; Pollard 2002; van der Ent et al. 201 3a;
Verbruggen et al. 20 09). The greatest numb ers of
hyperaccumulator plant species are known from Cuba,
New Caledonia and Southeast Asia (Reeves et al. 1999).
However, species of Brassicaceae from the Mediterra-
nean Region are the most widely studied for their Ni
phytomining potential (Bani et al. 2015a;Chaneyetal.
2007a). Most Ni hyperaccumulator plants accumulate
0.1–0.5 % Ni in their biomass, but for phytomining only
so-called ‘hypernickelophores’ (>1 % Ni) are
potentially suitable (Chaney et al. 2007a; b; van der
Entetal.2013a). Table 1 lists the Ni
‘hypernickelophore’ species that have been identified
as having especially high Ni phytomining potential for
use as ‘metal crops’.
Field and laboratory agronomic trials to optimise Ni
phytomining
Nutrient management to increase biomass production
Since the first field trial on a farmed ultramafic soil in
California (USA), using Streptanthus polygaloides
without any fertiliser application (Nicks and Chambers
1995), all other reported trials have incorporated nutri-
ent management. Due to the deficiency of macronutri-
ents in ultramafic soils, there is a strong positive re-
sponse of biomass production to fertilisation in Alyssum
spp. (Bani et al. 2015a). The hyperaccumulator species
Fig. 1 The effect of adjusted pH on (a) 1.0 M NH
4
-acetate-
extractable; (b) DTP A-extractable Ni; and (c) Ni accumulation in
shoots of Alyssum species grown for 120 days in 17 ultramafic
soils from Oregon and Maryland, USA. (d) Effect of pH on Ni
accumulation in shoots of Alyssum species grown for 120 days on
2 soils collected near a Ni refinery at Port Colborne, Ontario
(Quarry muck; Welland loam; organic and mineral soils respec-
tively), and the Brockman cobbly loam. (e) The effect of adjusted
pH (control treatment 2, and acidified treatment 6, which have
been described in Table 3)on1.0MNH
4
-acetate-extractable and,
(f) DTPA-extractable Ni in relation to Ni phytoextraction from 17
ultramafic soils from Oregon and Maryland, USA. Soil pH was
adjusted by addition of HNO
3
, followed by leaching of soluble
ions, and fertilization for the growth of Alyssum species to test the
effect of soil pH on Ni accumulation
Plant Soil
tested on ultramafic soils have proven to react strongly
to increasing levels of soil N, P and K, due to the very
low fertility of their native habitats. Trials using ultra-
mafic soils have shown that fertiliser application en-
hances shoot biomass production of Ni
hyperaccumulator plants and also increases their overall
Ni yield (Table 2). As such, N + P+ K fertilisation tri-
pled the biomass of Berkheya coddii drymatterto9tha
-
1
(Robinson et al. 1999a). There was also a significant
increase in the biomass of Alyssum murale from 3.2 t ha
-
1
in unfertilised plots to 6.3 t ha
-1
in the fertilised
treatment (Bani et al. 2013). Table 3 shows the effect
of P and Ca fertilisers and pH adjustment on Ni and
other element accumulation by A. murale from an Ore-
gon ultramafic soil that had received little fertiliser from
previous land use. Trials on the independent effect of N
application indicate signi ficant increases in Alyssum
biomass with negligible effect on the shoot Ni concen-
tration, subsequently increasing Ni yield (Bennett et al.
1998;Lietal.2003a). A significant effect on biomass
production has been observed for N application
(Bennett et al. 1998;Lietal.2003a), whereas that for
P has been negligible if soils had been fertilized for crop
production previously (Bani 2007;Banietal.2015a).
However, split N application could be employed to
minimise excessive N leaching (Li et al. 2003a). The
Ni content of B. coddii increased two-fold with N addi-
tion (Robinson et al. 1997a), whilst split N application
also increased annual biomass Ni yields (Bani et al.
2015a;Chaneyetal.2007a). Phosphorus has a particu-
larly strong effect on the biomass yield and Ni uptake by
hyperaccumulator species growing on soil not previous-
ly fertilized (Table 3) while previously fertilized soils
show a lesser response to P fertilizer (Bennett et al.
1998; Chaney et al. 2008; Robinson et al. 1997a;
Shallari et al. 2001). Additions of micronutrients have
also been considered during fertilisation trials because
ultramafic soils are usually deficient in B and Mo (Li
et al. 2003b). Some ultramafic soils rich in Fe have
proven deficient in Mo even for native ultramafic veg-
etation (Walker 1948; Walker 2001), while low levels of
B fertilisers may be beneficial in many previously un-
fertilized soils.
The effects of soil pH adjustments on Ni accumulation
Studies indicate that the uptake of Ni from ultramafic
soils by Ni hyperaccumulator plants is strongly influ-
enced by soil pH (Chaney et al. 1998;Chaneyetal.
