Environ Geochem Health
DOI 10.1007/s10653-007-9088-y
ORIGINAL PAPER
Interaction between cadmium, lead and potassium fertilizer
(K2SO4) in a soil-plant system
Su Chen Æ Lina Sun Æ Tieheng Sun Æ Lei Chao Æ
Guanlin Guo
Received: 28 February 2006 / Accepted: 7 February 2007

Springer Science+Business Media B.V. 2007
Abstract A pot experiment was conducted to
examine the influence of potassium (K) fertil-
izer (K2SO4) application on the phytoavailabil-
ity and speciation distribution of cadmium (Cd)
and lead (Pb) in soil. Spring wheat (Triticum
aestivum L.) was selected as the test plant.
There were seven treatments including single
and combined contamination of Cd and Pb.
CdCl2
2.5 H2O and Pb(NO3)2 were added to
the soil at the following dosages:
Cd + Pb = 0.00 + 0.00, 5.00 + 0.00, 25.0 + 0.00,
0.00 + 500, 0.00 + 1000, 5.00 + 500 and
25.0 + 1000 mg kg–1, denoted by CK, T1, T2,
T3, T4, T5 and T6, respectively. The K fertilizer
had five levels: 0.00, 50.0, 100, 200 and 400 mg
K2O kg–1 soil, denoted by K0, K1, K2, K3 and
K4, respectively. The results showed that the K
fertilizer promoted the dry weight (DW) of
wheat in all treatments and alleviated the
S. Chen (&)
T. Sun
L. Chao
G. Guo
Key Laboratory of Terrestrial Ecological Process,
Institute of Applied Ecology, Chinese Academy of
Sciences, Shenyang 110016, China
e-mail: mailchensu@yahoo.com.cn
S. Chen
L. Sun
T. Sun
Key Laboratory of Environment Engineering of
Shenyang University, Shenyang 110044, China
S. Chen
L. Chao
G. Guo
Graduate School of Chinese Academy of Sciences,
Beijing 100039, China
contamination by Cd and Pb. The application
of K2SO4 reduced the uptake of Cd in different
parts including roots, haulms and grains of
wheat; the optimum dosage was the K2 level.
K supply resulted in a significant (P < 0.05)
decrease in the soluble plus exchangeable (SE)
fraction of Cd and there was a negative corre-
lation (not significant, P > 0.05) between the
levels of K and the SE fraction of Cd in soil.
The application of the K fertilizer could obvi-
ously restrain the uptake of Pb by wheat and
there were significant (P < 0.05) negative cor-
relations between the concentrations of Pb in
grains and the levels of K in soil. K supply
resulted in a decrease in the SE fraction of Pb
(except the K1 level) from the K0 to K4 levels.
At the same time, the application of the K
fertilizer induced a significant (P < 0.05) de-
crease in the weakly specifically adsorbed
(WSA) fraction of Pb and a significant
(P < 0.05) increase in the bound to Fe–Mn
oxides (OX) fraction of Pb. At different K
levels, the concentration of Pb in the roots,
haulms and grains had a positive correlation
with the SE (not significant, P > 0.05) and WSA
(significant, P < 0.05) fractions of Pb in the soil.
All the K application levels in this experiment
reduced the phytoavailability of Cd and Pb.
Thus, it is feasible to apply K fertilizer (K2SO4)
to alleviate contamination by Cd and/or Pb in
soil. Moreover, the level of K application
123

