Marine Pollution Bulletin 89 (2014) 487–493

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Marine Pollution Bulletin

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Historical sediment record and distribution of polychlorinated biphenyls(PCBs) in sediments from tidal flats of Haizhou Bay, China

http://dx.doi.org/10.1016/j.marpolbul.2014.09.0010025-326X/� 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author at: School of Geodesy and Geomatics Engineering,Huaihai Institute of Technology, Lianyungang 222005, Jiangsu Province, China.

E-mail address: rzhang_838@163.com (R. Zhang).

Rui Zhang a,b,⇑, Fan Zhang c, Tiancheng Zhang b, Hongqiang Yan b, Wei Shao b, Li Zhou b, Hebing Tong c

a Key Laboratory of Marine Geology and Environment, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, Chinab School of Geodesy and Geomatics Engineering, Huaihai Institute of Technology, Lianyungang 222005, Jiangsu Province, Chinac Department of Chemical Engineering, Huaihai Institute of Technology, Lianyungang 222005, Jiangsu Province, China

a r t i c l e i n f o

Article history:Available online 23 September 2014

Keywords:Polychlorinated biphenylsSedimentPCBs source identificationCongener distribution

a b s t r a c t

The spatial and temporal variations and sources of polychlorinated biphenyls (PCBs) in sediment of tidalflat from Haizhou Bay, China were investigated. PCBs concentrations in surface sediments ranged from1.33 to 6.27 ng g�1 dry weight. Low-chlorinated PCBs, dominated by the tri-PCB homologs, were identi-fied as the prevalent contaminate of surface sediments. These results were in agreement with the factthat tri-PCB homologs are the dominant contaminants in China. In surface sediment, the highest levelappeared in the estuary, and it decreased with distance from the Linhong River estuary. PCBs concentra-tions started to rise from the mid-1950s, and reached a maximum in 2005. PCBs in sediment might orig-inate from surface runoff and discharges of local source as well as slight atmospheric deposition, based onPCA. Additionally, the PCBs levels in the sediments were considered to rarely pose hazard to the aquaticand human health, based on Sediment Quality Guidelines (SQGs).

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Polychlorinated biphenyls (PCBs), a class of persistent organicpollutants (POPs), are ubiquitous contaminants indifferent com-partments of the environments (Hong et al., 1999; Doong et al.,2002; Martin et al., 2003; Fu and Wu, 2006). PCBs are compoundswith a wide range of properties such as vapour pressure, solubility,partition coefficients. Starting from their first commercialization assynthetic organic compounds in 1929, PCBs were manufacturedand used extensively in industrial and commercial applications.Equipment and products commonly containing PCBs includetransformers, capacitors, paints, printing inks, pesticides, hydraulicfluids and lubricants (Erickson and Kaley, 2011). Although the pro-duction of PCBs was prohibited in China in 1981, approximately10,000 tons of PCBs were produced from 1965 to 1974, accountingfor 0.6% of the total global production, and 45% of all PCBs used inChina were used in the eastern China (Xing et al., 2005; Yamashitaet al., 2000). Despite the prohibition of PCB production in mostcountries, the products manufactured before the prohibition arestill used, mostly as dielectric fluid in electrical equipment servic-ing industries (Aries et al., 2006; Hong et al., 2005; Hu et al., 2008;Liu et al., 2009;Dodoo et al., 2012). In addition, PCBs can now be

found in low concentrations in virtually every sphere of the envi-ronment, which is directly related to anthropogenic pollution(Lohmann et al., 2007; Mai et al., 2005; Beyer and Biziuk, 2009).

Sediment is the main reservoir and a potential secondary sourceof various hydrophobic organic pollutants (HOPs), especially somePersistent Organic Pollutants (POPs) pollutants (Duan et al.,2013b). PCBs enter the aquatic environment through a variety ofpathways including atmospheric transport and deposition, riverinput, industrial and municipal wastewater discharge (Tottenet al., 2006; Zhou et al., 2001; Duan et al., 2013a). Once in the aqua-tic environment, PCBs, by virtue of their low-water solubility, tendto stick to particles and sediments in water. As a result, sedimentsat the bottom of large water bodies of act as a ‘‘reservoir’’ of PCBs.This association then leads to accumulation in sediments, whichmay play a role as secondary contamination sources. Therefore,PCBs use and disposal are now recognized as major environmentalproblems worldwide and, as a consequence, knowledge of PCBsconcentrations in the environment is needed to understand thepresent level of contamination, assess the risk, and plan remedia-tion actions.

Haizhou Bay lies on the western margin of the South YellowSea, near the city of Lianyungang, and receives water inflow fromthe Linhong River (Fig. 1). Haizhou Bay is a major fishery base.Lianyungang Harbor, a natural deep-water harbor, is located onthe southeast side of Haizhou Bay and is one of the most importantharbors in China. In the past, the regions near Haizhou Bay

Fig. 1. Sampling sites map. Surface sediment samples were taken at stationsHZ1-HZ10 from southern tidal flat and NH1-NH10 from northern tidal flat, while asediment core was taken at station LH3.

488 R. Zhang et al. / Marine Pollution Bulletin 89 (2014) 487–493

experienced significant economic development. Municipal domes-tic sewage and industrial waste water were either dischargeddirectly into the sea along the Linhong River and the coastal lineor discharged after simple aerobic treatment. However, due tothe high population density and rapid industrial development withsimultaneous developments in the construction of harbors, trans-portation and tourism, the bays are polluted with a variety ofchemicals, such as PAHs and heavy metals (Zhang et al.,2013a,b). In addition, the levels of PCBs in this area are not known.The aims of the current study can therefore be summarized as fol-lows: (1) to elucidate the spatial distribution and homolog compo-sition of PCBs in tidal flat sediment of Haizhou Bay and thehistorical records of PCBs pollution; (2) to trace the sources of PCBsand investigate the correlation between PCBs concentration andenvironmental factors such as TOC content and grain size in thestudy areas; and (3) to compare measured concentrations of PCBswith existing ecotoxicological and human health assessment crite-ria or guidelines.

