Marine Pollution Bulletin 62 (2011) 1140–1146

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Marine Pollution Bulletin

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Baseline

Sponges and sediments as monitoring tools of metal contaminationin the eastern coast of the Red Sea, Saudi Arabia

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

a r t i c l e i n f o

Keywords:SedimentsSpongesRed SeaMetalsSaudi Arabia

0025-326X/$ - see front matter � 2011 Elsevier Ltd.doi:10.1016/j.marpolbul.2011.02.043

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

a b s t r a c t

Sediments and sponges were collected from various locations along the eastern coast of the Red Sea, theKingdom of Saudi Arabia. Total concentrations of Cd, Zn, Ag, Cu, Pb, As and Hg in the sediments were mea-sured. Metal contamination was not significant in most of the studied sites and only one site was mod-erately polluted by Zn, Cu, and Pb. Sponges accumulated specific metals readily even though the metalexposure was low in the ambient environment. Contrasting interspecies differences in metal accumula-tion patterns were observed among the nine collected species of sponges. Significant positive correlationswere found between the metal concentrations in the two species of sponges collected from the samesites. The strong ability to accumulate specific metals and the diversity of sponges that live in the RedSea coastal areas make them a promising biomonitor of metal contamination in the areas.

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Coastal areas are often considered as receptacles for pollutantsfrom industrial and urban activities. Overexploitation in modernsociety has led to elevated inputs of anthropogenic contaminantsinto coastal and estuarine areas which are vulnerable to humanactivities (Peters et al., 1997; Lewis and Devereux, 2009). Metalsare one of the toxic pollutants of great concern because of their po-tential detrimental effects on aquatic ecosystems (Grimalt et al.,2001; Prouty et al., 2010). Meanwhile, metals are readily accumu-lated by aquatic organisms and subsequently transferred alongfood chains, ultimately posing a risk to human health through sea-food consumption (Wang, 2002; Gerstenberger et al., 2010).

The Red Sea is famous for its unique tropical coral reef, man-grove, and seagrass ecosystems (Odum and Odum, 1955; Priceet al., 1998; Ashworth et al., 2006). The coastline of the Kingdomof Saudi Arabia stretches for about 1840 km and accounts for 79%of the eastern coast of the Red Sea. This area provides various hab-itats for diverse communities of corals and sponges. As one of thelargest countries bordering the Red Sea, Saudi Arabia has under-gone a rapid transformation into a modern industrial country (Badret al., 2009). As a result, a significant part of the coast has been sub-jected to extensive exploitation, and metal pollution is fast becom-ing a threat to the coastal environments. Incidents of damaged oilwells, oil pipeline leaks, and domestic sewage from coastal citiesare contributing significantly to the coastal pollution (Al-Thukairet al., 2007). Kadi (2009) showed that soils in the urban areas ofJeddah—a Saudi Arabian city located on the coast of the RedSea—have been polluted by Zn and Pb found in traffic road dust.

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The highest concentration found in roadside soils was 105 mg kg�1

for Pb and up to 450 mg kg�1 for Zn. Recent records from sedimentcores also revealed that Jeddah was the most polluted area alongthe eastern coast, where over 3 mg kg�1 of Cd and 100 mg kg�1

of Pb was detected in the sediments and increasing metal concen-trations were observed in the upper layer of the cores (Badr et al.,2009). To date, limited data exist for an accurate assessment of themetal pollution of coastal environments in Saudi Arabia, especiallyfor the areas located near the coral reef and mangrove ecosystems.Field surveys of metal pollution must be conducted before appro-priate policies can be made to protect the vulnerable coastalenvironments.

