Environmental Toxicology and Chemistry, Vol. 32, No. 4, pp. 831–840, 2013
# 2013 SETAC
Printed in the USA
DOI: 10.1002/etc.2136
ENVIRONMENTAL CONCENTRATIONS AND BIOACCUMULATIONS OF
CADMIUM AND ZINC IN COASTAL WATERSHEDS ALONG THE
CHINESE NORTHERN BOHAI AND YELLOW SEAS
WEI LUO,y YONGLONG LU,*y TIEYU WANG,y PEIRU KONG,y WENTAO JIAO,y WENYOU HU,y
JUNMEI JIA,y JONATHAN E. NAILE,zx JONG SEONG KHIM,k and JOHN P. GIESYzx
yState Key Lab of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, China
zDepartment of Veterinary Biomedical Sciences, University of Saskatchewan, Saskatoon, Canada
xToxicology Center, University of Saskatchewan, Saskatoon, Canada
kSchool of Earth and Environmental Sciences, Seoul National University, Seoul, Republic of Korea
(Submitted 4 June 2012; Returned for Revision 12 July 2012; Accepted 2 December 2012)
Abstract—Cadmium (Cd) and zinc (Zn) in surface water, sediment, carp, and crab samples collected from upstream and downstream
regions of coastal watersheds along the Chinese Northern Bohai and Yellow Seas were analyzed to provide a comprehensive
understanding and assessment of their environmental concentrations and bioaccumulations. The results showed that downstream waters
contaminated with Zn would have adverse effects on aquatic organisms. Although nearly all sediments were contaminated with Cd due to
human activities, little potential existed for Cd toxicity in sediment-dwelling fauna. Concentrations of Cd and Zn in most water, sediment,
carp, and crab were less than published values. The downstream carp and crabs had higher mean bioaccumulation factors and biotasediment accumulation factors for Cd but lower mean biota-sediment accumulation factors for Zn than the upstream carp and crabs. Based
on the relationships among Cd and Zn concentrations in water, sediment, and biota, the authors conclude that Cd and Zn in crabs primarily
derived from sediment exposure. Although Cd and Zn in water and sediment originated from some of the same sources, the sources of Cd
or Zn in water were likely different from those in sediment. Environ. Toxicol. Chem. 2013;32:831–840. # 2013 SETAC
Keywords—Cadmium
Zinc
Water
Sediment
Bioaccumulation
1990s, concentrations of metals and metalloids in water and
sediments have exceeded the water quality standards in some
coastal areas [4–6].
Based on the results of previous studies, most metals entering
the Bohai and Yellow Seas originate from the more northern
regions in the vicinity of Liaodong Bay [7,8]. Due to their
concentrations and toxicities, Cd and Zn have been identified as
the two metals of greatest concern in the area [1,9–11]. Cadmium
and zinc loadings that exceed natural background pose a
potential problem for aquatic ecosystems and for humans [12].
The issue of contamination by these two metals is especially
critical for coastal areas in which riverine and land-based inputs
discharge into a semi-enclosed embayment, as in the Chinese
Northern Bohai and Yellow Seas. For this reason, significant
quantities of Cd and Zn are trapped within the catchments.
Most previous studies conducted in the area have focused on
Cd and Zn in water [3,13] and sediment [4,5,8,14,15]. However,
only sporadic studies have extended beyond water and sediment
to include biota [1,16]. Dietary metal uptake by aquatic
organisms is known to be as important as waterborne metal
uptake, and the relative importance of uptake from the water
versus uptake from the diet depends on the metal, its bioavailable
concentrations in water and diet, the habitat and feeding habits of
the organism, and finally the uptake rate, assimilation efficiency,
and detoxification/homeostatic processes in the organism.
Therefore, in addition to measuring concentrations of metals
in abiotic matrices, monitoring their bioaccumulation in aquatic
animals is important to fully assess the potential impact on
organism and human health [17]. Bioaccumulation of Cd and Zn
in aquatic foods is a potential problem from a public health
standpoint. Furthermore, serious concerns have arisen in
Chinese food safety, which also require knowledge of the
INTRODUCTION
During the past several decades, pollution in coastal
environments of China has become an increasingly serious
threat. In particular, metals and metalloids such as cadmium
(Cd), zinc (Zn), arsenic (As), and lead (Pb) have become
major pollutants along China’s coastal zone. As a consequence,
water and sediment qualities in coastal watersheds have
declined markedly, affecting the health of aquatic ecosystems
and possibly humans through consumption of contaminated
seafood [1]. The safety of seafood has been compromised by the
presence of metals, constituting a health risk for those who eat
foods from these affected coastal areas [2].
The Bohai and Yellow Seas in North China, around which are
positioned important economic development zones and large
harbors, are located in the northern Pacific Ocean. The coastal
areas of the Bohai and Yellow Seas contain some extensive
industrial areas in which both large- and middle-scale enterprises
are situated. These industries, including metallurgy, petroleum
refining, and chemical production, are frequently situated near
harbors. In addition, agriculture and mining create potential
sources of metals in the coastal river watercourses along the
Bohai and Yellow Seas. Considerable metal quantities are
released through human activities and are transported to
the coast and bays in the form of sewage effluents, industrial
discharges, urban and agricultural runoff, atmospheric fallout,
and deposits that are released farther upriver [3]. Since the
All Supplemental Data may be found in the online version of this article.
To whom correspondence may be addressed
(yllu@rcees.ac.cn).
Published online 25 January 2013 in Wiley Online Library
(wileyonlinelibrary.com).
831
832
Environ. Toxicol. Chem. 32, 2013
bioaccumulated concentrations of Cd and Zn and their potential
risks to humans. However, in China, integrated assessments of
the concentration distributions of Cd and Zn in various matrices
within the coastal watersheds on a regional scale and their
bioaccumulations in the muscle tissue of aquatic foods such as
carp and crabs are limited. In addition, the relative importance of
local- versus watershed-scale effects on concentrations of metals
along the Chinese Northern Bohai and Yellow Seas had not yet
been determined. Currently, the potential for Cd and Zn in
upstream areas of the watersheds, including surface waters, is
largely unknown, specifically in freshwater systems that influence the metal concentrations when transported to downstream
areas, such as coastal and estuarine systems and in particular
marine and brackish systems. Therefore, a systematic study was
needed to evaluate Cd and Zn in abiotic and biotic matrices from
upstream and downstream regions of coastal watersheds along
the Chinese Northern Bohai and Yellow Seas.
The specific objectives of the present study were (1) to
determine concentrations of Cd and Zn in water and sediment
and to assess their bioaccumulation by measuring their
concentrations in carp and crabs; (2) to characterize the spatial
distribution of Cd and Zn concentrations in water, sediment, and
human food of aquatic origin; (3) to ascertain sources and
relationships of Cd and Zn in surface water, sediment, and foods
of aquatic origin; and (4) to evaluate the potential hazards of
these two metals to wildlife and humans.
MATERIALS AND METHODS
Study area
A map of the study area and sample details of all sampling
sites along the Chinese Northern Bohai and Yellow Seas are
provided in Figure 1 and the Supplemental Data, Table S1,
respectively. Two receiving waters for the coastal rivers exist
along the Chinese Northern Bohai and Yellow Seas. One is the
Northern Bohai Sea, which collects water from rivers to the west
of Dalian. The other is the Northern Yellow Sea, which collects
water from rivers to the east of Dalian. The Liugu, Wuli, Daling,
Liaohe, Daliao, Daqing, and Fuzhou rivers flow north to south
into the Northern Bohai Sea, while the other rivers flow north
to south into the Northern Yellow Sea (Fig. 1). Approximately
28 million people live in the coastal watersheds along the
Chinese Northern Bohai and Yellow Seas, with the watersheds in
Tangshan having the largest population. The coastal watersheds
in Jinzhou and Panjin contain the largest proportion of farmland.
The largest proportions of urban and industrial areas are found in
the watersheds in Tangshan and Dalian, where the largest
quantities of industrial waste and sewage are discharged.
Sampling
Our research group had previously chosen 36 sites, selected
by simple random sampling to represent the typical characteristics of industry, agriculture, and urbanization along coastal
watersheds of the Chinese Northern Bohai and Yellow Seas. A
nested sampling scheme was applied to each site. All samples
were collected in October 2008 (Fig. 1).
