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Environ Earth Sci (2011) 64:1921–1929

DOI 10.1007/s12665-011-1005-0

ORIGINAL ARTICLE

Spatial distribution, source identification and affecting


factors of heavy metals contamination in urban–suburban
soils of Lishui city, China
Hongyan Wang • Shenggao Lu

Received: 2 May 2010 / Accepted: 8 March 2011 / Published online: 24 March 2011
Ó Springer-Verlag 2011

Abstract An investigation on spatial distribution, possible Introduction


pollution sources, and affecting factors of heavy metals in
the urban–suburban soils of Lishui city (China) was con- Accelerated industrialization and urbanization lead to an
ducted using geographic information system (GIS) tech- increased pollution of soil and water body and a growing
nique and multivariate statistics. The results indicated that risk for heavy metal uptake by human. Many studies
the topsoils in urban and suburban areas were enriched with indicated that industrialization and urbanization had caused
metals, such as Cd, Cu, Pb, and Zn. Spatial distribution maps the elevated contamination of heavy metals in urban and
of heavy metal contents, based on geostatistical analysis and suburban soils (Afshin et al. 2009; Imperato et al. 2003;
GIS mapping, indicated that Cd, Cr, Cu, Mn, Ni, Pb, and Zn Lee et al. 2006; Li et al. 2001, 2004; Möller et al. 2005; Shi
had similar patterns of spatial distribution. Their hot-spot et al. 2008; Sun et al. 2010; Yang et al. 2009). The elevated
areas were mainly concentrated in the densely populated old heavy metals in the urban topsoils can then pose a risk to
urban area of the city. Multivariate statistical analysis human health as a result of entering the food chain through
(correlation analysis, principal component analysis, and direct ingestion of dust or the ingestion of plants. There-
clustering analysis) showed distinctly different associations fore, research into the distribution of heavy metals in urban
among the studied metals, suggesting that Cr, Cu, Ni, Pb, soils and their likely effects on the human health is gaining
Cd, and Zn had anthropogenic sources, whereas Co and V more attention in the recent years. Several studies have
were associated with parent materials and therefore had reported the anthropogenic impact associated with rapid
natural sources. The Cd, Cr, Ni, Pb, and Zn contents were development of industrial and urban regions and suggested
positively correlated with soil organic matter, pH, and sand vehicle emissions, industrial waste, the atmospheric depo-
content (p \ 0.01). It is concluded that GIS and multivariate sition of dust and aerosol, and other uncontrolled factory
statistical methods can be used to identify hot-spot areas and emissions as possible sources of the heavy metal pollution
potential sources of heavy metals, and assess soil environ- (Afshin et al. 2009; Imperato et al. 2003; Lee et al. 2006;
ment quality in urban–suburban areas. Li et al. 2001, 2004; Möller et al. 2005; Shi et al. 2008; Sun
et al. 2010; Yang et al. 2009).
Keywords Heavy metals  Geostatistics  The study of the spatial distribution and source identi-
Multivariate statistical analysis  Urban soils  GIS fication of heavy metals in urban soils is very important in
order to identify the hot-spot areas of pollution and assess
the potential sources of pollutants (Afshin et al. 2009; Carr
et al. 2008; Imperato et al. 2003; Lee et al. 2006; Li et al.
H. Wang  S. Lu (&) 2004; Li and Feng 2010; Madrid et al. 2002; Shi et al.
College of Environmental and Resource Sciences, 2008; Zhang 2006). Usually, the identification of pollutant
Zhejiang Provincial Key Laboratory of Subtropical Soil sources is conducted with the aid of multivariate statistical
and Plant Nutrition, Key Laboratory of Environment
analyses, such as correlation analysis, principal component
Remediation and Ecological Health, Ministry of Education,
Zhejiang University, Hangzhou 310029, China analysis (PCA), and cluster analysis (CA). Some authors
e-mail: lusg@zju.edu.cn have used multivariate statistical methods to identify the

