heavy metal contamination and ecological risk assessments in the sediments and zoobenthos of...

Catena xxx (2014) xxx–xxx

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Heavy metal contamination and ecological risk assessments in thesediments and zoobenthos of selected mangrove ecosystems,South China

Jinling Liu a,c,1, Hao Wu b,1, Jianxiang Feng d, Zhengjie Li d, Guanghui Lin b,e,⁎a China University of Geosciences, Faculty of Earth Sciences, Wuhan 430074, Chinab Division of Ocean Science and Technology, Graduate School at Shenzhen, Tsinghua University, University Town, Shenzhen 518055, Chinac Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, Chinad Key Lab of MOE for Coast and Wetland Ecosystems, College of the Environment, Xiamen University, Xiamen 361005, Chinae Ministry of Education Key Laboratory for Earth System Modeling, Center for Earth System Science, Tsinghua University, Beijing 100084, China

⁎ Corresponding author at: Division of Ocean Science anat Shenzhen, Tsinghua University, University Town, She+86 0756 26036292.

E-mail addresses: [email protected], lin1 These authors contributed equally to this work.

http://dx.doi.org/10.1016/j.catena.2014.02.0090341-8162/© 2014 Elsevier B.V. All rights reserved.

Please cite this article as: Liu, J., et al., Heavymangrove ecosystems, South C..., Catena (20

a b s t r a c t
a r t i c l e i n f o
Article history:Received 23 July 2013Received in revised form 29 January 2014Accepted 20 February 2014Available online xxxx

Keywords:MangroveSedimentZoobenthosVegetationHeavy metalEcological risk

Mangrove ecosystems provide ideal habitats for many marine organisms, but few studies have been conductedon the possible impact of heavymetals on these fragile inter-tidal estuarine wetlands. This study aimed to inves-tigate heavy metal contamination in the sediments and zoobenthos in different mangrove ecosystems of south-ern China and to evaluate potential ecology risks of heavy metals in the sediment of mangrove ecosystems.Significant differences among different geographical regions were observed for the contents of Cu, Zn, As, Cd,and Pb in the sediment, while no significant differences were found among different vegetations. Except forPb, the heavymetal contents in two species of crabs (Perisesarma bidens and Parasesarma plicata) in the Aegicerascorniculatum forest were lower than those in Bruguiera gymnorrhiza forest or Pagatpat forest. The sediment in themost mangrove ecosystems of China posed considerable or moderate ecological risk. Correlation analysis andprincipal component analysis (PCA) revealed that Cr, Cu, Zn and Pb were mainly derived from anthropogenicactivities such as industrial effluents and domestic sewage.

© 2014 Elsevier B.V. All rights reserved.

1. Introduction

Mangrove ecosystems are critical inter-tidal estuarine wetlands,which provide ideal habitats for manymarine organisms andmigratorybirds (Cuong et al., 2005; Nagelkerken et al., 2008). The most specialcharacteristic of mangrove ecosystems is the high primary productivityrate, attributed to high decomposition rate and efficient recycling of nu-trients such as phosphorus, carbon, and nitrogen (Bosire et al., 2005). Itis well known that as one of the most important coastal ecosystems inthe tropics, mangroves stabilize mobile sediments and act as a bufferagainst coastal erosion (El-Said and Youssef, 2013; Tam and Wong,1996). However, this fragile ecosystem has been degraded seriouslybecause of environmental changes such as global climate change andenvironmental pollution (Gilman et al., 2006). Among various pollut-ants, heavy metals with persistence, non-biodegradation, toxicity andbioavailability pose a major threat to mangrove biodiversity andhuman health.

d Technology, Graduate Schoolnzhen 518055, China. Tel./fax:

[email protected] (G. Lin).

