Environmental Pollution 278 (2021) 116911

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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Heavy metal contamination risk assessment and correlation analysis

of heavy metal contents in soil and crops*
Mingtao Xiang a, Yan Li a, *, Jiayu Yang a, Kaige Lei a, Yi Li a, Feng Li b, Daofu Zheng c,
Xiaoqian Fang a, Yu Cao a
a
Institute of Land Science and Property, School of Public Affairs, Zhejiang University, Hangzhou, 310058, China
b
College of Materials and Environmental Engineering, Hangzhou Dianzi University, Hangzhou, 310018, China
c
Yueqing Branch of Wenzhou Ecological Environment Bureau, Wenzhou, 325600, China

a r t i c l e i n f o a b s t r a c t

Article history: Heavy metal pollution is a notable threat to agricultural production. Soil heavy metal pollution can cause
Received 8 December 2020 potential ecological risk (ERI), and crop heavy metal pollution can cause human health risk (HRI).
Received in revised form However, most previous studies partially focused on heavy metal pollution in soil or crop but often
20 February 2021
neglected the relationship between them. Actually, soil heavy metal can pollute crops to some extent,
Accepted 5 March 2021
Available online 10 March 2021
while not all heavy metal pollution in crops comes from soil. The inner relationship of pollution risk in
soil-crop system is worth attention. In this study, we selected Ningbo as the study region and used
sample data to assess both soil and crop heavy metal risks, in order to explore the differences between
Keywords:
Agricultural pollution
heavy metal contamination risks in soil and crops as well as the relationships between heavy metal
Ecological risk contents in soil and crops. Our results showed that Hg was the most polluted heavy metal in soil, which
Health risk led to the highest ecological risk in Jiangbei (Comprehensive ERI ¼ 567) with the maximum ERI of Hg
Spatial differentiation (430). However, As in crops contributed the most to health risk and caused the highest health risk in
Pollution risk control Fenghua (HRI ¼ 10) with the largest contribution of 64.5%. Such differences of pollution risk assessment
indicated that the contents of the same heavy metal were inconsistent in soil and crops. Our results
further showed that the heavy metals in soil had the greatest influence on Zn in crops. Pb and Cr in soil
had synergistic effects on the crop absorption of Zn, whereas As, Hg and Cu played antagonistic roles in
the crop absorption of Zn. Our study confirms that heavy metals in soil would variously influence heavy
metals in crops and the interaction of heavy metals is very important for pollution risk control, which
have been largely ignored yet.
© 2021 Elsevier Ltd. All rights reserved.

1. Introduction communique of soil pollution survey in 2014, the over-standard

Heavy metal pollution causes a noteworthy threat in agricul-
tural fields. For one thing, soil heavy metal pollution is becoming an
increasingly severe eco-environmental problem. In the past half
century, the global environment have received more than 0.03
million tons of Cr and 0.8 million tons of Pb that have mainly
accumulated in soil and led to serious heavy metal pollution (Yang
et al., 2018). The soil heavy metal pollution is even in more urgent
need of attention in China. According to China’s national
*
This paper has been recommended for acceptance by Philip N. Smith.
* Corresponding author. School of Public Affairs, Zhejiang University, Hangzhou,
310058, China.
E-mail address: liyan522@zju.edu.cn (Y. Li).
rate of soil heavy metal was 16.1% (Ministry of Environmental
Protection of China, 2014a). Cd pollution was the most serious,
followed by Hg pollution (Meng et al., 2018). In general, southeast
China were more heavily polluted than northwest China, and spe-
cifically heavy metal pollution in industrial regions was more
heavily than agricultural regions (Yang et al., 2018). Heavy metal
pollution in soil can cause potential ecological risk. Particularly, Cd
and Hg were found to pose the highest potential ecological risks
(Zhang et al., 2018; Zhao et al., 2019). For another, crop heavy metal
pollution is universal and crop cultivation on polluted agricultural
land is being carried out throughout the world (Sharma and Nagpal,
2020). In Northern Ethiopia, vegetables that grew near Ginfel river
accumulated large amounts of heavy metals (Gebrekidan et al.,
2013). In India, five out of ten vegetables grown in sewage water
irrigated fields showed massive accumulation of heavy metals