Tabl e 1 Nickel hyperaccumulator species with over 1 % Ni (‘hypernickelophores’) which have high potential for application as ‘metal crops’ in Ni phytomining operations
Species Potential application area Native distribution Height (m) Cropping system Shoot Ni (%) References
Alyssum spp. Mediterranean and Eurasian Region S & SE Europe, Turkey,
Armenia, Iraq, Syria
0.5–1 Perennial herb 1–2.5 (Brooks 1998)
Leptoplax spp. Mediterranean and Eurasian Region Greece 1–1.5 Perennial herb 1–3.5 (Reeves et al. 1980)
Bornmuellera spp. Mediterranean and Eurasian Region Greece, Albania, Turkey 0.3–0.5 Perennial herb 1–3 (Reeves et al. 1983)
Buxus spp. Tropical Central America Cuba 0.3–12 Ligneous shrub 1–2.5 (Reeves et al. 1996)
Leucocr oton spp. T ropical Central America Cuba 1–3.3 Ligneous shrub 1–2.7 (Reeves et al. 1996)
Phyllanthus spp. T ropical Asia-Pacific Region Southeast Asia and Central
America
1–6 Ligneous shrub 2–6(Bakeretal.1992;vander
Ent et al. 2015b)
Rinor ea bengalensis Tropical Asia-Pacific Region Southeast Asia 5–20 Ligneous shrub 1–2.7 (Brooks and Wither 1977;
Jopony and Tongkul 2011)
Berkheya coddii Southern Africa South Africa, Zimbabwe 1–2 Perennial herb 1.1 (Morrey et al. 1989)
Pearsonia metallifera Southern Africa Zimbabwe 0.35–1.5 Perennial herb 1.4 (W ild 1974)
Plant Soil
Table 2 Outcomes of Ni phytomining agronomic trials showing that N + P + K fertilisation and organic matter additions significantly increase the biomass of Ni hyperaccumulator plants,
with the former causing negligible dilution in shoot Ni concentrations whereas the latter may reduce it. Plant growth regulators increase the biomass of Ni hyperaccumulator plants, but the
effect on Ni yield is not clear. In addition, soil pH adjustment, S addition, N fertilisation, and bacterial inoculation increase uptake and accumulation of Ni shoots in Ni hyperaccumulator
species
Agronomic practices Species Field and/or pot trials Locations Substrates Effects on Ni yield References
N + P + K fertilisation Alyssum bertolonii, Berkheya coddii,
Streptanthus polygaloides Alyssum
murale
Alyssum serpyllifolium ssp. Lusitanicum
A. serpyllifolium ssp. malacitanum,
Noccaea goesingense
Field trial
Pot trials
Tuscany (Italy)
New Zealand
Pogradec (East of Albania)
Spain
Ultramafic soil
3 : 1 mixture of bark: crushed
serpentine rock
Increases Ni yield by increasing
biomass production while
causing negligible dilution in
shoot Ni
(Álvarez-López et al. 2016;
Bani et al. 2015a;Bennett
et al. 1998;Robinsonetal.
1997a; Robinson et al. 1997b)
Sulphur addition Berkheya coddii Pot trials Palmerston North, New Zealand 1:1 ultramafic soil : pumice
soil mixture
Increases Ni yield by increasing
Ni phytoavailability
(Robinson et al. 1999b)
Soil pH adjustment Alyssum murale
Alyssum corsicum
Pot trials Ontario, Canada Ni refinery contaminated soil
(Welland loam and Quarry
muck)
Ultramafic soil
Increases Ni yield while decreasing
Ni extractability
(Kukier et al. 2004;Lietal.2003b)
Different substrates on
the basis of soil Ni
phytoavailability
Leptoplax emarginata
Bornmuellera tymphaea
Thlaspi caerulescens
Alyssum murale
Pot trials France Ultramafic soil agricultural
Calcaric Cambisol acid
agricultural soil
(Haplic Luvisol)
High Ni phytoavailability
increases Ni yield
(Chardot et al. 2005)
Bacterial inoculation Alyssum murale
Alyssum murale + Noccaea tymphaea
Bornmuellera tymphaea + N. tymphaea
Pot trials Oregon, USA
France
Ultramafic soil Increases Ni yield by increasing
Ni uptake and biomass
production
(Abou-Shanab et al. 2006;
Durand et al. 2015)
Plant growth regulators Alyssum corsicum
Alyssum malacitanum
Alyssum murale
Noccaea goesingense
Pot trials Spain Ultramafic soil Positive effects on biomass,
but the effects on Ni yield
is not clear
(Cabello-Conejo et al. 2014)
Weed control Alyssum murale Field trial Pogradec, East of Albania Ultramafic soil Enhances Ni yield by reducing
competition for essential
nutrients and water between
the ‘metal crop’ and weeds
(Banietal.2015a)
Plant density Alys
sum murale Field trial Pojskë and Domosdovë, Albania Ultramafic soil Optimum plant density increases
Ni yield
(Banietal.2015b)
Organic matter additions Alyssum serpyllifolium ssp. lusitanicum
A. serpyllifolium ssp. malacitanum,
Alyssum bertolonii Noccaea goesingense
Pot trial Spain Ultramafic soil Increases Ni yield by significantly
increasing shoot biomass
although shoot Ni concentration
decreases
(Álvarez-López et al. 2016)
Plant Soil
2007b; Chaney et al. 2000; Chardot et al. 2005;
Echevarria et al. 2006). In both strongly acidic and
alkaline soil conditions, Ni u ptake is low in ultra-
mafic soils (Table 4;Fig.1c), but not in smelter
contaminated soils (Fig. 1d) (Chaney et al. 2007a;
Robinson et al. 1999b; Robinson et al. 1997a). The
solubility of Ni, as well as that of other divalent
cations including Zn, Cu, Fe, Co and Mn, generally
increases in acidic soil conditions (Chaney et al.