metal contamination and eco14), http://dx.doi.org/10.1016

Many previous studies focus on the heavy metal pollution in man-grove sediments (Cuong et al., 2005; El-Said and Youssef, 2013),mangrove plants (MacFarlane et al., 2003; Qiu et al., 2011), and otherorganisms (De wolf and Rashid, 2008). These studies have demonstrat-ed that mangroves have high capacity to accumulate heavy metals,which were discharged to the nearshore marine. Rich sulfide, highorganic matter content and redox conditions are widely believed to bethe main factors responsible for the retention of water-borne heavymetals in mangrove ecosystems (De Wolf and Rashid, 2008; Qiu et al.,2011). However, available heavy metals in the sediment could be alsoreintroduced to water or be uptake by plants and benthic organisms(De wolf and Rashid, 2008; MacFarlane et al., 2003). Therefore, the sed-iment in mangrove wetlands has been considered as a sink of contami-nants and a record for the anthropogenic pollutant input (El-Said andYoussef, 2013). To understand the behavior and fate of heavy metalsin mangrove wetlands, it is important to explore the heavy metal con-tamination in all compartments of an ecosystem. However, althoughgreat efforts have been undertaken to monitor pollution levels in thesediment of mangrove wetlands, very few studies have considered theeffect of sediment on the marine fauna and flora (Cuong et al., 2005;El-Said and Youssef, 2013; Marchand et al., 2011). Thus, the presentstudy aimed to investigate heavymetal contamination in the sedimentsand zoobenthos in different mangrove vegetations of South China and

logical risk assessments in the sediments and zoobenthos of selected/j.catena.2014.02.009

http://dx.doi.org/10.1016/j.catena.2014.02.009

mailto:[email protected]

mailto:[email protected]


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2 J. Liu et al. / Catena xxx (2014) xxx–xxx

to evaluate the potential ecology risks of heavy metals in the sedimentof mangrove ecosystems in China.

2. Materials and methods

2.1. Study area and sampling

Five mangrove nature reserves (MNRs) of China at different latitudeareas were selected for this study (Fig. 1). Three MNRs includingChangle (CL) (N 26°01′, E 119°38′), Quanzhou (QZ) (N 24°56′,E 118°40′), and Yunxiao (YX) (N 23°55′, E 117°24′) are located in Fujianprovince, where the mangrove vegetation was dominated by Kandeliaobovata. CL and QZ are industrial cities in Fujian Province, with signifi-cant annual productions from their textile, steel and food industries.The Zhanjiang (ZJ) MNR (N 21°33′, E 109°45′) with mangrove vegeta-tion of Aegiceras corniculatum, Bruguiera gymnorrhiza, and Sonneratiaapetala is located in Guangdong province. In ZJ, there are few industriesaround the mangrove area, so marine culture and agriculture providethe main financial resources for local residents and government.With large areas of mangrove vegetation dominated by Rhizophorastylosa, Bruguiera sexangula and S. apetala, Dongzhaigang (DZG) MNR(N 19°54′ ~ 19°20′, E 110°31′ ~ 110°38′) is located in Meilan District,Haikou, Hainan province, where the agriculture and tourist industriesare the pillar industry of local government.

Sampling campaign was carried out at these five MNRs between2009 and 2011. At each MNR, 3 or 5 field plots with dimensions of10 m × 10 m were established. In each field plot, the surface sediment(0–1 cm) and benthic organism samples (gastropod and crabs) werecollected. Each sediment samplewasmixedwith 5 sub-samples collect-ed from each sampling plot, while each gastropod sample consisted of8–10 animals and each crab sample consisted of 3–5 animals collectedfrom the same sampling plot. The most common crabs includingParasesarma plicata, Uca arcuata and Perisesarma bidens were collectedin all the studied areas. Chiromantes dehaani was only collected inChangle MNR. Dense astrologer, Metaplax longipes and Helice latimerawere only captured in Hainan Dongzhaigang MNR. Snail samples of

Fig. 1.Map of the southern China and study s

Please cite this article as: Liu, J., et al., Heavy metal contamination and ecomangrove ecosystems, South C..., Catena (2014), http://dx.doi.org/10.1016

Littoraria melanostoma, Cerithidea ornate and Certhidea microtera werecollected in the Quanzhou and Zhanjiang MNRs.

To avoid cross contamination, each sample was collected in a sealedpolyethylene bag and stored frozen in a cooler before bring back to thelaboratory for the analyses.