https://doi.org/10.1016/j.envpol.2021.116911
0269-7491/© 2021 Elsevier Ltd. All rights reserved.
M. Xiang, Y. Li, J. Yang et al.
(Tiwari et al., 2011). In Bangladesh, the contents of Cr, Ni, As, Cd and
Pb in foods around the industrial areas were higher than the
maximum standards (Islam et al., 2020). In active mining areas of
China, half of local rice exceeded the allowable limit of Cd specified
by the Chinese Grain Security Standards, and the quantities of “Cd
rice” were not in the minority (Du et al., 2013). Heavy metal
pollution in crops causes human health risk mainly through the
ingestion of rice (Wang et al., 2020) and vegetables (Zhou et al.,
2016). Food polluted by heavy metals poses significant health
risks to local residents, such as Itai-Itai disease (Hu et al., 2016) and
even cancer (Upadhyay et al., 2019).
Heavy metals in polluted soil can lead to crop pollution through
root accumulation, and heavy metal contents in soil and crops have
certain relationships. As could be transferred from highly polluted
agricultural soil to different tissues of wheat and accumulated in
wheat (Karimyan et al., 2020). Cd could be transferred from Cd-
polluted soil to rice, and lower pH as well as higher soil Cd con-
centration contributed to Cd accumulation in crops (Li et al., 2019).
It was significant that heavy metals could transfer from soil to
vegetables, but the movements automatically stopped while
reaching near the edible part of vegetables (Ahmad and Ansari,
2020). Furthermore, a certain crop shows different capacities of
absorbing different heavy metals in soil, leading to various degrees
of heavy metal accumulation. The ability of heavy metal accumu-
lation in rice varied as follows: Cd > Zn > Cu > As (Liu, S. et al.,
2020). Vegetables generally had the strongest ability to absorb
and accumulate Cd in the soil. However, there were also findings
that a few vegetables (e.g. cabbage, tomato and lettuce) had a
higher capacity for absorbing and accumulating Zn than Cd (Jan
et al., 2010). Thus it can be seen that not all heavy metal pollu-
tion in crops comes from soil (Zhang et al., 2020). Take atmospheric
deposition as an illustration. It has a dual effect on crops (Feng et al.,
2019). Firstly, heavy metals in the atmosphere enter the crop
through stomates of leaves and accumulate in cells, which pollutes
crops directly. Secondly, heavy metal particles fall to the soil to
accumulate and enter the crop through roots, which polluted crops
indirectly. Moreover, sewage irrigation is another source of crop
heavy metal pollution (Meng et al., 2016).
Some previous studies have taken heavy metals in both soil and
Fig. 1. Location of the study region and spatial distribution of heavy metal samples.
2
Environmental Pollution 278 (2021) 116911
crop into account, while less considering the in-between relation-
ship. For example, Pan et al. (2016) assessed potential ecological
risk and human health risk caused by soil heavy metals rather than
consider crops let alone their relationship. Zheng et al. (2020)
assessed human health risks caused by heavy metals in both soil
and crops, but still not take their relationship into account. Actually,
complex interactive relationships exist among heavy metals,
including synergistic effect and antagonistic effect. Zn showed a
synergistic effect on the absorption of Pb and Cd in wheat, while
showing an antagonistic effect on As absorption (Liu, Y. et al.,
2020a). For maize, Ni in soil inhibited the absorption of Cu and
Cd in roots, whereas: Cu and Ni in soil promoted the absorption of
Cu and Pb in stems; Cu, Pb and Ni in soil promoted the absorption of
Cu, Pb and Ni in leaves; Cr and Pb in soil promoted the enrichment
of Mn in grains (Huang and Gui, 2018). Although a few attempts
have been carried out to explore the interactions among heavy
metals in soil and crops, they focused on specific heavy metal
combinations of given crops. These existing studies were domi-
nated by field experiments while lacking studies on the regional
scale. In practice, multiple heavy metals concurrently exist in soil,
which necessarily affect each other during the process of crop ab-
sorption of heavy metals (Hu et al., 2020a). Therefore, the re-
lationships among multiple typical heavy metals in soil-crop
system on the regional scale might not have been fully explored.
In this study, we collected 1815 samples containing soil and crop
information and selected an industrial city in Southeast China as a
case study area, in order to better understand heavy metal pollu-
tion in soil-crop system. The specific aims are to explore: (1) what
are the differences between heavy metal contamination risks in soil
and crops? and (2) what are the relationships among heavy metal
contents in soil and crops?
2. Materials and methods
2.1. Study region
We select Ningbo (Zhejiang Province, Southeast China) as the
study area (Fig. 1). It is an industrial city that is located in the south
of Yangtze River Delta (Liu and Borthwick, 2011). The study area
M. Xiang, Y. Li, J. Yang et al. Environmental Pollution 278 (2021) 116911

belongs to a subtropical region where the climate is mild and hu- Table 1
mid with comfortable temperature and precipitation conditions. The soil environmental quality standard (Si ), the toxicity response parameter (Ti )
and the reference exposure dose (RFD ) of eight heavy metals.
And the fertile soil is mainly derived from alluvial deposits of the
Yangtze River. Due to favorable climatic and edaphic conditions, the Heavy metals Cr Pb Cd Hg As Cu Zn Ni
local agriculture is well-developed, which leads to a large quantity Si 52.9 23.7 0.07 0.086 9.2 17.6 70.6 24.6
of fertilizer and pesticide inputs. In addition, Ningbo is an impor- Ti 2 5 30 40 10 5 1 5
tant industrial base for chemical, machinery, electronic and met- RFD 0.003 0.0035 0.001 0.0003 0.0003 0.04 0.3 0.02