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1922 Environ Earth Sci (2011) 64:1921–1929

factors of lithogenic and anthropogenic origin responsible comprises two typical regions: the old urban area with a
for the heavy metal pollution of urban soils (Facchinelli long historic city center district with high urban activities
et al. 2001; Franco-Urı́a et al. 2009; Li et al. 2009; Lu et al. and a new suburban area with newly established industrial
2010; Martin et al. 2006; Ozan et al. 2008; Sollitto et al. parks and residential areas that commenced in the early
2010; Zheng et al. 2008). Furthermore, the geostatistical 2000s.
analysis and GIS-based spatial mapping have been used to A total of 126 topsoil samples were collected from the
study spatial distribution patterns and possible hot spots of old urban and suburban areas of the city. The sampling
elevated concentrations of heavy metal contamination in an sites covered all high density, inhabited, and commercial
urban environment (Carr et al. 2008; Facchinelli et al. centers of the old urban area, as well as new developing
2001; Lee et al. 2006; Li et al. 2004; Zhang 2006). Pol- industrial parks and un-urbanized suburban areas around
lution maps, based on GIS technique, may also provide the old urban area, representing different levels of pollution
information on pollution sources of heavy metals and the exposure. Locations of sampling sites are given in Fig. 1.
relative contribution of different sources. At each sampling site, five or six subsamples of topsoils
Most of the studies on heavy metals’ contamination in (0–20 cm) were taken with a stainless steel spade and
urban soils have usually been carried out in large cities mixed thoroughly to obtain a composite sample. Samples
with dense traffic and population or in industrial cities with were air-dried and then sieved through a 2.0-mm sieve to
a high degree of industrialization in developed countries; remove stones, coarse materials, and other debris. Portions
but limited data is available on accumulation of heavy of the soil samples (about 100 g) were further ground to
metals in the middle and small cities of a rapidly devel- pass through a 100-mesh nylon sieve for heavy metals’
oping region. There is also no information concerning the analysis. The physical and chemical properties of the
spatial distribution pattern of heavy metals in the course of studied soils are presented in Table 1.
rapid urbanization. The selected region is experiencing a
rapid industrialization and urbanization in the last 10 years. Chemical analysis
The rapid growth of industrial, population, and vehicles
exerts a heavy pressure on its urban environment quality. Soil physical and chemical properties were determined
Therefore, the knowledge on impact of rapid urbanization according to standard analysis procedure (Bao 2000). Soil
on urban pollution is an important issue for city planning pH was determined in distilled water in a soil-liquid ratio
and monitoring of urban environment quality. The research of 1:2.5. The hydrometer method determined the distribu-
results may be helpful for the city government in control- tion of soil particle sizes. The dichromate oxidation method
ling and alleviating heavy metal contamination in the determined soil organic matter. Total nitrogen (TN) was
course of urban sprawl. measured with a Rapid N Cube Nitrogen Analyzer. Total P
The aims of the present study are to: (1) determine the was determined colorimetrically as ammonium molybdate–
concentrations of heavy metals in the urban and suburban ascorbic acid, following H2SO4–HClO4 digestion. Con-
regions of a rapidly growing city in China; (2) map the centrations of heavy metals (Cr, Mn, V, Co, Ni, Cu, Zn, As,
spatial distribution of heavy metals through geostatistical Cd, and Pb) were analyzed using a strong acid digestion
analysis and GIS for the purpose of identifying their spatial
patterns and possible hot spots of elevated concentrations
of heavy metals; and (3) identify the possible pollution
sources of heavy metals in the soils using correlation
analysis, principal component analysis (PCA), and cluster
analysis (CA).

Materials and methods

Study area and soil sampling

The studied area, Lishui city (the geographical position


being N28°25–280 and E119°530 –580 ) is located in south-
western Zhejiang Province, eastern China (Fig. 1). Rapid
urban expansion and industrial development in the city
began in the 1990s. It is about 31 km2 in area with an urban
population of more than 200,000 in 2007. The studied area Fig. 1 Sketch map of the studied area and sampling sites

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Environ Earth Sci (2011) 64:1921–1929 1923

Table 1 Descriptive statistics of physical and chemical properties in Results and discussion
the urban and suburban soils of Lishui city
Soil property Units Range Mean SD Heavy metal concentrations