Investigating the concentration and distribution of metals insediments is an effective way to understand metal contaminationin marine ecosystems because sediments are a reservoir for metalsand can provide historical input records of metals (Hatji et al.,2002; Bell et al., 1997). Sediments are preferred as a monitoringtool because they generally show less variation over a short periodof time than dissolved metals in overlying water columns(Atkinson et al., 2007). Although the total metal concentration isa valuable piece of information and tells us about the integratedaccumulation of metals in sediments over a certain period of time,it is however inadequate to predict the mobility, bioavailabilityand potential toxicity of metals in hazard assessment. The fatesof metals in sediments are greatly dependent on their physico-chemical speciation and environmental conditions such as redox,pH, salinity, and temperature (Yu et al., 2010). Sediment geochem-istry can significantly control metal bioavailability. Previous stud-ies have shown that labile metals (such as metals bound inexchangeable phase) are more bioavailable than those bound with

Table 1Location of the sampling sites along the coast of the Red Sea, the Kingdom of SaudiArabia.

Site Site name Abbreviation Location

S1 Obhor Sharm (outlet) OSO 21042.323N 39004.230ES2 Marine station MSN 21042.642N 39005.685ES3 Obhor Sharm (inner) OSI 21045.687N 39008.061ES4 Abu Madafi reef AMR 22003.656N 38046.074ES5 Non-reef reference site NRR 22010.178N 38057.398ES6 Mangrove site MGR 22013.139N 39003.069ES7 Treatment plant outfall TRO 21019.400N 39005.887ES8 Entrance of fish market EFM 21029.622N 39009.617ES9 Fish market FMT 21029.260N 39010.540E

K. Pan et al. / Marine Pollution Bulletin 62 (2011) 1140–1146 1141

the sulfide species or the reducible phase (Chen and Mayer, 1999;Stecko and Bendell-Young, 2000; Fan et al., 2002a). Therefore,measurement of geochemical species of metals is a necessary sup-plement to the environmental assessment of contaminatedsediments.

Knowing the characteristics of either seawater or sediments isnot enough to predict unequivocally the bioavailability of metals.Benthic species such as bivalves, seagrasses, macroalgae andsponges have been utilized as biomonitors to indicate metal avail-ability in marine environments (Roberts et al., 2008). Sponges—animals of the phylum Porifera—have been recommended as asuitable biomonitor species for metal pollution because of theirstrong ability to concentrate metals in their tissues (Berthetet al., 2005; Patel et al., 1985; Johnston and Clark, 2007; Cebrianet al., 2007). They are one of the major benthic groups with a prom-inent role in many coral reef communities around the world,including in the Red Sea ecosystems (Ilan et al., 2004). Spongescan not only absorb dissolved metals but also take up particulatemetals by filtrating suspended matters. Meanwhile, sponges them-selves act as biogenic habitats that support abundant and highlydiverse epifaunal and infaunal microbial communities which makeup significant biomass of their host. To date, the number of studiesemploying sponges as biomonitors for metal contamination in theRed Sea is still limited despite their huge potential.

The aims of this study were therefore to perform a baselineinvestigation of the state of metal pollution along the eastern coastof the Red Sea by measuring the total metal concentrations andgeochemical speciation of metals in the sediments, and to evaluatethe use of sponges as biomonitors for metal contamination in thearea.

Sediments and sponges were collected from nine sites locatedalong the eastern coast of the Red Sea in Saudi Arabia in April2009. Both pristine areas and areas affected by human activitieswere included. The location of each site is shown in Fig. 1 and Ta-ble 1. The inner bay, marine station, treatment plant outfall, fishmarket and its entrance area in Obhor Sharm were considered asareas affected by human activities, whereas the bay outlet, themangrove site, Abu Madafi reef and the non-reef reference site inObhor Sharm were considered as pristine sites away from humandisturbance. Abu Madafi Reef is one of the most well-preserved

Fig. 1. Sampling sites along the eastern coast of the Red Sea, the Kingdom of SaudiArabia. Abbreviations are defined in Table 1.

coral reefs in the Red Sea; the non-reef reference site was selectedfor comparisons. The top 3–5 cm of surface sediments and spongesamples were collected by a scuba diver or a snorkeler at each site(n = 3), depending on the water depth (1–30 m). Sediment sampleswere stored at 4 �C, while sponge samples were stored at �20 �Cprior to metal analysis. Separate specimens of each sample werepreserved in 70% ethanol for species identification.