allurgy industries. In recent years, however, on account of the rapid
urban expansion and increased industrial manufacture, the envi-
ronmental pollution, especially heavy metal pollution caused by
industrial wastes, has posed an increasingly serious threat to soil
quality and crop security. Thus it can be seen that both agricultural
and industrial production can cause increasing pollutant inputs
sourced from human activities (Li et al., 2018). Therefore, Ningbo is
a proper study region to assess heavy metal pollution in both soil
and crops.
2.2. Data
Note: There is no unit for Ti , the unit of Si is mg/kg, and the unit of RFD is mg/kg/d.
(Hakanson, (1980)). ERIs of different ranges can be divided into five
grades, i.e. Slight risk (ERI < 40), Mild risk (40  ERI < 80), Moderate
risk (80  ERI < 160), Severe risk (160  ERI < 320) and Extremely
severe risk (ERI  320). Comprehensive ERIs of different ranges can
be divided into four grades, i.e. Slight risk (Comprehensive
ERI < 150), Mild risk (150  Comprehensive ERI < 300), Moderate
risk (300  Comprehensive ERI < 600) and Severe risk
(Comprehensive ERI  600).

A total of 1815 pairs of soil and crop samples were collected

based on systematic grid sampling method (Fig. 1b). For soil sam-
ples, five individual subsamples from five locations within 5 m
were collected and mixed together to make up a representative
one. To acquire more comprehensive information, grid sampling
was extended to increase partial sampling density with the prior
knowledge of local features. The stainless-steel shovel was used to
collect all soil subsamples at a depth of 0e20 cm and the differ-
ential global positioning system (GPS) was used to record their
coordinates. For crop samples, corresponding ones were collected
at the same soil sampling sites at different maturation times during
the harvest season. The total of 1815 crop samples consisted of 932
grain samples, 766 vegetable samples and 117 fruit samples.
According to the agricultural sector standard of the People’s
Republic of China, the contents of eight heavy metals (i.e. Cr, Pb, Cd,
Hg, As, Cu, Zn and Ni) in soil and crop samples were obtained. After
collection, in the lab, crop samples were oven-dried at 105  C for an
hour and then put at 70  C to constant weights. Afterwards, some
crop samples were comminuted with a pulveriser, ground to pass
through 100 meshes with a nylon sieve, and stored in closed
polyethylene bags for further analysis. The total concentrations of
Cr, Pb, As, Cu, Zn and Ni in crop samples were digested by the dry
ashing method and determined using inductively coupled plasma
optical emission spectrometry (ICP-OES 6300, Thermo Fisher Sci-
entific, Waltham, MA, USA). Total Cd and Hg in crops were treated
and determined by the same methods as those in soil. Details for
soil sample pretreatments and other information were introduced
in our previous studies (Xiang et al., 2020) and the Supplementary
Material.
2.3. Methods
2.3.2. Human health risk assessment
Health risk index (HRI) is applied to assess human health risk of
heavy metal ingestion through food with target hazard quotients
method proposed by U.S. Environmental Protection Agency
(USEPA) (USEPA, 2000). It can be calculated as:
FIR  EF  ED  Ccropi
HRIi ¼ (2)
WAB  TA  RFD
Where Ccrop i is the measured concentration of pollutant i in crop,
RFD is the reference exposure dose (Table 1). FIR is the daily inges-
tion of crop (kg/day), and the FIR values of grain, vegetable and fruit
for adults are 0.293, 0.255 and 0.036 (He et al., 2016; Wu et al.,
2015; Xu et al., 2018). EF is the exposure frequency (day/year), ED
is the exposure duration (year), WAB is the average body weight
(kg), TA is the averaging time (day). According to Ministry of
Environmental Protection of China (2014b), the EF , ED and WAB
values are 350, 24 and 56.8, and TA is calculated by ED  EF . When
HRI > 1, heavy metals accumulated in crop can pose a risk to human
health.
2.3.3. Geographical detector
Geographical detector is a good tool for geospatial analysis of
different fields, scales and data types. The differentiation and factor
detector is applied to analyze the spatial differentiation of potential
ecological risk and human health risk of heavy metal pollution. The
specific model is as follows:
Pn
SSW j¼1 nj  s2j
q¼1  ¼1 (3)
SST n  s2

