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Ecological risk and contamination history of

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Ecological risk and contamination history of heavy

metals in the Andong tidal flat, Hangzhou Bay,
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Aimin Jin, Lin Yang, Xue-Gang Chen, Pei-Sun Loh, Zhanghua Lou, Gang Liu &
Shilei Ji

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flat, Hangzhou Bay, China, Human and Ecological Risk Assessment: An International Journal, DOI:
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HUMAN AND ECOLOGICAL RISK ASSESSMENT
http://dx.doi.org/10.1080/10807039.2016.1263541

Ecological risk and contamination history of heavy metals in the

Andong tidal flat, Hangzhou Bay, China
Aimin Jin, Lin Yang, Xue-Gang Chen, Pei-Sun Loh, Zhanghua Lou, Gang Liu, and Shilei Ji
Ocean College, Zhejiang University, Zhoushan, China

ABSTRACT ARTICLE HISTORY

In this study, we collected two sediment cores (C1 and C2) from the Received 6 October 2016
Andong tidal flat, Hangzhou Bay, and studied the temporal variations Accepted 18 November 2016
of heavy metals in the cores. Vertical distributions of heavy metals KEYWORDS
were almost unchanged in both the cores before 2000. After 2000, Heavy metals; Sediment core;
however, the heavy metal concentrations increased dramatically, Hangzhou Bay; Potential
suggesting that the sediments have been affected by enhanced ecological risk;
human pollution in the recent decade. In the core C1, the sediments Anthropogenic activity
were severely polluted by Pb, moderately to considerably polluted by
Cr and Zn, and low to moderately polluted by other heavy metals. The
core C2 was relatively unpolluted before 2000 and low to moderately
polluted after 2000. Multi-statistical analyses indicated that the core C1
was additionally contaminated by local human activities such as
wastewater discharge and the Hangzhou Bay Bridge. The heavy metals
in the core C2, however, were largely contributed by the Yangtze River
and controlled by sedimentation process. The calculated sedimentary
flux (4–8 g m¡2 a¡1) of heavy metals generally increased with time. It
was closely related to the wastewater discharge in adjacent areas. This
study reconstructed the local heavy metal pollution history and
provides important information for environmental protection and
policy making.

Introduction
Heavy metals may pose negative effects on local environment, natural ecosystems, and
human health ascribed to their toxic and accumulative characteristics (Bryan and Langston
1992; Fu et al. 2014; Hanif et al. 2016; Williams et al. 1994). Sediment is a large reservoir for
heavy metals in estuary zone. When the heavy metals enter water column, part of dissolved
metals can be adsorbed onto suspended particles and precipitate into sediment, while part of
particulate metals can be aggregated and eventually deposited on the bottom floor (Chen
et al. 1996; Hiraizumi et al. 1978). Heavy metals in the coastal sediment could originate
from multiple sources, including industrial and municipal wastewater, wastewater dis-
charged from the mine field, irrigation discharge, local rivers, as well as erosion of rocks and
soils (Dai et al. 2007; Hosono et al. 2011). Sediment gradually accumulates with time, and

CONTACT Zhanghua Lou zhanghualou0621@163.com Ocean College, Zhejiang University, Zhoushan 316021,
China.
Color versions of one or more of the figures in this article can be found online at www.tandfonline.com/bher.
© 2017 Taylor & Francis Group, LLC
2 A. JIN ET AL.

the heavy metals therein were relatively stable in the under layers (Hogarh et al. 2016).
Therefore, the vertical profiles of heavy metals in the sediment can represent the temporal
variations of heavy metals, and consequently, sediment core can be used to trace the local
pollution history of heavy metals (Hogarh et al. 2016; Zahra et al. 2014). Numerous
researchers have investigated the sediment cores from Asian estuaries, e.g., the Pearl River
Estuary in China (Duan et al. 2014), the Masan Bay in Korea (Lim et al. 2012), southwestern
Taiwan (Hung and Hsu 2004), and Manila Bay in Malaysia (Hosono et al. 2010). They found
that the heavy metal contamination in those areas has been dramatically increased in last
decades, ascribed to the enhanced anthropogenic impacts. Consequently, it is important to
study sediment cores from estuary zones to understand the local contamination history as
well as to provide essential information for policy making (Bai et al. 2012; Hosono et al.
2010).
Hangzhou Bay is a funnel-shaped estuary zone in East China. China’s rapid urbanization
and industrialization after the “reform and opening up policy” have resulted in some serious
environmental issues all over China (Wang et al. 2014). The Hangzhou Bay also suffered
greatly from these anthropogenic activities. For instance, the water quality of the Hangzhou
Bay was ranked worse than Grade VI in 2011, which indicated that the water has been
severely contaminated and cannot be used in aquaculture (Ministry of Environmental Protec-
tion of China 2011). Because sediment can serve as both a source and a sink for heavy metals,
the research on the Hangzhou Bay sediment has attracted great attentions. Previous studies
focused on the distribution of heavy metals in the surface sediments of the Hangzhou Bay
(Fang et al. 2016; Liu et al. 2012). They found that the sediments and the heavy metals therein
mainly originated from the Yangtze River and the Qiantang River. In addition, significant
anthropogenic pollution was detected in the surface sediments near the Qiantang River mouth
and the western Hangzhou Bay. Nevertheless, the research on the sediment core of Hangzhou
Bay was rarely reported. Consequently, it is important to collect sediment cores from this area
to study the pollution history of heavy metals and to assess their potential ecological risks.
The Andong tidal flat is located in a hydrodynamic turning point of the Hangzhou Bay.
The sediments at this tidal flat come from both the Yangtze River and the Qiantang River.
Therefore, sediment cores from the Andong tidal flat can be used to reconstruct the local
pollution history of heavy metals, as well as to evaluate the impacts of the Yangtze River and
the Qiantang River on the sedimentation and heavy metal pollution of the Hangzhou Bay.
Few studies have sampled sediment core in this area and have conducted such research. In
this study, we collected two sediment cores from the Andong tidal flat and determined their
vertical profiles of heavy metals. We tried to link the heavy metal contamination with the
economic development of adjacent areas and reconstructed the pollution history of heavy
metals in the past decades. Furthermore, we evaluated the historical environmental pollution
levels and potential ecological risk of heavy metals in the Andong tidal flat.