should be considered to obtain an optimal
effect with the minimum dosage.
Keywords Cadmium
Lead
Potassium
fertilizer (K2SO4)
Soil-plant system
Introduction
Northeast China has been one of the most
important industrial bases and also a main agri-
cultural production area since the People’s
Republic of China came into existence in 1949.
With the rapid development of industrial produc-
tion in recent decades, anthropogenic activities
such as mining, smelting, electroplating, ore-
refining, land disposal of wastes and irrigating
with sewage have led to increasing heavy metal
contents in soil (Patel et al. 2006; Moussa et al.
2006) and pollution problems induced by heavy
metals are becoming prominent (Guo and Zhou
2006). According to Zhou (2003), the area of
agricultural land polluted by heavy metals such as
Cd, Pb, As, Cu, and Zn has reached 2.00 · 107 ha,
and concentrations of heavy metals in more than
1.00 · 107 tons of foodstuffs have annually ex-
ceeded their national food-safety standards. Since
toxic heavy metals can be transferred in food
chains and accumulated in human bodies, many
health problems such as itai-itai disease, renal
dysfunction, liver damage, lung edema, anemia
and hypertension can be induced by heavy metals.
Therefore, soil contamination by heavy metals
and plant uptake of those heavy metals has been
one of the focuses of environmental science
because of their potential risk to human health
(Li et al. 2006). In the meantime, the application
of chemical fertilizers has expanded rapidly in
northeast China in recent years in order to
increase per unit output of agricultural produc-
tion (Li et al. 2000). The fertilizer application is
not only a conventional measure in farming, but
also one of the indispensable factors sustaining
the productivity in soil-plant systems. The appli-
cation of chemical fertilizers has a broad influence
on the growth and metabolizability of plants
under the condition of different soil environ-
ments, especially farmland ecosystems.
123
Environ Geochem Health
Plenty of factors affects the transport and
accumulation of heavy metals in soil-plant
systems, such as soil pH, cation exchange
capacity (CEC), soil redox potential, plant
species and fertilizer application (Zhou and
Sun 2002; Zhou et al. 2003; Peter et al. 2005).
Relationships between the accumulation of
heavy metals in crops and pollution of heavy
metals in soils have been well documented
(Tungare and Sawant 2002). Moreover, some
work has been done on the interaction between
potassium (K) and 137Cs (Zhu 2001). Nitrogen
(N) and phosphorus (P) fertilizer application
may increase Cd accumulation in plants (Oliver
et al. 1993). Nie et al. (2004) dealt with the
effects of nutrient elements (N, P and K) on Pb
uptake by hyperaccumulators. Effective Pb
immobilization by the formation of pyromor-
phite was reported upon addition of apatite
(Zhang and Ryan 1998), phosphate rock (Basta
et al. 2001), phosphatic clay (Singh et al. 2001)
or soluble P (Hettiarachchi et al. 2001) to Pb-
contaminated soils at the laboratory scale. Tu
et al. (2000) examined the influence of N, P and
K fertilizers on the speciation distribution of Pb
and Cd in a red soil of China. Their findings
suggest that applying chemical fertilizers may
change the speciation and thus phytoavailability
of heavy metals. However, whether the trans-
port and accumulation of heavy metals in plants
is related to the nutritional level in soil envi-
ronment is still a question to be answered. How
to use the interactions between chemical fertil-
izers and heavy metals reasonably and to
restrain and avoid harm by metals is also an
area requiring further study, although attention
has been paid to the effects of different forms
and ions of fertilizers on the phytoavailability of
metals and some researches have investigated
the interactions between them (Zhou 2003).
As an important macronutrient and one of the
dominating factors of soil CEC, K may possibly
influence Cd, Pb transportation and accumulation
in soil-plant systems. In this work, Cd and Pb
were selected to examine the phytoavailability
and changes of their chemical forms after apply-
ing different levels of the K fertilizer K2SO4
because of their toxicity and presence in north-
east China.
Environ Geochem Health
Materials and methods
Soil
Meadow brown soil (0–20 cm) samples were
collected from the Shilihe experimental station,
Chinese Academy of Sciences, Shenyang (China),
using a five-point quincunx sampling method
(Zhou 1996). The soil samples were air-dried
and sieved (<2 mm plastic mesh) before analysis
of chemical properties. Some main soil properties
are listed in Table 1. Soil chemical properties
were measured using the methods recommended
by the Chinese Society of Soil Science (Lu 1999).
Soil pH was measured in a 1:2.5 soil/water
suspension with a combination electrode. Avail-
able N was extracted using 2.00 mol l–1 KCl
solution, available P was extracted using 0.50 mol
l–1 NaHCO3 and available K was extracted using
1.00 mol l–1 neutral NH4OAC solution. Organic
matter and CEC determinations were carried out
following the standard methods of chemical
analysis (Zhou 2003). Total metal contents were
determined after a strong acid digestion and the
acids used for soil samples were HNO3–HClO4
(3:1) (Guo et al. 2006).
Pot culture experiments
Artificially contaminated soil samples were made
from the above soil. There were seven treatments
including single and combined contamination of
Cd and Pb. The dosages of Cd (added as CdCl
2.5
H2O) and Pb [added as Pb(NO3)2] applied to the
soil are given in Table 2. The seven treatments
were denoted CK, T1, T2, T3, T4, T5 and T6,
respectively. After two weeks for equilibration of
heavy metals, each treatment was supplied with K
fertilizer (added as K2SO4) at five levels: K0
(0.00 mg K2O kg–1 soil), K1 (50.0 mg K2O kg–1
soil), K2 (100 mg K2O kg–1 soil), K3 (200 mg K2O
kg–1 soil) and K4 (400 mg K2O kg–1 soil). There
Table 1 Basic physical and chemical properties of the tested soil
pH CEC Organic Available Available
(cmol matter N (mg P (mg
kg–1) (%) kg–1) kg–1)
6.50 12.3 1.55 80.4 12.7
was uniform application of N and P fertilizer at
the level of 200 mg N kg–1 soil [added as
CO(NH2)2] and 100 mg P2O5 kg–1 soil [added as
Ca(H2PO4)2]. Each pot consisted of 2.50 kg air-
dried soil and three replicates.
Soil was allowed to equilibrate for one week
before sowing the seeds. Twenty seeds of spring
wheat (Triticum aestivum L.) were sown in each
pot and, when the seedlings had grown to about
3 cm, they were thinned to 10 per pot. The plants
were irrigated with deionized water daily, main-
taining the soil moisture content at 60% (w/w) by
weighing them. The pots were randomly arranged
and rearranged several times during the growth
period. After nine weeks, the plants were mature
and were harvested.
After being harvested, the plants were rinsed
thoroughly with deionized water and separated
into roots, haulms and grains. The fresh weights
and heights of the plants were determined. The
samples were oven dried at 70C for 48 h, and
then the dry weight (DW) of the plants was
recorded. Dried plant samples were finely ground
in a stainless-steel miller and stored prior to
analysis. Soil samples of different treatments were
also collected for the determination of Cd and Pb
speciation.
Sequential extraction of soils
The sequential extraction was developed from
Tessier et al. (1979) and was carried out progres-
sively on an initial weight of 1.00 g test soil, which
was contained in a centrifuge tube (polypropyl-
ene, 100 ml) and shaken at variable speed on a
reciprocal shaker. The shaking speed was kept at
220 strokes min–1. The extractants and operation-
ally defined chemical fractions were as follows:
fraction 1, SE (water soluble plus exchangeable):
the samples were extracted at room temperature
for 1 h with 8 ml of 1.00 mol l–1 MgCl2 (pH 7.00)
with continuous stirring; fraction 2, WSA (bound
Available Total Pb Total Cd Total Cu Total Zn Clay content
K (mg (mg (mg (mg (mg <0.002 mm
kg–1) kg–1) kg–1) kg–1) kg–1) (%)
76.9 18.4 0.12 32.9 28.1 32.1
123

