See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/348097830

Bioaccumulation and human health risk assessment of trace metals in the

freshwater mussel Cristaria plicata in Dongting Lake, China

Article  in  Journal of Environmental Sciences · June 2021

DOI: 10.1016/j.jes.2020.12.012

CITATIONS READS

4 200

7 authors, including:

Dianbao Li Baozhu Pan

Xi’an University of Technology Changjiang River Scientific Research Institute
5 PUBLICATIONS   6 CITATIONS    70 PUBLICATIONS   883 CITATIONS   

SEE PROFILE SEE PROFILE

Liang Chen Wang Jun

Chinese Academy of Sciences Xi'an University of Technology
26 PUBLICATIONS   803 CITATIONS    11 PUBLICATIONS   10 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

wind induced flow velocities and their role in destratification, nutrients resuspension and hypoxia reduction View project

freshwater ecology View project

All content following this page was uploaded by Dianbao Li on 15 January 2021.

The user has requested enhancement of the downloaded file.

 journal of environmental sciences 104 (2021) 335–350

Available online at www.sciencedirect.com

www.elsevier.com/locate/jes

Bioaccumulation and human health risk

assessment of trace metals in the freshwater
mussel Cristaria plicata in Dongting Lake, China

Dianbao Li, Baozhu Pan∗, Liang Chen, Yuzhu Wang, Taoyi Wang, Jun Wang,
Hao Wang
State Key Laboratory of Eco-hydraulic in Northwest Arid Region of China, Xi’an University of Technology, Xi’an
710048, Shaanxi, China

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

Article history: Trace metal contamination in water and bioaccumulation in aquatic organisms are human
Received 17 September 2020 health risks of increasing concern. However, the bioaccumulation of trace metals in the or-
Revised 8 December 2020 gans of the mussel Cristaria plicata in Dongting Lake, China and the human health risks of
Accepted 9 December 2020 mussel consumption are largely unknown. We investigated the concentrations of 15 trace
metals and metalloids in surface water, sediments, and C. plicata organs (foot, gill, mantle,
and visceral mass) and quantified the bioaccumulation and human health risk of these trace
Keywords: metals in specimens collected from Dongting Lake. The concentrations of most metals in
Trace metals surface water exceeded previously published background values. In contrast, the concen-
Bioaccumulation trations of most metals in sediments showed a decreasing trend. Overall, the metal concen-
Health risks trations in the gill and visceral masses of C. plicata were higher than those in the foot and
Cristaria plicata mantle, and higher bioaccumulation capacities were observed for essential metals than for
Dongting lake nonessential metals. The mean concentrations of the trace elements Zn, Pb, Cd, As, Cu, and
Cr in C. plicata foot samples were lower than the threshold values established by interna-
tional and Chinese organizations. The estimated daily intake (EDI) values of the essential
metal Mn in C. plicata foot was higher than the recommended tolerable daily intake (TDI)
values for juveniles. Only Mn for juveniles and As for both juveniles and adults may pose
noncarcinogenic health risks through foot consumption. The hazard index (HI) values for
adults and juveniles were higher than 1, suggesting significant risks of noncarcinogenic ef-
fects to humans by exposure to multiple metals.

© 2020 The Research Center for Eco-Environmental Sciences, Chinese Academy of

Sciences. Published by Elsevier B.V.

industrial and agricultural production (Omwene et al., 2018;

Introduction
Water pollution is a worldwide problem eliciting continued
concern, and is mainly caused by activities of human life and
Alahabadi et al., 2018). With the development of industrializa-
tion and urbanization, high amounts of industrial wastewa-
ter, agricultural runoff, urban domestic sewage and municipal
solid waste enter aquatic environments (Khosravi et al., 2011;

∗
Corresponding author.
E-mails: liberty0117@163.com (D. Li), zhuzipan@xaut.edu.cn (B. Pan).

https://doi.org/10.1016/j.jes.2020.12.012
1001-0742/© 2020 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V.
336 journal of environmental sciences 104 (2021) 335–350
Kilunga et al., 2017; Li et al., 2017). Without effective purifica-
tion, these wastewaters carry many pollutants into rivers and
lakes, including trace metals, which could cause a series of
problems for the environment and human health (Zhang et al.,
2017; Sun et al., 2017). Only small amounts of trace metals re-
main in the water column after they are discharged into the
aquatic ecosystem, and most of them are eventually deposited
in sediments (Malvandi, 2017), with more than 90% of trace
metals found in sediments (Salomons and Mook, 1977). How-
ever, sediment resuspension and desorption reactions may
occur, and many metals are again released into the water col-
umn under certain environmental conditions (IP et al., 2005).
The dissolved and particulate metals in water and sedi-
ment are easily absorbed by aquatic organisms, including fish,
shrimp, mussels, etc. For instance, trace metals enter mus-
sels, and fish directly ingest water and food through the di-
gestive tract as well as through permeable membranes, such
as gills, muscles, and tendons (Liu et al., 2001; Ribeiro et al.,
2005). Thus, trace metals participate in the biogeochemical cy-
cle and could bioaccumulate and biomagnify in the aquatic
food chain/web (Zhang et al., 2011; Atwell et al., 1998). Aquatic
organisms are inevitably impacted by favorable or harmful ef-
fects, which mainly depend on the concentration and bioavail-
ability of these metals in the environment (Rajeshkumar et al.,
2018; Bonsignore et al., 2018). Certain trace metals exhibit the
characteristics of toxicity, vast sources, nondegradability, sub-
sequent bioaccumulation and persistence in the aquatic en-
vironment (Gao et al., 2016; Ke et al., 2017; Islam et al., 2015).
Certain metals are essential for the physiological activities
of animals, and they are termed essential metals. However,
their dose determines their toxicity; thus, essential metals
may be toxic to organisms in excess of certain concentrations
(Merciai et al., 2014). Aquatic products, such as fish, shrimp,
and mussels, contain high contents of proteins and polyunsat-
urated fatty acids but low contents of saturated fats, and are
an important part of the human diet for a multitude of peo-
ple living in different parts of the world (Ersoy and Elik, 2010;
Mziray and Kimirei, 2016). Some aquatic animals such as fish,
shrimp and mussels acquire more trace metals along the food
chain/web because the metals occur at relatively high trophic
levels, which may result in health risks to humans when con-
taminated aquatic products containing higher than the al-
lowed daily intake levels are consumed (Ahmad et al., 2010;
Solgi and Mohammadi Galangashi, 2018).
China is the largest producer of aquatic products world-
wide and accounts for nearly 70% of world aquaculture pro-
duction (Li et al., 2011). Freshwater bivalves/mussels are one of
the most important members of aquatic ecosystems and pro-
vide important ecological functions and services (Vaughn and
Hakenkamp, 2001; Aldridge et al. 2007). Filter-feeding fresh-
water mussels, with a large size, long life cycle and relatively
fixed habitats, present a notable ability to filter algae and en-
rich pollutants to a certain extent. Therefore, they have been
adopted worldwide as bioindicators in biological monitoring
surveys (Lecoeur et al., 2004; Xia and Liu, 2011). The freshwa-
ter mussel Cristaria plicata widely occurs in large rivers, lakes,
and reservoirs and is also considered a filter feeder in aquatic
ecosystems (He et al., 2014; Xu et al., 2017). C. plicata is an eco-
nomically important species for aquaculture production and
a freshwater pearl industry cultivar in China (Wen et al., 2006;
Hu et al., 2012).
As an important ecological and economic zone, Dongting
Lake constitutes a major source of fishery production and
feeds a population of millions in the Yangtze River basin in
China (Zhou et al., 2016). With the rapid development of the
economy and society, the intensification of intensive anthro-
pogenic activities, such as the construction of water conser-
vancy projects, has caused increasing pollution in Dongting
Lake (Zhou et al., 2016; Wang et al., 2018b). To protect the eco-
logical environment of Dongting Lake, the implementation of
protection projects has achieved excellent results in control-
ling the external inputs (Zhu and Yang, 2018). However, serious
lake pollution remains, and the concentrations of metals such
as Cr, Cu, Pb, Cd, and the metalloid As in sediments are rela-
tively high (Liang et al., 2015). Certain elements, such as the
metalloid As and metals Cd and Pb are typical pollutants in
the Dongting Lake area, which are affected mainly by anthro-
pogenic activities (mining, emissions exhaust, sewage irriga-
tion, use of products containing heavy metals above standard
levels, etc.) (Zhang et al., 2018b; Wang et al., 2018a). To date,
there is limited information on the associated bioaccumula-
tion of trace metals and the human health risks of the con-
sumption of contaminated freshwater mussels from Dongting
Lake.
Consequently, the main objectives of this study were to
determine the concentrations of trace metals in the surface
water and sediments as well as the bioaccumulation of trace
metals in the organs of C. plicata collected from Dongting Lake,
China. Moreover, the potential risk to human health from the
ingestion of C. plicata foot tissue was evaluated by the esti-
mated daily intake (EDI) and target hazard quotient (THQ).
Thus, the results of this study are beneficial for the environ-
mental protection of Dongting Lake and food safety evaluation
of aquatic products.
1. Materials and methods
1.1. Study area and sampling location
Dongting Lake (28°30 -30°20 N, 111°40 -113°10 E), located in
the south of the middle reaches of the Yangtze River, is the
second largest freshwater lake in China, with a catchment
area of approximately 2625 km2 . The mean and maximum
depths are 6.39 m and 18.67 m, respectively (Zhang et al., 2016;
Wang et al., 2018b). The lake is a seasonally dynamic sys-
tem and experiences a characteristic subtropical monsoon cli-
mate originating from the southeast Pacific Ocean and the In-
dian Ocean, and it has distinct wet and dry periods every year
(Dai et al., 2016). At high and low water levels, extensive sur-
face water and an array of mudflats occur, respectively. Cur-
rently, the lake is geographically divided into three parts: east-
ern Dongting Lake (EDL), western Dongting Lake (WDL), and
southern Dongting Lake (SDL) (Liu et al., 2018a). To obtain an
overall picture of the trace metal pollution in Dongting Lake,
three areas across the main fishery areas of the lake were se-
lected to collect surface water, sediment, and C. plicata sam-
ples (Fig. 1).
 journal of environmental sciences 104 (2021) 335–350 337

Fig. 1 – Study area and sampling site locations. The lake is fed by four major rivers (Xiang River, Zi River, Yuan River, and Li
River) in Hunan Province and three channels (Songzi, Taiping, and Ouchi) directly connected to the Yangtze River, China.
Currently, it is divided geographically into three parts, namely the Eastern Dongting Lake (EDL), Western Dongting Lake
(WDL), and Southern Dongting Lake (SDL). Nine sampling sites were established in each sampling area.