Sand (2–0.02 mm) % 12.2–82.2 56.3 12.3 The descriptive statistics of heavy metal contents in the
Silt (0.02–0.002 mm) % 4.2–45.4 28.1 8.8 soils are summarized in Table 2. The soil background
Clay (\0.002 mm) % 1.8–53.4 15.6 6.6 values in the studied areas (Soil Survey Office of Zhejiang
pH – 3.0–9.7 6.0 1.4 Province 1994) are used as the reference values. The mean
Organic matter g/kg 1.2–110.7 30.0 15.2 contents of Cd, Cu, Pb and Zn in soils were 0.53, 35.75,
Total N g/kg 0.6–5.3 2.1 0.7 63.15 and 192.38 mg/kg, respectively, which are much
Total P mg/kg 19.6–1663.7 710.1 296.2 higher than the background values, indicating possible
SD standard deviation contamination that is probably caused by an anthropogenic
source. The enrichment of Cd, Cu, Pb, and Zn in soils was
method (Bao 2000) and inductively coupled plasma-mass considered to be the result of a gradual accumulation from
spectrometry (ICP-MS). The quality of the analysis was various pollution sources (especially human activities and
controlled according to standard procedure (Bao 2000). traffic) over time. When compared with the heavy metal
concentrations in the soils of other Chinese cities (Li et al.
Multivariate statistical analysis and GIS spatial 2004; Lu et al. 2004, 2007; Shi et al. 2008; Sollitto et al.
mapping 2010; Soil Survey Office of Zhejiang Province 1994; Sun
et al. 2010), the mean values of Cd, Cu, Pb, and Zn in the
The most common multivariate statistical methods, soils studied are lower than those of the soils in the big
including correlation analysis, principal component analy- cities and industrial regions as reported earlier. Therefore,
sis (PCA), and cluster analysis (CA) were used here to the relatively lower concentrations of heavy metals in the
evaluate the analytical data. The log or Box-cox transfor- soils studied could be the result of less accumulation time
mation of all data was made to ensure the normal distri- and rate.
bution of heavy metal concentrations. Statistical analyses The skewness values of heavy metal contents showed
were performed using SPSS for Windows 16.0 software larger variability of heavy metal contents, with positively
(SPSS Inc., Chicago, USA). Geostatistical analysis and skewed frequency distribution. This is common for heavy
GIS mapping techniques were employed to produce spatial metals because the presence of a point source contamina-
distribution maps for the ten studied metals, and the soft- tion may cause a significant increase of metal contents. The
ware used for this purpose was ArcGIS 9.2 (ESRI Co, coefficient of variation (CV) values of ten heavy metals in
Redlands, USA) and GS? version 3.1 for Windows the soils, ranged from 35 to 72%, indicated they had
(Gamma Design Software, Plainwell, MI, USA). The Kri- moderate variations. The CV value (72%) of Cd was the
ging interpolation was used for the interpolation of geo- highest of the ten heavy metals, suggesting that Cd had the
graphical data. Details of geostatistics analysis can be greatest variation among the studied metals and thus would
found in Shi and Li (2006). have the highest possibility of being influenced by the

Table 2 Descriptive statistical summary of heavy metal concentrations in the urban and suburban soils of Lishui city (mg/kg)
Element Range Mean Median SD Skewness Kurtosis CV (%) Background
value

Cr 9.41–105.10 34.66 32.36 15.79 2.08 6.78 45.7 36.73


Mn 90.53–950.83 345.80 341.66 157.43 0.94 1.38 45.5 nd
V 17.95–177.26 42.55 39.08 17.69 3.94 26.28 41.6 nd
Co 2.17–34.00 6.35 5.99 3.35 5.02 37.74 52.7 nd
Ni 3.70–50.21 14.35 12.74 7.26 2.16 6.44 50.6 nd
Cu 4.72–140.83 35.75 30.92 21.37 2.24 6.83 59.7 17.76
Zn 60.04–873.53 192.38 157.00 133.60 2.89 10.79 69.4 69.00
As 0.93–36.45 8.81 7.60 5.31 2.51 9.14 60.3 9.33
Cd 0.05–1.90 0.53 0.34 0.52 2.41 7.86 72.0 0.167
Pb 29.18–166.93 63.15 58.73 21.96 1.89 5.46 34.8 25.61
CV coefficient of variation, nd no data is available