Table 2 Concentrations of Cd and Pb applied in the soil samples (mg kg–1)
Treatment Code
CK T1 T2
Added Cd 0.00 5.00 25.0
Added Pb 0.00 0.00 0.00
to carbonate or weakly specifically adsorbed): the
washed residue from step 1 was extracted at room
temperature with 8 ml of 1.00 mol l–1 NaOAc
(adjusted to pH 5.00 with HOAc) for 2 h with
continuous stirring; fraction 3, OX (bound to Fe–
Mn oxides): the residue of step 2 was further
extracted with 20 ml of 0.04 mol l–1 NH2OH
HCl
in 25% HOAc (v/v) heated in a water bath for 6 h
at 96C with occasionally agitation; fraction 4,
OM (bound to organic matter): the residue from
the step 3 was extracted with 3 ml of 0.02 mol l–1
HNO3 and 5 ml of 30% H2O2 (adjusted to pH
2.00 with HNO3). The mixture heated at 85C for
2 h, with occasionally agitation. A second 3 ml of
30% H2O2 (pH = 2.00 with HNO3) was added
and the mixture heated at 85C for another 3 h
with intermittent agitation. After cooling, 5 ml
3.20 mol l–1 NH4OAc in 20% (v/v) HNO3 was
added and the samples was diluted to 20 ml and
agitated continuously for 30 min; fraction 5, RES
(residual): the residue of step 4 was digested with
9 ml HNO3 and 3 ml HClO4 in a 180 ± 5C
electrothermal tank. When the sample was closely
dried and became opalescent, it was diluted to
25 ml in a test tube with 2% HNO3.
After each successive extraction, separation
was done after centrifuging for 30 min. The
supernatant was filtered and placed in a tube for
measuring. The residue was washed with 20 ml
deionized water followed by shaking followed by
centrifuging for separation before the next extrac-
tion. The results are presented as the average of
three replicates.
Chemicals and analytical methods
All chemicals used in the experiments were of
analytical grade and deionized water was used to
prepare all solutions. Analysis of heavy metals in
supernatants was carried out using a Spectr AA-
200 atomic absorption spectrophotometer (AAS,
made in Australian) after the HNO3–HClO4 (3:1)
123
Environ Geochem Health
T3 T4 T5 T6
0.00 0.00 5.00 25.0
500 1000 500 1000
wet digestion (Guo et al. 2006). Reference mate-
rial (GBW07404) was used for quality control of
acid digestion and instrument performance. The
recovery and precision were found to be within
±10%.
Data treatment and statistic analysis
The results for each sample were expressed as the
average of three replicates. Statistic analysis was
performed using SPSS11.5 software for Windows.
Results and discussion
Plant dry weights
The application of the K fertilizer K2SO4 pro-
moted the dry weight of wheat in all treatments
(Table 3). In each treatment the maximum dry
weight of wheat appeared at the highest dosage of
K (K4 level). The result indicated that, indepen-
dent of the contaminative degree of soils con-
taminated by Cd and/or Pb, the presence of the K
fertilizer K2SO4 promoted the growth of wheat
and improved the biomass of wheat.
In single Cd contamination treatments (T1 and
T2), for example, at the K2 dosage, the dry weight
of T1 and T2 was 9.81 and 8.49 g pot–1; the dry
weight of wheat reduced gradually with increas-
ing concentration of Cd in soil. In the single Pb
contamination treatments (T3 and T4), the dry
weight of wheat also decreased with increasing
concentration of Pb in the soil. In combined
contamination of Cd and Pb (T5 and T6), at the
same dosage of the K fertilizer, the dry weight of
wheat took showed the same trend that the dry
weight reduced with increasing concentration of
Cd and Pb in soil. Comparing the combined
contamination treatments with the single contam-
ination treatments of Cd and Pb, the combination
aggravated the harm to the plants. Thus,
Environ Geochem Health

Table 3 Dry weight of wheat grown in pot culture with different levels of K fertilizer (g pot–1)a
Treatment CK T1 T2 T3 T4 T5 T6

K0 9.38 ± 0.68c 8.63 ± 0.15d 7.55 ± 0.04d 8.78 ± 0.59c 7.60 ± 0.03b 7.73 ± 0.96c 6.20 ± 0.10b
K1 9.73 ± 0.54bc 9.23 ± 0.20c 8.06 ± 0.20c 9.52 ± 0.84bc 8.13 ± 0.51b 8.69 ± 0.35bc 6.54 ± 0.66b
K2 10.8 ± 0.98ab 9.81 ± 0.01b 8.49 ± 0.25bc 9.88 ± 0.34b 9.10 ± 0.31a 9.35 ± 0.02ab 6.56 ± 0.03b
K3 11.3 ± 0.85a 9.99 ± 0.44ab 8.80 ± 0.29b 10.0 ± 0.13b 9.11 ± 0.56a 9.66 ± 0.64ab 6.84 ± 0.32b
K4 11.7 ± 0.04a 10.4 ± 0.37a 9.60 ± 0.32a 10.9 ± 0.14a 9.89 ± 0.47a 10.2 ± 0.55a 7.66 ± 0.08a
a
Values followed by the same letter within each column are not significantly different at the 0.05 level by Duncan’s
multiple range test

independent of whether single or combined con-
tamination of Cd and Pb was present, the dry
weight of wheat decreased with increasing pollu-
tion level. According to the dry weight of wheat
(Table 3), the growing sequence was
T3 > T1 > T5 > T4 > T2 > T6.
Transport and accumulation of Cd in wheat
As heavy metals entered the soil, wheat began to
absorb them through the metabolism of the root
systems. Once heavy metals entered the root
cells, a fraction was stored in the roots while
another fractions were transported to adjacent
cells via tracheas or transpiration and transferred
upwards and accumulated in the haulms and
seeds. The concentrations of Cd in different parts
of the wheat in all treatments had the following
sequence: root > haulm > grain (Table 4). This
was consistent with the results of other researches
(Mo et al. 2002).
The K fertilizer had no obvious influence on
the accumulation of Cd in grains of wheat under
the CK treatment (Table 4). Under all the
experiment levels of K fertilizer, applying the
fertilizer decreased the uptake of Cd in roots,
haulms and grains of wheat compared with the
control K0 (without the application of the K
fertilizer). However, the reduction in Cd contam-
ination due to the K fertilizer was not linar
function in the level of K. In single Cd contam-
ination treatments (T1 and T2), a small quantity
of K fertilizer decreased the assimilation of Cd,
with the minimum Cd concentrations appearing
at K2, but the Cd concentration began to rise
appreciably for higher K values (Table 4). For the
treatments of combined contamination (T5 and
T6), for increasing levels of K fertilizer the
concentration of Cd in the roots first reduced
and then rose appreciably. The uptake of Cd in
haulms and grains presented the same pattern as
above.
From the comparison between single and
combined contamination (T1 and T5; T2 and
T6), for example, at the K2 level (Table 4), the
concentration of Cd in the roots, haulms and
grains was 48.0, 17.9, 3.39 mg kg–1 (for T2) and
62.0, 24.3, 3.50 mg kg–1 (for T6), respectively, the
latter being markedly higher than the former. In
other words, the combined contamination of Cd
and Pb enhanced the uptake of Cd by wheat
compared with Cd contamination alone.
The effect of K fertilizer on plant accumulation
of Cd has rarely been studied in detail in the past.
Results obtained in the present work showed that
an increase in the application of K fertilizer
decreased Cd concentrations in roots, haulms and
grains (Table 4), which suggests that the K
fertilizer (K2SO4) may decrease plant uptake of
Cd. The various potassium forms differed in
terms of their effects on Cd accumulation in
plants. However, it was pointed out by Grant
et al. (1999) that the effect of K fertilizers may be
due more to the accompanying anions of the salt.
Some studies have demonstrated that the appli-
cation of K fertilizers as KCl could enhance Cd
solubility and phytoavailability (Yi et al. 1996;
Zhao et al. 2003). Chloride is well known for
forming relatively stable complexes with Cd,
CdCl+ and CdCl02. Simple stability calculations
indicate that the formation of Cd complexes with
Cl– become significant when the Cl– concentra-
tion in soil solution rises above about 10.0 mmol
l–1 (Norvell et al. 2000), which tends to shift