2.3.1. Potential ecological risk assessment Where q is the degree of spatial differentiation, whose value ranges
Ecological risk index (ERI) is applied to analyze pollution level of from 0 to 1. The bigger the q value is, the higher the spatial dif-
soil heavy metals and assess potential ecological risk, which can be ferentiation degree is. SSW is the within sum of squares, SST is the
calculated as: total sum of squares, j is one of subregions, nj and n are the number
of units in subregion j and whole region respectively, s2j and s2 are
X
n X
n
C
Comprehensive ERI ¼ ERIi ¼ ð i  Ti Þ (1) the variance of subregion j and whole region respectively. If the
Si mean risk index value is relatively high while q value is relatively
i¼1 i¼1
small, indicating low spatial differentiation in the study region, it is
Where i is a kind of heavy metal pollutant, ERIi is the ERI of adequate to adopt unified risk management and control measures.
pollutant i, Ci is the measured concentration of pollutant i, Si is the On the contrary, if the mean risk index value is relatively high and q
soil environmental quality standard of pollutant i and takes the soil value is relatively big, indicating high spatial differentiation in the
background values of Zhejiang province as standards (Table 1), Ti is study region, elaborate measures adapting to local conditions are
the toxicity response parameter of pollutant i according to needed.
3
M. Xiang, Y. Li, J. Yang et al.
2.3.4. Rank-size rule
Based on rank-size theory (Zipf, 1949), combining with heavy
metal risk assessment and geographical detector analysis, the risk
level (R) of different subregions can be calculated through the
model:
Pn
Pk
k¼1 P
Rj ¼ (4)
nj
Where k is one of samples, Pk is the risk index of sample k in sub-
region j, P is the mean risk index of whole region, nj is the number
of samples in subregion j. According to the national standard (State
Council of the People’s Republic of China, 2016), the subregions in
the study region can be divided into three grades, i.e. low-risk level
(R < 0:8), moderate-risk level (0:8  R < 1) and high-risk level (R 
1).
2.3.5. Multivariate statistical analysis
2.3.5.1. Partial correlation analysis. Correlation analysis is a statis-
tical approach to quantitatively describe and analyze the degree of
correlation between two or more variables. Simple correlation
analysis is suitable for correlation studies between two variables.
When more than two variables have complex relationships, partial
correlation analysis can only analyze the correlation between two
target variables while eliminating the influence of other variables.
Since the interaction of heavy metals in soil affects crop absorption,
it is suitable to apply partial correlation analysis to explore the
correlativity of a certain heavy metal in both soil and crop, which is
capable of eliminating the influence of other heavy metals. We
hypothesize that x1 is the independent variable, x2 is the control
variable, y is the dependent variable, so the partial correlation co-
efficient (r) of x1 and y is calculated as:
ry1  ry2 r12
r ¼ qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi (5)
ð1  r 2y2 Þð1  r 212 Þ
Where ry1 is the simple correlation coefficient of x1 and y, ry2 is the
simple correlation coefficient of x2 and y, r12 is the simple corre-
lation coefficient of x1 and x2 . If r is positive, there is a positive
correlation between the two variables, indicating the synergistic
effect of corresponding heavy metal in soil and crop. Contrarily, a
negative correlation indicates the antagonistic effect of corre-
sponding heavy metal in soil and crop.
2.3.5.2. Stepwise linear regression analysis. Linear regression anal-
ysis is used to describe the linear relationship between two or more
variables. Since soil quality is affected by multiple independent
variables, the multiple linear regression analysis is adopted and the
equation is:
y ¼ b0 þ b1 x1 þ b2 x2 þ … þ bn xn þ ε (6)
Where y is the dependent variable, x1 ; x2 ; x3 ; …; xn are independent
variables, b0 is the constant, b1 ; b2 ; …; bn are partial regression
coefficients, ε is the random variable.
Stepwise linear regression analysis is chosen to describe the
linear relationship between a crop heavy metal and multiple soil
heavy metals. During the process, F test is applied to check all
variables in the regression equation every time when a new vari-
able is introduced. F value is used to estimate the significance of the
regression equation, i.e. the overall linear relationship between the
dependent variable and all independent variables in the model. If
the F value is not significant and the probability (P value) is greater
than the preset significance level, the variable will be eliminated in
4
Environmental Pollution 278 (2021) 116911
order to guarantee the significant influence of introduced variables.
The introduction and elimination are carried out alternately until
all independent variables in the regression equation have signifi-
cant influence on the dependent variable. When the introduced
variables cannot be eliminated and the new variables cannot be
introduced, the stepwise linear regression process ends. R repre-
sents the goodness of fit to measure the matching degree between
the estimated model and the observed values. The closer the value
is to 1, the better the model fitting degree is. As for the study of the
interaction between variables, the reliability of the overall regres-
sion coefficient and the significance level (P value) of the regression
equation are more important.
3. Results
3.1. Risk assessment of heavy metal pollution in soil
3.1.1. Potential ecological risk of soil heavy metals
The ecological risks of soil heavy metals in the study region were
overall mild except prominent Cd and Hg risks (Fig. 2a). The ERI
values of Cd were generally high, ranging from 72 to 96, with a low
variation. Differently, the ERI values of Hg were pervasively high
with a high variation, whose maximum value peaked at 430 in
Jiangbei. On the contrary, the ERI values of the rest heavy metals
(i.e. Cr, Pb, As, Cu, Zn and Ni) were all lower than 15, indicating the
slight ecological risk caused by single heavy metal as well as a large
area of mild comprehensive ecological risk.
3.1.2. Spatial differentiation of potential ecological risk
The high ERI values of Hg concentrated in the urban area of
Ningbo contributed a lot to the comprehensive ecological risk,
causing moderate risks in Zhenhai, Jiangbei, Haishu and Yinzhou
(Fig. 2a). The spatial differentiation degree (q) acquired based on
geographical detector varied greatly among counties, which indi-
cated the potential ecological risks of different types of soil heavy
metals were significantly different within the study region
(Table 2). The q values of potential ecological risk were between
0.016 and 0.537, and those of soil heavy metals were ranked in the
descending order as Hg > Pb > As > Cr > Zn > Cu > Ni > Cd.
Obviously, Hg had the maximal q value among eight heavy metals,
indicating distinct spatial differentiation characteristics. Since the
mean index values of potential ecological risk of Hg were notably
high, it is urgent to carry out elaborate measures adapting to local
conditions. Contrarily, Cd had the minimal q value. Although the
mean index values of potential ecological risk of Cd were high, the
unapparent spatial differentiation characteristics make it possible
to adopt unified risk management and control measures within the
study region.
3.1.3. Potential ecological risk levels
The urban area of Ningbo had the high-risk level, whereas most
of other areas had the moderate-risk level (Fig. 3). The urban area
was the high-risk level area for Hg while the surroundings were all
low-risk level areas for Hg, which was highly consistent with the
spatial distribution of high ecological risk of Hg (Fig. 2a). Cu had the
same spatial aggregation with Hg but different risk levels. However,
Cr and Zn had the completely same spatial aggregation as well as
risk levels, e.g., the whole urban area and Xiangshan were in a high-
risk level. And the east part of the study region was high-risk level
areas for both As and Ni. Fenghua was the only low-risk level area
for As and Cixi was the only low-risk level area for Pb. With respect
to Yuyao, Cd was the only heavy metal that should be paid high
attention to.
M. Xiang, Y. Li, J. Yang et al. Environmental Pollution 278 (2021) 116911