Thirty-six surface-water samples were collected (Supplemental Data, Table S1). Clean sampling techniques were used
during sample collection, preservation, and storage [18].
Twenty-one water samples were obtained from upstream regions
of the rivers, and 15 were collected from downstream regions.
Each water sample consisted of five homogenized subsamples
(1 L) taken from 0- to 10-cm depths within an area of
approximately 25 m2. These subsamples were then placed into
W. Luo et al.
precleaned and labeled Teflon bottles. To keep the dissolved
metals in solution, the water samples were filtered through a
0.45-mm capsule filter and acidified with HNO3 to a pH of 2 at
the time of collection. Samples were then placed in a cooler and
immediately delivered to the laboratory.
Except for one location, surface sediments were collected
synoptically with water. Thirty-five sediment samples were
collected, of which 21 were from the upstream areas and 14 were
from the downstream areas (Fig. 1). Each sediment sample was
composed of five homogenized subsamples taken from the top
10 cm within a 5-m2 area. Composite sediment samples were
placed in dark-colored Teflon bottles, refrigerated, and returned
immediately to the laboratory where they were air-dried,
crushed, mixed thoroughly, passed through a 100-mesh nylon
sieve, and stored at 48C in the dark prior to analysis.
Crucian carp (Carassius carassius) and Asian shore crabs
(Hemigrapsus sanguineus) were selected as representative
aquatic foods because their habitats are evenly distributed
throughout the coastal areas along the Chinese Northern
Bohai and Yellow Seas. To remove effects of specimen size
within the same species, only individuals of approximately the
same size were collected. Crucian carp with a length of
9 2 cm (mean standard deviation [SD]) and a wet weight
of 180 30 g (mean SD) (estimated average age, 1–2 years)
and Asian shore crabs with a carapace width of 3.2 0.40 cm
(mean SD) and a wet weight of 20 3 g (mean SD;
estimated average age 1–2 years) were collected. A composite
sample of carp or crab contained three individuals that together
formed a representative sample for each sampling site. Forty-one
composite samples were collected. Ten of the 17 composite carp
samples were from the upstream regions, and seven were from
downstream regions. Six of the 24 composite crab samples were
from upstream regions, and 18 were from downstream regions
(Fig. 1 and Supplemental Data, Table S1). The biota samples
were placed in watertight polyethylene bags and frozen at –208C.
In the laboratory, the samples were dissected, and equal weights
of muscle from each replicate of the same species from each site
were combined. The muscle aliquots were dried at 1058C for
24 h.
Quantification of heavy metals
The surface waters were analyzed directly. The sediments
were digested using HNO3 and H2O2 according to U.S.
Environmental Protection Agency method 3051 [19]. The
aliquots of 0.10 to 0.45 g of dried muscle were homogenized,
weighed, and digested in Teflon bombs using HNO3, H2O2, and
HCl [20]. Concentrations of Cd, Zn, and iron (Fe) in the
digestates and reagent blanks were quantified via inductively
coupled plasma-mass spectrometry (Agilent 7500; Agilent
Technologies, Palo Alto, CA, USA).
Quality assurance and quality control for the quantification of
heavy metals were determined by analyzing duplicates, method
blanks, liquid standard solutions, and the certified reference
materials GB ESS1 and DORM-2 for the sediment and biota
samples, respectively. The limits of quantification for Cd and Zn
were 0.07 and 1 mg/L, respectively. Concentrations of Cd and
Zn in all method blanks were less than limits of quantification.
Recoveries of Cd spiked in water, sediment, and biota were
99 1, 98 4, and 94 2%, respectively, while recoveries of
Zn spiked in water, sediment and biota were 101 2, 97 3,
and 91 5%, respectively. Recoveries of Fe from the sediment
and biota were 101 4 and 104 3%, respectively. The
relative percentage of difference between the sample duplicates
was <10%.
Cd and Zn in coastal watersheds of North China
Environ. Toxicol. Chem. 32, 2013
833
Fig. 1. Sampling sites for surface water, sediment, and aquatic food samples in upstream and downstream regions of the coastal watersheds (with a different shade
representing a different administrative region) along the Chinese Northern Bohai and Yellow Seas. [Color figure can be seen in the online version of this article,
available at wileyonlinelibrary.com]
Enrichment factor, bioaccumulation factor, and biota-sediment
accumulation factor
Enrichment factors (EFs) were used to determine potential
sources of metals into riverine, estuarine, and coastal
environments [21]. To identify anomalous metal concentrations, a geochemical normalization of Cd and Zn concentrations to concentrations of a conservative element, such as
aluminum (Al), Fe, or silicon (Si), was employed. Several
authors have successfully used iron to normalize the concen-
trations of metal contaminants [22]. In the present study, Fe
was used as the conservative tracer to differentiate the
natural from the anthropogenic sources of Cd and Zn. The
EF for each metal was calculated using the following
Equation 1 [23]
EF ¼
M
Fe sample
M
Fe background
ð1Þ
834
Environ. Toxicol. Chem. 32, 2013
W. Luo et al.
M
in which EF is the enrichment factor, Fe sample is the ratio of the
concentrations
of either Cd or Zn to Fe in the sample, and
M
is
the
ratio of the metal to the Fe concentration in
Fe background
the background. Considering the regional differences in Fe
concentrations in sediment and the lack of data regarding the
background concentrations of Fe in riverine sediment of China,
the soil background Fe concentrations (mean = 28,800 mg/kg,
dry wt, with a range of 11,200–46,400 mg/kg, dry wt) in the
Liaoning Province where most coastal rivers along the Chinese
Northern Bohai and Yellow Seas are located, and the sediment
background Fe concentrations (mean = 34,800 mg/kg, dry wt,
with a range of 7,300–51,500 mg/kg, dry wt) in the Bohai Sea
were adopted as background values for the riverine and marine
sediments in the studied area, respectively [24,25].
Enrichment factor values between 0.5 and 1.5 indicated that
the metal originated entirely from crustal materials or natural
processes, whereas EF values greater than 1.5 suggested that
the metal was more likely the result of human activities [26].
Categories of contamination have been defined based on EF
values. For example, EF values 2 suggest a deficiency in
minimal metal enrichment. Alternatively, an EF value > 2
suggests various degrees of metal enrichment due to human
activities [27].
The bioaccumulation factor (BAF) is the ratio of a chemical
concentration in an organism to the concentration in water. The
biota-sediment accumulation factor (BSAF) is the ratio of a
chemical concentration in an organism to the concentration in
sediment [28]. Concentrations of Cd and Zn in muscle of carp
and crabs in the present study were expressed on a wet-weight
basis. These concentrations could be converted to a dry-weight
basis by use of a wet-to-dry-weight conversion factor [29]. In the
present study, the wet-to-dry conversion factors for carp and
crabs were 4.2 0.67 and 3.4 1.0, respectively.
Data analysis
Concentrations of Cd and Zn in water, sediment, carp, and
crabs as well as EFs, BAFs, and BSAFs were logarithmically
transformed to better approximate the normal distributions of
the values. The Shapiro–Wilk test was used to test for normality.
The t test for independent groups was used to determine whether
the concentrations of metals in water, sediment, carp, and crabs
as well as EFs, BAFs, and BSAFs for the upstream coastal
watersheds differed significantly from those for the downstream
coastal watersheds. Correlations between the metal concentrations in abiotic and biotic materials were also performed.
Pearson correlation coefficients (r) were calculated for
several pairs of variables. The significance level (a) was set
at 0.05. All statistical analyses were conducted using SPSS
version 16.0.