2007b;Robinsonetal.1996). On the other hand,
at relatively high soil pH, the concentration of Fe-
oxides in ultramafic soils increases the sorption of
Ni (Chaney et al. 2007a) limiting Ni availability
which ultimately leads to a reduced Ni uptake in
hyperaccumulator plants. Smelter contaminated soils
low in Fe-oxides showed an increase in Alyssum
species (A. murale and A. corsicum) shootNicon-
centration across the range from about pH 5 to 7 or
higher, while ultramafic soils revealed a maximum
shootNinearpH6.5(Table4;Fig.1c). Indeed, Ni
uptake decreased at elevated soil pH when both
B. coddii and A. bertolonii were grown in ultramafic
soils ( Robinson et al. 1999b; Robinson et al. 1997b).
Within a pH range of 5–6.5inultramaficsoils,Ni
accumulation by Ni hyperaccumulator plants in-
creases (Chaney et al. 2007b). Because of the dif-
ferent effects of s oil pH on extractability of soil Ni
and uptake by Alyssum species, it is not possible to
accurately predict shoot Ni from extractable Ni data
(Fig 1e , f ). On the other hand, when Ni accumulation
from 17 ultramafic topsoils was regressed (linear or
quadratic) on to the total soil Ni or DTPA-
extractable Ni, the DTPA-extractable Ni had R
2
0.47forlinearandR
2
0.53 for quadratic regressions,
but soil total Ni had R
2
0.65forlinearandR
2
0.72
for quadratic regression of shoot Ni (Fig. 2). Higher
soil Ni will always be a desired property of soils
intended for commerci al phytomining. More r e-
search is required for assessing the ways in which
hyperaccumulator plants access Ni pools in the soil,
Tabl e 3 Effect of amending Brockman cobbly loam ultramafic soil
(fine, magnesic, mesic Vertic Haploxerepts) from a unmanaged
pasture field in Josephine County, Oregon, USA with phosphate
(kg ha
-1
P), pH adjusting, or Ca fertiliser (CaSO
4
H
2
O, t ha
-1
)
treatments on terminal soil pH, mean yield and macronutrient
composition of shoots of two Alyssum species (A. murale and
A. corsicum) grown for 120 days (GM designates geometric mean).
For single variable treatments, all other nutrients were applied as
in treatment 2 (100 kg ha
-1
P; 1.0 t CaSO
4
2H
2
Oha
-1
). Bray-1
extractable P was 0.49, 11.1, 49.9 and 100 mg kg
-1
soil for the 0,
100, 250 and 500 kg ha
-1
P treatments (applied as
Ca(H
2
PO
4
)
2
2H
2
O); all except treatment 1 received 200 kg ha
-1
N
as NH
4
NO
3
. The experimental design, set-up and conditions have
been described by Li et al. (2003b) in which the data from the Port
Colborne soils were reported similar to the serpentine soil
treatments
Treatment Final pH GM-Yield GM-P Mg Ca K
gpot
-1
gkg
-1
1None6.56a
‡
4.1 c 1.04 e 4.06 d 17.5 ab 9.1 d
Phosphate treatments:
3 0 P 5.82 e 1.6 d 0.61 f 6.47 a 17.5 ab 10.0 cd
2 100 P 6.24 b 24.5 a 2.16 cd 6.20 bc 17.1 ab 16.5 b
4 250 P 6.14 bcd 23.2 ab 3.00 b 6.46 bc 19.8 a 19.9 a
5 500 P 6.16 bc 26.5 a 3.59 a 6.40 bc 18.2 ab 19.8 a
pH treatments:
6 Lo pH 5.42 g 27.4 a 2.03 d 4.92 cd 16.7 ab 18.4 ab
7 MLo pH 5.69 f 26.2 a 2.12 d 6.42 bc 18.5 ab 17.0 b
8 MHi pH 5.89 e 27.0 a 2.07 d 5.31 bcd 16.2 ab 18.4 ab
2 As is pH 6.24 b 24.5 a 2.16 cd 6.20 bc 17.1 ab 16.5 b
Ca:Mg treatments:
9 0.0 Ca 6.10 cd 19.3 b 2.43 c 5.66 bc 14.8 b 12.4 c
2 1.0 Ca 6.24 b 24.5 a 2.16 cd 6.20 bc 17.1 ab 16.5 b
10 2.5 Ca 6.04 cd 25.2 a 2.10 d 6.74 b 18.4 ab 17.7 ab
11 5.0 Ca 6.03 d 24.2 a 1.94 d 6.26 bc 16.2 ab 17.2 ab
‡
Means followed by the same letter are not significantly different (P < 0.05 level) according to the Duncan-Waller K-ratio t-test
Plant Soil
and to develop predictive tools for Ni uptake in
hyperaccumulator plants.
