Ecotoxicology and Environmental Safety 157 (2018) 1–8

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Ecotoxicology and Environmental Safety

journal homepage: www.elsevier.com/locate/ecoenv

Metal concentrations and risk assessment in water, sediment and economic T

fish species with various habitat preferences and trophic guilds from Lake
Caizi, Southeast China
⁎
Zhongguan Jianga, Nan Xub, Bingxiang Liua, , Lizhi Zhoua, Juan Wanga, Chao Wanga,
Bingguo Daia, Wen Xiongc
a
School of Resources and Environmental Engineering, Anhui University, Hefei 230601, PR China
b
Shenzhen Key Laboratory for Heavy Metal Pollution Control and Reutilization, School of Environment and Energy, Peking University Shenzhen Graduate School,
Shenzhen 518055, PR China
c
College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, PR China

A R T I C LE I N FO A B S T R A C T

Keywords: Despite the potential emissions of heavy metal pollution in Lake Caizi due to extensive agriculture, urban growth
Heavy metals and fishing activities, the risk posed by metal concentrations to aquatic environments and human populations
Fish has not yet been studied. In this study we compared the concentrations of Hg, As, Pb, Cd, Cr, Cu and Zn in water,
Habitat preference sediment, and economic fish species with different habitat preferences and trophic guilds across important
Trophic guild
fishery areas in Lake Caizi, located on the northern shore of the Yangtze River, Southeast China. The con-
Risk assessment
Lake Caizi
centrations of Cr in water were found approximately 6 times higher than the safety thresholds established by
international legislation. Cr, Zn, As and Cd concentrations in sediments surpassed the background values for
Yangtze River basin in Anhui Province. However, all the studied fish species in Lake Caizi had metal con-
centrations lower than legislation thresholds established by China and international organizations. Heavy metal
concentrations were found to be significantly higher in demersal (inhabiting near the sediments) and piscivorous
(possessing higher trophic level) fishes than in pelagic/benthopelagic (inhabiting the upper and lower water
column) and herbivorous/planktivorous (possessing lower trophic level) fishes. Our finding demonstrated that
the metal concentrations in fishes are simultaneously influenced by the habitat and bio-accumulation through
the food chain. According to target hazard quotient (THQ) calculations for heavy metal contents in the muscles
of fish species, all the determined heavy metals gave THQ values lower than 1, suggesting the inexistence of
health risks from the intake of fishes from Lake Caizi.

1. Introduction
Heavy metals are a group of the most important pollutants in the
environment due to their potential toxicity, persistence, non degrad-
ability and tendency to bioaccumulate (Ye et al., 2012; Pejman et al.,
2016; Zhang et al., 2016; Otansev et al., 2016). Biochemically, Copper
(Cu), Zinc (Zn), and Chromium (Cr) are classified as essential trace
elements. However, they have the potential to be toxic to biota above
certain threshold concentrations, which makes the identification of
contamination sources of these metals necessary (Vallee and Auld,
1990; Canli and Atli, 2003; Yu et al., 2012). Cadimium (Cd) and Lead
(Pb) are non-essential metals that exhibit extreme toxicity, even at trace
levels (Merian, 1991). Moderate exposure to Pb can significantly reduce
human semen quality, and thus impair human reproductive function
(Telisman et al., 2007). Arsenic (As) is one of the most toxic elements
for human and animal health, which can cause toxic and detrimental
biological effects such as liver, skin, and bladder cancer (Kapaj et al.,
2006). Mercury (Hg) is one of the major environmental concerns due to
its high carcinogenic toxicity to wildlife and humans (Crump and
Trudeau, 2009), as well as its propensity to biomagnify through the
food web of aquatic organisms (Kwon et al., 2012; Wiener et al., 2012;
Zhang et al., 2012).
The floodplain lakes in Yangtze River basin experienced rapid in-
dustrialization, urbanization, and agricultural modernization during
recent decades (Dearing et al., 2015). These activities have released
large amounts of harmful metals to soils, water, atmosphere and also
sediments, which have greatly altered the biogeochemical cycle of toxic
metals and caused widespread environmental contamination (Cheng

⁎
Corresponding author.
E-mail address: liubx@ustc.edu.cn (B. Liu).