2.2. Sample treatment and analysis

In the laboratory, the samples were freeze-dried, ground, sieved andhomogenized. Prior to chemical analysis, the sediment and organismsamples were microwave-digested in Teflon vessels containing nitricacid and hydrofluoric acid. The detailed procedures of sediment andorganism samples were described in a previous study (Yi et al., 2011).

All the samples were analyzed for the contents of Cu, Zn, Cr, Cd, Pband As using inductively coupled plasma mass spectrometry (ICP-MS)(DRC-II, Perkin Elmer, USA). Concentrations of Hg in the sediment andorganism samples were measured by cold atomic fluorescence spec-trometry (CAFS) (F732-V, Shanghai, China). Analytical quality controlincluded analysis of reagent blank, sample blank, reference material,and duplicate samples. The certified reference material GSD1-3(IGGEC, Institute of Geophysical and Geochemical Exploration, China)and TORT-2 (NRC, Institute of National Measurement Standards,Canada) were used to check the test quality of the sediment and organ-ism samples, respectively.

3. Results and discussion

3.1. Contents of heavy metals in mangrove sediments

The concentrations of common heavy metals (Cr, Cu, Zn, As, Cd, Pb,and Hg) in the sediments of the five MNRs are listed in Table 1.The ranges of average concentrations of Cr, Cu, Zn, As, Pb, Cd, and Hgwere 28.5–86.6 mg/kg, 10.3–30.9 mg/kg, 24.8–87.0 mg/kg, 2.44–20.1 mg/kg, 25.6–86.4 mg/kg, 0.07–0.39 mg/kg, and 0.061–0.24 mg/kg,respectively. All heavy metal contents in the sediment from the sam-pled mangrove areas did not exceed the Marine Sediment Quality

ites (MNR: Mangrove Nature Reserves).



Table 1Heavy metal concentrations (mg/kg) in sediments of Mangrove Nature Reserves.

Location Vegetation Cr Cu Zn As Pb Cd Hg

CL Kandelia obovata 84.3 ± 4.13 30.9 ± 0.65 77.2 ± 0.83 16.7 ± 0.46 86.4 ± 1.46 0.23 ± 0.01 0.24 ± 0.06QZ K. obovata 59.8 ± 6.57 14.3 ± 0.97 50.9 ± 2.66 13.8 ± 0.67 59.5 ± 2.44 0.11 ± 0.01 0.061 ± 0.02YX Avicennia marina 53.6 ± 2.33 23.1 ± 0.59 79.0 ± 2.25 5.60 ± 0.69 60.4 ± 2.61 0.29 ± 0.10 0.16 ± 0.03

Spartina alterniflora 63.9 ± 3.96 26.3 ± 0.66 87.0 ± 1.88 9.43 ± 0.41 67.3 ± 1.17 0.21 ± 0.01 0.11 ± 0.03K. obovata 84.2 ± 20.7 25.4 ± 0.72 83.4 ± 2.31 10.0 ± 0.38 64.4 ± 1.74 0.25 ± 0.03 0.15 ± 0.06Aegiceras corniculatum 78.3 ± 8.10 26.1 ± 1.13 85.3 ± 3.29 11.6 ± 0.63 70.9 ± 4.26 0.39 ± 0.14 0.16 ± 0.05Mudflat 57.7 ± 2.62 23.5 ± 0.24 80.1 ± 0.79 7.18 ± 0.28 63.5 ± 1.4 0.27 ± 0.07 0.15 ± 0.04

ZJ A. corniculatum 39.7 ± 1.27 12.1 ± 0.22 30.1 ± 0.42 14.0 ± 0.52 41.9 ± 1.25 0.08 ± 0.01 0.16 ± 0.02Bruguiera gymnorrhiza 44.6 ± 5.27 10.3 ± 0.94 24.8 ± 2.18 12.7 ± 0.65 37.6 ± 3.76 0.07 ± 0.01 0.16 ± 0.03Sonneratia spp. 32.3 ± 5.36 18.3 ± 1.45 42.1 ± 3.73 3.64 ± 0.49 28.7 ± 1.93 0.12 ± 0.01 0.16 ± 0.03Rhizophora stylosa 28.5 ± 16.6 15.3 ± 1.00 35.7 ± 2.4 2.44 ± 1.32 30.7 ± 3.73 0.36 ± 0.20 0.16 ± 0.03