The effects of soil Ca amendments on Ni accumulation
Nickel hyperaccumulator plants accumulate normal
foliar levels of Ca from soils with very low concen-
trations of exchangeable Ca and low Ca:Mg ratios,
which is part of the natural adaptation to growing on
ultramafic soils (Brooks 1987; Vlamis and Jenny
1948;Walkeretal.1955). Studies show that there
is a positive c orrelation between the exchangeable
Ca:Mg ratio and the labile Ni pools in ultramafic
soils (Cheng et al. 2011). Calcium supply to high
Mg ultramafic soils will be required to maintain the
annual Ni uptake i n Alyssum species because bio-
mass harvest a nd removal reduces the pool of
phytoavailable Ca in these soils, for example, the
annual removal of 1 t of biomass removes 20 kg of
Ca (Chaney et al. 2007a; Chaney et al. 2008). The
sequestration mechanisms for Ni is distinct from Ca
handling or storage in Ni hyperaccumulator plants
(Broadhurst et al. 2004a); but a positive correlation
exists in the foliar concentrations of Ca and Ni in
some ‘metal crop’ species (van der Ent and Mulligan
2015). Nickel hyperaccumulator species absorb
more Ca relative to Mg, which leads to high Ca:Mg
ratio in the leaf tissues (Bani et al. 2014); this
selective Ca accumulation from soils with very low
Ca:Mg ratios subst antially reduces Mg and Ni tox-
icity (Kruckeberg 1991). Unless Ca is actually defi-
cient, Ca addition has little effect on the Ni concen-
tration in the above-ground biomass and shoot yield
as well a s r oot -to- s hoot translo cat ion of Ni, but may
increase Ni tolerance (Chaney et al. 2008). Calcium
supply in the form of CaCO
3
increases Ni uptake in
hyperaccumulator plants growing on some soils, as a
result of the combined effect of Ca addition and soil
pH (Kukier et al. 2004). However, Ni tolerance in
hyperaccumulator plants may be improved by
CaSO
4
addition independent of soil pH (Chaney
et al. 20 0 8). Moreover, Ca is present in ultramafic
soils at low concentrations; hence Ca depletion
should be avoided in Ni phytomining operations
(Banietal.2015a;Chaneyetal.2007b;Chaney
et al. 2008). Apart from these observations, our
current understanding about the role of C a in
hyperaccumulator plants is limited.
Tabl e 4 Effect on terminal soil pH, mean yield and microelement composition of shoots of Alyssum species grown for 120 days (GM
designates geometric mean) under conditions noted in Table 3
Treatment Final pH GM-Yield GM-Ni GM-Co GM-Mn GM-Zn GM-Fe Cu
gpot
-1
mg kg
-1
1None6.56a
‡
4.1 c 14,740. a 34.3 c 56.5 e 63.4 bc 154. b 3.0 cd
Phosphate treatments:
3 0 P 5.82 e 1.6 d 6250. cd 19.4 ef 62.3 cde 118. a 273. a 2.8 d
2 100 P 6.24 b 24.5 a 6270. cd 19.9 ef 60.9 cde 59.9 bc 112. cd 3.6 bc
4 250 P 6.14 bcd 23.2 ab 6810. bc 22.6 def 65.2 cde 60.2 bc 104. d 4.2 ab
5 500 P 6.16 bc 26.5 a 5690. d 18.1 f 67.2 cde 55.1 cd 92. d 4.0 ab
pH treatments:
6 Lo pH 5.42 g 27.4 a 6150. cd 224. a 462. a 63.1 bc 144. bc 4.4 ab
7 MLo pH 5.69 f 26.2 a 6800. bc 50.4 b 132. b 68.7 b 117. bcd 4.6 a
8 MHi pH 5.89 e 27.0 a 5990. cd 28.8 cd 73.1 cd 58.2 bcd 96. d 3.6 bc
2 As is pH 6.24 b 24.5 a 6270. cd 19.9 ef 60.9 cde 59.9 bc 112. cd 3.6 bc
Ca:Mg treatments:
9 0.0 Ca 6.10 cd 19.3 b 7860. b 21.1 ef 55.6 e 49.4 d 87. d 3.1 cd
2 1.0 Ca 6.24 b 24.5 a 6270. cd 19.9 ef 60.9 cde 59.9 bc 112. cd 3.6 bc
10 2.5 Ca 6.04 cd 25.2 a 6050. cd 18.4 ef 58.2 de 59.6 bc 87. d 3.8 bc
11 5.0 Ca 6.03 d 24.2 a 5630. d 24.4 de 78.5 c 63.3 bc 93. d 3.6 bc
‡
Means followed by the same letter are not significantly different (P < 0.05 level) according to the Duncan-Waller K-ratio t-test.
Plant Soil
Soil S additions and Ni accumulation
Additions of soil S increase Ni yield in B. coddii but
does not have a significant effect on biomass production
(Robinson et al. 1999a). Sulphur additions in the form of
elemental finely ground sulphur lower the soil pH,
thereby increasing the NH
4
-acetate-extractable Ni frac-
tion (Robinson et al. 1999b). However, limited studies
exist on the use of S treatments in Ni phytomining
(Table 2). Sulphur additions to ultramafic soils may
enhance Ni uptake in Ni hyperaccumulator plants by
increasing the extractability of Ni (Chaney et al. 2007a;
Robinson et al. 1999a). Furthermore, S is reported to be
taken up intensively by all Brassicaceae (i.e. Alyssum
spp.) due to their specific metabolic requirements (e.g.
in glucosinolates) (Booth et al. 1995) apart from any
hyperaccumulation traits. Basic studies on Ni tolerance
by Noccaea Ni hyperaccumulators (Noccaea
goesingense, N. oxyceras,andN. rosulare) indicate that
glutathione plays a role in Ni tolerance in these
species (Freeman et al. 2004) and that a S-rich
precursor of glutathione (L-cysteine) may be in-
volved in Ni hyperaccumulation in Noccaea (Na
and Salt 2011). Broadhurst et al. (2004b; 2009)
reported co-localisation of Ni and S in vacuoles
of A. murale and A. corsicum grownonultramafic
soils and in nutrient solutions and suggested SO
4
2-
was needed as a counter-ion to maintain the
charge balance in vacuoles storing high concentra-
tions of Ni. Future studies need to assess the
independent role of S on phytoavailability of Ni
in ultramafic soils, at least for Brassicaceae Ni
hyperaccumulator plants.
