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The effect of mangrove reforestation on the accumulation of PCBs in sediment from different habitats in Guangdong, China Bo Zhao a,b , Yan-wu Zhou a,c , Gui-zhu Chen a,a School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou 510275, China b South China Institute of Environmental Science, Ministry of Environmental Protection, No.7 West Street, Yuancun, Guangzhou 510655, China c Marine Environmental Engineering Center, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China article info Keywords: Mangrove reforestation Sediments Polychlorinated biphenyls abstract To investigate the influence of mangrove reforestation on the accumulation of PCBs, the concentrations and homologue patterns of polychlorinated biphenyls in surface sediments from different mangrove for- ests and their adjacent mud flats in Guangdong Province were determined. The total PCB concentrations in the sediments ranged from 3.03 to 46.62 ng g À1 (dry weight). Differences in the accumulation and dis- tribution of PCBs were found between the mangrove sites and the mud flats. Furthermore, the natural forests and restored mangrove forests of native species showed slight PCB contamination, whereas the exotic species Sonneratia apetala exacerbated the PCB pollution at certain sites. It was suggested that the native mangrove species Kandelia candel and Aegiceras corniculatum could represent good choices for the phytoremediation of PCB contamination. Ó 2012 Elsevier Ltd. All rights reserved. 1. Introduction The polychlorinated biphenyls (PCBs) include 209 congeners and consist of a biphenyl group in which one to ten hydrogen atoms have been replaced by chlorine atoms. They are useful be- cause of their chemical properties of low vapor pressure, low water solubility, low reactivity, low degradability and high dielectric con- stants (Shui and Mackay, 1986). Although PCBs have useful proper- ties as industrial materials, they have been banned worldwide since the 1970s because they cause cancer, immunotoxic responses and reproductive disorders. Because of their lipophilic nature, hydrophobicity and low chemical and biological degradation rates, PCBs accumulate in biological tissues and subsequently concen- trate toward the top of the food chain (Guzzella et al., 2005). Along the coastlines of tropical and subtropical regions, the mangrove forest is one of the most productive ecosystems in the world, and it provides food sources and diverse habitats for large numbers of resident and migratory organisms. Economic and demographic developments have produced widespread overex- ploitation of the world’s mangrove forests despite their ecological importance and additional significance (FAO, 2003). Similarly, mangrove forests in China declined from the 1950s to the 1990s. To overcome these losses, China began to restore the mangrove forest and has achieved good success in south China (Wang and Wang, 2007). Rather than restoring native mangrove species, the Chinese government preferred to plant the exotic species Sonneratia apetala. This species was introduced from Bangladesh in 1985 and is well known for its rapid growth. At least 2300 ha of S. apetala forest have been planted since 1991 (Ren et al., 2009). Mangrove ecosystems are characterized by unique properties: they exhibit anaerobic conditions, and they are rich in organic mat- ter and sulfide. Pollutants from inland freshwater drainage and ti- dal flushing tend to retain and accumulate in mangrove sediments (Tam and Wong, 1995, 2000; Harbison, 1996; Tam et al., 1997, 2001). Therefore, pollution in mangrove forests is likely to reach beyond the resident species of the forests and might also affect fish species that use mangroves as a temporary habitat (Kruitwagen et al., 2006). Nevertheless, there are only a few studies on the pol- lution and distribution of trace-level persistent organic pollutants (POPs), such as PCBs, in the sediments of mangrove forests (Liang et al., 1999; Zheng et al., 2000; Tam and Yao, 2002; Kruitwagen et al., 2006; Souza et al., 2008; Vane et al., 2009; Binelli et al., 2009). Furthermore, although more than one-half of the total man- grove forests in China were restored (Ren et al., 2010), no studies of the influence of mangrove reforestation on PCB pollution in sedi- ments have been conducted. Our previous study clarified the influence of mangrove refores- tation on heavy metal accumulation and speciation in intertidal sediments (Zhou et al., 2010). In this study, restored mangrove for- ests from additional habitats were examined to investigate the influence of mangrove reforestation on the accumulation of PCBs by comparing restored forests with natural mangrove forests and mud flats. The concentration and distribution of PCBs in mangrove 0025-326X/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marpolbul.2012.05.029 Corresponding author. Tel./fax: +86 20 84039737. E-mail address: [email protected] (G.-z. Chen). Marine Pollution Bulletin 64 (2012) 1614–1619 Contents lists available at SciVerse ScienceDirect Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