DZG R. stylosa 39.3 ± 8.79 21.0 ± 1.01 45.3 ± 1.47 18.8 ± 0.65 25.6 ± 1.08 0.30 ± 0.03 0.20 ± 0.06A. corniculatum 57.5 ± 6.02 21.3 ± 2.76 44.4 ± 2.19 19.0 ± 1.06 29.8 ± 1.82 0.38 ± 0.20 0.21 ± 0.06Sonneratia apetala 86.6 ± 14.0 26.5 ± 2.97 59.2 ± 5.02 19.9 ± 1.35 31.2 ± 2.13 0.16 ± 0.01 0.18 ± 0.03Mudflat 52.0 ± 11.0 21.1 ± 1.15 47.5 ± 1.62 20.1 ± 0.53 27.3 ± 0.62 0.17 ± 0.01 0.23 ± 0.06BGa 47.2 ± 26.9 10.1 ± 5.18 51.9 ± 29.6 11.8 ± 3.87 26.5 ± 12.4 0.04 ± 0.03 0.035 ± 0.04MSQGsb 80 35 150 20 60 0.5 0.2SQG non-pollutedc b25 b25 b90 b3 b40 – b1.0SQG moderately pollutedc 25–75 25–50 90–200 3–8 40–60 – –

SQG heavily pollutedc N75 N50 N200 N8 N60 – N1.0

a Background value of coastal sediments in South China (Li and Zheng, 1988).b Marine sediment quality guidelines (AQSIQ, 2002).c Sediment quality guidelines (Luo et al., 2010).

3J. Liu et al. / Catena xxx (2014) xxx–xxx

Guidelines (MSQGs) of China (AQSIQ, 2002). However, the concentra-tions of Cu, Pb, Cd, and Hg in the sediments from the five MNRs werehigher than the background value of littoral saline soils in southernChina (Li and Zheng, 1988). In comparison with the sediment qualityguidelines (SQGs) of USEPA (Luo et al., 2010), our results indicatedthat the sediments from the five MNRs were in the range of moderateto heavy for Cr, non-polluted to moderate for Cu, non-polluted toheavy for As and Pb, and non-polluted for Zn and Hg (Table 1).

The results of two-way ANOVA analysis for the study site and vege-tation types showed that there was a significant difference amongdifferent study sites for the contents of Cu, Zn, As, Cd, and Pb(Table 2). These results could be explained by the regional social andeconomic conditions of the study areas. Both Changle and Yunxiao arethe major industrial cities of Fujian with significant annual productionsfrom their textile, steel and food industries. During the past twodecades, large amount of wastewater, not properly treated, have beendischarged from these industries into the coastal areas, which could

Table 2Two-way ANOVA for the comparison ofmangrove sediments on heavymetal contents be-tween different regions and vegetations.

Metals Factor df F P

Cr Location 2 6.85 0.12Vegetation 7 1.29 0.50Location ∗ Vegetation 2 1.54 0.23

Cu Location 2 25.02 0.04⁎

Vegetation 7 2.68 0.30Location ∗ Vegetation 2 1.97 0.16

Zn Location 2 58.19 0.02⁎


As Location 2 55.28 0.02⁎

Vegetation 7 5.30 0.17Location ∗ Vegetation 2 6.40 0.00⁎⁎

Cd Location 2 4.44 0.16Vegetation 7 2.88 0.27Location ∗ Vegetation 2 0.50 0.61

Pb Location 2 61.47 0.01⁎


Hg Location 2 7.56 0.10Vegetation 7 3.10 0.26Location ∗ Vegetation 2 0.70 0.50

⁎ p b 0.05.⁎⁎ p b 0.01.


lead to high levels of heavy metals such as Cu, Pb, Hg, Zn and Cd inChangle and Yunxiao MNRs. Dongzhaigang MNR is located in Hainanwhich is an agriculture and tourist industrial city where agricultureand geogenic origin (Qiu et al., 2011; Vane et al., 2009) could be thesource of higher As and Cr observed in this study. Moreover, the lowestconcentrations of heavy metals were found in the sediments fromZhangjiang MNR (Table 1), where there are few industries associatedwith heavy metals.