Fig. 2. Potential ecological risk (a) of soil heavy metals and human health risk (b) of crop heavy metals.

Table 2 (Table 3). The q values of human health risk were between 0.061
Mean index values and spatial differentiation degrees of potential ecological risk of and 0.299, and those of crop heavy metals were ranked in the
soil heavy metals.
descending order as Zn > Cr > Ni > Hg > Cu > As > Cd > Pb.
County Cr Pb Cd Hg As Cu Zn Ni Obviously, As had a relatively smaller q value among eight heavy
Beilun 2.66 8.79 89.9 97.5 8.06 10.1 1.61 6.19 metals, indicating inconspicuous spatial differentiation character-
Cixi 2.55 6.19 80.4 66.0 7.64 9.83 1.43 6.54 istics. Though the mean index values of human health risk of As
Fenghua 2.30 9.92 81.0 103 5.58 8.61 1.52 5.15 were particularly high, it is feasible to adopt unified risk manage-
Haishu 2.88 11.7 85.6 315 6.87 11.2 1.72 6.16
ment and control measures within the study region. Inversely, Cr
Jiangbei 3.25 12.3 92.0 430 8.53 12.8 1.72 6.94
Ninghai 2.29 9.25 81.7 48.1 6.92 9.42 1.57 5.94 had a relatively larger q value. Owing to the high mean index values
Xiangshan 2.85 8.45 71.8 45.4 10.8 9.82 1.65 7.41 of human health risk of Cr, the apparent spatial differentiation
Yinzhou 3.12 10.5 95.6 168 7.72 11.5 1.81 6.46 characteristics make it exigent to carry out elaborate measures
Yuyao 2.37 7.29 88.1 96.2 6.67 9.42 1.39 5.47 adapting to local conditions.
Zhenhai 3.29 9.90 87.7 196 9.64 11.5 1.92 7.50
q 0.104 0.357 0.016 0.537 0.177 0.069 0.096 0.040
3.2.3. Human health risk levels
The human health risk level in the south part of Ningbo was
3.2. Risk assessment of heavy metal pollution in crops higher than that in the north part (Fig. 4). For all types of crop heavy
metals, Fenghua was the only high-risk level area and Beilun was
3.2.1. Human health risk of crop heavy metals the only low-risk level area. The northwest part of the study region
The health risk of crop heavy metals in the study region were all was the high-risk level area for As while the surroundings were all
moderate except Beilun, due to the conspicuous contributions of As low-risk level areas for As. Cr, Zn and Ni had the similar spatial
(Fig. 2b). As contributed the most to human health risk with aggregation and risk levels, e.g., the south parts were in a high-risk
contribution rates ranging from 29.2% to 75.6%, which was followed level and adjacent to several moderate-risk level areas. With regard
by Cr with contribution rates varying between 6.2% and 35.8%. In to Pb, Hg and Cu, three levels of health risk areas were relatively
contrast, the contribution rates of health risks of the rest heavy evenly distributed. Among all counties, Fenghua, Yinzhou and
metals (i.e. Pb, Cd, Hg, Cu, Zn and Ni) were all lower than 15%. The Jiangbei were high-risk level areas, and Haishu was the only
contributions of Cd were almost lower than 10%. And Hg made the moderate-risk level area. Besides, most of the study region was
least contributions to human health risk, which were even all less overwhelming high-risk level areas for Cd except that Cixi and
than 2%. Beilun were low-risk level areas and Zhenhai was the moderate-
risk level area.