RESULTS
Cadmium and zinc concentrations in the water samples from
the upstream and downstream sites of the coastal watersheds
along the Chinese Northern Bohai and Yellow Seas are presented
in Table 1. In general, mean concentrations of Cd and Zn in
downstream waters within coastal watersheds along the Chinese
Northern Bohai and Yellow Seas were significantly higher than
those in the upstream waters (p < 0.01). No differences were
found in mean concentrations of Cd and Zn in upstream waters
between the Northern Bohai Sea and Northern Yellow Sea
(p > 0.05). However, mean concentrations of Cd and Zn in the
downstream waters of coastal rivers along the Northern Bohai
Sea were greater than those in downstream waters of the
coastal rivers along the Northern Yellow Sea (p < 0.05; Table
1). Water from upstream in the Yalu River contained the highest
Zn concentration, while water from downstream in the Wuli
River contained the highest Cd concentration (Fig. 2). Relatively
high Cd and Zn concentrations in downstream waters were
predominantly distributed around the Northern Bohai Sea,
especially around Liaodong Bay. The levels of Cd in water of
the Dou and Luan rivers, in seawater of Jinzhou and Liaodong
Bays, in the Yalu River Estuary, and even in the Northern
Bohai Sea can be considered small, compared to previous studies
of Cd and Zn in these regions (Supplemental Data, Table S2),
while Cd levels in the seawater of the Daliao Estuary and the
Northern Yellow Sea can be considered high in comparison
with previous studies. The mean Zn concentrations in the
seawater of the Northern Bohai Sea and Northern Yellow Sea
in the present study showed a slight increase, while those
from the Daliao River Estuary, Jinzhou Bay, and the Liaodong
Table 1. Cadmium (Cd) and zinc (Zn) concentrations in water (mg/L), sediments (mg/kg, dry wt), and their enrichment factor (EF) values in the coastal watersheds
along the Chinese Northern Bohai and Yellow Seas (CNBYS)
Environmental sample
Water
Sediment
Sampling location
Upstream regions of coastal watersheds along the NBS (n ¼ 17)
Downstream regions of coastal watersheds along the NBS (n ¼ 12)
Upstream regions of coastal watersheds along the NYS (n ¼ 14)
Downstream regions of coastal watersheds along the NYS (n ¼ 3)
Upstream regions of coastal watersheds along the CNBYS (n ¼ 21)
Downstream regions of coastal watersheds along the CNBYS (n ¼ 15)
Upstream regions of coastal watersheds along the NBS (n ¼ 17)
Downstream regions of coastal watersheds along the NBS (n ¼ 12)
Upstream regions of coastal watersheds along the NYS (n ¼ 4)
Downstream regions of coastal watersheds along the NYS (n ¼ 2)
Upstream regions of coastal watersheds along the CNBYS (n ¼ 21)
Downstream regions of coastal watersheds along the CNBYS (n ¼ 14)
Statistic
GM
GM
GM
GM
GM
GM
GM
EF
GM
EF
GM
EF
GM
EF
GM
EF
GM
EF
GM ¼ geometic mean; SD ¼ standard deviation; NBS ¼ Northern Bohai Sea; NYS ¼ Northern Yellow Sea.
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
Cd
0.20
0.37
0.19
0.28
0.20
0.35
0.13
2.2
0.11
5.0
0.13
1.4
0.10
1.3
0.13
2.0
0.11
4.7
0.031
0.18
0.0011
0.10
0.031
0.17
0.18
2.0
0.082
2.5
0.071
0.31
0.062
0.67
0.16
1.8
0.081
2.6
Zn
7.0
22
9.7
13
7.5
20
50
1.5
34
1.8
86
1.8
90
2.0
67
1.6
49
1.8
4.52
10
59
29
26
14
39
0.82
33
0.76
44
0.47
0.87
0.63
41
0.76
34
0.73
Cd and Zn in coastal watersheds of North China
Environ. Toxicol. Chem. 32, 2013
835
Fig. 2. Spatial distribution of Cd and Zn in water (A) and sediment (B) from upstream and downstream regions of the coastal watersheds along the Chinese
Northern Bohai and Yellow Seas. [Color figure can be seen in the online version of this article, available at wileyonlinelibrary.com]
Bay showed a large decrease (Fig. 2 and Supplemental Data,
Table S2).
Mean concentrations of Cd and Zn in upstream and
downstream sediments of coastal watersheds along the Chinese
Northern Bohai and Yellow Seas are provided in Table 1. Mean
concentrations of Cd and Zn in upstream sediments were not
significantly greater than those in downstream sediments
(p > 0.05). Mean concentrations of Zn in the up- and
downstream sediments that were collected from coastal watersheds along the Northern Yellow Sea were greater than those
from coastal watersheds along the Northern Bohai Sea
(p < 0.05). However, no differences were observed in mean
Cd concentrations in the up- and downstream sediments between
the Northern Bohai Sea and Northern Yellow Sea (p > 0.05;
Table 1). Sediments in both the up- and downstream areas of
rivers such as the Wuli, Yalu, and Yingna contained relatively
high concentrations of Cd and Zn (Fig. 2). Mean EF values for
Cd and Zn in sediments were greater than 1.5. Mean EFs for Zn
were less than 2 (EF < 2) in both upstream and downstream
sediments. The mean EF value for the Cd concentration in
the downstream sediments was greater than that in upstream
sediments (p < 0.05). However, the mean EF for Zn in upstream
sediments did not differ significantly from that in downstream
sediments (p > 0.05; Table 1). When these results were
compared with those in the literature (Supplemental Data,
Table S2), it was determined that (1) Cd concentrations in the
sediments of Liaodong Bay in the present study are comparable,
while those in other sediments are less (Fig. 2); (2) concentrations of Cd and Zn in upstream sediments of the Wuli, Liao,
and Daliao rivers in the present study decreased greatly; and (3)
the estuaries around Liaodong Bay (not including the
Daliao Estuary), the Yalu Estuary, Jinzhou Bay, and Liaodong
Bay had low concentrations of Zn; however, the mean Zn
concentration in the downstream sediments of the Northern
Yellow Sea was higher than that previously reported (Supplemental Data, Table S2).
Mean concentrations of Cd and Zn in muscles of carp are
provided in Table 2. The mean concentration of Zn in upstream
carp was significantly higher than that in downstream carp
(p < 0.01), while no significant difference was found in mean
concentrations of Cd in upstream and downstream carp
(p > 0.05). Although carp from upstream portions of watersheds of the Northern Bohai Sea contained a greater mean Zn
concentration than carp from upstream regions of watersheds of
the Northern Yellow Sea (p < 0.05), no differences were
detected in mean concentrations of Cd and Zn in carp between
the Northern Bohai Sea and Northern Yellow Sea (p > 0.05).
Carp from upstream areas of the Dou River in Tangshan and
downstream areas of the Xin River in Qinghuangdao contained
the highest Cd concentrations (Fig. 3). Higher Zn concentrations
were observed in carp from the upstream areas of the Dou, Xin,
Liugu,Wuli, and Fuzhou rivers. For the Northern Bohai Sea and
Northern Yellow Sea, the mean BAFs and BSAFs for Cd in
downstream carp were higher than those in upstream carp
(p < 0.05; Table 2). Furthermore, the mean BAFs for Cd in
upstream or downstream carp from the Northern Yellow Sea
were higher than those from the Northern Bohai Sea. However,
mean BSAF for Cd in upstream carp from the Northern Yellow
Sea was less than that from the Northern Bohai Sea, while the
mean BSAF for Cd in downstream carp from the Northern
Yellow Sea was higher than that from the Northern Bohai Sea.
