The uptake of metals and metalloids by rhodes

Phytoremediation: The Uptake of Metals
and Metalloids by Rhodes Grass Grown
on Metal-Contaminated Soil
Scott M. Keeling
Garry Werren
An experiment was performed to examine the phytoremediation potential of Rhodes grass
(Chloris gayana Kunth cv. ‘Pioneer’). The study sought to determine substrate tolerance, biomass
production, and plant uptake of antimony (Sb), arsenic (As), cadmium (Cd), lead (Pb), silver (Ag),
and zinc (Zn). The plants were grown on weight percent mixtures (5 percent, 15 percent, 25 percent, 35 percent, 50 percent) of a vertisol soil and base-metal mine tailings (7–2,040 µg/g As, 30 µg/g Cd, 30–12,000 µg/g Pb, and 72–4,120 µg/g Zn). The 5 percent and 15 percent amendment of mine tailings increased the biomass production of Rhodes grass (from 0.1 g/plant to ≈3.5
g/plant) without appreciably elevating plant concentrations of the elements. Plant growth decreased by greater than 50 percent for the substrate containing greater than 25 percent tailings
(3,023 µg/g Pb and 1,084 µg/g Zn). Reduced biomass production coincided with maximal Zn uptake by Rhodes grass (249.8 µg/g), indicating tailings induced phytotoxicity. The total concentrations of metals and metalloids tolerated by Rhodes grass in the plant-growth medium indicated
hypertolerance to elevated As, Pb, and Zn concentrations. Partial extraction of the plant-growth
medium determined that plant-available Pb was ten times higher than Ag, As, Cd, and Zn availability. However, Rhodes grass accumulated low levels of Pb, in addition to As and Cd, over the
experimental range, indicating low fodder toxicity risk to browsing livestock. This study concludes
that if there are no invasive species issues associated with conservation land uses, Rhodes grass
is well suited to metalliferous mined land revegetation and would therefore be highly effective for
such programs in subtropical and tropical Australia. © 2005 Wiley Periodicals, Inc.
Pasture-based systems, using exotic tussock-forming grasses such as Buffel grass
(Cenchrus ciliaris), Vetiver grass (Vetiveria zizaniodes), and Rhodes grass (Chloris gayana
Kunth cv. ‘Pioneer’), are commonly used in the revegetation of lands disturbed by
coal mining in Australia (Harwood et al., 1999; Truong, 1998). In most situations,
revegetated sites have been returned to pastoral land use (Grigg et al., 2000) because
Buffel grass and Vetiver grass are comparatively high in nutritional value for stock
(MacKenzie et al., 1982). Vetiver grass has also been used to revegetate metalliferous
mine spoils and exhibits a high tolerance to, and low accumulation potential for,
heavy metals and metalloids contained in these soils (Truong, 2000). Rhodes grass—
another hardy exotic pasture species in tropical and subtropical environments
(Mannetje & Kersten, 1992)—is less palatable to livestock than Vetiver grass
(Graham & Lambert, 1996). The tolerance of Rhodes grass to soils of poor nutrient
status, high salinity, or low pH, in addition to an extensive root system, has been ex© 2005 Wiley Periodicals, Inc.
Published online in Wiley Interscience ( DOI: 10.1002/rem.20042
The Uptake of Metals and Metalloids
This study was conducted
to determine two critical
aspects of the use of
Rhodes grass for metalliferous mined land rehabilitation in northern Australia.
ploited for slope stabilization and erosion control in a number of industrial and urban
environments (Carroll et al., 2000; Grigg et al., 2000; Meecham & Bell, 1977;
Naidu & Harwood, 1997). However, little research to date has been published on its
use in metalliferous land revegetation.
Northern Australia hosts an array of metallic mining operations, exploiting predominantly sulfidic base-metal mineralizations. Many mining tenements are surrounded by pastoral leases and, following mine closure, are required to support some
form of agricultural land-use capability. Excavated nonhazardous mine waste is usually
revegetated directly or after a thin veneer “cap” of plant-growth medium has been laid
down. Hazardous mine wastes are usually isolated from the environment in large tailings dam repositories, which are later capped, at considerable expense, with various
geologic and synthetic materials before being revegetated. The root systems of vegetation established on mine-waste materials will invariably become exposed to the wastes
containing metals and metalloids and may result in accumulation into aboveground tissues and contamination of the food chain (Nicholas & Egan, 1975). This study was
conducted to determine two critical aspects of the use of Rhodes grass for metalliferous mined land rehabilitation in northern Australia. First, the study sought to determine the species’ heavy metal tolerance and biomass production potential when
grown on soils polluted with varying levels of base-metal mine tailings. In addition,
the study determined the natural levels of silver (Ag), arsenic (As), cadmium (Cd),
lead (Pb), antimony (Sb), and zinc (Zn) accumulation by Rhodes grass grown on these
soils to consider potential fodder toxicity risks to livestock grazing.
