Contents

. . . .in Chinina . .. . . .. . . .as . .. . . .bivalve. . . .. . . .. . . .

4.6. Mercury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

Science of the Total Environment 421422 (2012) 316

Contents lists available at ScienceDirect

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l se5. Mercury in marine sh in China . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136. Conclusion and perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

1. Introduction anthropogenic pollutants. Toxic contaminants such as persistentCoastal and estuarine areas are among thfor human inhabitants, yet they are often the

Corresponding author. Tel.: +852 23587346; fax: +E-mail address: wwang@ust.hk (W.-X. Wang).

0048-9697/$ see front matter 2011 Elsevier B.V. Aldoi:10.1016/j.scitotenv.2011.03.013. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

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4.4. Lead . . . . . . . . . . . . . .4.5. Nickel and chromium . . . . . .1. Introduction . . . . . . . . . .2. Sources of marine metal pollution3. Metals in marine sediments in Ch

3.1. North China coastal areas3.2. East China coastal areas .3.3. Southeast China coastal are3.4. South China coastal areas

4. Accumulation of metals in marine4.1. Cadmium . . . . . . . .4.2. Zinc . . . . . . . . . .4.3. Copper . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3a . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11e most important placesultimate receptacles of

organic pollutanon coastal and eof enhanced huchemicals into ceterious effects opossible poisoniet al., 2004; Ip e

852 23581559.

l rights reserved.the alarm for more stringentTrace metal contamination in estuarine and coastal environments in China

Ke Pan, Wen-Xiong Wang Division of Life Science, The Hong Kong University of Science and Technology (HKUST), Clear Water Bay, Kowloon, Hong Kong

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

Article history:Received 22 November 2010Received in revised form 11 March 2011Accepted 12 March 2011Available online 5 April 2011

Keywords:Metal pollutionSedimentsBivalvesChinaFish

Rapid growthof the economy inChinahas beencoupledwith increasing environmental pollution. The coastal andestuarine ecosystems in China are now facing increasingmetal pollution pressures because of the elevatedmetaldischarges fromvarious sources. Industrial anddomestic sewagedischarges,mining, smelting, e-wastes recyclingare important sources contributing to coastal pollution in China. In this review, status of metal contaminationalong China's coasts is assessed by a comprehensive review of metal concentrations recorded in sediments andmarine organisms over the past ten years. Studies show thatmetal contamination in the coastal environments isclosely associatedwith accelerated economic growth in the past decades. Highmetal contents can be detected inthe sediments collected across the coasts in China. Alarmingly high metal concentrations are observed in thesediments, water and organisms collected from the heavily industrialized areas. Metal levels observed inmarinebivalves also consistently reect the elevatedmetal contamination. Elevated levels ofmetal contamination alongChina's coastal environment can increase the risk of metal exposure to humans by seafood consumption, raising

control of discharge of metals into environment. 2011 Elsevier B.V. All rights reserved.Review

j ourna l homepage: www.eal Environment

v ie r.com/ locate /sc i totenvts (POP) and metals have placed increasing pressuresstuarine ecosystems over the past decades becauseman activities in coastal areas. The input of toxicoastal areas from various sources can result in del-nwildlife habitats, degradation of the ecosystem, andng of humans (Morton and Blackmore, 2001; Fungt al., 2004).

4 K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316Metals are naturally occurring constituents in the environmentand vary in concentrations across geographic regions. Unlike organicpollutants which can be degraded to less harmful components bybiological or chemical processes, metals are considered as non-degradable pollutants. They can heavily accumulate in sediments, as asink, or be released from sediments, acting as a source back tooverlying water via natural or anthropogenic disturbance. The effectsof metal pollution on local environments and organisms can besubstantial and long lasting in spite of years of restoration efforts.More importantly, toxic metals can be taken up by marine organisms,entering the food chain and be potentially transferred to the uppertrophic levels, which can eventually lead to adverse effects on humansdue to the consumption of contaminated seafood (Bryan, 1979;Wang,2002). Ever since the mercury (Hg) and cadmium (Cd) poisoningtragedies of the 1950s and 1960s in Japan, there has been considerableconcern about metal contamination in aquatic environment. Nowa-days China is one of the coastal countries that face the threats of metalpollution. In 2009, the Ministry of Environmental Protections of Chinarecorded 12 serious cases of metal pollution in which a total of 4035people suffered from excessive blood lead level and 182 suffered fromexcessive cadmium levels, with numerous children among the victims(Wang, 2009). The frequent cases of metal contamination across thecountry have raised the alarm for the public and the authorities (Feng,2005; Wang, 2009).

China has been able to maintain an annual GDP growth of over 8%in the past few years (NBSC, 20012009). The rapid growth of theeconomy in China since 1979 under the reform policies has beenaccompanied by considerable environmental side effects. Rapidurbanization and industrialization are coupled with a burst ofproduction and usage of chemicals including metals. While contam-ination incidents of fresh water systems due to industrial emissionoccur frequently in China, the marine environment appears to be lessaffected by pollution due to the larger dilution capacity of coastalwaters. However, the coastal and estuarine ecosystems in China arenow facing increasing metal pollution stress because metals releasedalong with municipal and industrial wastes may enter the sea by rivertransportation, and ultimately accumulate in the coastal areas,introducing long-term accumulative effects. Statistical data from theChinese government indicates that 29,720 km2 of offshore areas ofChina are heavily polluted (NBO, 2009). China is one of the largestcoastal countries in the world. The coastal waters of China support aweb of interconnected coastal habitats: coral reefs, mangrove andseagrass ecosystems, all of which provide important habitats for themarine organisms living in the region (Morton and Blackmore, 2001).The levels of metal in the coastal environment of China deserve ourattention not only because of their potential ecological impacts butalso because of the concern for seafood safety. The domestic demandfor seafood in China has increased dramatically from an annualconsumption of 7 kg per person in 1985 to about 25 kg per person20 years later (Gao and Gao, 2005), reecting increasing potentialexposure to contaminants from seafood consumption in the popula-tion. At the same time, China is by far the most inuential seafood-exporting nation in the world, with a 47% increase in seafood exportvalue from 2002 to 2004 (Lindkvist et al., 2008). The amount ofshellsh exported to other countries was estimated to be 9.6 milliontons in 2002 (Wang and Zheng, 2004). There are major concernsabout the possible export of contaminated seafood from China.Overall, understanding the current extent of pollution is importantto China's seafood industry and to public health as well as to asustainable management of the coastal environment.

In this review, we aim to assess the metal contamination level incoastal and estuarine environments in China (Fig. 1). We rst give ageneral overview of the sources of metal pollution in the coastalenvironment, and then discuss the pollution levels in various areasalong the coasts of China. We largely select the data that were

published in both international and Chinese journals from the past10 years, and our discussion mainly focuses on the metal datarecorded in sediment and marine organisms. Sediment can be agood indicator of the anthropogenic input of metals because humanactivities are a primary cause of the variability inmetal concentrationsin sediments, although natural factors can have substantial effects onbaseline concentrations as well. Moreover, the measurement ofdissolved metals in seawater is much more difcult than that ofmetals in sediments and organisms, due to the low concentrations ofmetal in seawater, the inuence of seawater matrix effects, as well aspotential sampling and laboratory contamination. Expensive ultra-pure chemicals, clean techniques, and laborious pre-concentrationmeasures are essential for accurate measurement of dissolved metals.Bioaccumulation is often a good integrative measure of the metalexposures of organism in polluted ecosystems (Phillips and Rainbow,1993). Special attention is given to the metal concentrations recordedin bivalves in this review. Bivalves are considered as importantseafood species as well as good biomonitors for both metal andorganic contaminants (Cantillo, 1998; Fung et al., 2004; Kimbroughet al., 2008). We attempt to integrate the bivalve data collected fromdifferent locations along the coasts of China to provide baselineinformation on the current metal pollution status in coastal environ-ments. Efforts are also put into a summary of mercury accumulation inmarine sh.

2. Sources of marine metal pollution in China

Metals enter the sea via several major routes, most notablythrough river input, atmospheric deposition, and industrial wastedisposal (Kennish, 1997). Terrestrial runoff is one of the mostcommon routes for metals entering the coastal marine environment.Agricultural fertilizers, mining tailings, industrial and municipaldischarges are the main routes for metals to be released into riverswhich may eventually be carried into offshore areas. China is knownas the world's factory. A large number of manufacturing companiesare located in the Pearl River Delta and the Yangtze River Delta alongthe east coast of China. Heavy industrialization has led to the releaseof many pollutants into the local environment. In China, the amountof industrial sewage discharged into the aquatic environmentwas estimated to be 24 billion tons in 2008 (NBSC, 2009). Waterpollution is particularly serious in China. A report by the WorldBank showed that 54% of the seven main rivers in China actuallycontained water deemed unsafe for human use in the period of20012005, in spite of increasing urban wastewater treatmentcapacity (World Bank, 2007). In some cases, industrial sewagewater is directly discharged into coastal areas which can causeserious metal contamination. Over 130,000 t of industrial sewagewas released directly into the sea annually between 2004 and 2008in China (NBSC, 20052009). However, 88.4% of coastal sewageoutlets under monitoring actually failed to meet the requirementsfor pollutant discharge (NBO, 2008).

