Ecotoxicology and Environmental Safety 104 (2014) 143–151

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Ecological risk and pollution history of heavy metals in Nansha mangrove, South China Qihang Wu a,b,c,n, Nora F.Y. Tam c, Jonathan Y.S. Leung c, Xizhen Zhou d, Jie Fu e, Bo Yao a, Xuexia Huang a, Lihua Xia d a

School of Environmental Science and Engineering, Guangzhou University, Guangzhou 510006, China Key Laboratory of Water Quality Safety and Protection in Pearl River Delta, Ministry of Education, Guangzhou University, Guangzhou 510006, China c Department of Biology and Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China d School of Geographical Sciences, Guangzhou University, Guangzhou 510006, China e Department of Civil Engineering, Auburn University, Auburn, AL 36849, United States b

art ic l e i nf o

a b s t r a c t

Article history: Received 15 October 2013 Received in revised form 26 January 2014 Accepted 20 February 2014

Owing to the Industrial Revolution in the late 1970s, heavy metal pollution has been regarded as a serious threat to mangrove ecosystems in the region of the Pearl River Estuary, potentially affecting human health. The present study attempted to characterize the ecological risk of heavy metals (Cd, Cr, Cu, Mn, Ni, Pb and Zn) in Nansha mangrove, South China, by estimating their concentrations in the surface sediment. In addition, the pollution history of heavy metals was examined by determining the concentrations of heavy metals along the depth gradient. The phytoremediation potential of heavy metals by the dominant plants in Nansha mangrove, namely Sonneratia apetala and Cyperus malaccensis, was also studied. Results found that the surface sediment was severely contaminated with heavy metals, probably due to the discharge of industrial sewage into the Pearl River Estuary. Spatial variation of heavy metals was generally unobvious. The ecological risk of heavy metals was very high, largely due to Cd contamination. All heavy metals, except Mn, decreased with depth, indicating that heavy metal pollution has been deteriorating since 1979. Worse still, the dominant plants in Nansha mangrove had limited capability to remove the heavy metals from sediment. Therefore, we propose that immediate actions, such as regulation of discharge standards of industrial sewage, should be taken by the authorities concerned to mitigate the ecological risk posed by heavy metals. & 2014 Elsevier Inc. All rights reserved.

Keywords: Ecological risk assessment Heavy metal Pollution Mangrove Sediment Phytoremediation

1. Introduction Mangroves, which are distributed in the intertidal zone within circumtropical regions, provide various ecological services and sustain the integrity of coastal areas (Robertson and Duke, 1987; Harty, 1997; Krauss et al., 2008). Unfortunately, they have been globally menaced by urbanization and industrialization that their total area has been dwindling over the last few decades (Alongi, 2002; Bosire et al., 2008). In South China, for example, the health and integrity of mangroves are aggravated due to substantial discharge of industrial sewage into the Pearl River Estuary (PRE) from the coastal cities (Chen et al., 2006; Chen et al., 2013). It is estimated that the annual amount of industrial sewage has reached approximately 200 million tons (Chen et al., 2006). Among different types of pollutants in the sewage, heavy metals n Corresponding author at: School of Environmental Science and Engineering, Guangzhou University, Guangzhou 510006, China. Tel.: 86 20 39366945; fax: þ86 20 39366946. E-mail address: [email protected] (Q. Wu).

http://dx.doi.org/10.1016/j.ecoenv.2014.02.017 0147-6513 & 2014 Elsevier Inc. All rights reserved.

are of special concern since alarming levels of cadmium, lead and zinc were annually discharged into the Pearl River (Li et al., 2006), potentially causing far-reaching ramifications on human health and ecosystems. Since sediment in coastal areas is generally regarded as the primary sink for heavy metals (Montouris et al., 2002), it is surmised that heavy metals have insidious effects on mangrove ecosystems due to their toxicity, non-biodegradability and potential to bioaccumulation (Chaudhuri et al., 2014; Nath et al., 2013; Usman et al., 2013). Therefore, monitoring and assessment of heavy metals in sediment should be launched regularly to evaluate their ecological risk. To do so, a classical method is to calculate the potential ecological risk index (Hakanson, 1980), in which the concentrations of heavy metals in the study site are compared to those in the reference site (i.e. background level). For better monitoring and assessment, however, understanding the historical or pre-anthropogenic record of heavy metal pollution is also important. The pollution history of heavy metals can be reflected by the depth of sediment as long as the sedimentation rate is known (Abrahim and Parker, 2008; Rezaee et al., 2010; Liu et al., 2011). Elucidating the spatial and