123
 Environ Geochem Health

Table 4 Cd concentration in different parts of wheat with different levels of K fertilizer (mg kg–1)a
Treatment K levels Cd concentration (mg kg–1)
Root Haulm Grain

CK K0 1.13 ± 0.08a 0.39 ± 0.02a 0.11 ± 0.01a

K1 0.67 ± 0.03c 0.36 ± 0.03a 0.10 ± 0.00a
K2 1.00 ± 0.04b 0.30 ± 0.01b 0.10 ± 0.02a
K3 0.40 ± 0.02d 0.24 ± 0.02c 0.09 ± 0.02a
K4 1.11 ± 0.07a 0.26 ± 0.02bc 0.10 ± 0.01a
T1 K0 27.2 ± 1.20a 11.3 ± 0.52a 1.65 ± 0.55a
K1 22.8 ± 0.95bc 8.34 ± 0.27ab 1.13 ± 0.63ab
K2 18.7 ± 0.50d 7.06 ± 0.25b 0.57 ± 0.02b
K3 20.7 ± 1.25cd 7.59 ± 0.45b 0.64 ± 0.05b
K4 24.7 ± 1.68b 8.91 ± 0.33ab 1.37 ± 0.48ab
T2 K0 63.1 ± 2.50a 21.4 ± 1.05a 4.47 ± 0.22a
K1 63.4 ± 3.28a 19.6 ± 0.57ab 3.47 ± 0.14b
K2 48.0 ± 1.75b 17.9 ± 0.65b 3.39 ± 0.08b
K3 52.7 ± 2.35b 18.7 ± 0.89b 3.63 ± 0.25b
K4 63.1 ± 3.44a 20.0 ± 1.78ab 3.69 ± 0.15b
T5 K0 36.8 ± 1.65a 14.0 ± 0.50a 2.07 ± 0.10a
K1 29.6 ± 1.18b 10.6 ± 0.25b 1.89 ± 0.12a
K2 21.9 ± 0.56c 7.53 ± 0.48d 1.61 ± 0.05b
K3 23.3 ± 0.95c 8.65 ± 0.55c 1.65 ± 0.12b
K4 30.2 ± 1.00b 11.4 ± 0.68b 1.91 ± 0.08a
T6 K0 74.4 ± 4.00a 29.1 ± 1.34a 5.14 ± 0.30a
K1 72.5 ± 2.58a 26.4 ± 1.10b 3.87 ± 0.15c
K2 62.0 ± 3.25b 24.3 ± 0.58bc 3.50 ± 0.13c
K3 73.1 ± 3.98a 22.8 ± 0.67c 4.34 ± 0.25b
K4 74.0 ± 2.46a 24.4 ± 1.39bc 4.63 ± 0.18b
a
Values followed by the same letter within the same column and same Cd treatment are not significantly different at the
0.05 level by Duncan’s multiple range test

Cd from solid to soil solution, thus enhancing Cd
solubility and phytoavailability. It was also
suggested that the complexes CdCl2–nn and CdSO04
0
were available to plants as much as Cd2+
(Smolders and McLaughlin 1996; Smolders et al.
1996; McLaughlin et al. 1998a, b). However, SO2– 4
complexes with Cd are not as stable as chloride
complexes with Cd (Lindsay 1979), and the
results of both nutrient solution and soil experi-
ments by McLaughlin et al. (1998a, b) showed no
significant increase of Cd uptake by plants due to
SO2– 0
4 , although CdSO4 was equivalent to Cd .
2+
2–
They suggested that SO4 would not have the
same effect on plant uptake of Cd as Cl–.
Research by Sparrow et al. (1994) and Grant
et al. (1996) showed that K fertilizer in the form
of KCl increased Cd concentration in both potato
and barley, while K2SO4 resulted in a 20–30%
decrease in Cd concentration in the tubers and
leafstalks of potato compared with KCl treat-
ment.
Transport and accumulation of lead in wheat
The concentration of Pb in different parts of
wheat in all treatments obeyed the following
sequence: root > haulm > grain (Table 5). In the
treatments with only Pb (T3 and T4), the
concentration of Pb in the roots of wheat clearly
decreased with increasing application of K fertil-
izer (Table 5). The uptake of Pb in haulms and
grains followed the same pattern. For example,
with increasing K levels from K0 to K4, the
concentration of Pb in grains decreased between
0.19–0.12 mg kg–1 (for CK), 3.03–2.08 mg kg–1
(for T3) and 5.58–3.92 mg kg–1 (for T4), and all
the minimum concentrations of Pb appeared at
the highest dosage K4 (Table 5). In the treat-
ments T3 and T4, the uptake of Pb in wheat
increased with increasing concentration of Pb in
the soil.
Under combined contamination of Cd and Pb
(T5 and T6), the influence of the K level on the

123
Environ Geochem Health

Table 5 Pb concentration in different parts of wheat with different levels of K fertilizer (mg kg–1)a
Treatment K levels Pb concentration (mg kg–1)
Root Haulm Grain