Although no significant differences were found in the heavy metalconcentrations among different vegetation types (Table 2), synergisticeffect between study site and local vegetation type was found for thecontents of Zn (P b 0.05) and As (P b 0.01). Previous studies showedthat alternating anaerobic and aerobic conditions accelerated the accu-mulation of As in the plants (Abedin et al., 2002; Tuli et al., 2010).Similar to rice paddies, the redox conditions in mangrove wetlandsare periodically influenced by the tide. Thus, available As in the man-grove sediment was easily absorbed by plants and subsequentlyreturned to the sediment by mangrove litter. In addition, Kirby et al.(2002) found that the concentrations of As in fungi and algae growingon mangrove roots were much higher than those of flora and fauna inthe mangrove ecosystem. Mangrove plant could release some low mo-lecular weight organic acids (e.g. malate, citrate, and oxalate), whichwere responsible for increasing bioavailability of metals in sedimentsnear the rhizosphere (Jones et al., 1996; Lu and Yan, 2007). These inter-actions of sediment and mangrove plant will influence the distributionof As in sediment from different regions.

3.2. Concentrations of heavy metals in mangrove zoobenthos

In this study, 50 organism samples were collected from 7 crab spe-cies and 4 snail species. The concentrations of common heavy metals(Cr, Cu, Zn, As, Cd, Pb, and Hg) of these organisms are listed in Table 3.Regardless of species, the range of concentrations of Cr, Cu, Zn, As, Cd,Pb, and Hg in crabs was 3.83–77.3, 18.7–82.5, 42.3–157, 1.07–7.23,0.01–0.30, 0.02–15.9, 0.04–0.52 mg/kg, respectively. And the range ofconcentrations of Cr, Cu, Zn, As, Cd, Pb, and Hg in snails was 9.86–77.0,66.2–159, 18.7–39.7, 2.28–6.97, 0.27–2.03, 0.78–12.2, and 0.08–0.54 mg/kg, respectively. Among thesemetals, Cu exhibited the highestconcentration (range of 66.2–159 mg/kg, mean of 113 mg/kg) in snails,whichmay be related to the physiologic characteristic of snails. As withother mollusks, snails have hemocyanin with high copper content totransport oxygen in its blood (Idakieva et al., 1995). In contrast, the



Table 3Heavy metal concentrations (mg/kg) in zoobenthos of Mangrove Nature Reserves.

Sites Vegetation Zoobenthos Cr Cu Zn As Cd Pb Hg

QZ Kandelia obovata Uca arcuata (n = 1) 31.32 58.29 98.61 2.67 0.02 0.14 –

CL K. obovata Parasesarma plicata (n = 1) 77.32 30.25 123.31 2.09 – 0.45 0.33Chiromantes dehaani (n = 1) 60.19 52.12 156.55 1.31 0.01 2.41 0.52

YX K. obovata P. plicata (n = 1) 55.97 40.70 118.00 3.87 0.05 0.46 0.33ZJ Sonneratia apetala Perisesarma bidens (n = 3) 37.36 46.40 99.03 3.26 0.06 0.37 0.21

P. plicata (n = 3) 27.54 40.21 56.90 2.16 0.01 0.30 0.09U. arcuata (n = 3) 26.29 46.08 111.85 5.65 0.16 0.31 0.47

Bruguiera gymnorrhiza P. bidens (n = 3) 45.76 46.80 78.05 2.33 0.01 1.36 0.10P. plicata (n = 3) 36.44 43.71 65.81 3.02 0.01 0.33 0.09

Aegiceras corniculatum P. plicata (n = 3) – 23.43 42.28 1.61 0.02 2.35 0.04P. bidens (n = 3) 8.17 30.91 58.26 1.61 0.02 3.56 0.05U. arcuata (n = 1) 32.03 82.47 90.23 7.23 0.30 15.94 0.11