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extrinsic factors such as human activities, automobile of most of the anthropogenic metals show significantly
exhausts, and deposition of aerosols. increased concentrations compared to the rest of the soils
studied. The spatial distribution patterns of Co and V were
Spatial distribution of heavy metal concentrations distinctly different from the Cd, Cr, Ni, Pb, and Zn. Two
relatively large concentrations or hot spots of Co and V were
Geostatistics was applied in investigating and mapping soil found. One is in the southeastern part of the city, and the
heavy metals (Shi and Li 2006). Semivariogram calculation other is in the southwestern part of the city, which may be
was conducted and experimental semivariogram of soil attributed to the input from natural sources. As concentra-
heavy metal contents could be fitted with a spherical model tions were fairly uniformly distributed, and different rock
(Mn, Cu, Zn, Cd, and Zn), exponential model (Cr, V, Ni), types or a mixed source can explain larger variations within
and linear model (As). Semivariogram models and the studied area. Cu displays a different spatial distribution
parameters, including nugget value (C0), sill (C0 ? C), pattern from the other anthropogenic metals and has an
range (R) and coefficients of determination (R2), are shown especially high concentration in the northern edge part of the
in Table 3. The values of R2 showed that the semivario- city and old urban area, probably implying the existence of a
gram models gave good descriptions of spatial structure of different polluting source. Field surveys indicated that the
soil heavy metals. The ratio of nugget to sill (RNS) can be high Cu concentration in the northern part of the city where a
used to express the extent of spatial autocorrelations of soil grape plantation garden was located is most likely attributed
heavy metal contents. A low RNS (\25%) indicates the to the application of manure and Cu-containing chemicals. It
strong spatial autocorrelations of soil heavy metal contents. is concluded that the spatial variability of soil heavy metals is
If RNS is between 25 and 75%, the variable has moderate a useful visual aid to assess the possible sources of heavy
spatial dependence (Shi and Li 2006). Usually, strong metals and environmental quality evaluation.
spatial dependence of soil properties can be contributed to
intrinsic factors (soil formation factors), and weak spatial Inter-element relationships
dependence can be contributed to extrinsic factors. The
RNS of ten heavy metals varied from 7 to 64%. The RNS Inter-element relations can provide information on heavy
of Cu, Zn, As, and Pb, ranged from 35 to 50%, have metal sources and pathways (Imperato et al. 2003). The
moderate spatial dependence, indicating that anthropogenic correlation coefficient matrixes between heavy metals are
factors changed their spatial correlation. The RNS of Co, presented in Table 4. The Cd, Cu, Pb, and Zn were sig-
V, and Mn (\15%) showed that these metals have stronger nificantly correlated with each other (p \ 0.01), indicating
spatial dependence due to the effects of natural factors such that they may share a common origin. In contrast, V con-
as parent materials and topography. tent was correlated with only Co and Ni (p \ 0.01). Cr and
Figure 2 illustrates the spatial distribution of heavy met- Ni were significantly correlated with all heavy metals
als concentrations in the soils. The maps showed that Cd, Cr, (p \ 0.01) except for As. Element As did not show strong
Ni, Pb and Zn have some similar features. The spatial dis- correlation with other heavy metals, indicating that its
tribution of these metals were characterized by higher con- distribution was not controlled by same factor. These
centrations of heavy metals in heavily populated old urban of results indicated that there existed some original relation-
the city and lower at suburban area with low population ship between heavy metals, and suggested several different
density. One ‘hot spot’ was identified where concentrations possible sources of heavy metals.

Table 3 Semivariogram
Model Nugget Sill C0 ? C Ratio of nugget Range R2
models and fitted parameters for
value C0 to sill (%)C0/(C0 ? C) (km)
heavy metal concentrations in
the urban and suburban soils Cr Exponential 0.329 1.633 20.1 15.2 0.942
Mn Spherical 0.183 1.258 14.5 4.88 0.889
V Exponential 0.154 1.865 8.3 16.32 0.942
Co Exponential 0.163 2.295 7.1 22.77 0.951
Ni Exponential 0.276 1.315 21.0 8.52 0.813
Cu Spherical 0.561 1.535 36.5 13.86 0.792
Zn Spherical 0.408 1.147 35.6 4.47 0.662
As Linear 0.799 1.254 63.7 9.476 0.578
Cd Spherical 0.281 1.312 20.4 6.23 0.857
Pb Spherical 0.616 1.233 50.0 7.19 0.949

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Fig. 2 Spatial distribution


maps of heavy metal
concentrations in the soils

Principal component analysis (Franco-Urı́a et al. 2009; Lee et al. 2006; Li et al. 2009;
Zhang 2006). The results of PCA for the heavy metal
Principal component analysis (PCA) is widely applied to contents in the soils are presented in Tables 5 and 6. All the
assist in the identification of possible sources of pollutants elements were well represented by the first three principal