Sediments were collected from 20 sampling sites in tidal flat ofHaizhou Bay. The locations of the sampling stations are shown inFig. 1. The surface sediments (top 0–3 cm) were collected in June2007 using a stainless steel grab and then placed into prewashedglass bottles. Sediment core LH3 was manually collected fromthe south tidal flat of Haizhou Bay, near the Linhong River estuaryin April 2010, was shown in Fig. 1. The core is 65 cm in length and7.5 cm in diameter. In the laboratory core LH3 was sub sampled at1 cm intervals. All samples were immediately transferred to the

laboratory and kept at �20 �C. The sediments were freeze-driedovernight using a Christ Alpha 1–4 LSC freeze dryer (Martin Christ,Germany) operated at �60 �C and 0.560 mbar. The dried sedimentswere grounded and passed through a nylon sieve of 100 mesh toremove fine debris and dead organisms. All the equipment usedfor sample collection, transportation, and preparation were thor-oughly washed and rinsed with acetone and hexane to minimizethe likelihood of crosscontamination.

PCBs calibration check solution (PCBs 8, 18, 28, 44, 52, 66, 77,101, 105, 118, 126,128, 138, 153, 170, 180, 187, 195, 206, and 209)was purchased from AccuStandard, Inc. (New Haven, CT, USA), whiletwo single PCBs congeners (PCBs 171 and 183) were supplied byDr. Augsburg Ehrenstorfer, Germany. 13C12-labeled mono-deca PCBs(PCBs 3,15, 28, 52, 118, 153, 180, 194, 208, and 209), 13C12-labeledPCB-101 and 13C12-labeledPCB-202 were purchased fromCambridge Isotope Laboratories, Inc. (Andover, MA, USA). TheHPLC-grade methylene chloride and n-hexane were obtained fromMerck (Darmstudt, Germany). Neutral silica gel (70–230 mesh,Merck, Darmstudt, Germany) was Soxhlet extracted with a mixtureof 1:1 methylene chloride: n-hexane for 72 h prior to use.

210Pb was determined by alpha counting of the 210Po depositedonto Ag discs (Flynn, 1968) by using 209Po as a yield tracer. Thesediment was dissolved by adding a mixture of HNO3:HCl:HF(1:1:0.5 v/v/v) to 2 g of sediment and heating to 200 �C overnightin closed Teflon containers. Counting was conducted by computer-ized multichannel a-spectrometry with gold–silicon surface bar-rier detectors (Model Octetc PLUS, ORTEC Co., USA).

The sample extraction and cleanup procedures have beendescribed in detail elsewhere (Environment Canada, 1997). A10 g freeze-dried sediment sample was spiked with 200 ng of each13C12-labeled PCBs congeners (PCBs 3, 15, 28, 52, 118, 153, 180,194, 208, and 209) and was Soxhlet extracted with a mixture of120 mL n-hexane/methylene chloride (7:3 v/v) for 24 h. Activatedcopper granules were added to remove potential elemental sulfur.The extract was concentrated, and solvent exchanged to hexaneand purified on an 12 mm i.d. silica column packed, from the bot-tom to top, with 10% (weight ratio) silver nitrate silica gel (6 cm),neutral silica gel (2 cm, 3% deactivated), 33% sodium hydroxide sil-ica gel (6 cm), neutral silica gel (2 cm), 44% sulfuric acid silica gel(6 cm), neutral silica gel (4 cm) and anhydrous sodium sulfate.The column was eluted with 100 mL n-hexane/methylene chloride(95:5 v/v), and the eluent was then concentrated to 0.5 mL for GCanalysis. A known quantity of 13C12-labeled PCB-101 and13C12-labeled PCB-202 was added as an internal standard prior toGC–MS analysis. Sample analysis was performed on an FinniganPolarisQ gas chromatograph (GC) equipped with HP-5973 massselective detector (MS) and an HP-5 silica fused capillary column(30 m � 0.25 mm � 0.32 mm, Thermo Fisher Scientific Inc., USA),operated under selected ion monitoring (SIM) mode. Helium wasused as the carrier gas at a flow rate of 1.0 mL/min. The columntemperature was held at 60 �C for 1 min,10 �C/min to 160 �C, held1 min, 2 �C/min to 180 �C, 0.5 �C/min to 185 �C, held 1 min,then1 �C/min to 190 �C, held 1 min, 2 �C/min to 260 �C, held for5 min. Transfer line, ion source, and quadrupole temperatures werekept at 280, 230, and 150 �C, respectively. The PCBs congenerswere quantified using relative response factors (RRFs) establishedfrom calibration runs, which is the ratio of analyst response factorto the response factor of the corresponding labeled surrogate. Afive-point calibration curve was used to check the linearity of theMS. Along with native and surrogate responses from the samplerun, recovery-corrected concentrations of PCBs congeners werecalculated directly.

In addition, a grain size analysis was performed on homoge-nized sample (2 g) using a laser particle size analyzer (Mastersize2000, Malvern Instruments Ltd., UK), after the removal of carbon-ate with1 mol/L HCl and of organic matter using 30% H2O2. 0.2 g

R. Zhang et al. / Marine Pollution Bulletin 89 (2014) 487–493 489

freeze-dried samples were ground, and carbonate was removed bytreatment with 10% (v/v) hydrochloride acid for 24 h. After thesamples were dried at 60 �C for 24 h in an oven, the TOC contentof sediment (10 mg) was measured by a Flash 2000 Elemental Ana-lyzer (Thermal, USA) (King et al., 1998; Duan et al., 2013a; Yanget al., 2011).

