Plant Response to Metal Contamination at an

Oil Shale Tailing Site in Maoming, South China

by Aizhong Ding, Lirong Cheng, Puxin Liu, Philip J. Carpenter, and Yanguo Teng

Abstract
The performance of phytoextraction is evaluated at an oil shale tailing site in South China, where the soil is moderately
contaminated with heavy metals. Soil, wastes, and plant tissues (leaf, stem, and root) were collected from the site and
analyzed for metals. The analytical results show that the plants can extract more metal from the surrounding soil than
their nutrient requirements. Though the plants sampled are not hyperaccumulators for heavy metals as defined by other re-
searchers, they can translocate heavy metals to their leaves and tolerate acidic soil with pH as low as 3.4. This makes them
candidates for contaminated site remediation. Abelmoschus moschatus, Eleocharis quisetina J. et C.Presl, Acacia confusa
wild., and Eucalyptus saligna were particularly effective in translocating heavy metals to easily harvestable leaves and shoots.

Introduction The aim of this study was to assess the performance of

Mining activities generate large amounts of waste rock
and tailings, which are often unstable and become sources
of pollution (Wong 2003). These materials usually yield ex-
tremely harsh surroundings devoid of vegetation, eventually
producing severe soil erosion and off-site pollution. Thus,
the potential health and environmental risks associated
with mining activities are of great concern to populations
living near mines.
The Maoming Petro-Chemical Company (MPCC), one
of the China’s largest petrochemical companies, generated
large amounts of waste during oil shale processing opera-
tions between 1970 and the early 1990s. This waste is the
most conspicuous environmental issue for the company, as
well as for Maoming City (Xia 2004). The dumped solid
waste not only occupies large areas of land but also poses
a great threat to the soil, water, and ecologic system. The
major environmental problems associated with oil shale
tailings are acidification of soil and water, high contents of
heavy metals and sulfate in soil and ground water, and
even the presence of organic contaminants (e.g., polycyclic
aromatic hydrocarbon) in soil (Ding et al. 2003). Although
rehabilitation has been carried out since 1987 to reclaim
the destroyed land, more than 400 ha are still desolate (Xia
2004): no trees and extremely few shrubs exist naturally
on the waste piles (Liu et al. 2002). Therefore, the success-
ful restoration of the mined land, and particularly the
waste piles, is of great importance for pollution control
and remediation.
Copyright ª 2007 The Author(s)
Journal compilation ª 2007 National Ground Water Association.
rehabilitation measures adopted at the Maoming oil shale
tailing site by analyzing plants’ accumulation of metals
from the destroyed land. Plant species that most effectively
accumulate metals are identified and prospects for future
remediation examined.
Traditional methods of soil amelioration are very
costly and usually affect only the upper few meters of soil
(Rio et al. 2002). Recently, phytoremediation, through
which plants transport and concentrate metals from con-
taminated soils into the harvestable parts of roots and
aboveground shoots, has emerged as an alternative to tradi-
tional cleanup methods. Phytoremediation is aesthetically
superior to many other remediation methods, and costs
are often relatively small when compared with more aggres-
sive remediation methods. Phytoremediation also minimizes
the spread of contamination and efficiently captures or de-
grades pollutants in low-permeability, fine-grained sedi-
ments that are difficult targets for other remediation
methods. Developing nations, in particular, have shown
great interest in phytoremediation as a cost-effective means
of dealing with major soil and ground water contamination
problems (e.g., Leigh et al. 2001; Prasad 2001).
The efficiency of phytoremediation, however, is depen-
dent on the ability of plants to grow, develop their root
systems, and take up and accumulate the available metals
in their upper parts. The depth of soil to be restored is also
limited by the reach of plant roots. Even under optimum
conditions, remediation could be very slow and requires
several centuries to decontaminate deep, heavily contami-
nated areas (Vangronsveld and Cunningham 1988).
General reviews of phytoremediation, applied to
a wide variety of organic and inorganic pollutants, may be