For the Northern Bohai Sea and Northern Yellow Sea, mean
BAFs and BSAFs for Zn were less in the downstream carp than
in upstream carp. Furthermore, both BAF and BSAF for Zn in
upstream carp from the Northern Bohai Sea were higher than
those in upstream carp from the Northern Yellow Sea. However,
the mean BAF for Zn was less in downstream carp from the
Northern Bohai Sea than in downstream carp from the Northern
836
Environ. Toxicol. Chem. 32, 2013
W. Luo et al.
Table 2. Cadmium (Cd) and zinc (Zn) concentrations (mg/kg, wet wt), their bioaccumulation factors (BAFs), and bio-sediment accumulation factors (BSAFs) in
carp and crab collected from the coastal watersheds along the Chinese Northern Bohai and Yellow Seas (CNBYS)
Biota
Carp
Sampling location
Upstream regions of coastal watersheds along the NBS (n ¼ 8)
Downstream regions of coastal watersheds along the NBS (n ¼ 5)
Upstream regions of coastal watersheds along the NYS (n ¼ 2)
Downstream regions of coastal watersheds along the NYS (n ¼ 2)
Upstream regions of coastal watersheds along the NBYS (n ¼ 10)
Downstream regions of coastal watersheds along the NBYS (n ¼ 7)
Crab
Upstream regions of coastal watersheds along the NBS (n ¼ 6)
Downstream regions of coastal watersheds along the NBS (n ¼ 18)
Downstream regions of coastal watersheds along the NYS (n ¼ 4)
Upstream regions of coastal watersheds along the NBYS (n ¼ 6)
Downstream regions of coastal watersheds along the NBYS (n ¼ 22)
Statistic
GM
BAF
BSAF
GM
BAF
BSAF
GM
BAF
BSAF
GM
BAF
BSAF
GM
BAF
BSAF
GM
BAF
BSAF
GM
BAF
BSAF
GM
BAF
BSAF
GM
BAF
BSAF
GM
BAF
BSAF
GM
BAF
BSAF
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
Cd
0.0036
90.7
0.26
0.020
168.1
1.0
0.0026
140.0
0.17
0.01
245.4
2.3
0.0044
95.6
0.25
0.018
190.2
1.2
0.14
3,451.8
7.3
1.6
9,302.4
23.7
0.29
4,877.8
23.3
0.14
3,451.8
7.3
1.2
8,497.9
23.6
0.042
224.6
0.67
0.10
295.4
1.6
0.00042
368.6
0.54
0.11
361.5
3.6
0.04
212.3
0.63
0.09
294.7
1.5
2.5
7,448.7
15.7
4.7
12,008.2
21.2
1.8
5,427.5
25.9
2.5
7,448.7
15.7
3.8
11,135.1
21.5
Zn
38
9,042.0
1.0
10
536.3
0.54
14
2,454.2
0.24
19
1,516.6
0.22
39
8,383.2
0.85
14
816.4
0.48
27
1,842.2
1.2
31
1,496.8
0.64
44
6,180.4
0.49
27
1,842.2
1.2
35
2,348.3
0.61
15
12211
0.86
6.7
335.1
0.54
0.26
30,118.2
0.20
0.69
2,567.1
0.31
17
11,699.7
0.69
6.4
934.6
0.50
6.7
1,714.5
1.1
12
854.5
0.35
9.1
1,263.2
0.11
6.7
1,714.5
1.1
12
2,058.6
0.32
GM ¼ geometric mean; SD ¼ standard deviation; NYS ¼ Northern Yellow Sea; NBS ¼ Northern Bohai Sea; NBYS ¼ Northern Bohai and Yellow Seas.
Fig. 3. Spatial distribution of Cd and Zn in carp (A) and crabs (B) from the coastal watersheds along the Chinese Northern Bohai and Yellow Seas. [Color figure
can be seen in the online version of this article, available at wileyonlinelibrary.com]
Environ. Toxicol. Chem. 32, 2013
Cd and Zn in coastal watersheds of North China
Yellow Sea, while the mean BSAF for Zn was higher in
downstream carp from the Northern Bohai Sea than in
downstream carp from the Northern Yellow Sea. No studies
could be found in the literature regarding concentrations of Cd
and Zn in carp or other river fish in the studied areas. Therefore,
we compared our results with data for sea fish species
(Supplemental Data, Table S2). All Cd concentrations in carp
were significantly less than previously reported concentrations
of Cd in muscle of sea fishes. The Zn concentration in the carp
from the sea near Huludao was remarkably lower than that
previously reported for pomfret, blue-spot sierra, and gobies.
Furthermore, carp from downstream in the Liao River in the
present study had less concentrations of Zn than the wolf goby
previously collected from the Liao River Estuary. However,
the carp from the Northern Yellow Sea had a higher
concentration of Zn than the fish previously collected from
the Yellow Sea (Fig. 3, Supplemental Data, Table S2).
Mean concentrations of Cd and Zn in the upstream crabs were
significantly less than those in downstream crabs (p < 0.05;
Table 2). No crabs were collected from the upstream areas within
coastal watersheds along the Northern Yellow Sea. The mean Cd
concentration in crabs from downstream regions of the coastal
watersheds along the Northern Bohai Sea was greater than that in
crabs from downstream regions of the coastal watersheds along
the Northern Yellow Sea (p < 0.05), although no significant
difference was detected in their Zn concentrations. Higher
concentrations of Cd and Zn were primarily observed in crabs
from upstream regions of the Xin and Daliao rivers and from
downstream regions of the Wuli, Daliao, Daqing, Fuzhou, and
Yingna rivers (Fig. 3). Mean BAF and BSAF for Cd were higher
in downstream crabs than in upstream crabs. For the coastal
watersheds along the Chinese Northern Bohai and Yellow Seas,
the mean BAF for Zn was higher in downstream crabs than in
upstream crabs, while the mean BSAF for Zn was lower in
downstream crabs than in upstream crabs. We compared our
results with the literature data of the studied areas (Supplemental
Data, Table S2) and found that crabs from downstream in the
Liao River had higher Cd concentrations (Fig. 3) than Orithyia
sinica from the Liao River Estuary. Downstream crabs from
Jinzhou Bay had Cd concentrations higher than previously
reported for clams. However, downstream crabs from the sea
near Huludao had Cd concentrations lower than previously
reported for clams and mussels. The mean Cd concentration in
downstream crabs from coastal watersheds along the Northern
Yellow Sea was lower than previously reported concentration of
Cd in crustaceans from the Yellow Sea. Zinc concentrations in
carp from Jinzhou Bay were higher than those in clams and
mussels previously collected from the same region. However, Zn
concentrations in crabs from the Liao River Estuary and the sea
near Huludao in the present study (Fig. 3) were significantly
837
lower than those in clams and mussels collected in the same
regions (Supplemental Data, Table S2).
To examine the relationships between Cd and Zn, in water,
sediment, and biota (carp and crabs), a correlation table (Pearson
correlation coefficients) was established (Table 3). Cadmium
concentrations in crabs were significantly correlated with Cd and
Zn concentrations in sediments (p < 0.05). Zinc concentrations
in crabs had a significantly positive correlation with Zn in
sediments (p < 0.05). Furthermore, Zn and Cd concentrations in
crabs were significantly correlated with each other (p < 0.01).
Cadmium concentrations in carp were not significantly
correlated with Cd concentrations in water and sediments.
Zinc concentrations in carp were negatively correlated with Cd
concentrations in water (p < 0.01). Cadmium concentrations in
carp were positively correlated with Zn concentrations in water
and sediments (p < 0.01). Cadmium concentrations were
significantly correlated with Zn concentrations not only in
water but also in sediments. No significant correlations were
observed between Cd or Zn concentrations in water and those in
sediments.
DISCUSSION
Cadmium concentrations in waters from upstream were
lower than the Chinese environmental quality standard for
surface water (CEQSSW) Class I criterion (Supplemental Data,
Table S3). The mean concentration of Zn in upstream waters was
below the CEQSSW Class I criterion (Table 1 and Supplemental
Data, Table S3). Except for one water sample taken from
upstream in the Yalu River, which had a concentration of
123 mg Zn/L, all Zn concentrations were below the CEQSSW
Class I criterion.
Cadmium concentrations in waters from downstream were
lower than the Chinese sea water quality standard (CSWQS)
Class I criterion (Supplemental Data, Table S3). However, 67%
of concentrations of Zn in downstream waters, predominantly
located near Qinghuangdao, Huludao, Panjin, and Dalian along
Liaodong Bay of the Northern Bohai Sea, exceeded the CSWQS
Class I criterion. Downstream water from Dalian (DL3)
contained Zn concentrations that exceeded the CSWQS Class
II criterion (Fig. 2 and Supplemental Data, Table S3). Therefore,
most downstream waters from coastal sites along the Northern
Bohai Sea were contaminated with Zn. Several zinc-related
industries in addition to urbanization in Qinghuangdao,
Huludao, Yinkou, and Dalian could be responsible for the Zn
contamination in downstream water.
Based on the U.S. Environmental Protection Agency
guidelines for maximum allowable acute and chronic values
for Cd of 5.7 and 1.3 mg/L [30], and for Zn of 374 and 30 mg/L
[31] in freshwater, respectively, none of the Cd concentrations
Table 3. Correlation coefficients between concentrations of cadmium (Cd) and zinc (Zn) in water, sediment, and biota (number of samples in parentheses)
Pearson correlation
Cd-water
Zn-water
Cd-sediment
Zn-sediment
Cd-biotaa
Zn-biotaa
a
Cd-water
Zn-water
Cd-sediment
Zn-sediment
Cd-biotaa
Zn-biotaa
1
0.52c (36)
0.031 (35)
0.071 (35)
0.26 (28)
0.19 (28)
0.52c (36)
1
0.070 (35)
0.12 (35)
0.33 (28)
–0.20 (28)
0.031 (35)
0.07 0 (35)
1
0.69c (35)
0.46b (28)
0.13 (28)
–0.071 (35)
0.12 (35)
0.69c (35)
1
0.50c (28)
0.38b (28)
0.11 (17)
0.13 (17)
–0.39 (17)
0.011 (17)
1
0.49c (28)
–0.65c (17)
–0.44 (17)
–0.031 (17)
0.13 (17)
–0.080(17)
1
Pearson coefficients for carp and crabs are shown above and below the diagonal line, respectively.