The instrument detection limit (IDL) was calculated as threetimes the standard deviation (SD) of the peak heights from six injec-tions of the standard solutions, which ranged from 0.005 to0.016 ng g�1 (Table S1 of Supporting Information). For each batchof 10 field samples, a method blank (solvent), a spiked blank (stan-dards spiked into solvent) and a matrix spike (standards spiked intofresh sediment) were processed, none of the target compoundswere detected in the procedural blanks. All samples were spikedwith a labeled recovery standard (containing 13C analog of PCB3,15, 28, 52, 118, 153, 180, 194, 208, and 209) prior to extraction.Excellent recoveries were obtained, were obtained, ranging from71% to 105% for all the samples (Table S2). All the results were cor-rected with the recovery ratios and reported in ng g�1 dry weight.

In this study, correlation analysis was performed to obtaininformation about the interrelationships between PCBs and TOC,grain size. To assess the possible sources of PCBs, multivariate sta-tistical analysis was conducted using principal component analysis(SPSS 20.0 for Windows, SPSS Inc., USA). The computer packageSPSS (SPSS 20.0 for Windows, SPSS Inc., USA) was employed toperform the statistical analyses.

The core LH3 consists of relatively uniform fine-grained materi-als, with the percentage of silt (4–63 lm) and clay (<4 lm) exceed-ing 95% (Fig. S1 (a) and Table S3 of Supporting Information). Thesilt fraction ranges from 65.0% to 98.3%, and the clay fractionranges from 0.04% to 35.0%. The percentage of sand is very smallin these cores. The surface sediments are dominated by silt andclay, which exceed 65% (Fig. S1 (a) and Table S3). The surface sed-iment also mainly consists of silt, with average percentage of 66%(Fig. S1 (b)).

The profile of the excess 210Pb for the core LH3 was shown inFig. S2. The excess 210Pb activities exhibit an approximately expo-nentially decreasing trend with depth (Fig. S2). On the basis of the210Pbex activities, the constant initial concentration (CIC) modelwas used to calculate sedimentation rates. The mean sedimenta-tion rate was calculated to be 0.85 cm yr�1 for core LH3. The sedi-ments in these cores have accumulated over approximately the lastfifty years at a constant sedimentation rate. For core LH3, the layerat a depth of 47 cm corresponds to 1950.

Individual and total concentrations of PCBs congeners (P

22PCBs)are listed in Table S4 of Supporting Information. Total PCBs levelsvaried from 1.33 to 6.27 ng g�1, with the mean value of 4 ng g�1.Although we recognized that direct comparison is somewhat com-promised by the fact that different studies consider different PCBscongeners, it is still important to evaluate the quantitative patternsof PCBs contamination to get a sense of regional similarity. Com-pared to the PCBs concentration data of surface sediments reportedin other industrial/urban coastal environments (Table 1), concentra-tions of PCBs in tidal sediments of Haizhou Bay are low. However,concentrations of PCBs in surface sediments in this study were alsohigher than those reported from other locations in South Yellow Sea(Table 1), which is at great distance from the coast.

In Table S4 and Fig. 2, the spatial distribution of PCBs in surfacesediments of tidal flat in Haizhou Bay revealed that PCBs concen-trations varied widely depending on their location. The maximumconcentration of total PCBs was 6.27 ng g�1 at HZ2 station, whichwas near estuary in the southern tidal flat of Haizhou Bay. Theminimum concentration was 1.33 ng g�1 at NH3 station, whichwas at northern tidal flat of Haizhou Bay.

In addition, the results showed that the PCBs concentrations intidal flat decreased with the increase of the distance to the Linhong

River estuary. Moreover, the region with the highest concentra-tions of PCBs was observed in samples from HZ1, HZ2 and HZ3,probably due to the confluence of Linhong River inflow. LinhongRiver flows through the highly populated and industrialized cityof Lianyungang, and is used to be the main drainage channel fordisposal of wastes. The industrial wastewater discharge may havecaused serious PCBs contamination in the Lianyungang Riverinflow. In addition, PCBs in the surface soil and atmospherethroughout the watershed might be incorporated into the ground-water through frequent rainfalls and storms, thus increase thePCBs levels in the river flow. Therefore, Linhong River inflow wassuggested to be a major contributor of PCBs to the Haizhou Bay.This mechanism was also reported to be the cause for the accumu-lation of both aliphatic and poly aromatic hydrocarbons in sedi-ments of the Obriver entering to the Kara Sea and ChangjiangRiver estuary (Nemirovskaya, 2009; Yang et al., 2012). However,the second highest concentration of total PCBs was found in sedi-ments from sites NH1 in northern tidal flat, which was located atestuary of Xiuzhen River. The high level at site NH1 is likelyexplained by the fact that NH1 is near the large harbor of Rizhao,Shandong Province, where many factories and shipping activitiesdischarge various organic pollutants. As a result, the explanationof the distribution of PCBs in coastal sediments from HaizhouBay could be enhanced by more information about riverine, atmo-spheric, and point source inputs.