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temporal variations of heavy metals in sediment can offer precious information for policy makers or environmentalists to manage mangrove habitats more effectively. To combat moderate level of heavy metal pollution in mangrove habitats, phytoremediation has been recommended in view of its eco-friendliness and cost-effectiveness (reviewed by Cheng, 2003; Weis and Weis, 2004). While many heavy metals, such as Pb, in the anoxic sediment are often not readily bioavailable, plants can remobilize them and hence promote their bioavailability (De Lacerda et al., 1993), through oxidation by aerenchyma tissues of roots (Moorhead and Reddy, 1988) or acidification by plant exudates (Doyle and Otte, 1997). Consequently, the remobilized heavy metals can be removed by plants through various processes such as phytoextraction (reviewed by Ali et al., 2013). The plants are then harvested to prevent heavy metals from reentering into the sediment when they have accumulated certain amount of heavy metals in their tissues. Nevertheless, plants cannot ad infinitum extract heavy metals from sediment because pernicious effects would be incurred if their threshold tolerance value is exceeded. In this regard, suitable candidates for phytoremediation of heavy metals should have high tolerance, accumulation capability, growth rate and above-ground biomass (reviewed by Ali et al., 2013). In the present study, the spatial and temporal variations of heavy metals in the sediment in Nansha mangrove, the second largest mangrove forest in the region of the PRE, were examined to characterize the ecological risk and pollution history of heavy metals, respectively. Moreover, the concentrations of heavy metals accumulated in different dominant plants in Nansha mangrove were measured to estimate their phytoremediation potential. The findings could shed light on the degree of heavy metal pollution in the PRE as well as provide crucial information for monitoring, management and conservation of coastal environments.

2.3. Heavy metal analysis of sediment and plant samples The sediment samples were freeze-dried, ground into powder and passed through a 2 mm sieve. To extract the heavy metals, 0.3 g sediment sample was digested by a mixture of concentrated hydrochloric acid (HCl) and nitric acid (HNO3) (3:1, v/v) using microwave digestion method. As for plant samples, the roots were rinsed with deionized water and immersed in 20 mmol l  1 Na2-EDTA for 20 min to remove the aluminum adhered on the surface. The plant samples were then dried in an oven at 80 1C for 72 h. 0.3 g plant sample, which was powdered using an agate mill, was digested by a mixture of concentrated HNO3 and perchloric acid (HClO4) (4:1, v/v). The concentrations of heavy metals in the extract, namely chromium (Cr), copper (Cu), manganese (Mn), nickel (Ni), lead (Pb) and zinc (Zn), were determined by inductively coupled plasma-optima emission spectrometry (ICP-OES, Optima 5300DV, Perkin-Elmer Instruments, USA), while cadmium (Cd) was determined by an atomic absorption spectrometer (AAnalyst 800, Perkin-Elmer Instruments, USA). To estimate the accuracy of this method, a certified reference material from the State Oceanic Administration of China (GBW 07334) was used for recovery test. The recoveries for all the metals ranged from 90% to 97% (RSD: 3.81–5.75%). 2.4. Statistical analyses The potential ecological risk coefficient (Eir Þ was calculated to evaluate the ecological risk of each heavy metal according to the following formula (Hakanson, 1980): Eir ¼ T ir  C if ¼

T ir  C is C in

T ir

where is the toxic-response factor of heavy metal i, which reflects the toxicity level and sensitivity of organisms to it; C if is the contamination factor of heavy metal i; C is is the measured concentration of heavy metal i in the sediment; C in is the background value of heavy metals i, adopted from Li and Zheng (1988). The toxicresponse factor for Cd, Cr, Cu, Mn, Pb and Zn was 30, 2, 5, 1, 5, and 1, respectively (Hakanson, 1980). The degree of ecological risk can be categorized as follows: Eir o 40: low risk, 40r Eir o 80: moderate risk, 80r Eir o 160: considerable risk, 160 r Eir o 320: high risk, and Eir Z 320: very high risk. The potential ecological risk index (RI), which represents the overall ecological risk of multiple heavy metals in the sediment, was calculated using the following formula (Hakanson, 1980): n

RI ¼ ∑ Eir i¼1

2. Materials and methods 2.1. Study site Nansha mangrove (113133'00”E, 22139'14”N) was chosen as the study site with an estimated area of 55 hm2 in Sanmin Island, South China (Fig. 1). This mangrove was highly dominated by the introduced, mature, true mangrove plants Sonneratia apetala (average height: 8 m; average diameter at breast height: 11.8 cm), which were uniformly distributed with density of approximately 230 ind hm  2. Apart from mangrove plants, sedge Cyperus malaccensis was ubiquitously distributed in the open forest gap, while water hyacinth Eichhornia crassipes was a rare species in the study site.