All growth experiments were conducted in shade houses at James Cook University
(JCU), Cairns, Australia (16° 47' S, 145° 37' E).The climate is humid tropical, with
mean daily temperatures ranging from January maxima (≈31° C) to June minima (≈23°
C). Growth lamps were used to maintain illumination similar to the open-pasture environment at this latitude, and plants were hand-watered daily.
The plant growth medium consisted of an A-horizon soil of low organic matter content and base-metal mine tailings composed of quartzofeldspathic gangue with trace
amounts of sulfides. Both materials were air-dried, crushed, and sieved ( 2 mm), and
mixed at varying weight proportions in a barrel roller (three revolutions per minute) for
30 minutes.The resulting soil-tailings mixtures (i.e., 5T 5 percent tailings mixed
with 95 percent soil) were loaded into 280-mL plant propagation pots watered daily for
four weeks prior to seedling transplantation.
Six-week-old seedlings of Rhodes grass, propagated in a commercially available
germination mix, were transplanted into 280-mL pots containing the various soil-tailings substrates. Four replicates of each substrate were prepared for cultivation. After
two weeks, any plants that did not survive the original transplanting were replaced
with fresh seedlings. Periodically during the course of the trial, exploratory roots
were trimmed from the exterior of the pots to ensure maximum root density, and
pots were rearranged to randomize growth effects inside the shade house. After a further 12 weeks, all aboveground biomass was harvested, double-rinsed with deionized
water, and oven-dried at 70º C before the constant dry weight (DW) was recorded.
Biomass from each sample was hand-ground and accurately weighed into borosilicate
© 2005 Wiley Periodicals, Inc.
ANZECC, 1999
bd below detection.
Note: ANZECC (1999) environmental guidelines are loosely equivalent to the health-based investigation limits outlined in the National Environmental Protection Council Guidelines Schedule B (7a).
Exhibit 1. Soil pH, and total element concentrations (µg/g or wt %) of the soil-tailings mixtures
used in this experiment, including the ANZECC Investigation Limits for metal and metalloid
contaminated industrial and commercial sites (ANZECC, 1999)
test tubes for ashing at 520° C in a muffle furnace. The resulting ash was digested in
near-boiling 2M HCl and diluted with deionized water prior to analysis by Inductively
Coupled Plasma Mass Spectrometry (Cd, Pb, and Zn) and Atomic Absorption
Spectrometry (As) at the Advanced Analytical Centre, JCU.
Post-harvest, the soil contaminated with 25 percent tailings was sampled, ovendried to a constant weight at 65º C, and hand-ground with mortar and pestle to break
up soil peds. A sequential extraction technique was performed on the sample to operationally define the distribution of elements (As, Cd, Pb, and Zn) between various mineral phases. Such analysis allowed an understanding of the plants’ response to the
bioavailable elements.The sequential extraction proceeded via the scheme: deionized
H2O—water-soluble metal fraction (Gatehouse et al., 1977); 1M NH4OAc (pH 7)—
ion-exchangeable fraction (Almås et al., 1999); 1M NH4OAc (pH 5)—carbonate (and
the majority of the sulfate) fraction (Almås et al., 1999); 0.04M NH4HCl in 25 percent
(v/v) HOAc—oxide (and remaining sulfate) fraction (Tessier et al., 1979); and a twostage sulfide extraction using conc. HCl and KCl followed by 4M HNO3 (Tessier et al.,
1979).The combined water-soluble and ion-exchangeable fractions may be considered
an estimate of the plant-available metals and metalloids in the substrate.