DZG Avicennia marina P. bidens (n = 3) 4.65 18.65 53.52 1.79 0.01 2.90 0.07Rhizophora stylosa P. bidens (n = 3) 15.00 27.88 59.87 1.54 0.01 0.12 0.05S. apetala Metaplax longipes (n = 3) – 47.39 78.68 2.76 0.07 0.18 0.13K. obovata Helice latimera (n = 3) 3.83 52.80 81.13 1.34 0.05 0.04 0.32R. stylosa Dense astrologer (n = 3) 8.53 23.95 62.53 1.07 0.01 0.02 0.09

QZ K. obovata Cerithidea cingulata (n = 3) 63.70 120.10 33.30 5.97 0.49 4.65 –

Cerithidea ornate (n = 1) 9.86 112.38 25.84 5.60 0.35 6.43 0.08YX K. obovata C. ornate (n = 1) 76.99 159.14 39.68 6.97 0.31 12.23 0.21

Certhidea microtera (n = 1) 76.01 110.89 38.85 2.90 0.28 1.87 0.54ZJ K. obovata Littoraria melanostoma (n = 3) – 66.24 18.71 2.28 0.27 2.01 0.28

A. corniculatum L. melanostoma (n = 1) 20.95 108.06 28.55 3.81 2.03 0.78 0.22

– not detected.

0

45

90

20

40

60

60

120

0

2

4

0.00

0.08

0.16

0

3

6

AC SA BG AC SA BG0

200

400

Cr

ab

b

a

b b

a b

Cu

a

b b

Zn

a

bab

a b c

Perisesarma bidens Parasesarma plicate

As

a ab a b

c

a

Cd

a

aaa

a

a

aa

a

aaaa

a

Pb

bb

aHg

Fig. 2. Comparison of heavy metal concentrations in Perisesarma bidens and Parasesarmaplicata among different mangrove nature reserves (all data in mg/kg, except for Hgwhich is in ng/g). AC: Aegiceras corniculatum; SA: Sonneratia apetala; BG: Bruguieragymnorrhiza.


highest Zn concentration of 157 mg/kg was found in the crab species. Itcould be explained by easy absorption of Zn in the crab's exoskeleton,which was found to be an important storage site for Zn (Chan andRainbow, 1993). The carapace of crab was also a good biosorbent forZn in solutions, as shown in a previous study (Lu et al., 2007).

In order to evaluate possible impact of vegetation on heavymetal ac-cumulation in benthic organisms, two common species of crabs(P. bidens and P. plicata) were selected to avoid the sampling of othermore rare fauna species at the study sites. As shown in Fig. 2, the con-centrations of common heavy metals in these two crab species belowdifferent mangrove vegetations in Zhanjiang MNR were compared.The result showed that except for Pb, heavy metal contents in thesetwo crab species in the A. corniculatum forest were lower than those inB. gymnorrhiza forest or Pagatpat forest. This finding revealed that vege-tation could be an important factor influencing heavy metal accumulat-ed by benthic organism. It could be explained by the feeding habits andecological habitat of benthic organisms. P. bidens and P. plicata belong toomnivorous crustacean zoobenthos, feeding mainly on the organic de-tritus of the sediment surface. Mangrove leaf litter is the main foodsource for crab species (Skov and Hartnoll, 2002; Thongtham andKristensen, 2005). Previous study demonstrated that heavy metal con-centrations in leaves of A. corniculatum were lower than those ofKandelia candel, B. gymnorrhiza, Avicennia marina and R. stylosa (Wanget al., 1997). Therefore, A. corniculatum provides relatively clean foodfor the zoobenthos, making the heavy metal content of the zoobenthoslower in the A. corniculatum forest than in other vegetation types.More-over, the specificity and activity of mangrove root system could influ-ence the length of waterlogging and redox conditions, andsubsequently affect the bioavailability of heavy metals in the sediment.Previous study reported that the heavy metals in the sediment ofAvicennia root systemwere more bioavailable andmobile than beneathRhizophora stand (Marchand et al., 2011). In addition, mangrove sedi-ment was also considered as a major sink for metal pollution and foodsource for benthic animals (Clark et al., 1997; Harbison, 1986; LacerdaandCarvalho, 1993; TamandWong, 1996). However, therewere no sig-nificant correlations between heavymetal concentrations in benthic an-imals and sediments in present study. This finding suggested thatvegetationwas themajor factor influencing heavymetal concentrationsin benthic animals.