2.2. Collection of sediment and plant samples In November 2012, the study site was uniformly divided into twenty sampling points along the Island with a distance of about 200 m between two consecutive sampling points (Fig. 1). At each sampling point, three random samples of surface sediment were collected by a rectangular sampler (10 cm long  10 cm wide  15 cm deep). To analyze the pollution history of heavy metals in the mangrove, three core sediment samples were collected by a PVC core (10 cm in diameter  66 cm deep) in the unvegetated area at sampling points N5, N10 and N15 to minimize the effect of root uptake (Fig. 1). According to the previous results of 210Pb dating, the sedimentation rate in Nansha mangrove is approximately 2 cm yr  1 (Chen and Luo, 1991). Thus, the sediment sample in each core was cut into 33 layers from the top at 2 cm depth interval by a PVC knife to represent the pollution history from 1979 to 2011. Roots, stems and leaves of the dominant plants, namely S. apetala and C. malaccensis, were also collected from sampling points N5, N10 and N15. Stems and leaves of S. apetala were collected by cutting. Roots of S. apetala were collected together with sediment using the PVC core, followed by washing away the sediment. C. malaccensis was collected by carefully removing the whole individual from sediment and each collected individual was then separated into roots and leaves. At each sampling point, three individuals were collected for each plant species.

where n is the number of heavy metals analyzed in the sample (i.e. n¼ 7 in the present study). RI can be classified into four levels: RIo150: low risk, 150rRIo300: moderate risk, 300rRIo600: considerable risk, and RIZ600: very high risk. Bioconcentration factor (BCF) and translocation factor (TF) were calculated to estimate the efficiency of a plant to accumulate heavy metals from sediment and to translocate the heavy metals from its roots to its stems or leaves, respectively. BCF and TF are calculated by the following formulas (Wilson and Pyatt, 2007; Zacchini et al., 2009): BCF ¼

C plant ; C sediment

TF ¼

C stem=leaf C root

where C plant and C sediment are the concentrations of a particular heavy metal in the plant and sediment, respectively; C stem , C leaf and C root are the concentrations of a particular heavy metal in the stem, leaf and root, respectively. Pearson correlation analysis was applied to examine the relationship among heavy metals in the surface sediment. Linear regression analysis was conducted to examine the correlation between concentration and sediment depth. One-way analysis of variance (ANOVA), followed by Tukey's test for pair-wise comparisons, was used to compare the concentrations of heavy metals in different plant organs of each plant species. Statistical analyses were performed using software SPSS 20.0 for Windows.

3. Results 3.1. Concentration and ecological risk of heavy metals in the surface sediment The concentrations of heavy metals in the surface sediment at different sampling points are shown in Fig. 2. Four distinct patterns were observed based on spatial variation. Pattern 1 (Cd): a dramatic fluctuation in concentration appeared from N1 to N20 with an overall slightly decreasing trend (Fig. 2a); Pattern 2 (Cr and Cu): the concentrations decreased remarkably from N1 to

Q. Wu et al. / Ecotoxicology and Environmental Safety 104 (2014) 143–151

Pearl River

145

Water flow

Sanmin Island 1 km

N20

N15

N17

N19 N18

N16

N14

N13

N11

N12

N10

N8

N6

N1

N3

N5

N7

N9

N4

N2

0.5 km Fig. 1. The sampling points, shown by , in Nansha mangrove in the present study (retrieved from Google Earth). At each sampling point, three replicates of surface sediment are collected. Three core sediment and plant samples are collected at sampling points N5, N10 and N15 as replicates.

