Chapter 11

Chromium and Nickel

Cristina Gonnelli and Giancarlo Renella

Abstract Nickel (Ni) and chromium (Cr) are elements naturally present in all rock
types and present in the pedosphere in a range from trace amounts to relatively high
concentrations, as compared to other trace elements. Particularly high Ni and Cr
concentrations are found in serpentine rocks and soils, originating from this rock
type and colonized by a specialized flora that may present some curious species
capable of hyperaccumulating extraordinary high concentrations of Ni in their
above-ground parts. In recent decades, the large release of Cr and Ni by industrial
activities, mainly the manufacture of stainless steel, as well as the use of sewage
sludge as soil amendment in agricultural soils, have caused an impressive increase in
the levels of these two metals in the pedosphere and other environmental matrices.
This has led to increasing environmental concern as, while relatively low concent-
rations of Ni and Cr are essential for plants and other living organisms including
humans, both the elements are toxic for all living organisms if present in excessive
concentrations. This chapter reviews the distribution and the geochemical behaviour
of Ni and Cr, their main dynamics in the soil environment, with regards to the natural
and anthropogenic sources. The relationships of Ni and Cr with the plants, in
particular with some Ni hyperaccumulator species are also discussed.

Keywords Nickel • Chromium • Solubility • Pollution • Ultramafic rocks

• Serpentine • Hyperaccumulators

C. Gonnelli (*)
Department of Evolutionary Biology, University of Florence,
via P.A. Micheli 1, 50121 Florence, Italy
e-mail: [email protected]
G. Renella
Department of Plant, Soil and Environmental Sciences, University of Florence,
P.le delle Cascine 28, 50144 Florence, Italy
e-mail: [email protected]

B.J. Alloway (ed.), Heavy Metals in Soils: Trace Metals and Metalloids in Soils 313
and their Bioavailability, Environmental Pollution 22, DOI 10.1007/978-94-007-4470-7_11,
# Springer Science+Business Media Dordrecht 2013
314 C. Gonnelli and G. Renella

11.1 Introduction

Nickel (Ni) is positioned between cobalt (Co) and copper (Cu) in Group 10 of the
periodic table, the so-called ‘iron–cobalt–nickel’ group of metals. Ten isotopes
of Ni exist in nature and the most abundant stable isotope has atomic number 28,
atomic mass of 58.71 g mol
1, electron configuration [Ar]3d84s2, electronegativity
value of 1.8, density of 8.9 g cm
3 at 20  C, ionic radius of 0.069 nm for Ni(II)+
and 0.06 nm for Ni(III)+, van der Waals radius of 0.124 nm, standard potential

0.25 V and melting and boiling points at 1,453  C and 2,913 C, respectively.
Normally, the Ni oxidation states are 0 or +2, although the +1 and +3 states can
exist under certain conditions. The dominant inorganic species is Ni(II) throughout
the pH and Eh range of most natural waters as it readily loses two electrons and,
in any case, Ni(I) and Ni(III) ions are not stable in aqueous solution [3].
Elemental Ni is a silvery white, hard, malleable metal. Even though the use of
Ni can be traced back to the beginning of the Bronze Age in Mesopotamia in
3500 BC, the identification of Ni as an element is relatively recent. In 1751
the Swedish chemist and metallurgist Axel Fredrik Cronstedt isolated a white
metal from minerals originating from a Cu–Co mine, while he was attempting
to extract Cu. The Ni containing mineral, from which Cronstedt extracted this
metal, was probably now called Niccolite (NiAs). The name nickel was derived by
the German word ‘kupfernicke’ used for Niccolite, meaning ‘Devil’s copper’ or
‘St Nicholas’s (Old Nick’s) copper’. Although the aspect of Niccolite is that of a Cu
mineral, no Cu can be extracted from it and for this reason the Saxon miners had
named the mineral according to the spiteful dwarf ‘Nickel’, who had apparently
turned the Cu in the ore into a non-available form.
Nickel is a transition element with a broad range of applications in modern
industry, being used in everything from coins to automobiles to jewellery. The
largest Ni use by far is the manufacture of stainless steel, an alloy consisting of 8%
Ni, 18% Cr and 74% Fe. Moreover, Ni is an excellent catalyst for many reactions
and so it is used for a large number of industrial and research applications alone or
in combination with other metals.
A primordial, but still conserved today, role of Ni in a different scenario, that is
the biological one, accounts for the industrial chemistry of this metal. In fact,
some industrial processes, such as hydrogenation, desulfurization, and carbonyla-
tion are based on some chemical properties of Ni just as the corresponding
Ni-dependant enzymes, i.e., hydrogenase, carbon monoxide dehydrogenase, and
methyl-coenzyme M reductase [81]. So, Ni is well known as an essential trace
element for plants and cyanobacteria [77, 118]. Furthermore, Ni can be regarded
as a “catalyst of early life” [65]. In fact, the environment in which life began was
most likely electron-rich, and gases, such as H2 and CO2, and metal sulphides were
available [97, 98]. Thus, special catalysts were needed to handle these gases and so
this element was employed for a rich biochemical role by early-life forms [84].
The mineral greigite [Fe5NiS8], an Fe–Ni sulphide, could be regarded as a possible
candidate for an early Ni catalyst as its molecular structure is very similar, for
11 Chromium and Nickel 315