Correlation is significant at the 0.05 level (two-tailed).
c
Correlation is significant at the 0.01 level (two-tailed).
b
838
Environ. Toxicol. Chem. 32, 2013
observed in any river in the present study should produce
potential toxic effects, but 17% of the water samples had Zn
concentrations within the acute and chronic guidelines, which
would indicate some adverse effects on aquatic organisms.
The mean Cd concentration in downstream sediments within
the coastal watersheds was 73% higher than the background
concentration in the marine sediments (95% confidence limits
were 0.080–0.17 mg/kg, dry wt). However, mean Zn concentrations in both upstream and downstream sediments were less
than the regional background concentration (Table 1 and
Supplemental Data, Table S3).
Except for upstream sediments of the Wuli River, concentrations of Cd and Zn in nearly all sediments were less than the
marine sediment quality Class I criteria (Fig. 2 and Supplemental
Data, Table S3). Based on the threshold effect level, the effects
range-low concentration and the probable effect level for Cd and
Zn in sediment (Supplemental Data, Table S3), only 9% of
sediments, located in the upstream regions of the Wuli and Yalu
rivers, had Cd and Zn concentrations above the low-range values
(threshold effect levels or effects range-low concentration; Fig.
2). Thus, only at these sites is there a possibility of toxicity from
Cd and Zn in sediment-dwelling fauna.
Previous reports have indicated that ecosystems of the Wuli
River have been significantly impacted by past and current
loadings of Cd and Zn from certain industrial complexes such as
the Huludao zinc plant (established in 1935) and the Jinzhou
chemical refinery plant (established in 1937) [8,32]. Sediments
of the Yalu River have been polluted with Cd and Zn discharged
by copper mining, automobile manufacturing, paper making,
dyeing, and textile industries in Dandong [14,15]. Furthermore,
Cd and Zn can enter water and sediments from other industrial
activities such as coal combustion, electroplating processes,
iron and steel production, and pigment making, which occur
along the Wuli and Yalu rivers. In addition, agricultural uses
of phosphate fertilizers and sewage sludge and wastewater
discharged from households in coastal cities may be identified
as other sources of Cd and Zn to the water and sediments
[4,5,8,14,15,33].
All of the EF values for Cd and Zn in the sediments were
greater than 1.5, indicating that the sources of Cd and Zn were
likely due to human activity. Based on previously reported
results [27], because mean EF values for Cd were greater than 2,
Cd in up- and downstream sediments should be given more
attention than Zn.
Three composite carp samples from the Dou and Biliu rivers
and a coastal site in Qinghuangdao (Fig. 3) contained Cd
concentrations greater than the quality standard set by the
Ministry of Agriculture of China for the protection of human
health (Supplemental Data, Table S3). Cadmium concentrations
in other carp were below permitted concentration prescribed by
the Food and Agriculture Organization. Carp from most
watersheds were not contaminated with Cd. A total of 60% of
the carp from upstream areas, primarily distributed around
Liaodong Bay, had Zn concentrations higher than standard
regulated by China. However, all downstream carp had Zn
concentrations below this standard. Thus, most upstream carp
contained sufficient Zn concentrations to be deemed unfit for
human consumption.
The bioaccumulation factor provides an indication of
accumulation efficiency of Cd and Zn in muscles of carp. The
data in Table 2 clearly indicate that a high BAF for Cd was
recorded in downstream carp while a high BAF for Zn was
observed upstream carp. Zinc exhibited higher BAFs in the
W. Luo et al.
muscles of carp than Cd. Values of BSAF higher than 1 reveal
that capacities of downstream carp to accumulate Cd and
upstream carp to accumulate Zn are greater than those in
sediments. In carp, the mechanism of bioaccumulation of Cd is
different from that of Zn. This is likely because Zn is a required
element and concentrations in tissues are homeostatically
regulated [34].
Apart from one crab from the upstream region of the Daliao
River (YK2) that contained the highest Cd concentration
(6.3 mg/kg; Fig. 3), concentrations of Cd and Zn in crabs
from other upstream areas were not only less than the limits
prescribed by the Food and Agriculture Organization but were
also less than the standards regulated by China (Supplemental
Data, Table S3). However, approximately 70% of downstream
crabs contained Cd concentrations higher than the concentration
recommended by the Food and Agriculture Organization and
China. Approximately 40% of downstream crabs contained Zn
concentrations greater than the concentration prescribed by
the Food and Agriculture Organization, but none of the Zn
concentrations in crabs exceeded the limit established by China.
It can, therefore, be concluded that muscle residues of Cd
exceeded the guideline trigger values. Given that governmental
guidelines for risk (to aquatic life and to human health) are very
conservative, exceeding them could signify the potential for
risks. In addition, Figure 3 shows that these crabs were primarily
distributed around Liaodong Bay and in the central parts of
coastal regions along the Northern Yellow Sea.
The BAFs and BSAFs for Cd indicate that elevated Cd
concentrations in downstream crabs originate more from water
and food than those in upstream crabs. There was variation of
BAF and BSAF of Zn in crabs. The reason may be that Zn is an
essential metal and has normal physiological regulatory
functions, but can bioaccumulate and reach toxic levels [35].
Concentrations of essential Zn in organisms tend to be highly
regulated compared with nonessential metals such as Cd [34].
Cadmium exhibited relatively higher BAFs and BSAFs than
Zn in muscle of crabs. More attention should be given to
bioaccumulated Cd in muscle of crabs, which can pose potential
risks to humans. By comparing BAFs and BSAFs for Cd and Zn
between carp and crabs, it can be concluded that carp has
relatively high accumulation of Zn while crab has a relatively
high accumulation of Cd. Most biotic factors that influence metal
bioaccumulation are associated with diet and include metal
concentrations in prey species and feeding rate. Therefore, future
studies analyzing Cd and Zn in the most important food sources,
as well as their uptake rates, assimilation efficiencies, and
detoxification mechanisms by crabs, could yield more insights
into the contribution of each pathway [36,37].
The significantly positive correlation between concentrations
of Cd in crabs and concentrations of Cd and Zn in sediments
indicated that the relative abundance of Cd in crabs reflects an
accumulation that is proportional to concentrations of Cd and Zn
in sediments. The positive correlation between the Zn concentrations in crabs with Zn concentrations in sediments suggested
that Zn concentrations increased in muscle of crabs as a result of
indirect exposure through the food chain. Crabs are closely
associated with surface sediments because they are bottom
dwellers. Thus, Cd and Zn can be taken up indirectly by eating
sediment-dwelling invertebrates. Similar results have been
observed in bivalves; concentrations of metals in tissue are
related to concentrations of metals in sediments [38]. A strong
positive association between concentrations of Zn and Cd in
crabs implied that the Cd and Zn originated from a common
Cd and Zn in coastal watersheds of North China
source. Blackmore and Wang (2002) found the same results in
green mussels [39]. Positive relationships between the Cd and
Zn in water and sediment implied that Cd and Zn had common
sources in water and sediment. It has been shown that Cd is
commonly found in association with Zn. Rather surprisingly, no
significant correlations in Cd or Zn concentrations were found
between water and sediment, suggesting that sources of Cd or Zn
in water were likely to differ from those in sediment.
Based on varied environmental concentrations of Cd and Zn
as well as biological characteristics in the fields, single EF, tissue
concentration, BAF, or BSAF could not be used as an indicative
of pollution sources or hazards posed by these metals. Therefore,
different methods should be applied in the investigation of
environmental concentrations of metals and their bioaccumulations in the future.
CONCLUSIONS
Mean concentrations of Cd and Zn in downstream waters
were significantly greater than those in upstream waters within
the coastal watersheds along the Chinese Northern Bohai and
Yellow Seas. This fact was especially true for waters in the
watersheds along the Northern Bohai Sea. Most downstream
waters were contaminated by Zn. Apart from upstream areas of
the Wuli and Yalu rivers, concentrations of Cd and Zn in
sediments were not sufficient to cause adverse effects on the
sediment-dwelling fauna. Cadmium and Zn were present in the
highest concentrations in water and sediment of up- and
downstream areas of the Liugu, Wuli, Daliao, and Yalu rivers.