Ground Water Monitoring & Remediation 27, no. 3/ Summer 2007/pages 111–117 111
found in Salt et al. (1995), Schnoor et al. (1995), Chaney Published applications of phytoextraction to oil shale
et al. (1997), Raskin et al. (1997), Salt et al. (1998), wastes are rare and focus on removal of organic contami-
Meagher (2000), Raskin and Ensley (2000), McCutcheon nants. Existing studies appear to have limited applicability
and Schnoor (2003), and Pilon-Smits (2005). Most of these to the Maoming site. Lohmus et al. (2006) described the
studies subdivide phytoremediation into phytodegradation, use of black alder trees for remediation of oil shale mine
rhizofiltration, phytostabilization, phytovolatization, and wastes, and Truu et al. (2003) described field experiments
phytoextraction. in which soil amendments enhanced phytoremediation of
Phytodegradation uses plants and microorganisms to phenol compounds at an oil shale mining site in the Baltic
break down organic pollutants in situ. This may be accom- region of northern Europe.
plished directly through enzymes secreted by roots
(Fletcher and Hedge 1995) or indirectly by increasing dis-
solved organic carbon (OC) levels in underlying aquifers, Site Description
which enhances other in situ degradation processes (e.g., The study area, a retorted oil shale disposal site, is
Eberts et al. 2005). Rhizofiltration uses plant roots to ad- located on the outskirts of the city of Maoming, approxi-
sorb pollutants, typically within wetlands (e.g., Dushenkov mately 300 km south of Guangzhou, Guangdong Province,
and Kapulnik 2000; Leeson et al. 2001). In phytostabiliza- China (Figure 1). The climate of the area is of marine mon-
tion, contaminant migration is stopped or retarded, typi- soon, with an average annual rainfall of 1.7 m, temperature
cally using root secretions to chemically transform mobile 23
C, and relative humidity 81%. Approximately 80% of
contaminants into inert forms (e.g., Salt et al. 1995). Plant- the yearly rainfall occurs between the months of April
ing trees to increase transpiration and slow or change the and September. The Xiaodong and Baisha rivers, flowing
direction of ground water flow is also a form of phytostabi- from north to south, are the major overland streams passing
lization (Halford 1998). Phytovolatization releases vola- through the area, collecting surface and subsurface runoff.
tile organic compounds through transpiration. Chlorinated They each have an average flow rate of 26 m3/s (Chen and
solvents such as trichloroethylene, chlorobenzene, vinyl Deng 1988).
chloride, and tetrachloroethene have been treated this way. The North Landfill shown in Figure 1 had been used
Hybrid poplar trees are commonly used for this purpose for oil shale waste disposal from the 1970s until the early
since they have a high root density, extending to depths of 1990s when the mining activity ceased (Li and Tang 1992).
3 m or more (e.g., Burken 2001). It is estimated that about 50 million tons of waste have been
Phytoextraction, which is the focus of this study, uses placed at the site, consisting of processed oil shale and
plants to transport and concentrate contaminants from the
soil into the harvestable parts of roots and aboveground
shoots or leaves. Phytoextraction has successfully removed
both organic and inorganic contaminants from soils. For
example, Leavitt (2001) described phytoextraction of pesti-
cides by poplar trees. Polychlorinated biphenyl compounds
have also been taken up by tree species such as black
locust, birch, willow, and alder (Leigh et al. 2001).
Phytoextraction of heavy metals from mining and re-
fining wastes is the specific objective at the Maoming North
Landfill. Some plants, such as sunflowers, mustard plants,
natural prairie species, and even some types of ferns, accu-
mulate heavy metals to levels that are 100 times those
found in normal plants (Baker and Brooks 1989; Salt et al.
1998; Gambale et al. 2001; Sahli 2001; Bennett et al. 2003;
Peer et al. 2005). Such species are called hyperaccumu-
lators. Some metals, such as nickel, may be harvested from
plant shoots, concentrated, and resold (Chaney et al. 2000).
In other cases, harvestable portions of hyperaccumulator
plants must be disposed of in landfills or incinerated.
Hyperaccumulator species are, in general, relatively slow
growing. However, Chaney et al. (2000), LeDuc et al. (2004),
and Pilon-Smits and Freeman (2006) described experi-
ments under way to transfer metal hyperaccumulation genes
to faster-growing, higher biomass plants. Heavy metal
uptake by other plants may also be enhanced when various
chelating agents (organic acids) are added to the soil Figure 1. Sketch map of study area near Maoming (from
(Salt et al. 1998; Gambale et al. 2001). A long-range goal Ding et al. 2003) showing sampling sites (n), villages (s), and
at the Maoming site is to identify suitable hyperaccu- monitoring well (n). Maoming is approximately 10 km south-
east of the map shown. Inset shows the location of Maoming in
mulator species that could be efficiently used to remove southern China.
heavy metals from the mine tailings and surrounding areas.