CK K0 13.9 ± 0.85a 6.57 ± 0.25a 0.19 ± 0.01a

K1 12.9 ± 0.50ab 6.13 ± 0.39ab 0.16 ± 0.01b
K2 12.7 ± 0.45ab 5.69 ± 0.15bc 0.15 ± 0.00bc
K3 12.6 ± 0.60b 5.22 ± 0.22c 0.13 ± 0.02cd
K4 12.2 ± 0.95b 4.08 ± 0.55d 0.12 ± 0.01d
T3 K0 237 ± 14.7a 20.5 ± 2.35a 3.03 ± 0.12a
K1 214 ± 10.7b 17.3 ± 0.58b 2.96 ± 0.20a
K2 191 ± 13.5c 15.5 ± 0.95bc 2.48 ± 0.05b
K3 178 ± 14.3c 14.3 ± 0.35cd 2.44 ± 0.15b
K4 152 ± 9.35d 12.9 ± 0.67d 2.08 ± 0.14c
T4 K0 412 ± 27.2a 37.9 ± 2.05a 5.58 ± 0.32a
K1 404 ± 19.2a 36.5 ± 1.58a 5.27 ± 0.18a
K2 361 ± 12.4b 29.5 ± 0.65b 5.13 ± 0.25a
K3 348 ± 7.58b 27.1 ± 1.63b 4.38 ± 0.40b
K4 314 ± 17.5c 22.0 ± 0.75c 3.92 ± 0.11b
T5 K0 208 ± 9.25a 17.3 ± 1.05a 1.86 ± 0.04a
K1 170 ± 8.55b 16.7 ± 0.50a 1.84 ± 0.06a
K2 145 ± 5.36c 14.4 ± 0.36b 1.75 ± 0.05b
K3 127 ± 4.12d 13.5 ± 0.95b 1.48 ± 0.04c
K4 110 ± 5.74e 11.8 ± 0.66c 1.07 ± 0.02d
T6 K0 385 ± 22.5a 25.8 ± 1.50a 3.86 ± 0.15a
K1 315 ± 18.7b 24.6 ± 2.02a 3.42 ± 0.10b
K2 278 ± 9.58c 23.2 ± 1.45ab 2.70 ± 0.22c
K3 251 ± 11.3d 21.8 ± 1.33b 2.55 ± 0.08c
K4 211 ± 6.55e 21.5 ± 0.85b 2.14 ± 0.12d
a
Values followed by the same letter within the same column and same Pb treatment are not significantly different at the
0.05 level by Duncan’s multiple range test

uptake of Pb was similar to that of single Increasing the application of K (K2SO4)

contamination of Pb. The application of K also
decreased the accumulation of Pb. Furthermore,
by comparing T3 with T5 (Table 5), for example,
at the highest dosage of K (K4), the concentration
of Pb in roots, haulms and grains was 151, 12.9,
2.08 mg kg–1 (for T3) and 110, 11.8, 1.07 mg kg–1
(for T5), respectively, and the Pb concentration of
the latter was lower than that of the former. The
same situation applied to T4 and T6. This
indicates that the coexistence of Cd and Pb
restrains the uptake of Pb by wheat. During the
interactions between Cd and Pb, Pb may scramble
the adsorption sites of Cd in soil (Lin et al. 2000).
Due to the strong adsorptive ability of Pb in soil,
Pb prefers to fixate on soil, forming steady
compounds, and had difficulty moving. The Cd
replaced by Pb improved the phytoavailablity of
Cd. Thus Pb was always inferior to Cd during
competition and the phytoavailability of Pb
decreased with the presence of Cd.
decreased the Pb concentration in the roots,
haulms and grains of wheat. There were signifi-
cant (P < 0.05) negative relationships between
the concentration of Pb in the grain of wheat and
the amount of K2SO4 applied to the soil (Fig. 1).
Speciation distribution of Cd and Pb in soil
When an external source of heavy metals is
spiked into soil, they react with the soil surface
and are correspondingly retained in soil (Darm-
awan and Wada 1999; Zhou et al. 2002). Intrinsic
heavy metals in the soil are less mobile (Martinez
and Motto 2000; Tu et al. 2000), so metal
fractions in the soil at a zero loading rate are
not considered in this work. The speciation of Cd
and Pb in soils for different K levels is listed in
Tables 6 and 7. There were five metal fractions
including soluble plus exchangeable (SE), weakly
specially adsorbed (WSA), bound to Fe–Mn

123
 Environ Geochem Health

Fig. 1 Relationship

Mean Pb concentration in grain (mg kg-1)

6
between Pb concentration
in grains of wheat and the 5
dosage of the applied K
CK
fertilizer 4
T3

3 T4
T5
2 T6

0
0 100 200 300 400 500
-1
Daosage of K fertilizer (mg kg )

Table 6 Speciation distribution of Cd in soils for different levels of K fertilizer (mg kg–1)a
Fraction K levels Cd
T1 T2 T5 T6

SE K0 2.32 ± 0.02a 15.6 ± 0.15a 2.50 ± 0.04a 16.0 ± 0.16a

K1 2.12 ± 0.03b 15.2 ± 0.20b 2.27 ± 0.07b 15.5 ± 0.27b
K2 1.77 ± 0.03d 14.2 ± 0.32c 1.93 ± 0.05c 14.5 ± 0.22c
K3 2.06 ± 0.05b 14.5 ± 0.26c 2.19 ± 0.06b 14.8 ± 0.15c
K4 1.98 ± 0.07c 14.3 ± 0.24c 2.03 ± 0.06c 14.6 ± 0.16c
WSA K0 1.48 ± 0.03b 5.34 ± 0.12a 1.54 ± 0.03c 5.78 ± 0.11a
K1 1.47 ± 0.03b 5.28 ± 0.06a 1.70 ± 0.03b 4.77 ± 0.11c
K2 1.63 ± 0.01a 4.82 ± 0.12b 1.76 ± 0.02a 5.19 ± 0.10b
K3 1.44 ± 0.03b 4.86 ± 0.21b 1.65 ± 0.04b 5.09 ± 0.17b
K4 1.62 ± 0.05a 5.03 ± 0.12b 1.77 ± 0.03a 5.36 ± 0.20b
OX K0 0.59 ± 0.01c 3.19 ± 0.11c 0.52 ± 0.01c 2.68 ± 0.07d
K1 0.64 ± 0.01b 3.22 ± 0.13c 0.53 ± 0.01c 2.83 ± 0.10cd
K2 0.69 ± 0.02a 4.62 ± 0.16b 0.62 ± 0.01a 3.21 ± 0.11a
K3 0.64 ± 0.02b 4.60 ± 0.14b 0.57 ± 0.02b 3.08 ± 0.10ab
K4 0.66 ± 0.02ab 5.04 ± 0.13a 0.58 ± 0.02b 2.99 ± 0.13bc
OM K0 0.36 ± 0.01b 0.37 ± 0.01c 0.16 ± 0.00c 0.34 ± 0.01a
K1 0.31 ± 0.01c 0.34 ± 0.01d 0.12 ± 0.00d 0.29 ± 0.01a
K2 0.38 ± 0.01a 0.34 ± 0.01d 0.19 ± 0.00b 0.28 ± 0.10a
K3 0.31 ± 0.01c 0.43 ± 0.01b 0.17 ± 0.01c 0.25 ± 0.09a
K4 0.29 ± 0.01c 0.45 ± 0.01a 0.27 ± 0.01a 0.33 ± 0.01a
RES K0 0.35 ± 0.01b 0.84 ± 0.02d 0.35 ± 0.01c 1.03 ± 0.03c
K1 0.44 ± 0.02a 1.03 ± 0.02c 0.41 ± 0.02b 1.11 ± 0.03b
K2 0.46 ± 0.02a 1.11 ± 0.03b 0.44 ± 0.02b 1.16 ± 0.02a
K3 0.44 ± 0.01a 1.02 ± 0.03c 0.43 ± 0.01b 1.17 ± 0.03a
K4 0.47 ± 0.02a 1.19 ± 0.02a 0.47 ± 0.02a 1.05 ± 0.03c
a
Values followed by the same letter within the same column and same fraction are not significantly different at the 0.05
level by Duncan’s multiple range test