The physicochemical characteristics of sediments (e.g. TOC,grain size, and clay minerals) were found to be correlated withPCBs concentrations in sediments (Chen et al., 2003; Song, 2004;Bondi et al., 2006; Yang et al., 2011, 2012; Duan et al., 2013a).The TOC and clay contents in sediment were shown in Table S3.There was a positive, significant linear correlation between PCBsconcentrations and TOC contents of the surfacial sediments inHaizhou Bay (Fig. S3; r = 0.60, n = 43, p < 0.01). In addition, PCBsconcentrations and the contents of clay was significantly corre-lated (Fig. S3; r = 0.51, n = 43, p < 0.01). These results suggestedthat the organic matter in sediment may play more significant rolein the PCBs levels. This was consistent with the previous studiesthat TOC content of fine sediment reflected more accurately thelevels of toxic organic pollutants, such as PCBs, PAHs and organo-chlorine compounds in sediments (Edgar et al., 2003; Hung et al.,2007; Zhang et al., 2007; Duan et al., 2013a). The PCBs concentra-tions in tidal flat have declined with distance from estuary, imply-ing that TOC had an important effect on the PCBs distribution. Inaddition, coastal currents in Haizhou Bay always flowed southwardalong coastal line, and the south tidal flat acted as sink of finer sed-iment particles (Wang et al., 1980). Consequently, the characteris-tics of the sediments controlled by hydrodynamic conditions werealso factor impacting on PCBs distribution.

The homolog composition of PCBs in most samples was charac-terized by mixtures with a low chlorination level. Octa-PCB, nona-PCB and deca-PCB were absent, hexa-PCB and hepta-PCB were verylow. The average homolog composition of PCBs in all surficial sed-iment samples decreased in the following order: tri-PCB (49.5%),tetra-PCB (22.9%), penta-PCB (12.8%), di-PCB (12.1%), hexa-PCB(2.4%), hepta-PCB (1.1%) (Fig. 3). The most prevalent congeners inP

22PCBs composition of sediments are lighter chlorinated congen-ers (PCB 8, PCB 18 and PCB 28), this composition in our study is inagreement with previous reports of PCB congener distributions insediments from China (Ren et al., 2007; Jiang et al., 1997). Approx-imately 10,000 tons of PCBs were produced in China from 1965 to1974 (when production was banned), with 9000 tons as trichloro-biphenyl, known as #1 PCB, and 1000 tons as pentachlorobiphenyl,known as #2 PCB (Xing et al., 2005). Trichlorobiphenyl was usedprimarily in power capacitors, while pentachlorobiphenyl wasused mainly as a paint additive (China SEPA, 2003). In addition,#1 PCB was similar to Aroclor 1242, which was contained 42%

Table 1Comparison of PCBs concentrations in the surface sediments of different coastal areas.

Location PCBs (ng/g) References

Narragansett Bay, USA 20.8–1760 Hartmann et al. (2004)Naples harbor, Italy 10–899 Sprovieri et al. (2007)Masan Bay, Korea 1.24–41.4 Hong et al. (2003)Hong Kong’s coast 3.5–25.1 Hong et al. (1999), Connell et al. (1998)Singapore’s coast 1.4–329.6 Wurl and Obbard (2005)Pearl River Estuary, China 11.54–485.45 Kang et al. (2000), Xing et al. (2005)Dalian Bay 58.1 (average) Xing et al. (2005)Minjiang River Estuary, China 15.8–57.9 Zhang et al. (2003)Daya Bay, China 0.85–27.37 Zhou et al. (2001)South Yellow Sea 0.09–5.8 Zhang et al. (2007), Duan et al. (2013b)

Fig. 2. Spatial distribution of PCBs in surface sediment of tidal flat, Haizhou Bay.

Fig. 3. Composition of PCBs congeners in Chinese transformer oil, Chinese PCBproducts (Jiang et al., 2007) and surface sediment of tidal flat, Haizhou Bay.

490 R. Zhang et al. / Marine Pollution Bulletin 89 (2014) 487–493

chlorine, and #2 PCB was similar to Aroclor 1254, which was con-tained 53% chlorine (Jiang et al., 1997; Breivik et al., 2002). It is alsonoted that the prevalence of less chlorinated PCB homologs (di- totetra-PCBs) in sediments agrees closely with PCB contaminationsin Chinese rural soils but deviates from PCB homologs (Ren et al.,2007), in which tri-PCB ranged 21–45%, tetra-PCB 12–38%, anddi-PCB 9–28%, respectively (Breivik et al., 2002; Zhang et al.,2008). These results imply that agricultural soils can be an impor-tant input for PCBs accumulated in sediments of the study region.

The primary goals of principal component analysis (PCA) wereto identify the possible sources and evaluate the similarity of thePCB patterns found in the coastal sediments. PC 1 and 2 accountedfor 46.1% and 23.2% of the total variance, respectively. PC1 repre-sents surface runoff and point source deposition and PC 2 repre-sents atmospheric deposition.

PC 1 was dominated by penta-PCB and hexa-PCB (Fig. 4). InChina, more than 90% of the PCBs produced were tri-PCB andhexa-PCB. Following the ban of production and usage of PCBs in1974, they continue to be used in electrical capacitors, electricaltransformers, vacuum pumps and gas transmission turbines. Theyare accidentally released from these sources the environment fromlandfills, surface runoff and sewage sludge incineration (Konat andKowalewska, 2001). We suggest that PCBs entered the rivers orwere directly discharged to Haizhou Bay, and entrained by partic-ulates, thence being deposited in sediment of Haizhou Bay. Theprevalence of penta-PCB and hexa-PCB in the sediments of HaizhouBay tidal flats are consistent with those reported previously in Chi-nese surface soils, Yellow Sea, Changjiang Estuary and adjacentEast China Sea (Ren et al., 2007; Yang et al., 2012; Duan et al.,2013b). Therefore, penta-PCB and hexa-PCB of PC 1 represents sur-face runoff.