Substrate Characterization
X-ray diffraction analysis determined that semiquantitative mineral contents of the substrate materials were:
1. Soil (60 percent quartz, 13 percent albite, 8 percent microcline, 6 percent
kaolin, 6 percent expanding clays, 3 percent muscovite, and 3 percent illite); and
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The Uptake of Metals and Metalloids
Exhibit 2. The natural uptake of Ag, As, Cd, Pb, Sb, and Zn (µg/g) by Rhodes grass (C. gayana)
when grown on mixtures of soil and mine tailings (wt %), including biomass production (g/plant),
substrate pH, ANZECC Investigation Limits for Pb and As, and estimated phytotoxic Zn concentration
2. Tailings (46 percent quartz, 17 percent magnetite, 12 percent fluorite, 5 percent
kaolin, 4 percent anorthite/cordierite/wollastonite, 3 percent pyrrhotite/rutile,
2 percent huntite and only one ore mineral; and 2 percent galena).
The pH range of the soil-tailings mixtures was slightly alkaline (Exhibits 1 and 2),
and the presence of acid-generating sulfides in the tailings caused the pH of the soil to
decline by just 0.6 units over the experimental range.Total element concentrations indicate that soil-tailings mixtures greater or equal to 25 percent tailings exceeded the
Australian and New Zealand Environmental Conservation Council (ANZECC)
Investigations Limits (exposure setting F) for As contamination (500 µg/g), and mixtures containing greater or equal to 15 percent tailings exceeded the Pb Investigation
Limit (1,500 µg/g) (ANZECC, 1999). In addition, substrates containing greater than 15
percent tailings contained total Zn concentrations (greater than 650 µg/g) that may be
considered toxic to common agricultural crops (Glendinning, 2000).
Sequential Extraction of Soil-Tailings Mixtures
A sequential extraction of the 25T soil-tailings mixture (Exhibit 3) indicated that Ag, As,
and Sb were predominantly contained in sulfide (30–45 percent) and silicate (≈50 per56
© 2005 Wiley Periodicals, Inc.
Water Soluble
Ion Exchangeable
bd below detection.
Exhibit 3. The distribution of sequentially extracted elemental fractions (% of total conc.) in the
25T soil-tailings mixture
cent) phases, whereas high proportions of Cd (5–13 percent), Pb (8–45 percent), and Zn
(3–15 percent) were present as ion-exchangeable oxide and carbonate phases. An estimate of the plant availability of the elements (soluble ion-exchangeable fractions) indicated high proportions of total Cd (32.2 percent) and Pb (8.1 percent) were potentially
plant-available. However, absolute metal and metalloid extractability indicates that Pb
availability (243 µg/L) was significantly greater than Ag (0.04 µg/L), As (4.7 µg/L), Cd
(2.4 µg/L), Sb (2.4 µg/L), and Zn (37 µg/L).Therefore, the order of plant availability of
metals and metalloids in the 25T substrate is Pb Zn As Cd Sb Ag.
Plant Growth
Rhodes grass tolerated the range of tailings concentrations investigated, indicating the
species is highly tolerant to elevated concentrations of base metals and metalloids in the
plant-growth medium (Ernst et al., 1992). Rhodes grass appeared visibly healthy on substrates containing less than 25 percent (3,023 µg/g Pb) tailings after three months of plant
growth.The biomass production of Rhodes grass (Exhibit 2) greatly improved (≈300 percent) when cultivated on substrates containing 5–15 percent tailings (629–1,826 µg/g Pb)
compared to unpolluted soil. Exploratory root growth was vigorous from pots containing
less than 35 percent tailings (4,220 µg/g Pb). Plant growth decreased greatly with increased tailings content above this level. A reduction in root mass was also noted for substrates containing greater than or equal to 50 percent tailings (6,015–12,000 µg/g Pb).
Natural Uptake of As, Cd, Pb, and Zn by Rhodes Grass
Rhodes grass accumulated low levels ( 250 µg/g) of all the elements over the range of
tailings concentrations investigated, indicating a high potential to exclude nonessential elements from uptake (Baker, 1981). Maximum accumulations of Ag (0.02 µg/g), As (0.59
µg/g), and Zn (249.8 µg/g) occurred on substrates containing 25 percent tailings,
whereas maximum Cd (8.8 µg/g) and Pb (35.2 µg/g) uptake occurred on substrates
containing 35 percent tailings. Zinc uptake increased tenfold between substrates containing 15 percent tailings (679 µg/g Zn) and those containing 25 percent tailings (1,084
µg/g Zn). Above 25 percent tailings, the Zn concentrations in Rhodes grass decreased
(65–95 percent), with increasing concentrations of tailings in the plant-growth medium.