The effect of mangrove reforestation on the accumulation of PCBs in sediment from different habitats in Guangdong, China

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Page 1: The effect of mangrove reforestation on the accumulation of PCBs in sediment from different habitats in Guangdong, China

Marine Pollution Bulletin 64 (2012) 1614–1619

Contents lists available at SciVerse ScienceDirect

Marine Pollution Bulletin

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

The effect of mangrove reforestation on the accumulation of PCBs in sedimentfrom different habitats in Guangdong, China

Bo Zhao a,b, Yan-wu Zhou a,c, Gui-zhu Chen a,⇑a School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou 510275, Chinab South China Institute of Environmental Science, Ministry of Environmental Protection, No.7 West Street, Yuancun, Guangzhou 510655, Chinac Marine Environmental Engineering Center, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China

a r t i c l e i n f o

Keywords:Mangrove reforestationSedimentsPolychlorinated biphenyls

0025-326X/$ - see front matter � 2012 Elsevier Ltd.http://dx.doi.org/10.1016/j.marpolbul.2012.05.029

⇑ Corresponding author. Tel./fax: +86 20 84039737E-mail address: [email protected] (G.-z. Chen)

a b s t r a c t

To investigate the influence of mangrove reforestation on the accumulation of PCBs, the concentrationsand homologue patterns of polychlorinated biphenyls in surface sediments from different mangrove for-ests and their adjacent mud flats in Guangdong Province were determined. The total PCB concentrationsin the sediments ranged from 3.03 to 46.62 ng g�1 (dry weight). Differences in the accumulation and dis-tribution of PCBs were found between the mangrove sites and the mud flats. Furthermore, the naturalforests and restored mangrove forests of native species showed slight PCB contamination, whereas theexotic species Sonneratia apetala exacerbated the PCB pollution at certain sites. It was suggested thatthe native mangrove species Kandelia candel and Aegiceras corniculatum could represent good choicesfor the phytoremediation of PCB contamination.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

The polychlorinated biphenyls (PCBs) include 209 congenersand consist of a biphenyl group in which one to ten hydrogenatoms have been replaced by chlorine atoms. They are useful be-cause of their chemical properties of low vapor pressure, low watersolubility, low reactivity, low degradability and high dielectric con-stants (Shui and Mackay, 1986). Although PCBs have useful proper-ties as industrial materials, they have been banned worldwidesince the 1970s because they cause cancer, immunotoxic responsesand reproductive disorders. Because of their lipophilic nature,hydrophobicity and low chemical and biological degradation rates,PCBs accumulate in biological tissues and subsequently concen-trate toward the top of the food chain (Guzzella et al., 2005).

Along the coastlines of tropical and subtropical regions, themangrove forest is one of the most productive ecosystems in theworld, and it provides food sources and diverse habitats for largenumbers of resident and migratory organisms. Economic anddemographic developments have produced widespread overex-ploitation of the world’s mangrove forests despite their ecologicalimportance and additional significance (FAO, 2003). Similarly,mangrove forests in China declined from the 1950s to the 1990s.To overcome these losses, China began to restore the mangroveforest and has achieved good success in south China (Wang andWang, 2007). Rather than restoring native mangrove species, the

All rights reserved.

..

Chinese government preferred to plant the exotic speciesSonneratia apetala. This species was introduced from Bangladeshin 1985 and is well known for its rapid growth. At least 2300 haof S. apetala forest have been planted since 1991 (Ren et al., 2009).

Mangrove ecosystems are characterized by unique properties:they exhibit anaerobic conditions, and they are rich in organic mat-ter and sulfide. Pollutants from inland freshwater drainage and ti-dal flushing tend to retain and accumulate in mangrove sediments(Tam and Wong, 1995, 2000; Harbison, 1996; Tam et al., 1997,2001). Therefore, pollution in mangrove forests is likely to reachbeyond the resident species of the forests and might also affect fishspecies that use mangroves as a temporary habitat (Kruitwagenet al., 2006). Nevertheless, there are only a few studies on the pol-lution and distribution of trace-level persistent organic pollutants(POPs), such as PCBs, in the sediments of mangrove forests (Lianget al., 1999; Zheng et al., 2000; Tam and Yao, 2002; Kruitwagenet al., 2006; Souza et al., 2008; Vane et al., 2009; Binelli et al.,2009). Furthermore, although more than one-half of the total man-grove forests in China were restored (Ren et al., 2010), no studies ofthe influence of mangrove reforestation on PCB pollution in sedi-ments have been conducted.