https://doi.org/10.1016/j.ecoenv.2018.03.078
Received 16 January 2018; Received in revised form 25 March 2018; Accepted 27 March 2018
Available online 30 March 2018
0147-6513/ © 2018 Elsevier Inc. All rights reserved.
Z. Jiang et al.
Fig. 1. Study area with the designed sampling sites around the main fishery areas of Lake Caizi.
et al., 2015). Fish inhabiting in these lakes might be exposed to high
level of heavy metals. Once heavy metals propagate through the food
web, they may accumulate to levels that can pose a potential risk to
human health (Ofukany et al., 2014). The accelerating growth of urban
areas along the Yangtze River basin, combined with the uncontrolled
increase in industrial and agricultural activities and the poor control of
wastewater, have raised serious concerns about heavy metal pollution
and aquatic products safety (Gao et al., 2015; Liang et al., 2016).
Sediments are the main sink of heavy metals in lakes (MacDonald
et al., 2000; Alloway, 2013), which contain greater amount of heavy
metals than the water column (Ünlü et al., 2008). However, measuring
metal concentrations only in water or sediment does not provide suf-
ficient information on the risk posed by metal bioaccumulation or
biomagnification (Ricart et al., 2010; Maceda-Veiga et al., 2013). Fish
are suitable bioindicators for metal pollution because they occupy a
range of trophic levels and have a known ability to concentrate heavy
metals (Bervoets and Blust, 2003; Agarwal et al., 2007). The life span of
fishes also enables detection of the long-term consequences of metals
(Jorgensen, 2011). In addition, as freshwater fish is particularly fre-
quently consumed in China (Liu and Chen, 2014), the fish best reflect
the consequences of metal pollution in lakes for wildlife and humans.
While analyses of heavy metals in different fish species indicated that
habitat types and trophic levels were important factors influencing
2
Ecotoxicology and Environmental Safety 157 (2018) 1–8
metal accumulation in fishes (Monroy et al., 2014; Yi et al., 2017), few
studies have quantitatively revealed the metal accumulation patterns
for fish species among different trophic guilds and habitat preferences.
Meanwhile, most previous studies of metal pollutants have exclusively
focused on isolated biotic or abiotic components (Wei et al., 2014;
Cheng et al., 2015), a more comprehensive study assessing the mag-
nitude of metal pollutions in water, sediment, and fish species in
Yangtze River basin has been lacking.
Lake Caizi is a large floodplain lake lying on the northern shore of
the Yangtze River, acting as an important source of drinking water for
local people. Lake Caizi is also an important wintering and stopover
habitat for migratory waterbirds on the East Asia-Australia Flyway, and
the key transition section for the upcoming Yangtze River-Lake Chao
water transfer project (Chen et al., 2011). Human populations living in
the area depended strongly on the protein supply by fish from Lake
Caizi as inland fisheries are the most economic and prevalent source of
protein in China (Welcomme, 2001). Fisheries in Lake Caizi went
through a considerable development process in the 1950's, from fishing
wild resources to managed stock-enhanced fish (pen aquaculture). Pen
aquaculture of herbivorous fish and mitten crabs achieved a relatively
higher production in the first few years and then declined later to ac-
company a reduction in macrophytes. In recent decades, the trophic
state of Lake Caizi is transforming from oligotrophic to eutrophic due to
Z. Jiang et al.
the increasing human activities in the catchment (Chen et al., 2011; Liu
et al., 2012). Like other floodplain lakes along the Yangtze River basin,
the lacustrine environment of Lake Caizi has undergone extensive
agriculture, fishing, farming and urbanization during recent decades,
which could be potential sources of heavy metal contamination (Chen
et al., 2011; Cheng et al., 2015). Despite the widespread environmental
deterioration in Lake Caizi, no study on heavy metal monitoring has
been reported.
The present study compared the concentrations of Cu, Cd, Zn, Hg,
Pb, Cr and As in water, sediment and fish species across the main
fishery areas in Lake Caizi. We compared our results with international
and background threshold values in order to make an estimation of the
ecological risk in the study area. Data were also processed to investigate
whether there were significant differences of metals concentrations
between fish species with different trophic guilds and habitat pre-
ferences, to further reveal the factors that influence the enrichment
level of metal elements. Furthermore, the health risk of consuming
fishes in Lake Caizi was also assessed based on daily intake calculation.
2. Material and methods
2.1. Study area and sampling location
Lake Caizi (30°43′−30°58′N; 117°01′−117°09′E) is a large flood-
plain lake lying on the northern shore of the Yangtze River. It covers a
surface area of 242.3 km2 in summer, but can shrink to 145.2 km2 in
winter due to the decline of water level. The water level is 9.5 m with
the average water depth of 1.7 m. This shallow lake is subjected to a
subtropical monsoon climate, with mean annual precipitation of
1200–1389 mm/y, and mean annual air temperature of 16.5 °C. Lake
Caizi collects water from Dasha River, Guache River, Longmian River
and Kongcheng River, and discharges into the Yangtze River passing
through the Zongyang Sluice (Xu et al., 2011; Wang et al., 2012). In