example to that of the thiocubane [4Fe–4S] unit of the ferredoxins [96]. The relative
importance of Ni for primordial forms of life most likely decreased following the
changes in the atmosphere’s chemical composition, particularly the massive photo-
synthetic O2 production [35].
While Ni is essential in certain bacteria, plants, and domestic animals, its
essentiality for humans is still not very clear and the toxicity and carcinogenicity
of high doses of Ni are well documented and depend mainly on its potential to
damage proteins and nucleic acids [58].
Chromium (Cr) was first discovered in a Siberian red lead (Pb) ore in 1798 by the
French chemist Louis Nicholas Vauquelin, who obtained metallic Cr from crocoite
(PbCrO4). Chromium is a steel-grey, lustrous, hard, brittle metal of Group 6 of the
transition series.
The most abundant stable isotope has the following physico-chemical pro-
perties: atomic number of 24, atomic mass of 51.996 g.mol
1, electronic configura-
tion [Ar]3d54s1, electronegativity value of 1.6, density of 7.19 g cm
3 at 20 C, an
ionic radius of 0.061 nm (Cr III) or 0.044 nm (Cr VI), a van der Waals radius of
0.127 nm, standard potential
0.71 V (Cr III/ Cr), and melting and boiling points at
1,907 C and 2,672 C, respectively. The trivalent Cr(III) and the hexavalent Cr(VI)
species are the stable forms of this element, other oxidation states can transiently
exist in living organisms [107].
The origin of the name comes from the Greek word “chroma” meaning color as
many of its compounds are intensely and variously colored. Its use can be dated
back to the third century BC from the analysis of weapons found in some Chinese
burial pits from more than 2,000 years ago. Such archaeological finds showed no
sign of corrosion, because the bronze was coated with Cr.
Chromium is used on a large industrial scale including metallurgy, electroplating,
production of paints and pigments, tannery, wood preservation, chromium chemical
production, and pulp and paper production. Due to its high corrosion resistance and
hardness, chromium is largely used to form stainless steel. This application and
electroplating are currently the highest volume uses of the metal. Wastes from
Cr industries (e.g., sludge, fly ash, slag, etc.) have been employed as a fill material
at numerous locations [100] at which leaching and seepage of Cr(VI) from the soils
into the groundwater poses a considerable health hazard. Water resources can also be
contaminated instead by Cr mainly from the tanning industry [25].
Chromium(III) is essential for humans and Cr deficiency can have detrimental
effects on the metabolism of glucose and lipids (e.g., impaired glucose tolerance,
elevated fasting insulin, elevated cholesterol and triglycerides, and hypoglycaemic
symptoms) [5, 6]. On the other hand, ingestion of large amounts of Cr(III) may
cause health problems such as lung cancer [34, 121]. Cr(VI) is toxic to biota at
concentrations in the order of 10–100 times lower than Cr(III) [59], being a carcino-
gen and may cause death to animals and humans if swallowed in large doses [110].
Human exposure to Cr-containing substances includes ingestion of food and water,
inhalation of airborne particulates, and contact with numerous manufactured items
containing Cr compounds [110]. The limit concentration for drinking water
established by the World Heath Organization is 50 mg L
1 of Cr(VI) . This value
316 C. Gonnelli and G. Renella

can be often exceeded in drinking waters of areas with ophiolitic rocks such as
California, Italy, Mexico and New Caledonia [44].
This chapter describes the main natural and anthropogenic sources of Ni and Cr
in soil, their main chemical forms and reactions, and the interactions of these two
elements with plants, with special emphasis on the so-called nickel-plants, peculiar
plant species adapted to serpentine soils and also used for phytoextraction and
phytoremediation of Ni contaminated soils.

11.2 Origin of Nickel and Chromium in Soils

(Geochemical and Contamination Sources)

The environment reservoir of Ni is the Earth’s Fe–Ni molten core (10% of global Ni),
followed by the Ni dissolved in the sea (ca. 8 109 t). Considerable amounts of Ni
are also present in coal and oil. The abundance of Ni in the Earth’s crust is about
80 mg kg
1 [3] and it is generally distributed with other siderophilic elements, such
as Co and Fe. Nickel is located in the igneous rocks and it can be found associated
with all the geochemical phases of mineralogical cycles, i.e. metamorphic and
sedimentary rocks, soils and sediments [113].
Geochemically, Ni is siderophilic and also has great affinity for sulphur (S); this
leads to the formation of many different sulfides, arsenides as well as antimonides
in nature, such as millerite (NiS), niccolite (NiAs) and breithauptile (NiSb). Nickel
can be also associated with carbonates, phosphates, and silicates.
The ionic properties of Ni allow it to substitute for several alkaline and metallic
cations, such as Mg, Al, Li, Fe(II), Fe(III), Mn(II), Mn(III), Cu, in primary
minerals [75]. Nickel in minerals can substitute for Fe even in pyrite. However,
among the metallic rock forming elements, the Ni isotopic fractionation has
been relatively less studied as compared to other elements.
In igneous rocks, Ni forms mainly octahedral coordination in silicate minerals
such as olivine, hornblende, augite and biotite and magnetite. Such minerals are
poorly stable and undergo rapid weathering. For this reason, Ni in developed
soils is generally associated with clays such as vermiculites and chlorites, saponite
in the serpentine soils, and Fe or Mn (hydro)oxides and concretions, and its con-
centrations decrease with increasing acidity of rocks down to 5–15 mg kg
1 in
granites [57]. Sedimentary rocks contain Ni in the range of 5–90 mg kg
1, with the
highest range being for argillaceous rocks and the lowest for sandstones.
Nickel contents are particularly high in ultramafic rocks (in the order of
2,000 mg kg
1). The two main types of commercially exploitable Ni deposits are
laterites, where the principal ore minerals are nickeliferous limonite (Fe, Ni)O(OH)
and the hydrous Ni silicate garnerite ((Mg,Ni)3(OH)4[Si2O5]) formed during tro-
pical weathering, and sulfide ores, with pyrrhotite, pyrite and chalcopyrite and
especially pentlandite ((Ni, Fe)9S8) as the main Ni-containing minerals.
The total content of parent rocks greatly affects the Ni content in soils, although
the concentration of Ni in surface soils also depends on soil-forming processes
11 Chromium and Nickel 317