Soil organic matter additions and Ni accumulation
The use of organic amendments in the culture of the Ni
hyperaccumulators Al yssum serpyllifolium subsp.
lusitanicum, A. serpyllifolium subsp. malacitanum,
A. bertolonii and N. goesingense demonstrated substan-
tial positive effects on the biomass yield of the plants
(Álvarez-López et al. 2016). The authors found that the
Ni yield was significantly increased due to the stimula-
tion of biomass production while the organic
amendments decreased both soil Ni availability
and shoot Ni concentrations. T he increase in bio-
mass production could be due to improvements in
the soil physical properties such as soil structure,
porosity and water-holding capacity. Organic
amendments could therefore be beneficial in Ni
phytomining operations, but this need to be dem-
onstrated in field trials.
Plant management practices
Nickel phytomining pot and field trials have shown that
plant management practices, beyond fertiliser treatment
and pH adjustment, may enhance Ni yield in Ni
hyperaccumulators via a number of ways: (i) plant den-
sity is important to optimise biomass production per unit
area (Bani et al. 2015b;Lasat2002); (ii) weed control
reduces competition for essential nutrients and water
Fig 2 Relation of Alyssum shoot Ni to (a) DTPA-extractable Ni in 17 ultramafic topsoils; and (b) total soil Ni in 17 ultramafic topsoils
Plant Soil
between the ‘metal crop’ and weeds (Bani et al. 2015a;
Chaney et al. 2007a); (iii) plant growth regulators may
increase biomass production (Cabello-Conejo et al.
2014; Cassina et al. 2011) but can reduce their Ni
yield (Cabello-Conejo et al. 2014), althou gh a
recent study shows positive effects on both bio-
mass yield and Ni accumulation in two
hyperaccumulator species (Durand et al. 2015);
(iv) rhizobacteria may increase the
phytoavailability of soil Ni (Abou-Shanab et a l.
2006; Abou-Shanab et al. 2003) and (v) mycorrhi-
zas may be critical for those hyperaccumulator
species which are strongly associated by mycorrhi-
zas, such as B. coddii (Orł owska e t a l . 2011).
In the only study to date that has used plant
breeding techniques to produce improved ‘metal
crop’ cultivars, Li et al. (2003b) showed a wide
range of shoot Ni concentrations and yield of
diverse A. murale and A. corsicum germplasm
(Fig. 3). Using recurrent selection (required for
self-incompatible species), the authors significantly
increased shoot Ni concentration and yield of Ni
during three cycles of selection. In this study,
plant lines were also selected for reten tion of
leaves during flowering so that the high Ni foliar
biomass was not lost before harvest of the
flowering crop. Collection of diverse germplasm
followed by normal plant breeding techniques to
improve the ‘metal crop’ is clearly a key step in
developing the agronomy of phytomining.
Soil physical properties
Soil physical properties influence Ni yield of
hyperaccumulator plants, for example adequate soil
drainage is an important factor in the agronomy of Ni
phytomining. In a wet climate when soils are poorly
drained, the growth of hyperaccumulator plants is ad-
versely affected and plants may die before normal har-
vest time. Chaney et al. (2007a) have demonstrated in
field trials that such conditions may be corrected by
establishing plants with ridge tilling. Good soil water-
holdin g capacity is also important for ec onomic Ni
phytomining. Soil moisture affects soil Ni extractability,
Ni uptake by hyperaccumulator species, plant growth
and ultimately Ni yield (Angle et al. 2003). A. murale
and B. coddii grow well at high moisture content; Ni
foliar concentration increases with increasing soil mois-
ture content despite a decreasing trend in the soil Ni
extractability (Angle et al. 2003). Addition of compost
generally improves soil structure, porosity and water-
holding capacity, and is likely beneficia l for Ni
phytomining operations.
Potential lifespan of profitable Ni phytomining
operation
There is a time limitation for commercial Ni
phytomining operations due to depleting soil Ni re-
sources. To date, there have been no long-term repeated
hyperaccumulator cropping experiments to ascertain the
number of crop years that are possible for profitable Ni
phytomining. We stress that an attempt to predict the
lifespan via traditional soil extraction modelling may
not be useful. From a five-year field trial, Bani et al.
(20
15a) suggested that economic Ni phytomining oper-
ations could be undertaken for at least several years
(>10 years) before the need for soil modification (for
example, ploughing). Many ultramafic soils contain
>0.1 % total Ni concentrations and Ni yields of 200
and 110 kg ha
-1
could be achieved under intensive and
extensive phytomining production systems, respective-
ly. Considering 1 ha ultramafic substrate with total soil
Ni 2000 μgg
-1
to a depth of 1 m, and assuming a bulk
density of 1.5 kg L
-1
, the resource contains about 30 t of
Ni. Annual Ni yields of 200 and 110 kg ha
-1
on such a
substrate only constitute 1/150 and 1.1/300, respectively
of the total resource. If 10–20 % of the total soil Ni is
available to plants over the time-scale of operations,
profitable Ni phytomining of an intensive and extensive
Fig 3 Variation in shoot Ni concentrations among A. murale
genotypes grown to (mid-flowering) harvest stage on an Oregon
Brockman variant ultramafic soil with 5500 mg kg
-1
Ni (Adapted
with permission from Li et al. 2003b)
Plant Soil
systems could be sustainable over 15–30 years and 27–
54 years, respectively.