Based on measured enrichment factors, Cd contamination in all
sediments is of concern. Mean Zn concentration in upstream
carp was higher than that in downstream carp. Upstream carp
from the Northern Bohai Sea had a greater mean concentration of
Zn than upstream carp from the Northern Yellow Sea. The mean
Cd concentration in downstream crabs from the coastal
watersheds along the Northern Bohai Sea was greater than
that in downstream crabs from the coastal watersheds along
the Northern Yellow Sea. Concentrations of Cd and Zn in
most waters and sediments were below the published values,
indicating a recent improvement in water and sediment qualities.
Compared to the literature, concentrations of Cd and Zn in most
carp and crabs can be considered low. Downstream carp and
crabs had higher mean BAFs and BSAFs for Cd than upstream
carp and crabs, while upstream carp and crabs had higher BSAFs
for Zn than downstream carp and crabs. Concentrations of Cd
and Zn in crabs were significantly correlated with those in
sediments, indicating that both the Cd and the Zn in the crabs
originated from the sediments. Cadmium and Zn shared
common sources in water and sediment. However, sources of
Cd or Zn in water were likely to differ from those in sediment.
SUPPLEMENTAL DATA
Tables S1–S3. (215 KB DOC).
Acknowledgement—This research was supported by the National Natural
Science Foundation of China under grants 41271502 and 41071355,
Strategic Priority Research Program of the Chinese Academy of Sciences,
Grant No. XDB03030504, the National International S&T Cooperation
Program under grant 2012DFA91150, the Einstein Professorship Program,
Chinese Academy of Sciences, and the Project of the State Key Lab of Urban
and Regional Ecology under grant SKLURE2008-1-04. Portions of the
research were supported by a Discovery Grant from the Natural Science and
Engineering Research Council of Canada (Project 6807). We are grateful to
two anonymous reviewers and the editor for their constructive comments and
suggestions.
Environ. Toxicol. Chem. 32, 2013
839
REFERENCES
1. Liu W, Chen J, Lin X, Fan Y, Tao S. 2007. Residual concentrations of
micropollutants in benthic mussels in the coastal areas of Bohai Sea,
North China. Environ Pollut 146:470–477.
2. Cao W, Wong MH. 2007. Current status of coastal zone issues and
management in China: A review. Environ Int 33:985–992.
3. Wei M, He B. 2004. Change trend of water environment index in recent
20a in Jinzhou Bay and content distribution of trace metal and its source
analysis. Mar Environ Sci 29–32, (in Chinese).
4. Xu B, Yang X, Gu Z, Zhang Y, Chen Y, Lv Y. 2009. The trend and
extent of heavy metal accumulation over the last one hundred years in the
Liaodong Bay, China. Chemosphere 75:442–446.
5. Ma J, Shao M. 1994. Variation in heavy offshore sedimentary metal
pollution of cores in Jinzhou Bay. China Environ Sci 14:22–29, (in
Chinese).
6. Luo W, Wang T, Jiao W, Hu W, Naile EJ, Khim JS, Giesy PJ, Lu Y.
2012. Mercury in coastal watersheds along the Chinese Northern Bohai
and Yellow Seas. J Hazard Mater 215–216:199–207.
7. Wang S, Jia Y, Wang S, Wang X, Wang H, Zhao Z, Liu B. 2009. Total
mercury and monomethylmercury in water, sediments, and hydrophytes
from the rivers, estuary, and bay along the Bohai Sea coast, northeastern
China. Appl Geochem 24:1702–1711.
8. Zheng N, Wang Q, Liang Z, Zheng D. 2008. Characterization of heavy
metal concentrations in the sediments of three freshwater rivers in
Huludao City, Northeast China. Environ Pollut 154:135–142.
9. Chen J, Liu W, Liu S, Lin X, Tao S. 2004. An evaluation on heavy
metal contamination in the surface sediments in Bohai Sea. Mar Sci
28:16–21, (in Chinese).
10. Feng M, Long J, Yu L, Li J. 2003. Ecological risk evaluation of heavy
metals of marine sediment in Liaodong Bays shallow waters. Mar Sci
27:52–56, (in Chinese).
11. Zhang Y, Wang L, Huo C, Guan D. 2008. Assessment on heavy metal
pollution in surface sediments in Jinzhou Bay. Mar Environ Sci 27:178–
181, (in Chinese).
12. Bennet-Chambers M, Davies P, Knott B. 1999. Cadmium in aquatic
ecosystems in Western Australia: A legacy of nutrient-deficient soils.
J Environ Manage 57:283–295.
13. Wan L, Wang N, Li Q, Sun B, Zhou Z, Xue K, Ma Z, Tian J, Song L.
2008. Distribution of dissolved metals in seawater of Jinzhou Bay,
China. Environ Toxicol Chem 27:43–48.
14. Luo W, Lu Y, Wang T, Hu W, Jiao W, Naile JE, Khim JS, Giesy JP.
2010. Ecological risk assessment of arsenic and metals in sediments of
coastal areas of northern Bohai and Yellow Seas, China. Ambio 39:367–
375.
15. Gao J, Li J, Wang Z, Wang Y, Bai F, Cheng Y. 2008. Heavy metal
distribution and their influence factors in sediments of Yalu River
Estuary and its adjacent Sea area. Geochim 37:430–438, (in Chinese).
16. Wang Y, Liang L, Shi J, Jiang G. 2005. Study on the contamination of
heavy metals and their correlations in mollusks collected from coastal
sites along the Chinese Bohai Sea. Environ Int 31:1103–1113.
17. Bervoets L, Blust R. 2003. Metal concentrations in water, sediment and
gudgeon (Gobio gobio) from a pollution gradient: Relationship with fish
condition factor. Environ Pollut 126:9–19.
18. Patterson CC, Settle DM. 1976. Accuracy in Trace Analysis: Sampling,
Sample Handling, and Analysis. US. National Bureau of Standards
Special Publication 422. U.S. Government, Printing, Office, Washington, DC.
19. U.S. Environmental Protection Agency. 1992. Test methods for
evaluating solid waste: Physical/chemical methods, 3rd ed. SW-846.
Washington, DC.
20. Kimbrough KL, Lauenstein GG. 2006. Trace metal analytical methods
of the National Status and Trends Program: 2000–2006. U.S.
Department of Commerce, NOAA Technical Memorandum 29. Silver,
Spring, MD, USA.
21. Sinex SA, Wright DA. 1988. Distribution of trace metals in the
sediments and biota of Chesapeake Bay. Mar Pollut Bull 19:425–
431.
22. Mucha AP, Vasconcelos MTSD, Bordalo AA. 2003. Macrobenthic
community in the Doura estuary: Relations with trace metals and natural
sediment characteristics. Environ Pollut 121:169–180.
23. Ghrefat H, Yusuf N. 2006. Assessing Mn, Fe, Cu, Zn, and Cd pollution
in bottom sediments of Wadi Al-Arab Dam, Jordan. Chemosphere
65:2114–2121.
24. Geology Laboratory of the Institute of Oceanology of the Chinese
Academy of Sciences. 1985. Bohai Geology. Science Press, Beijing,
China, (in Chinese).
840
Environ. Toxicol. Chem. 32, 2013
25. Chinese National Environmental Monitoring Center. 1990. The
Background Concentrations of Soil Elements in China. Chinese
Environmental Science Press, Beijing, China, (in Chinese).
26. Zhang J, Liu CL. 2002. Riverine composition and estuarine geochemistry of particulate metals in China—weathering features, anthropogenic
impact and chemical fluxes. Estuar Coast Shelf Sci 54:1051–1070.
27. Han YM, Du PX, Cao JJ, Posmentier ES. 2006. Multivariate analysis of
heavy metal contamination in urban dusts of Xi’an, Central China. Sci
Total Environ 355:176–186.
28. Gobas FAPC, Morrison HA. 2000. Bioconcentration and biomagnification in the aquatic environment. In Boethling RS, Mackay D, eds,
Handbook of Property Estimation Methods for Chemicals. Lewis, Boca
Raton, FL, USA, pp 189–231.