and pollution. The Ni content of the pedosphere varies within a broad range, mainly
from 0.2 to 450 mg kg
1, with a calculated world mean of 22 mg kg
1 [104], or a
range of 0.2 and 5,000 mg kg
1 and an average value varying between 20 and
50 mg kg
1, if ultramafic soils are included. However, the concentration ranges
found the in literature depend on the surveyed areas, and also on the soil texture,
with clay soils being richer in Ni than coarser textured soils [69].
In a comprehensive report on the metal background concentrations of European
soils on the basis of the parent material and independently on the soil use, Utermann
et al. [114] reported Ni background values ranging between 3 and 48 mg kg
1, with
the lowest concentrations in soils formed on sandy materials and higher values
in soils originating from volcanic rocks. Nickel concentrations in the soil depend
more on its concentration in the parent material in the less developed soils, whilst its
concentration in the most developed soils depends on the predominant pedogenic
factors [112]. In particular, high intensities of leaching and erosion deplete soils
in Ni. In natural ecosystems, soil enrichment with Ni occurs in alluvial soils or in
soils subjected to the deposition of volcanic ashes. Total Ni concentrations up to
7,000 mg kg
1 can be found in ‘ultramafic; soils originating from igneous ultra-
mafic rock [18]. Clay and loamy soils, e.g. rendzinas, cambisols, and kastanozems,
typically contain total Ni concentrations in the upper range of the mean values quoted
above. Relatively high Ni concentrations have been also found in soils originating
from basic and volcanic rocks, in some organic-rich soils and in soils of arid and
semi-arid regions.
Anthropogenic sources of Ni have resulted in a significant increase in the Ni
content of soils. Main Ni sources are emissions from metal processing oper-
ations and fumes from combustion of coal and oil. The application of sludges and
phosphate fertilisers also may be important sources of Ni in agricultural soils.
Nickel concentrations in the rain have been reported to vary between 0.17 and
17 mg L
1 [10], representing an annual input of 0.002–0.2 mg kg
1 in the topsoil of
areas with 1,000 mm of annual rainfall [113].
Nickel in sewage sludge, where it is present mainly in organic chelated forms, is
readily available to plants and therefore may be highly phytotoxic. Nickel concen-
tration in the solution of heavy metal polluted soils is generally higher and it can
be in the order of mg L
1, depending on the soil total concentration, Ni source and
age of pollution.
Chromium presents an average concentration of 100 mg kg
1 in the Earth’s crust
[41] whereas the concentration range in soil is between 1 and 3,000 mg kg
1 [61].
Chromium is mainly associated with mafic and ultramafic rocks in which it can
reach values of 3,000 mg kg
1. Acid igneous and sedimentary rocks display much
lower Cr contents, commonly ranging from 5 to 120 mg kg
1, with the highest
content in argillaceous sediments.
Chromium (III) has ionic properties close to those of Fe(III)+ and Al(III)+ and
therefore similar geochemical properties. Chromium substitutes for Fe or Al in
chromite (FeCr2O4), the primary geological source for Cr. Chromite is relatively
resistant to weathering, diagenesis, and metamorphic reactions [85]. Under progres-
sive oxidation, the chromate ion (CrO42
) is formed; this form of Cr is more mobile
318 C. Gonnelli and G. Renella

and also readily sorbed by clays and hydrous oxides. Though native Cr deposits are
rare, some metallic Cr has been discovered in the Russian mine Udachnaya Pipe
that is a kimberlite pipe rich in diamonds, where the reducing environment helped
produce both elemental Cr and diamonds.
The main source of Cr in natural soils is the weathering of their parent materials.
Total Cr concentration in soil varies from 0.5 to 250 mg kg
1, with average
values varying between 40 and 70 mg kg
1, depending on the surveyed areas
[33, 93]. The Cr background concentrations of European soils on the basis of the
parent material and independently on the soil use, are in the range 5–68 mg kg
1,
with the lowest concentrations in soils formed on sandy materials and higher
values in soils originating on volcanic rocks [114]. Higher Cr concentrations, up
to 10,000 mg kg
1, are present in soils formed from mafic and volcanic rocks.
In fact, in mafic and ultramafic rocks the Cr concentrations can be higher than
3 g kg
1, typically in the form of chromite, associated with variable amounts of
MgO, Al2O3 and SiO2.
Sandy soils and organic-rich Histosols usually show low Cr concentrations,
containing an average of 47 and 12 mg kg
1, respectively. Total Cr concentrations
are generally positively correlated with the fine granulometric fractions [57].
Chromium total concentrations higher than the local background values originate
from atmospheric fallout and inputs of Cr from Cr-rich sludge and wastes from
industrial activity incorporated into soils.
Chromium in natural soils from the weathering of the parent material is pre-
sent mostly as insoluble Cr(OH)3 or as Cr(III) adsorbed to soil colloids [12]. The
most common Cr form is Cr(OH)2+, bound to clays and humic substances, which
are negatively charged at pH >5.5 [94]. In neutral-alkaline soils, with pH values
>7.0, Cr precipitates as Cr(OH)3, also in combination with alkaline metals and
heavy metals. In strongly acidic soils (e.g. pH <4), Cr(H2O)3+6 is the predominant
Cr form.
The Cr(VI) is typically associated with oxygen as chromate (CrO42
) or dichro-
mate (Cr2O72
) oxyanions. The Cr(III) is less mobile, less toxic and is mainly found
bound to organic matter in soil and aquatic environments [107]. The relation
between Cr(III) and Cr(VI) strongly depends on pH and oxidative conditions, but
in most cases, the Cr(III) is the dominating species [61].
High concentrations of about 2,000 mg kg
1 of both Ni and Cr can be found in the
so-called “serpentine” soils [18]. Serpentinization is a geological low-temperature
metamorphic process, in which low-silica mafic and ultramafic rocks are oxidized
and hydrolyzed into serpentinite. The process can be described by the following
reaction:
 