order to obtain an overall picture of the metal pollution in Lake Caizi, 6
locations across the main fishery areas of Lake Caizi were selected to
collect water, sediment and fish samples (Fig. 1).
2.2. Sample collection and processing
Water, sediment and fish samples were collected from the 6 sam-
pling locations across the main fishery areas of Lake Caizi in August
2017 (Fig. 1). Triplicate water samples were collected at each location
in 250-mL polyethylene bottles pre-cleaned with nitric acid (10%) for
24 h and rinsed three times with Milli-Q ultrapure water. Water samples
were immediately filtered through a 0.45-μm Millipore membrane filter
and kept acidified with nitric acid (pH ~2) until metal concentrations
were determined. At each sampling location, three random surface se-
diments (0–10 cm) were collected by a Peterson grab sampler and
brought back to the laboratory. The samples were then freeze-dried,
ground and sieved through a 100-mesh sieve. After that, the dried and
powered surface sediment samples (0.2 g) were treated at 180 °C for
approximately 1 h by microwave digestion with an acid mixture
(HNO3/HCl/HF = 6:3:2).
Fish samples were captured using fyke net (75 × 2 m lead,
50 m × 10 m trap, 3 mm mesh) by local fishermen. A total of 38 in-
dividuals representing 8 species, which are commonly consumed, were
collected. The ecological and biological information of the fishes are
listed in Table 1. After capture, fish were dispatched, ice-cooled, and
transported to the laboratory, where they were dissected, separating
and placing the muscle into a clean Corning centrifuge tube washed
with Milli-Q ultrapure water. The samples were freeze-dried in a va-
cuum freeze-dryer before being ground and homogenized to 100 mesh
with an agate mortar and pestle. Fish muscle samples were mineralized
using teflon tubes. First, approximately 0.2 ± 0.01 g of muscle samples
were weighed and digested with 10 mL of HNO3 (sub boiling grade) and
0.5 mL of HClO4 (sub boiling grade), in closed Teflon tubes on heating
3
Ecotoxicology and Environmental Safety 157 (2018) 1–8
plates set as follows: 120 °C/0.5–1 h, rising to 180 °C/2–4 h, and finally
200–220 °C. After the full digestion, the digested samples were trans-
ferred to a clean PET bottle and diluted with Milli-Q ultrapure water to
80 mL prior to analysis.
2.3. Determination of metals
Concentrations of six heavy metals in all digested solutions, in-
cluding As, Cr, Cd, Cu, Pb and Zn, were determined by an Agilent
7500cx Inductively Coupled Plasma Mass Spectrometer (ICP-MS)
(Agilent Technologies, Santa Clara, CA, USA). All of the ICP-MS mea-
surements were performed by using In and Rh as internal standards
before instrumental analysis. Standards and instrumental and proce-
dural blanks were determined together with samples, and the mean of
three runs was obtained for each sample. Full quantitative analysis was
performed against calibration standard solutions for each metal ele-
ment. However, Concentrations of total Hg in the freeze-dried powder
including sediments and fish muscle samples were analyzed with a di-
rect combustion atomic absorption spectrophotometer (AAS, Milestone
DMA-80, CT, USA). In addition, concentration of total Hg in water was
determined using a Hydra-II AA Mercury Analyzer (Teledyne Leeman
Labs, NH, USA). Before each analysis session, calibration standards
were freshly prepared from the mercury stock solution and used to
establish a standard calibration curve.
2.4. Quality control and assurance
Quality control (QC) and quality assurance (QA) were operated by
procedural blanks, duplicates run in each batch of ten samples, as well
as two standard reference materials, including Certified Reference
MaterialsGSD-5a (National Research Center for Geo-analysis, China,
stream sediment) and European Reference Materials ERM-BB422
(Institute for Reference Materials and Measurements, Belgium, fish
muscle). All results were in good agreement with the certified values
and the recoveries of the reference samples ranged from 86% to 113%.
Concentrations of heavy metals were expressed as mg/kg dry weight for
sediments and fish muscle, and recorded as μg/L for water in this paper.
2.5. Human health risk assessment
The human health risk assessment of heavy metals from fish con-
sumption was estimated using the following equations:
EDI = (C × DC)/(1000 × BW) (1)
THQ = EDI/RfD (2)
where C is the mean concentration of heavy elements in fish (mg/kg);
DC is the daily fish consumption (71 g/day/person) as recorded by the
Food and Agricultural Organization (2008); BW is the average Chinese
adult body weight (58.1 kg) (Gu et al., 2006); RfD is the oral reference
dose (μg/kg/day), which is an estimate of a daily dose of contaminants
that is likely to be without appreciable risk or deleterious effects on
human health (IRIS, 2015; USEPA, 2013).
2.6. Statistical analyses
The means and standard deviations of the metal concentrations in
water, sediment and fish species were calculated. The differences of
heavy metal concentrations among various trophic guilds and habitat
preferences were analyzed with a one-way ANOVA, followed by post-
hoc Tukey tests. If data did not comply with the parametric assumption
of normality and homogeneity of variance, the non-parametric Kruskall
Wallis test and Mann Whitney U test for post-hoc pair-wise comparisons
were used.
Principal components analysis (PCA) was used as an unsupervised
multivariate statistical method that summarizes the variation of a data
Z. Jiang et al. Ecotoxicology and Environmental Safety 157 (2018) 1–8