However, PC 1 was also characterized by hepta-PCBs. Highlychlorinated congeners originated mainly from the release ofman-made pollution (Hong et al., 2005). In addition, LianyungangHarbor, a natural deep-water harbor, is located on the southeastside of Haizhou Bay and is one of the most important harbors inChina. The shipping industry promotes the economic development

Fig. 4. Principal component analysis of PCBs compositions in surface sediment.

Fig. 5. Historical trends of PCBs concentration in a sediment core (LH3) from tidalflat of Haizhou Bay.

R. Zhang et al. / Marine Pollution Bulletin 89 (2014) 487–493 491

of Lianyungang City, but inevitably brings serious pollution tocoastal waters (Hong et al., 2005; Yuan et al., 2001). Therefore,the hepta-PCBs of PC 1 revealed the pollutants discharged directlyinto the water from local sources.

In a marine environment with competing activities and com-merce, such as mariculture, fishing, shipping, and industry, sourcesof PCBs are generally diffuse and difficult to identify precisely.There are multiple sources of PCBs in Haizhou Bay, and we arenot able to identify their precise origins or sources. There are othergeologic and environmental processes, such as sediment resuspen-sion, coastal transport or dechlorination, which modify the PCBsstructures from their source configurations (Tyler and Millward,1996). Thus, PC 1 represents the mix source of surface runoff anddischarges of local source.

PC 2 was dominated by di-PCB, tri-PCB and tetra-PCB. In Chi-nese air, the PCB homologs were dominated by di- to hexa-PCBs(Zhang et al., 2008). However, lower chlorinated congeners wereeasily degraded by hydroxyl radicals in the air. Many studies(Gioia et al., 2006; Totten et al., 2006) have shown that PCB con-centration level in lower atmosphere near the water was sustainedby low chlorinated congeners volatilized from the upper waterlayer. Thus PC 2 revealed the input of PCBs from atmosphericdeposition.

The historical trends of total PCBs concentrations in a datedsediment core LH3 are shown in Fig. 5. The concentrations of

P22-

PCBs at the 1950–1970 horizons were lower than the post-1970shorizons. The lowest concentration in the lower horizons wasfound at a depth of 46.5 cm (2.1 ng g�1), corresponding to sedi-ment deposited in 1956. From 1950 to mid-1970s, the concentra-tions of

P22PCBs increased at a slow steady rate. This time

period corresponds to the timeframe of increased PCBs use inChina (Xing et al., 2005; Meng et al., 2000). This trend has beenreported in sediments from the Pearl River Delta (Mai et al.,2005) and Yellow Sea (Zhang et al., 2007; Duan et al., 2013b) andis believed to be related to importation of PCB-containing electricequipment from industrialized countries prior to the time of PCBsproduction in China. The maxima of PCBs in sediments of the studyareas was in agreement with the maxima reported between themid-1960s in the USA and early 1980s in Japan (Yamashita et al.,2000; Oliver et al., 1989).

There is a very evident decrease of PCBs concentrations in thelate-1970s (Fig. 5), correlated with the legal ban in China in1974. The trend reversed itself in the 1980s, continuing to increasein concentrations until 2005. Despite the termination of produc-tion in China in 1974, concentrations increased from the late1970s to the highest concentrations near surface horizons, having

doubled from those of the 1980s. These results reflect the contin-ued local economic development in Lianyungang, and are similarto PAHs sediment profiles in Haizhou Bay (Zhang et al., 2013b).These historical trends of PCBs contamination in coastal marinesediments are similar to those found elsewhere in developed coun-tries (Santschi et al., 2001; Xing et al., 2005). Following the ban onproduction and use of PCBs in the 1970s in the USA, the PCBs levelsin Mississippi River Delta, Galveston Bay and Tampa Bay (Gulf ofMexico) decreased sharply within the following decade, but laterthey obviously increased due to the fast-growing economy(Santschi et al., 2001). Similar sediment PCBs profiles wereobserved in Changjiang Estuary and adjacent East China Sea(Yang et al., 2012; Duan et al., 2013a), being particularly evidentin areas where the economy developed rapidly. PCBs concentra-tions have declined since 2005 (Fig. 5), possibly due to increasedpollution abatement measures and efforts by the government. Italso could be due to other environmental factors (meteorogicalchanges, weather, degradation), which have not been directly asso-ciated with the declines. This trend of PCBs concentrations incoastal sediments has been reported for the Changjiang Estuaryand adjacent marginal sea (Yang et al., 2012).

Fig. 6 illustrates the profile of PCBs homologues in the HaizhouBay sediment core. The di- to hepta-PCB are the major constituentsof the total PCBs in sediment. These PCBs homolog distributionshave increased slightly from the bottom of sediment core (1956).The maximum in profile is found at a depth of 18.5 cm, corre-sponding to sediment deposited in 1989. The PCBs homolog distri-butions are also similar to the profiles of PCBs concentrations. Inaddition, this trend was also found in the Pearl River Delta (Maiet al., 2005), Yellow Sea (Zhang et al., 2007), Changjiang Estuary(Yang et al., 2012) and East China Sea (Duan et al., 2013a).

Concentrations of PCBs in surficial sediments of Haizhou Baytidal flats are lower than the pollutant control standards prescribedby the National Environmental Protection Agency of China(50 mg kg�1, GB13015) (Zhang et al., 2007), and is in the lowestcategory of reported global PCBs measurements in sediments(0.2–400 ng g�1) (Flower, 1990; Mai et al., 2005). Because thereare no published ecotoxicological standards for evaluation of con-centrations of PCBs in sediments in China, we used the US NOAASediment Quality Guidelines (SQGs) (Long et al., 1995) for compar-ative purposes. These guidelines incorporate two values, an effectsrange-low (ERL, bio-nocuousness probability < 10%) and effectsrange-median (ERM, bio-nocuousness probability > 50%) bench-marks, for assessing a number of trace metals and organic com-pounds including PCBs in the environment. The ERL (50 ng g�1)and ERM (400 ng g�1) values are intended to define chemicalconcentration ranges that are rarely, occasionally, or frequently

Fig. 6. Composition of PCBs homologs in a sediment core (LH3) from tidal flat ofHaizhou Bay.