Geological settings
The Hangzhou Bay is a macro-tidal bay located at the estuary of the Qiantang River. This
funnel-shaped bay covers an area of approximately 8500 km2 (Xie et al. 2010), with a width
varying from 25 km to about 100 km and a length of about 100 km (Xie et al. 2009). The
Qiantang River system annually discharges 444 £ 108 m3 water and 786 £ 104 t sediment
into the Hangzhou Bay (Han 2003). As a comparison, the average water discharge and
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 3

sediment load from the Yangtze River are 925 £ 109 m3 a¡1 and 486 £ 106 t a¡1, respec-
tively. Consequently, both the sedimentation and geochemical characteristics of the Hang-
zhou Bay sediments are dominated by the Yangtze River (Milliman and Meade 1983;
Milliman and Syvitski 1992; Milliman et al. 1985; Williams et al. 1978). As shown in
Figure 1A, the residual current of the Yangtze River travels along the north bank of the
Hangzhou Bay and then turns toward the southeast, due to the hydrodynamic force of the
Qiantang River (Li et al. 1987; Xie et al. 2013; Zou et al. 2009). This pattern is constant
perennially although the current flux may change with seasons.
The Andong tidal flat is one of the sandy tidal flats at the southern bank of the Hangzhou
Bay. It is situated at the turning point where the Qiantang River encounters the Yangtze
River current. Therefore, the sediments at the Andong tidal flat are influenced by both the
Qiantang River and the Yangtze River, as well as the tidal current from the East China Sea.
The Andong tidal flat is an accretion flat (Wang et al. 2008; Wegen and Roelvink 2008) with
a tidal range of 2–8 m and wave amplitude of 1–2.5 m s¡1. In addition, this 300-km2 tidal
flat can be divided into a high, a middle, and a low tidal flat from onshore to offshore
(Figure 1B). The high flat is characterized by fine sediments with black-gray silty clay and
clayey silt, which is densely covered by Spartina alterniflora. The middle flat is occupied by
clayey silt and silt, and Spartina alterniflora is scattered in this area. The low flat consists of
coarse sediments composed of silt and sandy silt, where plants are absent (Li and Xie 1993).

Sampling and methods

Sampling
The sediment cores were collected on October 14 and 15, 2015. The details of the collected
two sediment cores are (Figure 1): C1 from the low tidal flat, depth 130 cm, coordinates

Figure 1. A) The Hangzhou Bay and its hydrodynamic environment and B) the sampling sites at the
Andong tidal flat, located the southern side of the Hangzhou Bay.
4 A. JIN ET AL.

(121
100 1900 E, 30
220 4100 N); C2 from the middle tidal flat, depth 165 cm, coordinates
(121
120 1900 E, 30
220 2600 N). The sampling area will be covered by water with a depth of
<1 m at high tide and no water covering at low tide. The cores were sampled using a gravity
columnar sampler equipped with a polyvinyl chloride (PVC) barrel with a diameter of
60 mm. The sediment cores were preserved at ¡18
C before subsequent analyses.

Sample analyses
210
Pb dating was widely used to estimate the sedimentation rate and to determine the age of
sediment core (Goldberg 1963; Krishnaswamy et al. 1971). It is applicable to the sediments
that are deposited during the last 100–150 years according to the 210Pb half-life of 22.3 years
(Appleby et al. 2003; Jweda and Baskaran 2011). In this study, samples were taken at 10-cm
intervals for the 210Pb measurements. The 210Pb dating was conducted at the Nanjing Insti-
tute of Geography and Limnology, Chinese Academy of Sciences by high-purity germanium
low gamma spectrometer (GWL Series High-Purity Germanium, Coaxial Well Photon
Detector System, AMETEK-AMT ORTEC Co, USA). The accuracy and precision of the test
were controlled by the Chinese National Standard GB/T11743-2013 (radionuclide in the soil
of gamma energy spectrum analysis method).
The samples were taken at 5-cm intervals for the determination of elemental concentrations,
total organic carbon (TOC), and average grain size. The sediment samples were first dried in an
oven at 55
C and were ground with an agate grinder until uniform particles were obtained; then,
they were separated into three parts as duplicate samples. Approximately 0.5 g of dried sediment
sample was weighed and was put into a Teflon digestion vessel. Then, the samples were digested
by nitric acid, hydrochloric acid, and hydrogen peroxide (3:9:2.5) assisted by microwave irradia-
tion. After digestion, the mixture was shaken gently, poured into polyethylene tubes, diluted to
50 mL, and centrifuged prior to the analysis of elemental concentrations. The concentrations of
Al and Fe were measured by an ARL ADVAN’X Intellipower TM 4200 X-ray fluorescence spec-
trometer (XRF, Thermo Fisher, USA). The concentrations of heavy metals (Cr, Co, Ni, Cd, Pb,
Mn, Cu, and Zn) were measured by the Inductively Coupled Plasma-Mass Spectrometry (ICP-
MS, Thermo Fisher Scientific, XSeries II, USA). Hg concentration was determined by an atomic
fluorescence spectrometry (AFS-9130, Beijing Titan Instrument Company, China). Reagent
blanks, duplicate samples, and Chinese National Standard (GBS-04 series) were used for quality
controls. Relative standard errors of the analyses were less than 10%.
The TOC contents of the samples were determined using a vario ISOTOPE cube elemen-
tal analyzer (Elementar, Germany) after removing the inorganic carbon. Sulfanilamide was
used as the standard reference material. The precision was 0.02% for the TOC analysis. The
grain size of the samples was analyzed by a laser particle size analyzer (BT-9300Z, Dandong
Baite Instruments Co. Ltd., China) after H2O2 digestion and (NaPO3)6 dispersion. The aver-
age grain size was reported, and the standard error of the analysis was <2%. The mean grain
size was transformed to Mz according to the following equations (Folk and Folk 1968):