Table 1
Descriptive summary of 8 fish species collected from Lake Caizi.
Common name Scientific name Trophic guild Habitat preference N Standard length/cm (mean ± SD) Weight/g(mean ± SD)

Bighead carp Aristichthys nobilis Invertivore Pelagic 4 36 ± 2.2 971.3 ± 161.3

Silver carp Hypophthalmichthys molitrix Invertivore Pelagic 5 40.4 ± 2.6 1190 ± 251.9
Wuchang bream Megalobrama amblycephala Herbivore Benthopelagic 5 23.2 ± 2.6 276.6 ± 69.4
Grass carp Ctenopharyngodon idellus Herbivore Benthopelagic 3 37.3 ± 3.9 963.3 ± 126.2
Common carp Cyprinus carpio Omnivore Benthopelagic 6 26.6 ± 3.3 503.6 ± 50.5
Crucian carp Carassius auratus Omnivore demersal 7 17.3 ± 1.6 170.6 ± 54
Catfish Silurus asotus Piscivore demersal 4 22.3 ± 3.7 135.4 ± 14.02
Topmouthculter Culter alburnus Piscivore Benthopelagic 3 16.9 ± 2.3 64.9 ± 11.9

set between samples to a set of uncorrelated components. This method
was performed to determine the differentiation of fish species with
various trophic guilds and habitat preferences based on the elemental
level. Since PCA results are sensitive to measurement scales, the ori-
ginal metal contents in fish muscles were transformed by log (x + 1).
The “varimax” rotation method was used to increase the interpretation
of axes and the number of PCA axes was determined using Kaiser's rule
(eigenvalue ≥ 1) (Legendre and Legendre, 1998). All statistical ana-
lyses were performed with the R statistical software (R Development
Core Team, 2016), and a significance level of 0.05 was employed.
3. Results and discussion
3.1. Heavy metal concentrations in water samples and surface sediments
The concentrations of heavy metals in water and sediments from
Lake Caizi are presented in Table 2, together with the background va-
lues or legislation thresholds. Hg, Cu, Zn, As, Cd and Pb concentrations
in water from all the studied locations were lower than the toxicity
reference value (TRV) for freshwater established by USEPA (2009). In
contrast, the highest mean value of Cr (66.7 μg/L) in water was 6 times
higher than legal limits (11 μg/L). In fact, mean Cr values in water from
all sampling sites were higher than the TRV, indicating serious Cr
contamination in water columns of Lake Caizi.
Only As concentrations in sediments from all the studied locations
exceed the legislation thresholds based on sediment quality guidelines
for freshwater systems (MacDonald et al., 2000). The mean content of
Cu in sediments of Lake Caizi was lower than the background value for
Yangtze River Basin in Anhui Province (Fang et al., 2017) and for Lake
Caizi in 2004 (Cheng et al., 2015), while those of Hg and Pb were
comparable with the both background values. However, the averaged
concentrations of Cr, Zn, As and Cd exceeded the background values
shown in Table 2, with the maximum value of As and Cd being 4.7 and
3.3 times higher than background values for Yangtze River Basin in
Anhui Province (Fang et al., 2017). These results showed that there
were obvious accumulations of As and Cd in sediments of Lake Caizi.
In our study, heavy metal concentrations in water and sediments
were relatively high and in some cases (Cr, Zn, As and Cd) exceeded the
background or threshold concentration values. Rapid industrialization,
urbanization, and agricultural modernization surrounding the catch-
ment of Lake Caizi could be potential sources of heavy metal con-
tamination (Chen et al., 2011; Cheng et al., 2015). The run-off from
adjacent agricultural areas might be responsible for Cr, Zn, As and Cd
release since these metals are often present in fertilizers or pesticides
(Alloway, 2013). In addition, the release of domestic wastewater might
increase concentrations of some metals (Cu, Zn, Pb and Fe) due to the
frequent uses of the household products, such as cleaning materials,
toothpaste and cosmetics (Alloway, 2013). Lake sediments rich in