1.2. Sample collection and processing
Surface water, sediment and C. plicata samples were collected
from the EDL, SDL, and WDL areas in October 2018, when
Dongting Lake exhibited a normal water level of 24.78 m
(Fig. 1). Nine sampling sites were established in each sam-
pling area, and surface water and sediment samples were col-
lected at each site. Polyethylene bottles were washed with
10% (V/V) nitric acid (HNO3 , guaranteed reagent (GR) grade,
Xilong Scientific Co., Ltd., China), and 500-mL water samples
(0-0.5 m depth) were collected at each site and immediately
filtered through a 0.45-μm polyethersulfone membrane (ø 47-
mm, Jinlong company, China). The processed water samples
were acidified to pH < 2 with HNO3 (65%-68%, GR grade, Xilong
Scientific Co., Ltd., China) and then transported to the labora-
tory, where they were stored at 4°C before determination. Sur-
face sediments (0-10 cm) were collected with a Peterson grab
sampler, kept on ice in the field, transported to the laboratory,
and stored in a refrigerator at -80°C. The samples were freeze-
dried, ground, and sieved through a 100-mesh sieve. Then, the
dried sediment samples were immediately stored in a desic-
cator before determination.
Two to three C. plicata samples were collected at each site,
and a total of 20 samples were collected in each area. The size
of the C. plicata samples is listed in Appendix A Table S1. The
C. plicata samples were placed in an icebox and immediately
transported to the laboratory, where they were dissected. Four
organs, including foot, gill, mantle, and visceral masses, were
collected, weighed (wet weight, ww), freeze-dried, weighed
again (dry weight, dw), and ground. The powdered organ sam-
338 journal of environmental sciences 104 (2021) 335–350
ples were immediately stored in a desiccator before metal
concentration determination.
The surface sediment and C. plicata organ samples were
treated with a microwave digestion system (ETHOS UP, Mile-
stone Inc., Italy). Approximately 0.1 g (accurate to 0.0001 g)
of the dried sediment samples was treated with an acid mix-
ture (6 mL HNO3 (65%-68%, GR grade), 3 mL HCl (36%-38%, GR
grade), Xilong Scientific Co., Ltd., China) and 2 mL HF (40%,
GR grade, Xilong Scientific Co., Ltd., China). Approximately 0.2
g (accurate to 0.0001 g) of the dried C. plicata organ samples
was treated with an acid mixture (8 mL HNO3 (65%-68%, GR
grade) and 2 mL H2 O2 (30%, GR grade), Xilong Scientific Co.,
Ltd., China). All samples were digested by the following pro-
cess: the temperature was raised to 140°C over 15 min at a
power level of 1000 W, then raised to 190°C over 15 min at 1000
W and finally maintained at 190°C for 20 min at 1000 W. Next,
the sample digestion tanks were placed on an electric plate to
drive acid volatilization until the remaining liquid amounted
to approximately 0.5 mL. After cooling to room temperature,
the digested samples were transferred to clean polyethylene
terephthalate (PET) centrifuge tubes and diluted with Milli-Q
ultrapure water (18.25 M/cm resistivity) to 25 mL. The sam-
ple solutions were filtered before analysis if necessary. In ad-
dition, blanks and two certified reference materials (CRMs),
namely, GBW 10024 (scallops) and GBW 07309 (stream sedi-
ments), obtained from Beijing Zhongkezhijian Biotechnology
Co., Ltd., China, were digested using the same methods de-
scribed above.
1.3. Trace metal analysis
The metal concentration was determined using an induc-
tively coupled plasma mass spectrometry (ICP-MS) instru-
ment (iCAP Q, Thermo Fisher Scientific, Germany) as previ-
ously described (Xia et al., 2019), with modifications. The con-
centrations of 15 trace metals and metalloids (Be, V, Cr, Mn,
Fe, Co, Ni, Cu, Zn, As, Mo, Cd, Sb, Ba, and Pb) in the digested
solutions (samples, blanks and CRMs) were measured three
times for each sample. Mixed standard stock solutions (con-
taining 10 mg/L of each element) were provided by the China
National Center of Analysis and Testing for Nonferrous Met-
als and Electronic Materials (NCATN). The stock solutions were
diluted to different concentrations (0, 0.5, 1, 5, 10, 50, 100, 300,
and 500 μg/L) and employed to establish standard calibration
curves. Moreover, the Ge, Bi, In, and Rh mixed standard stock
solutions (provided by the NCATN, containing 10 mg/L of each
element) were diluted to 10 μg/L and then utilized as mixed
internal standards, and the recovery rates were calculated.
1.4. Quality control and assurance
All the reagents employed in this study were of GR grade.
Blanks were run in each batch of samples and employed for
background correction. In other words, the concentrations of
the trace metals in the blanks were deducted from the con-
centration values of the samples. Additionally, two CRMs, i.e.,
GBW 10024 (scallops) and GBW 07309 (stream sediments),
were adopted to verify the accuracy and precision. A qual-
ity control sample (CRM) was remeasured after every twenty
samples. Calibration curves (R2 ≥ 0.999) were developed for
each trace metal element. The limits of detection (LODs) for
the determination of the 15 trace elements were 0.001 μg/L
for Be, 0.016 μg/L for V, 0.051 μg/L for Cr, 0.163 μg/L for Mn,
0.131 μg/L for Fe, 0.005 μg/L for Co, 0.014 μg/L for Ni, 0.013 μg/L
for Cu, 0.103 μg/L for Zn, 0.034 μg/L for As, 0.008 μg/L for Mo,
0.002 μg/L for Cd, 0.004 μg/L for Sb, 0.067 μg/L for Ba, and 0.011
μg/L for Pb. The recoveries of the 15 metals ranged from 83.5%
to 114.6% (the relative standard deviation (RSD) ranged from
3.64% to 7.82%), which means that the results of this study
could accurately reflect the true concentrations in the sam-
ples.
1.5. Bioaccumulation factor (BAF) and biota-sediment
accumulation factor (BSAF)
The Bioaccumulation factor (BAF) is adopted to measure the
level of biological accumulation. The BAF is defined as the ra-
tio of the metal concentration in organisms (ww basis) to that
in water in the steady state or equilibrium state (Wang et al.,
2017; Zhong et al., 2018). The BAF was calculated by Eq. (1):
BAF = COW /CW (1)
where, BAF (L/kg ww) is the bioaccumulation factor, COW
(mg/kg ww) is the metal concentration in the C. plicata organ,
with the metal concentration in the organs converted into the
ww using the water content (Wei et al., 2014; Xia et al., 2019);
and CW (mg/L) is the metal concentration in the water of the
corresponding region.
The biota-sediment accumulation factor (BSAF) is usually
implemented to evaluate the efficiency of metal accumulation
by organisms. This model relates the ratio of metal concen-
trations in organisms to the sediment metal concentrations
(Thomann et al., 1995). The BSAF was calculated by Eq. (2):
BSAF = CO /CS (2)
where, CO (mg/kg dw) is the average metal concentration in
the C. plicata organ samples; and CS (mg/kg dw) is the average
metal concentration in the corresponding surface sediments.
In this study, the BAF and BSAF were calculated in the
three regions, i.e., EDL, SDL, and WDL, and the results were
expressed as the mean ± the standard deviation (SD).
1.6. Human health risk assessment
1.6.1. Estimated daily intake (EDI)
The metal concentrations in the C. plicata foot samples were
adopted to evaluate food safety in this study since people
usually only consume the foot of mussels. The Estimated
daily intake (EDI) of each trace metal was calculated by
Eq. (3) (USEPA, 1989; Griboff et al., 2017):
EDI = CFW × FIR /WAB (3)
where, CFW (mg/kg ww) is the mean trace metal concentration
in the C. plicata foot sample, with the metal concentration in
the foot sample converted into the ww by the water content
(Wei et al., 2014; Xia et al., 2019); FIR (g/(person•day)) is the Chi-
nese daily aquatic product consumption (approximately 55.8
 journal of environmental sciences 104 (2021) 335–350
g/day for an adult, and approximately 52.5 g/day for a juve-
nile); and WAB (kg) is the average Chinese body weight (bw) (an
adult weighs 60 kg, while a juvenile weighs 30 kg) (Tong et al.,
2016). The EDI was expressed as μg/kg (bw)/day.
1.6.2. Target hazard quotient (THQ) and hazard index (HI)
To evaluate the noncarcinogenic human health risk of local
inhabitants due to the intake of trace metals from mussel con-
sumption, the target hazard quotient (THQ) was calculated by
Eq. (4) (USEPA, 1989; Chien et al., 2002):
THQ = 10−3 × (EF × ED × FIR × CFW ) / RfDO × WAB × TA (4)
where EF is the exposure frequency (365 days/year); ED is the
exposure duration (70 years for adults and 6 years for juve-
niles in this study) (Zhong et al., 2018); RfDo (mg/(kg•day)) is
the oral reference dose of the elements as established by the
United States Environmental Protection Agency (USEPA, 2019)
and the European Food Safety Authority (EFSA, 2010); WAB is
the average Chinese bw (an adult weighs 60 kg, and a juve-
nile weighs 30 kg) (Tong et al., 2016); and TA is the mean expo-
sure time (365 days/(year × ED )). THQ < 1 indicates that mus-
sel consumption is safe, whereas THQ ≥ 1 suggests that con-
sumption has highly adverse health risks (Taweelet al., 2013;
Łuczyńska et al., 2018; Zhong et al., 2018).
There might be additive effects when organisms are ex-
posed to two or more pollutants. For the risk assessment of
the multiple trace metals in mussels, the total target hazard
quotient (TTHQ) or hazard index (HI) was calculated as the
arithmetic sum of the THQ values for the determined trace
metals calculated by Eq. (5) (Chien et al., 2002; Ahmed et al.,
2016; Jovic and Stankovic, 2014):
TTHQ/HI = Total THQ = THQ(metal 1 ) + THQ(metal 2 )
+ . . . + THQ(metal n ) (5)
where n is 15 in the present study.
1.7. Statistical analysis
Distribution maps of the sampling areas were generated with
ArcGIS 10.2 software. Data analysis and plotting were con-
ducted in the R (vision 3.6.0) statistical software environment
(R Core Team, 2020). The means and SDs of the trace metal
concentrations in the surface water, surface sediment and C.
plicata organ samples were calculated. A one-way repeated-
measures analysis of variance (ANOVA) was performed on the
data of the trace metal concentrations in the C. plicata or-
gan samples to detect their differences among the 3 regions
(EDL, WDL, and SDL) and 4 organs (foot, gill, mantle, and vis-
ceral masses). If the variance was homogeneous, the signifi-
cance of the differences among the regions or organs was as-
sessed with Tukey’s honestly significant difference (HSD) mul-
tiple comparison method, and if the variance was not homo-
geneous, the Games-Howell test was conducted. The mean,
SD, and ANOVA results were generated in R using base codes.
To investigate the similarity of the trace metal concentration
distributions in the different organs and regions, we applied
an unconstrained ordination method, namely, the nonmetric
multidimensional scaling analysis (NMDS) method, which is
339
suitable for cases where the preliminary dataset matrix does
not meet linearity conditions (Bonsignore et al., 2018). Pear-
son’s correlation analysis between the trace metals in C. plicata
explained the homology in the organisms. The different low-
ercase letters above the box plots and correlation heatmaps
indicate statistical significance at the 0.05 level, and “∗ ”, “∗∗ ”,
and “∗∗∗ ” indicate statistical significance at the 0.05, 0.01, and
0.001 levels (two-tailed), respectively.
2. Results
2.1. Trace metal concentrations in the surface water and
sediments
The mean concentrations of the 15 trace metals in the sur-
face water and sediment samples from EDL, WDL, and SDL are
listed in Table 1. The mean trace metal concentrations ranged
from (0.04 ± 0.02) μg/L (Be) to (132.54 ± 31.58) μg/L (Fe) in the
surface water across the entire lake area. In each area, the se-
quence of the metal concentration was consistent with the
trend in the entire area, except for V, As, Sb, Co and Mo. Spa-
tially, the Fe and Co concentrations in the surface water fol-
lowed the order of EDL > SDL > WDL (P < 0.05), and the V and
Sb concentrations were the highest in SDL and then WDL and
EDL (P < 0.05). The Cr, Mn, Ni, Cu, Zn, and As concentrations
were the lowest in EDL (P < 0.05), while there were no signifi-
cant differences between WDL and SDL (P > 0.05). Only the Mo
concentration was not significantly different across the three
areas (P > 0.05) (Table 1).
With regard to the mean concentrations (mg/kg dw) of the
15 trace metals and metalloids in the surface sediments of the
entire lake area, the sequence was Fe > Mn > Zn > Ba > V > Cr
> Ni > Pb > Cu > As > Co > Sb > Be > Mo > Cd. The highest Fe
concentration (12,817.98 ± 1524.04 mg/kg) was approximately
10,000 times the lowest Cd concentration (1.19 ± 0.59 mg/kg).
The ranking trends of the Fe, Mn, Zn, Ba, V and Cr concentra-
tions in the spatial distribution of each area were consistent
with those in the spatial distribution of the entire area, while
slight differences occurred in the ranking trends of the other
trace metal concentrations (Table 1). The V, Cr, Mn, Fe, Co, Cu,
Zn, Sb, and Ba concentrations in the sediments were not sig-
nificantly different among the three areas (P > 0.05). Both the
Be and Cd concentrations were significantly the highest in SDL
(P < 0.05), while no significant differences were observed be-
tween EDL and WDL (P > 0.05). With regard to Pb and As, EDL
exhibited the highest concentrations, although significant dif-
ferences were not observed between WDL and SDL (P > 0.05)
(Table 1).
2.2. Trace metal concentrations in C. plicata
In general, metal elements enter aquatic organisms from the
environment through respiration, ingestion and body sur-
face contact and are not completely excreted via biological
metabolism, resulting in metal accumulation in organisms.
Fig. 2 shows the trace metal concentrations (mg/kg dw) in the
foot, gill, mantle, and visceral masses of C. plicata obtained
from Dongting Lake. The trace metal concentrations in the or-
gans varied greatly. The ranges of the Be and Sb concentra-
 340 journal of environmental sciences 104 (2021) 335–350