F D ¡ log2 a (1)

Mz D ðF16 C F50 C F84Þ=3 (2)

where Mz (F) and a (mm) are the transformed and original grain size values, respectively.
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 5

F16, F50, and F84 are the grain sizes (F) when the cumulative percentage reaches 16%,
50%, and 84%, respectively.

Statistical analyses
Multi-statistical analyses on the heavy metals were evaluated by SPSS with a version of Win-
dows 21.0. The bivariate correlations were calculated using Pearson correlation coefficients
with a two-tailed test of significance. Principal component analysis (PCA) was used to esti-
mate the sources of heavy metals by extracting the principal components.

Pollution indexes
In this study, four indexes were used to assess the heavy metal contamination in the sedi-
ments from the Andong tidal flat: enrichment factor (EF) (Hernandez et al. 2003), contami-
nation factor (CF) (Savvides et al. 1995), geo-accumulation index (Igeo) (M€
uller 1979), and
potential ecological risk index (RI) (Hakanson 1980).
The chemical compositions of the continental crust were used as the background values
in this study: Cr, 100 mg kg¡1; Cd, 0.20 mg kg¡1; Hg, 0.08 mg kg¡1; Pb, 12.5 mg kg¡1; Co,
25 mg kg¡1; Ni, 75 mg kg¡1; Mn, 950 mg kg¡1; Cu, 55 mg kg¡1; Zn, 70 mg kg¡1; Al, 8.23%;
and Fe, 5.36% (Taylor et al. 1981). The continental crust data represent the natural values
without disturbance by anthropogenic activities. Their use as background values can help to
evaluate the heavy metal contamination caused by human pollution (Deng et al. 2012; Pang
et al. 2015).
The EF is calculated according to the following equation:

ðX=AlÞsample
EF D (3)
ðX=AlÞbackground

where X refers to the concentration of a certain heavy metal in the sample or in the back-
ground value. Al was used as a reference element to calculate the EF values due to its conser-
vative behavior during geochemical processes (Duman et al. 2012; Jain et al. 2005; Loska
et al. 1997; Zhang et al. 2007). EF values 1 indicate no enrichments or depletions of heavy
metals, while EF values >1 imply natural or anthropogenic pollutions.
CF values were obtained by dividing the heavy metal concentrations in the samples with
the background values, which is expressed as:

ðX Þsample
CF D (4)
ðX Þbackground

CF values <1 suggest low contamination of the assessed element, values of 1–3 indicate
moderate contaminations, values of 3–6 demonstrate considerable contamination, and CF
values >6 indicate high contamination.
6 A. JIN ET AL.

The Igeo index was originally defined by M€

uller (1979). The equation can be expressed as:


Cn
Igeo D log2 (5)
1:5Bn

where Cn and Bn are the heavy metal concentrations in the sample and the background,
respectively. The constant 1.5 is used on account of variations of background values caused
by lithogenic effects (Ardini et al. 2010; Zhang et al. 2009). The Igeo index can be classified as
seven classes: Igeo values 0 suggest practically uncontaminated, values of 0 < Igeo  1 indi-
cate unpolluted to moderately polluted, 1 < Igeo  2 represent moderately polluted, 2 < Igeo
 3 suggest moderately to strongly polluted, 3 < Igeo  4 indicate strongly polluted, Igeo val-
ues of 4–5 show strongly to extremely polluted, and values >5 demonstrate an extremely
high contamination.
The potential ecological risk of heavy metals in the samples was evaluated by the ecologi-
cal RI (Hakanson 1980). The RI was calculated as the sum of risk factors of the heavy metals:

i
C
Eir D Tri
£ i (6)
Co
X
n
RI D Eri (7)
iD1

where Eri is the monomial potential ecological risk factor, Tri is the toxic response factor. The
Tri values for Cr, Cd, Hg, Pb, Co, Ni, Mn, Cu, and Zn are 2, 30, 40, 5, 5, 5, 1, 5, and 1, respec-
tively (Hakanson 1980; Xu et al. 2008). C i is the measured concentration and Coi is the back-
ground concentration of the assessed heavy metal (mg kg¡1, dw). The potential ecological
risk of heavy metals can be classified into five classes (Zhang et al. 2012): Eri < 30 and RI <
100 indicate low risk, 30  Eri < 50 and 100  RI < 150 suggest moderate risk, and 50  Eri
< 100 and 150  RI < 200 indicate considerable risk. 100  Eri < 150 and 200  RI < 300
demonstrate very high risk, and disastrous risk when Eri > 150, RI > 300.

Results and discussion

210Pb
dating
210
Pb in sediment can come from either atmospheric precipitation or natural 226Ra decay.
Although Pb is continuously accumulated in sediment due to enhanced anthropogenic
impact, the 210Pb activity is determined by its natural decay over time because the natural
abundance of 210Pb is trace. Therefore, 210Pb dating was widely used to determine the age of
sediments (Putyrskaya et al. 2015; Zalewska et al. 2015). In this study, the 210Pb activity in
both sediment cores increases linearly with decreasing depth, suggesting that 210Pb dating is
feasible. The data fitted well with the widely used constant initial concentration model
(Krishnaswamy et al. 1971; Wang et al. 2016). The calculated sedimentation rates are C1 D
5.03 cm a¡1 (age of the core is 25 years) and C2 D 4.89 cm a¡1 (age of the core is 33 years)
(Figure 2). Considering measurement errors, both sediment cores show sedimentation rates
of about 5 cm a¡1. Therefore, both sediment cores should have experienced comparable sed-
imentation processes.
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 7

Figure 2. Sedimentation rates of core C1 and core C2 calculated from 210Pb dating.