Estuarine and coastal areas are often regions of high populationdensity and intense human activity, when compared to innermainland China. The spatial distribution of cities in China is suchthat city density is far higher in eastern coastal areas than in westernChina (Yue et al., 2003). Cities in China spatially concentrate incoastal areas, especially the Yangtze River Delta, the Pearl RiverDelta, and the BeijingTianjinTangshan area. A large proportion ofindustries are concentrated in eastern coastal areas as well. Theeastern coastal region accounts for 14% of China's land area butactually supports 42% of the population and makes up 58% of theGDP (Fung et al., 2004). The annual municipal sewage discharge inChina has been increasing in the past few years, from 45 billion tonsin 2003 to 57 billion tons in 2008 (NBSC, 20042009), and thenumber is expected to increase continuously. The Yangtze River,the Pearl River, and the Minjiang River are the main rivers that

carry metals into coastal areas, all of which contributed over 78% of

5K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316the total discharge of metals in 2008. The large amount of sewagehas caused substantial effects on coastal environments, such asincreasing eutrophication and decreasing diversity. The averageannual input of metals by major rivers was approximately 30,000 tbetween 2002 and 2008 (NBSC, 20032008). The oceanic environ-ment quality reported by the government of the Guangdong Provinceindicated that about one-fth of the coastal waters had been pollutedby industrial and domestic sewage by 2007. In 2009, the area ofheavily polluted coastal waters had reached about 3800 km2 in theGuangdong Province, which constitutes an increase of 11.8% whencompared with that in 2008 (BOGP, 2009).

China is a country abundant in metallic mineral resources. Thecountry has become a major metal producer and consumer in theworld. Mining, which is an important source of metal contamination,has contributed to a signicant part of the GDP in China. Chinaproduces the largest amount of zinc (Zn) in the world, which was1.95 million tons in 2000 and will grow to 14.9 million tons in 2010(Liu and Ou, 2003; BMI, 2010). China is a major player in steel

Fig. 1. Map of coastaproduction, which grew considerably to 22.8% (220 Mt) of the world'soutput in 2003 compared to 12.3% in 1993 (Zhang and Wang, 2007).China also leads in the production of gold, copper (Cu), coal andaluminum. Behind the large annual production of metals are thenumerous mining and smelting industries. The efuent or weatheringprocesses of mining tailings, and smelting of metalliferous ores canlead to local and regional pollution of metals in soils and waters. Up to4400 mg kg1 of Hg was reported for mine wastes in the Wanshanmercury mine in the Guizhou province (Qiu et al., 2005). Recently, anextremely high arsenic (As) pollution level was reported at anabandoned tungsten mine in the coastal city of Shantou in southeastern China. Results showed that concentration of As in agricul-tural soils ranged from 3.5 to 935 mg kg1 with an average valueof 129 mg kg1. In the groundwater, As concentration reached325 mg L1, and the maximum As concentration in local food was1.09, 2.38 and0.60 mg kg1 for brown rice, vegetable andsh samples,respectively, suggesting that the local water resource and food havebeen severely contaminated with As (Liu et al., 2010).

l areas in China.

6 K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316Atmospheric deposition is another route through which metalsenter into the sea. For example, Zhang et al. (1997) estimated China'sannual emission of dusts to be 1 million tons, 50% of which issubjected to long-range transport to the Pacic Ocean and beyond.The East China Sea (ECS) is situated in the paths of the Asian duststorms. As a result, it is expected that the atmospheric deposition mayprovide a substantial amount of chemical constituents to the ECS. It issuggested that atmospheric inux of metals such as Cu is increasing inYangtz River and Pearl River estuaries (NBO, 2009). Lead (Pb) and Hgcan easily be transported for hundreds of miles by air from their placeof origin. For example, high concentrations of metals were found inaerosols in Hong Kong and Guangzhou. Besides local emissions, airmass from northern China is also closely associated with the airpollution in Hong Kong, reecting the long-range air transport ofmetal contaminants from northern inland areas to the South Chinacoast (Lee et al., 2007). China's fast-growing economy has led to anenormous demand for energy. The total energy consumption in Chinahas increased to 70% between 2000 and 2005 (World Bank, 2007).Combustion of fossil fuels has contributed to China's economic growthbut has also led to signicant Hg emission. A large quantity of coal,1531 Mt or 28% of the world's total coal consumption, was consumedin 2003 in China (Jiang et al., 2006). China's annual coal consumptionis also expected to double to 3037 Mt by 2020 (USUIA, 2005). Thetotal Hg emissions from all anthropogenic sources in China increasedat an average annual rate of 2.9% during the period of 19952003,reaching 696 (307)t in 2003 (Wu et al., 2006). Nonferrous metalssmelting and coal combustion are the two major Hg sources in China(Wu et al., 2006). Streets et al. (2005) estimated that approximately45% of the Hg comes from non-ferrous metals smelting, 38% from coalcombustion, and 17% from miscellaneous activities. Among thesmelting industries, zinc smelting contributes signicantly to thesource of atmospheric Hg emission in China (Zhang andWang, 2007).

The increasing global trade of waste electrical and electronicequipments (WEEE, or e-waste), both legal and illegal, has raisedmuch concern about their environmental pollution. Being one of thefastest growingmarkets for electrical and electronic equipment, Chinais a large generator of these types of waste but has poor recyclingtechnologies. About 5080% of the e-waste collected for recycling inindustrialized countries ends up in recycling centers in China, India,Pakistan, Vietnam and the Philippines (C.S.C. Wong et al., 2007; M.H.Wong et al., 2007). The toxic chemicals released during e-wasteprocessing activities can cause deleterious ecotoxicological effects forlocal environments (Qin et al., 2009). The process of recycling WEEEincludes burning printed circuit boards and cables, toner sweeping,plastic chipping and melting, all of which notoriously release varioushazardous substances including metals, polybrominated dipheny-lethers (PBDEs), polychlorinated dioxins and furans, as well aspolybrominated dioxins and furans (PCDD/Fs and PBDD/Fs) (C.S.C.Wong et al., 2007; M.H. Wong et al., 2007; Seplveda et al., 2010).These toxic chemicals enter the environment in the forms ofleachates, particles, y ashes, fumes, and wastewaters which are alleasily spread to other areas. Uncontrolled dumping of materialscontaining metals will also cause metal contamination. For example,the Nanyang river sediments in Guiyu, a city in the easternGuangdong province, were seriously contaminated with Cd(~10.3 mg/kg), Cu (~4540 mg kg1), nickel (Ni) (~543 mg kg1), Pb(~590 mg kg1), and Zn (~324 mg kg1) (C.S.C. Wong et al., 2007;M.H. Wong et al., 2007).

3. Metals in marine sediments in China

Upon discharge into the environment, metals can be partitionedinto different compartments including water, air, soils, sediment andorganisms. In the marine environment, sediment represents aconcentrated mass of metals in potentially reactive form that is

biologically available and toxic and dispersed widely if not contained(Luoma and Rainbow, 2008). The mobility, bioavailability and toxicityof metals in the sediments are closely related to their specic chemicalforms which are associated with the various components of thesediments (Tessier et al., 1979; Bryan and Langston, 1992; Campbelland Tessier, 1996; Wang et al., 2002). For example, metals bound tothe exchangeable phase in the sediment may be more easily desorbedwithin the animal gut, while metals bound to the reducible phasemayrepresent an inert fraction that has low bioavailability to the animals(Thomas and Bendell-Young, 1998; Wang et al., 2002). Metals areheterogeneously distributed in sediments and form various hot spotalong the coasts. We discuss metal contamination in sediments alongChina's coast geographically, from the north to the south, by splittingChina's coastal areas into four subsections North China, East China,Southeast China, South China (Fig. 1).

3.1. North China coastal areas

Water pollution is considered to be worse in northern China thanin the southern part. The Liao, Hai, Huai, and Songhua Rivers located innorthern China are affected bymetal contamination. The northeasternChina coastline has been extensively studied for metal concentrationsin recent years (World Bank, 2007). The health of Bohai Sea hasattracted a huge amount of attention in recent years due to the highinput of anthropogenic pollutants from adjacent terrestrial areas. TheBohai Sea is an economically and ecologically important region withan area of 77,000 km2. Surrounded by highly industrialized regionsand suffering from poor water exchange conditions, Bohai Bay isconsidered as one of the most contaminated coastal areas in China.The shery resource in Bohai Bay has declined dramatically in the pasttwenty years because of overexploitation, eutrophication, andcontamination.