tions were 0.0003 (foot)-0.1177 (visceral mass) mg/kg dw and

Table 1 – Concentrations of 15 trace metals in surface water (μg/L, mean ± SD) and sediments (mg/kg dry weight (dw), mean ± SD) collected from three areas of Dongting

185.25B
0.0002 (foot)-0.0932 (gill) mg/kg dw, respectively. The ranges

34.00D
88.29B

47.48B

29.71B

60.99B
2.57D
4.65B
NA
NA

NA
NA
NA

NA

NA
of the relatively high Fe and Mn concentrations were 21.7032
BS (foot)-4976.9335 (visceral mass) mg/kg dw and 11.2726 (foot)-

BW: the background values of trace metals in water from Dongting Lake. BS: the background values of trace metals in sediments from Dongting Lake. NA: not available. NA: not available.
11,970.9052 (gill) mg/kg dw, respectively. Except for Cr, Zn, Mo,
Sb, and Pb, the concentrations of the other metals in the gill,

11,361.99 ± 1400.66a
mantle, and visceral mass samples were significantly higher
than those in the foot samples (P < 0.05). In this study, the dw
537.62 ± 193.57a

39.57 ± 8.09ab
73.62 ± 12.53a

98.76 ± 70.24a
11.34 ± 4.11b

23.18 ± 2.90b
45.23 ± 8.16a

10.99 ± 2.10a

24.29 ± 8.79a
76.41 ± 8.14a
of the C. plicata foot samples was 17% of the ww. The mean
2.61 ± 0.22b

0.65 ± 0.31b
1.88 ± 0.62a

3.37 ± 2.25a

n is the number of water and surface sediment samples collected in Dongting Lake. The different lowercase letter letters stand for statistical significance at the 0.05 level.
SDL (n=9)

concentrations of the trace elements Zn, Pb, Cd, As, Cu, and
Cr (9.2, 0.2, 0.2, 0.6, 0.7, and 0.5 mg/kg ww), respectively) in the
foot of C. plicata were lower than the threshold values (100,
2.0, 1.0, 1.0, 40, and 2.0 mg/kg ww, respectively) established
by international and Chinese organizations (FAO/WHO, 1998;
FAO/WHO, 2014; EC, 2006; CNS, 2017). The average Be, Mn, Co,
13,880.84 ± 76.00a

Ni, Zn, Cd, Sb, Ba, and Pb concentrations were the highest in
452.10 ± 66.09a

77.95 ± 26.92a

the gill samples, while the V, Fe, Cu, and As concentrations

1.53 ± 0.39ab
12.07 ± 0.99b

25.36 ± 2.69b
74.47 ± 9.44a
50.89 ± 9.24a

10.18 ± 1.67a
47.21 ± 8.92a
20.62 ± 3.01a
87.34 ± 8.37a
3.12 ± 0.44a

1.29 ± 0.38a
3.74 ± 1.37a
WDL (n=9)

were highest in the visceral mass samples (Fig. 2).

From the perspective of the spatial distribution, the se-
quence of the heavy metal concentrations in each organ was
consistent with the overall results (Fig. 2 and Appendix A Fig.
S1). The concentrations of most trace metals, such as Be, V, Fe,
Cu, As, Mo, and Pb, were low in the foot samples and relatively
13,211.10 ± 1263.46a

high in the gill and visceral mass samples. Overall, the Be, V,
584.65 ± 140.86a

Cu, As, Mo, Cd, and Pb concentrations were higher in EDL than
67.76 ± 13.51a

87.59 ± 15.41a

74.24 ± 21.77a
38.33 ± 5.58b
50.06 ± 6.07a

11.40 ± 1.94a

26.80 ± 5.31a

17.78 ± 1.51a

39.86 ± 3.15a

WDL and SDL. For some trace metal (such as Cr, Ni, Cu, Cd, Ba)
1.14 ± 0.36b
3.25 ± 0.24a

1.63 ± 0.55a
3.07 ± 1.02a
Sediments
EDL (n=9)

concentrations in the foot, there was no significant difference

in the three areas (Appendix A Fig. S1).
As shown in Fig. 3, there were significant positive correla-
tions between Be and V (r = 0.80, P < 0.001) and Pb (r = 0.72, P
< 0.001) in C. plicata. Significant positive correlations were ob-
served between the Co concentration and the V (r = 0.58, P <
20.91C

0.01), Cr (r = 0.56, P < 0.01), Ni (r = 0.59, P < 0.01), Cu (r = 0.59, P

1.51C

4.2A

0.1A
1.9E
BW

10A
NA
NA

NA
NA
NA

NA

NA
4A

3A

Liu et al., 2015a; B Li et al., 2013; C Bi et al., 2018; D Xie et al., 2017; E Ouyang et al., 2016.