The way ahead and challenges
Numerous Ni phytomining pot and field trials have
been undertaken in Albania, Canada, France, Italy,
New Zealand, Spain and USA. The Ni-rich soils
that were used include ultramafic soils and Ni-
contaminated soils. Studies have shown that soils
with>0.1%NiandalargeavailablesoilNipool
are suitable for Ni phytomining. Several Ni
hyperaccumulator plants have been identified as
suitable ‘metal crops’ of which Alyssum spp. and
B. coddii have proven especially successful. Exten-
sive soil and plant managem ent practice s have
been tested for their effects on the Ni yield and
biomass yield of the ‘metal crops’ (Table 2). Since
the first field trial in California on a farmed ultra-
mafic soil (USA), using S. polygaloides without
fertiliser application, all other trials have
incorporated nutrient management. By way of con-
clusion, the agronomic trials undertaken to date
have demonstrated that:
i) N + P + K fertilisation, organic matter additions and
plant growth regulators substantially increase the
biomass yield of ‘metal crops’ without causing di-
lution in shoot Ni yields.
ii) Soil pH adjustments, S additions, N fertilisation,
and bacterial inoculation generally increase Ni
phytoavailability, and consequently, Ni yield in
‘metal crops’.
iii) Traditional chemical soil extractants used to
estimate p hytoavailability of trace elements
are of limited use to predict Ni
phytoavailability to ‘metal crop’ species and
hence Ni uptake.
iv) Calcium soil amendments are necessar y during
phytomining because substantial amounts of Ca
are removed through harvesting of ‘bio-ore’.Fu-
ture studies must provide information on the effect
Tabl e 5 Major challenges and research priorities for developing Ni phytomining around the world
Steps to develop Ni phytomining Challenges Research priorities
Selection of Ni-rich soils Phytoavailability of Ni in soils
Topography/landform of sites
Size of available land area
Lease of land
Identify soils where Ni phytomining
could be profitable.
Develop Ni phytoavailability assays
to predict Ni yield in metal crops.
Negotiate land ownership agreements.
Undertake repeated hyperaccumulator
cropping experiments to assess the
number of crop years possible for
profitable phytomining.
Discovery and selection of ‘metal crops’ Native crops are most suitable requiring
screening to happen at each locality
Hypernickelophore species are very
rare globally
There is the need for increased surveys
especially in tropical regions.
Breeding of improved cultivars to optimise
growth rate and biomass production.
Soil and plant management practices The Ni uptake and biomass
yield of most potential phytomining
‘metal crops’ remain untested at scale
Greenhouse or growth chamber trials to
assess Ni uptake and biomass yield of
such crops.
Test the effect of other plant management
practices such as fertilization, crop
rotation and mixed cropping on Ni yield.
Harvesting techniques Different cropping systems may require
different harvesting technique
Identify appropriate harvesting technique
suitable for each cropping system.
Post-harvest processing of nickel Nickel recovery using smelter is profitable,
while other high value products such as
pure Ni salts currently have limited markets
Explore more methods of producing high
value Ni products with potential markets
in the near future from the biomass ash.
Explore the production of Ni catalysts
from biomass.
Plant Soil
of Ca additions on labile Ni pools and Ni
phytoavailability.
v) Phosphorus fertilisation has a large effect on bio-
mass yield of ‘met al crops’ when cult ivated on
ultramafic soils not previously fertilized with P.
vi) Additions of organic matter enhance soil
physical properties; soil moisture has positive
effects on s oil Ni extractability, Ni u ptake by
hyperaccumulator species, plant growth and
ultimately Ni yi eld.
vii) Repeated hyperaccumulator cropping may not on-
ly deplete soil phytoavailable Ni, but also promote
transfer of non-labile soil Ni to phytoavailable
forms.
Nickel phytomining has high economic potential, but
large-scale demonstrations are needed to provide ‘real-
life’ evidence for commercial operations (van der Ent
et al. 2015a). Table 5 highlights the major challenges
facing the commercial development and implementa-
tion of Ni phytomining, and presents the main research
priorities.
Acknowledgments The authors acknowledge the French Na-
tional Research Agency through the national BInvestissements
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 Re-
search 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 under-
taken 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
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 158:219–224
Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoc-
ulants affecting nickel uptake by Alyssum murale from low,
moderate and high Ni soils.SoilBiolBiochem38:
2882–28 89
Alexander EB (2004) Serpentine soil redness, differences among
peridotite and serpentinite materials, Klamath Mountains,
California. Int Geol Rev 46:754–764
Álvarez-López V, Prieto-Fernández Á, Cabello-Conejo MI, Kidd
PS (2016) Organic amendments for improving biomass pro-
duction and metal yield of Ni-hyperaccumulating plants. Sci
Tot Environ 548–549:370–379
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 67:407–415
Angle JS, Baker AJM, Whiting SN, Chaney RL (2003) Soil
moisture effects on uptake of metals by Thlaspi, Alyssum,
and Berkheya. Plant Soil 256:325–332
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
11:406–415
Baillie IC, Evangelista PM, Inciong NB (2000) Differentiation of
upland soils on the Palawan ophiolitic complex, Philippines.