The situation in Jinzhou Bay is a typical case of metal contamina-tion in China. Jinzhou Bay is one of the important bays in thenorthwest of Liaodong Bay at the northwestern bank of the Bohai Seain China. It is a semi-closed shallow area with an average depth of3.5 m and an approximate area of 120 km2. The coast of Jinzhou Bay isan industrial area where multiple industries are located. The adjacentareas have been seriously contaminated by the sewage efuent ofpetrochemical producers/companies, chlor-alkali facilities, and non-ferrous metal smelting industries. The concentrations and burialuxes of Zn, Pb, Cd, and Hg increased abruptly after the late 1970s (Xuet al., 2009). The most contaminated site on the coast is where theHuludao Zinc Plant is located, which is one of the largest zinc plants inAsia. Extremely high metal concentrations were found along the coastin the seawater and sediment. Zheng et al. (2008) reported that themaximum concentrations of Hg, Pb, Cd, Zn and Cu in the riversediments surrounding the plant were 133, 1551, 1463, 19,789 and1072 mg kg1, respectively. The concentrations of Cu, Pb, Zn, and Cdin the seawater collected from Jinzhou Bay ranged from 1.73.5, 0.41.2, 21.839.2, to 1.72.0 g L1, respectively (Wan et al., 2007). Up to100 g L1 of Zn was found in the seawater collected in 2006 andconcentrations of other metals also appeared alarmingly high. Theconcentration of Cd, Zn, Cu, Pb, Hg, As, Chromium (Cr), and Ni in thesediments also reached 488, 13,933, 1227, 1828, 41, 820, 72, and96 mg kg1, respectively (Table 1). A signicant part of Cd wasassociated with exchangeable fractions, and the bioavailability ofsediment-bound Cd increased with increasing contamination of thesediment, as a result of the increasing partitioning of Cd into the easilyexchangeable phase, and decreasing partitioning into the reduciblephase (Wang et al., 2002). Mercury contamination also appeared to bea big problem for this area. Wang et al. (2009) have shown thatconcentrations of total Hg (THg) in sediment and in water in JinzhouBay was 0.564 mg kg1 and 392700 ng L1, respectively, whichwere 13 orders of magnitude higher than the background concen-tration. The highest methylmercury (MeHg) concentration found in

1water was 3 ng L . The concentrations of THg and MeHg found in

Table 1Metal concentrations (mg kg1 dry wt) in sediments collected from coastal areas of China. Ranges are given as the minimum and maximum values reported in the references.Numbers within braces are the reported average values.

Coastal areas Collection site Cd Zn Cu Pb Hg As Cr Ni Reference

North China Liaodong Bay 09.7(1.2)

48322(105)

549(17)

6.7131(23.9)

n.d. n.d. n.d. n.d. Zhou et al. (2004)

Jinzhou Bay n.d. 8913,933(6419)

91227(417)

21.81828(753.2)

n.d. 20.4820(396.5)

44.072(60.6)

n.d. Zhang et al. (2008)

Jinzhou Bay 2.6488.2 18010,447 27619 29.81650 14.641.1 n.d. n.d. 36.495.8 Fan et al. (2006)Qingdao 0.020.2

(0.1)7109(58)

638(22)

1739(27.6)

0.010.15(0.05)

3.923.2(8.4)

1692(55.61)

n.d. H.J. Wang et al.(2007)

Bohai Bay 0.070.2(0.1)

74148(99)

2532(27)

15.219.4(17.3)

0.250.97(0.57)

5.57.5 (6.7) n.d. n.d. J.G. Wang et al.(2007)

Bohai Bay 0.040.8(0.2)

57309(102.5)

744(28)

5.997(21.2)

0.010.18(0.05)

n.d. n.d. n.d. Zhan et al. (2010)

Bohai Bay n.d. 48181(88)

1832(25)

16.627.4(22.1)

n.d. n.d. 7.849(25.4)

19.235.8(26.9)

Qin et al. (2006)

Bohai Bay 0.11.0 69393 1127 16.634.9 0.020.85 6.513.0 18191 Meng et al. (2008)Jiaozhou Bay 0.031.0

(0.15)10295(73)

10137(27)

20.063.0(30.9)

0.010.59(0.08)

4.513.6(8.4)

21.0130(65.5)

n.d. J.H. Wang et al.(2007)

Jiaozhou Bay 0.0727.6 29957 7.2603.7 20.3203 n.d. n.d. 29.8124 8.3126 Deng et al. (2010)Haihe Estuary 0.42.1

(0.7)n.d. 21246

(56)21.778.9(39.4)

n.d. n.d. 63.2155(100.7)

n.d. Liu et al.(2006a, 2006b)

Yellow Sea 0.1 70 18 16.3 0.02 6.9 n.d. n.d. He et al. (2009)Yellow RiverEstuary

0.110.2(0.1)

2138(31)

1522(19)

11.615.0(13.0)

0.030.05(0.04)

6.512.6(9.0)

n.d. 16.823.5(19.7)

Wu et al. (2007)

East China Yangtze RiverEstuary

0.020.3(0.06)

34105(69)

236(13)

9.744.3(22.2)

0.030.39(0.12)

n.d. 96.6167(146.2)

n.d. Zhao et al. (2008)

Yangtze RiverEstuary

0.060.3(0.2)

45125(78)

1247(28)

14.832.7(21.9)

0.020.1(0.04)

6.517.6(11.6)

10.5113(52.1)

n.d. An et al. (2010)

Lianyungang 0.040.3(0.1)

n.d. 1459(36)

3.042.5(14.8)

0.010.28(0.05)

4.311.4(8.4)

n.d. n.d. He et al. (2008)

Hangzhou Bay 0.048.4 n.d. 1158 2.0175 n.d. n.d. n.d. n.d. Che et al. (2003)East China Sea n.d. 18114

(60)442(6)

1049(27)

n.d. n.d. n.d. 8.449.0(26)

Fang et al. (2009)

Southeast China(Fujian)

Xiamen 0.11.0 65223(139)

1997(44)

44.959.8(54.0)

n.d. n.d. 36.7134(74.5)

24.864.8(37.4)

Zhang et al. (2007)

Xiamen 0.030.1(0.05)

91135(109)

1432 (20) 29.560.5(41.5)

0.040.10(0.06)

6.2513.2(8.5)

n.d. n.d. Ruan et al. (2002)

Luoyuan Bay 0.120.2(0.16)

95105(99)

1725(23)

28.232.2(30.1)

0.040.08(0.06)

9.013.7(11.6)

33.437.7(35.2)

n.d. Lin (2008)

Quanzhou Bay 0.151.0 71167 1953 42115 0.000.01 7.811.8 26.083.0 15.035.0 Gong et al. (2007)Fujian coastal areas 0.011.2

(0.08)4319(96)

264(22)

7.7144(37.1)

0.000.22(0.05)

2.415.1(9.1)

4.5279(57.4)

2.153.3(27.4)

Zhang (2008)

Southeast China(Guangdong)

Shantou 0.301.8(0.70)

85249(153)

2479(49)

35.664.9(50.3)

n.d. n.d. 36.174.2(53.5)

17.031.7(23.5)

Qiao and Huang(2009)

Pearl River Estuary 0.040.7(0.2)

64237(130)

1567(39)

30.9116(53.3)

0.010.40(0.20)

5.535.6(21.1)

53.7120(86.3)

n.d. Huang et al.(2006)

Pearl River Estuary 5.07.2(5.6)

108196(140)

64105(81)

89.2124(105.9)

0.200.53(0.33)

15.753.6(33.1)

93.2223(118.1)

n.d. Yang et al. (2009)

Pearl River Estuary 2.84.7 240346 15141 28.539.4 n.d. n.d. 40.2111 24.8122 Li et al. (2007)Shenzhen Bay 1.26.6

(4.6)356566(489)

8102(69)

12.063.0(38.0)

n.d. n.d. 40.0168(115.0)

9.0115(75.0)

Zuo et al. (2008)

Daya Bay 0.020.1(0.05)

95.6140(113)

15.728.2(20.8)

35.454.6(45.7)

n.d. n.d. n.d. 27.735.5(31.2)

Gao et al. (2010)

Dapeng Bay 0.2 86 5 9.4 0.03 n.d. 24 n.d. Huang et al.(2005)

Hong Kong 0.003.5(1.05)

56328(149)

1987(43)

17.190.7(52.6)

n.d. n.d. 10.541.6(22.4)

17.351.7(36.4)

Liang and Wong(2003)

Hong Kong 0.105.3(0.3)

17790(148)

14000(119)

9.0260(53.6)

0.108.00(0.19)

n.d. 5.0560(48.9)

5.0220(24.7)

Zhou et al. (2007)

Hailing Bay 0.10.4(0.27)

36136(93)

464(31)

16.856.1(36.6)

0.010.10(0.06)

n.d. n.d. n.d. Qiu and Zhu(2004)

Zhanjiang 0.40.5(0.46)

3899(55)

1440(21)

30.164.3(41.7)

n.d. 7.818.2(13.1)

61.879.2(72.2)

15.732.1(19.6)

Guo and Huang(2004)

South China Lianzhou Bay 0.23 67 14 28.4 0.11 n.d. 15.9 n.d. Xia et al. (2008)Yintan Bay 0.18 59 13 5.4 0.03 n.d. 3.4 n.d. Xia et al. (2008)Tieshan Bay 0.20 72 11 13.5 0.07 n.d. 11.1 n.d. Xia et al. (2008)Yingluo Bay 0.28 80 13 21.7 0.09 n.d. 5.81 n.d. Xia et al. (2008)Beihai n.d. 9 3 7 b0.04 b3 9 3 Vane et al. (2009)South China Sea 0.41.3

(0.7)3274(45)

419(9)

15.136.1(22.6)

n.d. n.d. 6.867.4(19.9)

7.826.1(19.9)

Gan et al. (2003)

Sanya Bay 0.060.2(0.1)

71411(145)

12110(36)

10.341.4(17.4)

n.d. n.d. 9.722.7(16.8)

n.d. Zhang et al. (2003)

Sanya Bay 0.040.1(0.06)

2581(50)

610(8)

4.611.9(8.0)

n.d. n.d. 6.914.9(12.9)

n.d. Zhang et al. (2003)

Yalong Bay 0.07 77 17 5.2 n.d. n.d. 19.1 n.d. Zhang et al. (2003)Haikou n.d. 74121 2553 1635 0.040.06 813 118437 51159 Vane et al. (2009)

n.d.: not determined.