Vertical profiles
The vertical profiles of elemental concentrations in the sediments are depicted in Figures 3
and 4. The raw data can be found in Table S1 (heavy metal concentrations are expressed as
mean values). Both sediment cores show analogous Al and Fe concentrations. In the sedi-
ment core C1, the Al contents ranged from 7.10% to 8.21% (average value 7.64%). While in
the C2 core, the Al concentrations varied from 5.99% to 8.62% (average 7.70%). The Fe con-
tents in the sediment core C1 and C2 were in the range of 2.74–3.24% (average 2.96%), and
2.52–3.83% (average 3.24%), respectively. Because both Fe and Al are major metals in the
sediment cores, it is indicated that the sediment sources for both cores were comparable
(Bao et al. 1992; Ma et al. 2007).
Both sediment cores showed similar vertical distribution patterns of heavy metals. Except
for Hg and Mn in the C1 core and Cd and Hg in the C2 core, which were relatively constant
throughout the vertical profiles, the contents of all the other heavy metals increased with
decreasing depth. Before 2000, these increases were relatively smooth, and almost all the
heavy metals exhibited temporarily constant contents. After 2000, however, the heavy metal
concentrations increased dramatically with decreasing depth. Therefore, the heavy metal
contamination in the sediments was significantly intensified in the recent decade. The
enhanced pollution was probably ascribed to anthropogenic activities accompanied by fast
economic development (Yuan et al. 2004), concerning that the natural conditions of the
Hangzhou Bay were relatively unchanged. After 2000, the areas surrounding the Hangzhou
Bay experienced rapid urbanization and economic development. Many electronic and chem-
ical factories were constructed near the Andong tidal flat and the coastal zone of Hangzhou
Bay. The possible direct discharge of industrial and municipal wastes polluted the Qiantang
River and the Yangtze River, and the heavy metals therein were partly accumulated in the
sediments through sedimentation processes (Chen et al. 2000).
Accompanied with the heavy metals, the TOC and Mz of both cores also generally
increased with decreasing depth. The TOC contents of core C1 and C2 were in the range
of 0.10–0.66% (average 0.36%) and 0.18–0.66% (average 0.44%), respectively. The Mz
8 A. JIN ET AL.

Figure 3. Vertical profiles of metals, total organic carbon (TOC), and mean grain size (Mz) in the sediment
core C1 from the Andong tidal flat, Hangzhou Bay. Units: Fe, Al and TOC, %, Mz: F, all the other elements:
mg kg-1.

values of the core C1 fall in the range of 4.84–5.27 F (average value 5.05 F), while the
core C2 exhibited Mz values of 4.92–7.01 F (average value 5.70 F). It is indicated that
both sediment cores showed analogous TOC values, and the core C2 presented slightly
smaller grain sizes. In addition, the core C1 showed larger temporal variations of TOC
and Mz values, suggesting that the core C1 received higher disturbance from anthropo-
genic activities.
Co, Ni, Mn, Cu, and Zn in both the sediment cores suddenly decreased in contents at
2003–2005, together with the declined Al and Fe concentrations. All these metals were
closely related to lithogeochemical processes (Zhang et al. 2014), and therefore, these
decreases should be largely ascribed to the construction of the Hangzhou Bay Bridge, which
is located just to the east side of the Andong tidal flat. The construction of this bridge began
in 2003 and completed in 2007. Presumably, the building blocks such as piers and box gird-
ers had significantly affected the hydrodynamic and sedimentation processes. As a result,
the heavy metal input into the studied area was reduced. This hypothesis can be verified by
the sudden decrease of Mz since 2003, indicating that the grain size of the sediments
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 9

Figure 4. Vertical distributions of metals, total organic carbon (TOC), and mean grain size (Mz) in the sedi-
ment core C2 from the Andong tidal flat, Hangzhou Bay. Units: Fe, Al and TOC, %, Mz: F, all the other ele-
ments: mg kg-1.

increased since the construction of the bridge. It is proposed that the Hangzhou Bay Bridge
declined the input of fine-grained particles into the Andong tidal flat, while sediment with
smaller grain size usually carries higher heavy metal concentrations because of its larger sur-
face and higher affinity for metals (Adiyiah et al. 2014). After the completion of the bridge
at 2007, the Al and Fe contents in the core C1 continued to decrease, while the Mz values
maintained at about 5.01 F. It is implied that the sedimentation process at C1 was still influ-
enced by the bridge, which restricted the input of fine-grained particles into this area. The
heavy metal contents in the core C1, however, constantly increased with decreasing depth
after 2007. It is proposed that the heavy metal contamination was severely enhanced
although the Hangzhou Bay Bridge reduced the input of fine-grained sediments. Therefore,
the heavy metals in the core C1 may be greatly influenced by anthropogenic pollution after
sedimentation (Han et al. 2002).
Another significant decrease in the heavy metal concentrations was observed at the year
after 2010. The heavy metal contents decreased at about 10% from 2010 to 2014. It is proba-
bly attributed to the strictly waste management of local government in the most recent years
10 A. JIN ET AL.