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Table 4 Correlation coefficient matrix of heavy metals concentrations in the studied soils
Cr Mn V Co Ni Cu Zn As Cd Pb

Cr 1
Mn 0.280** 1
V 0.401** 0.113 1
Co 0.552** 0.505** 0.733** 1
Ni 0.855** 0.313** 0.461** 0.609** 1
Cu 0.483** 0.220* 0.089 0.155 0.509** 1
Zn 0.546** 0.490** 0.082 0.306** 0.486** 0.488** 1
As 0.214* -0.139 0.159 0.073 0.192* 0.144 0.011 1
Cd 0.628** 0.485** 0.133 0.356** 0.604** 0.562** 0.703** 0.186* 1
Pb 0.504** 0.284** 0.060 0.257** 0.419** 0.444** 0.514** 0.036 0.548** 1
* Correlation is significant at the 0.05 level
** Correlation is significant at the 0.01 level

components (PC) with an eigenvalue higher than 1, which showed a greater value in the third component (PC3), and
accounts for over 73% of the total variance. The 43.6% of the mean level of As in soils was comparable to the
total variance was controlled by PC1, showing higher background value (Table 2). It could be concluded that the
loading for Cr, Ni, Cu, Zn, Cd, and Pb, reflecting the parent materials of soils and agricultural activities con-
anthropogenic contamination in the urban soils. Meanwhile trolled As concentration. Previous studies indicated that the
there were significant positive correlations between their anthropogenic sources of heavy metals could be generally
levels in urban soils (Table 2), which imply that these classified into three categories: ‘urban elements’, ‘natural
heavy metals in the soils may originate from similar pol- elements’ and elements of a mix origin (Afshin et al. 2009;
lution sources. PC2 (18.0% of total variance) accounts for Facchinelli et al. 2001; Imperato et al. 2003). Similar
high contribution of V and Co, reflecting the input of studies have revealed that metal contamination in urban
parent materials. Combined with the fact that V and Co has soils is significantly related with industrial production,
highly significant correlation (Table 4), PCA analysis vehicle exhaust, waste disposal, fossil fuel combustion as
suggested that the two metals are probably from similar well as human activities. Because there is not larger
sources. PC3 with a variance loading of 11.8% was dom- industry in the studied city, traffic emissions and other
inated by the loading As. human activities may be a common source governing the
In the case of Cu, this metal displayed a combined distribution of Cd, Cu, Pb, and Zn in soils.
relationship with PC1 and PC3, suggesting that this metal
has a combined origin. Taking into the spatial distribution Cluster analysis
of metal (Fig. 2), the enrichment of Cu in the suburban
soils may be related with the application of commercial The CA results for the heavy metal contents in the studied
fertilizers, manure, and Cu-contained agrochemicals. As soils are illustrated in Fig. 3. In general, the results of CA
agree very well with those of PCA analysis. Three distinct
clusters are observed from the dendrograms for the metals
Table 5 Eigenvalue and contribution principal component analysis
in soils. Cluster I contained Cd, Cu, Pb, and Zn, All these
Component 1 2 3 4 5 6 7 elements show high mean concentrations, compared with
Total 4.4 1.8 1.2 0.7 0.5 0.5 0.4
the background values in the studied area. This group of
elements has had previously been interpreted as anthro-
% of variance 43.6 18.0 11.8 7.1 5.5 5.1 3.6
pogenic metals. Cluster II consisted of Cr and Ni. It was
Cumulative (%) 43.6 61.6 73.4 80.5 86.0 91.1 94.7
observed, however, that Cluster I and II join together at a

Table 6 Matrix of the principal component analysis loadings of heavy metals in the urban and suburban soils
Component Cr Mn V Co Ni Cu Zn As Cd Pb

PC1 0.859 0.569 0.426 0.665 0.84 0.625 0.743 0.206 0.788 0.605
PC2 0.133 -0.106 0.802 0.617 0.259 -0.339 -0.386 0.251 -0.387 -0.449
PC3 0.152 -0.611 -0.018 -0.286 0.088 0.308 -0.122 0.76 0.055 0.065

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processes of heavy metals in soils (Franco-Urı́a et al. 2009;