Our previous study clarified the influence of mangrove refores-tation on heavy metal accumulation and speciation in intertidalsediments (Zhou et al., 2010). In this study, restored mangrove for-ests from additional habitats were examined to investigate theinfluence of mangrove reforestation on the accumulation of PCBsby comparing restored forests with natural mangrove forests andmud flats. The concentration and distribution of PCBs in mangrove

Page 2: The effect of mangrove reforestation on the accumulation of PCBs in sediment from different habitats in Guangdong, China

B. Zhao et al. / Marine Pollution Bulletin 64 (2012) 1614–1619 1615

sediments were determined. Furthermore, the discrepancy be-tween exotic and native mangrove species in South China in theaccumulation of PCBs was clarified to address the many previousarguments about the exotic species S. apetala.

2. Materials and methods

2.1. Site description

The mangrove forests examined in this study are located inthree special economic zones, Zhuhai, Shantou and Shenzhen, inGuangdong Province, China. These plantations of mangroves wereestablished in island, estuary and aquaculture pond habitats inZhuhai, Shantou and Shenzhen, respectively. The rapid develop-ment of industry and the economy in these areas led to seriousenvironmental pollution, and all of the study sites are located nearpotential hot spots for PCBs. The restored mangrove forests in Zhu-hai and Shantou have grown for more than 15 years, and the nat-ural forests have grown for more than 30 years. In contrast, therestored mangrove forests in Shenzhen are only 2 years old. Inall, seven mangrove species are included in this study: Sonneratiaapetala, Kandelia obovata, Pongamia pinnata, Aegiceras corniculatum,Acanthus ilicifolius, Avicennia marina and Bruguiera gymnorrhiza. Adetailed description of the sampling stations is given in Table 1.

2.2. Sample collection

Five surface (5 cm) sediment samples (in duplicate) were col-lected from each of the mangrove sites and then mixed. The sam-ples were wrapped in aluminum foil and sealed in polyethylenebags for transport to the shore, where they were immediatelystored in a freezer. The sediment samples were air-dried at roomtemperature and sieved through 2 mm mesh.

2.3. Analytical procedure

The samples were extracted with microwave-assisted extrac-tion (MAE), purified on chromatographic columns and determinedwith combined gas chromatography–mass spectrometry (GC–MS).

The analytical methods followed those described in US EPAMethod 3245 (2007a) and Xiong et al. (2000), with several modifi-cations. Briefly, a 5 g sediment sample was accurately weighed andtransferred into a PTFE-lined vessel. In addition, 2,4,5,6-tetrachloro-m-xylene was added as the recovery reference stan-dard, and 15 mL n-hexane and 15 mL methanolic 1 M KOH solutionwere added to the vessel. The extraction was performed in a micro-wave at 110 �C with a heating time of 15 min. Upon completion ofthe extraction, the vessels were cooled to room temperature. The

Table 1Description of the sampling stations in this study.

Stations Mangrove species Forest type Location

ZH1 Mud flat None Qi’ao Island, ZhZH2 S. apetala PlantationZH3 K. obovata and P. pinnata Natural mingled forestZH4 A. corniculatum and A. ilicifolius Natural mingled forest

ST1 Mud flat None Su’ai wan, ShanST2 A. corniculatum and A. marina Natural mingled forest

ST3 Mud flat None Yifeng estuary,ST4 K. obovata PlantationST5 S. apetala Plantation

SZ1 Mud flat None Aquaculture poSZ2 K. obovata PlantationSZ3 B. gymnorrhiza PlantationSZ4 A. corniculatum Plantation

extract was filtered through glass fiber filters and then concen-trated with a rotary evaporator. The sample cleanup of the extractswas performed by elution through chromatographic columnspacked with 3% water-deactivated silica gel, florisil and basic alu-mina. Pentachloronitrobenzene (PCNB) was then added as theinternal standard. The volume was eventually reduced to approxi-mately 200 lL with a gentle stream of nitrogen gas. The target ana-lytes included 19 individual PCBs (IUPAC Nos. 1, 5, 18, 31, 44, 52,66, 87, 101,110, 138, 141, 151, 153, 170, 180, 183, 187, 206) listedin EPA Method 8082. All of the standards and solvents were pur-chased from J & K CHEMICAL, USA.