N4, but slightly fluctuated from N4 to N20 (Fig. 2b and c); Pattern 3 (Zn): the concentration decreased slightly from N1 to N20 with small fluctuation (Fig. 2g); Pattern 4 (Mn, Ni and Pb): the concentrations remained more or less the same from N1 to N20 with occasional large fluctuations (Fig. 2d–f). The concentrations of all metals were above their respective background level, suggesting that the sediment was contaminated with heavy metals. Furthermore, the concentrations of Cd, Cr, Cu and Zn were too high to meet their respective guideline values of class I marine sediment quality standards in China (GB 18668-2002), which aim to protect human health and natural environment. Pearson correlation analysis found that significantly positive correlations were found in the pairs Cu–Zn (0.595), Cd–Zn (0.449), Cr–Cd (0.555), Cr–Cu (0.724) and Mn–Ni (0.823), suggesting that Cd, Cr, Cu and Zn may come from the same source while Mn and Ni from another. The pattern of Eir of each heavy metal was more or less the same as its concentration (Fig. 3). The ecological risk of Cd and Cu was very high (Eir Z 320) and moderate (40 r Eir o 80), for most sampling points (Fig. 3a and c). The ecological risk of the rest (i.e. Cr, Mn, Ni, Pb and Zn) was low (Eir o 40) for all sampling points (Fig. 3b, d–g). Overall, the ecological risk of heavy metals in Nansha mangrove, indicated by RI, was very high (RIZ600) for most sampling points (Fig. 3h), largely due to Cd contamination.

3.2. Concentration of heavy metals in the core sediment The concentrations of heavy metals along the depth gradient are shown in Fig. 4. Linear regression analysis showed that the concentrations of all heavy metals, except Mn, were significantly negatively correlated with depth (i.e. the deeper the sediment, the lower the concentration of heavy metals). This indicated that heavy metal pollution has been deteriorating at a relatively constant rate from 1979 onwards.

3.3. Concentration of heavy metals in the dominant plants The concentrations of heavy metals in different organs of the dominant plants are shown in Table 1. Higher concentrations of heavy metals were found in the roots than the stems and leaves for both plants, with only few exceptions in S. apetala (Cr and Pb). The concentrations of Ni and Zn in the leaves of S. apetala were higher than those in the stems. All heavy metals were highly localized in the roots of C. malaccensis that their concentrations in the roots were higher than those in the leaves. Comparing the phytoremediation potential of these two plants, the BCF of C. malaccensis was higher than that of S. apetala by more than 2-fold for all heavy metals, except Mn (Table 1). Nevertheless, the low TF ( o0.2) of C. malaccensis for all the heavy metals indicated that C. malaccensis could not effectively translocate heavy metals from its roots to its leaves (Table 1). In contrast, S. apetala could readily translocate Cr, Pb and Zn from its roots to its aboveground biomass, indicated by the high TF (40.9).

4. Discussion 4.1. Ecological risk of heavy metals in Nansha mangrove The present study clearly showed that the sediment in Nansha mangrove was severely contaminated with heavy metals. More importantly, the ecological risk of heavy metals was very high, largely due to Cd contamination. Such a high contamination can be related to high silt and clay contents of sediment (ca. 45% in total), which have a higher affinity to bind to heavy metals (Dube et al., 2001). However, it is more likely that anthropogenic inputs, such as discharge of industrial and domestic sewage (Li et al., 2000; Cheung et al., 2003; Liu et al., 2003; Li et al., 2007; Wong et al., 2007; Liu et al., 2011), combined with the effect of river flow, were

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Fig. 2. The concentrations of a) Cd, b) Cr, c) Cu, d) Mn, e) Ni, f) Pb, and g) Zn (mg g  1) of the surface sediment in Nansha mangrove at different sampling points (mean 7 S.D., n¼ 3). The dashed line indicates the background level of each heavy metal according to Li and Zheng (1988). The dotted line indicates the guideline level of each heavy metal, except Mn and Ni, based on the class I marine sediment quality standards in China (GB 18668-2002).

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147

Fig. 3. The potential ecological risk coefficients (Eir ) of a) Cd, b) Cr, c) Cu, d) Mn, e) Ni, f) Pb, and g) Zn, as well as h) the potential ecological risk index (RI) of the surface sediment in Nansha mangrove at different sampling points (mean 7 S.D., n¼ 3).