3.2.2. Spatial differentiation of human health risk
In terms of the whole study region, Beilun was the only county
that had mild health risk, where As, Cr and Cd all made great
contributions (over 15%) to human health risk (Fig. 2b). The spatial
differentiation degree (q) acquired based on geographical detector
differed greatly among counties, indicating diverse human health
risks of different types of crop heavy metals within the study region
5
3.3. Relationship between heavy metal contents in soil and crops
Hg and Cd had the highest ecological risk in soil but contributed
little to human health risk, whereas As and Cr contributed the most
to human health risk but had low ecological risk in soil. Moreover,
all the eight heavy metals had spatially different risk levels. Espe-
cially, the ecological risk levels and health risk levels of As in all
M. Xiang, Y. Li, J. Yang et al. Environmental Pollution 278 (2021) 116911

Fig. 3. Potential ecological risk level of soil heavy metals in different counties based on rank-size rule method.

Table 3 in crops and soil (Table 4). Overall, Zn in crops was the most
Mean index values and spatial differentiation degrees of human health risk of crop affected by heavy metals in soil, followed by Cr and Pb. Specifically,
heavy metals.
the Cr content in crops was significantly positively correlated with
County Cr Pb Cd Hg As Cu Zn Ni both Pb content and Hg content in soil, which indicated that Pb and
Beilun 0.07 0.02 0.08 0.01 0.14 0.06 0.06 0.01 Hg in soil could promote the absorption of Cr by crops. And the Cr
Cixi 0.27 0.08 0.09 0.01 0.35 0.16 0.09 0.03 content in crops had an extremely significant negative correlation
Fenghua 2.15 0.08 0.37 0.06 6.56 0.36 0.40 0.20 with the As content in soil. Moreover, the Cd content in crops was
Haishu 0.55 0.07 0.25 0.03 1.35 0.22 0.26 0.09
extremely significantly negatively correlated with the Cd content in
Jiangbei 0.70 0.16 0.25 0.10 6.05 0.32 0.33 0.09
Ninghai 0.76 0.07 0.24 0.02 1.59 0.19 0.24 0.11 soil, indicating that the Cd in soil might not be the main source of
Xiangshan 0.98 0.03 0.27 0.02 0.80 0.24 0.29 0.11 Cd in crops. Differently, the Pb content in crops had extremely
Yinzhou 0.66 0.08 0.24 0.04 2.04 0.27 0.28 0.12 significant positive correlations with both Hg content and As con-
Yuyao 0.27 0.04 0.23 0.03 3.20 0.26 0.20 0.07
tent in soil, with correlation coefficients of 0.108 and 0.037
Zhenhai 0.25 0.06 0.19 0.04 1.60 0.19 0.18 0.05
q 0.262 0.061 0.074 0.139 0.097 0.138 0.299 0.230
respectively. The Cu content in crops was extremely significantly
positively correlated with Cu in soil (r ¼ 0:072) but significantly
negatively correlated with Cr in soil (r ¼  0:057). Besides, the Zn
content in crops had extremely significant positive correlations
counties were totally different. It can be seen that the soil pollution
with Cr and Pb contents in soil, whereas it had significant negative
risk and crop pollution risk caused by heavy metals are inconsis-
correlations with Hg, As and Cu contents in soil. With regard to Hg,
tent, which may be attributed to numerous external influences
As and Ni in crops, all of their contents showed no significant
such as climate, acid rain, tillage and fertilization. The heavy metal
correlations with the contents of eight heavy metals in soil.
contents in crops depend on the heavy metal contents in soil and
the absorption capacities of crops (Hu et al., 2020b), which are also
closely related with soil properties like soil organic matter (Wan
3.3.2. Regression of heavy metal contents in soil and crops
et al., 2018), pH (Shen et al., 2020) and heavy metal morphology
At the significance level, all the heavy metals except Hg in crops
(Liu, Y. et al., 2020b). Except for the secondary pathway of uptake by
had linear regression relationships with heavy metals in soil to
leaves, the root system is the uppermost pathway for crop ab-
varying degrees (Table 5). Overall, the synergistic and antagonistic
sorption of heavy metals. Therefore, the heavy metal contents in
effects of soil heavy metals on crop heavy metals mainly focused on
crops are ultimately determined by soil.
Pb, Hg, As and Cu. To be specific, Pb in soil had synergistic effects on
the crop absorption of six heavy metals (i.e. Cr, Cd, As, Cu, Zn and
3.3.1. Correlation of heavy metal contents in soil and crops Ni), while As in soil had antagonistic effects. Hg in soil played a
There existed strong correlations between heavy metal contents synergistic role in the crop absorption of Cr, while it played
6
M. Xiang, Y. Li, J. Yang et al. Environmental Pollution 278 (2021) 116911

Fig. 4. Human health risk level of crop heavy metals in different counties based on rank-size rule method.

Table 4
Partial correlations between heavy metal contents in crops and soil.