The procedures for the identification and quantification of PCBcongeners were modified from the US EPA Method 8275 (1996)and US EPA Method 8082 (2007b). Combined gas chromatogra-phy–mass spectrometry (GC–MS) was performed on a ThermoTrace GC Ultra-DSQ, and the DSQ was operated in the selected-ion monitoring (SIM) mode for the quantification of target PCBs.The GC was fitted with a fused silica TR-5MS capillary column(30 m � 0.25 mm � 0.25 lm). The GC oven was temperature-pro-grammed from 100 �C (2 min isothermal) to 180 �C (at 15 �C/min.) to 240 �C (at 3 �C/min) to 285 �C (at 10 �C/min) and held iso-thermally at 285 �C for 10 min. Helium was used as a carrier gas ata constant flow of l mL min�1.

The percentage of organic matter in the surface sediments wasmeasured with the potassium dichromate oxidation method (GB,9834–88).

2.4. Quality control and quality assurance

For each batch of 15 field samples, a method blank, a spikedblank, a matrix spiked sample, and sample duplicates were pro-cessed to monitor the precision and reliability of the analytical re-sults. The blank samples contained no detectable amounts of thetarget analytes, and the spiked sample recoveries ranged from75.4% to 105.3%. The limit of detection in the present study wasestimated as 0.16 ng g�1 for PCBs based on the matrix spiked massplus five standard deviations.

3. Results

The concentrations and distributions of individual PCB congen-ers as well as the organic content in the surface sediments of themangrove forests and the mud flat are summarized in Table 2.The homologue levels and patterns of PCBs are shown in Table 3and Fig. 1.

According to Table 2, the concentrations of total PCBs in thesediments (19 congeners) ranged from 13.68 to 41.33 ng g�1 inZhuhai, 3.03 to 24.62 ng g�1 in Shantou, and 22.25 to 46.62 ng g�1

Station description

uhai This island is located in the Pearl River estuary

tou It is located in the south outskirt of Shantou

Shantou It is located in the mouth of Yifeng river

nds, Shenzhen It is located in the industrial area of Baoan district of Shenzhen

Page 3: The effect of mangrove reforestation on the accumulation of PCBs in sediment from different habitats in Guangdong, China

Table 2PCB congeners levels (ng g�1-dw) and organic content (%) in sediments of mangrove forests and mud flat.

ZH1 ZH2 ZH3 ZH4 ST1 ST2 ST3 ST4 ST5 SZ1 SZ2 SZ3 SZ4

PCB1 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D.PCB5 10.50 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D.PCB18 N.D. 2.99 N.D. 0.19 0.28 N.D. 0.35 N.D. N.D. 3.64 3.18 3.58 3.36PCB31 1.42 3.91 1.01 1.41 1.56 0.19 1.88 0.39 1.18 2.99 2.31 2.47 2.89PCB52 0.86 2.66 0.86 1.10 1.40 0.05 2.21 0.40 1.43 10.59 1.52 3.50 1.68PCB44 1.70 2.61 1.04 1.58 1.01 0.05 2.43 0.61 1.13 2.84 1.80 1.54 2.10PCB66 1.48 2.61 1.10 1.30 1.20 0.23 2.39 0.84 1.57 7.54 1.35 1.54 1.87PCB101 2.04 2.37 1.05 0.77 0.92 0.32 1.63 0.60 1.27 0.67 0.60 0.50 0.60PCB87 1.11 2.15 0.87 0.71 0.82 0.12 1.39 0.46 1.04 0.99 0.61 0.66 0.78PCB110 1.65 1.89 0.60 0.59 0.88 N.D. 1.41 0.66 1.04 0.78 0.77 0.63 0.92PCB151 1.06 1.60 0.11 0.36 0.16 N.D. 0.80 0.03 0.44 1.57 0.76 0.56 1.21PCB153 0.24 1.65 0.23 N.D. 0.51 N.D. 0.45 0.14 0.44 1.02 0.93 0.84 1.63PCB141 0.27 2.15 1.11 0.66 1.02 0.13 1.44 0.83 1.00 2.22 1.55 1.68 2.17PCB137 N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. N.D. 1.90 0.83 1.04 1.40PCB187 0.36 2.91 1.66 0.96 1.01 0.22 1.59 1.50 1.40 1.83 1.08 1.35 1.59PCB183 0.85 2.91 1.66 0.99 1.40 0.11 1.55 1.21 1.55 1.85 1.09 1.34 1.52PCB180 1.02 3.19 1.85 1.50 1.94 0.53 1.98 2.20 1.97 1.96 1.09 1.32 1.76PCB170 1.37 3.84 1.98 1.35 2.08 0.50 2.23 2.04 2.06 1.70 1.18 1.05 1.53PCB206 0.04 1.88 0.87 0.21 0.96 0.58 0.87 1.50 0.91 2.53 1.60 1.33 2.15P