7K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316

8 K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316freshwater hydrophytes were 5.2100 g kg1 and 0.1512 g kg1,respectively. Clearly, the ecosystem in Jinzhou Bay is seriouslydamaged by the metal contamination and few living organisms canbe found around the outfalls. The people around northwestern BohaiSea are at a high risk of metal poisoning (Zheng et al., 2007).

Jiaozhou Bay is another semi-closed bay in north China which isalso under the stress of metal contamination. More than 10 rivers arelocated around Jiaozhou Bay, all of which carry large amounts ofindustrial and household discharge into coastal areas. Sewage isconsidered as the largest source of metals in this area. It is estimatedthat about 23107 t of sewage enters Jiaozhou Bay each year, ofwhich 40% is from industrial factories (Zhang et al., 2006). A studyconducted by Deng et al. (2010) indicated that the northeast areas ofthe bay are more contaminated than the rest because of worseseawater exchange conditions. A heavy contamination of Zn, Ni, andCd was found in the Licun River Estuary and the Moshui River. Theconcentrations of Cu, Zn, Pb and Cd in the contaminated estuarinesediment were found to be up to 600 mg kg1, 950 mg kg1,195 mg kg1, and 27 mg kg1, indicating that large amounts ofmetals were transported by rivers.

3.2. East China coastal areas

The Yangtze River Estuary is the third largest river in the worldwith a mean annual water discharge of 29,400 m3/s and a sedimentload of 500 Mt/year (Zhang, 1995). The metal contents in thesuspended sediments from the Yangtze River were found to beseveral times higher than those found in rivers in other countries(Mller et al., 2008), implying that signicant quantities of metals aredischarging into the ECS via this river. Elevated concentrations of tracemetals were generally found in the Hangzhou Bay and along the innershelf of the ECS, and more than 80% of the sedimentation uxes oftrace metals are deposited in the inner shelf and the Yangtze Riverestuarine zone. Lin et al. (2000) reported that the mean concentrationof dissolved Pb (~128 ng L1) in the southern part of the East ChinaSea upper waters (b50 m) was approximately several times higherthan those in the Pacic Ocean, and spatial distributions of dissolvedPb in the surface water showed a pattern of increasing concentrationswith offshore distance, indicating that deposited aerosols from Chinacan signicantly affect surface dissolved Pb in the ECS. A recent studyby Daz-Somoano et al. (2009) suggested that coal is an important Pbsource in China, and the Pb isotope signature of the Chinese coalsoverlapped well with that of western U.S. aerosols, implying thatlong-range transport of aerosols from China to U.S. via the westerliesis possible. Fang et al. (2009) calculated that the annual sedimentationuxes of trace metals in the ECS were 3.48107, 9.07105, 1.08105,4.48104, 4.32104, 3.10104t per year for Fe, Mn, Zn, Ni, Pb, Cu,and Fe, respectively. Approximately 5570% and 1017% of thesedimentation uxes of trace metals were deposited in the inner shelfand the Changjiang estuarine zone. However, the percentage ofatmospheric ux of trace metals by aerosol dry deposition to theriverine annual uxes is rather small: around 2% for Cu and Zn, andless than 0.1% for Pb, Mn, Ni, and Fe.

3.3. Southeast China coastal areas

HongKong is another extreme case ofmetal contamination in China.Hong Kong is one of the busiest ports and transportation hubs in theworld. Uncontrolled disposal of industrially polluted wastes from themid-1950s to 1970s had resulted in the contamination ofmuch of HongKong's harbor seabed. There are over 2000 major and 200,000 minorindustries in the history of HongKong,many ofwhich aremetal-relatedindustries involved in can production, enamelware, batteries, basicindustrial chemicals, paints, lacquers, integrated circuit boards, electro-plating, ship building and boat yards (Blackmore, 1998). High

concentrations of metals in sediment are found near the industrialand coastal areas such as Tolo Harbour and Victoria Harbour, due to theenclosed nature of the areas and high loadings of metal input. Extremelevels of Cu (N 6 gkg1) and Cr (N1.3 gkg1) can be found in thesediment core collected from Typhoon Shelters (Tanner et al., 2000).Although many of the industries previously polluting Hong Kong haverelocated to the mainland today and more stringent control of thedischarge of pollutants has been realized, metal concentrations insediments in some areas of Hong Kong still remain high (EPD, 20012008).

Being the second largest river system in southern China and amajor waterway, the Pearl River Estuary (PRE) is known as one of themost industrialized and urbanized regions in China and acts as amajorsink for contaminants and nutrients in the surrounding ecosystem.Much effort has been expended to assess the health status of thisimportant estuary in the past 10 years (Li et al., 2001; Ip et al., 2005;Shi et al., 2010). Pollution in the PRE has resulted from thedevelopment of cities on the fringe of the Pearl River Delta. Studieshave demonstrated that the Pearl River Delta is the main source ofpersistent organic pollutants discharged into the adjacent coastalwaters, such as OCPs, PAHs, PCBs, and PBDEs as well as metals (S.S.Wang et al., 2008; X.N. Wang et al., 2008; Guan et al., 2009). Ip et al.(2004) found that there has been a signicant increase in inuxes ofCu, Pb and Zn in the PRE since the 1970s. Shi et al. (2010) used the210Pb dating technique to investigate the historical changes in theconcentrations and inuxes of Hg in the last 100 years and found thatthe concentrations of Hg in the sediments ranged from 1.5 to201 g kg1, and the Hg inuxes in sediment cores obviouslycorrelate with the economic development and urbanization in thisarea. The sediments in coastal wetlands of the PRE were signicantlycontaminated by Cd, Zn and Ni with concentration ranges of 2.84.7,239346 and 25122 mg kg1, respectively. Moreover, a majorportion (3547%) of Pb, Cd, and Zn was strongly associated withexchangeable fractions, indicating higher bioavailability and mobilityof these metals (Li et al., 2007). The sediments collected fromShenzhen Bay, which is located at the eastern part of the PRE, and themouth of Shenzhen River, contained a high concentration of Zn of upto 566 mg kg1. Gao et al. (2010) investigated surface sediments fromDaya Bay where a nuclear power station is located. Results showedthat the surface sediments have not yet been polluted by metals. Amore recent investigation on metal contamination along the south-east coast of China (Vane et al., 2009) has shown that mangrovesediments in the developed cities such as Shenzhen and Xiamen havebeen polluted by Zn (252 mg kg1 and 194 mg kg1, respectively).The total Hg concentrations in surcial sediments from mangrovewetlands along southeast China ranged from 2.3 to 903 g kg1 withan average value of 189 g kg1.

3.4. South China coastal areas

The number of investigations in metal contamination along thesouthern China coastal area is relatively low. A scant amount of datafrom the literature indicates that these areas were less affected bymetal pollution when compared to the economically developed areas.Metal concentrations in the sediment collected from Hainan, Guangxiand the southern Guangdong provinces generally contained lowerconcentrations of metals than those collected from other parts ofChina (Table 1), probably due to lower urbanization and industrial-ization in these places. The sediment from mangroves in the HainanProvince, however, showed high levels of Zn (up to 437 mg kg1) andHg (up to 903 g kg1) (Zhang et al., 2003; Ding et al., 2009).

4. Accumulation of metals in marine bivalves

Metals accumulated in sediments provide historical input recordsof metals for local environment, whereas metals accumulated in biota

indicate metal bioavailabilities. We purposely select metals

accumulated in bivalves to assess the status of metal contamination incoastal environments in China. Bivalve molluscs can accumulate highlevels of metals in their tissues in proportion to the degree of metalpollution. In the past two decades, mussels and oysters have beenemployed in theMusselWatch Program (MWP) in USA tomonitor thetrace metals, PCBs, PAHs, and radionuclides, to evaluate the levels ofcontamination and their spatial and temporal differences (Kimbroughet al., 2008). Today the International Mussel Watch Program (IMWP),as a counterpart of the MWP, has been successfully extended to othercountries including China (Monirith et al., 2003). Tables 27 show theCd, Zn, Cu, Pb, Ni, Cr and Hg concentrations recorded in bivalvescollected from the coasts of China in the past ten years. Unlessspecied, data are all expressed in dry weight (dry wt) units. Part ofthe data are calculated from wet weight (wet wt) data using a dryweight to wet weight conversion factor of 7, and assuming a watercontent of 85% in the soft tissues.