112 A. Ding et al./ Ground Water Monitoring & Remediation 27, no. 3: 111–117
various chemical wastes generated from the MPCC. The
landfill is about 6 to 7 km long, 2 to 3 km wide, and 15 to
20 m high, with a flat top that is partially covered by vege-
tation (e.g., the tree Eucalyptus and grass Eragrostis spp.).
This vegetation was planted soon after mining ceased to
reduce erosion and to limit water infiltration across the site;
these plants were not chosen for the purpose of phytoex-
traction. The landfill overlies an unconfined aquifer about
36 m thick, with the water table 6 to 8 m below the ground
surface. This aquifer consists of coarse sand and clay,
incorporating Paleocene coal beds and thin red sands. A
deeper alluvial sand and pebble aquifer is confined. The
coarse particle size of the tailings and cracks from uneven
settlement of the waste have permitted rain water to infil-
trate the waste pile. Previous investigations revealed that
landfill leachate (mostly from surface seeps) had substan-
tially damaged rice fields near the landfills (Li and Tang
1992), and the ground water contamination poses a serious
health risk (Ding et al. 2003). The depth and extent of
ground water contamination from the landfill are unknown.
Sampling and Analysis
Soil and plant samples were collected along the top
and sides of the landfill, as well as along the base. Leach-
ate was collected from a monitoring well located at the
top of landfill in May 2004 (Figure 1).
The soil samples were collected from 5 to 30 cm depth,
using a spade to dig out the sample. Extracted soil at the
same site was mixed in a polyethylene bag, air dried, and
then sieved to 2 mm before analysis. The remaining rocks
and other debris were discarded. The sieved soil samples
were then measured for pH (1:2 soil:water suspension) and
metals (digested with HNO3 1 HClO4). Plant tissue sam-
ples were dried in a forced air oven at 80
C, ground to
about 2 mm, and digested using HNO3 1 HClO4. The pH
was measured with a M90 pH meter (Corning Inc., Lowell,
Massachusetts). Trace elements in soil and plant tissue
were analyzed using an inductively coupled plasma-mass
spectrometer (an ICP-MS Model ELAN 6000; Perkin-
Elmer, Walthan, Massachusetts). Organic C (inorganic C
removed with HCl), H, and N were measured using an
element analysis system (LSA Systems GmbH, Aachen,
Germany). The total organic carbon (TOC) in leachate was
analyzed using a Phoenix 8000 TOC analyzer (Teledyne-
Tekmar, Mason, Ohio). Total and available concentrations
of the elements in soil are given on a dry weight basis.
Results
Soil Characteristics
Table 1 lists pH values and trace metal concentrations
for the oil shale tailings, soil, and leachate from the North
Landfill. The oil shale waste characteristics represent an
average of all the samples, whereas a range in sample val-
ues is shown for the other constituents. Oil shale tailings
are mainly composed of oil-refining wastes containing
higher concentrations of OC, Cr, Ni, and Cu than the
underlying soil. Although the soil organic matter content is
not low, the nutrients N, P, and K required for plant growth
are scarce (Xia 2004). Furthermore, the pH of soil is as low
as 3.4, which is generally hostile to the growth of plants.
The soil at the tailing site also contains higher concen-
trations of Pb, Ni, Cu, and Zn than the background values
in local soil (shown in the right column of Table 1).
Plant Description
The five plant species collected from the study area
were the predominant vegetation in the area during the col-
lecting time. Plant species belonging to the Eucalyptus
family were the most frequently found at the tailings site.
The average metal concentration in the different plant tis-
sues is shown in Table 2, with the maximum concentration
of each heavy metal shown in bold. The lower concentra-
tion of Cr, Ni, and Cu found in the plant tissues suggests
that these metals are bound by organic matter and iron
oxides within the oil shale wastes. Khan (2001) reported
a similar effect.