oxides (OX), bound to organic matter (OM) and associated with RES (3.32–9.38%) and OM (0.99–
residual fractions (RES). The added Cd existed 7.78%). The percentage of Cd fractions had the
almost as a non-residual fraction (the sum of sequence: SE > WSA, OX > RES > OM. Unlike
other fractions excluding RES). Most of the Cd in Cd, most of the lead in T3, T4, T5 and T6 was
T1, T2, T5 and T6 was presented in SE (35.9– found in OX (41.0–47.6%) and WSA (31.0–
63.3%), followed by WSA (19.2–34.6%), OX 37.2%), followed by RES (9.00–10.0%) and OM
(10.3–19.4%), and a small percentage of Cd was (7.53–9.46%), while SE (2.11–4.82%) was small.

123
Environ Geochem Health

Table 7 Speciation distribution of Pb in soils for different levels of K fertilizer (mg kg–1)a
Fraction K levels Pb
T3 T4 T5 T6

SE K0 11.3 ± 0.15b 38.6 ± 0.99b 12.4 ± 0.24b 44.1 ± 1.06b

K1 12.5 ± 0.21a 42.8 ± 1.22a 13.9 ± 0.32a 48.5 ± 1.36a
K2 11.2 ± 0.18b 38.0 ± 0.80bc 12.6 ± 0.40b 41.2 ± 1.02c
K3 10.8 ± 0.22c 36.2 ± 1.02cd 11.5 ± 0.26c 40.2 ± 0.96c
K4 10.6 ± 0.17c 35.2 ± 1.05d 11.2 ± 0.16c 41.1 ± 1.01c
WSA K0 188 ± 1.02a 369 ± 4.39a 181 ± 1.03a 367 ± 2.60a
K1 179 ± 0.98b 352 ± 3.60b 178 ± 1.20b 327 ± 2.04b
K2 179 ± 1.12b 345 ± 3.15c 174 ± 0.98c 320 ± 2.12c
K3 174 ± 1.25c 341 ± 2.69c 171 ± 0.96d 313 ± 1.99d
K4 171 ± 1.00d 335 ± 2.31d 168 ± 1.01e 313 ± 2.05d
OX K0 210 ± 1.99c 411 ± 2.56e 218 ± 1.01d 420 ± 3.00d
K1 214 ± 1.88b 420 ± 2.32d 220 ± 1.13c 456 ± 2.57c
K2 215 ± 2.01b 436 ± 2.69c 230 ± 1.03a 469 ± 2.03b
K3 220 ± 2.03a 445 ± 2.15b 227 ± 1.05b 472 ± 1.86b
K4 221 ± 2.13a 451 ± 2.22a 226 ± 1.13b 479 ± 2.54a
OM K0 47.0 ± 0.60ab 83.6 ± 1.04b 45.9 ± 0.58b 77.5 ± 0.53ab
K1 47.4 ± 0.77a 85.3 ± 1.30ab 44.2 ± 0.27c 75.7 ± 0.64c
K2 45.4 ± 1.01b 86.1 ± 1.01ab 43.5 ± 0.35c 77.8 ± 0.55a
K3 46.2 ± 0.97ab 84.5 ± 1.35a 45.9 ± 0.23b 76.5 ± 0.72bc
K4 46.8 ± 1.03ab 85.3 ± 1.37ab 47.4 ± 0.35a 77.5 ± 0.69ab
RES K0 48.5 ± 1.02a 98.8 ± 1.65ab 47.4 ± 0.33b 99.3 ± 0.71a
K1 48.5 ± 0.96a 99.3 ± 1.60a 50.3 ± 0.41a 99.8 ± 1.02a
K2 48.4 ± 0.86a 94.9 ± 1.54c 45.2 ± 0.51c 96.5 ± 1.07c
K3 49.2 ± 0.77a 96.1 ± 1.23bc 47.3 ± 0.27b 98.4 ± 0.99ab
K4 49.5 ± 1.20a 97.6 ± 1.34abc 50.5 ± 0.33a 96.8 ± 1.00bc
a
Values followed by the same letter within the same column and same fraction are not significantly different at the 0.05
level by Duncan’s multiple range test

The percentage of Pb fractions had the sequence:
OX, WSA > RES > OM > SE. These results are
in line with other investigations in northeast
China (Wang and Zhou 2003).
Fertilizers can alter soil properties such as pH
and surface charges or directly react with heavy-
metal ions in the soil. All these effects would
result in changes in the form of the heavy metals.
After harvesting the wheat, the pH of soil in each
treatment (data not listed) was determined. The
results indicated that K application had no
significant (P > 0.05) influence on soil pH, so
the changes of Cd and Pb specification were not
induced by changes of soil pH. In the treatments
T1, T2, T5 and T6, the application of the K
fertilizer significantly (P < 0.05) lowered the SE
fraction of Cd. The SE fraction of Cd decreased
with increasing K level from K0 to K2, and then
began to increase from K3 to K4 (Table 6).
However, K supply resulted in an increase in the
OX and RES fractions. Under different levels of
K, the concentration of Cd in the roots, haulms
and grains had a positive correlation (not signif-
icant, P > 0.05) with the SE fraction of Cd and a
negative correlation (not significant, P > 0.05)
with the OX, RES fractions of Cd in soil. Because
the SE fraction of metals is considered the most
important available fraction for plant uptake
(Vulkan et al. 2000; Huang et al. 2005), a possi-
bility is that K application could reduce the SE
fraction of Cd in soil, thus decrease the phyto-
availability of Cd.
In the treatments T3, T4, T5 and T6, the
application of K resulted in a significant
(P < 0.05) decrease in the WSA fraction of Pb
in the soil, a phenomenon also observed by Tu
et al. (2000). In this work, applying K fertilizer
significantly (P < 0.05) increased Pb bound to Fe–
Mn oxides (OX). While the SE fraction of Pb
increased at the K1 level, it decreased gradually
for the K2 to K4 levels (Table 7). Under different
levels of K, the concentration of Pb in roots,