Bioaccumulation of a specic metal is not only dependent onmetalexposure and its bioavailability in the environment, but also thestrategies through which a specic organism deals with metals(Rainbow, 2002; Luoma and Rainbow, 2008). On the one hand,environmental factors such as metal concentration, speciation, foodquality and quantity can be critical in inuencing the metalaccumulation in organisms living in different environments; on theother hand, different organisms accumulate metals from the envi-ronment differently depending on their ltration rate, ingestion rate,gut uid quality, as well as the detoxication strategies they adopt(e.g. storage in non-toxic form or elimination) (Marigmez et al.,2002;Wang and Rainbow, 2008; Pan andWang, 2008b, 2009). Recentstudies have revealed that dietary pathway, which was neglected inprevious equilibrium approach studies, actually plays a signicantrole in metal uptake in aquatic organisms (Wang and Fisher, 1999a,1999b; Chong and Wang, 2001; Pan and Wang, 2009). Such ndings

quality standards in the future. Species-related concentration differ-ences are commonly seen for some metals. For example, oystersaccumulate more Cu and Zn than mussels, while mussels tend to havea higher Pb concentration than oysters (see below). Caution must betaken before any comparison is made between species. As such,interpretation of the bioaccumulation data should be based on thespecic characteristics of metal accumulation for each species.

4.1. Cadmium

Cd is a non-essential metal for organisms except for its newlydiscovered biological role in marine diatoms (Lane and Morel, 2000).It has been demonstrated as a highly toxic metal to wildlife andteratogenic and carcinogenic to humans (Ronald, 2000). A well-known example is the human poisoning incident in Japan in which Cdin wastewater irrigation led to the itaiitai disease. The concentrationof Cd in seawater can range from 0.110 ng L1 in open waters to 1060 ng L1 in coastal waters (Kennish, 1997). Cadmium is a deleteriouscontaminant in seafood and can be highly accumulated by marineorganisms. Scallops typically have higher Cd concentrations thanother bivalves due to the extremely high Cd assimilation efcienciesand low elimination rate in this species (Pan and Wang, 2008a). A Cdrange of 5.738.7 mg kg1 was found in scallops of different sizescollected from unpolluted waters in Shenzhen, Guangdong province(Pan and Wang, 2008a, 2008b). However, Cd is mainly concentratedin the digestive glands of scallops, and is low in muscles which are themain parts for human consumption. Mussels generally have lower Cdconcentrations and approximately 15 mg kg1 Cd are commonlyobserved in mussels collected from coastal regions worldwide(Kennish, 1997). There is a 10-fold difference between the lowestrecorded and the highest mean values of Cd concentrations in themussels collected from the coastal areas in China (Table 1). The

asta

tion

200

200

200

200

9K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316may have signicant impacts on the setting of regulatory water

Table 2Cd concentrations (mg kg1 dry weight) in marine bivalves collected from different co

Organism Species Location Collec

Oysters Crassostrea talienwhanensis Bohai Bay 2002Crassostrea rivularis Guangdong 2007

Crassostrea rivularis Shantou 2002Crassostrea gigas Guangdong 2007

Crassostrea gigas Shenzhen 2002Saccostrea cucullata Zhejiang 1998Saccostrea cucullata Xiamen 2005Saccostrea cucullata Hong Kong 2004

Clams Ruditapes philippinarum Bohai Bay 2002Ruditapes philippinarum Jiaozhou Bay 2004Ruditapes philippinarum Zhejiang 2002Ruditapes philippinarum Xiamen 2005Ruditapes philippinarum Xiapu 2001Ruditapes philippinarum Guangdong 2007

Mussels Perna viridis Minjiang Estuary 2001Perna viridis Jiulongjiang

Estuary2001

Perna viridis Guangdong 2007Perna viridis Shantou 2002Perna viridis Hong Kong 2003Perna viridis Hong Kong 2004Mytilus edulis Bohai Bay 2002Mytilus edulis Dalian 2001Mytilus edulis Qingdao 2001Mytilus edulis Shanghai 2001Mytilus edulis Zhoushan 2001Mytilus edulis Ningbo 2001

Scallops Chlamys nobilis Shenzhen 2006

a Converted from wet weight using a wet wt/dry wt ratio of 7.average Cd concentration in the Mussel Watch Program in USA

l areas of China.

period Average value and the range(mg kg1 dry wt)

Reference

11.6 (3.623.0)a Liang et al. (2004)10.2 (4.318.0)a (S.S. Wang et al., 2008;

X.N. Wang et al., 2008)3 10.0 (6.020.7) Sun et al. (2004)

2.0 (0.82.9)a (S.S. Wang et al., 2008;X.N. Wang et al., 2008)

3.2 (3.249.5)a Cheng et al. (2004)17.0 (8.934.0)a Fang et al. (2004)0.5 (2.75.0)a Ruan (2007)

5 0.9 (0.71.0) Cheung and Wang (2008)2.4 (1.04.4)a Liang et al. (2004)0.6 (0.40.7) Ma et al. (2009)3.3 (0.58.5)a Huang et al. (2007)1.4 (0.82.5)a Ruan (2007)0.7 (0.60.8)a Ruan et al. (2003)2.2 (0.65.0) X.N. Wang et al. (2008)0.5 (0.50.6) Fung et al. (2004)1.0 (0.81.1) Fung et al. (2004)

2.0 (0.42.7)a X.N. Wang et al. (2008)3 5.6 (1.68.3) Sun et al. (2004)

0.8 (0.31.5) Ng and Wang (2005)5 0.3 (0.01.5) Fang et al. (2008)

6.2 (2.413.7)a Liang et al. (2004)2.3 (2.02.7) Fung et al. (2004)1.2 (1.21.3) Fung et al. (2004)2.7 (2.72.8) Fung et al. (2004)5.0 (4.55.3) Fung et al. (2004)2.4 (2.42.4) Fung et al. (2004)

5.738.7 (10.3) Pan and Wang (2008a, 2008b)

(20042005) is 2.8 mg kg1 (Kimbrough et al., 2008). However, anaverage Cd concentration of 6 mg kg1 was found in Mytilus eduliscollected from the Bohai Sea by Liang et al. (2004), which is in linewith the well known fact that the Bohai Sea is the most contaminated

Minjiang Estuary and the Jiulongjiang Estuary, possibly due to ahigher contamination of Cd in the Yangtze River. High Cd concentra-tions (of up to 49 mg kg1) were also observed in the oysterscollected from the coasts of Bohai Bay, the Guangdong and the

Table 3Zn concentrations (mg kg1 dry weight) in marine bivalves collected from different coastal areas of China.

Organism Species Location Collection period Average value and the range(mg kg1 dry wt)

Reference

Oysters Crassostrea talienwhanensis Bohai Bay 2002 1337 (8122653)a Liang et al. (2004)Crassostrea rivularis Shantou 20022003 8260 (388417,618) Sun et al. (2004)Saccostrea cucullata Xiamen 2005 952 (6301145)a Ruan (2007)Saccostrea cucullata Hong Kong 20042005 1613 (11172108) Cheung and Wang (2008)

Clams Ruditapes philippinarum Zhejiang 2002 43 (2674)a Huang et al. (2007)Ruditapes philippinarum Xiamen 2005 108 (87125)a Ruan (2007)Ruditapes philippinarum Xiapu 2001 94 (71116)a Ruan et al. (2003)Ruditapes philippinarum Jiaozhou Bay 2004 70 (6687) Ma et al. (2009)Ruditapes philippinarum Bohai Bay 2002 100 (70141)a Liang et al. (2004)

Mussels Perna viridis Shantou 20022003 91 (94179) Sun et al. (2004)Perna viridis Hong Kong 20042005 65 (21109) Fang et al. (2008)Perna viridis Minjiang Estuary 2001 66 (63231) Fung et al. (2004)Perna viridis Jiulongjiang Estuary 2001 170 (147193) Fung et al. (2004)Mytilus edulis Bohai Bay 2002 108 (83157)a Liang et al. (2004)Mytilus edulis Dalian 2001 77 (6688) Fung et al. (2004)Mytilus edulis Qingdao 2001 105 (103108) Fung et al. (2004)Mytilus edulis Shanghai 2001 141 (121165) Fung et al. (2004)Mytilus edulis Zhoushan 2001 128 (109165) Fung et al. (2004)Mytilus edulis Ningbo 2001 86 (7496) Fung et al. (2004)

Scallops Chlamys nobilis Shenzhen 2006 188 (127579) Pan and Wang (2008a, 2008b)Argopecten irrandians Bohai Bay, Jiaozhou Bay 2005 452 (298646)a H. Wang et al. (2007)Chlamys farreri Bohai Bay, Jiaozhou Bay 2005 899 (5681468)a H. Wang et al. (2007)

a Converted from wet weight using a wet wt/dry wt ratio of 7.