Upon transportation back to the laboratory, sediments werefreeze-dried and large stones and debris were removed. The finefraction of sediment (<63 lm) was separated by passing it througha polyethylene sieve. The <63 lm fraction was used because thisfraction proved to be the most chemically active sediment phase,consisting primarily of clay and silt particulates (Förstner, 1987).The sponge samples were carefully rinsed with 0.22 lm filteredseawater to clean off any foreign material such as loosely-boundsediments and epibionts, and were later freeze-dried. Homoge-nized samples were made by cutting the sponges into small piecesfollowed by grounding with a mortar and pestle.

To measure the total metal contents in the sediment samples,approximately 0.2 g of the representative sample was placed intoa Teflon reactor, and then digested in a solution consisting of2 mL of 70% Suprapur nitric acid (HNO3), 6 mL of 37% hydrochlo-ride acid (HCl) and 100 lL of hydrofluoric acid (HF) at a tempera-ture of 180 �C for 15 min in a microwave digestion system(BERGHOF� Speedwave MWS-3, Germany). Approximately 0.2 gof sponge samples were digested with 3 mL of 70% nitric acidand 1 mL of H2O2 as described in previous studies (Cebrian et al.,2007). The digested samples were measured for Cd, Zn, Ag, Cu,As and Pb using an atomic absorption spectrometer (AAS, PerkinEl-mer, AAnalyst 800) or an inductively coupled plasma optical emis-sion spectrometer (ICP-OES, PerkinElmer, Optima 7000 DV). TotalHg concentrations were measured by employing QuickTrace™ M-8000 Cold Vapor Atomic Fluorescence mercury analyzer (USA).Cd, Zn, Cu, Ag, As and Hg were analyzed in this study because theyare common metal contaminants and reports of Ag and Hg valuesfor the Red Sea coasts are rare. The analytical accuracy waschecked by concurrent digestion and comparing measurementswith NIST reference materials: estuarine sediment (SRM 1646a)and oyster (SRM 1566b). The recoveries were all within 90–110%of the reference values and the data were not corrected forrecovery.

Metal speciation of Cd, Zn, Pb, Ag, and Cu was only measured inthe sand-silt texture samples collected from the inner bay, fishmarket and its entrance area in Obhor Sharm (S3, S8 and S9). Metalspeciation in the sediments was quantified using the sequentialextraction method described in previous studies (Tessier et al.,1979; Fan et al., 2002b). The five operationally defined geochemi-cal fractions were as follows:

(1) Phase 1 (exchangeable fraction): extracted by placing in 1 MMgCl2 at pH = 7 for 1 h.

1142 K. Pan et al. / Marine Pollution Bulletin 62 (2011) 1140–1146

(2) Phase 2 (carbonate bound fraction): extracted by placing in1 M NaOAc at pH = 5 for 5 h.

(3) Phase 3 (Fe or Mn oxides bound fraction): extracted by plac-ing in 0.04 M NH2OH-HCl in 25% HOAc for 6 h at 96 �C.

(4) Phase 4 (organic matter bound fraction): extracted by plac-ing in 0.02 M HNO3 and 30% H2O2 (adjusted to pH = 2 withHNO3) at 85 �C for 2 h, followed by the addition of 30%H2O2 for another 3 h. After cooling, 3.2 M NH4OAc in 20%HNO3 was added and the mixture was continuously agitatedfor 30 min.

(5) Phase 5 (residual phase): extracted by placing in concen-trated HNO3 (70%) and HClO4 (60%) and heated to dryness.The remaining material was further digested in 10 ml of2% HNO3 at 70 �C for 1 h.