Table 1
Characteristics of Oil Shale Waste and Soil and Total Metal Content

Background
Characteristics Oil Shale Waste Soil Leachate (Chen and Deng 1988)

pH 3.8 3.4–5.0 3.1 4.7

N (%) 0.32 0.07–0.09 NA NA
H (%) 0.78 0.97–1.67 NA NA
OC (%) 2.71 0.60–0.76 0.94–1.601 NA
Pb (mg/kg) 25.1 41.0–91.9 15.4 6 0.72 24.0
Cr (mg/kg) 54.0 1.2–4.4 18.8 6 1.32 34.1
Ni (mg/kg) 39.0 8.7–21.3 18.1 6 0.42 9.0
Cu (mg/kg) 42.9 4.7–36.4 30.6 6 0.22 10.5
Zn (mg/kg) 30.0 27.9–85.0 396.1 6 37.62 22.0

Note: NA ¼ not available.

1
mg/L.
2
lg/L.

A. Ding et al./ Ground Water Monitoring & Remediation 27, no. 3: 111–117 113
 Table 2
Metal Contents in Plant Species and Tissues

Metal (mg/kg)
Species Pb Cr Ni Cu Zn

Eu. saligna
Leaf 2.11 0.51 7.91 6.55 20.98
Stem 0.80 0.17 2.33 4.85 18.72
Root 1.74 0.11 1.75 4.61 14.71
Ac. confusa wild.
Leaf 1.33 0.11 4.63 7.30 23.31
Stem 0.82 0.07 1.61 8.20 21.18
Root 0.65 0.11 3.80 3.14 9.26
Ab. moschatus
Leaf 7.29 0.27 3.29 6.77 18.21
Stem 4.07 0.21 5.58 10.40 25.69
Root 3.41 0.20 5.58 13.43 18.20
El quisetina J.et C.Presl Figure 3. Percent metal distribution in soil and plant tissues.
Leaf 2.50 0.11 1.15 4.71 18.74
Stem 0.28 0.06 0.52 1.28 4.43
Root 4.80 0.25 2.28 3.05 8.63 (48.04 mg/kg) in the root of Lepironia articulate (Ret2)
Lepironia articulate (Ret2) Domin L.C.Rich Domin L.C.Rich.
Leaf 0.04 0.08 0.72 1.16 8.21 In terms of phytoextraction, the rank for Pb concentra-
Root 1.02 0.19 2.59 2.06 48.04 tions in leaves is Ab. moschatus > Eleocharis quisetina J. et
C. Presl > Eu. saligna > Acacia confusa wild. > Lepironia
articulate (Ret2) Domin L.C.Rich; for Cr Eu. saligna >
Ab. moschatus > El quisetina J.et C.Presl ’ Ac. confusa
Metal Distribution wild. > Lepironia articulate (Ret2) Domin L.C.Rich; for
Figure 2 compares metal concentration in plant tissues Ni Eu. saligna > Ac. confusa wild. > Ab. moschatus > El
to that in soil. In Figures 3 and 4, metal concentration in quisetina J.et C.Presl > Lepironia articulate (Ret2) Domin
the plant tissues or soils was normalized to the total con- L.C.Rich; for Cu Ac. confusa wild. ’ Eu. saligna ’ Ab. mo-
centration in the plant tissues and soils. From the compari- schatus > El quisetina J.et C.Presl > Lepironia articulate
son of metal distribution in plant tissues and soil shown in (Ret2) Domin L.C.Rich; and for Zn Ac. confusa wild. > Eu.
Figures 2 and 3, it appears that the soil retains most of the saligna > El quisetina J.et C.Presl ’ Ab. moschatus > Lepir-
metal and only small amounts are extracted by the plants. onia articulate (Ret2) Domin L.C.Rich.
Metals absorbed by the plants, however, appear to be easily
translocated from the root to stems and leaves, as shown in
Figure 4. Discussion
The highest Pb concentration (7.29 mg/kg) was found
Although none of the species listed previously are
in Abelmoschus moschatus leaves, the highest Cr con-
hyperaccumulators, the relatively high concentration of
centration (0.51 mg/kg) in Eucalyptus saligna leaves, the
highest Ni concentration (7.91 mg/kg) also in Eu. saligna
leaves, the highest Cu concentration (13.43 mg/kg) in the
Ab. moschatus root, and the highest Zn concentration