6½ðMg1:5 Fe0:5 SiO4 Þ þ 7H2 O⇆3 Mg3 Si2 O5 ðOHÞ4 þ Fe3 O4 þ H2 : (11.1)

In this process, Ni may be released from the olivine and co-precipitate with
magnetite. However, when layered silicates or trioctahedral lattices are present
(e.g. saponite, chlorite), Ni may preferentially react with them.
11 Chromium and Nickel 319

The name derives from the Latin word serpens meaning ‘snake’ as
serpentine-rich rock has an olive greenish-grey colour, striped in different shades,
that looks like the skin of a snake [15]. Serpentine soils are derived from the
weathering of ultramafic rocks (“ma” stands for Mg and “f” for ferrum, or Fe),
igneous or metamorphic rocks that comprise at least 70% hydrous Mg Fe phyllo-
silicate, or mafic, minerals with the general formula Mg3Si2O5(OH)4 and including
antigorite and chrysotile [18, 63]. Serpentine rocks originate from metamorphic
alterations of peridotite and pyroxene with water and they may form in the upper
part of the earth mantle or near the earth’s surface during subduction events.
The strong enrichment in siderophile (Fe-loving) elements, such as Cr and Ni,
of ultramafic rocks derives from the fact that the ionic radii of Ni(II)+ and of Cr(III)+
are respectively very close to those of Mg(II)+ and of Fe(III)+, so that ionic
substitution easily takes place into Mg-rich minerals, such as olivine and pyroxene
which are dominant in these rocks [18]. Even though Ni and Cr concentrations
in serpentine soils are often similar, Cr is less soluble than Ni. Although only about
1% of the total Ni in soils is available to plants, this far exceeds the percentage
of available Cr [18].
Apart from their anomalously high concentrations of Ni and Cr, serpentine
soils are characterized also by elevated levels of Fe and Co, they also contain low
Ca: Mg ratios and are often deficient in essential plant nutrients such as N, P and
K [18]. These peculiar chemical properties, along with elevated soil temperatures
and drought, make serpentine soils particularly toxic and unsuitable for most
plant species [17, 31, 63] and for many microorganisms [70]. Ultramafic rocks
and serpentinites of ophiolite complexes constitute about 1% of the terrestrial
landscape [86]. Nevertheless, their study allows a better understanding of Ni and
Cr enrichment of surface water and Ni and Cr transfer to living organisms.

11.3 Chemical Behaviour of Nickel and Chromium in Soils

Nickel has a relatively high affinity for soil organic matter (SOM), with 5% of
total soil Ni being generally associated with this soil component. The main SOM
electron donors are O, and N and S to a lesser extent, with Ca, Mg and Cu as main
competitors. Nickel(II) organic complexes in soil can be formed with low molecu-
lar weight organic ligands (LMWOLs), humic substances or particulate organic
matter. Association of metals, including Ni to humic substances has been mainly
studied by chemical extractions with strongly alkaline solvents (e.g. NaOH) [109].
These data are questionable because Ni solubility strongly depends on pH, with
maximum ionic Ni(H2O)62+ concentration at pH values below 6, whereas at
alkaline pH, Ni may precipitate as hydroxides such as Ni(OH)3
or Ni4(OH)44+,
with very limited solubility. Extractions with strong alkaline solutions followed by
acidification and classical SOM fractionation may also cause artefacts due to
Ni re-distributions among the various SOM fractions. However, currently no
chemical extraction method distinguishes between the forms of metals in soil.
320 C. Gonnelli and G. Renella

Anyway, complexes with LMWOLs are labile, whereas formation of inner sphere
complexes with soil solid phases form less reversible complexes. Among the ide-
ntified organic complexes, Ni has been reported to be present also in porphyrin-like
compounds, likely originating by reactions of Ni with chlorophyll and co-factors of
methanogenic bacteria [29].
Due to its high affinity for organic and inorganic ligands, Ni concentrations in
the soil solution are relatively low. Nickel concentrations in the solution of uncon-
taminated soils are in the range of 0.03–51 mg L
1, whereas in serpentine soils from
various locations the range is in the order of 500–900 mg L
1 [55].
Chromium can exist in oxidation states varying from 0 to VI, but only Cr(III) and
Cr(VI) are sufficiently stable in the soil environment, whilst Cr(IV) and Cr(V) are
generally unstable intermediates in Cr(III) oxidation and Cr(VI) reduction reactions.
Reduction of Cr(VI) depends on its high positive redox potential in both acidic and
alkaline solutions [36] in the presence of electron donors, according to the following
chemical equations:

HCrO
þ

4 þ 7H þ 3e ⇆Cr
3þ
þ 4H2 O and CrO2


4 þ 4H2 O þ 3e ⇆CrðOHÞ3 þ 5OH

(11.2)