< 0.01), and Sb concentrations (r = 0.66, P < 0.01). The Mn and

Fe concentrations (r = 0.56, P < 0.01) and the Ba concentration
(r = 0.66, P < 0.01) also revealed positive correlations. The Cd
concentration and the Zn (r = 0.68, P < 0.01), As (r = 0.58, P <
135.32 ± 15.39b

56.31 ± 10.85a

0.01), and Pb concentrations (r = 0.75, P < 0.001) also exhibited

0.04 ± 0.01ab

36.00 ± 1.81b
33.84 ± 2.50a

12.62 ± 5.66a
1.09 ± 0.15b

0.10 ± 0.02b

6.03 ± 1.57b
3.91 ± 0.44a
7.70 ± 0.60a

4.10 ± 0.84a

2.14 ± 0.57a
0.78 ± 0.29a

2.00 ± 0.24a
SDL (n=9)

significant positive correlations.

NMDS was performed to observe the trace metal concen-
tration specifics of the various organs and Dongting Lake ar-
eas (Fig. 4). The model showed that the foot preferentially ac-
cumulated Cr, Mo, and Pb, the gill preferentially accumulated
Mo and Mn, the mantle preferentially accumulated Be, Cr, Cd,
101.08 ± 11.89c

51.03 ± 10.02a

Mo, and Mn, and the visceral mass preferentially accumulated

36.63 ± 5.03a

12.49 ± 3.43a
64.19 ± 9.65a

10.16 ± 1.79a
3.32 ± 0.36b

1.75 ± 0.16b
0.05 ± 0.03a

7.59 ± 0.68a

3.65 ± 0.66a

2.32 ± 0.40a
0.78 ± 0.08a
0.13 ± 0.02a
0.90 ± 0.12c
WDL (n=9)

Mo, Mn, Cd, and Pb (Fig. 4a). In terms of the spatial distribu-
tion of the trace metal concentrations (the average of the 4
organs) in C. plicata, Cd, Pb, and Cd were the main enriched
metals in EDL and Mo, Fe, Mn, Ba, and Pb were the main en-
Concentration

riched metals in WDL and SDL (Fig. 4b). Cu, Pb, and Cd were
the main enriched metals in the foot samples obtained from
161.22 ± 28.18a

EDL, while the other metals were the core enriched elements
24.36 ± 5.64b

43.50 ± 5.35b

33.62 ± 6.08b
0.03 ± 0.02b

5.79 ± 0.48b

2.03 ± 0.32b
6.82 ± 1.00b

1.52 ± 0.05b
1.95 ± 0.18a

0.89 ± 0.21a
0.13 ± 0.00a
1.56 ± 0.15c

0.88 ± 0.21c

2.51 ± 0.76c

in WDL and SDL (Fig. 4c). The other organs, including the gill
EDL (n=9)

(Fig. 4d), mantle (Fig. 4e), and visceral mass (Fig. 4f), also ex-
Water

hibited approximately similar enrichment characteristics.

2.3. Trace metal bioaccumulation in C. plicata

Lake.

metal
Trace

The BAF and BSAF values of the 15 trace metals in the 4 organs
Mn

Mo
Cu
Zn

Cd
Co

As

Ba
Be

Sb

Pb
Cr

Ni
Fe

A
V

of C. plicata are summarized in Appendix A Table S2. The BAF

 journal of environmental sciences 104 (2021) 335–350 341

Fig. 2 – Concentrations of 15 trace metals in foot, gill, mantle, and visceral mass of C. plicata (n=60) from the three areas of
Dongting Lake. Different lowercase letters above the Box-plots show statistical significance at the 0.05 level.

values ranged from 0.001 × 103 L/kg ww (Sb accumulation in
the mantle) to 28.357 × 103 L/kg ww (Fe accumulation in the
visceral mass). Regarding Ba accumulation, the highest BAF
values > 1.0 × 103 L/kg ww were found in the gill samples, and
the BAF values of the foot samples were significantly lower
than those of the gill and visceral mass samples (P < 0.05).
The BAF values of Mn, Fe, and Cd in all organs were higher
than 1.0 × 103 L/kg, and the Mn bioaccumulation level in the
gill was significantly higher than that in the other organs (P <
0.05). Significant differences were not observed in the Cr, Ni,
Cu, Zn, Cd, Sb, or Pb bioconcentrations across all organs (P >
0.05).
The BSAF values ranged from 0.002 ± 0.001 (Be accumu-
lation in the foot) to 11.317 ± 1.356 (Mn accumulation in the
gill). The BSAF values of Mn and Ba in the gills were signif-
icantly higher than those in the other organs. Regarding Be,
Mn, Fe, Ni, Cd and Ba, the BSAF values in the feet were signif-
icantly lower than those in the other three organs (P < 0.05).
No significant differences in the BSAF values among the dif-
ferent organs were observed for many elements, including Cr,
Cu, Mo, Sb, and Pb (P > 0.05).
The correlation heatmaps showed significant positive and
negative correlations among the different trace metals in the
surface water (Fig. 5a) and sediments (Fig. 5b), respectively.
342 journal of environmental sciences 104 (2021) 335–350

Fig. 3 – Pearson’s correlations (r) between the concentrations of 15 trace metals in C. plicata. Average concentrations in foot,
gill, mantle, and visceral mass of C. plicata were used for the analysis. The histogram on the main diagonal of the matrix
reflects the distribution of the trace metal elements; the upper triangular panel shows the correlation coefficient between
the variables, the larger the correlation coefficient, the larger the font size; the scatter linear fitting graph of the lower
triangle reflects the data distribution characteristics. ∗ Coefficients at 0.05 significance level, P < 0.05; ∗∗ Coefficients at 0.01
significance level, P < 0.01; ∗∗∗ Coefficients at 0.001 significance level, P < 0.001.

Except for Mo, Cd, and Ba, most of the metals in the surface
water were significantly related to each other to varying de-
grees. In addition, V, Cr, Co, and the other metals revealed ex-
tremely significant correlations (P < 0.001), and the absolute
value of the correlation coefficient was between 0.30 and 0.84
(V and Sb, respectively). In the sediments, significant correla-
tions were only observed between certain metals, including
Cr, Cu, Zn, and Mn. For example, the element pairs of Cr-Cu
(r = 0.68), Mn-Zn (r = 0.55), and Cr-Zn (r = 0.58) demonstrated
significant negative correlations at P < 0.001. There were cer-
tain differences in the correlation between the metal concen-
trations in C. plicata (individual organs and the average of the
4 organs) and the corresponding metal concentrations in the
surface water (Fig. 5a) or sediments (Fig. 5b). In general, the
metals in C. plicata were significantly correlated with V, Mn,
Co, Cu, and Pb in the surface water and Be, Cu, Mo, Cd, Pb in
the sediments. For instance, a significant correlation was ob-
served for the element pair Co-Co (r = 0.62, P < 0.001) between
the gill and surface water samples and Mn-Mn (r = 0.34, P <
0.01) between the visceral mass and surface water samples,
while the element pair Cu-Cu showed a significant correla-
tion between the sediment samples and the foot (r = 0.51, P <
 journal of environmental sciences 104 (2021) 335–350 343

Fig. 4 – Ordination plots of NMDS applied on concentrations of trace metals of C. plicata. Concentrations of 15 trace metals in
foot, gill, mantle, and visceral mass of C. plicata in Dongting Lake (a); concentrations of trace metals of C. plicata in Eastern
Dongting Lake (EDL), Western Dongting Lake (WDL), and Southern Dongting Lake (SDL) (b); concentrations of trace metals in
foot (c), gill (d), mantle (e), and visceral mass (f) of C. plicata in EDL, WD and SDL. The arrows show the direction of the
gradient, and the length is proportional to the correlation between the vectors (metal concentrations) and the ordination.
The metals with significant correlation with the axes were circled. Ellipses indicate the 95% confidence intervals for each
group, dashed ellipses represent 99% confidence intervals.

0.001), gill (r = 0.59, P < 0.001), mantle (r = 0.49, P < 0.001), and > Mn > Co > Pb > Fe > Ba ≈ Zn > Cu ≈ Cd > Mo > Sb ≈ Ni >
visceral mass (r = 0.46, P < 0.001). V > Be ≈ Cr. The TTHQ and HI values for adults and juveniles
were 3.128 and 5.885, respectively (Table 2).

2.4. Estimated daily intake and risk of the trace metals in

C. plicata
Among the 15 trace metal elements in this study, Be, As, Cd, Sb,
Ba, and Pb are toxic elements while V, Cr, Mn, Fe, Co, Ni, Cu, and
Zn are essential elements for the human body. However, these
essential trace elements could affect human health when ex-
posure exceeds critical thresholds. The EDI and THQ values for
the 15 trace metal elements via consumption of the C. plicata
foot from adults and juveniles are listed in Table 2. The high-
est EDI values were observed for Mn (75.236 μg/kg (bw)/day for
adults and 141.573 μg/kg (bw)/day for juveniles) and Fe (66.110
μg/kg (bw)/day for adults and 124.400 μg/kg (bw)/day for ju-
veniles), while the lowest values occurred for Sb (0.003 μg/kg
(bw)/day for adults and 0.006 μg/kg (bw)/day for juveniles).
The THQ values for the essential trace element Mn (1.011
for juveniles) and toxic element As (1.910 for adults and 3.593
for juveniles) were the highest and exceeded 1. Mn (essen-
tial element) only posed a potential health risk for juveniles
(THQ = 1.011) but not for adults (THQ = 0.537), while As (toxic
element) posed a potential health risk for both juveniles and
adults. The THQ values for the individual metals for both
adults and juveniles decreased in the following sequence: As
3. Discussion
3.1. Trace metal concentrations in the environment
Dongting Lake is one of the two largest lakes still linked with
the middle reaches of the Yangtze River. Dongting Lake is fed
by four major rivers (Xiang River, Zi River, Yuan River, and Li
River) in Hunan Province, and three channels (Songzi, Taiping,
and Ouchi) directly connect it to the Yangtze River (Hu et al.,
2018). In addition, it is affected by the Three Gorges Dam (TGD),
which likely exchanges water and sediments with the Yangtze
River (Xu and Li, 2019). Therefore, the pollutants transported
by water and sediments into the lake and their migration and
transformation in the lake are relatively complicated. In this
study, the average concentrations of Cu (10.65 μg/L) and Zn
(54.67 μg/L) were slightly higher than the type I water qual-
ity standards (Cu, 10 μg/L; Zn, 50 μg/L) in the Environmental
Quality Standards for Surface Water of China (GB 3838-2002) (P
> 0.05), while the concentrations of the other common metal
elements, such as Cr (7.02 μg/L), As (1.99 μg/L), Cd (0.12 μg/L)
and Pb (6.24 μg/L), were significantly lower than the type I wa-
344 journal of environmental sciences 104 (2021) 335–350

