Environmental Pollution 220 (2017) 1138e1146

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

Mercury exposure and source tracking in distinct marine-caged sh

farm in southern China*
Xiaoyu Xu a, b, c, Wen-Xiong Wang a, b, *
a
Marine Environmental Laboratory, HKUST Shenzhen Research Institute, Shenzhen 518000, China
b
Division of Life Science, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong
c
Savannah River Ecology Lab, The University of Georgia, PO Drawer E, Aiken, SC 29802, United States

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

Article history: Coasts of South China have experienced an unprecedented growth in its marine-caged sh industry. We
Received 19 August 2016 analyzed mercury concentrations and stable mercury isotope ratios in fourteen sh species from two
Received in revised form cage-cultured farms in Southern China. Total mercury concentrations of all species were lower than the
7 November 2016
human health screening values, but the human exposures through consumption of several carnivorous
Accepted 7 November 2016
Available online 28 November 2016
sh exceeded the USEPA's reference dose. Isotopic compositions in the sediment (d202Hg:
1.45
to
1.23; D199Hg:
0.04 to e0.01) suggested that mercury in these farms were from coal com-
bustion and industrial inputs. Commercial food pellets and fresh sh viscera provided the major sources
Keywords:
Mercury
of methylmercury to the farmed sh and dominated their mercury isotopic signatures. Non-carnivorous
Source tracking sh presented lower d202Hg and D199Hg values than the carnivorous sh. Using a mixing model, we
Farmed sh demonstrated that the majority of mercury in non-carnivorous species came from pellets and in
Diets carnivorous sh came from combined diets of pellets and viscera. Meanwhile, methylmercury concen-
Methylmercury trations and % methylmercury in the sh were positively correlated with d202Hg values but not with
D199Hg values, mainly because sh eating similar feeds maintained similar D199Hg values. Environmental
inuences of cage farming such as sh feces and uneaten viscera that continuously provide organic
mercury to the environments need to be considered.
2016 Elsevier Ltd. All rights reserved.

1. Introduction manufactures, and sh processor (Gopakumar, 2009).

The aquaculture industry in China has rapidly expanded as de-
mand for domestic and international seafood rises (FAO, 2014).
About 74% of the total sheries production now comes from
aquaculture and 38% of the aquaculture production comes from
marine cage industry (NBS, 2014). Marine cage farming began in
1970s and developed to a commercial scale in 1980s in the South
China. Fujian is one of the most important provinces for marine
cage culture, with more than 40 cultured species (Chen, 2006) and
3.6 million tons production in the year of 2015 (CNFM, 2016). The
rapid growth is attributed to the suitable nearshore sites in Fujian,
well established breeding techniques, improvement of culture
systems, and availability of supporting industries such as feed, net
*
This paper has been recommended for acceptance by David Carpenter.
* Corresponding author. Marine Environmental Laboratory, HKUST Shenzhen
Research Institute, Shenzhen 518000, China.
E-mail address: wwang@ust.hk (W.-X. Wang).
Marine cage culture utilizes existing coastal water resources but
encloses the sh in a cage that allows the water to pass freely
(Masser, 1988). The environmental inuences include direct im-
pacts on water quality, such as eutrophication, turbidity and
decrease of dissolved oxygen, as well as secondary impacts on
primary production, like the formation of harmful algal blooms
(Price et al., 2015; Price and Morris, 2013). Sitting farms in deep and
well-ushed waters usually provide the best protection of water
quality (Price et al., 2015; Price and Morris, 2013). However, most
sh farms in Southern China provinces are located in nearshore
sites with minimal ushing and they use fresh sh viscera as feeds
that introduce a large amount of nutrient loading (Onsanit et al.,
2012). High accumulation rates of organic matter were already
observed in both the estuarine and coastal environments in the
southeastern China (Zhang et al., 2009). More importantly, estu-
aries in Southern China receive massive metal discharges from the
e-waste recycling, domestic sewage, agricultural and industrial
output from the coastal Special Economic Zones (Pan and Wang,
2012). The complicated environments raise discussions on the