(Beyer 2006; Zhang et al. 2008). The heavy metal contents in the industrial and municipal
wastes were reduced, and as a result, the heavy metal concentrations in the Andong sediment
decreased.
Here, we discuss the occurrence and potential pollution sources of heavy metals in the
sediment cores in detail. The average Cr concentrations in the cores C1 and C2 were
165.86 mg kg¡1 and 72.65 mg kg¡1, respectively. The temporal increasing rate of Cr concen-
tration is relatively faster than that of the other heavy metals, suggesting the potentially
heavy load from anthropogenic activities. Cr is closely associated with relatively coarse par-
ticles (Soto-Jimenez et al. 2001) and comes mainly from industrial manufacturing and wood
antisepsis preservation. High Cr concentrations coupled with high variations suggest strong
anthropogenic alteration for Cr in the sediments (Chen et al. 2016; Manta et al. 2002). Co
and Pb concentrations were in the range of 9.09–33.07 mg kg¡1 and 10.13–144.06 mg kg¡1,
respectively. The major sources of both metals can be ascribed to the vehicular emissions
(Olivier et al. 2011; Rahman and Ishiga 2012) after the construction of the Hangzhou Bay
Bridge. Because the core C1 is located closer to the bridge than the core C2, this process is
especially significant for the core C1 where both metal concentrations increased sharply after
the completion of the bridge at 2007. Cd and Hg concentrations in both sediment cores were
less than 0.3 mg kg¡1. Both metals are recognized as extremely harmful pollutants due to
their high genotoxicity and ecotoxicity (Mortazavi et al. 2016; Wang et al. 2005).
The Ni concentrations in the cores C1 and C2 were in the range of 28.67–88.46 mg kg¡1
and 24.38–42.37 mg kg¡1, respectively. It was almost doubled after 2004 in the core C1.
Industries such as electroplating, battery production, and stainless steel production are the
main anthropogenic sources for Ni (Cao et al. 2015). The average Mn concentrations in the
core C1 and C2 were 386.74 mg kg¡1 and 554.24 mg kg¡1, respectively. The temporal
increasing rate of Mn was not as significant as that of other heavy metals. It is suggested that
the occurrence of Mn in the sediment was largely controlled by natural processes rather
than human activities (Cao et al. 2015). The concentrations of Cu and Zn were in the range
of 24.8–89.99 mg kg¡1 and 72.37–240.21 mg kg¡1, respectively. Both elements show similar
geochemical characteristics and are essential micronutrients for aquatic life in freshwaters
and sediments. However, they can be toxic at elevated levels (Gu et al. 2015; Tuzen 2009).
The anthropogenic sources for both elements include the dumping of municipal waste,
domestic wastewater discharge, combustion of fossil fuels, copper wires manufacturing
industry, steel manufacturing industry, and so on. In addition, Co, Ni, Cu, Zn, and Mn are
siderophile elements that are closely related to Fe (Gaetani et al. 1997; Palme et al. 2014).
Their occurrences are significantly affected by Fe and are controlled by lithogeochemical
processes. Therefore, the accumulation of these metals in the sediments was also greatly
affected by natural processes such as sedimentation.
Note that both sediment cores showed distinctive heavy metal concentrations despite
their proximity. This phenomenon can be explained by the following hypotheses: (1) the
effects of TOC and grain size. As shown in Figure 5, the total heavy metal contents of both
cores increase with TOC and Mz values. It is suggested that the difference of heavy metal
contents in both cores may be partly ascribed to their different TOCs and grain sizes. Nor-
mally, fine particles with lower grain size can adsorb higher heavy metals (Adiyiah et al.
2014; Golterman 2004), while organic matter is enriched in fine-grained sediment and can
bind to a variety of heavy metals (Gao et al. 2013; Wangersky 1986). (2) Nevertheless, the
correlation coefficients between total heavy metal contents and TOC/Mz are much lower in
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 11

Figure 5. Correlations between total heavy metal contents (vertical coordinates, mg kg-1) and TOC/Mz.
Red cubes indicate the sediments from core C1 and blue triangles suggest the core C2 samples.

the core C1 than those in the core C2. In addition, the core C1 showed much higher heavy
metal contents than C2 at similar grain sizes or TOC contents. This result may be attributed
to their different sedimentation processes. The core C1 is located at the low tidal flat, while
the core C2 situates at the middle tidal flat. Therefore, the core C1 sediments experienced
higher mass exchange with heavy-metal-bearing water bodies (the currents from the Yangtze
River and the Qiantang River). Another explanation is that there is a main creek near the
core C1. The core C1 may have been additionally recharged by the municipal and industrial
wastewater from the adjacent area. In addition, the Hangzhou Bay Bridge imposed higher
vehicular emissions onto the core C1. The vehicular emissions may also have input heavy
metals into the sediments.

Contamination assessments
We assessed the temporal variations of heavy metal contamination in the sediment cores
from the Andong tidal flat. As shown in Figure 6, in the core C1, Cr, Hg, Pb, Co, and Zn
were significantly enriched with EF values greater than 1. Only Mn showed EF values less
than 1, indicating that it was not enriched in the sediments. The EF values of Cd, Ni, and Cu
were less than 1 before 2000. These values increased to higher than 1 after 2000. In the sedi-
ment core C2, Cr, Ni, Mn, and Cu showed EF values less than 1. The EF values of Cd, Hg,
Pb, Co, and Zn values were slightly larger than 1 and relatively invariable throughout the
sediment core. It is suggested that the heavy metals in the core C2 were relatively less con-
taminated by anthropogenic activities when compared with the core C1.
12 A. JIN ET AL.

Figure 6. Vertical profiles of enrichment factor (EF) values of heavy metals in the sediment cores from the
Andong tidal flat, Hangzhou Bay.