492 R. Zhang et al. / Marine Pollution Bulletin 89 (2014) 487–493

associated with adverse biological effects including altered benthiccommunities (depressed species richness or total abundance), his-topathological disorders in demersal fish, EC50 or LC50 concentra-tions, and toxicity predicted by models. Sediments are below theUS NOAA SQGs for PCBs and pose little or no ecotoxicological riskto the marine environment. In fact, the PCBs concentrations in ourstudy are one order of magnitude less than ERL. Consequently,PCBs rarely imposed a reverse risk on the eco-environment ofHaizhou Bay.

Low concentrations of PCBs, when compared to other highlyurbanized areas in the world, were common features of tidal flatin Haizhou Bay. In surface sediments of tidal flat in Haizhou Bay,P

22PCBs ranged between 1.33 and 6.27 ng g�1 (with a mean valueof 4.0 ng g�1), with the highest concentrations occurred near estu-ary of Linhong River. In addition, the total PCBs concentrationshave gradually increased since the mid-1950s, and peaked in thelate 1980s, which may track the economic development of Lian-yungang. The homolog profile of PCBs was dominated by di-PCB,tera-PCB and penta-PCB congeners (accounting for 85.1%), whichwas compatible with the fact that tri-PCB compounds are the dom-inant contaminants in China. PCBs in the sediments came from sur-face runoff and discharges of local source as well as atmosphericdeposition, based on PCA. Additionally, the PCBs concentrationsare less than ERL, and they rarely produced a negative influenceon local eco-environments.

Acknowledgments

This work was financially supported by the National NaturalScience Foundation of China (No. 41406055 and 41306114), OpenFund of State Key Laboratory of Pollution Control and ResourcesReuse (No. PCRRF11024), the Project of Innovation for Undergrad-uate in Jiangsu Province (No. SY201311641107001), the ProjectFunded by the Priority Academic Program Development of JiangsuHigher Education Institutions, Natural Science Foundation ofJiangsu Provincial Department of Education (No. 14KJB170001),China Postdoctoral Science Foundation (No. 2014M561973), andPostdoctoral Science Foundation of Qingdao City.

Appendix A. Supplementary material

Supplementary data associated with this article can be found,in the online version, at http://dx.doi.org/10.1016/j.marpolbul.2014.09.001.

References

Aries, E., Anderson, D.R., Fisher, R., Fray, T., Hemfrey, D., 2006. PCDD/F and ‘‘Dioxin-like’’ PCB emissions from iron ore sintering plants in the UK. Chemosphere 65,1470–1480.

Beyer, A., Biziuk, M., 2009. Environmental fate and global distribution ofpolychlorinated biphenyls. Rev. Environ. Contam. Toxicol. 201, 137–158.

Bondi, G., Mirza, U.B., Al-Omair, A., Murad, H., Jamal, Z., 2006. Spatial distribution ofpolychlorinated biphenyls in coastal marine sediments receiving industrialeffluents in Kuwait. Arch. Env. C 50, 166–174.

Breivik, K., Sweetman, A., Pacyna, J.M., Jones, K.C., 2002. Towards a global historicalemission inventory for selected PCB congeners—a mass balance approach1.Global production and consumption. Sci. Total Environ. 290, 181–198.

Chen, M.R., Yu, L.Z., Xu, S.Y., Feng, K., Han, X.F., 2003. Spatial distribution ofpolychlorinated biphenyls (PCBs) contaminants in the tidal-flat sediments ofYangtze Estuary. Mar. Pollut. Bull. 5, 22–28.

China SEPA, 2003. Building the Capacity of the People’s Republic of China toImplement the Stockholm Convention on POPs and Develop a NationalImplementation Plan, GEF Project Brief (GF/CPR/02/010).

Connell, D.W., Wu, R., Richardson, B.J., Leung, K., Lam, P., Connell, P.A., 1998.Occurrence of persistent organic contaminants and related substances in HongKong marine areas: an overview. Mar. Pollut. Bull. 36, 376–384.

Dodoo, D.K., Essumang, D.K., Jonathan, J.W.A., Bentum, J.K., 2012. Polychlorinatedbiphenyls in coastal tropical ecosystems: distribution, fate and risk assessment.Environ. Res. 118, 16–24.

Doong, R.A., Peng, C.K., Sun, Y.C., Liao, P.L., 2002. Composition and distribution oforganochlorine pesticide residues in surface sediments from the Wu-Shi Riverestuary. Taiwan, Mar. Pollut. Bull. 45, 246–253.

Duan, X.Y., Li, Y.X., Li, X.G., Li, M.F., Zhang, D.H., 2013a. Distributions and sources ofpolychlorinated biphenyls in the coastal East China Sea sediments. Sci. TotalEnviron. 463–464, 894–903.

Duan, X.Y., Li, Y.X., Li, X.G., Zhang, D.H., Li, M.F., 2013b. Polychlorinated biphenyls insediments of the Yellow Sea: distribution, source identification and fluxestimation. Mar. Pollut. Bull. 76, 283–290.

Edgar, P.J., Hursthouse, A.S., Matthews, J.E., Davies, I.M., 2003. An investigation ofgeochemical factors controlling the distribution of PCBs in intertidal sedimentsat a contamination hot spot, the Clyde Estuary. UK. Appl. Geochem. 18, 327–338.