PCBs 25.98 41.33 15.97 13.68 17.15 3.03 24.62 13.42 18.43 46.62 22.25 24.93 29.16OC 1.37 6.19 8.90 1.78 2.80 2.73 2.49 2.24 3.40 2.30 1.04 1.46 0.99

N.D.: Not detected

Table 3PCB homologues levels (ng g�1-dw) in the sediments of mangrove forests and mud flat.

ZH1 ZH2 ZH3 ZH4 ST1 ST2 ST3 ST4 ST5 SZ1 SZ2 SZ3 SZ4

Di- 10.50 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00Tri- 1.42 6.90 1.01 1.61 1.84 0.19 2.23 0.39 1.18 6.63 5.49 6.05 6.25Tetra- 4.03 7.89 2.99 3.98 3.62 0.32 7.04 1.84 4.13 20.96 4.67 6.57 5.65Penta- 4.80 6.41 2.51 2.07 2.62 0.45 4.43 1.72 3.36 2.45 1.98 1.79 2.30Hexa- 1.58 5.40 1.44 1.02 1.69 0.13 2.69 1.00 1.88 6.72 4.07 4.13 6.41Hepta- 3.60 12.86 7.15 4.80 6.43 1.37 7.35 6.96 6.98 7.34 4.45 5.06 6.40Nano- 0.04 1.88 0.87 0.21 0.96 0.58 0.87 1.50 0.91 2.53 1.60 1.33 2.15

Fig. 1. Homologue patterns of PCBs in surface sediments of mangrove forests and mud flat surface sediments.

1616 B. Zhao et al. / Marine Pollution Bulletin 64 (2012) 1614–1619

in Shenzhen. The sites with the lowest level of contamination werefound in the natural mangrove forests in Zhuhai and Shantou, andthe sites with the highest contamination were found in the mudflats in Shantou and Shenzhen. An interesting result was that thehighest concentration of total PCBs was found at site ZH2 in Zhu-hai. S. apetala was the only species that was used for restorationfor a 15 year period at this site. The occurrence of the highest con-centration of total PCBs at this site indicated that S. apetala exacer-bated the pollution caused by PCBs (Table 4).

The concentrations of low- and moderately chlorinatedbiphenyls, such as di- to hexachlorinated homologues, in the

sediments were higher at site ZH1 than at sites ZH3 and ZH4,whereas the concentrations of highly chlorinated biphenyls, suchas hepta- and nanochlorinated homologues, at site ZH1 were lowerthan those at sites ZH3 and ZH4. A similar distribution pattern wasobserved at sites ST3, ST4 and ST5. These results suggested that thedistributions of PCB homologues in the mangrove forests and themud flats were very different. The results indicated that the mudflats tended to accumulate the low- and moderately chlorinatedbiphenyls, whereas the mangrove forests accumulated the highlychlorinated biphenyls more easily. However, obvious differenceswere found at site ZH2 and at the sites in Shenzhen. It is probable

Page 4: The effect of mangrove reforestation on the accumulation of PCBs in sediment from different habitats in Guangdong, China

Table 4Polychlorinated biphenyls pollution levels in marine sediments of nearby sites and other mangrove sediments.