Table 2
Heavy metal concentrations in water (μg/L) and surface sediments (mg/kg, dry weight) collected from each sampling site in Lake Caizi.
Sites Hg Cr Cu Zn As Cd Pb

Water
S1 0.04 67.85 4.05 32.76 3.02 0.21 3.50
S2 0.04 66.45 1.84 33.02 2.18 0.07 1.57
S3 0.04 68.75 2.01 34.18 5.15 0.15 3.11
S4 0.04 65.30 3.22 35.60 5.44 0.11 2.48
S5 0.05 66.25 2.08 33.72 1.77 0.09 1.67
S6 0.05 65.60 2.07 36.70 1.74 0.09 2.16
Range 0.04–0.05 65.3–68.75 1.84–4.05 32.76–36.7 1.74–5.44 0.07–0.21 1.57–3.5
Mean ± SD 0.04 ± 0.004 66.7 ± 1.339 2.54 ± 0.887 34.33 ± 1.536 3.21 ± 1.676 0.12 ± 0.054 2.42 ± 0.776
TRV 2 11 1300 5000 150 5 2.5
Sediments
S1 0.04 89.55 21.34 90.50 40.30 0.53 29.35
S2 0.05 94.60 23.78 110.65 40.58 0.51 36.50
S3 0.05 81.20 17.70 79.28 40.73 0.48 24.31
S4 0.04 82.45 19.00 75.38 40.73 0.51 26.18
S5 0.08 102.20 26.63 136.30 38.10 0.57 35.90
S6 0.06 106.08 28.73 140.70 45.48 0.58 46.55
Range 0.04–0.08 81.2–106.08 17.7–28.73 75.38–140.7 38.1–45.48 0.48–0.58 24.31–46.55
Mean ± SD 0.05 ± 0.014 92.68 ± 10.198 22.86 ± 4.319 105.47 ± 28.406 40.98 ± 2.419 0.53 ± 0.04 33.13 ± 8.241
LT 1.06 111 149 459 33 4.98 128
BR 0.05 80.00 32.00 83.00 8.80 0.16 29.00
BC 0.051 80 32.5 98 10.3 0.202 38.3

SD is the standard deviation.

TRV stands for toxicity reference value for freshwater proposed by USEPA (2009).
LT stands for legislation thresholds reported for metal concentrations in sediments based on sediment quality guidelines for freshwater systems (MacDonald et al.,
2000).
BR is the background value of regional ecological geochemical survey of the Yangtze River Basin in Anhui Province (Fang et al., 2017).
BC is the background value of Lake Caizi in 2004 (Cheng et al., 2015).