Fig. 5 – Correlation analysis between the concentration of metals in the average of 4 organs in C. plicata, foot, gill, mantle,
and visceral mass, and the corresponding metal concentration in surface water, sediments. Gradient colors indicate
Pearson’s correlation coefficients (E s r) of the different trace metal concentrations in (a) surface water or (b) sediments,
respectively. “∗ ”, “∗∗ ” and “∗∗∗ ” indicate statistically significant correlations at the levels of 0.05, 0.01 and 0.001, respectively.
Arc width corresponds to the Pearson’s correlation coefficient ((C.-E)’s |r|) statistic for the corresponding correlations between
the concentration of the same trace metals in organs and (a) surface water or sediments (b), and arc color denotes the
statistical significance ((C.-E)’s P). C.: C. plicata, E: surface water or sediments.
 journal of environmental sciences 104 (2021) 335–350 345

μg
Table 2 – Estimated daily intake (EDI, μg/kg (bw)/day), tolerable daily intake (TDI, μg/kg (bw)/day), RfDo (mg/(kg•day)), target
hazard quotient (THQ) and hazard index (HI) of heavy metals from C. plicata foot consumption for adults and juveniles
(n=60).

Trace metals EDI for adults EDI for juveniles TDIa RfDo b THQ for adults THQ for juveniles
c
Essential V 0.032 0.061 NA 5 0.006 0.012
Cr 0.511 0.961 300 1500 0.000 0.001
Mn 75.236 141.573 140 140 0.537 1.011
Fe 66.110 124.400 800 700 0.094 0.178
Co 0.053 0.100 30 0.3 0.177 0.334
Ni 0.141 0.265 12 20 0.007 0.013
Cu 0.629 1.184 500 40 0.016 0.030
Zn 8.582 16.149 300 300 0.029 0.054
Mo 0.059 0.110 NA 5 0.012 0.022
Toxic Be 0.001 0.002 2 2 0.001 0.001
As 0.573 1.078 2.14 0.3 1.910 3.593
Cd 0.152 0.287 0.8 1 0.016 0.030
Sb 0.003 0.006 6 0.4 0.007 0.014
Ba 5.870 11.047 210 200 0.029 0.055
Pb 0.224 0.421 1.5 1.5c 0.149 0.281
TTHQ/HI - - - - 3.128 5.885

EDI values more than TDI and THQ values more than one are marked in bold prints.
bw: body weight; n: number of C. plicata; NA: not available; -: No data.
a
Tolerable daily intake. The values of TDI are referenced from the report of Varol et al. (2017) and Guidelines for drinking-water quality (4th
Ed.) by the WHO (World Health Organization) (2011).
b
Oral reference dose of elements as established by the USEPA (United States Environmental Protection Agency) (2019).
c
For Pb not available, and the EFSA (European Food Safety Authority) (2010).