Heavy metals Crsoil Pbsoil Cdsoil Hgsoil Assoil Cusoil Znsoil Nisoil

Crcrop 0.036 0.074** 0.037 0.060* 0.073** 0.008 0.027 0.001

Pbcrop 0.042 0.048 0.005 0.108** 0.037** 0.037 0.025 0.022
Cdcrop 0.001 0.042 0.132** 0.033 0.017 0.028 0.009 0.007
Hgcrop 0.009 0.010 0.010 0.018 0.004 0.008 0.008 0.004
Ascrop 0.033 0.001 0.019 0.003 0.024 0.021 0.027 0.019
Cucrop 0.057* 0.009 0.012 0.023 0.025 0.072** 0.049 0.003
Zncrop 0.117** 0.082** 0.004 0.059* 0.073** 0.083** 0.035 0.020
Nicrop 0.011 0.044 0.012 0.041 0.038 0.002 0.026 0.014

Note: * represents a bilaterally significant correlation at 5% level, i.e., P < 0.05. ** represents a bilaterally significant correlation at 1% level, i.e., P < 0.01.

Table 5
Stepwise linear regressions between heavy metal contents in crops and soil.

Heavy metals Regression equations F values Adjusted R2 P values

Cr Crcrop ¼ 0:31Pbsoil þ 0:20Hgsoil  0:16Assoil  0:08Cusoil þ 0:45 38.4 0.09 0.00

Pb Pbcrop ¼ 0:10Cusoil þ 0:05 16.1 0.01 0.00
Cd Cdcrop ¼ 0:33Pbsoil  0:14Assoil  0:13Hgsoil  0:10Cusoil þ 0:08Crsoil  0:02Cdsoil þ 0:01 32.3 0.11 0.00
As Ascrop ¼ 0:13Pbsoil  0:08Assoil þ 0:13 18.5 0.02 0.00
Cu Cucrop ¼ 0:23Pbsoil  0:08Hgsoil  0:06Assoil þ 1:40 21.6 0.04 0.00
Zn Zncrop ¼ 0:48Pbsoil  0:20Assoil þ 0:17Crsoil  0:15Hgsoil  0:12Cusoil þ 5:59 72.2 0.18 0.00
Ni Nicrop ¼ 0:30Pbsoil  0:16Hgsoil  0:10Assoil  0:09Cusoil þ 0:32 28.7 0.07 0.00

antagonistic roles in the crop absorption of Cd, Cu, Zn and Ni.
Similarly, Cu in soil had a synergistic effect on the crop absorption
of Pb, but had antagonistic effects on the crop absorption of Cr, Cd,
Zn and Ni. In addition, the absorption of Cd and Zn by crops were
affected by many heavy metals in soil. Apart from the aforesaid four
heavy metals, the crop absorption of Cd and Zn were subject to the
synergistic effects of Cr in soil. It was notable that an extremely
significant negative regression relationship was shown between Cd
contents in crops and soil, indicating that Cd in crops was antago-
nistic to the absorption of the same heavy metal in soil. And the
same case happened to As.