29. Schmitt CJ, Brumbaugh WG. 1990. National contaminant biomonitoring program: Concentrations of arsenic, cadmium, copper, lead,
mercury, selenium, and zinc in U.S. freshwater fish, 1976–1984. Arch
Environ Contam Toxicol 19:731–747.
30. U.S. Environmental Protection Agency. 1986. Quality criteria for
water. Office of Water Regulations and Standards, EPA 440/5-85/001.
Washington, DC.
31. U.S. Environmental Protection Agency. 1982. Ambient aquatic life
water quality criteria for zinc. Office of Water Regulations and
Standards, EPA 440/5-80/079. Washington, DC.
W. Luo et al.
32. Zheng N, Wang Q, Zheng D. 2007. Mercury contamination and health
risk to crops around the zinc smelting plant in Huludao City, northeastern
China. Environ Geochem Health 29:385–393.
33. Hu N, Shi X, Huang P, Liu JH. 2010. Distribution of metals in surface
sediments of Liaodong Bay, Bohai Sea. Chin Environ Sci 30:380–388,
(in Chinese).
34. Fernandesa C, FontaÍnhas-Fernandes A, Peixotoc F, Salgado MA. 2007.
Bioaccumulation of heavy metals in Liza saliens from the Esmoriz–
Paramos coastal lagoon, Portugal. Ecotox Environ Saf 66:426–431.
35. Rainbow PS, Luoma SN. 2011. Metal toxicity, uptake and bioaccumulation in aquatic invertebrates—Modelling zinc in crustaceans. Aquat
Toxicol 105:455–465.
36. Reinfelder JR, Fisher NS, Luoma SN, Nichols JW, Wang WX. 1998.
Trace element trophic transfer in aquatic organisms: A critique of the
kinetic model approach. Sci Total Environ 219:117–135.
37. Wang WX, Rainbow PS. 2010. Significance of metallothioneins in metal
accumulation kinetics in marine animals. Comp Biochem Phys C 152:1–8.
38. de Astudillo L, Yen I, Bekele I. 2005. Heavy metals in sediments,
mussels and oysters from Trinidad and Venezuela. Rev Biol Trop 53:
41–53.
39. Blackmore G, Wang W. 2002. Uptake and efflux of Cd and Zn by the
green mussel Perna viridis after metal preexposure. Environ Sci Technol
36:989–995.
1
Supplemental Data
MANUSCRIPT TITLE:
Environmental concentrations and bioaccumulations of
cadmium and zinc in coastal watersheds along the Chinese
Northern Bohai and Yellow Seas
AUTHORS:
Wei Luo, Yonglong Lu, Tieyu Wang, Wentao Jiao, Wenyou Hu,
Jonathan E. Naile, Jong Seong Khim, John P. Giesy
ADDRESS:
State Key Lab of Urban and Regional Ecology, Research Center for
Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing
100085, China
Department of Veterinary Biomedical Sciences and Toxicology
Centre, University of Saskatchewan, Canada
NO. OF FIGURES:
0
NO. OF TABLES:
3
NO. OF PAGES:
4
2
Table S1. Sample details of all sampling sites along the Chinese Northern Bohai and Yellow Seas (CNBYS)
Sampling
Sub-sample number
Latitude
(º)
118.19920
Water a
Sediment a
Crab b
Carp b
TS1
Longitude
(º)
39.51171
5
5
0
4
Qionglong River
TS2
39.26820
118.52379
5
5
6
0
Bohai Sea
TS3
39.14441
118.33938
5
5
7
0
Shuanglong River
TS4
39.19876
118.33888
5
5
0
0
Bohai Sea
TS5
39.41793
119.27580
5
5
5
0
Luan River
TS6
39.46074
119.13412
5
5
5
0
Luan River
TS7
39.58211
118.80655
5
5
0
0
Bohai Sea
QH1
39.70235
119.33615
5
5
4
6
Xin River
QH2
39.84100
119.51119
5
5
5
8
Xin River
QH3
39.83960
119.51538
5
5
8
3
Bohai Sea
QH4
39.83131
119.52674
5
5
3
4
Tianma River
QH5
39.98022
119.21003
5
5
5
4
Bohai Sea
HL1
40.19749
120.37373
5
5
3
0
Liugu River
HL2
40.25276
120.35999
5
5
4
0
Liugu River
HL3
40.36981
120.25814
5
5
7
3
Wuli River
HL4
40.72748
120.89366
5
5
3
0
Bohai Sea
HL5
40.69957
120.94760
5
5
6
5
Daling River
JZ2
41.08476
121.13304
5
5
0
5
Daling River
JZ3
41.39898
121.41084
5
5
0
6
Daling River
JZ4
41.17702
121.37771
5
5
8
0
Bohai Sea
JZ5
40.90400
121.73938
5
5
5
0
Shuangtaizi River
PJ1
41.09955
121.59080
5
5
3
6
Bohai Sea
PJ2
40.81268
121.98571
5
5
4
0
Daliao River
YK1
40.82095
122.13346
5
5
5
0
Bohai Sea
YK2
40.66532
122.16431
5
5
5
5
Bohai Sea
YK3
40.42683
122.27681
5
5
3
4
Bohai Sea
DL1
39.61074
121.49876
5
5
8
0
Fuzhou River
DL2
39.69397
121.73738
5
5
0
8
Bohai Sea
DL4
38.99975
121.30857
5
5
0
0
Yellow Sea
DL3
38.87093
121.55736
5
0
0
6
Biliu River
DL5
39.46474
122.50038
5
5
5
0
Yellow Sea
DL6
39.65726
122.98590
5
5
4
7
Dayang River
DD1
39.94152
123.62830
5
5
0
0
Yalu River
DD2
40.17621
124.45491
5
5
0
0
Yellow Sea
DD3
39.94077
124.28782
5
5
0
5
Yalu River
DD4
40.00564
124.36262
5
5
0
0
Sea
Coastal region
River/Sea
Site
Northern Bohai Sea
Tangshan
Dou River
Qinhuangdao
(Liaodong Bay)
Huludao
Jinzhou
Panjin
Yingkou
Dalian
Northern Yellow Sea
Dandong
a
b
A composite sediment sample contained five collected sub-samples.
A composite sample of carp or crab contained three the same species individuals from the collected sub-samples.
3
Table S2. Mean concentrations and standard deviations for cadmium and zinc in water (μg/l), sediment (mg/kg,
dry weight) and biota (mg/kg, wet weight) in coastal watersheds along the CNBYS in previous studies
Sampling
Cd
Zn
Reference
Sample
Sampling location
size
River water
Dou River
7
6.2±9.6
—
[1]
River water
Luan River
6
1.8±1.3
—
[2]
Sea water
Daliao Estuary
3
0.15±0.080
39±5.3
[3]
Sea water
Yalu Estuary
6
0.43±0.30
—
[4]
Sea water
Bohai Sea
42
0.45±0.15
8.1±2.1
[5]
Sea water
Jinzhou Bay, Bohai Sea
90
1.9±0.65
28±19
[6]
Sea water
Liaodong Bay, Bohai Sea
160
1
31.5
[7]
Sea water
Northern Yellow Sea
74
0.19±0.05
6.0±1.8
[5]
River sediment
River sediment
River sediment
River sediment
Marine sediment
Marine sediment
Marine sediment
Marine sediment
Marine sediment
Marine sediment
Pomfret
Blue-spot sierra
Gobies
Wolf goby
Fish
Orithyia sinica
Hairy clam
Four angle clam
Hairy clam
Short necked clam
Four angle clam
Chinese clam
Mussel
Crustacean
Luan River
Wuli River
Liao River
Daliao River
Daliao Estuary
Yalu Estuary
Estuaries around Liaodong Bay
Northern Yellow Sea
Jinzhou Bay
Liaodong Bay
10
10
8
8
3
48
22
145
14
56
2
4
3
1
—
1
2
3
3
5
2
2
2
—
0.15±0.12
8±11
1.3±1.1
1.1±1.6
0.16±0.11
0.24±0.15
1.2±1.9
—
248.1±266.8
0.1±0.1
76±46
525±576
174.7±208.2
87.5±40.2
30±17
108.4±7.8
105.3±60.4
65.6±16.1
6419±5342.3
57.8±18.8
[8]
[9]
[10]
[11, 12]
[3]
[13]
[14]
[15]
[16]
[17]
0.28±0.20
0.28±0.23
0.45±0.15
0.88
0.26
1.21
0.59±0.0025
0.72±0.14
29.3±8.5
8.4±12.1
0.83±0.33
5.3±0.71
14±0.71
0.92
26.08±5.9
14.8±1.8
23.2±8.7
47.3
10.05
92.7
27.2±10.4
20.8±15.2
92.7±33
79.1±68.4
96.3±77.7
50.7±11.5
72±30.3
52
[18]
[18]
[18]
[19]
[20]
[19]
[21]
[21]
[18]
[18]
[18]
[18]
[18]
[20]
“
”
Sea near Huludao
Sea near Huludao
Sea near Huludao
Liao River Estuary
Yellow Sea
Liao River Estuary
Jinzhou Bay
Jinzhou Bay
Sea near Huludao
Sea near Huludao
Sea near Huludao
Sea near Huludao
Sea near Huludao
Yellow Sea
— indicates that data is not available.