http://dx.doi.org/10.1016/j.envpol.2016.11.021
0269-7491/ 2016 Elsevier Ltd. All rights reserved.
 X. Xu, W.-X. Wang / Environmental Pollution 220 (2017) 1138e1146
safety of consuming seafood from these sh farms and creates
serious concerns about the ecological and public health.
Mercury (Hg) is a major environmental concern due to its global
atmospheric dispersion, propensity to biomagnication, and high
toxicity to wildlife and humans (USEPA, 2000, 2011). Many studies
reported that anthropogenic Hg from various sources were released
in China after 1990s though signicant efforts have been made to
reduce its emission (Feng, 2005; Zhang and Wong, 2007). Mercury
accumulation in the seafood from Chinese market has become a
crucial issue in recent years, which leads to a major problem of
source tracking. The high mobility of Hg, various pollutions along
the coastal lines of southeastern China, and the mixed sh feeds
applied by the sherman all contributed to the difculty of iden-
tifying Hg sources in the cage-farmed sh.
Stable Hg isotopes have been applied to study the sources and
biogeochemical pathways of Hg in the environment (Bergquist and
Blum, 2007; Perrot et al., 2010; Yin et al., 2016). The isotopic sig-
natures of mass dependent fractionation (MDF) and mass inde-
pendent fractionation (MIF) are used as a two-dimensional
source tracer (Yin et al., 2013). Marine caged sh farm, with mul-
tiple sources of Hg input, will be a unique system to employ this
technique. However, previous studies only analyzed Hg concen-
trations in these areas (Onsanit et al., 2012; Pan et al., 2014; Pan and
Wang, 2012; Yatawara et al., 2010). In the present study, we
collected fourteen species of commonly eaten sh from two large
sh farms in Fujian province, including herbivores, omnivores, and
carnivores. Mercury concentrations and stable Hg isotopic com-
positions were analyzed in their axial muscle. Meanwhile, we
collected and analyzed samples of surface sediment and different
types of sh feeds. This is the rst study that adopt stable Hg iso-
topes to track sources of Hg in the cage cultured sh farms. We
investigated Hg bioaccumulation and speciation, and tracked Hg
sources by comparing its isotopic compositions to the sediment and
dietary sources. We evaluated human exposure to Hg through the
consumption of sampled sh by calculating people's daily meth-
ylmercury intake rate. Mercury concentrations and isotopic signa-
tures were also compared between the cage cultured and wild
caught sh in order to better understand the differences of Hg
biomagnication in different environments.
2. Materials and methods
2.1. Filed sampling
Two sh farms along the coast of South China Sea were sampled
during the summer of 2015 (Fig. 1). Dongshan Island and Luoyuan
Bay that locate in the Fujian Province (China) are both famous for
cage culture industries. Dongshan Island produced a variety of sh
species, but Luoyuan Bay focused on groupers (predatory). We
collected fteen species of marine-caged sh: rabbitsh (Siganus
fuscescens), turbot (Paralichthys olivaceus), spotted seatrout (Cyn-
oscion nebulosus), blackhead seabream (Acanthopagrus schlegelii),
yellown seabream (Acanthopagrus latus), red seabream (Pagrus
major), Japanese eel (Anguilla japonica), large yellow croaker (Lar-
imichthys crocea) and sardine (Sardinella jussiu) were sampled in
the Dongshan Island Fish Farm (Fig. 1); small yellow croaker (Lar-
imichthys polyactis), orange spotted grouper (Epinephelus coioides),
eightbar grouper (Epinephelus octofasciatus), and Japanese seabass
(Lateolabrax japonicus) were sampled in the Luoyuan Bay Fish Farm
(Fig. 1). Except sardines that are difcult to be cultured and have
relatively low commercial values, the other species are popular
during cage cultures in southern China due to their well-developed
breeding technology, high consumption rates, and high commercial
and nutritive values. Meanwhile, we collected the surface sediment
and the sh feeds. Duplicated cages were randomly selected at each
1139
site, and the surface sediment under each cage was sampled. Four
types of sh feeds that are commonly used were collected. The
feed-1 (Dongwan, China, 4 mm diameter, dry) and feed-2 (Tongwei,
China, 9 mm diameter, dry) are commercial food pellets composing
of marine krill, herring, sh oil, algae, vitamins, and wheat our.
The feed-1 was sampled from Dongshan Island and the feed-2 was
sampled from Luoyuan Bay. The feed-3 and feed-4 are self-made
feeds (wet) composing of fresh sh viscera from the sold food
sh and trash sh. There are a large amount of seafood restaurants
locating at Dongshan Island and Luoyuan Bay. Food sh (cultured
sh) in such places is usually killed, processed, and cooked right
after being selected by the customers, and the left viscera is kept
and used to feed other carnivorous sh in the farms. Trash sh is
any small sh that has little value as a food sh such as the anchovy
or clupeids (Onsanit et al., 2012). The feed-3 was from Dongshan
Island and the feed-4 was from Luoyuan Bay.
2.2. Sample preparation
The sampled sh were killed on ice in the sh farm, cleaned
with water, placed in a plastic bag, and stored at
20  C prior to
process. Fish species, body weight, total length, and sex were
determined. The axial muscle of individual sh was dissected,
weighted, and freeze-dried at
80  C (Freeze-Dryer, ilShinBioBase
Co. Ltd., South Korea) for 72 h. The dry weight was also measured
after freeze drying, and the wet to dry weight quotients were
calculated. Each dried sample was ground before digestion. The
sediment and sh feeds were kept in dark plastic bags at
20  C
and freeze dried at
80  C for a week. The Hg concentrations for
sh muscle in this study were either based on wet weight (ww) or