However, as the Cr(VI) oxidizing capacity decreases on consumption of H+ and

also on the Cr(OH)3 hydrolysis forming Cr(OH)2+H2O and Cr(OH)2+H2O [78],
its oxidation potential in soil normally deviates from the theoretical Eh/pH
diagrams [61].
Chromium chemical reactivity in soil varies as a function of soil pH , redox
potential, presence of potential electron donors and Cr adsorption on colloids. In
neutral or sub-neutral soil pH and natural Cr concentrations, both Cr(III) and Cr(VI)
may form various hydrolysis and deprotonated products, which may dominate over
the others. In fact, although the Cr(OH)3 is sparingly soluble at pH 5.5–12.0 [90],
the dominant species of Cr(III) should be the product of the hydrolytic product
Cr(OH)2+. However, with increasing Cr(III) concentration, polynuclear hydrolytic
products (e.g., Cr2(OH)42+, Cr3(OH)54+ and Cr4(OH)66+) may also be formed [90].
In acidic (e.g. pH value <5.5) and strongly acidic soils (e.g. pH value <4),
Cr(OH)2+and Cr(H2O)63+, respectively, may be the predominant forms of Cr(III) [94].
The hydrolysis products of the Cr(III) are commonly adsorbed onto clay
minerals, and the strength of this adsorption generally increases upon alkalinization
of the soil pH, also due to the increase of negative charge on the clay surfaces and
deprotonation of organic ligands such as humic substances [53], whereas at neutral-
alkaline pH precipitation of Cr(OH)3.H2O prevents the organic Cr complexation.
Hexavalent Cr in soils may naturally originate from chromite weathering pro-
cesses in the presence of Mn minerals (e.g. birnessite), which may act as potential
oxidants of the released Cr(III) [86]. For Cr(VI), the relative proportions among the
various forms mainly depend on soil pH and total Cr(VI) concentration, being the
HCrO4
and CrO42
the prevailing forms at acidic and alkaline pH values,
respectively. Condensed dichromate (Cr2O72
) may be formed at Cr concentrations
11 Chromium and Nickel 321

higher than 10
2 M [78]. In neutral-alkaline soils, the Cr(VI) may form soluble Na
or K chromates or less soluble Ca and Ba chromates [53].
Hexavalent Cr can be lost from soil by leaching, or be retained in soil by
adsorption onto Fe (hydro)oxides such as goethite, Al oxides and other positively
charged colloids, whereas in acidic soils, chromate is soluble and is more easily
leached [54]. It has been reported that adsorption of Cr(VI) onto Al- and Fe-oxides
causes a kinetic 53Cr/52Cr isotope effect between the soluble and the adsorbed
species [40], and that the microorganism-mediated dissimilatory Cr(VI) reduction
discriminates between 53Cr and 52Cr isotopes, reducing preferentially the 52Cr(VI)
isotope [108].
Chemical oxidation of Cr(III) to Cr(VI) can occur in the presence of Mn oxides
(e.g. buserite), involving Mn(III, IV) (hydr)oxides, reduced to Mn(II) [11].
This reaction depends also on the redox conditions, soil pH and presence of inte-
rmediate reducers [54]. Chemical reduction of Cr(VI) to Cr(III) by magnetite and
Fe(II)-containing minerals has been reported [39]. The Cr(VI) reduction by hema-
tite and biotite over a wide range of pH has been reported by Eary and Rai [38],
in the presence of dissolved Fe(II), not necessarily occurring with solid Fe-bearing
phases. For the above mentioned ionic properties, Cr in soil is strongly retained by
the solid phases, and is generally poorly soluble and not mobile. However, soil
acidification, as well as increase of Cl
or F
concentrations may drastically
increase Cr solubility [102]. Increase of Cr(VI) in soil pore water by phosphate
following P fertilisation of ultramafic soils of New Caledonia, possibly due to a
Cr(VI)-phosphate ligand exchange mechanisms has been reported [13].
Trivalent Cr forms complexes with organic and inorganic ligands containing the
electron donors O, N, S such as ammonia, urea, ethylenediamine, sulphide. How-
ever, partition of organo-Cr(III) complexes between the soil solid and solution
phases depends on the molecular dimensions of the ligand. Relatively small ligands
such as LMWOLs, increase the Cr solubility, whereas relatively large or particulate
organic ligands such as humic substances may immobilize Cr(III). Relatively high
abundance of fulvic acids or LMWOLs such as citrate may promote the Cr
redistribution among goethite, FeO(OH), Al oxides and other soil colloids, through
the formation of soluble Cr(III) complexes and transient oxidation to Cr(VI) [53].
In the soil environment, the Cr(VI) chemical reduction by S2
can be increased
in the presence of clay minerals such as montmorillonite and kaolinite [22]. Lan
et al. [66] reported that in the presence of sulphide, illite promoted the Cr(VI)
reduction, Al oxides had no effect, whereas kaolinite, montmorillonite, amorphous
SiO2 prevented the Cr(VI) reduction. The reason for the kaolinite to prevent the Cr
reduction was the elemental S sorption onto its surface.

11.4 Soil – Plant Relationships

Nickel has been proven to be essential for the fundamental metabolism of soil
bacteria, fungi and algae, although its precise function has not always been
elucidated [71]. A fundamental role of Ni in microbial metabolism may be the
322 C. Gonnelli and G. Renella

function of Ni in the synthesis of urease. Theoretical calculations by Zantua and