asta

olle

10 K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316coastal areas in China. Fung et al. (2004) reported a mussel-basedmonitoring program which was carried out along the east coast ofChina using Perna viridis and M. edulis and found that the Cdconcentration was between 0.53 and 4.96 mg kg1, with the highestvalue found in Zhoushan. The Cd concentrations in mussels collectedfrom the area around the Yangtze River Estuary (Shanghai, Zhoushan,and Ningbo) were several times higher than those found in the

Table 4Cu concentrations (mg kg1 dry weight) in marine bivalves collected from different co

Organism Species Location COysters Crassostrea talienwhanensis Bohai Bay 2002Crassostrea rivularis Guangdong 2007Crassostrea rivularis Shantou 2002Crassostrea gigas Guangdong 2007Crassostrea gigas Shenzhen 2002Saccostrea cucullata Xiamen 2005Saccostrea cucullata Hong Kong 2004Saccostrea cucullata Hong Kong 2008

Clams Ruditapes philippinarum Jiaozhou Bay 2004Ruditapes philippinarum Zhejiang 2002Ruditapes philippinarum Xiamen 2005Ruditapes philippinarum Guangdong 2007Ruditapes philippinarum Xiapu 2001Ruditapes philippinarum Bohai Bay 2002

Mussels Perna viridis Guangdong 2007Perna viridis Shantou 2002Perna viridis Minjiang Estuary 2001Perna viridis Jiulongjiang Estuary 2001Perna viridis Hong Kong 2004Mytilus edulis Bohai Bay 2002Mytilus edulis Dalian 2001Mytilus edulis Qingdao 2001Mytilus edulis Shanghai 2001Mytilus edulis Zhoushan 2001Mytilus edulis Ningbo 2001

Scallops Chlamys nobilis Shenzhen 2006Argopecten irrandians Bohai Bay, Jiaozhou Bay 2005Chlamys farreri Bohai Bay, Jiaozhou Bay 2005

a Converted from wet weight using a wet wt/dry wt ratio of 7.Zhejiang province. Generally, the Cd levels in clams are between 0.4and 8.5 mg kg1 in these areas.

Food is recognized as the major source of Cd intake in humans. Theseafood safety limits for cadmium in bivalves in China, Hong Kong andUSA are 1, 2, and 3.7 mg kg1 wet wt, respectively. The recommendedupper limit for Cd intake is 75 g day1 or put another way, a Cdconcentration of 100 g kg1 in food should not be exceeded,

l areas of China.

ction period Average value and the range Reference

(mg kg1 dry wt)

356 (219767)a Liang et al. (2004)668 (1411554)a X.N. Wang et al. (2008)

2003 1383 (4673006) Sun et al. (2004)34 (1854)a X.N. Wang et al. (2008)

1701 (1123836)a Cheng et al. (2004)268 (146422)a Ruan (2007)

2005 225 (293257) Cheung and Wong, (2008)719 (2051674) Pan and Wang (2009)

8 (89) Ma et al. (2009)11 (1114)a Huang et al. (2007)10 (716) Ruan (2007)8 (610)a X.N. Wang et al. (2008)

15 (1022)a Ruan et al. (2003)15 (931)a Liang et al. (2004)10 (813)a X.N. Wang et al. (2008)

-2003 19 (1525) Sun et al. (2004)7 (68) Fung et al. (2004)9 (611) Fung et al. (2004)

2005 14 (068) Fang et al. (2008)12 (818)a Liang et al. (2004)2 (12) Fung et al. (2004)

22 (454) Fung et al. (2004)11 (322) Fung et al. (2004)23 (1329) Fung et al. (2004)5 (45) Fung et al. (2004)

13 (1015) Pan and Wang (2009)20 (1031)a H. Wang et al. (2007)44 (1672)a H. Wang et al. (2007)

Table 5Pb concentrations (mg kg1 dry weight) in marine bivalves collected from different coastal areas of China.

Organism Species Location Collection period Average value and the range(mg kg1 dry wt)

Reference

Oysters Crassostrea talienwhanensis Bohai Bay 2002 2.5 (1.54.3)a Liang et al. (2004)Crassostrea gigas Guangdong 2007 1.5 (0.82.3)a X.N. Wang et al. (2008)Crassostrea gigas Shenzhen 2002 8.4 (4.914.7)a Cheng et al. (2004)Crassostrea rivularis Guangdong 2007 1.5 (1.11.8)a X.N. Wang et al. (2008)Crassostrea rivularis Shantou 20022003 2.5 (1.53.8) Sun et al. (2004)Saccostrea cucullata Xiamen 2005 2.0 (1.42.6)a Ruan (2007)

Clams Ruditapes philippinarum Jiaozhou Bay 2004 1.0 (0.51.4) Ma et al. (2009)Ruditapes philippinarum Xiamen 2005 1.3 (0.62.0)a Ruan (2007)Ruditapes philippinarum Zhejiang 2002 0.3 (0.20.4)a Huang et al. (2007)Ruditapes philippinarum Guangdong 2007 0.2 (0.82.7)a X.N. Wang et al. (2008)Ruditapes philippinarum Hong Kong 20042005 1.7 (0.411.1) Fang et al. (2008)Ruditapes philippinarum Xiamen 2001 0.4 (0.30.6)a Ruan et al. (2003)Ruditapes philippinarum Bohai Bay 2002 1.7 (0.92.4)a Liang et al. (2004)

Mussels Perna viridis Guangdong 2007 2.3 (1.52.9)a X.N. Wang et al. (2008)Perna viridis Shantou 20022003 6.5 (4.89.2) Sun et al. (2004)Perna viridis Minjiang Estuary 2001 1.4 (1.21.7) Fung et al. (2004)

202020202020202020

11K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316assuming a daily food intake of 0.75 kg for an adult (Ahmed, 1991). Aconcentration of 2 mg kg1 wet wt of Cd was found in the shrimpMetapenaeus ensis collected from the Pearl River Estuary (Ip et al.,2005). Fang et al. (2004) reported that Cd concentration in the oysterSaccostrea cucullata collected from the coasts of Zhejiang Provincewasup to 34 mg kg1. High levels of Cd can also be observed in the oysterscollected from Bohai Bay and the Guangdong province where up to10 mg kg1 is common in oysters. Fang et al. (2003) reported veryhigh concentrations of Cd (4650 mg kg1) in oysters collected from

Perna viridis Jiulongjiang EstuaryMytilus edulis Bohai BayMytilus edulis DalianMytilus edulis QingdaoMytilus edulis ShanghaiMytilus edulis ZhoushanMytilus edulis Ningbo

Scallops Argopecten irrandians Bohai Bay, Jiaozhou BayChlamys farreri Bohai Bay, Jiaozhou Bay

a Converted from wet weight using a wet wt/dry wt ratio of 7.the PRE. These values have far exceeded the guideline limits set forseafood in different regions. Caution must be taken when consumingseafood from these regions because one contaminated oyster mayalready contain more Cd than is acceptable for daily intake.

4.2. Zinc

Zinc is present in all organisms and is an essential trace element formetabolic processes. Zinc canbehighly regulated inorganismsbut somemarine invertebrates tend to accumulate Zn to very high body

Table 6Ni concentrations (mg kg1 dry weight) in marine bivalves collected from different coasta

Organism Species Location

Oysters Crassostrea talienwhanensis Bohai BayCrassostrea rivularis ShantouCrassostrea gigas Shenzhen

Clams Ruditapes philippinarum Bohai BayMussels Perna viridis Shantou

Perna viridis Minjiang EstuaryPerna viridis Jiulongjiang EstuaryMytilus edulis DalianMytilus edulis QingdaoMytilus edulis ShanghaiMytilus edulis ZhoushanMytilus edulis NingboMytilus edulis Bohai Bay

a Converted from wet weight using a wet wt/dry wt ratio of 7.concentration. For example, barnacles usually accumulate zinc withno signicant excretion and themass of zinc can represent a signicantpart of their bodyweights (Rainbow andWang, 2005). Marine bivalveshave contrasting abilities to assimilate Zn from diets. Green mussels P.viridis assimilate 2136% of the Zn from ve species of marinephytoplanktons, whereas the assimilation efciency for clams is 2959% and that for oysters Crassostrea rivularis is 4180% (Wang andFisher, 1999a, 1999b; Chong andWang, 2000; Ke andWang, 2001). Thelevel of Zn varies between 26 and 141 mg kg1 for clams Ruditapes

01 2.4 (1.72.9) Fung et al. (2004)02 2.0 (1.11.8)a Liang et al. (2004)01 0.5 (0.50.6) Fung et al. (2004)01 0.9 (0.71.0) Fung et al. (2004)01 0.7 (0.70.8) Fung et al. (2004)01 0.7 (0.40.8) Fung et al. (2004)01 0.9 (0.81.0) Fung et al. (2004)05 0.7 (0.41.2)a H. Wang et al. (2007)05 1.3 (0.81.8)a H. Wang et al. (2007)philippinarum and those for green mussels P. viridis are between 21 and230 mg kg1, with the maximum concentration recorded in theMinjiang Estuary (Table 3). Green mussels P. viridis generally containless than 100 mg kg1 of Zn in their tissues (Blackmore, 1998).However, high concentrations of Zn (100230 mg kg1) are found ingreenmussels P. viridis collected at different locations from north Chinato south China, indicating that Zn pollution is common across thecountry. Mussels M. edulis have comparable Zn concentrations (66165 mg kg1) to P. viridis. Oyster is a typical species that can accumulatea large amount of Zn which was found to be stored either as phosphate

l areas of China.