dry weight (dw), but the concentrations for sediment and sh feeds
were all based on dry weight.
2.3. Mercury analysis
Total mercury (THg) and methylmercury (MHg) concentrations
were analyzed for each sample, and the percentage of THg pre-
senting as MHg was expressed as %MHg. For THg analysis, dried
muscle and sh feeds were digested with mixed acids
(H2SO4:HNO3 1:4, v/v, ultrapure, Sigma, USA) on the block heater
(BT5D, Grant Instruments, UK) at 95  C for 3e4 h (Yin et al., 2013),
and Hg in the sediment was extracted with mixed acid
(H2SO4:HNO3 4:5, v/v) for 24 h (Perrot et al., 2010). Digested
sample was appropriately diluted, oxidized to Hg(II) with a hy-
drochloride/bromate/bromide mixture (USEPA, 2007), and intro-
duced to the cold vapor atomic uorescence spectrometry (Quick
Trace M-8000, CETAC Technologies, USA). The Hg(II) in the systems
was converted to Hg(0) with stannous chloride (USEPA, 2007),
which was then separated from the solution by purging with ni-
trogen, collected by gold traps, and thermally desorbed from the
analytical trap into a uorescence detector. For MHg analysis,
samples were digested with alkaline (25% KOH in methanol) at
75  C in the oven for 3 h. The appropriate aliquots of digested
samples were taken, buffered with sodium acetate to pH 4.9, and
ethylated by sodium tetraethylborate (Liang et al., 1994a, 1994b).
MHg concentration was analyzed by an automated MHg analytical
system (MERX, Brooks Rand, USA). The quantication of MHg was
automatically performed by the gas chromatographic separation
and pyrolysis, following the atomic uorescence detection.
Standard curves were established using liquid Hg standards
(THg: PerkinElmer, USA; CH3HgCl: Brooks Rand, USA) within each
analytical session. Precision and accuracy for the analytical system
were quantied with blanks, 10% analytical duplicates, and 10%
standard reference material (DORM-2 and DORM-4, National
Research Council of Canada). Precision expressed as relative
1140 X. Xu, W.-X. Wang / Environmental Pollution 220 (2017) 1138e1146
Fig. 1. Map of sampling sites (Dongshan Island and Luoyuan Bay) along the coastal line of South China Sea.
percent difference for duplicate samples averaged 3.0 (SD 6.2%,
n 18) for THg analysis and 4.4 (SD 3.5%, n 12) for MHg
analysis. The mean percent recoveries of THg analysis were 100.4
(SD 6.4%, n 8) for DORM-2 and 100.9 (SD 5.5%, n 22) for
DORM-4. The mean percent recoveries of MHg analysis were 99.4
(SD 10%, n 12) for DORM-4.
2.4. Mercury exposure and consumption advice
Estimated dietary intakes of MHg associated with consumption
of sampled sh were calculated. Assuming a person selected only
one sh species to eat per day, the annual-average daily MHg intake
rate was calculated using the following equation (USEPA, 2011):
MHgC*a*CR
DIR
BW
where DIR daily intake rate (mg/kg BW-day), MHgC MHg
concentration (ng/g, ww) in the muscle, a food preparation/
cooking adjustment factor, CR consumption rate (g/day), and
BW body weight (kg). Results of MHg concentrations in this study
were used as MHgC. We included the food preparation/cooking
adjustment factor (a) because the cooking procedure usually
removes non-muscle tissue such as water and fat and increases Hg
concentrations in the tissue. The USEPA recommended 1.5 for this
factor (USEPA, 2011). Consumption rates (CR) derived from a di-
etary survey in the South China were adopted in this equation
because their sampling area, the Pearl River Delta, was very close
our sampling locations (Guo et al., 2010). Their nsh consumption
rates of 64 g/day for male and 55 g/day for female (age > 18) were
used as CR (Guo et al., 2010). The average body weight (BW) was
60 kg (Wang et al., 2011).
The widely used limit of dietary intake rate of MHg is the
reference does (RfD) of 0.1 mg/kg-day recommended by USEPA
(USEPA, 2000). Assuming a person selects only one sh species to
eat per day and the DIR equals to the established limits, the
maximum consumption rate (mCR, g/day) relative to a seafood
species can be calculated as shown in equation (2):
RfD*BW
mCR
MHgC*a
Assuming the seafood meal size (MS, g/meal) of an adult in the
sampling area is about 249 g/meal (Xu and Newman, 2015), the
maximum meal frequencies (MF, meal/month) relative to a seafood
species can be calculated as shown in equation (3):
mCR
MF *30 (3)
MS
2.5. Mercury stable isotope analysis
The digests for THg analysis were diluted to 1e3 ng/mL of THg
with Milli-Q water (Yin et al., 2013, 2016). Standard reference
material (DORM-2, dogsh muscle) was prepared in the same way.
Mercury isotopic ratios were determined by MC-ICP-MS (Nu
Plasma HR, Nu Instruments, Great Britain) with a modied cold
(1) vapor generation system that introduced Hg to the detection sys-
tem (Lin et al., 2015). The internal standard thallium (Tl) was added
to the Hg vapor with a desolvating nebulizer (DSN-100, Nu In-
struments, Great Britain), and the Hg isotope ratios were corrected
for instrumental mass discrimination by simultaneously moni-
toring the 205Tl/203Tl ratio of a standard solution (Yin et al., 2013).
Instrumental mass bias was also corrected using a sample-standard
bracketing with NIST 3133 (in 10% HCl), whose concentration and
matrix matched with that of the samples (Yin et al., 2016). Mercury
isotopic compositions were reported in delta notation as permil
() deviation from NIST 3133 Hg standard with equation (4)
(Bergquist and Blum, 2007), where xxx is mass of each Hg
isotope between 199 and 202. The d202Hg values were reported to
indicate mass dependent fractionation (MDF) in this study, and the
mass independent fractionation (MIF) were reported in capital
delta notation (DxxxHg) using equations (5) and (6) (Bergquist and
Blum, 2007).