Environment Canada, 1997. Reference Method for the Analysis of PolychlorinatedBiphenyls (PCBs). In: Report of Environmental Protection Series Regulations/Guidelines/Codes of Reference Methods (Report EPS 1/RM/31).

Erickson, M.D., Kaley, R.G., 2011. Applications of polychlorinated biphenyls.Environ. Sci. Pollut. Res. 18, 135–151.

Flower, S.W., 1990. Critical review of selected heavy metal and chlorinatedhydrocarbon concentrations in the marine environment. Mar. Env. Res. 29, 1–46.

Flynn, W.W., 1968. The determination of low level of polonium-210 inenvironmental materials. Analyt. Chim. 43, 221–226.

Fu, C.T., Wu, S.C., 2006. Seasonal variation of the distribution of PCBs in sedimentsand biota in a PCB-contaminated estuary. Chemosphere 62, 1786–1794.

Gioia, R., Steinnes, E., Thomas, G.O., Mejier, S.N., Jones, K.C., 2006. Persistent organicpollutants in European background air: derivation of temporal and latitudinaltrends. J. Environ. Monitor 8, 700–710.

Hartmann, P.C., Quinn, J.G., Cairns, R.W., King, J.W., 2004. Polychlorinated biphenylsin Narragansett Bay surface sediments. Chemosphere 57, 9–20.

Hong, H.S., Chen, W.Q., Li, X., Wang, X.H., Zhang, L.P., 1999. Distribution and fate oforganochlorine pollutants in the Pearl River Estuary. Mar. Pollut. Bull. 39, 376–382.

Hong, S.H., Yim, U.H., Shim, W.J., Oh, J.R., Lee, I.S., 2003. Horizontal and verticaldistribution of PCBs and chlorinated pesticides in sediments from Masan Bay,Korea. Mar. Pollut. Bull. 46, 244–253.

Hong, S.H., Yim, U.H., Shim, W.J., Oh, J.R., 2005. Congener-specific survey forpolychlorinated biphenlys in sediments of industrialized bays in Korea:regional characteristics and pollution sources. Environ. Sci. Technol. 39, 7380–7388.

Hu, D.F., Martinez, A., Hornbuckle, K.C., 2008. Discovery of non-Aroclor PCB (3,3’-dichlorobiphenyl) in Chicago air. Environ. Sci. Technol. 42, 7873–7877.

Hung, C.C., Gong, G.C., Chen, H.Y., Hsieh, H.L., Santschi, P.H., Wade, T.L., Sericano, J.L.,2007. Relationships between pesticides and organic carbon fractions insediments of the Danshui River estuary and adjacent coastal areas of Taiwan.Environ. Pollut. 148, 546–554.

Jiang, K., Li, L.J., Chen, Y.D., Jin, J., 1997. Determination of PCDD/Fs and dioxin-likePCBs in Chinese commercial PCBs and emissions from a testing PCB incinerator.Chemosphere 34, 941–950.

Jiang, Q.L., Zhou, H.Y., Xu, D.D., Chai, Z.F., Li, Y.F., 2007. Characteristics of PCBcongeners and homologs in Chinese transformer oil, China. J. Environ. Sci. 27,608–612 (in Chinese).

Kang, Y., Sheng, G., Fu, J., Mai, B., Zhang, G., Lin, Z., 2000. Polychlorinated biphenylsin surface sediments from the Pearl River Delta and Macau. Mar. Pollut. Bull. 40,794–797.

King, P., Kennedy, H., Newton, P.P., Jickells, T.D., Brand, T., Calvert, S., Cauwet, G.,Etcheber, H., Head, B., Khripounoff, A., Manighetti, B., Miquel, J.C., 1998. Analysisof total and organic carbon and total nitrogen in settling oceanic particles and amarine sediment: an interlaboratory comparison. Mar. Chem. 60, 203–216.

R. Zhang et al. / Marine Pollution Bulletin 89 (2014) 487–493 493

Konat, J., Kowalewska, G., 2001. Polychlorinated biphenyls (PCBs) in sediments ofthe southern Baltic Sea- trends and fate. Sci. Total Environ. 280, 1–15.

Liu, G.R., Zheng, M.H., Ba, T., Liu, W.B., Guo, L., 2009. A preliminary investigation onemission of polychlorinated dibenzo-p-dioxins/dibenzofurans and dioxin-likepolychlorinated biphenyls from coke plants in China. Chemosphere 75, 692–695.

Lohmann, R., Breivik, K., Dachs, J., Muir, D., 2007. Global fate of POPs: current andfuture research directions. Environ. Pollut. 150, 150–165.

Long, E.R., Macdonald, D.D., Simth, S.L., Calder, F.D., 1995. Incidence of adversebiological effects within ranges of chemical concentrations in marine andestuaries sediments. Envir. Manag. 19, 81–97.

Mai, B.X., Zeng, E.Y., Luo, X.J., Yang, Q.S., Zhang, G., Li, X.D., Sheng, G.Y., Fu, J.M., 2005.Abundances, depositional fluxes, and homologue patterns of polychlorinatedbiphenyls in dated sediment cores from the Pearl River Delta. China. Environ.Sci. Technol. 39, 49–56.

Martin, M., Richardson, B.J., Lam, P.K.S., 2003. Harmonisation of polychlorinatedbiphenyl (PCB) analyses for ecotoxicological interpretations of southeastAsian environmental media: what’s the problem? Mar. Pollut. Bull. 46, 159–170.

Meng, Q., Chu, X., Xu, X., 2000. The proceeding on the environmental sorptionbehavior of polychlorobiphenys (PCBs). Chin. Sci. Bull. 45, 1572–1583 (inChinese).