100
Pb
80 Cr
Metal in plant tissues

Ni
1:1
Cu
60
(mg/kg)

Zn

40

20

0
0 20 40 60 80 100
Metal in soil (mg/kg)

Figure 2. Metal distribution in plant tissues and soil. Figure 4. Percent metal distribution in plant tissues.

114 A. Ding et al./ Ground Water Monitoring & Remediation 27, no. 3: 111–117
metals found in the plant leaves indicates that these plants
could be potential species for phytoremediation of the site.
The metal concentration measured for the soil was the
total concentration in the soil, not the bioavailable fraction.
If only the bioavailable fraction were used, the accumulat-
ing capacity of the plants would appear much greater.
Also, a greater shoot biomass and higher growth rate can
more than compensate for a lower shoot metal concentra-
tion—thus, plant species suitable for phytoremediation
may not be limited to hyperaccumulators (Kumar et al.
1995; Salt et al. 1995; Ebbs and Kochian 1997).
Triangular plotting of normalized metal concentrations
in plant tissues and soil (Figures 3 and 4) is a helpful tool
for plant selection in phytoremediation of heavy metal-
contaminated soils. Plant species with a high percentage of
metals in block B represent optimum plants for phyto-
extraction since metals would accumulate in plant leaves
and be easily harvestable, whereas blocks A, C, and D are
not ideal for plant selection because more metals are accu-
mulating in soil and nonharvestable tissues of plants. This
explanation is based on the metal distribution in only soil
and plant tissues; how the bulk biomass affects phyto-
remediation is not discussed in this work.
These plants grow on the Maoming tailings site, in
some places abundantly, even though the soil lacks nu-
trients like N (0.08%) and has a low pH value. As stated
by Wong (2003), selection of appropriate plant species for
such soil conditions would be very important to ensure
a self-sustainable vegetation cover. Adjustment of pH in
the soil and leachate treatment would enhance plant growth
and site remediation.
Conclusions
Analysis of soil, waste, and plant tissues from the
Maoming oil shale North Landfill and surrounding areas
suggests the following:
1. This disposal site is moderately contaminated with
heavy metals. An acidic soil (pH as low as 3.4) and
acidic landfill leachate (pH 3.1) enhance the mobility of
heavy metals.
2. The plants growing at this site can tolerate low pH
conditions, can accumulate heavy metals from the sur-
rounding soil beyond their nutrient requirements, and
can translocate these heavy metals to their leaves, which
makes them potential cleaners for this site.
3. The most effective accumulators for heavy metals
include Ab. moschatus, El. quisetina J.et C.Presl, Ac.
confusa wild., and Eu. saligna. These species also trans-
locate the metals to easily harvestable leaves and stems.
Results of this work could be applied to phytoremedia-
tion of other mining sites. First, the analysis of phyto-
extraction potential is facilitated by the use of triangular
diagrams, as shown in Figures 3 and 4. This type of plot
quickly identifies species with the highest phytoextraction
potential. Second, the species listed previously in (3) could
be used for phytoremediation of oil shale wastes in similar
climatic regimes, both in China and other countries, for
example, Brazil.
A. Ding et al./ Ground Water Monitoring & Remediation 27, no. 3: 111–117
Future work should concentrate on identifying species
that might grow on the still-barren portions of the North
Landfill, on whether hyperaccumulators could be grown
at the sites, and on how the results of this study could be
used to provide quantitative estimates of phytoextraction