h . i
dxxx Hg xxx Hg=198 Hgsample xxx Hg=198 HgNIST 3133


1 *1000
(4)
D199 Hgzd199 Hg
d202 Hg*0:252 (5)
(2)
D201 Hgzd201 Hg
d202 Hg*0:752 (6)
 X. Xu, W.-X. Wang / Environmental Pollution 220 (2017) 1138e1146 1141

The analytical uncertainty was quantied by analysis of stan-
dard reference materials: the mean values and 2 standard de-
viations (SDs) of UM-Alma den were
0.58 0.09 for
d202Hg,
0.05 0.04 for D201Hg, and
0.02 0.03 for D199Hg
(n 15); the mean values and 2 SDs of DORM-2 were 0.11 0.07
for d202Hg, 0.91 0.05 for D201Hg, and 1.00 0.06 for D199Hg
(n 8), which were in the range of previous results (Bergquist and
Blum, 2007; Blum and Bergquist, 2007). Meanwhile, duplicate di-
gests for each sample were analyzed. The larger value of the mea-
surement uncertainties of either the duplicate samples or the UM-
Alma den were adopted as the data uncertainties in this study.
3. Results
3.1. Mercury concentrations in the ecosystem
Mercury concentrations were generally low in marine-caged
sh and all the sampled species had THg concentrations (ww,
Table 1) lower than the USEPA's human health screening value
(300 ng/g, ww) (USEPA, 2001). The sampled species can be divided
into three groups based their trophic positions and diets during the
cage culture: (1) the herbivores (rabbitsh) and omnivores
(sardine, turbot, and croakers) feeding on algae, plankton, in-
vertebrates, molluscs, or crustaceans in nature; (2) the carnivores
(seatrout, eel, and seabreams) feeding on invertebrates, shrimp,
crustaceans, or small shes in nature; (3) the piscivores (seabass
and groupers) that are predators and mostly feed on other shes in
nature. Mercury accumulation in the sh, especially the MHg
accumulation, were closely related to the feeds. As shown in Fig. 2,
Hg (THg and MHg) concentrations and %MHg generally increased in
the sequence of herbivores, omnivores, and carnivores. For
instance, the mean %MHg was <50% in the rabbitsh, sardine, and
turbot, 60%e80% in the spotted seatrout, blackhead seabream,
Japanese eel, large yellow croaker, and yellown seabream, and
>80% in the Japanese seabass, orange spotted grouper, and eightbar
grouper (Fig. 2). Relatively high Hg levels were observed in grou-
pers, especially the eightbar grouper whose THg and MHg con-
centrations (ww) were statistically the highest among all studied
species.
Total Hg concentrations in the sediment were 64 ng/g
(SD 13 ng/g) for the Dongshan Island and 64 ng/g (SD 4.3 ng/g,
n 3) for the Luoyuan Bay. They both presented extremely low
MHg concentrations with %MHg lower than 3% (Fig. 2, Table 1).
Mercury concentrations (THg and MHg) in the commercial food
pellets (feed-1 and -2) were much lower than that in the self-made
feeds (feed-3 and -4, Fig. 2 and Table 1). The %MHg were 7.9
(SD 6.0, n 3) and 8.4 (SD 3.6, n 3) in feed-1 and -2, and 37.9
(SD 5.8, n 3) and 32 (SD 0.37, n 3) in feed-3 and -4.
3.2. Dietary methylmercury exposure
Estimated dietary intakes of MHg associated with marine-caged
sh in Dongshan Island and Luoyuan Bay are presented in Table 2.
The mean MHg exposure (DIR) of males were generally higher than
that of females. The daily intake rates (DIR) were higher than the
EPA's RfD with consumption of red seabream, Japanese seabass,
orange spotted grouper, or eightbar grouper. Extremely low con-
sumption rates and meal frequency of orange spotted grouper and

Table 1
Mercury concentrations and stable mercury isotope compositions for sh muscle, surface sediment and sh feeds.

Sample name Site N Total Hg Total Hg Methyl-Hg %Methyl-Hg d202Hg () D199Hg () D201Hg () Total Body

(Latin name) (ng/g, wet) (ng/g, dry) (ng/g, dry) length (cm) weight (g)