Bremner [119] demonstrated that ultra-trace amounts of Ni (in the order of
2 mg kg
1) are sufficient to let the soil urease activity work at the maximum
velocity, therefore Ni total content cannot be considered a limiting factor for soil
urease activity.
Nickel is an essential element for plants, ranging generally from 0.05 to
10 mg kg
1 DM [67, 81]. Nickel deficiency is very rarely found in plants, due
to the very small amount needed for normal metabolism, whereas, with increasing
Ni contamination, excess Ni is more commonly found in these organisms [28].
Symptoms of Ni deficiency, such as leaf tip necroses [42, 43], interveinal necrosis
and patchy necrosis of younger leaves [21] are a result of the lack of urease, which
leads both to urea accumulation to toxic levels and to N deficiency.
With regard to Ni toxicity, threshold concentrations are commonly reported
to be less than 100 mg g
1 [3, 80]. Responses to toxicity differ significantly accord-
ing to plant species, growth stage, cultivation conditions, Ni concentration and
exposure time [57, 67]. In general, critical toxicity levels are >10 mg g
1 DM
in sensitive species and >50 mg g
1 DM in moderately tolerant species (as reviewed
in Chen et al. [28]). Among the toxic effects of high Ni concentrations in plants,
retardation of germination, inhibition of growth, reduction of yield, induction of leaf
chlorosis and wilting, disturbance of photosynthesis, inhibition of CO2 assimilation
and diminution in stomatal conductance [28] are the most frequently reported.
Soil Ni toxicity thresholds to plants are difficult to predict because, as for all
the other elements, only a small fraction of the total metal is bioavailable, and
the phytoavailability of Ni varies greatly depending on soil properties [65].
Soil toxicity threshold concentrations for Ni are commonly reported to be in the
order of 100 mg kg
1 [3, 80]. In view of this, the maximum admissible Ni
concentration established for agricultural soils on the basis of the 86/278/EEC
directive of 30 mg kg
1 for acidic soils and 75 mg kg
1 for neutral alkaline soils
seems to be protective for plants.
Nickel is quickly taken up by plants from soils in the form Ni(H2O)62+ and, until
toxic concentrations in plant tissues are reached, this absorption is positively
correlated with the soil Ni concentrations [57].
The solubility of Ni in the rhizosphere may be affected by the release of
LMWOLs by plant roots [32, 67]. There are several examples showing that the
presence of particular compounds in the substrate can either increase or decrease
Ni uptake, depending on their quantity, quality, and the characteristics of the plant
in question. The presence of organic acids or inorganic ligands in soil solution
results in the formation of Ni complexes with different characteristics that may
inhibit or enhance root uptake [81]. In this context, Molas [74] showed that Ni(II)-
EDTA was less toxic and less accumulated than Ni(II)-citrate or Ni(II)-Glu in
hydroponically-grown cabbage plants.
In contrast to animals, the essentiality of Cr for plant metabolism has not been
definitively proven, although stimulatory effects on plant growth and yield from
the addition of small amounts of Cr have been reported [120]. The positive effect of
Cr(III) on plant growth was suggested to be related to influence on the levels of
11 Chromium and Nickel 323

plant growth hormones, such as cytokinin, interaction with nucleic acids or

chromium-induced increase in polyamine levels [88].
Chromium concentrations in shoots of plants living on non-contaminated soils
are usually in the range of 0.02–0.2 mg kg
1 DM and rarely higher than 5 mg g
1
DM [57, 120]. These very low Cr concentrations are mainly due to the relative
immobility of this element in both soils and plants, probably because of the
predominance of the more insoluble Cr(III)+ form. The low Cr availability, from
0.01 to 4 mg kg
1, also leads to poor correlation between Cr concentrations in plant
tissues and soils [120]. Plant Cr uptake in non-contaminated soils may be partially
explained by natural Cr(III) oxidation in the presence of Mn-rich minerals, particu-
larly due to the peculiar reactivity (e.g. metal concentration, acidification) in the
rhizosphere [79]. Nevertheless, different plant species show differences in their
ability to accumulate Cr in their tissues, being the highest in members of the
cabbage family (Brassicaceae). These plants, known to be sulfurophile, if supplied
with CrO42
, can accumulate large amounts of Cr, possibly due to the chemical
similarity between chromate and sulfate ions [120]. However, Cr concentrations in
edible plant parts are so low that they rarely meet the nutritional requirements for
the human diet.
In most plants the range of critical leaf Cr concentrations is 1–10 mg g
1
DM [120]. Stunted growth, poorly developed root system, curled and discoloured
leaves [89], leaf chlorosis, narrow leaves [52], chlorotic bands [57], yield reduc-
tion [50] are the most common visual symptoms of Cr toxicity in plants. Under field
conditions, Cr is hardly ever toxic to plants, with a few exceptions [3], and
75–100 mg kg
1 is thought to be the total soil Cr concentration above which
plant toxicity can occur [117]. It is noteworthy to underline that while the 86/278/
EEC directive established no maximum limits for total Cr concentrations, individ-
ual member states included maximum values or concentration ranges for total
Cr for agricultural soils in their national statutory values. The range of total Cr
permitted in various EU Countries varied from 30 (Netherlands) to 300 (Portugal)
and 400 (United Kingdom) mg kg
1, although the British limit was not statutory.
The Italian legislation established limits for Cr(VI) at 1 mM. As for the available
form, 1–5 mg kg
1 of available Cr estimated by soil extractions with various
electrolytes, is supposed to be toxic for most plant species [2]. Factors such as
soil properties, plant species, soil characteristics, and Cr species may greatly affect
the level at which Cr is phytotoxic; for example Cr is more toxic to plants growing
on sandy soils compared with peat soils [73].