7
M. Xiang, Y. Li, J. Yang et al.
4. Discussion
4.1. Applications of geographical detector and rank-size rule
We applied the geographic detector and rank-size rule to
describe spatial characteristics of heavy metal pollution risks. The
geographic detector has been widely used in environmental (He
et al., 2019), social (Liu et al., 2018) and economic (Wang et al.,
2018) fields. It is a powerful tool for detecting the spatial differ-
entiation characteristics of variables or the consistency between
variables at different scales. Thus, the geographic detector is very
applicable for exploring the spatial differentiation of different
subregions within a certain region. In this study, the new attempt in
the heavy metal pollution field can not only enrich the practical
application field of geographic detector, but also provide supportive
spatial information for the follow-up risk level analysis. In addition,
the rank-size rule is initially used to reflect that the urban devel-
oping scale has fractal properties in a certain space and time (Chen
and Liu, 1999). Some researchers further optimized the theory and
applied the model to other fields, such as geography and economics
(Jiang et al., 2018). Hence, this study extends this method to
ecological environment field. Combining with spatial differentia-
tion results, the rank-size rule can evaluate subregional risk se-
quences based on multiple soil heavy metal points to demonstrate
the comprehensive levels of ecological risk and health risk.
4.2. Human health risk caused by soil heavy metals
As a potentially persistent toxic pollutant, the heavy metal can
chronically exist in the soil due to the incapable biodegradation,
which leads to the accumulation and increase of heavy metals in
crops. The ingestion of heavy metals in crops is actually an indirect
way to damage human health. Apart from that, heavy metals in soil
can directly cause human health risk through three ways, i.e.
inhalation, dermal absorption and soil ingestion (Yeganeh et al.,
2012). It does harm to human health through exposure to ele-
ments (e.g. soil, surface water and food) that are polluted by soil
heavy metals. Such heavy metal pollution in soil can pose both non-
carcinogenic risk and carcinogenic risk to human of all ages. In most
cases, children are more likely to be seriously threatened by heavy
metal pollution than adults (Pan et al., 2018). Therefore, many re-
searchers paid much attention to human health risk caused by soil
heavy metals (Huang et al., 2018; Zhao et al., 2012). In the current
study, such direct human health risk is not taken into consideration.
This is because the amounts of heavy metals into the human body
via soil are all less than 1% of that via crop, and crop ingestion is the
dominant way for the human body to absorb heavy metal (Baghaie
and Aghili, 2019).
4.3. Absorption abilities of soil heavy metals for specific crops
Heavy metals in crops are destined to cause human health risk
through crop absorption and accumulation. However, different
kinds of crops show different abilities of absorbing and accumu-
lating heavy metals in soil (Zheng et al., 2020). In terms of general
crops, the absorption and accumulation abilities of heavy metals
follow the order of tea > grain > vegetable > fruit (Hu et al., 2017).
Differences also exist among vegetables. For instance, the concen-
trations of five common heavy metals (Pb, Cd, Cu, Zn and As) in
various categories of vegetables decrease in the sequence as leafy
vegetables > stalk/root/solanaceous vegetables > legume/melon
vegetables (Zhou et al., 2016). Furthermore, the absorptions and
accumulations of heavy metals differ from species to species even
within the same category of vegetables. Take the leafy vegetable as
an illustration. Though both the spinach and the lettuce belong to
8
Environmental Pollution 278 (2021) 116911
leafy vegetables, the former possesses higher concentrations of
heavy metals (Fe, Zn, Mn, Cu, Pb, Cr and Co) than the latter (Waheed
et al., 2019). To top it all, diverse cultivars of one species present
varying degrees of absorptions and accumulations to a certain
heavy metal (Duan et al., 2017), and harmful heavy metals are
absorbed and accumulated in different parts with various levels for
a certain plant (Karimyan et al., 2020). As a consequence, in order to
better assess human health risk caused by heavy metals in crops, it
is of vital significance to specifically subdivide crops into tea, grain,
vegetable and fruit in future works.
5. Conclusion
We assessed and integrated the potential ecological risk caused
by soil heavy metals and the human health risk caused by crop
heavy metals, in order to explore the relationships among heavy
metals in soil and crops. For one thing, the ecological risks of soil
heavy metals were mostly mild except prominent Hg and Cd risks.
And the high risk of Hg concentrated in the urban area contributed
a lot to the high comprehensive ecological risk. Since Hg in soil had
the maximal spatial differentiation degree (q ¼ 0.537) and notably
high potential ecological risk, it is urgent to carry out elaborate
measures adapting to local conditions. With regard to ecological
risk levels of Hg, the urban area was the high-risk level area while
the surroundings were all low-risk level areas, which was highly
consistent with its spatial distribution of high ecological risk.
Overall, the urban area of Ningbo had the high-risk level of
ecological risk, whereas most of other areas had the moderate-risk
level. For another, the health risk of crop heavy metals were almost
all moderate due to the conspicuous contribution of As (ranging
from 29.2% to 75.6%). Since As in crops had a relatively smaller
spatial differentiation degree (q ¼ 0.097) but particularly high hu-
man health risk, it is feasible to adopt unified risk management and
control measures within the study region. With respect to health
risk levels of As, the northwest part was the high-risk level area
while the surroundings were all low-risk level areas. Overall, the
human health risk level in the south part of Ningbo was higher than
that in the north part. Therefore, the contents of same heavy metal
were inconsistent in soil and crops, indicating different interaction
relationships. Our study showcases that Zn in crops was the most
influenced by heavy metals in soil, followed by Cr and Pb. In terms
of the crop absorption of Zn, Pb and Cr in soil had synergistic effects
while As, Hg and Cu had antagonistic effects. Our study further
implies that the specific types of crops need to be considered in
future pollution risk assessment studies. It further sheds light on
heavy metal pollution studies through detailed crop information.
Credit author statement
Mingtao Xiang: Data curation, Formal analysis, Methodology,
Writing e original draft. Yan Li: Conceptualization, Funding
acquisition, Resources, Writing e review & editing. Jiayu Yang:
Methodology, Software, Data curation. Kaige Lei: Investigation,
Visualization. Yi Li: Validation, Visualization. Feng Li: Software,
Writing e review & editing. Daofu Zheng: Software, Data curation.
Xiaoqian Fang: Supervision, Visualization. Yu Cao: Project admin-
istration, Supervision, Writing e review & editing. All authors
contributed to results interpretation and paper writing.
Declaration of competing interest
The authors declare that they have no known competing
financial interests or personal relationships that could have
appeared to influence the work reported in this paper.
M. Xiang, Y. Li, J. Yang et al.
Acknowledgments
This work is financed by the National Natural Science Founda-
tion of China (41771244), Natural Science Foundation of Zhejiang
Province (LZ21D010002), and the National Key Research and
Development Program of China (2016YFD0201200). The authors
also thank the contributions of the reviewers for this manuscript.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.envpol.2021.116911.
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