Nemirovskaya, I.A., 2009. Transformation of hydrocarbons in the marginal filter ofthe Ob River. Geochemistry 429A, 1536–1541.

Oliver, B.G., Charlton, M.N., Durham, R.W., 1989. Distribution, redistribution, andgeochronology of polychlorinated biphenyl congeners and other chlorinatedhydrocarbons in Lake Ontario sediments. Environ. Sci. Technol. 23, 200–208.

Ren, N.Q., Que, M.X., Li, Y.F., Liu, Y., Wan, X.N., Xu, D.D., Sverko, E.D., Ma, J.M., 2007.Polychlorinated biphenyls in Chinese surface soils. Environ. Sci. Technol. 41,3871–3876.

Santschi, P.H., Presley, B.J., Wade, T.L., Garcia-Romero, B., Baskaran, M., 2001.Historical contamination of PAHs, PCBs, DDTs, and heavy metals in MississippiRiver Delta, Galveston Bay and Tampa Bay sediment cores. Mar. Environ. Res.52, 51–79.

Song, J.M., 2004. The Biogeochemistry of China Offshore. Technology Press, Jinan, p.591.

Sprovieri, M., Feo, M.L., Prevedello, L., Manta, D.S., Sammartino, S., Tamburrino, S.,Marsella, E., 2007. Heavy metals, polycyclic aromatic hydrocarbons andpolychlorinated biphenyls in surface sediments of the Naples harbor(southernItaly). Chemosphere 67, 98–1009.

Totten, L.A., Panangadan, M., Eisenreich, S.J., Cavallo, G.J., Fikslin, T.J., 2006. Directand indirect atmospheric deposition of PCBs to the Delaware River Watershed.Environ. Sci. Technol. 40, 2171–2176.

Tyler, A.O., Millward, G.E., 1996. Distribution and partitioning of polychlorinateddibenzo-p-dioxins, polychlorinated dibenzofurans and polychlorinatedbiphenyls in the Humber Estuary UK. Mar. Pollut. Bull. 32, 397–403.

Wang, B.C., Yu, Z.Y., Liu, C.Z., Jin, Q.X., 1980. The change of coasts and beaches andthe movement of longshore sediments of Haizhou Bay. Act. Oceanol. S. 2, 79–96(in Chinese).

Wurl, O., Obbard, J.P., 2005. Organochlorine pesticides, polychlorinated biphenylsand polybrominated diphenyl ethers in Singapore’s coastal marine sediments.Chemosphere 58, 925–933.

Xing, Y., Lu, Y., Dawson, R.W., Shi, Y., Zhang, H., Wang, T., Liu, W., Ren, H., 2005.Aspatial temporal assessment of pollution from PCBs in China. Chemosphere 60,731–739.

Yamashita, N., Kannan, K., Imagawa, T., Villeneuve, D.L., Hashimoto, S., Miyazaki, A.,Giesy, J.P., 2000. Vertical profile of polychlorinated dibenzo-p-dioxins,dibenzofurans, naphthalenes, biphenyls, polycyclic aromatic hydrocarbons,and alkylphenols in a sediment core from Tokyo Bay. Jpn. Environ. Sci.Technol. 34, 3560–3567.

Yang, H.Y., Xue, B., Jin, L.X., Zhuo, S.S., Liu, W.P., 2011. Polychlorinated biphenyls insurface sediments of Yueqing Bay, Xiangshan Bay, and Sanmen Bay in EastChina Sea. Chemosphere 83, 137–143.

Yang, H.Y., Zhuo, S.S., Xue, B., Zhang, C.L., Liu, W.P., 2012. Distribution, historicaltrends and inventories of polychlorinated biphenyls in sediments from YangtzeRiver Estuary and adjacent East China Sea. Environ. Pollut. 169, 20–26.

Yuan, D., Yang, D., Wade, T.L., Qian, Y., 2001. Status of persistent organic pollutantsin the sediment from several estuaries in China. Environ. Pollut. 114, 101–111.

Zhang, Z.L., Hong, H.S., Zhou, J.L., Huang, J., Yu, G., 2003. Fate and assessment ofpersistent organic pollutants in water and sediment from Minjiang RiverEstuary, Southeast China. Chemosphere 52, 1423–1430.

Zhang, P., Song, J.M., Liu, Z.G., Zheng, G.X., Zhang, N.X., He, Z.P., 2007. PCBs and itscoupling with eco-environments in Southern Yellow Sea surface sediments.Mar. Pollut. Bull. 54, 1105–1115.

Zhang, Z., Liu, L.Y., Li, Y.F., Wang, D.G., Jia, H.L., Harner, T., Sverko, E., Wan, X.N., Xu,D.D., Ren, N.Q., Ma, J.M., Pozo, K., 2008. Analysis of polychlorinatedbiphenyls inconcurrently sampled Chinese air and surface soil. Environ. Sci. Technol. 42,6514–6518.

Zhang, R., Zhou, L., Zhang, F., Ding, Y.J., Gao, J.R., Chen, J., Yan, H.Q., Shao, W., 2013a.Heavy metal pollution and assessment in the tidal flat sediments of HaizhouBay, China. Mar. Pollut. Bull. 74, 403–412.

Zhang, R., Zhang, F., Zhang, T.C., 2013b. Sedimentary records of PAHs in a sedimentcore from tidal flat of Haizhou Bay, China. Sci. Total Environ. 450–451, 280–288.

Zhou, J.L., Maskaoui, K., Qiu, Y.W., Hong, H.S., Wang, Z.D., 2001. Polychlorinatedbiphenyl congeners and organochlorine insecticides in the water column andsediments of Daya Bay, China. Environ. Pollut. 113, 373–384.