Following each extraction in steps (1)–(4), the mixtures werecentrifuged at 4000 rpm for 30 min at room temperature and thesupernatants were heated to dryness in an aluminum heatingblock at 140 �C. The remaining material was further digested in10 mL of 2% HNO3 at 70 �C for 1 h. Recoveries of the metals werechecked by extracting the metals from NIST 1646a sediments usingthe same procedure above. Metal concentrations of the extractedsolution were measured using the same AAS from PerkinElmer asdescribed above.

Statistical analysis was performed using the SPSS� 16.0 soft-ware package. All the data were tested for homogeneity of varianceand normal distribution before the statistical analysis. Statisticallysignificant differences among the sites/sponges were detectedthrough one-way analysis of variance using a least-significant-difference post hoc test (p < 0.05). Differences in metal concentra-tion in sediments were assessed by one-way ANOVA. Differences inmetal accumulation between Hyrtios erectus and Stylissa carteriwere analyzed by two-way ANOVA. Regression analysis of themetal concentrations in H. erectus and S. carteri was performedusing the software package SigmaPlot 9.0.

The total metal concentrations in the sediments collected fromnine sampling sites are summarized in Table 2. Huge differences(up to 20 times) in metal concentrations were observed betweenthe least and the most contaminated site, showing the contrastingvariation in mineralogical composition or the different levels ofanthropogenic input at each site. The concentration range for eachmetal was: 0.024–0.24 mg kg�1 for Cd, 5.3–179.0 mg kg�1 for Zn,0.05–0.95 mg kg�1 for Ag, 0.45–82.99 mg kg�1 for Cu, 0.46–69.38mg kg�1 for Pb, 1.4–21.0 mg kg�1 for As, and 3.0–132.8 lg kg�1

for Hg. A relatively higher metal concentration was found in innerObhor Sharm bay (S3) and the adjacent areas of the fish market (S8

Table 2Metal concentration in the Red Sea sediment samples (mean ± SD, mg kg�1, except lg kg�

concentrations and numerical sediment quality guidelines.

Site Cd Zn Ag

S1 Obhor Sharm (outlet) 0.035 ± 0.007 10.0 ± 0.6 0.050 ± 0.0S2 Marine station 0.024 ± 0.005 9.0 ± 0.6 0.067 ± 0.S3 Obhor Sharm (inner) 0.049 ± 0.009 45.5 ± 1.5 0.060 ± 0.0S4 Abu Madafi reef 0.027 ± 0.004 5.3 ± 0.4 0.069 ± 0.S5 Non-reef reference site 0.027 ± 0.002 4.9 ± 0.9 0.071 ± 0.S6 Mangrove site 0.029 ± 0.003 13.8 ± 0.4 0.068 ± 0.S7 Treatment plant outfall 0.080 ± 0.021 46.6 ± 1.4 0.138 ± 0.S8 Entrance of fish market 0.110 ± 0.024 39.3 ± 1.3 0.387 ± 0.S9 Fish market 0.238 ± 0.024 179.0 ± 28.8 0.945 ± 0.

Crust concentrationa 0.098 71 0.05SQG TEC 0.99 120 1.6SQG MEC 3.0 290 1.9SQG PEC 5.0 460 2.2

TEC, threshold effect concentration; MEC, median effect concentration; PEC, probable efa (Taylor and Mclennan, 1995; Hare et al., 2010).

and S9), due possibly to the result of high shipping activities in theareas. The fish market (S9) was the most polluted site out of allnine sites sampled in terms of the total metal concentrations ofCd, Zn, Ag, Cu, and Pb (p < 0.01). The pristine sites, the bay outletof Obhor Sharm, the mangrove site, Abu Madafi reef and thenon-reef reference site, accumulated much less metals in the sed-iments. The sediments deposited in the Red Sea coastal areas canbe classified into three principle categories: biogenous, terrigenousand authigenic. Biogenous sediments are mainly composed oferoded coral reefs and various calcareous remains from marineorganisms (Basaham, 2009). High carbonate contents are generallyassociated with low concentrations of trace metals (Rubio et al.,2000). The low metal contents found in S4 may be due to the high-er proportions of biogenic carbonate and aragonite in the samplesthat originated from the coral areas. When compared to numericalsediment quality guidelines (SQGs, Long et al., 1998; MacDonaldet al., 2000), the concentrations of Zn, Cu, and Pb in the fish market(S9) exceeded the threshold effect concentration (TEC, Table 2), butbarely reached or exceeded the median effect concentration (MEC).The concentration of arsenic (As) in the mangrove site exceededthe MEC, indicating possible As contamination in the area. The con-centrations of metals in other sites were far below the TEC or theaverage crust concentration. Generally, the metal concentrationsof most sites in our study were low, indicating that the local envi-ronment was less affected by metal contamination than otherindustrialized coastal areas.