Rabbitsh D 5 13 1.7 59 8.7 16 2.3 28 1.7
0.46 0.07 0.82 0.04 0.68 0.11 14 2.0 37 19
(Siganus fuscescens)
Sardine D 4 20 11 92 48 25 11 29 3.3
0.74 0.05 0.74 0.21 0.64 0.27 13 0.30 31 2.3
(Sardinella jussiu)
Turbot D 5 41 9.4 183 42 74 31 39 8.1
0.46 0.32 0.18 21 0.35 99 40
(Paralichthys olivaceus)
Spotted seatrout D 6 34 11 152 47 99 23 66 5.7
0.46 0.15 0.46 0.06 0.30 0.10 19 1.8 89 16
(Cynoscion nebulosus)
Blackhead seabream D 5 48 25 215 112 151 88 68 11 0.29 0.24 1.56 0.52 1.31 0.48 15 1.9 68 25
(Acanthopagrus schlegelii)
Japanese eel D 5 47 20 211 91 143 70 66 10
0.51 0.17 0.65 0.27 0.59 0.17 41 6.1 47 19
(Anguilla japonica)
Large yellow croaker D 5 48 9.3 216 42 136 39 62 6.2 0.05 0.14 1.13 0.03 0.95 0.004 24 2.7 144 55
(Larimichthys crocea)
Yellown seabream D 5 72 47 323 213 261 186 77 8.3
0.29 0.18 0.50 0.08 0.40 0.10 140.45 50 11
(Acanthopagrus latus)
Red seabream D 5 79 35 305 117 280 111 92 1.2 0.46 0.06 1.02 0.04 0.80 0.02 30 2.3 697 206
(Pagrus major)
Red seabream L 5 93 38 356 138 301 106 85 3.1 0.26 0.01 1.13 0.03 0.99 0.08 34 0.71 650 87
(Pagrus major)
Small yellow croaker L 8 23 11 102 47 40 20 40 14
0.15 0.15 1.07 0.03 0.88 0.05 14 1.2 36 13
(Larimichthys polyactis)
Japanese seabass L 5 115 62 517 278 474 264 91 1.9 0.17 0.03 1.14 0.10 0.92 0.06 43 12 883 589
(Lateolabrax japonicus)
Orange spotted grouper L 5 162 23 678 76 602 117 88 7.4 0.51 1.13 1.05 21 3.2 195 65
(Epinephelus coioides)
Eightbar grouper L 5 235 24 949 179 836 83 89 8.0 0.40 0.02 1.06 0.03 0.94 0.06 24 0.71 178 3.5
(Epinephelus octofasciatus)
Feed-1 D 3 18 0.96 1.4 1.0 7.9 5.9
0.63 0.21 0.62 0.09 0.45 0.14
Feed-2 L 3 37 5.4 3.2 1.8 8.4 3.6
0.42 0.26 0.60 0.08 0.52 0.09
Feed-3 D 3 182 13 68 5.7 38 5.8 0.11 0.13 1.25 0.23 0.98 0.13
Feed-4 L 3 243 34 78 10 32 0.37 0.06 0.05 1.56 0.03 1.28 0.01
Sedimeng-D D 2 64 13 0.68 0.05 1.1 0.14
1.34 0.15
0.04 0.003
0.04 0.001
Sedimeng-L L 2 60 4.3 1.6 0.38 2.7 0.43
1.38 0.04
0.01 0.01
0.01 0.01

Note: D indicates Dongshan Island Fish Farm; L indicates Luoyuan Bay Fish Farm.
1142 X. Xu, W.-X. Wang / Environmental Pollution 220 (2017) 1138e1146

Fig. 2. Total mercury, methylmercury, and %methylmercury in sh muscle, sh feeds, and surface sediments. Sample names on the X-axis are abbreviated: S. seatrout spotted
seatrout; J. eel Japanese eel; Ly. croaker/Sy. croaker large/small yellow croaker; B. seabream blackhead seabream; Y. seabream yellown seabream; R. seabream red
seabream; J. seabass Japanese seabass; Os. grouper orange spotted grouper; E. grouper eightbar grouper; Sediment-D/Sediment-L sediment from Dongshan Island/Luoyuan
Bay.

eightbar grouper were suggested, which were as low as 19 g/meal
(2.3 meals/month) and 28 g/meal (3.4 meals/month) for an adult
eating orange spotted grouper and eightbar grouper, respectively.
3.3. Stable mercury isotope ratios
Mercury isotopic compositions (d202Hg and D199Hg) of muscle
samples, sediments, and sh feeds are presented in Fig. 3. The
d202Hg values in the surface sediment were relatively low (
1.45
to
1.23) and the D199Hg values (
0.04e0.01) were almost
equal to zero. The isotope ratios (d202Hg and D199Hg) of commercial
food pellets (feed-1 and -2: dry pellets) were statistically lower
than that of the self-made feeds (feed-3 and -4: sh viscera). Fish
feeding on different feeds showed different isotopic signatures: the
non-carnivorous sh (sardine, rabbitsh, turbot, Japanese eel, yel-
lown seabream, and spotted seatrout) had d202Hg values ranging
from
0.77 to
0.19 and D199Hg values from 0.32 to 0.98,
which were higher than the carnivorous sh (small and large yel-
low croaker, Japanese seabass, Japanese seabream, orange spotted
grouper, and eightbar grouper) with d202Hg values ranging
from
0.33 to 0.51 and D199Hg values from 0.91 to 2.00.
The non-carnivorous sh presented D199Hg values close to the
commercial food pellets, and the carnivorous sh presented iden-
tical D199Hg values that were between the food pellets and sh
viscera. Blackhead seabream showed the highest D199Hg signa-
tures, making its isotope ratios distinct from both the non-
carnivorous and carnivorous species. The d202Hg values in the
muscle increased with both log-MHg concentrations (r2 0.56,
p < 0.01) and %MHg (r2 0.59, p < 0.01), but the D199Hg values did
not correlate with either MHg concentrations or %MHg.
3.4. Stable isotope mixing models
Previous studies have indicated the abiotic photochemical
reduction is the only proved process causing MIF of stable Hg iso-
topes (Bergquist and Blum, 2007). The observed MIF signatures of
Hg in the biota were closely related to their MHg sources and
explained with bioaccumulation of MHg through trophic web and
different isotopic ratios between inorganic and organic Hg species
(Kwon et al., 2012, 2014; Xu and Wang, 2015). Since dietary intake
is the only Hg source for farmed sh (Onsanit et al., 2012), the Hg
isotopic compositions were much likely the pure reection of their

Table 2
Estimated daily intake rates (DIR) of methylmercury through consumption of marine-caged sh, and the recommended maximum consumption rates (mCR) and meal fre-
quency (MF).