Collection period Average value and therange in brackets inmg kg1 dry wt

Reference

2002 1.8 (0.83.0)a Liang et al. (2004)20022003 3.8 (1.09.6) Sun et al. (2004)2002 6.7 (2.79.1)a Cheng et al. (2004)2002 10.2 (5.020.7)a Liang et al. (2004)20022003 33.9 (23.350.1) Sun et al. (2004)2001 3.3 (3.03.6) Fung et al. (2004)2001 4.5 (4.16.0) Fung et al. (2004)2001 1.5 (1.31.8) Fung et al. (2004)2001 3.3 (3.23.4) Fung et al. (2004)2001 3.1 (2.93.2) Fung et al. (2004)2001 2.4 (2.53.0) Fung et al. (2004)2001 3.1 (2.03.6) Fung et al. (2004)2002 1.5 (1.31.8)a Liang et al. (2004)

Table 7Cr concentrations (mg kg1 dry weight) in marine bivalves collected from different coastal areas of China.

Organism Species Location Collection period Average value and the range(mg kg1 dry wt)

Reference

Oysters Crassostrea rivularis Guangdong 2007 1.3 (0.32.5)a X.N. Wang et al. (2008)Crassostrea rivularis Shantou 20022003 5.5 (1.611.7) Sun et al. (2004)Crassostrea gigas Guangdong 2007 0.9 (0.35.9)a X.N. Wang et al. (2008)Crassostrea gigas Shenzhen 2002 2.8 (1.84.4)a Cheng et al. (2004)

Clams Ruditapes philippinarum Guangdong 2007 2.9 (0.214.5)a X.N. Wang et al. (2008)Ruditapes philippinarum Jiaozhou Bay 2004 2.4 (1.04.0) Ma et al. (2009)

Mussels Perna viridis Guangdong 2007 1.8 (0.82.6)a X.N. Wang et al. (2008)Perna viridis Shantou 20022003 6.3 (4.88.0) Sun et al. (2004)Perna viridis Hong Kong 20042005 1.0 (0.32.2) Fang et al. (2008)Perna viridis Minjiang Estuary 2001 4.5 (4.24.8) Fung et al. (2004)Perna viridis Jiulongjiang Estuary 2001 5.4 (4.56.0) Fung et al. (2004)Mytilus edulis Dalian 2001 2.2 (1.52.7) Fung et al. (2004)

01010101

12 K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316granules or bound to highmolecularweight protein (Webb et al., 1985).Zinc concentrations in oysters are usually 10 times higher than thosefound inmussels and clams. Ahigh level of zinc (~2000mg kg1) canbedetected in rock oysters S. cucullata collected even from unpollutedwaters in Hong Kong (Cheung and Wang, 2008). An indicativeconcentration of contamination of 4000 mg kg1 was proposed byCantillo (1998). In contaminated sites, for example, the RestronguetCreek in England which is a heavily contaminated area by miningactivities, the mean concentration of zinc in oysters can be more than10,000 mg kg1 (Kennish, 1997). A similar value (17,000 mg kg1) canalsobeobserved in the oysters collected fromametal contaminatedportshelter in Shantou, Guangdong province (Table 3). Scallops can alsoaccumulate a high level of Zn due to their high assimilation abilities forZn (Pan and Wang, 2008a), but they generally have lower Zn contentsthan oysters because of their faster elimination rates. The levels of Zn inthe scallops Chlamys nobilis and Argopecten irrandians are comparable,and ranged from 127 to 646 mg kg1. Higher concentrations werefound in the scallops Chlamys farreri, with 1468 mg kg1 being thehighest value. Such a high concentration was probably caused by Znpollution in the local environment. Zinc in food is generally not harmfulto humans except if taken in high doses and there is no recommendedsafety level for zinc in seafood products by United States FDA.

4.3. Copper

Mytilus edulis Qingdao 20Mytilus edulis Shanghai 20Mytilus edulis Zhoushan 20Mytilus edulis Ningbo 20

a Converted from wet weight using a wet wt/dry wt ratio of 7.Copper is present in all aquatic environments. It is an essentialelement for all living organisms, but can be toxic when taken in highdoses. Copper is a common ingredient in antibiofouling paints which areapplied on the surfaces ships and in offshore engineering. Thebioaccumulation of Cu in marine bivalves has been well known eversince the discovery of green-sick oysters 120 years ago (Lankester,

Table 8Total Hg concentrations (mg kg1 dry weight) in marine bivalves collected from different

Organism Species Location C

Oysters Crassostrea talienwhanensis Bohai Bay 2Crassostrea gigas Shenzhen 2Oystrea sp. Fuzhou 2Oystrea sp. Xiapu 2

Clams Ruditapes philippinarum Xiapu 2Ruditapes philippinarum Bohai Bay 2

Mussels Mytilus edulis Bohai Bay 2Scallops Argopecten irrandians Bohai Bay, Jiaozhou Bay 2

Chlamys farreri Bohai Bay, Jiaozhou Bay 2

a Converted from wet weight using a wet wt/dry wt ratio of 7.1886). Contrasting intraspecic and interspecic difference of Cuaccumulation can be observed in bivalves. For examples, Cu concentra-tionswithin different individuals of oysters S. cucullata collected from thesame sampling site and period can vary by up to 8-folds (2051674 mg kg1) (Pan and Wang, 2009). However, oysters generallycontain higher concentrations of Cu than the other bivalve species. Arecent studyon theCubiokinetics of bivalves, including scallops C. nobilis,clams R. philippinarum, green mussels P. viridis, black mussels Septifervirgatus, and oysters S. cucullata, has demonstrated that such differencesare largely dependent on their contrasting abilities to eliminate Cu (PanandWang, 2009). The elimination rates of Cu in scallops, clams andgreenmussels are several timeshigh than thoseof othermetals (PanandWang,2009). ClamsR. philippinarum collected fromcoasts of China contained630 mg kg1 Cu in their tissue (Table 4). Copper concentration in greenmussels P. viridis uctuated between undetectable and 67 mg kg1.Copper concentrations in the three common scallops in China range from10 to 72 mg kg1. There is generally no obvious pattern in terms ofconcentration in mussels and clams collected across the coastal areas,probably because Cu can be highly regulated by these organisms.

4.4. Lead

Lead is also known as a cumulative metabolic poison. The UnitedStates FDA action level for lead in clams, oysters and mussels is1.7 mg kg1 wet wt (Kimbrough et al., 2008), but Canada has a much

1

10.9 (7.115.7) Fung et al. (2004)7.6 (6.08.8) Fung et al. (2004)5.9 (3.47.6) Fung et al. (2004)6.3 (4.78.2) Fung et al. (2004)lower action level of 0.5 mg kg wet wt for these bivalves (Ahmed,1991). Low Pb concentrations are often observed in marine organismsdue to both dissolved and dietary leads which were observed to havea low bioavailability tomarine animals (Amiard et al., 1985, 1986). Forexample, the bioaccumulation of Pb in mussel M. edulis transplantednear mine drainages in Greenland was very slow (Riget et al., 1997).

coastal areas of China.

ollection period Average value and the range(mg kg1 dry wt)

Reference

0022003 0.14 (0.080.45)a Wang et al. (2005)002 0.14 (0.070.21)a Cheng et al. (2004)0022003 0.14 (0.070.35)a Cai and Xiao (2006)001 0.07 (0.070.14)a Ruan et al. (2003)001 0.07 (0.040.09)a Cheng et al. (2004)0022003 0.14 (0.080.27)a Wang et al. (2005)0022003 0.23 (0.041.36)a Wang et al. (2005)005 0.08 (0.040.17)a H. Wang et al. (2007)005 0.13 (0.100.17)a H. Wang et al. (2007)

However, the efux of accumulated lead was also slow. Overall,the average concentration of Pb in bivalves from the coasts of Chinawas found to be between 0.3 and 8.4 mg kg1. Oysters had a Pbconcentration of between 0.77 and 14.7 mg kg1, with the highestconcentration found in the oysters collected from Shenzhen (Table 5).Clams R. philippinarum have lower Pb concentration than oysters, butup to 11 mg kg1 can also be observed in this species collectedfrom Hong Kong. Mussels P. viridis have a higher Pb concentration(19 mg kg1) when compared with the other mussel species M.edulis, in which the typical Pb concentration is less than 1 mg kg1.

4.5. Nickel and chromium

Nickel is a ubiquitous, biologically essential trace element that iswidely distributed in the environment. The United States FDA proposedan action level of 80 mg kg1 forNi (US FDA, 2001). Thebioaccumulationof Ni varies greatly among different species of organisms. A typicalbioconcentration factor of 2191 Lkg1 is commonly observed formolluscs (Sigel and Sigel, 1988). The Ni concentrations in bivalvescollected from China are generally less than 5 mg kg1 (Table 6). Higherconcentrations are reported in the greenmussels P. viridis collected fromthe Shantou port shelter (~33 mg kg1) and in the clam R. philippinarumcollected from Bohai Bay (~10 mg kg1).