Location Sampling yearP

PCBs conc. (ng/g, dw) References

Xiamen Harbour 1995 0.05–7.24 Hong et al. (1995)Pearl River Delta 1997 11.5–485 Kang et al. (2000)Macau 1997 12.5–339 Kang et al. (2000)Victoria Harbour, Hongkong 1999 25.0–97.9 Richardson and Zheng (1999)Pearl River estuary 2000 11.13–23.23 Nie et al. (2005)Gaoping River, Taiwan 2000 0.38–5.89 Doong et al. (2008)Pearl River Delta 2003 6.01–287.67 Fung et al. (2005)Mai Po marshes nature reserve of Hong Kong 2000 4.9–27.6 Zheng et al. (2000)Mangroves of Hong Kong 2002 0.1–25.1 Tam and Yao (2002)Mangroves of Guanabara Bay, Brazil 2003–2004 17.83–184.16 Souza et al. (2008)Mangroves of Tanzania 2003–2005 N.D.–3.65 Kruitwagen et al. (2006)Mangroves of South China 2006 2.2–6.0 Vane et al. (2009)Sunderban mangrove wetland of N.E.India 2009 0.5–26.9 Binelli et al. (2009)Mangroves of Guangdong 2009–2010 3.03–46.62 This research

The locations of boldface are mangrove forests.

Fig. 2. Correlation between PCBs concentrations and organic carbon contents.

B. Zhao et al. / Marine Pollution Bulletin 64 (2012) 1614–1619 1617

that S. apetala aggravated the pollution resulting from almost all ofthe PCBs. Note also that the mangrove forests were established inShenzhen only 2 years ago.

The compositions of the homologues in the sediments were gen-erally similar to the industrial mixture Aroclor 1254, which includedtetra-, penta-, hexa- and heptachlorinated biphenyls. This resultwas consistent with the findings of previous studies in this SouthChina area (Hong et al., 1999; Kang et al., 2000; Nie et al., 2005).

The PCB congeners identified in the sediments from the Zhuhaisites were predominantly moderately chlorinated and high-chlori-nated, i.e., tetra- and heptachlorinated, except for site ZH1, atwhich the predominant homologues were low-chlorinated ordichlorinated. A similar situation was observed at the Shantousites. At the Shenzhen sites, the predominant homologues of PCBswere tri- and tetrachlorinated. Generally, higher proportions ofhigh-chlorinated congeners were observed in places farther fromdirect pollutant sources, where precipitation was the principalsource and distribution pathway of the PCBs (Goerke and Weber,1998). Therefore, it could be concluded that the sources of PCB pol-lution were far from the study sites in Zhuhai and Shantou andnear the study sites in Shenzhen.

Because of their lipophilic nature and hydrophobicity, PCBshave an affinity for particles in certain mangrove sediments thatare rich in organic carbon (Tam and Yao, 2002). Nevertheless, thedirect correlation between PCB concentrations and organic carbon

content was weak in this study, as shown in Fig. 2. For example,site SZ1 showed the highest concentration of PCBs but exhibitedan organic carbon content of only 2.3%. In contrast, the concentra-tion of PCBs at site ZH3 was not high, whereas the organic carboncontent was significantly high. These values may be influenced byother accumulation factors, such as the grain size and the differentaccumulation patterns of PCBs for the mangrove sediments and themud flat. In particular, the mangrove sediment accumulated thehigh-chlorinated biphenyls more easily, whereas the mud flattended to accumulate the low- and moderately chlorinatedbiphenyls.

The levels of total PCBs in mangrove sediments (except site ZH1,46.62 ng/g, dw) in this study were comparable with those obtainedfrom the Pearl River estuary and other mangrove forests from HongKong and N.E. India, higher than those found in Tanzania and otherSouth China mangroves, and lower than those found in Brazil.These comparisons indicate that the surface sediments in thisstudy appeared to be slightly contaminated by PCBs.

Vane et al. (2009) reported contamination by PCBs in surfacemangrove sediments in South China. However, they found a levelof contamination much lower than that obtained in this study. Itis possible that this difference resulted because the sampling sitesinvestigated by the present study were all located in more heavilyindustrialized regions. These regions may exhibit more serious pol-lution by PCBs.

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1618 B. Zhao et al. / Marine Pollution Bulletin 64 (2012) 1614–1619

4. Discussion

4.1. The rehabilitation of mangrove forest

Few studies have addressed the environmental and ecologicalinfluences of mangrove reforestation. Reforestation has been foundto change the physico-chemical conditions of the reforested sites(McKee and Faulkner, 2000; Bosire et al., 2003) and could facilitatenatural colonization by mangroves, primarily by altering localhydrodynamics and other physico-chemical factors (Bosire et al.,2003). It is reported that mangrove reforestation could also en-hance litter degradation and concomitant nutrient remineraliza-tion (Bosire et al., 2005). A previous study also showed that thefine particle and organic matter content increased and the accumu-lation of heavy metals in the upper sediment layers was facilitatedafter mangrove reforestation (Zhou et al., 2010).