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Z. Jiang et al. Ecotoxicology and Environmental Safety 157 (2018) 1–8

Table 3
Heavy metal concentrations in 8 fish species (mg/kg, dry weight) sampled from Lake Caizi (mean ± SD).
Fish species Hg Cr Cu Zn As Cd Pb

Aristichthys nobilis 0.055 ± 0.009 0.688 ± 0.063 0.562 ± 0.049 14.226 ± 0.735 0.246 ± 0.116 0.008 ± 0.001 0.102 ± 0.009
Hypophthalmichthys molitrix 0.092 ± 0.012 0.582 ± 0.104 0.540 ± 0.061 13.817 ± 0.696 0.296 ± 0.086 0.007 ± 0.001 0.104 ± 0.016
Megalobrama amblycephala 0.108 ± 0.014 0.555 ± 0.095 0.651 ± 0.084 17.039 ± 2.390 0.240 ± 0.110 0.009 ± 0.001 0.184 ± 0.054
Ctenopharyngodon idellus 0.028 ± 0.012 0.687 ± 0.069 0.583 ± 0.035 15.356 ± 0.579 0.055 ± 0.012 0.009 ± 0.001 0.073 ± 0.007
Cyprinus carpio 0.061 ± 0.023 0.634 ± 0.069 0.721 ± 0.084 24.210 ± 3.810 0.337 ± 0.218 0.009 ± 0.002 0.103 ± 0.014
Carassius auratus 0.101 ± 0.043 0.817 ± 0.050 0.903 ± 0.137 51.179 ± 11.281 0.397 ± 0.211 0.011 ± 0.002 0.201 ± 0.052
Silurus asotus 0.176 ± 0.013 1.028 ± 0.120 1.270 ± 0.132 25.018 ± 2.540 0.069 ± 0.014 0.010 ± 0.001 0.127 ± 0.017
Culter alburnus 0.148 ± 0.043 1.031 ± 0.035 0.673 ± 0.134 60.833 ± 2.346 0.537 ± 0.230 0.008 ± 0.001 0.103 ± 0.021
Legislation thresholds 0.5a 2a 40b 100c 6b 0.1a 0.5a

SD is the standard deviation.

a
China National Standards (2017).
b
European Commission (2006).
c
Food and Agriculture Organization, World Health Organization (1998).