potential for the species listed in (3) previously. Specifi-
cally, for a certain plant density and harvestable biomass
production rate, can realistic estimates be made for the
rate of metal extraction rate from the soil? Such informa-
tion could then be used to estimate the time required for
phytoremediation of the upper several meters of the North
Landfill.
Acknowledgments
This work was supported by the Natural Science
Foundation of Guangdong Province (990537), Science &
Technology Project of Guangdong Province (2KM06506S),
and the National Natural Science Foundation of China
(40202026). We thank Dr. J. Liu for identification of the
plants used in this study. We also thank the reviewers and
editors for valuable comments and suggestions that greatly
improved this manuscript.
Editor’s Note: The use of brand names in peer-reviewed
papers is for identification purposes only and does not con-
stitute endorsement by the authors, their employers, or the
National Ground Water Association.
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Biographical Sketches
Aizhong Ding, corresponding author, is professor of environ-
mental engineering in the College of Water Sciences, Beijing Nor-
mal University, No. 19 Xinwai St., Beijing 100875, China; phone
86-10-5880-9289; ading@bnu.edu.cn. His current research inter-
ests include geochemical modeling of soil and groundwater con-
tamination in landfills, PAH transport and transformation
processes, and bioremediation of contaminated land and ground-
water. He obtained his Ph.D. from the Chinese Academy of Geo-
sciences, Beijing, his Mphil. from Sheffield University, UK, and his
M.S. from Changchun College of Geology, Changchun, China..
Lirong Cheng, recently completed her Ph.D. from Sheffield
University, UK, in reactive transport modeling in groundwater.
She can be reached at Beijing Water International Ltd., 15th
Floor, Zhongtian Plaza 5 Xiaoying Road, Chaoyang District,
Beijing 100101, China; phone/fax: 86-10-8233-6364; cheng.bwi@
gmail.com.
Puxin Liu, is a hydrogeologist at the Maoming Environmen-
tal Protection Bureau, Maoming 525000, No. 2 Jiankang Road,
Maoming, 525000, Guangdong Province, China; phone/fax:
86-668-2701189; email: 303liu@mail.china.com. His duties
include groundwater sampling, monitoring and ensuring pro-
A. Ding et al./ Ground Water Monitoring & Remediation 27, no. 3: 111–117
tection of public water supplies in the Maoming area of Guang-
dong Province.
Philip J. Carpenter, is a currently a professor in the Geology
and Environmental Geosciences, Department at Northern Illinois
University, 312 Davis Hall, Northern Illinois University, DeKalb,
IL 60115; phone 815-753-1523; fax 815-753-1945; phil@geol.niu.
edu. He has previously worked as a postdoctoral researcher at
Los Alamos National Laboratory and as a visiting researcher at
Argonne and Oak Ridge National Laboratories. He obtained his
M.S. in geophysics and Ph.D. in geosciences from New Mexico
Institute of Mining and Technology. His current research includes
integration of geophysical and hydrogeological data sets to pro-
vide better conceptual models of groundwater contamination from
landfills and in karst settings.
Yanguo Teng, is an associate professor of environmental
geochemistry at the College of Water Sciences, Beijing Normal
University, No. 19 Xinwai St., Beijing 100875, China; phone
86-10-5880-5051; teng1974@163.com. His primary research
interests include ecological risk assessment, environmental and
groundwater geochemistry, and environmental planning and man-
agement. He obtained his M.S. and Ph.D. from Chengdu Institute
of Technology, Chengdu, China.
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