Boruvka et al. 2005; Imperato et al. 2003). The basic
physical and chemical properties of soils were shown in
Table 1. Soil pH ranged from strong acidity (3.0) to strong
alkalinity (9.7). Mean organic matter was 30.0 g/kg and
varied between 1.2 and 110.7 g/kg. The mean clay content
was 15.6% and varied between 1.8 and 45.4% and the
mean sand was 56.3% and varied between 12.2 and 82.2%.
The mean total N and P are 2.1 and 710.1 g/kg,
respectively.
A Pearson’s correlation analysis had been applied to
analyze the relationships between these soil parameters and
Fig. 3 Dendrogram derived from the cluster analysis of heavy metal the heavy metal contents in the studied soils. The results
concentrations in the studied soils
were shown in Table 7. The results indicated that pH had
relatively higher level, implying perhaps common source. highly significant positive correlation with the contents of
Cluster III contained V, Co, Mn, and As. However, As Cr, Mn, V, Co, Ni, Zn, Cd, and Pb; and no significant
element was obviously separated from the V, Co, and Mn correlation with Cu. Organic matter was correlated posi-
elements in CA. tively (p \ 0.01) with Cr, Ni, Cu, Cd, Zn, and Pb. Clay was
Based on PCA and CA results, three main sources can negatively correlated with contents of Cr, Mn, Ni, Zn, Cd,
be identified: (1) Cd, Cr, Cu, Ni, Pb, and Zn, comprised the and Zn. Sand was positively correlated with Cr, Mn, Ni,
first factor extracted by PCA, are mainly derived from Zn, Cd, and Pb (p \ 0.01). The correlation analysis
human activities and traffic sources in the course of between metals and soil properties indicated that heavy
urbanization; (2) Co, V, Mn, and As, obviously separated metals, which were mostly due to anthropogenic sources
from the other elements in CA, are mainly originate from (Cr, Ni, Zn, Cd, and Pb) had significant correlation with
the soil parent materials; (3) Cu and As, separated from the soil pH, organic matter, and sand contents. These anthro-
other metals in same cluster, has an mixed source. The pogenic metals were negatively correlated with clay con-
results suggested again that Cr, Ni, Cd, Cu, Pb, and Zn tent in the soils. These results were in agreement with the
were mainly controlled by anthropogenic sources, while V, previous findings by Lu et al. (2004) who found that
Co, Mn and As had natural sources. Overall, clustering anthropogenic heavy metals were significantly positively
analysis gave similar results, enabling the identification of corrected with sand content, and negatively with clay
three different sources of heavy metals in the soils. content in the urban soils of Nanjing.
On the contrary, heavy metals (Co and V) came from
Relationships with soil properties natural sources and did not present any correlation with
sand content, organic matter, and total P contents. No
It was well known that a number of physical and chemical significant correlation between As content and soil prop-
properties of soils affected mobilization–immobilization erties was also observed for the studied soils. Specifically,

Table 7 Correlation coefficients matrix between heavy metal concentrations and soil properties in the studied soils
Sand Silt Clay pH OM TN TP

Cr 0.250** -0.213** -0.222** 0.383** 0.403** 0.250** 0.115


Mn 0.278** -0.178* -0.366** 0.522** -0.059 -0.236** -0.033
V -0.053 0.046 0.046 0.216** -0.063 -0.203* -0.008
Co 0.082 -0.028 -0.158* 0.341** -0.084 -0.241** 0.004
Ni 0.271** -0.170** -0.364** 0.369** 0.301** 0.152* 0.197*
Cu 0.119 -0.086 -0.136 0.057 0.551** 0.348** 0.123
Zn 0.483** -0.450** -0.349** 0.398** 0.522** 0.177* 0.081
As 0.037 -0.010 -0.077 0.160* -0.027 -0.132 -0.073
Cd 0.482** -0.436** -0.376** 0.481** 0.412** 0.061 0.038
Pb 0.21** -0.159** -0.227** 0.307** 0.517** 0.241* 0.061
* Correlation is significant at the 0.05 level
** Correlation is significant at the 0.01 level

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1928 Environ Earth Sci (2011) 64:1921–1929

organic matter and total N seem to play an important role Acknowledgments This project was supported by the National Key
in Cu accumulation. This may indicated a common origin Technologies R&D Program of China (2008BADA7B06) and Science
and Technology Department of Zhejiang Province (2007C23057).
of Cu and organic matter and nitrogen due to the applica- Opinions in the paper do not constitute an endorsement or approval by
tion of manure. the funding agencies and only reflect the personal research views of
the authors.

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