organic matter act as more stable sinks for metals compared to water
since humic substances in sediments can form strong metal complexes
(Balogh et al., 1999; Rognerud and Fjeld, 2001). Lake sediments also
play an important role in the bioaccumulation through the food web as
the long-term release of metals from contaminated sediments is well
known (Burton, 2002). In comparison to Lake Chao, one of its adjacent
water bodies, the averaged Cr, As and Cd concentrations in sediments of
Lake Caizi were higher than those of Lake Chao (Cr = 68.5, As = 10.8
and Cd = 0.357 mg/kg) (Fang et al., 2017). The excessive heavy mental
pollutants in the sediments of Lake Caizi entailed a considerable po-
tential ecological risk as metals can be incorporated into the biota
through the aquatic food webs (MacDonald et al., 2000).
3.2. Levels of metal accumulation in fish species
Metal concentrations in the muscle of eight fish species from Lake
Caizi are shown in Table 3. In this study, the wet and dry weight of fish
muscles were determined before and after freeze drying, and the dry
weight of fish muscle was 20% of the wet weight. The studied fish
species in Lake Caizi showed metal concentrations (dry weight) lower
than Legislation thresholds established by China and international or-
ganizations (CNS, 2017; EC, 2006; FAO/WHO, 1998). The converted
metal concentrations in wet weight (1/5 of dry weight) would be even
lower than the limits which were proposed as metal contents in wet
weight. Our results suggested that metal toxicity accumulated through
the consumption of fish species from Lake Caizi is probably not a sig-
nificant threat to human health. Concentrations of all the studied heavy
metals in fish muscles were lower in Lake Caizi in comparison to other
polluted water ecosystems along the Yangtze River basin. In Lake
Taihu, for example, averaged metal concentrations in the muscles of
fish were reported to be 3.27 mg/kg for Cu, 16.54 mg/kg for Pb,
145.10 mg/kg for Zn, 2.59 mg/kg for Cr, 1.15 mg/kg for Cd, 3.28 mg/
kg for As and 0.25 mg/kg for Hg (Fu et al., 2013). Compared with
adjacent lake, the heavy metal concentrations in fish muscles from Lake
Caizi were also relatively lower than those from Lake Chao. Though
comparable metal concentrations in fish muscles were observed for Pb,
Cr, Cd, and Hg, the mean concentrations of Cu, Zn and As in the present
study were lower than those reported in the fish muscles collected from
Lake Chao (Fang et al., 2017). Our results revealed that heavy metal
concentrations in all analyzed fish species from Lake Caizi were rela-
tively low and at a safe level.
We found the highest Hg and Cu concentrations in Silurus asotus,
highest Cr, Zn, and As concentrations in Culter alburnus, and the highest
Cd and Pb concentrations in Carassius auratus (Table 3). In contrast, the
lowest concentrations of Cu, Zn, and Cd were detected in Hy-
pophthalmichthys molitrix. The lowest concentrations of Hg, As and Pb
were detected in Ctenopharyngodon idellus. The lowest concentrations of
Cr were found in Megalobrama amblycephala (Table 3). It is noted that
the highest concentrations of all the eight heavy metals tended to
appear in the piscivorous fishes with higher trophic level (e.g., Silurus
asotus and Culter alburnus) or fish species living in the demersal layers of
lacustrine environment (e.g., Silurus asotus and Carassius auratus). In
contrast, the pelagic and planktivorous fishes (e.g., Hypophthalmichthys
molitrix and Ctenopharyngodon idellus), and the herbivorous fishes (e.g.,
Megalobrama amblycephala) with low trophic level were inclined to
accumulate less heavy metals.
The concentrations of all metals analyzed except for As and Pb
differed significantly among trophic guilds (p < 0.05). Concentrations
of Hg and Cr in piscivorous fishes were significantly higher than other
trophic guilds (p < 0.05). Piscivorous and omnivorous fishes had
higher Cu and Zn concentrations than planktivorous and herbivorous
fishes (p < 0.05). Concentrations of Cd in planktivorous fishes were
significantly lower than those of other trophic guilds (p < 0.05). We
also detected significant differences for all studied metals except for As
among different habitat preferences (p < 0.05). Concentrations of Hg
and Cd in pelagic fishes were significantly lower than fishes prefer other
habitats while the concentrations of Cr and Pb in demersal fishes were
significantly higher than others (p < 0.05). Meanwhile, concentrations
of Cu and Zn exhibited a clear gradient (p < 0.05) from pelagic to
demersal fishes: pelagic < benthopelagic < demersal (Fig. 2).
To summarize, our results suggested that demersal fishes inhabiting
near the sediments and piscivorous fishes with higher trophic level
were likely to accumulate higher heavy metal concentrations than
fishes inhabiting the upper water column and other feeding habits. Our
results supported the hypothesis that the sediment was the major up-
take pathway for trace metal pollution and played a crucial role in the
heavy metal uptake for fish (Luoma and Bryan, 1978). Fish living near
the lake sediments and feeding on humic substances or benthic in-
vertebrates promoted the transfer and accumulation of heavy metals
from sediments to fish species (Burrows and Whitton, 1983). Therefore,
bottom dwelling fishes are found to exhibit higher concentration of
trace metals than pelagic fishes (Wei et al., 2014; Yi et al., 2017).
Meanwhile, our results suggested a biomagnification of heavy metals
along the trophic levels as piscivorous species had higher level of metal
contents than omnivorous and herbivorous species. Similar results were
reported in previous studies (Phillips et al., 1980; Yi et al., 2017). These
results were due to fish species feeding on algae or vegetations accu-
mulating lower heavy metal contents (Yi and Zhang, 2012). Metal
bioconcentration and bioaccumulation processes have long been pur-
ported to be complex and difficult to interpret (Mendoza-Carranza
et al., 2016). Our finding demonstrated that the metal concentrations in
fishes are simultaneously influenced by the habitat and bio-accumula-
tion through the food chain.
The first two axes of the Principle Component Analysis (PCA) ex-
plained approximately 65.4% of the variation in heavy metal con-
centrations among the studied fish species(Fig. 3). The first principal
component (PC1) explained 44.7% of the variation and loaded strongly
for Hg, Cr, Cu, Zn and Cd, while the second component (PC2) explained

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Fig. 2. Metal concentrations (mg/kg dry weight) in the muscle of fish species among different trophic guilds (Pla: planktivore; Omn: omnivore; Pis: piscivore; Her:
herbivore) and habitat preferences (Pel: pelagic; Dem: demersal; Ben: bnthopelagic). The letters (a, b, c) group fish species by variable, considered homogenous at
p < 0.05.