Catena 39:283–299
Baker AJM (1999) Revegetation of asbestos mine wastes.
Princeton Architectural Press, New York
Baker AJM, Brooks R (1989) Terrestrial higher plants which
hyperaccumulate metallic elements: a review of their distri-
bution, ecology and phytochemistry. Biorecovery 1:81–126
Baker AJM, Walker PL (1989) Physiological responses of plants
to heavy metals and the quantification of tolerance and tox-
icity. Chem Spec Bioavailab 1:7–17
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,
Andover
Bani A (2007) In-situ phytoextraction of Ni by a native population
of Alyssum murale on an ultramafic site (Albania). Plant Soil
293:79–89
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 22:1792–1801
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 186:4431–4442
Bani A, Echevarria G, Sulçe S, Morel JL (2015a) Improving the
agronomy of
Alyssum murale fo
r extensive phytomining: a
five-year field study. Int J Phytoremediat 17:117–127
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 w ith Alyssum murale in
Albania. Aust J Bot 63:72–77
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 103:291–306
Bennett F, Tyler E, Brooks R, Gregg P, Stewart R (1998)
Fertilisation of hyperaccumulators to enhance their potential
for phytoremediation and phytomining. CAB International,
Wallingford
Booth EJ, Batchelor SE, Walker KC (1995) The effect of foliar-
applied sulfur on individual glucosinolates in oilseed rape
seed. Z Pflanz Bodenkunde 158:87–88
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 T echnol 38:5797–5802
Plant Soil
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 265:225–242
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 314:35–48
Brooks RR (1987) Serpentine and its vegetation: a multidisciplin-
ary approach. Dioscorides Press, Oregon, USA
Brooks RR (1998) Plants that hyperaccumulate heavy metals: their
role in phytoremediation, microbiology, archaeology, mineral
exploration, and phytomining. CAB International,
Wallingford
Brooks RR, Wither ED (1977) Nickel accumulation by Rinorea
bengalensis (Wall.) O.K. J Geochem Explor 7:295–300
Brooks R, Chiarucci A, Jaffré T (1998) Revegetation and
stabilisation of mine dumps and other degraded t errain.
CAB International, Wallingford
Cabello-Conejo MI, Prieto-Fernández Á, Kidd PS (2014)
Exogenous treatments with phyt ohormones can improve
growth and nickel yield of hyperaccumulating plants. Sci
Total Environ 494–495:1–8
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 ser-
pentine soil: implications for phytoextractio n. Int J
Phytoremediat 13:90–101
Centofanti T, Siebecker MG, Chaney RL, Davis AP, Sparks DL
(2012) Hyperaccumulation of nickel by Alyssum corsicum is
related to solubilit y of Ni mineral species. Plant Soil
359:71–83
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 1998
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 129–158
Chaney RL, Angle JS, Li YM et al. (2007) Recovering metals
from soil. US Patent 7268273 B2, 11 September 2007
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 36:1429–1433
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 31 1:131–140
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 7:323–335
Chardot V, Echevarria G, Gury M, Massoura S, Morel JL (2007)
Nickel bioavailability in an ultramafic toposequence in the
Vosges Mountains (France). Plant Soil 293:7–21
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
75:659–668
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 53:649–668
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 48:11926–11933
Durand A, Piutti S, Rue M et al. (2015) Improving nickel
phytoextraction by co-cropping hyperaccumulator plants in-
oculated by plant growth promoting rhizobacteria. Plant Soil:
1–14
Echevarria G, Morel JL, Fardeau JC, Leclerc-Cessac E (1998)
Assessment of phytoavailability of nickel in soils. J Environ
Qual 27:1064–1070
Echevarria G, Stamatia Tina M, Thibault S, Becquer T, Schwartz
C, Morel JL (2006) Assessment and control of the bioavail-
ability of nickel in soils. Environ Toxicol Chem 25:643–651
Ernst WHO (1996) Bioavailability of heavy metals and decontam-
ination of soils by plants. Appl Geochem 11:163–167
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 environ-
ments (Albania). Earth Planet Sci Lett 423:24–35
Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W,
Pickering IJ, Salt DE (2004) Increased glutathione biosyn-
thesis plays a role in nickel tolerance in Thlaspi nickel
hyperaccumulators. Plant Cell 16:2176–2191
Golightly J (1979) Nickeliferous laterites: a general description.
In: International Laterite Symposium, New Orleans. Soc
Mining Eng, Am Instit Mining, Metallurgical, Petroleum
Eng 38–56
Hseu Z-Y (2006) Concentration and distribution of chromium and
nickel fractions along a serpentinitic toposequence. Soil Sci
171:341–353
Hunt AJ (2014) Phytoextraction as a tool for green chemistry.
Green Process Synthesis 3:3–22
Jenny H (1980) The soil resource: origin and behaviour
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 dif-
ferent woo ds. Schriftenreihe der SRH Hochschule
Heidelberg, Verlag Berlin GmbH. Logos Verlag Berlin
GmbH, Verlag, pp 129–142
Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev
PlantBiol61:517–534
Kruckeberg AR (1985) California serpentines: Flora, vegetation,
geology, soils, and management problems. vol 78. University
of California Press, USA
Kruckeberg AR (1991) Plant life of western North American
ultramafics. Springer, Netherlands
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 33:2090–2102
Lasat MM (2002) Phytoextraction of toxic metals: a review of
biological mechanisms. J Environ Qual 31:109–120
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 techni-
cal considerations. Plant Soil 249:107–115
Plant Soil
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 T echnol 37:1463–1468
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:
933–938
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 136:28–37
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 55:171–177
Na G, Salt DE (2011) Differential regulation of serine acetyltrans-
ferase is involved in nickel hyperaccumulation in Thlaspi
goesingense. J Biol Chem 286:40423–40432
Nicks L, Chambers M (1995) Farming for metals. Min Environ
Manag 3:15–18
O’Dell RE, Claassen VP (2009) Serpentine revegetation: a review.