4
Table S3. Guidelines for water, sediment and biota
Guidelines
Cd
Zn
Referernce
Chinese environmental quality standard for surface water-Class I (μg/l)
1
50
[22]
Chinese environmental quality standard for surface water-Class II (μg/l)
5
100
[22]
Chinese sea water quality standard- Class I (μg/l)
1
20
[23]
Chinese sea water quality standard-Class II (μg/l)
5
50
[23]
Sediment background for Chinese rivers (mg/kg, dw)
0.13
68
[24]
Sediment background for the Northern Bohai and Yellow Seas (mg/kg, dw)
0.069
57
[25]
Chinese marine sediment quality-Class I (mg/kg, dw)
0.5
150
[26]
Sediment threshold effect level (TEL) (mg/kg, dw)
0.6
123
[27]
Sediment probable effect level (PEL) (mg/kg, dw)
3.53
315
[27]
Sediment effect range low (ERL) (mg/kg, dw)
5
120
[27]
Sediment effect range median (ERM) (mg/kg, dw)
9
410
[27]
Limit standard for the toxic substance in fishes (mg/kg, ww)
0.1
40
[28]
Limit standard for the toxic substance in crustaceans (mg/kg, ww)
0.50
150
[28]
5
REFERENCES
[1] Gong X. 2009. Water quality monitoring and pollution source analying of Dou River in city (in Chinese)
Journal of Hebei PolytechnicUniversity 31:132-136.
[2] Li Y, liu J. 2009. Health Risk Assessment on Heavy Metai Pollution in the Water Environment of Luan
River. Journal of Agro-Environment Science 28:1177-1184 (in Chinese).
[3] Liu J, Sun Q, Mo C, Guo N. 2008. The Pollution Status and Characteristics of Daliaohe Estuary and its
Adjacent Sea Area. Fisheries Science 27:286-289 (in Chinese).
[4] Liang T. 2005. Water contmanination and prevention along the coastal area of Dandong. Liaoning Urban
and Rural Environmental Science & Technology 25:21-23(in Chinese).
[5] TIAN L, Chen H, DU J, WANG X. 2009. Factors influencing distribution of soluble heavy metals in North
Yellow Sea surface seawaters. Periodical of Ocean University of China 39:617-621.
[6] Wan L, Wang N, Li Q, Sun B, Zhou Z, Xue K, Ma Z, Tian J, Song L. 2008. Distribution of dissolved metals
in seawater of Jinzhou Bay, China. Environ Toxicol Chem 27:43-48.
[7] Wan L, Wang NB, Li QB, Zhou ZC, Sun B, Xue K, Ma ZQ, Tian J, Du N. 2008. Estival distribution of
dissolved metal concentrations in liaodong bay. Bulletin of Environmental Contamination and Toxicology
80:311-314.
[8] Liu J, Li Y, Zhang B, Cao J, Cao Z, Domagalski J. 2009. Ecological risk of heavy metals in sediments of the
Luan River source water. Ecotoxicology 18:748-758.
[9] Zheng N, Wang Q, Liang Z, Zheng D. 2008. Characterization of heavy metal concentrations in the sediments
of three freshwater rivers in Huludao City, Northeast China. Environ Pollut 154:135-142.
[10] Shi J, Yu W, liu Z, Wang D. 1995. Heavy metal pollution and their potential ecological hazards in
Shuangtaizi River. Irrigation Works and Fishery:21-24 (in Chinese).
[11] Fan Y, Lin C, He M, Yang Z. 2008. Transport and Bioavailability of Cu , Pb , Zn and Ni in Surface
Sediments of Daliao River Watersystem. Environmental Science 29:3469-3476 (in Chinese).
[12] Fan Y, Lin C, He M, Yang Z. 2008. Kinetics and bioavailability of Cd in the surface sediments of the Daliao
River watersystem. Acta Scientiae Circumstantiae 28:2583-2589 (in Chinese).
[13] Gao J, Li J, Wang Z, Wang Y, Bai F, Cheng Y. 2008. Heavy metal distribution and their influence factors in
sediments of Yalu River Estuary and its adjacent Sea area. Geochim 37:430-438 (in Chinese).
[14] Zhou X, Wang E, Liu X, Wang W. 2004. Environmental geochemistry of heavy metals in bottom sediments
of the river mouths in Liaodong Bay. Geochimica 33:286-290 (in Chinese).
[15] Zou J, Shi X, Li S. 2007. Distributions of minor elements in near surface sediments in North Yellow Sea and
the early diagenesis. Marine Geology & Quaternary Geology 27:43-50 (in Chinese).
[16] Zhang Y, Wang L, Huo C, Guan D. 2008. Assessment on heavy metals pollution in surface sediments in
Jinzhou Bay. Mar Environ Sci 27:178-181(in Chinese).
[17] Hu N, Shi X, Huang P, Liu JH. 2010. Distribution of metals in surface sediments of Liaodong Bay, Bohai
Sea. China Environmental Science 30:380-388 (in Chinese).
[18] Yue L, Shi B. 2001. Monitoring the contaminated situation of the aquatic animals caused by heavy metals in
the inshore maritime area of Hulu island. Environmental Monitoring in China 17:45-47 (in Chinese).
[19] Ma MH, Hai Z, Feng Z, Guan C, Chen H. 1999. Study on the contents, temporal and spatial trends of the
contaminants in the marine animals along the coastal area near the mouth of Shuangtaihe river Liaodong Bay.
Marine Environmental Science 18:61-64,76 (in Chinese).
[20] Wei X, Tong J. 1993. The Pollution State of Huanghai (Yellow Sea) and Bohai Seas and in Ecolgical Impact.
Journal of Oceanography of Huanghai and Bohai Seas 11:76-82 (in Chinese).
[21] Wan L, Wang N, Ding Q, Zhang Q, Yu B. 2009. The distribution of heavy metal pollution in Jinzhou Bay,
Bohai Sea. Fisheries Science 28:801-804 (in Chinese).
[22] SEPAC (State Environment Protection Administration of China). 2002. Environmental quality standard for
surface water (GB 3838-2002) (in Chinese).
[23] SEPAC (State Environment Protection Administration of China). 1997. Sea water quality standard (GB
3097-1997) (in Chinese). Vol GB 3097-1997.
[24] Ma L, Yang X, Tong C, Wu A, Liu M. 2008. The geochemical characteristics of heavy metal elements in
sediments of Hunhe drainage area in Liaoning Province Rock Miner Anal 27:184-188 (in Chinese).
[25] Luo W, Lu Y, Wang T, Hu W, Jiao W, Naile JE, Khim JS, Giesy JP. 2010. Ecological risk assessment of
arsenic and metals in sediments of coastal areas of northern Bohai and Yellow Seas, China. Ambio 39:367-375.
[26] CSBTS(China State Bureau of Quality and Technical Supervision). 2002. National Standards GB
18668-2002-Marine Sediment Quality (GB 18668-2002). The People's Republic of China, p. 10 (in Chinese).
[27] MacDonald DD, Ingersoll CG, Berger TA. 2000. Development and evaluation of consensus-based Sediment
Quality Guidelines for freshwater ecosystems. Arch Environ Contam Toxicol 39:20-31.
5
6
[28] Ministry of Agriculture PRC. 2006. The limit standard for the toxic substance in the non-environmental
pollution aquatic products (NY 5073-2006) (in Chinese).
6