ter quality standards (Cr, 10 μg/L; As, 50 μg/L; Cd, 1 μg/L; Pb,
10 μg/L; P < 0.05). However, most of the concentrations in the
surface water exceeded previously published background val-
ues (Liu et al., 2015a; Bi et al., 2018; Ouyang et al., 2016) ex-
cept for As and Sb (Table 1). This finding clearly indicates that
the metal pollution level in the water of Dongting Lake is in-
creasing, which may be related to the contribution of several
tributaries. In terms of the spatial distribution, the concentra-
tions of most elements in EDL were lower than those in WDL
and SDL, which is primarily related to human activities as well
as the clear dilution effect in EDL due to Yangtze River inter-
change.
When metals enter a river, most will be adsorbed and en-
riched in sediments, and only a small portion of the metal ions
is contained in the water column; therefore, the concentra-
tions of the metals stored in the sediments are much higher
than those stored in the water column (Gaur et al., 2005).
In the surface sediments, the Be, Ni, As, and Pb concentra-
tions exceeded previously published background values, while
those of the other elements (V, Cr, Mn, etc.) were lower than
the background values (Li et al., 2013; Xie et al., 2017). Al-
though these results showed that Be, Ni, As, and Pb accumu-
lated in the sediments of Dongting Lake, during the China’s
12th Five-year Plan period (2011-2015), more than 1000 enter-
prises associated with heavy metal pollution were closed over
two rounds of the Three-year Action Plan for Xiangjiang Pro-
tection and Treatment by the Hunan government, which re-
duced the total amount of heavy metals entering the lake dis-
trict (Bi et al., 2018). Compared to several other large freshwa-
ter lakes (Poyang Lake, Taihu Lake, Chaohu Lake, and Honghu
Lake) in the Yangtze River basin, the concentrations of most
heavy metals in the surface sediments of Dongting Lake were
the highest (Zhang et al., 2018a; Liu et al., 2015b; Fang et al.,
2019; Makokha et al., 2016). Therefore, although most of the
metal pollution in the sediments of Dongting Lake revealed a
decreasing trend, pollution control and treatment measures
are still required. It is worth noting that the change trends of
the metal concentrations in the surface water and sediments
were not consistent with those of the previously published
background values, which may be related to the smaller fluc-
tuations in the metals in the sediments compared with those
in the surface water as well as the instantaneous nature of
sampling, the spatial limitations of the sample sites, and the
different literature sources and publication times of the back-
ground data. Thus, to guarantee data accuracy and quality,
more studies are required to clarify the relationships of the
metal concentrations in the surface water and sediments.
3.2. Trace metal bioaccumulation in mussels
The accumulation of metals in organisms is not only related
to the metal concentration in the habitat but is also influ-
enced by many physical and biological factors, such as the
metallothionein level and physical conditions (Kumar et al.,
2015; Laura, 2009). Most metal concentrations in C. plicata foot
and gill were higher than those reported by Türkmen and
Ciminli (2007) for the two mussels Unio terminalis and Potamida
littoralis, respectively. This difference may have been caused
by the different habitats, species, and growth rates. Our re-
sults showed that C. plicata is more likely to accumulate es-
sential elements and the toxic metal Ba, which presented high
concentrations in the surface water and sediments of Dongt-
ing Lake (Table 1, Fig. 2 and Appendix A Fig. S1). Generally,
the concentrations of essential trace elements, such as Fe,
346 journal of environmental sciences 104 (2021) 335–350
Mn, Cu, and Zn, are high in invertebrates. Essential trace el-
ements play an important role in the metabolism and growth
of organisms; therefore, they are easily absorbed and enriched
(Bahnasawy et al., 2011; McGeer et al., 2003). Although essen-
tial elements are necessary for the biological activities of mus-
sels, excessive intake may pose a potential hazard. For exam-
ple, Mn is involved in the synthesis of various enzymes in or-
ganisms; however, it is easily converted into Mn2+ for biolog-
ical utilization and even results in poisoning in anoxic envi-
ronments (Oweson et al., 2008). Moreover, most toxic heavy
metals (Cd, Pb, Hg, etc.) could reach a biologically signifi-
cant or even harmful concentration in tissues at low levels
(Dallinger et al., 1987), which results in potential threats to the
growth and development of C. plicata.
In general, the enrichment of trace metals in bivalves and
other aquatic animals mainly occurs through digestive or-
gans via feeding for particulate metal forms and through
surface penetration and gills for dissolved forms (Wang and
Fisher, 1996; Ribeiro et al., 2005). Bivalve mollusks possess
gill lamellae that contain many branchial filaments and are
rich in capillaries (Liu and Zheng, 2009). The special structure
of the mussel gill is beneficial to ion permeation and takes
up metal ions from water and sediments as the main route
(Liu et al., 2001). The metal ions entering the mussel partic-
ipate in metabolism, and also become enriched in the inter-
nal organs, such as the liver and kidney (Chandurvelan et al.,
2012). When the metals in the liver reach saturation, they
are transferred to the muscle tissue of organs because of the
low metallothionein concentration therein (Ovemell and Ab-
dullah, 1988; Le Croizier et al., 2018), which results in a rela-
tively low metal concentration in the foot and mantle com-
pared with that in the gill and visceral mass (Fig. 2 and Ap-
pendix A Fig. S1, respectively). The NMDS model revealed var-
ious organ- and area-specific bioaccumulation patterns in this
study. The essential trace metals in organisms are involved in
metabolism. For example, Mn is a part of the metalloenzymes
in living organisms and acts as an activator of these enzymes,
while Mo plays a role in the transfer of electrons in the re-
dox reaction in organisms and is a constituent of many en-
zymes (Hänsch and Mendel, 2009). These two metal elements
are easily absorbed by C. plicata and become preferentially en-
riched (Fig. 4a). Toxic metals Cd and Pb are easily combined
with certain substances in organisms and are stably present,
resulting in bioaccumulation (Allen, 1995). Therefore, Cd and
Pb also preferentially accumulate in the visceral mass (Fig. 4a).
The spatial distributions of the trace metal concentrations in
C. plicata (the average of the 4 organs) revealed significant dif-
ferences among the sampling areas (Fig. 4b), which may be
due to the different background values of the trace metals in
the environment.
The BAF and BSAF were adopted to assess the bioaccumu-
lation ability of aquatic organisms from the surface water and
sediments, respectively (Liu et al., 2018b). The metal biocon-
centration ability of different organs varies. In addition to the
varying affinities, i.e., specific accumulation patterns, and the
bioavailability of different metal ions for organs, the biocon-
centration ability is also influenced by environmental condi-
tions (Liu et al., 2018b). The BAF values of Mn, Fe, and Cd in all
organs were higher than 1 × 103 L/kg ww. As discussed earlier,
C. plicata exhibited a high enrichment ability for the essen-
tial elements. The BAF values of Mn and Ba in the gills were
higher than those in the other organs in this study (P < 0.05).
Similar to the BAF values, the BSAF values of Mn and Ba in
the gills were significantly higher than those in the other or-
gans. These results were consistent with previous reports on
aquatic organisms (Liu et al., 2018b). In this study, most metals
presented significant correlations in the surface water while
relatively few metals were correlated in the sediments. Be-
cause the lake water exhibits connectivity and fluidity, stud-
ies of metal homology in water may exhibit data uncertain-
ties. The content and ratio of each metal in the sediments are
relatively stable. Therefore, it is more scientific to determine
the source of these metals through correlation analyses of the
trace metals in the sediments. The corresponding metals in C.
plicata were significantly correlated with the Be, Cu, Mo, Cd,
and Pb contents in the sediments, which further illustrates
that a certain relationship was present between the metals in
C. plicata and their distribution and concentration levels in the
environment. A correlation analysis between the trace metals
in aquatic organisms indicated that these metal elements ex-
hibited bioaccumulation homology and dispersion properties
(Sivaperumal et al., 2007). Co and V, Cr, Ni, and Cu were signifi-
cantly positively correlated, which indicated that these metals
in C. plicata were homologous, and a correlation was also ob-
served between Zn and Cd and Pb. A similar pollution source
is probable, because Zn is the primary inducer of metalloth-
ionein in organisms while the other metal ions are more read-
ily bound to the sulfhydryl group in thionein, thereby replac-
ing Zn (Roesijadi et al., 1996). In addition, the metal interac-
tion mechanism in organisms includes synergistic effects, dis-
placement reactions, competition sites, etc., which also leads
to metal correlation differences.
3.3. Human health risk assessment of C. plicata
consumption
Since people usually only consume the muscle tissue of bi-
valves, the C. plicata foot was selected in this study to eval-
uate food safety through consumption. In this study, the EDI
values of the 15 trace metals were calculated for adults and
juveniles and then compared to the respective tolerable daily
intake (TDI) values (Varol et al., 2017; WHO, 2011). Only the EDI
values of the essential element Mn 141.573 (μg/(kg bw.day)) for
juveniles were higher than the recommended TDI values (140
μg/(kg bw.day)) (P < 0.05), which indicates a slight risk from Mn
caused by the consumption of C. plicata feet. The EDI values of
all other elements for juveniles and adults were lower than
the TDI values. Although Mn is an essential element required
by the human body, excessive intake may pose a certain risk
to humans (Sabina et al., 2019).
The THQ value assesses the health risks of a single metal,
while the TTHQ or HI value, which was calculated as the arith-
metic sum of the THQ values of the determined trace metals,
is used to evaluate the health risks of complex exposure to
multiple metals (Ahmed et al., 2016; Jovic and Stankovic, 2014).
The average THQ values of most metals (such as Cr, Cu, and
Zn) in the C. plicata foot samples were lower than 1, indi-
cating that these metals do not pose a health risk to people
through C. plicata consumption. However, the THQ values of
Mn for juveniles and As for juveniles and adults exceeded 1,
 journal of environmental sciences 104 (2021) 335–350
which indicates that exposure to Mn and As could still cause
significant noncarcinogenic health risks (Yi et al., 2017). The
ingestion dose does not fully reflect the metal enrichment
level under actual conditions. It is worth pointing out that al-
though THQ > 1, local residents did not experience obvious
adverse reactions. Moreover, the TTHQ or HI values for adults