Northeast Nat 16:253–271
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 159:3730–3738
Pollard AJ (2002) The genetic basis of metal hyperaccumulation in
plants. Crit Rev Plant Sci 21:539–566
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 469–494
Proctor J, Woodell SR (1975) The ecology of serpentine soils. Adv
Ecol Res 9:255–366
Quantin C, Becquer T, Rouiller JH, Berthelin J (2001) Oxide
weathering and trace metal release by bacterial reduction in
a New Caledonia ferrasol. Biogeochemistry 53:323–340
Quantin C, Becquer T, Rouiller JH, B erthelin J (2002)
Redistribution of metals in a New Caledonia Ferralsol after
microbial weathering. Soil Sci Soc Am J 66:1797–1804
Raous S, Becquer T, Garnier J, Martins ED, Echevarria G,
Sterckeman T (2010) Mobility of metals in nickel mine spoil
materials. Appl Geochem 25:1746–1755
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 bear-
ing and reactive phases. Geoderma 192:111–119
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 180:169–181
Reeves RD, Brooks RR, Press JR (1980) Nickel accumulation by
species of Peltaria Jacq. (Cruciferae). Taxon 29:629–633
Re
eves 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
Reeves RD, Baker AJM, Borhidi A, Berazaín R (1996) Nickel-
accumulating plant s from the ancient serpentine soils of
Cuba. New Phytol 133:217–224
Reeves RD, Baker AJM, Borhidi A, BerazaÍN R (1999) Nickel
hyperaccumulation in the serpentine flora of Cuba. Ann Bot-
London 83:29–38
Robinson BH, Brooks RR, Kirkman JH, Gregg PEH, Gremigni P
(1996) Plant‐available elements in soils and their influence
on the vegetation over ultramafic (Bserpentine^) rocks in
New Zealand. J Roy Soc New Zeal 26:457–468
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 60:115–126
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 59:75–86
Robinson BH, Brooks RR, Clothier BE (1999a) Soil amendments
affecting nickel and cobalt uptake by Berkheya coddii:po-
tential use for phytomining and phytoremediation. Ann Bot-
London 84:689–694
Robinson BH, Brooks RR, Greg g PEH, Kirkman JH (199 9b)
The nickel phytoextraction potenti al of some ultramafic
soils as determined by sequential extraction. Geoderma
87:293–30 4
Robinson B, Fernández J-E, Madejón P, Marañón T, Murillo J,
Green S, Clothier B (2003) Phytoextraction: an assessment of
biogeochemical and economic viabili ty. Plant Soil 249:
117–125
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 97:568–570
Tappero R et al (2007) Hyperaccumulator Alyssum murale relies
on a different metal storage mechanism for cobalt than for
nickel. New Phytol 175:641–654
Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction
procedure for the speciation of particulate trace metals. Anal
Chem 51:844–851
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 41:396–408
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 362:319–334
van der Ent A, Baker AJM, van Balgooy MMJ, Tjoa A (2013b)
Ultramafic nicke l laterite s in Indonesia (Sulawesi,
Halmahera): mining, nickel hyperaccumulators and opportu-
nities for phytomining. J Geochem Explor 128:72–79
va
n der Ent A, Baker AJM, Reeves RD, Chaney RL (2015a)
Agromining: farming for metals in the future? Environ Sci
Technol 49:4773–4780
van der Ent A, Erskine P, Sumail S (2015b) Ecology of nickel
hyperaccumulator plants from ultramafic soils in Sabah
(Malaysia). Chemoecology 25:243–259
Verbruggen N, Hermans C, Schat H (2009) Molecular mecha-
nisms of metal hyperaccumulation in plants. New Phytol
181:759–776
Viets FG (1962) Micronutrient availability, chemistry and avail-
ability of micronutrients in soils. J Agr Food Chem 10:
174–178
Plant Soil
Vithanage M, Rajapaksha AU, Oze C, Rajakaruna N, Dissanayake
CB (2014) Metal release from serpentine soils in Sri Lanka.
Environ Monit Assess 186:3415–3429
Vlamis J, Jenny H (1948) Calcium deficiency in serpentine soils as
revealed by adsorbent technique. Science 107:549
Walker RB (1948) Molybdenum deficiency in serpentine barren
soils. Science 108:473–475
Walker RB (2001) Low molybdenum status of serpentine soils of
western North America. S Afr J Sci 97:565–568
Walker RB, Walker HM, Ashworth PR (1955) Calcium-
magnesium nutrition with special reference to serpentine
soils. Plant Physiol 30:214–221
Wild H (1974) Indigenous plants and chromium in Rhodesia.
Kirkia:233–241
Plant Soil
- A preview of this full-text is provided by Springer Nature.
- Learn more
Preview content only
Content available from Plant and Soil
This content is subject to copyright. Terms and conditions apply.