Metals were sequentially extracted from select sediment sam-ples, all of which had a sand-silt texture, from Site 3, Site 8, and Site9 (Fig. 2). The portion of metals distributed in the exchangeablephase, an indication of the anthropogenic origin and of high poten-tial bioavailability, were found to be low (<10%) for all metals andfor all sites. Fe or Mn oxides were important binding sites for Cd,Zn, and Pb in the sediments from the three sites (30–60%). Thetwo oxides are important metal scavengers in sediments throughvarious mechanisms including coprecipitation, adsorption, surfacecomplex formation, ion exchange and penetration of the lattice(Filgueiras et al., 2002). Cu was found to be mainly bound to the or-ganic fraction in the samples collected from the fish market (S9).This may be due to the high input of organic matters from the fishmarket itself. Cu can easily form complexes with organic matterdue to the high stability constant of the organic–Cu complex. Theclose association of Cu with the organic phase indicated theanthropogenic origin of this metal (Fan et al., 2002b). A significantportion (30–90%) of Ag, Cu, and Zn was also distributed in the res-idue fraction, indicating their principally non-anthropogenic ori-gin. Although the Ag concentration in Site 9 was high, it

1 for Hg, dry weight basis, n = 3). Results are compared with crust metal background

Cu Pb As Hg

03 0.69 ± 0.09 0.93 ± 0.15 1.5 ± 0.6 3.7 ± 0.9012 1.44 ± 0.09 2.74 ± 0.29 4.2 ± 0.3 40.4 ± 9.4

02 18.48 ± 0.45 5.79 ± 0.18 6.3 ± 0.9 9.8 ± 0.7001 0.65 ± 0.20 0.49 ± 0.06 1.4 ± 0.8 3.2 ± 0.3001 0.45 ± 0.12 0.46 ± 0.06 2.1 ± 0.7 3.0 ± 0.3004 5.99 ± 0.23 1.52 ± 0.44 21.0 ± 7.7 4.6 ± 0.8002 8.69 ± 3.55 1.48 ± 0.21 2.2 ± 0.9 18.6 ± 4.2014 21.38 ± 0.66 2.72 ± 0.37 5.9 ± 1.1 50.4 ± 7.3054 82.99 ± 6.04 69.38 ± 7.55 2.5 ± 0.9 132.8 ± 20.0

25 20 1.5 2032 36 9.8 18091 83 21.4 640150 130 33 1100

fect concentration; SQG, sediments quality guidelines.

Cd

S3 S8 S90

20

40

60

80

100

Exchangeable

Carbonate

Fe & Mn oxides

Organic matters

Residue

Ag

S3 S8 S9

% E

xtra

cted

0

20

40

60

80

100Pb

S3 S8 S9

Zn

Site

S3 S8 S9

0

20

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60

80

100Cu

Site

S3 S8 S9

Fig. 2. Relative distribution of metals in different geochemical species and in sediments.