Normal name DIR (ug/kg-day) mCR MF

Male Female (g/day) (# meals/month)

Rabbitsh 0.01 0.01 1092 132

Sardine 0.01 0.01 685 83
Small yellow croaker 0.01 0.01 434 52
Turbot 0.03 0.02 250 30
Spotted seatrout 0.04 0.03 180 22
Large yellow croaker 0.05 0.04 134 16
Japanese eel 0.05 0.04 130 16
Blackhead seabream 0.05 0.04 123 15
Yellown seabream 0.09 0.08 72 8.7
Red seabream 0.12E 0.10E 53 6.4
Japanese seabass 0.17E 0.14E 38 4.6
Orange spotted grouper 0.23E 0.20E 28 3.4
Eightbar grouper 0.33E 0.29E 19 2.3
E
Note: represents the DIRs that exceeded the USEPA's reference does of 0.1 mg/kg-day.
 X. Xu, W.-X. Wang / Environmental Pollution 220 (2017) 1138e1146
Fig. 3. Stable mercury isotopic compositions (d202Hg and D199Hg) in sh muscles,
surface sediments, and sh feeds. Circles and error bars on individual data point reect
means and 1 SD of eld sampling replicates. Representative 2 SD of analytical uncer-
tainty during mercury isotope analysis is shown. Fish names in the gure are abbre-
viated: S. seatrout spotted seatrout; J. eel Japanese eel; Ly. croaker/Sy.
croaker large/small yellow croaker; B. seabream blackhead seabream; Y.
seabream yellown seabream; J. seabream Japanese seabream; J.
seabass Japanese seabream; Os. grouper orange spotted grouper; E.
grouper eightbar grouper.
feeds (Fig. 3). Therefore, we established a two-end isotope mixing
model to explain the variations of Hg MIF in the studied sh.
Commercial food pellets and fresh sh viscera were dened as two
dietary sources. We calculated the fraction of pellet Hg in the
muscle using the following equation:


D199 Hgfish f p D199 Hgp 1
f p D199 Hgv
D199 Hgfish
D199 Hgv
fp *100
D199 Hgp
D199 Hgv
where D199Hgsh is the D199Hg values of sh muscle. The D199Hgp
and D199Hgv are the mean D199Hg values of the pellets and viscera,
respectively. The fp (%) is the fraction of pellet Hg source as shown
in Fig. 4. Six out of nine species sampled from Dongshan Island had
fp higher than 50%, but all species sampled from Luoyuan Bay had fp
lower than 50%. In other words, herbivores and omnivores such as
rabbitsh, sardine, turbot, and Japanese eel presented fp higher
than 50%, and carnivores such as red seabream, Japanese seabass,
and groupers presented fp lower than 50%. Black seabream was an
exception with negative fp values, suggesting the existence of Hg
sources other than the pellets and viscera used in this mixing
model.
4. Discussion
After 1970s, the anthropogenic Hg rapidly increased to account
for the large portion of Hg deposition in China (Feng, 2005). The
accumulation of Hg in food webs and its toxicity to wildlife and
human beings create general concerns about human health and
safety of seafood consumption, especially in the estuarine and
coastal areas with developed aquaculture and high sh production
(Ginsberg and Toal, 2009; NBS, 2014; Oken et al., 2005). However,
despite the high concentrations of Hg in the environment, the
concentrations of Hg in the market-sold sh were generally low
(Cheng and Hu, 2012). This is because about 70% of sh production
in the current seafood market of China is dominated by farmed
1143
Fig. 4. Estimated fraction of pellet Hg in sh muscle collected from Dongshan Island
and Luoyuan Bay. Columns and error bars reect means and 1 SD of eld sampling
replicates.
freshwater sh that convert feeds into body tissue more efciently,
grow faster, and reproduce more frequently than the wild sh. Thus
they have lower potentials for Hg bioaccumulation and present low
Hg concentrations (Cheng and Hu, 2012). Meanwhile, wild caught
marine sh and marine-caged sh also accumulate relatively low
levels of Hg. Pan et al. (2014) reported THg concentrations of 571
wild caught sh from 54 species in the southern China which were
at least 10 times lower than the USEPA's human health screening
value (300 ng/g ww). Onsanit et al. (2012) selected four carnivorous
sh from marine-caged species in Fujian province and found out
(7) their THg concentrations ranged from 30 to 301 ng/g (ww). Our
results were consistent with the previous studies as THg concen-
trations of all fourteen species did not exceed the 300 ng/g (ww)
(8) criterion (Fig. 2). These studies revealed the fact that the commonly
consumed sh species, including the freshwater farmed, marine-
caged, and wild caught sh, all present low Hg levels. Though
more data are required to thoroughly investigate the Hg contami-
nations in the seafood market, the existing results support the
proposed paradox of Hg contamination in the seafood market of
China (Cheng and Hu, 2012).
Methylmercury is the major organic form that humans are
exposed to (USEPA, 2000). The primary risk of MHg is the toxic
effects on neurodevelopment and cardiovascular disease (Ginsberg
and Toal, 2009; Oken et al., 2005). We calculated the daily MHg
intake through the consumption of sampled sh, and found that
the exposures associated with red seabream, Japanese seabass,
orange spotted grouper and eightbar grouper exceeded the USEPA's
RfD of 0.1 mg/kg-day (USEPA, 2000). These are the very popular
farmed species in southern China, especially the groupers in Fujian
province, Guangdong province, and Hong Kong that are with high
commercial values (Chen, 2006). The marine cage culture of grou-
pers and seabreams in recent years has increased tremendously
and replaced their capture sheries due to the convenience of
purchase and the relatively lower price than the wild reef shes
(Kongkeo et al., 2010). Considering the rapidly expanded culture
industries of carnivorous sh, we also recommended their
maximum consumption rates and frequency which are as low as
19 g/day and 2.3 meals/month for an adult eating eightbar grouper
(Table 1). Therefore, people should be cautious that the dietary
MHg intake through eating farmed groupers, seabass, and seab-
ream may easily exceed the recommended health limits though
their THg concentrations are below the human health screening
1144 X. Xu, W.-X. Wang / Environmental Pollution 220 (2017) 1138e1146
value (Fig. 1) (Cheng and Hu, 2012; Onsanit et al., 2012; Pan et al.,
2014). In addition, it is always safer to eat non-carnivorous sh
like turbot and croakers instead of carnivorous sh like seabass and
groupers since MHg is accumulated through trophic intake.
Meanwhile, the detailed seafood consumption survey and con-
sumption advisories are urgently needed, especially for people
living in the estuarine and coastal region as well as pregnant
woman and breast feeding mothers.
Mercury isotopic compositions in the sediment presented
negative MDF signatures (Dongshan:
1.34; Luoyuan:
1.36)
and zero MIF signatures (Dongshan:
0.04; Luoyuan:
0.01.
Fig. 3 and Table 1). Liu et al. (2011) studied the Hg isotope ratios in
the estuarine sediment in southern China and demonstrated the
isotopic signatures from different sources: the industrial Hg coming
from mineral deposits that present a mean d202Hg value of
0.6
and D199Hg value of zero, the combusted Hg coming from fossil
fuels that present the d202Hg value of
2.43 and D199Hg value of
zero, and the continental background Hg with d202Hg value
of
2.16 and D199Hg value of
0.27 (Liu et al., 2011; Yin et al.,
2015). Among the three end members, Hg isotopic compositions in
our sediment stand between combusted Hg and industrial Hg but
slightly close to the industrial sources. Though microbial methyl-
ation and demethylation can cause MDF of Hg and modify the
d202Hg values in the substrates and reactants, these processes could
unlikely inuence the THg isotope signatures in the sediments
given their low %MHg (<3%, Fig. 2 and Table 1). Therefore, the major
portion of input Hg to the Dongshan Island and Luoyuan Bay was
from industrial activities, with a minor portion from coal com-
bustion. Nevertheless, THg concentrations (Dongshan: 64 ng/g;
Luoyuan: 63 ng/g, Table 1) in our sediment were similar to the
background levels of the marine sediment in southern China and
were even lower than some samples (Shi et al., 2010; Yin et al.,
2015; Yu et al., 2012). For instance, THg concentrations of the
Pearl River Delta, the largest estuary in the South China Sea, ranged
from 109 ng/g to 453 ng/g in the sediment (Yu et al., 2012). Previous
study displayed a decreasing pattern of Hg concentrations in the
sediment with increasing distance to the anthropogenic emissions
(Yu et al., 2012). Dongshan Island Fish Farm and Luoyuan Bay Fish
Farm were both built in the areas further from industrial facilities
compared to the Pearl River Estuary, thus they presented relatively
low levels of Hg contamination in the sediments.