Domestic and industrial products are rich in Cr. The bioavailability ofCr is complicatedby its speciation and redoxbehavior. Chromiumoccursmainly in two major valency states: as the particle reactive form Cr(III)and as the more soluble hexavalent form Cr(VI). Chromate [Cr(VI)] ismore toxic than Cr(III) which is relatively non-toxic to organisms and isan essentialmicronutrient for mammals. The assimilation efciencies of

than oysters (5 mg kg1) (Table 7). The US FDA action limit for Cr is13 mg kg1 wet wt for bivalve molluscs, while China has a lower Crregulatory limit of 2 mg kg1 wet wt for seafood.

4.6. Mercury

Mercury is a highly toxic, naturally-occurring trace metal. Both Hgand methylmercury (MeHg) can complex with organic matter inseawater and sediments. Although both inorganic Hg complex andMeHg are lipophilic, MeHg is more readily bioaccumulated thaninorganic Hg in marine organisms. The Hg concentrations, especiallyMeHg concentrations, in seafood from China remain largely unknown.Limited data indicate a concentration of between0.1 and 0.5 mg kg1 oftotal Hg (THg) in bivalves collected from China (Table 8), which iscomparable with the levels found in theMusselWatch Program (20042005).Wang et al. (2005) reported a concentration of 0.041.4 mg kg1

of THg in bivalves collected from Bohai Bay. The MeHg concentrationswere relatively low, frombelowdetection limit (~0.001 mg kg1) to thehighest level of 0.35 mg kg1. The highest THg concentrationwas foundin the musselsM. edulis collected from Penglai, Shandong province.

5. Mercury in marine sh in China

The consumption of marine sh is one of the primary pathways ofexposure to Hg for humans, and Hg contamination in marine sh is awidespread problem with major public health concerns owing to itspotential neurotoxicity. High concentrations of Hg can be found inmarine sh muscle with methylmercury (MeHg) as the principal form.Concentrations of MeHg in marine sh typically increase with

es fr

Collichthys lucidus Zhejiang 1998Cynoglossus joyneri Zhejiang 1998

13K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316Mugil cephalus Zhejiang 1998Halichoeres nigrescens Hong Kong 20092010Atherinomorus lacunosus Hong Kong 20092010Terapon jarbua Hong Kong 20092010Siganus canaliculatus Hong Kong 20092010Epinephelus fasciatomaculosus Hong Kong 20092010Sebastiscus marmoratus Hong Kong 20092010Lutjanus russellii Hong Kong 20092010Gerres macrosoma Hong Kong 20092010Acanthopagrus australis Hong Kong 20092010Parupeneus ciliatus Hong Kong 20092010Apogon cookii Hong Kong 20092010

aCr(III) by various bivalves are generally less than 5% (Wang and Fisher,1999a, 1999b). Higher assimilation efciencies (10.524.4%) werefound in green mussels P. viridis and the clams R. philippinarum(Chong and Wang, 2000). Mussels collected from the coasts ofChina have somewhat similar Cr concentrations (0.315.7 mg kg1)

Table 9Total Hg (THg) and methylmercury (MeHg) concentrations found in marine sh muscl

Fish species Location Collection period

Platycephalus indicus Hong Kong 2004Epinephelus bleekeri Hong Kong 2004Priacanthus macracanthus Hong Kong 2004Nemipterus virgatus Hong Kong 2004Siganus punctatus Hong Kong 2004Epinephelus coioides Hong Kong 2004Trachinotus blochii Hong Kong 2004Cynoglossus robustus Hong Kong 2004Pseudosciaena crocea Hong Kong 2004Acanthopagrus latus Hong Kong 2004Pampus argenteus Zhejiang 1998Periophthamus sericus Zhejiang 1998Coilia mystus Zhejiang 1998Harpodon nehereus Zhejiang 1998Converted from wet weight basis using a wet wt/dry wt ratio of 7.increasing body size or trophic levels, and high concentrations ofMeHg can be found in the top predator sh such as tuna and swordshcollected from remote sea areas. The action limit set by the US FDA forMeHg in sh is 1 mg kg1 wet wt (US FDA, 2001), while the limits forTHg in seafood in Canada and China are 0.5 and 0.3 mg kg1 wet wt

om China.

THg/MeHg Average value and the range(mg kg1 dry wt)

Reference

THg 1.260.01a Cheung et al. (2008)THg 2.660.49a Cheung et al. (2008)THg 0.980.04a Cheung et al. (2008)THg 2.240.98a Cheung et al. (2008)THg 0.630.14a Cheung et al. (2008)THg 3.010.07a Cheung et al. (2008)THg 2.590.07a Cheung et al. (2008)THg 0.350.07a Cheung et al. (2008)THg 3.570.42a Cheung et al. (2008)THg 2.520.21a Cheung et al. (2008)THg 0.10 (0.010.12)a Fang et al. (2004)THg 0.07 (0.070.08)a Fang et al. (2004)THg 0.09 (0.060.12)a Fang et al. (2004)THg 0.06 (0.010.13)a Fang et al. (2004)THg 0.07 (0.030.10)a Fang et al. (2004)THg 0.13 (0.070.22)a Fang et al. (2004)THg 0.12 (0.050.18)a Fang et al. (2004)MeHg 0.09 (0.020.17) unpublished dataMeHg 0.17 (0.070.44) unpublished dataMeHg 0.09 (0.060.14) unpublished dataMeHg 0.02 (0.000.06) unpublished dataMeHg 0.05 (0.040.06) unpublished dataMeHg 0.15 (0.050.29) unpublished dataMeHg 0.14 (0.050.32) unpublished dataMeHg 0.04 (0.000.28) unpublished dataMeHg 0.05 (0.020.10) unpublished dataMeHg 0.03 (0.020.04) unpublished dataMeHg 0.23 (0.220.24) unpublished data

14 K. Pan, W.-X. Wang / Science of the Total Environment 421422 (2012) 316respectively (Ahmed, 1991; Ma et al., 2009). A person in Hong Kongconsumes sh or shellsh four or more times a week averaging about60 kg of sh per year, which is equal to 164.4 gday1 (Dickman andLeung, 1998). A study conducted by the Food and EnvironmentalHygiene Department of Hong Kong indicated that the daily intake of Hgin secondary school children is 0.43 g kg1 day1, which is greaterthan the guideline limits of 0.1 g kg1 day1 as recommended by theUS EPA (Cheung et al., 2008). A survey indicated that a male adult in acoastal city (Zhoushan) consumes up to 240 g of sh muscle per day,which is far higher than the average rate (23 g/person per day) ofconsumption of marine products in China (Cheng et al., 2009). A higherconsumption of marine sh could mean a higher intake of MeHg.

Data on Hg concentration in marine sh collected from China arerather limited. Fang et al. (2004) found that the marine sh collectedfrom the Zhejiang Province had concentrations of 0.010.22 mg kg1 oftotal Hg. Our most recent study on marine sh caught in Hong Kongwaters indicated MeHg concentrations of 0.0030.32 mg kg1

(Table 9). The low MeHg concentrations were probably due to thesmall size of sh examined in our study (2200 g wet wt). However,Cheung et al. (2008) found that the Hg contents in most of themarine sh collected from local sh markets were between 0.35 and3.57 mg kg1, with the majority of their observations close to theinternational standards.

6. Conclusion and perspectives

China is currently confronted with increasing metal contaminationof its coastal areas.Metals fromvarious sources have putmuch pressureon the health of coastal ecosystems. Industrial discharge, coalcombustion, and increasing e-waste are the major sources of metalcontamination. Hot spots of metal contamination can be found alongthe coasts of China, from the north to the south, especially in theindustry-developed estuaries, such as the Pearl River Estuary andLiaodong Bay. High metal contents can be detected in the sedimentscollected from across the country. Site-specic geographical conditionssuch as poor water exchange conditions can aggravate metal pollutionin coastal areas. Metal contamination in Jinzhou Bay has causedsubstantial adverse effects on local environments and poses greatthreat to human health. Such environmental damage can be irreversibleand devastating to local ecosystems. Metal levels observed in marinebivalves also consistently reect elevated metal pollution in China,althoughmostmetal concentrations in seafood generally did not exceedthe safety guideline limits. Limited data have shown thatmarineshhasbeen affected by elevated Hg concentration.

Measures should be taken immediately to reduce the discharge ofmetals from various anthropogenic sources, given the expectationthat continued rapid economic growth is feasible in China. Policieswith heavy emphasis on economic development should be amendedbecause environmentally friendly and sustainable long-term growthis needed in China. Risk assessments of the economic impacts ofcoastal pollution and the exposure of contaminated seafood tohumans in China are needed as background information to policymakers and to increase public awareness of environmental protection.

Acknowledgments

We thank the two reviewers for their comments on this work. Thisstudy was supported by General Research Funds from the Hong KongResearch Grants Council (663009 and 662610) to W.-X. W.

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