11.4.1 Serpentine Soils

Both Cr and Ni are present at phytotoxic concentrations in serpentine soils. In fact,

although these soils are characterized not only by a high metal content, but also by
other unfavorable conditions (e.g. low water retention) for plant growth, they are
colonized by plant species adapted to survive in such an extreme environment [17].
324 C. Gonnelli and G. Renella

These species have often become endemic to such substrates and actually the tight
relationship between serpentine soils and its flora was documented as long ago
as the sixteenth century [115]. In fact, serpentine endemic plants can act as flag
species, faithfully indicating the presence of such mineralized substrates and thus
have been used for mineral prospecting already from a long time [19].
The relationship between serpentine soils and plants finds expression not only in
a particular flora composition, but also in the so-called ‘serpentinomorphoses’ [82],
which are unusual and characteristic features showed by serpentine species, such as
xeromorphic foliage, development of a large root system, dwarfism, plagiotropism,
glabrescence or pubescence, glaucescence and erythrism [17, 116], that concur
to plant adaptation to the serpentine factor [63].
Metal tolerant plants are often excluders [7], limiting uptake and root-to-shoot
translocation of trace metals. They are more rarely accumulators, concentrating
metals in their tissues [7]. Serpentine plants evolved a variety of physiological
strategies to accumulate and tolerate a wide range of concentrations of Ni and Cr in
their tissues, from typical values of the non serpentine plants to values far higher
than the typical toxicity thresholds [see for example 60, 87, 106]. Among accu-
mulators, a group of bizarre plants shows extraordinarily high metal concentrations
in their above ground parts, exceeding 2,000 mg g
1 DM [8], and they are the
so-called “hyperaccumulators” [20]. Whatever the reason for the evolution of this
particular phenomenon was, probably a defense strategy against natural enemies
[16], metal hyperaccumulators can surely be one of the most representative emblem
of the indissoluble relationship between serpentine soil and plants because of their
inability to compete in non-serpentine environments.
The term metal “hyperaccumulator” was first coined by Brooks et al. [20] to
define plants living on serpentine soils with Ni concentrations higher than
1,000 mg kg
1 DM in their above-ground parts. The discovery of a large number
of taxa (more than 400) that accumulate Ni in their tissues suggested that the
concentration of this metal can be one of the main factors in determining the flora
and vegetation in many serpentine areas [18, 95, 115], whereas no serpentine plants
are known that hyperaccumulate Cr [18, 30, 95]; which is likely to be due to its low
solubility in these soils.
The first metal hyperaccumulator discovered was the Tuscan nickel plant Alys-
sum bertolonii [72] and the well-known connection between serpentine soil and this
cruciferous plant was already recorded in the sixteenth century by Cesalpino [24].
The soil-plant relationship for A. bertolonii is peculiar as, to our knowledge, so far it
is the only hyperaccumulator plant that is not only a faithful indicator of serpentine
soils for geobotanical prospecting, but also a useful tool for biogeochemistry as it is
representative of the degree of Ni mineralisation of the soil [47].
In metal hyperaccumulator plants the metal is quickly taken up by roots, rapidly
transported into shoots and leaves, and sequestrated in the vacuole [62]. For this
reason, these plants have been used as solar-driven ion-pumps for removing the
metal from polluted soils in phytoextraction experiments [92, 99]. The benefits of
this ‘green’ technology relies on the low costs of growing and harvesting crops, and
low impact compared to the ‘dig and dump’ approach to soil remediation [26].
11 Chromium and Nickel 325

Phytoextraction, also protects polluted soils from erosion [105] and may provide
financial returns thanks to ‘phytomining’ practices [91], which is the recovery of
metals from hyperaccumulator plants. Phytomining of Ni has more potential than
other metals [27] because most of the known hyperaccumulators are able to concen-
trate 1–3% Ni in dry matter, providing 12% to >20% in the ash; these values are an
order of magnitude higher than lateritic ores [37], which, based on the Ni economic
value, may balance the costs of crop production.

11.5 Soils Contaminated with Nickel and Chromium

Nickel contamination of soils is a serious problem as a result of anthropogenic

activities. Generally, localised Ni contamination occurs near to a smelter or
plating works or is associated with mining activity [4]. A significant source of Ni
in soil can be represented also by the use of both P -containing fertilisers and wastes,
such as sewage sludge and pulverised fuel ash. For example, coal can contain up to
70 mg kg
1 Ni which can become highly concentrated in ash residues [4]. Moreover,
the burning of oil and coal account for the widespread atmospheric deposition of
Ni. Worldwide production of Ni has increased from about 20,000 t year
1 in 1930 to
about 800,000 t year
1 in 1985 [103] and to about 1.25 Mt year
1 in 2000 [49].
In both naturally rich and Ni contaminated soils, Massoura et al. [68] through
isotope equilibration experiments reported that the labile fraction ranged between
0.1% and 50% of total soil Ni. The Ni solubility in contaminated soils is likely to
be controlled by the contents of crystalline Fe oxides [46]. A large body of literature
exists on the occurrence and importance of slow reactions between Ni and Fe
oxides (e.g. goethite), due to the slow diffusion towards the interior of the goethite
particles [76], although the formation of Ni-enriched phases cannot be excluded
[101]. In a recent experiment, Fischer et al. [45], reported that slow reactions of
Ni and Cr with goethite have a different dynamic as compared to those of Cd, Co,
Cu, Hg, Mn, Pb, and Zn. This experimental evidence highlights the importance of
the Fe–Al bearing minerals in controlling sorption in Ni–Cr contaminated soils.
As for the bioavailability of Ni in soils polluted by long term sludge application,
Hooda et al. [51] reported that the potential phytoavailable Ni estimated by the
DGT technique in ten consecutive deployments, accounted for 0.7% of total
Ni (56 mg kg
1), which was a higher proportion as compared to Cd, Co, Cu, Pb,
but lower than that of Zn (3%) in the same soil.
Soil Cr contamination arises mainly from the uncontrolled emissions from
metallurgical industries, improper disposal of dye, tannery and textile industrial
wastes, and incorporation of sewage sludge into agricultural soils [83]. Chromium
production worldwide has increased from about 500,000 t year
1 in 1930 [103]
to about 3 Mt year
1 in 1985 and to about 4.5 Mt year
1 in 2000 [49]. Although the
predominant industrially emitted form is Cr(III), significant levels Cr(VI) have been
detected in soils of various world regions (e.g. India, China), especially where no
soil protection legislation is enacted. A particular form of Cr contamination is found
326 C. Gonnelli and G. Renella