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Fig. 4. The concentrations of a) Cd, b) Cr, c) Cu, d) Mn, e) Ni, f) Pb, and g) Zn (mg g  1) of the sediment in Nansha mangrove along the depth gradient (cm), representing the pollution history of heavy metals from 1979 to 2011.

the major causes of severe heavy metal contamination. Since Nansha mangrove is located near the outlet of the PRE, heavy metals are highly concentrated due to the convergence of several sewage-polluted tributaries (Li and Liang, 1995). Spatial variation of heavy metals was generally not obvious in the present study, probably because the sediment properties, especially grain size (Sand: 50.87–60.48%; Silt: 36.94–46.50%; and Clay: 2.34–3.22%), were similar among sampling points. Nonetheless, the concentrations of Cd, Cr and Cu were particularly higher from N1 to N3. We propose that sewage discharge from the electroplating plants

located on the opposite site could be a possible cause as the sewage was carried along the river flow. Alarmingly, heavy metal pollution, except Mn, was shown to be steadily deteriorating since 1979. The disparate pattern of Mn is enigmatic but it might be due to its strong association with the geochemical matrix with iron or early diagenetic processes (Jonathan et al., 2010). The trend of heavy metal pollution in the present study was generally consistent with the previous study in which heavy metals were seriously contaminated in the top 45 cm sediment in Qi’ao Island owing to the rapid socio-economic

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149

Table 1 The concentrations (mg g  1) of heavy metals in different organs (i.e. roots, stems and leaves) of Sonneratia apetala and Cyperus malaccensis as well as their bioconcentration factors (BCF) and translocation factors (TF) (mean 7 S.D., n¼ 3).

Sonneratia apetala

Cyperus malaccensis

Roots Stems Leaves Roots Leaves

Sonneratia apetala Cyperus malaccensis Sonneratia apetala Cyperus malaccensis

Stems/Roots Leaves/Roots Leaves/Roots

Cd

Cr

Cu

Mn

N.D. N.D. N.D. 0.36 7 0.05 N.D.

2.22 7 0.18b 3.20 7 0.01a 1.03 7 0.14c 7.337 1.27a 1.40 7 0.17b

13.0 7 3.70a 3.18 70.05b 2.667 0.36b 56.6 79.38a 6.25 70.64b

N.A. 0.231

0.001 0.003

0.056 0.278

N.A. N.A. N.A.

1.441 0.464 0.191

0.245 0.205 0.110

Ni

Concentration (mg g  1) 1857 16.4a 4.127 0.21a 1197 6.57b 1.05 7 0.04c 87.6 7 9.32c 2.007 0.34b 258 7 18.9a 18.3 7 2.92a 39.17 5.92b 1.647 0.03b Bioconcentration factor 0.148 0.049 0.169 0.206 Translocation factor 0.643 0.255 0.474 0.485 0.152 0.090

Pb

Zn

1.40 7 0.36b 2.08 7 0.10a 0.51 70.15c 7.42 7 2.93a 0.36 7 0.10b

19.17 6.34a 10.17 0.55b 17.6 7 3.36a 79.4 7 11.2a 15.4 70.63b

0.024 0.070

0.098 0.298

1.486 0.364 0.049

0.529 0.922 0.194

The same superscript letters within each species and heavy metal indicate no significant difference according to Tukey’s test (p 40.05). Stems/Roots: Ratio between the concentrations of a particular heavy metal in the stems and roots; Leaves/Roots: Ratio between the concentrations of a particular heavy metal in the leaves and roots. N.D.: Not detected; N.A.: Not available.