The CF values of heavy metals in the cores are displayed in Figure 7. In the sediment core
C1, Cr and Zn showed CF values between 1 and 4, indicating moderate pollution. The CF
values of Pb varied significantly from 1 to 12, suggesting that the Pb pollution was affected
by anthropogenic activities, which caused the pollution degree to increase from moderate to
high. The core was relatively unpolluted by Mn with its CF values less than 1. The values of
Cd, Hg, Co, Ni, and Cu were less than 1 before 2000 and higher than 1 after 2000, indicating
that the pollution of these heavy metals was enhanced in the recent decade. In the sediment
core C2, Cr, Co, Ni, Mn, and Cu showed CF values <1, indicating that C2 was unpolluted
by these heavy metals. The CF values of Cd, Hg, Pb, and Zn ranged from 1 to 3, suggesting
moderate pollutions.
The calculated Igeo values of heavy metals expressed similar information with the CF and
EF assessments. In the core C1, as shown in Figure 8, the Igeo values of the sediment fall in
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 13

Figure 7. Vertical variations of contamination factor (CF) values of heavy metals in the sediment cores
from the Andong tidal flat, Hangzhou Bay.

the range of between unpolluted to moderately polluted by Cr, Cd, Hg, and Zn ascribed to
their Igeo values of 0–1 after 2000 and less than 0 before 2000. Pb exhibited Igeo values of 0–3
after 1990, suggesting an unpolluted to strongly polluted level. All the other heavy metals
showed Igeo values <0, indicating that the core was unpolluted by these metals. All the heavy
metals (except for Hg and Pb) showed that Igeo values <0 in the core C2, indicating that the
core C2 was practically unpolluted by these heavy metals. The Igeo values of Hg and Pb
ranged from ¡1 to 1, suggesting unpolluted or moderated polluted levels.
Figure 9 shows the potential ecological risks of heavy metal pollutions in both sediment
cores. The RI values of the core C1 increased from about 85 before the 1990s to 200 after
2010. It is suggested that the potential ecological risk of heavy metal contamination doubled
in the past two decades, and the risk was considerable in recent years. The sediment core C2
14 A. JIN ET AL.

Figure 8. Vertical distributions of geoaccumulation index (Igeo) values of heavy metals in the sediment
cores from the Andong tidal flat, Hangzhou Bay.

showed relatively constant RI values ranged between 30 and 150, suggesting low to moderate
potential ecological risk.
In conclusion, the contamination assessments indicate that: (1) The sediment core C1 was
moderately to considerably polluted by Cr and Zn, low to moderately polluted by Cd, Co, Ni,
Cu, and Hg, and unpolluted by Mn. This core was severely polluted by Pb, which reached
high contamination level in recent years. (2) The sediment core C2 was relatively unpolluted
by all the assessed heavy metals before 2000, and was low to moderately polluted by Cd, Hg,
Pb, Co, and Zn after 2000. (3) The heavy metal pollution in both the cores before 2000
showed moderate potential ecological risks, while the potential ecological risk in the core C1
was increased to a considerate level after 2000. (4) The heavy metal pollution in the core C1
was dramatically aggravated after 2000, ascribed to the enhanced anthropogenic impact
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 15

Figure 9. Temporal variations of potential ecological risk index (RI) values of the sediment from the
Andong tidal flat, Hangzhou Bay. Red cubes indicate the sediments from core C1 and blue triangles sug-
gest the core C2 samples.

accompanied with rapid industrialization and economic development. The heavy metal pol-
lution in the core C2, however, was relatively constant.

Multi-statistical analyses
Correlation and PCA analyses are widely used methods to estimate the potential sources of
heavy metals (Mohanty and Samanta 2016; Yin et al. 2016). As shown in Table 1, in the sedi-
ment core C1, Al and Fe are not significantly correlated with almost all the assessed heavy met-
als. They show a positive significant correlation with each other at the 0.01 level. Hg is
significantly correlated with Al at the 0.01 level and Fe at the 0.05 level. All the other heavy
metals, including Cr, Co, Ni, Cd, Pb, Cu, Zn, and Mn, positively correlate with each other at
the 0.01 level. TOC shows a positive correlation with Cd at 0.05 level but no significant correla-
tions with all the other elements. The Mz values significantly correlated with Hg, Al, and Fe at
0.01 level, and Ni, Zn, and Pb at 0.05 level. In the sediment core C2, as shown in Table 2, all
the elements except Hg show positively significant correlations with each other. Hg, however,
does not show significant correlations with all the other heavy metals. The PCA analyses, as
shown in Tables 3 and 4, suggest similar results with the correlation analyses. All the elements
in the sediment core C1 can be classified as three components. The first component (PC1) con-
sists of Cr, Co, Ni, Cd, Pb, Mn, Cu, and Zn. It occupies 55.711% of the total variance. The sec-
ond component (PC2) is composed of Hg, Al, Fe, and Mz, which accounts for 22.583% of the
total variance. TOC forms the third component (PC3). In the sediment core C2, the elements
can be grouped into two components. The first component (PC1) consists of Cr, Co, Ni, Cd,
Pb, Mn, Cu, Zn, Al, Fe, and Mz. It accounts for 66.197% of the total variance. The second com-
ponent (PC2) occupies 11.287% of the total variance and only includes Hg.
Al and Fe are the most abundant metals on the earth. They are conservative elements, and
their occurrences were mainly caused by natural inputs (Duman et al. 2012; Fernandez et al.
2008). In the core C1, Mz and Hg are positively correlated with Al and Fe, suggesting that
Hg was mainly originated from the same source with Al and Fe, and the Hg contents were
relatively undisturbed after sedimentation (Hu et al. 2013). All the other heavy metals show
insignificant correlations with Fe and Al, indicating that these heavy metals were originated
from a source different than Fe and Al. These heavy metals significantly correlated with each
other, suggesting that they were originated from the same source. The positive correlation
between TOC and Cd indicates that Cd may be additionally provided by the biomass in the
 16
A. JIN ET AL.