at former wood treatment plants where chromated copper arsenate (CCA) has been
used for decades as a wood preservative. In these peculiar industrial sites, the
Cr accumulation into the surface soil may vary depending on the pedo-climatic
conditions. In a sandy acidic CCA polluted soil from northern Sweden, Kumpiene
et al. [64] reported soil Cr total concentrations in the range of 3–4,000 mg kg
1
(plus As and Cu in the order of 5–6,000 and 1,500 mg kg
1, respectively), whereas
in a sandy neutral French soil, Bes and Mench [14] reported no Cr and As accu-
mulation, but only Cu enrichment (1,500–2,600 mg kg
1) of topsoil from a wood
impregnation plant.
The presence of Cr(VI) in soils incorporated with Cr-rich residues may be due
to mineral-mediated (e.g. Mn oxides) chemical oxidation described in the previous
paragraph. Notwithstanding the extensive research on the speciation of Cr in soil,
the complex behaviour of the various Cr species in different forms still results in
a high level of uncertainty on the prediction of Cr mobility and potential risks for
humans and ecosystems posed by Cr contamination of soils.
In volcanic soils affected by repeated Cr-polluted river flooding, Adamo et al. [1]
reported that among the several trace elements (Cu, Ni, Zn) exceeding the local
background values, Cr soil contamination was the only metal clearly related to
flooding events, and was mainly associated with short-range-order aluminosilicates
and organo-mineral complexes, and progressive Cr insolubilization with ageing
was also observed. In this study, soil micromorphology/SEM/WDS analyses also
revealed Cr and Cu enriched silt and clay coatings in surface and subsurface soil
horizons, suggesting a transfer of metal-rich sediments along the soil pore network
with water movement [1].
While Cr forms in contaminated wastewater have been characterized, less
information is available on Cr in the atmosphere. It is known that both Cr(III)
and Cr(VI) are generally present in the atmosphere in which Cr is dissolved in
aerosol or associated with particles of various radii. In the atmospheric aerosol, the
main Cr forms are: Cr(H2O)36+, Cr(OH)2+, HCrO4
and Cr2O72
. Therefore, the
air-borne Cr is expected to be the form of chromium that undergoes to major
transformations in the soil environment.
In an interesting comparative experiment, Jones [56] evaluated the sorption of
Cr with that of other trivalent ions (Y, Rh, La, Pr, Gd) in two acidic soils with
different soil organic matter content. The main result of the study was that more
than 99% of the metals were associated with the exchangeable phase, and that
the main factors controlling the Cr solubility were the Al(III)+ release at acidic
pH (<4.5) and the organic matter dissolution at pH >5.0. In the same study, the
competitive binding of carboxylic acid was also shown [56]; this may have implica-
tions for the assessment of Cr phytoavailability in contaminated soils, due to the
relatively high concentrations of bi- and tri-carboxylic acid in the rhizosphere.
In a survey of six French soils polluted by atmospheric metal inputs, Gandois
et al. [48] reported that among several measured heavy metals Cr was larger than
Ni contamination, whereas Ni was more soluble than Cr using 0.01 M CaCl2 as
extractant, with soil pH and dissolved organic matter having the most significant
effect on Ni and Cr partitioning. This paper also well illustrates the differences in
11 Chromium and Nickel 327

the chemical behaviour of Ni and Cr in terms of solubility in relation to soil pH.

In fact, for acid soils soluble and exchangeable Ni, but not for Cr, was negatively
correlated with soil pH [48].
An important emerging aspect of soil pollution by trace elements is related
to the properties and environmental behaviour of the so called ‘nanoparticles’,
i.e. discrete entities with size in the order of 10
8–10
7 m, today largely used for
production of new materials such as polymers, textiles, fuel and solar energy cell
liners, composite materials, biomarkers, diagnostics and sensors. Nanoparticles
behave differently from elements or polynuclear molecular aggregates, due to
their surface physico-chemical properties and reactivity.
Nickel and Cr nanoparticles are produced in large amounts mainly by
manufacturing and smelting activities. Their inhalation can lead to asthma, pulmo-
nary fibrosis and ultimately lung cancer [23].
Nickel in bimetallic commercially available Ni/Fe nanoparticles, has been dem-
onstrated to have catalytic properties towards LMWOCs and chlorinated organic
xenobiotics, mainly altering the reducing capacity of Fe in aqueous solutions [111].
However, information on the stability of these bimetallic nanoparticles in soil and
the eventual Ni leaching and toxicity is still poor. Among the fundamental pro-
perties, Cr containing nanoparticles of 20–200 nm size may exhibit a net magnetic
moment at the surface [9], which influence their behaviour in the soil environment,
where magnetic minerals are largely present. Even for Cr-containing nanoparticles,
knowledge of their reactivity and stability in the soil environment is still scarce.

11.6 Concluding Comments

Nickel and Cr concentrations in soils and sediments have increased worldwide

during the last century due to mining, smelting and industrial activities. So, a
continuous research effort is needed not only to check the spread of these metals
in the environment, but especially to assess their real environmental mobility.
In this context, the study of the mechanisms responsible for the transfer of Ni and
Cr from environmental matrices to living organisms has fundamental importance in
order to clarify metal exposure routes to all biota and predict the relative
consequences. Furthermore, much research has to be dedicated both to the reduc-
tion of emissions of Ni and Cr into the environment during anthropogenic activities
and to the remediation of metal polluted soils, taking into account of the great
advantage of the availability of the naturally evolved Ni hyperaccumulating plants.

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