20.7% of the variation, with strong loadings of As and Pb. Heavy metal
concentrations among different trophic guilds and habitat preferences
exhibited a clear gradient along PC1. The herbivorous and plankti-
vorous fish species were positioned to the negative end of PC1, whereas
piscivorous fish species were grouped to the positive end of PC1.
Meanwhile, pelagic and demersal fish species posited to the negative
and positive end of PC1 respectively. Concentrations of Hg, Cr, Cu, Zn
and Cd contributed most of the differentiations. The grouped results on
PCA are consistent with the paired comparisons of the averaged con-
centrations of metal contents among different trophic guilds and habitat
preferences. The consisted Hg, Cr, Cu, Zn and Cd on PCA indicates
homogeneous anthropogenic pollution sources for these five metals.
3.3. Health risk assessment
Food safety is one of the current major public health issues in the
world, especially in developing countries (Wong, 2017). Fishes from the
studied lake are important aquatic products around Anqing City region.
In addition, these species of fish are mostly consumed by the local
people. Therefore, it is necessary to assess the health risks caused by the
consumption of these fish species. The RfDs were listed in Table 4 based
on the USEPA (USEPA, 2017). The estimated maximum daily intake

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Z. Jiang et al. Ecotoxicology and Environmental Safety 157 (2018) 1–8

Fig. 3. Principal component analysis of heavy

metal concentrations in fish species from Lake
Caizi, with biplots showing the main patterns
of variation of the 7 metals in 8 fish species
grouped in 4 trophic guilds (A) and 3 habitat
preferences (B). A: Circles represent herbi-
vorous fishes, squares represent piscivorous
fishes, triangles represents planktivorous
fishes, and cross represent omnivorous fishes;
B: Circles represent pelagic fishes, squares re-
present benthopelagic fishes, triangles re-
present demersal fishes.

Table 4
Estimated target hazard quotients (THQ) for 7 metals from fish consumption.
Heavy metal Hg Cr Cu Zn As Cd Pb

RfD (mg/kg/day) 0.00016 0.003 0.04 0.3 0.0003 0.001 0.004

EDI-mean (mg/kg/day) 2.329E−05 1.798E−04 1.830E−04 6.892E−03 6.947E−05 2.221E−06 3.244E−05
EDI-max (mg/kg/day) 4.807E−05 2.944E−04 3.569E−04 1.619E−02 1.948E−04 3.233E−06 6.818E−05
THQ-mean 0.146 0.060 0.005 0.023 0.232 0.002 0.008
THQ-max 0.300 0.098 0.009 0.054 0.649 0.003 0.017

RfD: oral reference dose; EDI-mean: estimated averaged daily intake; EDI-max: estimated maximum daily intake; THQ-mean: averaged target hazard quotients; THQ-
max: maximum target hazard quotients. All the units of concentrations are based on the wet weight.

(EDI-max) for Hg, Cr, Cu, Zn, As, Cd and Zn were 4.807 × 10−4,
2.944 × 10−4, 3.569 × 10−4, 1.619 × 10−4, 1.948 × 10−4,
−4 −4
3.233 × 10 and 6.818 × 10 mg/kg/day respectively, which were
lower than the corresponding RfDs. The THQ-max of each metal
through consumption of fish followed the descending order of As >
Hg > Cr > Zn > Pb > Cu > Cd. The THQ-mean of each metal from
fish consumption based on the average concentration were all lower
than 1, suggesting that people would not experience significant health
risks from the intake of fish species from Lake Caizi (Table 4).
4. Conclusions
This study provides new information on concentrations of Hg, As,
Pd, Cd, Cr, Cu and Zn in water, sediment and economic fish species
across important fishery areas in Lake Caizi. Heavy metal concentra-
tions in water and sediments were relatively high and in some cases
exceeded the background or threshold concentration values, illustrating
a considerable potential ecological risk. However, the relatively low
metal concentrations in fish muscles with all the target hazard quotients
less than 1 suggested that metal toxicity through the consumption of
fish species from Lake Caizi would not pose a threat to human health.
We detected significantly different metal accumulations in fish species
among various trophic guilds and habitat preferences. Our results de-
monstrated that metal concentrations in fishes are simultaneously in-
fluenced by the habitat and bio-accumulation through the food chain.
Acknowledgments
This work was financially supported by the National Natural Science
Foundation of China (No. 31600438), the Key Foundation of Anhui
Province Education Department (KJ2016A025), the China Postdoctoral
Science Foundation (2017M622020), and the Science and Technology
Planning Project of Shenzhen, China (JCYJ20150629144818001).
Thanks are given to Quanzhong Li, Yi Gao, and Xiaoli Wang, for their
help during the analyses.
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