123

haulms and grains had a positive correlation with
the SE (not significant, P > 0.05) and WSA
(significant, P < 0.05) fractions of Pb in the soil.
An increase in the application of K (K2SO4)
decreased the phytoavailability of Pb. One main
reason for this was the positive correlation (sig-
nificant, P < 0.05) between the Pb concentration
in wheat and the WSA fraction of Pb, while the K
fertilizer significantly (P < 0.05) reduced the
WSA fraction of Pb, thus decreased the uptake
of Pb. It was well known that Pb prefers to form
compounds whose solubility is small, such as
PbCO3, Pb3(PO4)2 or PbSO4 and so Pb rarely
moves in soil. With increasing levels of K2SO4 the
quantity of SO2– 4 in the soil was increased
accordingly. So another probability is that Pb2+
combined with SO2– 4 to form PbSO4, thus reduc-
ing the SE fraction of Pb (except at the K1 level),
the quantity of available Pb and the phytoavail-
ability of Pb. What needs to be pointed out is that
the K1 level of fertilizer increased the SE fraction
of Pb, but that Pb accumulation was reduced
compared with the control K0 level. A possibile
explanation is that K+ promoted the growth of the
plant and diluted the concentration of Pb in the
plant.
Conclusions
In heavy-metal-contaminated soils, application of
chemical fertilizers not only provides plant nutri-
ents, but may also change the speciation and
phytoavailability of heavy metals. The application
of K fertilizer (K2SO4) increased the dry weight
of wheat and alleviated the threat from Cd and
Pb. The fertilizer K2SO4 decreased the assimila-
tion of Cd in roots, haulms and grains of wheat
under different dosages of K; the optimum dosage
was the K2 level. K supply resulted in a significant
(P < 0.05) decrease in the SE fraction of Cd and
there was a negative correlation (not significant,
P > 0.05) between the levels of K and the SE
fraction of Cd in soil. The application of the K
fertilizer could clearly decrease the uptake of Pb
by wheat and there were significant (P < 0.05)
negative correlations between the concentration
123
Environ Geochem Health
of Pb in grains and the level of K in soil. The K
supply resulted in a decrease in the SE fraction of
Pb (except the K1 level) from the K0 to K4 levels.
At the same time, the application of K fertilizer
induced a significant (P < 0.05) decrease in the
WSA fraction and a significant (P < 0.05) in-
crease in the OX fraction of Pb. Under different
levels of K, the concentration of Pb in roots,
haulms and grains had a positive correlation with
the SE (not significant, P > 0.05) and WSA
(significant, P < 0.05) fractions of Pb in soil. All
levels of K application in this experiment reduced
the phytoavailability of Cd and Pb. Thus, it is
feasible to apply the K fertilizer K2SO4 to
alleviate contamination of Cd and/or Pb in soil.
When applying the K fertilizer K2SO4 to Cd-
contaminated soil, we suggest that the level of K
should be considered to obtain an optimal effect
with minimum dosage.
Acknowledgments The authors acknowledge the
financial support from the National Natural Science
Foundation of China (no. 20477029) and the National
Key Basic Research Program of China (no.
2004CB418506).
References
Basta, N. T., Gradwohl, R., Snethen, K. L., & Schroder, J.
L. (2001). Chemical immobilization of lead, zinc, and
cadmium in smelter-contaminated soils using bioso-
lids and rock phosphate. Journal of Environmental
Quality, 30, 1222–1230.
Darmawan, I., & Wada, S. (1999). Kinetics of fraction of
copper, lead and zinc loaded to soils that differ in
cation exchange composition at low moisture content.
Commum. Soil Science and Plant Analysis, 30(17),
2363–2375.
Grant, C. A., Baily, L. D., & McLaughlin, M. J. (1999).
Management factors which influence cadmium con-
centrations in crops. In: M. J. McLaughlin, & B. R.
Singh (Eds.), Cadmium in soils and plants (pp. 151–
198). Dordrecht, the Netherlands: Kluwer Academic
Publishing.
Grant, C. A., Bailey, L. D., & Therrien, M. C. (1996).
Effect of N, P, and KCl fertilizers on grain yield and
Cd concentration of malting barley. Fertilizer Re-
search, 45, 153–161.
Guo, G. L., & Zhou, Q. X. (2006). Evaluation of heavy
metal contamination in Phaeozem of northeast China.
Environmental Geochemistry and Health, 28, 331–340.
Guo, G. L., Zhou, Q. X., Koval, P. V., & Belogolova, G. A.
(2006). Speciation distribution of Cd, Pb, Cu and Zn
in contaminated phaiozem in north-east China using
Environ Geochem Health
single and sequential extraction procedures. Austra-
lian Journal of Soil Research, 44(2), 135–142.
Hettiarachchi, G. M., Pierzynski, G. M., & Ransom, M. D.
(2001). In situ stabilization of soil lead using phospho-
rus. Journal of Environmental Quality, 30, 1214–1221.
Huang, Y., Tao, S., & Chen, Y. J. (2005). The role of
arbuscular mycorrhiza on change of heavy metal
speciation in rhizosphere of maize in wastewater
irrigated agriculture soil. Journal of Environmental
Sciences, 17(2), 276–280.
Lindsay, W. L. (1979). Chemical equilibria in soils. New
York: Wiley.
Li, J., Xie, Z. M., Xu, J. M., & Sun, Y. F. (2006). Risk
assessment for safety of soils and vegetables around a
lead/zinc mine. Environmental Geochemistry and
Health, 28, 37–44.
Li, R., Yang, S., Xia, Y., & Gong, J. (2000). Sustainable
and high-effective agriculture in coastal areas of China.
Hangzhou: Zhejiang University Press (in Chinese).
Lin, Q., Chen, H. M., Zheng, C. R., & Chen, Y. X. (2000).
Chemical behavior of Cd, Pb and their interaction in
rhizosphere and bulk. Journal of Zhejiang University
(Agriculture and Life Science), 26(5), 527–532 (in
Chinese).