Please cite this article as: Liu, J., et al., Heavy metal contamination and ecological risk assessments in the sediments and zoobenthos of selectedmangrove ecosystems, South C..., Catena (2014), http://dx.doi.org/10.1016/j.catena.2014.02.009


Fig. 3. PCA loadings of components 1 and 2 for the seven heavy metals in the mangrovesediments from five mangrove nature reserves.


3.3. Sources of heavy metals in mangrove sediment

The accumulation of heavy metals in the sediment of the mangrovewetlands depends largely on watershed pollution, local soils, terrestrialand coastal erosion (Marchand et al., 2012). Firstly, watershed pollutionis tightly coupled with the local economic development and miningactivities (Li et al., 2012; Pan andWang, 2012). Rapid growth of the eco-nomic development in China has resulted in increasing environmentalpollution, especially in coastal areas. A large scale investigation of Hgpollution inmangrove areas of China revealed that theHg accumulationin the mangrove sediment was related to the local economic develop-ment (Ding et al., 2009). Secondly, hydrological and geological condi-tions are important factors influencing the distribution of heavymetals in mangrove sediment (Ding et al., 2009; Marchand et al.,2012). In the present study, Dongzhaigang estuary is a Liman baytype,which is in favor for the accumulation of heavymetals in sediment.In addition, the textural characteristic andmineralogical composition ofsediment also influence the concentrations of heavy metals (Fernandesand Nayak, 2012). For example, the sediment grand size in ZhanjiangMNR was sandy, which was difficult to retain heavy metals, thus theconcentrations of heavy metals were relatively low at this site.

In order to identify possible sources of heavy metals in mangrovesediment, correlation analysis and principal component analysis (PCA)were performed. As shown in Table 4, very significant correlationswere found among Cr, Cu, Zn and Pb. The significant correlationsbetween heavy metals in the sediments indicated same sources ofpollution (Li et al., 2009; Yi et al., 2011). The results of PCA for theheavy metal concentrations are shown in Fig. 3. The concentrations ofCr, Cu, Zn, As, Cd, and Pb could be grouped into a 2-component model,which accounted for 68% of all the data variation. The first componentexplains 46.1% of the total variation influenced by 4 heavy metalsincluding Zn, Cu, Pb and Cr (loading 0.946, 0.871, 0.844, and 0.727, re-spectively). It was in accordancewith the results of the correlation anal-ysis. These results implied that these metals could be derived fromanthropogenic activities like industrial effluents and domestic sewagedischarge. The second component was dominated by As (loading0.883) with a contribution rate of 23.0%, which is different from thefirst component. Itmay reflect the geological source or agriculture activ-ity. Inorganic Aswas often used in agriculture as insecticides, herbicides,fungicides, desiccants, defoliants, and animal feed additives (Nriagu,1994; Matschullat, 2000; Smedley and Kinniburgh, 2002; Cheunget al., 2008). Previous studies reported high level of As in the mangrovesediments from Hainan due to geogenic origin (Qiu et al., 2011; Vaneet al., 2009).

The PCA results for the heavy metals in the sediments from 5 MNRsare shown in Fig. 4. According to this analysis, the heavy metal concen-trations in the sediments of these 5 MNRs could be grouped into a twocomponent model, which accounted for 99.5% of all the data variation.The results showed that the heavy metal concentrations inDongzhaigang MNR were different from those of Yunxiao, Changle,Zhanjiang, or Quanzhou. The heavy metals in Dongzhaigang MNRwere considered to be of the geological source (Qiu et al., 2011). Thus,

Table 4Pearson correlation coefficients between different heavy metals in sediment.