Table 1. Pearson correlation coefficients of heavy metals, TOC, and Mz in the sediment core C1 from the Andong tidal flat, Hangzhou Bay. The statistically significant
pairs (P < 0.05) are shown in bold.
Cr Co Ni Cd Hg Pb Mn Cu Zn Al Fe TOC Mz

Cr 1
Co 0.863 1
Ni 0.894 0.960 1
Cd 0.918 0.868 0.928 1
Hg 0.252 0.233 0.286 0.284 1
Pb 0.931 0.934 0.950 0.916 0.327 1
Mn 0.342 0.568 0.562 0.310 ¡0.057 0.450 1
Cu 0.880 0.954 0.984 0.924 0.216 0.941 0.574 1
Zn 0.908 0.943 0.981 0.937 0.251 0.951 0.515 0.977 1
Al ¡0.033 ¡0.193 ¡0.151 ¡0.038 0.547 ¡0.075 ¡0.501 ¡0.176 ¡0.111 1
Fe ¡0.104 ¡0.186 ¡0.205 ¡0.201 0.412 ¡0.139 ¡0.295 ¡0.245 ¡0.195 0.754 1
TOC 0.322 0.294 0.351 0.399 ¡0.116 0.242 ¡0.107 0.323 0.309 ¡0.079 ¡0.062 1
Mz 0.393 0.325 0.385 0. 370 0.603 0.419 ¡0.069 0.320 0.414 0.687 0.560 0.157 1

Correlation is significant at the 0.05 level (2-tailed).

Correlation is significant at the 0.01 level (2-tailed).
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 17

Table 2. Pearson correlation coefficients of heavy metals, TOC, and Mz in the sediment core C2 from the
Andong tidal flat, Hangzhou Bay. The statistically significant pairs (P < 0.01) are shown in bold.
Cr Co Ni Cd Hg Pb Mn Cu Zn Al Fe TOC Mz

Cr 1
Co 0.912 1
Ni 0.915 0.968 1
Cd 0.413 0.443 0.502 1
Hg 0.174 0.240 0.190 ¡0.037 1
Pb 0.908 0.917 0.936 0.498 0.167 1
Mn 0.801 0.782 0.823 0.445 0.022 0.816 1
Cu 0.774 0.827 0.875 0.327 0.284 0.790 0.694 1
Zn 0.879 0.932 0.964 0.458 0.214 0.907 0.788 0.893 1
Al 0.694 0.638 0.621 0.343 0.010 0.665 0.638 0.423 0.551 1
Fe 0.773 0.716 0.716 0.390 0.011 0.744 0.700 0.533 0.654 0.937 1
TOC 0.648 0.756 0.717 0.249 0.131 0.663 0.491 0.677 0.687 0.378 0.465 1
Mz 0.670 0.676 0.665 
0.434 
¡0.058 0.708 0.674 0.445 0.599 0.794 0.781 0.281
 
1

Correlation is significant at the 0.05 level (2-tailed).

Correlation is significant at the 0.01level (2-tailed).

sediment. In the sediment core C2, however, most of the heavy metals show significant cor-
relation with Fe, Al, TOC, and Mz. It is suggested that these heavy metals, together with Fe
and Al, were originated from the same source. Hg was insignificantly correlated with all the
other heavy metals in both sediment cores. The Hg pollution was possibly contributed by
onshore contamination rather than the pollutants from the rivers.
According to Pang et al. (2015), the sediments in the Andong tidal flat were mainly ter-
rigenous materials that were carried by the downward current of the Yangtze River. The
East China Sea and the Qiantang River posed minor influence on the sediments. Therefore,
the positive correlations among metals in the core C2 suggest that all these metals were
mainly contributed by the Yangtze River. The heavy metals may be continuously added
into the water body during transportation from the Yangtze River to the Andong tidal flat.

Table 3. Rotated PCA analyses of metals, TOC, and grain size in the sediment core C1 from the Andong
tidal flat, Hangzhou Bay.
PC1 PC2 PC3

Eigenvalues 7.242 2.936 1.160

% of variance 55.711 22.583 8.921
Cumulative % 55.711 78.294 87.216
Eigenvectors
Cr 0.929 0.071 0.087
Co 0.962 ¡0.070 ¡0.060
Ni 0.993 ¡0.031 ¡0.018
Cd 0.946 0.045 0.158
Hg 0.292 0.707 ¡0.315
Pb 0.970 0.053 ¡0.057
Mn 0.522 ¡0.443 ¡0.531
Cu 0.983 ¡0.088 ¡0.024
Zn 0.987 ¡0.008 ¡0.013
Al ¡0.119 0.938 0.031
Fe ¡0.185 0.827 ¡0.055
TOC 0.346 ¡0.022 0.857
Mz 0.408 0.807 0.006

PCA loadings > 0.5 are shown in bold. The Eigenvalues, percent of variance and cumulative variance, eigenvectors are given
for the three principal components (PC1–PC3). Rotation method: Varimax with Kaiser Normalization.
18 A. JIN ET AL.

Table 4. Rotated PCA analyses of metals, Mz, and TOC in the sediment core C2 from the Andong tidal flat,
Hangzhou Bay.
PC1 PC2

Eigenvalues 8.606 1.467

% of variance 66.197 11.287
Cumulative % 66.197 77.484
Eigenvectors
Cr 0.942 0.042
Co 0.960 0.160
Ni 0.972 0.143
Cd 0.519 ¡0.217
Hg 0.163 0.656
Pb 0.955 0.044
Mn 0.862 ¡0.115
Cu 0.835 0.381
Zn 0.936 0.216
Al 0.756 ¡0.471
Fe 0.830 ¡0.388
TOC 0.701 0.361
Mz 0.759 ¡0.481

PCA loadings > 0.5 are shown in bold. The Eigenvalues, percent of variance and cumulative variance, eigenvectors are given
for the two principal components (PC1–PC2). Rotation method: Varimax with Kaiser Normalization.