© 2005 Wiley Periodicals, Inc.
The Uptake of Metals and Metalloids
. . . Fe deficiency caused
by high concentrations of
other tailings constituents,
particularly the alkali elements, may also have
affected plant growth.
Rhodes grass tolerated the entire range of tailings concentrations investigated, although
biomass production was greatly reduced ( 50 percent) above a substrate content of 25
percent tailings. Substrates containing 15 percent tailings exceeded the ANZECC
Investigation Limit for Pb contamination to industrial and commercial sites. Substrates
containing 25 percent tailings exceed the As Investigation Limit (ANZECC, 1999), in
addition to having Zn concentrations that would be toxic to common agricultural crop
species (Glendinning, 2000). As, Pb, and Zn hypertolerance in Rhodes grass was considerably higher than reported for Buffel grass (Harwood et al., 1999) and Vetiver grass
(Truong & Baker, 1998) grown on soils of similar total element concentrations.The
species may also be hypertolerant to the elevated concentrations of magnesium (Mg; 1.1
percent), manganese (Mn; 2.2 percent), and iron (Fe; 17 percent) contained in the mine
tailings (Keeling, unpublished).
Sequential extraction of the 25 percent tailings substrate determined that the plant
availability of Pb (243 µg/L) was significantly higher than that of Zn (37 µg/L), As (4.7
µg/L), Cd/Sb (2.4 µg/L), and Ag (0.04 µg/L), respectively. However, Zn uptake
(249.78 µg/g) exceeded that of Pb (35.2 µg/g) and the other elements, and its accumulation peaked in Rhodes grass for substrates containing 25 percent tailings (1,084 µg/g
Zn).The maximum concentrations of metals and metalloids accumulated by Rhodes grass
were lower than those reported for Buffel grass and Vetiver grass grown on soils of similar total element concentrations (Harwood et al., 1999;Truong, 1999;Ye et al., 2000).
The biomass production of Rhodes grass (Exhibit 2) increased by over 100 percent
when grown on substrates containing mine tailings, compared to unpolluted soil (0.1
g/plant) and undiluted tailings. Plant growth was maximal (3.9 g/plant) from substrates
containing 5 percent tailings (629 µg/g Pb), implying low concentrations of tailings may
act as fertilizers in nutrient-deficient soils. Improved plant growth may therefore have resulted from elevated Zn (72–274 µg/g) concentrations in the substrate, or perhaps from
the addition of calcium (0.4–0.7 percent), sulfur (0.02–0.1 percent), or Mn (0.06–0.2
percent) contained in the mine tailings (Keeling, unpublished). Biomass production decreased with increasing tailings contents ( 5 percent), indicating that heavy metal toxicity had occurred over the experimental range. Maximum Zn accumulation in Rhodes
grass coincided with the maximum rate of decline in biomass production (15–25 percent
tailings), indicating that substrates containing greater than 25 percent tailings (3,023
µg/g Pb, 1,084 µg/g Zn, and 515 µg/g As) were phytotoxic. Reduced plant growth has
therefore most likely resulted from phytotoxic levels of total and plant-available Pb and
Zn in the substrate. In addition, Fe deficiency caused by high concentrations of other tailings constituents, particularly the alkali elements, may also have affected plant growth.
While this study appears to demonstrate the suitability of Rhodes grass for phytoremediation of metalliferous mine tailings in the Australian tropics and subtropics, it
would be remiss of us to fail to cite precautionary principles and to consider potential
drawbacks of using exotic pasture grasses. All of the grass species mentioned here are introduced exotic species. Many species currently used as high-utility plants to increase
stock production in pastoral systems are also high-risk plants for the conservation of native plant communities. Most are inherently aggressive competitors with native species
and can rapidly invade native ecosystems. Buffel grass is a well-recognized weed of the
Burdekin Rangelands in north central Queensland (Grice, 2004), and considerable at© 2005 Wiley Periodicals, Inc.
tention is given to its control in various parts of Australia (Pitts & Albrecht, 2000). It is
also considered a threat to the biological integrity of places such as the Sonoran Desert
of northwestern Mexico and the southwestern United States (James, 1995) and an agent
of change in the grasslands and shrub lands of Texas and Hawaii, along with Australia
(Tix, 2000). On the other hand, recent research (Woolnough & Foley, 2002) has documented its role in providing an important nutritional source for Australia’s most critically endangered mammal, the northern hairy-nosed wombat (Lasiorhinus krefftii).