Lu, R. K. (1999). Analytical methods for soils and agri-
cultural chemistry. Beijing: China Agricultural Science
and Technology Press (in Chinese).
Martinez, C. E., & Motto, H. I. (2000). Solubility of lead,
zinc and copper added to mineral soil. Environmental
Pollution, 107, 153–158.
McLaughlin, M. J., Andrew, S. J., Smart, M. K., & Smol-
ders, E. (1998a). Effects of sulfate on cadmium uptake
by Swiss chard: I. Effects of complexation and calcium
competition in nutrient solutions. Plant Soil, 202, 211–
216.
McLaughlin, M. J., Lambrechts, R. M., Smolders, E., &
Smart, M. K. (1998b). Effects of sulfate on cadmium
uptake by Swiss chard: II. Effects due to sulfate
addition to soil. Plant Soil, 202, 217–222.
Mo, Z., Wang, C. X., Chen, Q., Wang, H., Xue, C. J., &
Wang, Z. J. (2002). Distribution and enrichment of
heavy metals of Cu, Pb, Zn, Cr and Cd in paddy plant.
Environmental Chemistry, 21(2), 110–116 (in Chi-
nese).
Moussa, M. D., Jill, S. L., Dave, U., Nicholas, A., Leeanne,
M., James, G. C., David, B. S., & James, C. (2006).
Arsenic, Cadmium, Lead, and Mercury in surface
soils, Pueblo, Colorado: implications for population
health risk. Environmental Geochemistry and Health,
28, 297–315.
Nie, J. H., Liu, X. M., & Wang, Q. R. (2004). Effects of
nutrient elements on the lead uptake by hyperaccu-
mulators. Ecology and Environment, 13(3), 306–309,
(in Chinese).
Norvell, W. A., Wu, J., Hopkins, D. G., & Welch, R. M.
(2000). Association of cadmium in durum wheat grain
with soil chloride and chelate-extractable soil
cadmium. Soil Science Society of America journal, 64,
2162–2168.
Oliver, D. P., Schultz, J. E., Tiller, K. G., & Merry, R. H.
(1993). The effect of crop rotations and tillage
practices on cadmium concentration in wheat grain.
Agricultural Research, 44, 1221–1234.
Patel, K. S., Shrivas, K., Hoffmann, K., & Jakubowski, N.
(2006). A survey of lead pollution in Chhattisgarh
State, central India. Environmental Geochemistry and
Health, 28, 11–17.
Peter, S., Tibor, N., & Ilona, M. (2005). Distribution and
possible immobilization of lead in a forest soil (Luv-
isol) profile. Environmental Geochemistry and Health,
27, 1–10.
Singh, S. P., Ma, L. Q., & Harris, W. G. (2001). Heavy
metal interactions with phosphatic clay: sorption and
desorption behavior. Journal of Environmental
Quality, 30, 1961–1968.
Smolders, E., & McLaughlin, M. J. (1996). Effect of Cl on
Cd uptake by Swiss chard in nutrient solutions. Plant
Soil, 179, 57–64.
Smolders, E., McLaughlin, M. J., & Tiller, K. G. (1996).
Influence of chloride on Cd availability to Swiss chard:
a resin buffered solution culture system. Soil Science
Society of America journal, 60, 1443–1447.
Sparrow, L. A., Saladini, A. A., & Johnstone, J. (1994).
Field studies of Cd in potatoes (Solanum tuberosum
L.): III. Response of cv. Russet Burbank to sources of
banded potassium. Australian Journal of Soil Re-
search, 45, 243–249.
Tessier, A., Campbell, P. G. C., & Bisson, M. (1979).
Sequential extraction procedure for the speciation of
particulate trace metals. Analytical chemistry, 51(7),
844–851.
Tu, C., Zheng, C. R., & Chen, H. M. (2000). Effect of
applying chemical fertilizers on forms of lead and
cadmium in red soil. Chemosphere, 41, 133–138.
Tungare, S. M., & Sawant, A. D. (2002). Lead and cad-
mium in selected species of shrimp around the
Mumbai coast, India. Bulletin of Environmental
Contamination Toxicology, 68, 455–462.
Vulkan, R., Zhao, F. J., & Barbosa, J. V. (2000).
Copper speciation and impacts on bacterial bio-
sensors in the pore water of copper-contaminated
soils. Environmental Science & Technology, 34(24),
5115–5121.
Wang, X., & Zhou, X. Q. (2003). Distribution of forms for
cadmium, lead, copper and zinc in soil and its influ-
ences by modifier. Journal of Agro-Environment Sci-
ence, 22(5), 541–545 (in Chinese).
Yi, C. Z., Fu, G. P., Zhang, F. S., & Li, H. F. (1996). Effects
of potash fertilizer on uptake and accumulation of
cadmium by crops. Journal of China Agricultural
University, 1(5), 79–84 (in Chinese).
Zhang, P., & Ryan, J. A. (1998). Formation of pyromor-
phite in anglesite–hydroxyapatite suspensions under
varying pH conditions. Environmental Science &
Technology, 32, 3318–3324.
Zhao, Z. Q., Zhu, Y. G., Li, H. Y., Smith, S. E., & Smith,
A. F. (2003). Effects of forms and rates of potassium
fertilizers on cadmium uptake by two cultivars of
spring wheat (Triticum aestivum L.). Environment
International, 29, 973–978.
Zhou, D. M., Chen, H. M., Hao, X. Z., & Wang, Y. J.
(2002). Fractionation of heavy metals in soils as af-
123

fected by soil types and metal load quantity. Pedo-
sphere, 12(4), 309–319.
Zhou, Q. X. (1996). Soil-quality guidelines related to
combined pollution of chromium and phenol in agri-
cultural environments. Human and Ecologycal Risk
Assessment, 2, 591–607.
Zhou, Q. X. (2003). Interaction between heavy metals and
nitrogen fertilizers applied in soil-vegetable systems.
Bulletin of Environmental Contamination Toxicology,
71(2), 338–344.
Zhou, Q. X., & Sun, T. H. (2002). Effects of chromium
(VI) on extractability and plant uptake of fluorine in
123
Environ Geochem Health
agricultural soils of Zhejiang Province, China. Water
Air Soil Pollution, 133(14), 145–160.
Zhou, Q. X., Wang, X., Liang, R. L., & Wu, Y. Y. (2003).
Effects of cadmium and mixed heavy metals on rice
growth in Liaoning, China. Soil & Sediment Contam-
ination, 12(6), 851–864.
Zhu, Y. G. (2001). Effects of external potassium (K) supply
on the uptake of 137Cs by spring wheat (Triticum aes-
tivum cv. Tonic): A large-scale hydroponic study.
Journal o f Environmental Radioactive, 55, 303–314.