Mercury accumulation and isotopic signatures are very different
between the cultured and wild sh. Two related studies analyzed
Hg concentrations and isotope ratios in the sh from Pearl River
Estuary in South China (Pan et al., 2014; Yin et al., 2016). They
focused on herbivorous, omnivorous, and carnivorous sh as we
did in this study, and their sampling area was adjacent to Fujian
Province in the South China Sea. Therefore, we compared the Hg
data between their wild caught and our cultured sh in order to
study Hg transport in different ecological systems. Fig. 5 showed
MHg concentrations and stable Hg isotopic compositions for the
most popular carnivorous sh in this region: groupers. Though the
included groupers were different species, but they come from the
same family Epinephelus with similar ecologies as well as close
sampling ages (Table 1). The cultured groupers presented much
higher tissue Hg concentrations than the wild caught species
(Fig. 5), because they are always fed with sh viscera that have
higher Hg concentrations and trophic levels than the prey of wild
groupers (Fig. 4). Meanwhile, the high feeding rate of sh in the
farm industry may also explain their fast Hg accumulation (Cheng
and Hu, 2012). We also plotted Log-MHg concentrations versus
D199Hg values, and identied a strong positive correlation
(r2 0.99, p < 0.05, Fig. 5) between these two factors. Since the MIF
cannot occur during the metabolic process and are usually seen as
reections of MHg signatures in the food, we contribute the large
Fig. 5. Relationships of methylmercury concentrations and isotopic compositions
(d202Hg and D199Hg) in the muscle of cultured and wild caught groupers. Individual
data points reect means of the same sh species. Analytical uncertainties of the
cultured groupers were the same as Fig. 3, and of the wild caught groupers were
indicated in Yin et al. (2016).
differences of D199Hg values between the wild and cultured sh to
the different MHg sources in their diets (Bergquist and Blum, 2007;
Kwon et al., 2012; Xu and Wang, 2015). According to previous
studies, the biotic D199Hg values increased with trophic positions in
the food web, meaning that organisms occupying high trophic
levels usually present high D199Hg values (Xu et al., 2016). The
cultured groupers feeding on tuna and viscera of seabass, seab-
ream, and even groupers, will certainly have higher trophic levels
than the wild groupers, and thus present high MIF signatures
(Onsanit et al., 2012).
Unlike the wild sh that accumulate MHg through trophic
transfer, farmed sh ingest MHg directly from the feeds. Though
industrial and combusted Hg was released to the waters of the sh
farms, the primary source of MHg for cultured sh still come from
the feeds and their Hg isotopic signatures were dominated by the
diets. Fig. 3 demonstrated the close relationships between Hg iso-
topic compositions and the applied feeds: (1) the isotope ratios
were distinctly separated between non-carnivorous sh (sardine,
rabbitsh, turbot, Japanese eel, yellown seabream, and spotted
seatrout) and carnivorous sh (small and large yellow croaker,
Japanese seabass, Japanese seabream, orange spotted grouper, and
eightbar grouper) according to the isotopic signatures of their
feeds; (2) the carnivorous species had higher d202Hg and D199Hg
values than other species; (3) the D199Hg values in non-carnivorous
sh were close to that in the commercial food pellets (feed-1 and
-2), indicating their single food source; (4) carnivorous sh showed
identical D199Hg values that were between food pellets and sh
viscera (feed-3 and -4), indicating their combined food sources. The
mixing model in Fig. 4 also indicated that the major source of Hg
was dry food pellets for non-carnivorous sh and combined diets of
pellets and fresh viscera for carnivorous sh. Meanwhile, the
identical MIF signatures among sh at similar trophic level also
explained the absence of correlation between D199Hg values and
MHg contents in Fig. 4. No matter how much Hg was accumulated
by a sh, their MIF signatures were similar as long as they used the
same food. However, we identied one exception: blackhead
seabream had much higher D199Hg values than all the other species
and the sampled feeds, but with only medium high Hg concen-
trations and %MHg (Figs. 2 and 3). Because the MIF signatures in the
farmed sh are primarily determined by their diets, we attributed
this exception to a different feed that had dissimilar isotope ratios
 X. Xu, W.-X. Wang / Environmental Pollution 220 (2017) 1138e1146
than feed-1, -2, -3, and -4. It was reported the D199Hg values in the
oceanic sh were usually higher than that in the coastal sh, thus
the feeds used for these blackhead seabreams may be composed of
several oceanic species like tuna (Li et al., 2014). A relevant study
reported that tuna was sometimes used as sh feed for marine-
caged species in this region (Onsanit et al., 2012).
Marine-caged sh farms are unique ecosystems, sitting in
nearshore sites with minimal ushing and providing massive
nutrient inputs to the ecosystems (Onsanit et al., 2012). Fish den-
sities in the farms are much higher than the natural environment
and their feeding strategies are much simpler than the wild sh.
Though anthropogenic contaminations of Hg were not as serious as
other estuaries surrounded by great populations and industrial
activities in southern China (Yu et al., 2012), the large amount of Hg
eliminated by the cultured sh and the high concentrations of
organic matters that interact with metals can both improve Hg
methylation potentials and increase Hg exposures to the ecosystem
(Hammerschmidt and Fitzgerald, 2006). For instance, MHg in sh
feces and the uneaten viscera feeds will deposit to the sediment,
gradually accumulate and transfer upwards in the food webs. The
body burdens of Hg in the cultured sh may not exceed the human
health criterion considering the low Hg concentrations in the feeds,
but their feces and the viscera feeds will become continuous source
of MHg to organisms living in these estuaries, especially threat-
ening the wild sh occupying high trophic positions. Therefore, we
suggest using commercial dry feeds and organisms with low Hg
concentrations such as shrimp, as an alternative food. Avoid using
sh viscera as feeds will not only decrease Hg concentrations in the
food sh and thus decrease Hg exposures to human beings, but also
decrease nutrient loadings and remove a potential Hg source in
such marine-cage sh farms and adjacent areas.
Acknowledgement
We thank the anonymous reviewers for their comments on this
work. This study was supported by a grant from Basic Research
Program of Shenzhen Science, Technology and Innovation Com-
mission (SZSTI). We are indebted to Caihuan Ke, Qiaoguo Tan, Jian
Wang for their help on eld sampling. We thank Haiying Lin, Fei Pu,
Dongxing Yuan, and Weitao Zhou who provided assistance on the
use of MC-ICP-MS.
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