K. Pan et al. / Marine Pollution Bulletin 62 (2011) 1140–1146 1143

appeared that 95% of the Ag was bound to the residue fraction.Metals distributed in the residual phase are generally assumed tohave low mobility and bioavailability. Overall, the results ofsequential extraction further confirmed that the anthropogenic in-

Table 3Metal concentration in sponge samples (mean ± SD, mg kg�1, except lg kg�1 for Hg, dry w

Sponge species Sampling location Cd Zn

Hyrtios erectus S1 0.19 ± 0.05 24.3 ± 0.7S2 0.23 ± 0.09 34.3 ± 3.2S4 0.33 ± 0.03 7.7 ± 1.4S5 0.56 ± 0.05 96.0 ± 15.9

Hyrtios sp. S5 0.43 ± 0.05 27.1 ± 1.6Stylissa carteri S1 0.17 ± 0.02 13.9 ± 1.3

S2 0.17 ± 0.07 18.0 ± 1.5S4 0.22 ± 0.07 5.6 ± 0.6S5 0.14 ± 0.05 47.5 ± 8.6

Chalinula sp. S1 0.75 ± 0.04 179.6 ± 6.0S2 0.27 ± 0.03 200.7 ± 5.0

Xestospongia testudinaria S1 0.16 ± 0.08 14.2 ± 1.2S2 0.49 ± 0.11 19.5 ± 2.0

Phyllospongia papyracea S2 0.23 ± 0.04 55.1 ± 6.3Amphimedon sp. S5 0.03 ± 0.02 86.7 ± 14.0Spongia arabica S6 0.69 ± 0.11 43.6 ± 5.5Spheciospongia inconstans S6 21.5 ± 5.10 154 ± 19.3

put of metals was not significant in the studied areas except in thefish market.

A total of nine species of sponges was collected from S1, S2, S4,S5 and S6 as listed in Table 3. The pattern of the bioaccumulation of

eight basis, n = 3).

Ag Cu Pb As Hg

0.07 ± 0.02 23.9 ± 2.7 0.44 ± 0.02 23.5 ± 0.6 361 ± 17.90.04 ± 0.01 19.3 ± 4.4 0.29 ± 0.02 63.9 ± 7.0 360 ± 31.20.06 ± 0.01 18.4 ± 1.0 0.43 ± 0.06 15.0 ± 1.1 164 ± 20.70.22 ± 0.02 25.3 ± 1.3 0.35 ± 0.01 48.8 ± 4.9 384 ± 55.90.07 ± 0.01 6.7 ± 1.6 0.44 ± 016 2.3 ± 0.5 60.2 ± 7.00.05 ± 0.01 21.2 ± 1.1 0.56 ± 0.07 10.7 ± 4.8 74.6 ± 8.50.06 ± 0.01 16.3 ± 1.2 0.24 ± 0.02 8.1 ± 3.5 63.0 ± 10.10.06 ± 0.01 11.2 ± 0.9 0.36 ± 0.04 8.0 ± 3.8 55.5 ± 5.30.05 ± 0.01 22.5 ± 4.8 0.37 ± 0.23 7.5 ± 1.4 120 ± 4.40.06 ± 0.01 9.1 ± 0.7 0.73 ± 0.05 13.7 ± 2.2 108 ± 10.20.05 ± 0.01 15.5 ± 1.2 0.88 ± 0.10 22.1 ± 2.4 160 ± 7.00.06 ± 0.02 4.5 ± 1.1 0.28 ± 0.05 20.7 ± 2.1 231 ± 7.00.07 ± 0.02 6.7 ± 2.1 0.27 ± 0.04 42.2 ± 3.9 274 ± 20.20.08 ± 0.01 22.4 ± 2.1 2.07 ± 0.23 8.0 ± 2.2 29.8 ± 1.50.03 ± 0.01 8.3 ± 0.8 0.43 ± 0.01 11.2 ± 11.8 124 ± 3.50.09 ± 0.01 22.7 ± 2.3 1.79 ± 0.63 106.1 ± 6.5 266 ± 28.00.01 ± 0.01 8.0 ± 1.5 0.73 ± 0.22 15.0 ± 3.0 16.2 ± 0.6