Cr Cu Zn As Cd Pb Hg

Cr 1Cu 0.752⁎⁎ 1Zn 0.697⁎⁎ 0.832⁎⁎⁎ 1As 0.369 0.171 −0.161 1Cd 0.104 0.432 0.409 −0.121 1Pb 0.606⁎ 0.523⁎ 0.790⁎⁎⁎ −0.193 0.154 1Hg 0.070 0.323 −0.155 0.452 0.170 −0.274 1

⁎ p b 0.05.⁎⁎ p b 0.01.⁎⁎⁎ p b 0.001.


our results imply that anthropogenic activities are the main pollutionsources of the heavy metals in Yunxiao, Changle, Zhanjiang and Quan-zhou MNRs, but the geological source plays more important role inthe Dongzhaigang MNR.

3.4. Ecological risk assessment

In order to evaluate the degree of heavy metal pollution in the sedi-ments of mangrove ecosystems, ecological risk assessment was con-ducted using the Håkanson ecological risk index (RI) (Håkanson,1980), which could be calculated by the following equations:

RI ¼X

Eir ð1Þ

Eir ¼ TirC

if ð2Þ

Cif ¼ Ci

0=Cin ð3Þ

Fig. 4. PCA loadings of components for the sediment heavy metal concentrations in thesediments from five mangrove nature reserves.




where RI represents the sum of all risk factors for heavy metals in sedi-ments. Eir is the monomial potential ecological risk factor, Tir is the tox-icity coefficient which represents the toxic-response factor for a givenmetal. The value of Tir for Hg, Cd, As, Cu, Pb, Cr, and Zn was 40, 30, 10,5, 5, 2, and 1, respectively (Hilton et al., 1985). Cif is the contaminationfactor, Ci0 is the concentration of metal in the sediment of mangroveecosystem, and Cin is the background value of the heavymetal in coastalsediments of south China (Li and Zheng, 1988) (Table 1).

Based on the Eqs. (1)–(3), ecological risk indexes of heavy metals inthe five mangrove MNRs were calculated and listed in Table 5. Theresults indicated that there was a relatively severe ecological risk ofheavy metal in the whole mangrove areas. The potential ecologicalrisk index of single element Eir showed that Hg and Cd exhibited thetwomost severity of potential pollution risk among seven heavy metalsin the sediments of all the MNRs, due to highest toxicity coefficients ofHg and Cd.

As shown in Table 5, the ecological risk indexes (RI) of heavy metalsin themangrove sediments from different MNRs indicated that Changleand Yunxiao were suffering relatively high and considerable ecologicalrisk of heavy metals. Zhanjiang, Dongzhaigang and Quanzhou MNRswere in the state of moderate ecological risk. These results indicatedthat heavy metal pollution in the sediment of mangrove ecosystemChina is considerable or moderate.

4. Conclusions

The present study analyzed seven heavy metals in the sedimentsand zoobenthos from five MNRs of southern China with different vege-tation covers. Significant differences among five MNRs were found forthe contents of Cu, Zn, As, Cd, and Pb in the sediments. The correlationbetween vegetation type and heavy metal concentrations in mangrovesediments was not significant, indicating that vegetation was not animportant factor influencing heavy metal concentrations in mangrovesediment. However, significant impact of vegetation type on heavymetal concentrations in selected benthic animals was observed. Thesediments in the mangrove ecosystems of China were estimated topose considerable or moderate ecological risks. Heavy metals (Cr, Cu,Zn and Pb) in the mangrove sediments were derived mainly fromanthropogenic activities such as industrial effluents and domesticsewage discharge.

Acknowledgments

This studywas funded in part by China Postdoctoral Science Founda-tion (No. 2012M510201), Ocean Public Funded Project from StateOceanic Administration (201305021) and a key project from NationalNature Science Foundation of China (No. 30930017). The first author

Table 5Ecological risk index of heavy metals in mangrove sediments of different areas.

Eri Potential ecological risk for single regulator

Eri b 40 Low

40 ≤ Eri b 80 Moderate

80 ≤ Eri b 160 Considerable

160 ≤ Eri b 320 High

Eri ≥ 320 Very high

Sites Eri

Cr Cu Zn As

YX 2.8 11.2 1.5 8.0QZ 2.5 6.8 1.0 11.7CL 3.6 14.7 1.5 14.2ZJ 1.6 6.9 0.7 6.8DZG 2.5 10.7 0.9 16.5


also gratefully acknowledges the support of K.C.Wong Education Foun-dation, Hong Kong.

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