In this study, the natural mangrove forests showed slight PCBpollution. This finding suggested that the forests could preventthe PCB contamination of sediments or rehabilitate an environ-ment contaminated with PCBs. This conclusion was the same asthat of a previous study in Hong Kong (Tam et al., 2001; Zhenget al., 2000). The reforestation of native mangrove species playeda similar role in these sites. It was suggested that the concentrationand distribution of PCBs in the surface sediments could be influ-enced by mangrove reforestation in different habitats. In addition,different mangrove species accumulated markedly differentamounts of PCBs. Clearly, the native mangrove species K. obovataand A. corniculatum were effective in the rehabilitation of differenthabitats. This result indicated that these native species should berestored along most of the contaminated coastline of South China.

Furthermore, previous simulation experiments showed that K.candel and A. corniculatum could remediate PCB-contaminated sed-iments through phytoextraction by the root system (Liu, 2006) andbioremediation of indigenous microbes (Sun, 2007). These rehabil-itation mechanisms could remediate PCB pollution in the man-grove forests investigated in this study.

4.2. The arguments about reforestation with S. apetala

In contrast to the remediation effects of native species, the exo-tic species S. apetala exacerbated the pollution of PCBs in certainhabitats, such as the island. This difference may result from differ-ent hydrological and geographic characteristics. Furthermore, sed-iments may affect aquatic organisms by acting as a secondarysource of contaminants. The contamination of the sediment byPCBs may then change the morphology and growth of the strictlymangrove-resident species (Kruitwagen et al., 2006).

There are many critical arguments about the ecological effectsof S. apetala reforestation. For example, certain studies suggestedthat S. apetala could greatly improve the soil fertility and act as apioneer restoration species (Pan et al., 2006; Wang and Wang,2007; Ren et al., 2009). However, the overgrowth of this speciesand its great ability to spread eventually affected the structureand function of the local mangrove ecosystem. As a consequence,S. apetala was even listed as an invasive exotic species (Wanget al., 2004; Liao et al., 2004; Ren et al., 2008, 2009). In this study,S. apetala was compared with natural mangrove forests and refor-ested native species. Both of these comparisons indicated that itwas not desirable to reforest the contaminated coastline with S.apetala.

4.3. The benefit of reforestation with mixed-species mangrove forests

Despite the small possibility of restoring full ecosystemfunction, most mangrove reforestation involved monospecific

rehabilitation (Lewis, 2005) because this approach offered highcash-crop value and easier planting (Kelty, 2006). This restorationpattern may also reduce the ability of the forest to phytoremediatePCBs. As Table 2 shows, the lowest concentrations of certain PCBcongeners at the Shenzhen sites occurred at SZ2 (e.g., the congen-ers PCB18 and PCB52) and at SZ3 (e.g., PCB110 and PCB153). Thisresult may suggest that the PCB phytoremediation abilities of dif-ferent mangrove species differ substantially. However, other fac-tors, such as differences between the original concentrations ofPCBs, may also have affected the outcome. If differences betweenthe original concentrations of PCBs are not involved, reforestationwith mixed-species mangrove forests could represent the best ap-proach to phytoremediation.

5. Conclusions

The concentrations of PCBs in the surface sediments collectedfrom 13 sites in this study ranged from 3.03 to 46.62 ng g�1 drywt. Clear differences in the concentrations and homologue patternsof the PCBs between the mangrove sediments and the mud flatswere observed. The differences in the homologue patterns at theShenzhen sites were not clear. This result may be a consequenceof the very recent restoration of mangroves at these sites. It canbe hypothesized that both the natural mangrove forests and thereforestation of native mangrove species could alter the accumula-tion and distribution of PCBs in sediments. Furthermore, the nativemangrove species K. candel and A. corniculatum could representgood choices for the phytoremediation of PCBs. However, the com-monly restored mangrove species S. apetala exacerbated pollutionby PCBs at Zhuhai, Qi’ao Island. This result indicates that this exoticspecies should not be used for the restoration of the contaminatedcoastline.

Acknowledgments

This research was supported by the United Nations Environ-ment Programme/Global Environment Facility (UNEP/GEF) (No.GF/2010-07-03).

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