Rhodes grass is itself also officially documented as an environmental weed (Queensland
Government, 2002).Therefore, it is recommended that caution be applied in selecting
even demonstrably suitable species for phytoremediation when they are not native, particularly in or near areas where conservation of native biodiversity is a desired outcome.
The study has shown Rhodes grass to be an extremely hardy species capable of surviving in undiluted base-metal mine tailings and tailings-polluted soils containing up to
0.2 percent As, 1.2 percent Pb, and 0.4 percent Zn.The addition of tailings to vertisol
soils at low concentrations (≈5 percent wt) appeared to act as a fertilizer by dramatically improving biomass production of the species. Plant growth was significantly reduced on substrates containing greater than 25 percent tailings (515 µg/g As, 3,023
µg/g Pb, and 1,084 µg/g Zn) where Zn accumulation was maximal, indicating phytotoxicity to elevated concentrations of Zn or Pb in the substrate.The accumulation of
As, Cd, Pb, and Sb in Rhodes grass was low over the experimental range, and exclusion
of As, Cd, and Pb appears more efficient in Rhodes grass compared to Vetiver grass
(Truong, 1999).
This study concludes that Rhodes grass is well suited to the revegetation of mine
tailings–polluted soils, and at low levels of contamination, mine tailings may improve the
species’ growth potential. Low levels of metal and metalloid accumulation in aboveground tissues indicate a low fodder toxicity risk and suggest the species may be better
suited to revegetation of metalliferous soils than Vetiver grass and Buffel grass. However,
it is likely that Zn toxicity ( 1,000 µg/g) will significantly affect plant growth. It is
recommended as a species for mine-tailings rehabilitation where there are no major issues for biodiversity conservation and where pastoral land use is a desired outcome.
The authors would like to acknowledge receipt of an Australian Postgraduate Award
Industry scholarship and support by an Australian Research Council Grant
(#LP0219428). BHP Billiton gave approval for publication, and Miss Kate Smith is
thanked for her assistance with cultivation, sampling, and data analysis.
Mr. Keeling would also like to acknowledge his coauthor, Garry Werren, who
passed away suddenly from a heart attack.This article is dedicated in his memory.
Almås, Å., Singh, B. R., & Salbu, B. (1999). Mobility of cadmium-109 and zinc-65 in soil influenced by equilibrium time, temperature, and organic matter. Journal of Environmental Quality, 28, 1742–1750.
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The Uptake of Metals and Metalloids
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Scott M. Keeling is a PhD student in the School of Earth Sciences, James Cook University, Cairns, Australia.
In 2000, Scott graduated with an M.Sc. in soil science from Massey University, New Zealand following his B.Sc.
in earth science in 1993 and postgraduate diploma in quaternary science in 1994. He was awarded the
Student Research Prize from the New Zealand Geological Society in 1993 for his work on volcaniclastics. Scott
has five years’ experience in Australian mineral exploration, mining, and resource modelling complemented by
commercial and research experience in soil physics, photogrammetric analysis, and vegetation mapping.
The late
Garry Werren was an ecologist with the Australian Centre for Tropical Freshwater Research and a
senior lecturer in the School of Tropical Biology at James Cook University, Queensland, Australia. Garry completed an M.Sc. at McGill University, Montreal, Canada, in 1978 following his B.Sc. (Hons) from the University
of Newcastle (1973), New South Wales, Australia, during which he was awarded the university medal for outstanding academic achievement. During his career, Garry held instrumental positions in various environmental
organizations, including Rehabilitation Planning Officer for the North Queensland Joint Board for Wetland
Conservation, a Wet Tropics Planning/Conservation Officer for Queensland Parks and Wildlife Service, and a
Management Policy Officer for the Australian Government’s Department of Arts, Sport, Environment, Tourism
and Territories. Garry also freelanced as an environmental consultant and was a tutor with the Department of
Geography at the University of New South Wales, Sydney, and Monash University, Melbourne.
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