and juveniles were 3.128 and 5.885, respectively, which were
higher than 1. These results indicated significant risks of non-
carcinogenic effects to humans by exposure to multiple met-
als (Zhuang et al., 2009). Additionally, humans are exposed
to heavy metals not only by C. plicata consumption but also
by several other routes, including the consumption of drink-
ing water and other aquatic products. Therefore, the effects of
heavy metal contamination on human health should be care-
fully evaluated.
4. Conclusions
Most trace metal concentrations in the surface water revealed
significant spatial variations in the three areas EDL, SDL, and
WDL of Dongting Lake, and were lower or slightly higher than
the corresponding type I water quality standards in the En-
vironmental Quality Standards for Surface Water of China.
However, most of the concentrations exceeded existing back-
ground values, indicating an increasing metal pollution trend
in the Dongting Lake water. Although the concentrations of
most metals in the surface sediments showed a decreasing
trend, they were still higher than those in the sediments of
several other large freshwater lakes (Poyang Lake, Taihu Lake,
Chaohu Lake, and Honghu Lake) in the Yangtze River basin. C.
plicata exhibits a high enrichment ability for essential metal
elements, and the metal concentrations in the gill and visceral
mass samples were generally higher than those in the foot and
mantle samples. The mean concentrations of trace elements
Zn, Pb, Cd, As, Cu, and Cr in C. plicata feet were lower than the
threshold values established by international and Chinese or-
ganizations. The estimated EDI value of the essential metal
Mn in C. plicata feet for juveniles was higher than the recom-
mended TDI value. The THQ values of Mn (for juveniles) and
As (for juveniles and adults) exceeded 1, indicating that these
metals could cause noncarcinogenic health risks through C.
plicata foot consumption. The TTHQ and HI values for adults
and juveniles were 3.128 and 5.885, respectively, suggesting
significant risks of noncarcinogenic effects to humans by ex-
posure to multiple metals.
Declaration of Competing Interest
The authors declare that they have no known competing fi-
nancial interests or personal relationships that could have ap-
peared to influence the work reported in this paper.
Acknowledgments
This work was jointly supported by the National Natural Sci-
ence Foundation of China (Nos. 51622901, 51709225) and the
Young Scientific Research Innovation Team Project of Xi’an
347
University of Technology (No. 104/256051715). The authors
sincerely thank all staff and students that helped with field
sample collection. We also greatly appreciate Dr. Xiaoming
Jiang from Xi’an University of Technology, and Dr. Wei Zhang
from Shanghai Ocean University for his revision and sugges-
tions. The authors are grateful to the two anonymous review-
ers for their very constructive comments.
Supplementary materials
Supplementary material associated with this article can be
found, in the online version, at doi:10.1016/j.jes.2020.12.012.
references
Ahmad, M.K., Islam, S., Rahman, M.S., Haque, M.R., Islam, M.M.,
2010. Heavy metals in water, sediment, and some fishes of
Buriganga River. Bangladesh. Int. J. Environ. Res. 4 (2), 321–332.
Ahmed, M.K., Baki, M.A., Kundu, G.K., Islam, M.S., Islam, M.M.,
Hossain, M.M., 2016. Human health risks from heavy metals in
fish of Buriganga river. Bangladesh. SpringerPlus 5 (1), 1697.
Alahabadi, A., Malvandi, H., 2018. Contamination and ecological
risk assessment of heavy metals and metalloids in surface
sediments of the Tajan River, Iran. Mar. Pollut. Bull. 133,
741–749.
Aldridge, D.C., Fayle, T.M., Jackson, N., 2007. Freshwater mussel
abundance predicts biodiversity in UK lowland rivers. Aquat.
Conserv. -Mar. Freshw. Ecosyst. 17, 554–564.
Allen, P., 1995. Soft-tissue accumulation of lead in the blue tilapia,
Oreochromis aureus (Steindachner), and the modifying effects
of cadmium and mercury. Biol. Trace Elem. Res. 50 (3), 193–208.
Atwell, L., Hobson, K.A., Welch, H.E., 1998. Biomagnification and
bioaccumulation of mercury in an Arctic marine food web:
insights from stable nitrogen isotope analysis. Can. J. Fish.
Aquat. Sci. 55 (5), 1114–1121.
Bahnasawy, M., Khidr, A.A., Dheina, N., 2011. Assessment of heavy
metal concentrations in water, plankton, and fish of Lake
Manzala, Egypt. Turk. J. Zool. 35 (2), 271–280.
Bi, B., Liu, X.H., Guo, X.C., Lu, S.Y., 2018. Occurrence and risk
assessment of heavy metals in water, sediment, and fish from
Dongting Lake, China. Environ. Sci. Pollut. Res. 25 (34),
34076–34090.
Bonsignore, M., Manta, D.S., Mirto, S., Quinci, E.M., Ape, F.,
Montalto, V., et al., 2018. Bioaccumulation of heavy metals in
fish, crustaceans, molluscs and echinoderms from the
Tuscany coast. Ecotox. Environ. Safe. 162, 554–562.
Chandurvelan, R., Marsden, I.D., Gaw, S., Glover, C.N., 2012.
Impairment of green-lipped mussel (Perna canaliculus)
physiology by waterborne cadmium: relationship to tissue
bioaccumulation and effect of exposure duration. Aquat.
Toxicol. 124, 114–124.
Chien, L.C., Hung, T.C., Choang, K.Y., Yeh, C.Y., Meng, P.J.,
Shieh, M.J., et al., 2002. Daily intake of TBT, Cu, Zn, Cd and As
for fishermen in Taiwan. Sci. Total Environ. 285 (1-3), 177–185.
Dai, J., Wu, H.P., Zhang, C., Zeng, G.M., Liang, J., Guo, S.L., et al.,
2016. Responses of soil microbial biomass and bacterial
community structure to closed-off management (an
ecological natural restoration measures): a case study of
Dongting Lake wetland, middle China. J. Biosci. Bioeng. 122 (3),
345–350.
Dallinger, R., Prosi, F., Senger, H., 1987. Contaminated food and
uptake of heavy metals by fish: a review and proposal for
further research. Oecologia 73 (1), 91–98.
348 journal of environmental sciences 104 (2021) 335–350
EFSA (European Food Safety Authority), 2010. European Food
Safety Authority Panel on Contaminants in the Food Chain
(CONTAM). Scientific Opinion on Arsenic in Food, EFSA
Journal 7, 1351–1355.
Ersoy, B., Çelik, M., 2010. The essential and toxic elements in
tissues of six commercial demersal fish from Eastern
Mediterranean Sea. Food Chem. Toxicol. 48 (5), 1377–1382.
Fang, T., Lu, W.X., Cui, K., Li, J., Yang, K., Zhao, X.X., et al., 2019.
Distribution, bioaccumulation and trophic transfer of trace
metals in the food web of Chaohu Lake, Anhui, China.
Chemosphere 218, 1122–1130.
Gao, L., Wang, Z.W., Shan, J.J., Chen, J.Y., Tang, C.Y., Yi, M., et al.,
2016. Distribution characteristics and sources of trace metals
in sediment cores from a trans-boundary watercourse: an
example from the Shima River, Pearl River Delta. Ecotox.
Environ. Safe. 134, 186–195.
Gaur, V.K., Gupta, S.K., Pandey, S.D., Gopal, K., Misra, V., 2005.
Distribution of heavy metals in sediment and water of river
Gomti. Environ. Monit. Assess. 102 (1-3), 419–433.
Griboff, J., Wunderlin, D.A., Monferran, M.V., 2017. Metals, As and
Se determination by inductively coupled plasma-mass
spectrometry (ICP-MS) in edible fish collected from three
eutrophic reservoirs. Their consumption represents a risk for
human health? Microchem J 130, 236–244.
Hänsch, R., Mendel, R.R., 2009. Physiological functions of mineral
micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr. Opin. Plant
Biol. 2009 12 (3), 259–266.
He, H., Liu, X.B., Liu, X.L, Yu, J.L., Li, K.Y., Guan, B.H., et al., 2014.
Effects of cyanobacterial blooms on submerged macrophytes
alleviated by the native Chinese bivalve Hyriopsis cumingii: a
mesocosm experiment study. Ecol. Eng. 71, 363–367.
Hu, B.Q., Deng, L.R., Wen, C.G., Yang, X.L., Pei, P.Z., Xie, Y.H., 2012.
Cloning, identification and functional characterization of a
pi–class glutathione–S–transferase from the freshwater
mussel Cristaria plicata. Fish Shellfish Immunol 32 (1), 51–60.
Hu, J.Y., Xie, Y.H., Tang, Y., Li, F., Zou, Y.A., 2018. Changes of
vegetation distribution in the East Dongting lake after the
operation of the three gorges dam. China. Front. Plant Sci. 9,
1–9.
Ip, C.C.M., Li, X.D., Zhang, G., Wong, C.S.C., Zhang, W.L., 2005.
Heavy metal and Pb isotopic compositions of aquatic
organisms in the Pearl River estuary, South China. Environ.
Pollut. 138 (3), 494–504.
Islam, M.S., Ahmed, M.K., Raknuzzaman, M.,
Habibullah-Al-Mamun, M., Islam, M.K., 2015. Heavy metal
pollution in surface water and sediment: a preliminary
assessment of an urban river in a developing country. Ecol.
Indic. 48, 282–291.
Jovic, M., Stankovic, S., 2014. Human exposure to trace metals and
possible public health risks via consumption of mussels
Mytilus galloprovincialis from the Adriatic coastal area. Food
Chem. Toxicol. 70, 241–251.
Ke, X., Gui, S.F., Huang, H., Zhang, H.J., Wang, C.Y., Guo, W., 2017.
Ecological risk assessment and source identification for heavy
metals in surface sediment from the Liaohe River protected
area. China. Chemosphere 175, 473–481.
Khosravi, M., Bahramifar, N., Ghasempouri, M., 2011. Survey of
heavy metals (Cd, Pb, Hg, Zn and Cu) contamination in
sediment of three sites Anzali Wetland. Iran. J. Health Environ.
4 (2), 223–232.
Kilunga, P.I., Sivalingam, P., Laffite, A., Grandjean, D., Mulaji, C.K.,
De Alencastro, L.F., et al., 2017. Accumulation of toxic metals
and organic micro–pollutants in sediments from tropical
urban rivers, Kinshasa, Democratic Republic of the Congo.
Chemosphere 179, 37–48.
Kumar, V., Sinha, A.K., Rodrigues, P.P., Mubiana, V.K., Blust, R., De
Boeck, G., 2015. Linking environmental heavy metal
concentrations and salinity gradients with metal
accumulation and their effects: a case study in 3 mussel
species of Vitória estuary and Espírito Santo bay, Southeast
Brazil. Sci. Total Environ. 523, 1–15.
Laura, V., 2009. Metallothioneins in aquatic organisms: fish,
Crustaceans, Molluscs, and Echinoderms. Met. Ions Life Sci. 5,
99–237.
Le Croizier, G., Lacroix, C., Artigaud, S., Le Floch, S., Raffray, J.,
Penicaud, V., et al., 2018. Significance of metallothioneins in
differential cadmium accumulation kinetics between two
marine fish species. Environ. Pollut. 236, 462–476.
Lecoeur, S., Videmann, B., Berny, P., 2004. Evaluation of
metallothionein as a biomarker of single and combined Cd/Cu
exposure in Dreissena polymorpha. Environ. Res. 94 (2), 184–
191.
Li, F., Huang, J.H., Zeng, G.M., Yuan, X.Z., Li, X.D., Liang, J., et al.,
2013. Spatial risk assessment and sources identification of
heavy metals in surface sediments from the Dongting Lake,
Middle China. J. Geochem. Explor. 132, 75–83.
Li, J., He, L., Chen, Y.Z., Song, X.S., Lu, H.W., 2017. A bilevel
groundwater management model with minimization of
stochastic health risks at the leader level and remediation
cost at the follower level. Stoch. Environ. Res. Risk Assess. 31
(10), 2547–2571.
Li, X.P., Li, J.R., Wang, Y.B., Fu, L.L., Fu, Y.Y, Li, B.Q., et al., 2011.
Aquaculture industry in China: current state, challenges, and
outlook. Rev. Fish. Sci. 19 (3), 187–200.
Liang, J., Liu, J.Y., Yuan, X.Z., Zeng, G.M., Lai, X., Li, X.D., et al., 2015.
Spatial and temporal variation of heavy metal risk and source
in sediments of Dongting Lake wetland, mid-south China. J.
Environ. Sci. Heal. A 50 (1), 100–108.
Liu, C.F., Tao, S., Long, A.M., 2001. Accumulations of lead and
cadmium in goldfish, Carassius auratus. Acta Hydrobiol. Sinica
25 (4), 41–46.
Liu, X.P., Jiang, J.Y., Yan, Y., Dai, Y.Y., Deng, B., Ding, S.L., et al.,