growth in the region of the PRE (Liu et al., 2011). In fact, such growing trend of heavy metal pollution owing to rapid urbanization and industrialization is observed not only in China (Zuo et al., 2009), but also in other countries such as India and Canada (Percival and Outridge, 2013; Senthilkumar et al., 2013). Correlation analysis is a useful way to determine the number of possible sources of pollutants. The present study suggested that Cd, Cr, Cu and Zn might stem from the same source while Mn and Ni from another. We suggest that Cd, the most toxic heavy metal with a very high ecological risk, was likely from multiple sources. In addition to the industrial sewage from electroplating and electronic industries (Cheung et al., 2003; Wong et al., 2007), runoffs from agricultural sites as well as from mining and smelting sites also contributed to the high level of Cd (Wong et al., 2002; Li et al., 2009). Cu also originated from the municipal and industrial sewage, in addition to the agricultural runoff with Cu-containing herbicides (Ip et al., 2007). A significant correlation between Cr and Zn was found because they stemmed from the industrial sectors such as electroplating factories (Liu et al., 2003; Li et al., 2000). It is noted that Cd, Cr, Cu and Zn could be originated from the industrial sewage, explaining why they usually had a positive correlation. Besides, a high correlation coefficient between Mn and Ni was observed. Metal industries, especially stainless steel industry, are so prevalent in Zhongshan and Guangzhou, resulting in the contamination of Mn and Ni (Cheung et al., 2003; Xu et al., 2012). 4.2. Heavy metal uptake by dominant plants Concentrations of heavy metals in the roots of C. malaccensis were much higher than those in the leaves (i.e. very low TF). Since heavy metals per se can trigger toxic effects on plants when they were translocated in plant tissues (Weis and Weis, 2004), plants can respond by restricting the flow towards the vascular tissue (Peverly et al., 1995). The translocation of heavy metals by Eichhornia crassipes, for instance, was restricted by the root epidermis or endodermal Casparian strip which serves as a barrier (Vesk et al., 1999). Such mechanism was also found in Phragmites australis (Peverly et al., 1995; Keller et al., 1998). The distribution of heavy metals in S. apetela, however, was slightly different. For example, no significant difference in the concentration of Zn between the roots and leaves was found; the concentrations of Cr and Pb were higher in the stems than those in the roots. Weis and Weis (2004) reviewed that Zn can be readily accumulated in leaves through translocation and the degree of accumulation is positively correlated with the concentration of Zn in sediment. Fitzgerald et al. (2003) also revealed that Pb can highly accumulate

in the stem of dicots, compared to the root. Nonetheless, the very low concentration of Pb in S. apetala, irrespective of the concentration in sediment, suggested an avoidance mechanism performed by S. apetala to prevent the uptake of Pb. The underlying mechanisms of translocation of heavy metals in S. apetala still merit further investigation. All plants have a potential to stabilize, selectively extract and translocate heavy metals from sediment through various mechanisms, which can be reflected by BCF and TF (reviewed by Ali et al., 2013). Generally speaking, a good candidate for phytoremediation should have both BCF and TF greater than one (Yoon et al., 2006; Usman et al., 2013). Unfortunately, the dominant plants in Nansha mangrove obviously could not fulfill these criteria with a few exceptions. The low BCF can be attributed to the very high concentration of heavy metals in sediment that the plants have to elicit exclusion mechanisms to prevent excessive uptake of heavy metals (MacFarlane et al., 2003). Despite the low BCF of S. apetala, its TF for Pb, Cr and Zn was greater than or close to one, implying an effective translocation from the roots to the aboveground biomass. In addition, the very high biomass of mature S. apetala suggests that it can store huge amount of heavy metals from sediment. In contrast, the TF of C. malaccensis was very low in spite of the higher BCF than S. apetala. This indicates C. malaccensis can only stabilize and extract heavy metals from sediment. Overall, we suggest that S. apetala has a higher phytoremediation potential than C. malaccensis although its capability is seemingly insufficient to purify the highly contaminated sediment.

4.3. Comparison with other mangroves worldwide Compared to other mangroves all over the world, the sediment in Nansha mangrove was highly contaminated with Cr, Cu and Mn (Table 2). It is noted that the concentration of Cd in most of the mangroves in Central and South America is very high and thus the ecological risk in these mangroves must also be high. In contrast, the mangroves in Singapore and Australia are much less contaminated with heavy metals, probably due to better management of anthropogenic sources. Within Asia, the sediment in Nansha mangrove is more contaminated with Cd, Cr, Cu and Zn than the other cities in China like Futian, Taishan and Zhanjiang, likely owing to the rapid socio-economic development in the region of the PRE. Similarly, Hong Kong suffers from serious contamination of Cd, Cu, Pb and Zn due to discharge of industrial sewage and poor water circulation in the bottle-neck of Deep Bay.