However, the sediment at C2 was less disturbed by secondary local contamination after
sedimentation. In the sediment core C1, however, the correlations among metals were sig-
nificantly influenced by local human activities after sedimentation. These anthropogenic
activities include wastewater discharge from local industries and the vehicular emissions
from the Hangzhou Bay Bridge. In addition, the secondary human pollution in the core
C1 was also responsible for its elevated heavy metal contents with respect to the core C2.

Annual fluxes of sedimentary heavy metals

In this study, the sedimentary fluxes of heavy metals in the Andong tidal flat were estimated
using the following formula:

Fsed D Cdg (6)

where C is the measured heavy metal concentration in the sediment (mg kg¡1 dw), d is the
sediment density (1.3 g cm¡3), and g (cm a¡1) is the mean sedimentation rate that is deter-
mined from the 210Pb dating on the sediment cores. Fsed (g m¡2 a¡1) is the sedimentary
fluxes of heavy metals.
The estimated heavy metal fluxes from both cores are summarized in Figure 10. The sedi-
mentary fluxes of heavy metals in the sediment core C1 increased gradually from about 4 g
m¡2 a¡1 at 1990 to higher than 8 g m¡2 a¡1 at 2015. In the core C2, however, it maintained
at about 5 g m¡2 a¡1 from 1988 to 2000 and then reached a maximum of nearly 7.4 g m¡2
a¡1 at 2003. Then, the fluxes decreased and maintained at 5–6 g m¡2 a¡1 thereafter. Accord-
ing to the average annual deposition volume of sediment of 6 £ 107 t a¡1 at the Andong tidal
flat in recent decades (Cao et al. 2015), the estimated annual heavy metal input into the
Andong tidal flat ranged from 2.5 £ 107 to 8.4 £ 107 kg.
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 19

Figure 10. Sedimentary fluxes of heavy metals estimated from the metal contents in the two sediment
cores and historical economic development and waste water emissions of Zhejiang, Jiangsu and Shanghai
in the past 35 years. GIOV and WE represent gross industrial output and wastewater emissions,
respectively.

When we considered the historical economic development (GIOV) wastewater emissions

(WE) of adjacent provinces (Zhejiang, Jiangsu, and Shanghai, Figure 10), we found that the
heavy metal fluxes of the Andong tidal flat varied with the increasing economic development
and WE. Especially the heavy metal fluxes significantly correlated with the wastewater dis-
charge. The sediment of Hangzhou Bay was mainly provided by the Yangtze River and
minorly contributed by the Qiantang River and the East China Sea. It is suggested that the
heavy metals in the Hangzhou Bay sediment were also contributed by these sources, while
these sources were controlled by anthropogenic activities. Nevertheless, the heavy metal con-
tent of wastewater is also a key factor for the sedimentary heavy metal fluxes. If the wastewa-
ter was properly treated before discharging, the heavy metal fluxes will be decreased even
though the wastewater discharge was increased. This hypothesis could explain the decrease
of the sedimentary fluxes in recent several years when local governments conducted the
“Green GDP” strategy. Note that both sediment cores showed sharp decreases in heavy
metal fluxes from 2003 to 2005. As stated before, it is probably related to the construction of
the Hangzhou Bay Bridge, which changed the hydrodynamic condition of the Andong tidal
flat.
Our results indicated that the heavy metal contamination in the sediment of the
Andong tidal flat has been significantly elevated due to anthropogenic activities. These
activities included the discharge of industrial and municipal wastewater without proper
treatment, and the vehicle emissions from the nearby bridge. In order to protect the local
ecological structure and environment from heavy metal contamination, (1) the government
should establish a strict environmental protection regulation to reduce the wastewater
input and to decrease the heavy metal contents of the wastewater. (2) The related
20 A. JIN ET AL.

industrial plants should update their equipment and wastewater treating technology to
diminish the direct input of heavy-metal-bearing wastewater into the water system. (3)
The local government should try to remediate the sediment using either chemical or bio-
logical methods (Yuan et al. 2016).

Conclusions
In summary, we collected two sediment cores from the Andong tidal flat, Hangzhou Bay,
and investigated the occurrence and pollution indexes of heavy metals in the cores. The
deposition rate of the sediments was about 5 cm a¡1, and the sediment core can be traced
back to »30 years ago. Before 2000, both sediment cores showed relatively constant heavy
metal concentrations. After 2000, however, the core C1 exhibited dramatically enhanced
heavy metal contamination. The overall increasing trends of heavy metals in both cores sug-
gested that the studied area may be affected by enhanced anthropogenic activities in recent
decades. The contamination assessments indicate that the core C1 was severely polluted by
Pb, moderately to considerably polluted by Cr and Zn, and low to moderately contaminated
by Cd, Co, Ni, Cu, and Hg. The sediment core C2, however, was relatively unpolluted before
2000 and low to moderately contaminated after 2000. In core C1, Fe and Al can be classified
into a different group with heavy metals. In core C2, however, Fe, Al, TOC, grain size, and
(Cr, Co, Ni, Pb, Mn, Cu, and Zn) were closely correlated with each other. It is suggested that
the sediment core C1 was additionally polluted after sedimentation, e.g., the local wastewater
discharge, the vehicular emissions from the Hangzhou Bay Bridge, and so on. This hypothe-
sis can also explain the elevated heavy metal contents in the core C1. The calculated sedi-
mentary fluxes of heavy metals were in the range of 4–8 g m¡2 a¡1 in the core C1, which
was closely related to the wastewater discharge in adjacent areas. Therefore, the government
should establish strict environmental protection regulation and remediate the tidal flat to
protect the local environment and ecological system. In the near future, we will continue to
study the occurrence of heavy metals in the Hangzhou Bay and try to unveil their geochemi-
cal characteristics.

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