2018b. Distribution and risk assessment of metals in water,
sediments, and wild fish from Jinjiang River in Chengdu,
China. Chemosphere 196, 45–52.
Liu, J.Y., Liang, J., Yuan, X.Z., Zeng, G.M., Yuan, Y.J., Wu, H.P., et al.,
2015a. An integrated model for assessing heavy metal
exposure risk to migratory birds in wetland ecosystem: a case
study in Dongting Lake Wetland. China. Chemosphere 135,
14–19.
Liu, L., Zheng, G., 2009. Zoology (4th Ed.). Higher Education Press,
Beijing.
Liu, X.H., Lu, S.Y., Meng, W., Wang, W.L., 2018a. Occurrence, source,
and ecological risk of antibiotics in Dongting Lake. China.
Environ. Sci. Pollut. Res. 25 (11), 11063–11073.
Liu, Y., Peng, Y.K., Yue, D.M., Yin, Q., Xiao, L., 2015b. Assessment of
heavy metal enrichment, bioavailability, and controlling
factors in sediments of Taihu Lake. China. Soil Sediment
Contam. 24 (3), 262–275.
Łuczyńska, J., Paszczyk, B., Łuczyński, M.J., 2018. Fish as a
bioindicator of trace metals pollution in aquatic ecosystem of
Pluszne Lake, Poland, and risk assessment for consumer’s
health. Ecotox. Environ. Safe. 153, 60–67.
Makokha, V.A., Qi, Y., Shen, Y., Wang, J., 2016. Concentrations,
distribution, and ecological risk assessment of heavy metals
in the East Dongting and Honghu Lake. China. Expos. Health 8
(1), 31–41.
Malvandi, H., 2017. Preliminary evaluation of heavy metal
contamination in the Zarrin-Gol River sediments, Iran. Mar.
Pollut. Bull. 117 (1-2), 547–553.
McGeer, J.C., Brix, K.V., Skeaff, J.M., DeForest, D.K., Brigham, S.I.,
Adams, W.J., et al., 2003. Inverse relationship between
bioconcentration factor and exposure concentration for
metals: implications for hazard assessment of metals in the
aquatic environment. Environ. Toxicol. Chem. 22 (5),
1017–1037.
 journal of environmental sciences 104 (2021) 335–350
Merciai, R., Guasch, H., Kumar, A., Sabater, S., García-Berthou, E.,
2014. Trace metal concentration and fish size: variation
among fish species in a Mediterranean river. Ecotox. Environ.
Safe. 107, 154–161.
Mziray, P., Kimirei, I.A., 2016. Bioaccumulation of heavy metals in
marine fishes (Siganus sutor, Lethrinus harak, and Rastrelliger
kanagurta) from Dar es Salaam Tanzania. Reg. stud. Mar. Sci. 7,
72–80.
Omwene, P.I., Öncel, M.S., Çelen, M., Kobya, M., 2018. Heavy metal
pollution and spatial distribution in surface sediments of
Mustafakemalpaşa stream located in the world’s largest
borate basin (Turkey). Chemosphere 208, 782–792.
Ouyang, M.F., Xie, Y.A., Li, L.Q., Tian, Q., Zhang, Y., Zhang, G.G.,
et al., 2016. Distribution characteristics and ecological risk of
heavy metals in surface sediment of East Dongting Lake and
its lake inlet. Ecol. Environ. Sci. 25 (7), 1195–1201.
Overnell, J., Abdullah, M.I., 1988. Metallothionein and metal levels
in flounder Platichthys flesus from four field sites and in
flounder dosed with water-borne copper. Mar. Ecol. Prog. Ser.
46, 71–74.
Oweson, C., Sköld, H., Pinsino, A., Matranga, V., Hernroth, B., 2008.
Manganese effects on haematopoietic cells and circulating
coelomocytes ofAsterias rubens (Linnaeus). Aquat. Toxicol. 89
(2), 75–81.
R Core Team, 2020. R: A Language and Environment for Statistical
Computing. R Foundation for Statistical Computing, Vienna,
Austria. https://www.R-project.org.
Rajeshkumar, S., Liu, Y., Zhang, X.Y., Ravikumar, B., Bai, G., Li, X.Y.,
2018. Studies on seasonal pollution of heavy metals in water,
sediment, fish and oyster from the Meiliang Bay of Taihu Lake
in China. Chemosphere 191, 626–638.
Ribeiro, C.A.O., Vollaire, Y., Sanchez–Chardi, A., Roche, H., 2005.
Bioaccumulation and the effects of organochlorine pesticides,
PAH and heavy metals in the Eel (Anguilla anguilla) at the
camargue nature reserve, France. Aquat. Toxicol. 74 (1), 53–69.
Roesijadi, G., 1996. Metallothionein and its role in toxic metal
regulation. Comp. Biochem. Physiol., Part C: Pharmacol.,
Toxicol. Endocrinol. 113 (2), 117–123.
Sabina, R.O., Santos, E.S., Abreu, M.M., 2019. Accumulation of Mn
and Fe in aromatic plant species from the abandoned
Rosalgar Mine and their potential risk to human health. Appl.
Geochem. 4, 42–50.
Salomons, W., Mook, W.G., 1977. Trace metal concentrations in
estuarine sediments: mobilization, mixing or precipitation.
Neth. J. Sea Res. 11 (2), 119–129.
Sivaperumal, P., Sankar, T.V., Nair, P.G.V., 2007. Heavy metal
concentrations in fish, shellfish and fish products from
internal markets of India vis–a–vis international standards.
Food Chem. 102 (3), 612–620.
Solgi, E., Mohammadi Galangashi, M., 2018. Assessing the health
of marine and lacustrine wetland using measurement of
heavy metals in fish species: case study from two Iranian
international wetland (Gomishan and Zarivar). Environ.
Nanotechnology, Monit. Manag. 10, 73–78.
Sun, C., Wei, Q., Ma, L.X., Li, L., Wu, G.H., Pan, L., 2017. Trace metal
pollution and carbon and nitrogen isotope tracing through the
Yongdingxin River estuary in Bohai Bay, Northern China. Mar.
Pollut. Bull. 115 (1-2), 451–458.
Taweel, A., Shuhaimiothman, M., Ahmad, A.K., 2013. Assessment
of trace metals in tilapia fish (Oreochromis niloticus) from the
Langat River and Engineering Lake in Bangi, Malaysia, and
evaluation of the health risk from tilapia consumption.
Ecotox. Environ. Safe. 93, 45–51.
Thomann, R.V., Mahony, J.D., Mueller, R., 1995. Steady-state model
of biota-sediment accumulation factor for metals in two
marine bivalves. Environ. Toxicol. Chem. 14 (11), 1989–1998.
Tong, Y.D., Zhang, W., Deng, C.Y., Wang, X.J., 2016. Pollution
characteristics analysis and risk assessment of total mercury
349
and methylmercury in aquatic products of the Haihe Stem
River. Environ. Sci. 37 (3), 942–949.
Türkmen, M., Ciminli, C., 2007. Determination of metals in fish
and mussel species by inductively coupled plasma-atomic
emission spectrometry. Food Chem 103 (2), 670–675.
USEPA (United States Environmental Protection Agency), 1989.
Assessing Human Health Risks from Chemically
Contaminated Fish and Shellfish: A Guidance Manual.
USEPA (United States Environmental Protection Agency), 2019.
Regional Screening Levels (RSLs)–Generic Tables (Summary
Table). Tables as of: May 2019 https://www.epa.gov/risk/
regional–screening–levels–rsls–generic–tables.
Varol, M., Kaya, G.K., Alp, A., 2017. Heavy metal and arsenic
concentrations in rainbow trout (Oncorhynchus mykiss) farmed
in a dam reservoir on the Firat (Euphrates) River: Risk-based
consumption advisories. Sci. Total Environ. 599, 1288–1296.
Vaughn, C.C., Hakenkamp, C.C., 2001. The functional role of
burrowing bivalves in freshwater ecosystems. Freshw. Biol. 46,
1431–1446.
Wang, Q., Chen, M., Shan, G.Q., Chen, P.Y., Cui, S., Yi, S.J., et al.,
2017. Bioaccumulation and biomagnification of emerging
bisphenol analogues in aquatic organisms from Taihu Lake.
China. Sci. Total. Environ. 598, 814–820.
Wang, L.Q., Dai, L.J., Li, L.F., Liang, T., 2018a. Multivariable
cokriging prediction and source analysis of potentially toxic
elements (Cr, Cu, Cd, Pb, and Zn) in surface sediments from
Dongting Lake. China. Ecol. Indic. 94, 312–319.
Wang, W.X., Fisher, N.S., 1996. Assimilation of trace elements by
the mussel Mytilus edulis: effects of diatom chemical
composition. Mar. Biol. 125 (4), 715–724.
Wang, W.F., Yuan, W.K., Chen, Y.L., Wang, J., 2018b. Microplastics
in surface waters of Dongting Lake and Hong Lake. China. Sci.
Total Environ. 633, 539–545.
Wei, Y.H., Zhang, J.Y., Zhang, D.W., Tu, T.H., Luo, L.G., 2014. Metal
concentrations in various fish organs of different fish species
from Poyang Lake. China. Ecotox. Environ. Safe 104, 182–188.
Wen, C.G., Nie, P., Zhu, Z.M., 2006. Population dynamics of the
water mite Unionicola arcuata (Unionicolidae) in the freshwater
bivalve Cristaria plicata (Unionidae) in Poyang Lake, eastern
China. Dis. Aquat. Org. 70 (1-2), 123–127.
WHO (World Health Organization), 2011. Guidelines for
Drinking-Water Quality, 4th Ed. World Health Organization,
Geneva, Switzerland.
Xia, T.X., Liu, X.H., 2011. Copper and zinc interaction on water
clearance and tissue metal distribution in the freshwater
mussel, Cristaria plicata, under laboratory conditions. Front.
Environ. Sci. Engin. China 5 (2), 236–242.
Xia, W.L., Chen, L., Deng, X.W., Liang, G.D., Giesy, J.P., Rao, Q.Y.,
et al., 2019. Spatial and interspecies differences in
concentrations of eight trace elements in wild freshwater
fishes at different trophic levels from middle and eastern
China. Sci. Total. Environ. 672, 883–892.
Xie, Y.N., OUYANG, M.F., Huang, D.Z., Ou, F.P., Tian, Q., Zhang, Y.,
et al., 2017. Pollution characteristics, sources and ecological
risk of heavy metals in sediments from Dongting Lake and its
lake inlets. Environ. Chem. 36 (10), 2253–2264.
Xu, C., Li, Y.T., 2019. Effect of flow-sediment regime on benthic
invertebrate communities: long-term analysis in a regulated
floodplain lake. Sci. Total Environ. 649, 201–211.
Xu, X.M., Pan, B.Z., Shu, F.Y., Chen, X.F., Ni, J.R., 2017. Distribution
of rare earth elements in the soft tissue of Hyriopsis cumingii
and the correlation with metal speciation of sediments in
Poyang Lake. Acta Sci. Nat. Univ. Pekin. 53 (5), 921–928.
Yi, Y.J., Tang, C.H., Yi, T.C., Yang, Z.F., Zhang, S.H., 2017. Health risk
assessment of heavy metals in fish and accumulation
patterns in food web in the upper Yangtze River. China.
Ecotox. Environ. Safe. 145, 295–302.
350 journal of environmental sciences 104 (2021) 335–350
Zhang, H., Wan, Z.W., Ding, M.J., Wang, P., Xu, X.L., Jiang, Y.H.,
2018a. Inherent bacterial community response to multiple
heavy metals in sediment from river–lake systems in the
Poyang Lake, China. Ecotox. Environ. Safe. 165, 314–324.
Zhang, C., Yuan, Y.J., Zeng, G.M., Liang, J., Guo, S.L., Huang, L., et al.,
2016. Influence of hydrological regime and climatic factor on
waterbird abundance in Dongting Lake Wetland, China:
implications for biological conservation. Ecol. Eng. 90, 473–481.
Zhang, G.L., Bai, J.H., Xiao, R., Zhao, Q.Q., Jia, J., Cui, B.S., et al., 2017.
Heavy metal fractions and ecological risk assessment in
sediments from urban, rural and reclamation-affected rivers
of the Pearl River estuary. China. Chemosphere 184, 278–288.
Zhang, Y.X., Tian, Y., Shen, M.C, Zeng, G.M., 2018b. Heavy metals in
soils and sediments from Dongting Lake in China: occurrence,
sources, and spatial distribution by multivariate statistical
analysis. Environ. Sci. Pollut. Res. 25 (14), 13687–13696.
Zhang, W.W., Ma, J.Z., 2011. Waterbirds as bioindicators of wetland
heavy metal pollution. Procedia Environ. Sci. 10, 2769–2774.
View publication stats
Zhong, W.J., Zhang, Y.F., Wu, Z.H., Yang, R.Y., Chen, X.Y., Yang, J.,
et al., 2018. Health risk assessment of heavy metals in
freshwater fish in the central and eastern North China.
Ecotox. Environ. Safe. 157, 343–349.
Zhou, Y.Q., Jeppesen, E., Li, J.B., Zhang, Y.L., Zhang, X.P., Li, X.C.,
2016. Impacts of Three Gorges Reservoir on the sedimentation
regimes in the downstream–linked two largest Chinese
freshwater lakes. Sci. Rep. 6, 35396.
Zhu, G.R., Yang, Y., 2018. Variation laws and release
characteristics of phosphorus on surface sediment of
Dongting Lake. Environ. Sci. Pollut. Res. 25 (13), 12342–12351.
Zhuang, P., McBride, M.B., Xia, H.P., Li, N.Y., Li, Z.A., 2009. Health
risk from heavy metals via consumption of food crops in the
vicinity of Dabaoshan mine, South China. Sci. Total Environ.
407 (5), 1551–1561.