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Table 2 The concentration of heavy metals (mg g  1) in the sediment of the mangroves worldwide. Location

Country/Area

Cd

Cr

Cu

Mn

Ni

Pb

Zn

Reference

Nansha Futian Taishan Zhanjiang Deep Bay Mai Po Sungei Buloh Brisbane River Mazatlan Harbor Galetea Payardia Punta Mala Bay Toro Pointa Punta Piuta Punta Portete Cienaga Grande Buffalo River Guanabara Bay

China China China China Hong Kong Hong Kong Singapore Australia Mexico Panama Panama Panama Panama Costa Rica Costa Rica Colombia Brazil Brazil

0.78 / 0.127 0.16 0.167 0.09 3 1.2 0.18 0.1–1.9 2 7.2 7.5 o 10 6.6 6.0 7.3 1.92 3.64 /

155 58.0 19.9 7 8.96 5.127 2.63 40 33.0 16.6 13.3–54.3 7.6–42.5 12.8 10.0 23.3 13.7 19.8 22.6 13.2 118 37.7–43.3

113 45.6 30.9 7 9.01 16.9 76.86 80 67.1 7.06 3.1–30.2 7.7–90.9 4 4 56.3 4.9 9.8 8.4 23.3 76.0 79.6–91.7

880 / / / / / / / / 143 228 295 294 525 268 623 524 5247 27.6

48.4 62.8 / / 30 70.8 7.44 2.4–57.6 6.1–30.3 74.0 91.8 27.3 82.4 99.0 102 32.5 / /

55.3 69.9 67.7 7 10.1 32.8 715.4 80 135 12.3 20.1–81.9 14–100 32.5 33.3 78.2 38.0 25.6 34.5 12.6 131 166–170

159 125 79.9 7 3.59 49.07 16.9 240 222 51.2 40.8–144 46.4–348 10.9 16.1 105 19.9 11.4 14.7 91.0 479 448–505

Present study Zan et al. (2002) Li (2008) Li (2008) Tam and Yao (1998) Ong Che (1999) Cuong and Obbard (2006) Mackey and Hodgkinson (1995) Soto-Jiménez and Paez-Osuna (2001) Guzman and Jiménez (1992) Guzman and Jiménez (1992) Defew et al. (2005) Guzman and Jiménez (1992) Guzman and Jiménez (1992) Guzman and Jiménez (1992) Perdomo et al. (1998) Kehrig et al. (2003) Kehrig et al. (2003)

5. Conclusions The foregoing findings revealed that, despite unclear spatial variation, heavy metal pollution in Nansha mangrove was very serious probably owing to the discharge of industrial sewage in the region of the PRE. Consequently, the ecological risk of heavy metals, largely due to Cd, in Nansha mangrove was very high. The core sediment samples revealed that heavy metal pollution, except Mn, in Nansha mangrove has been deteriorating at a relatively constant rate from 1979 onwards. Unfortunately, the dominant plants in Nansha mangrove, including C. malaccensis and S. apetala, had limited capability to immobilize, extract and translocate the heavy metals. Therefore, inspection of the potential sources should be enforced immediately, whereas environmental policy, such as regulating the discharge standards of industrial sewage, should be implemented to alleviate the heavy metal pollution so that the public health and integrity of Nansha mangrove can be maintained sustainably. Acknowledgments The project was supported by Guangzhou Science and Technology Project (No. 11C72010683), Guangzhou Municipal Colleges and Universities Science and Technology Project (No. 10A064), Open fund of Key Laboratory of Water Quality Safety and Protection in Pearl River Delta (No. GZ201102), and the National Natural Science Foundation of China (No. 41203058). References Abrahim, G.M.S., Parker, R.J., 2008. Assessment of heavy metals enrichment factors and the degree of contamination in marine sediments from Tamaki Estuary, Auckland, New Zealand. Environ. Monit. Assess. 136, 227–238. Ali, H., Khan, E., Sajad, M.A., 2013. Phytoremediation of heavy metals – concepts and applications. Chemosphere 91, 869–881. Alongi, D.M., 2002. Environ. Conserv. Present state and future of the world's mangrove forests 29, 331–349. Bosire, J.O., Dahdouh-Guebas, F., Walton, M., 2008. Functionality of restored mangroves: a review. Aquat. Bot. 89, 251–259. Chaudhuri, P., Nath, B., Birch, G., 2014. Accumulation of trace metals in grey mangrove Avicennia marina fine nutritive roots: the role of rhizosphere processes, Mar. Pollut. Bull 79, 284–292. Chen, F.R., Yang, Y.Q., Zhang, D.R., Zhang, L., 2006. Heavy metal associated with reduced sulfur in sediments from different deposition environments in the Pearl River estuary, China. Environ. Geochem. Health 28, 265–272. Chen, X.Y., Gao, H.W., Yao, X.H., Chen, Z.H., Fang, H.D., Ye, S.F., 2013. Ecosystem health assessment in the Pearl River Estuary of China by considering ecosystem coordination. PLoS One 8, e70547.

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