1144 K. Pan et al. / Marine Pollution Bulletin 62 (2011) 1140–1146

metals varied among different species. Although the metal concen-trations in the ambient environments were low, significant accu-mulation of Cd, Zn, Cu, and Hg was found in the sponges. In factthe concentrations of metals in these sponges were several to hun-dreds of times higher than those in the sediments reported in pre-vious studies (Patel et al., 1985; Philp, 1999; Cebrian et al., 2007).For example, the concentration of Zn in Chalinula sp. was found tobe 180–200 lg g�1, which was higher than the reported values(�100 lg g�1) in some bivalve species such as clams and greenmussels (Blackmore, 1998). The strong ability to accumulate met-als in sponges may be attributed to their high filtration rates of sea-water (Hansen et al., 1995; Turon et al., 1997). For example,Riisgärd et al. (1993) reported that the maximum pumping ratefor Halichondria panacea and Haliclona urceolus can be up to86 L day�1 g�1. Both metals dissolved in water and adsorbed onparticles can be accumulated by sponges because sponges can re-tain up to 80% of suspended particles including the free-living bac-teria particles and the size of the particles retained can be as smallas 0.028 lm (Reiswig, 1971; Milanese et al., 2003). In contrast, theconcentrations of Ag and Pb in sponges were found to be compara-ble to those in sediments, suggesting that the enrichment factors ofAg and Pb were lower than those of the other metals. Indeed,Cebrian et al. (2007) observed that sponges contained a low Pbconcentration even in an environment highly contaminated byPb, indicating that Pb was less bioaccumulated by sponges thanthe other metals.

Distinct metal concentrations were found for different spongespecies collected from the same sites. For example, H. erectus gen-erally had higher metal concentrations of Zn, As, Hg than S. carteri.A typical concentration of around 300 ng g�1 Hg was found for H.erectus, which was higher than that for S. carteri (p < 0.01). Mostsponge species generally had relatively low Zn concentrations(<50 lg g�1 except for S. inconstans), but Chalinula sp. accumulatedup to 200 lg g�1 of Zn which was several times higher than the lev-els accumulated by the other sponges sampled from the same sites(p < 0.01). A high concentration of Cd (21.5 lg g�1) was found in S.inconstans. Interestingly, Zn was also highly accumulated in thissponge (154 lg g�1). The enrichment factor of Cd (calculated asthe ratio of metal concentration to that of sediments) for S. incon-stans was 700, which was about 70 times that of other sponge spe-cies. The background level of dissolved Cd in the pristine sites wasreported to be 20–40 ng L�1 (Hall et al., 1996; Jensen and Bro-Rasmussen, 1992). The bioconcentration factor of Cd for S. incon-stans reached 106 L kg�1, indicating the sponge’s special preferencefor Cd. Another species of sponge S. arabica accumulated relativelyhigh concentrations of As and Hg (106 lg g�1 and 265 ng g�1,respectively). However, the reason why the sponges accumulatedsuch high concentrations of specific metals remains unclear.

The interspecies variations in metal concentrations observed inthe sponges in this study are not uncommon. Patel et al. (1985)measured the concentrations of 17 trace metals in two species ofsponges, Spirastrella scupidifera and Prostylyssa foetida, and foundthat the former accumulated significantly higher Ni (400–2250 lg g�1) than the latter (7–15 lg g�1). It was possible thatthe interspecies difference may reflect the dissimilarity of pumpingphysiology in various species, such as the volume of choanocytechambers (Cebrian et al., 2007). Other studies attributed the vari-ation to the influences of environmental conditions such as pH,salinity and geographical features (Philp, 1999; Bargagli et al.,1996). Apart from the above factors, it is possible that the arrayof microorganisms attached to the sponges may also contributeimportantly to the metal accumulation, an area remains ratherunexplored in previous studies. In this study, there was actuallycontrasting difference in the microbial community structure forH. erectus and S. carteri. Proteobacteria, Firmicutes and Chloroflexialtogether constitute up to 52–73% of the community attached to

H. erectus, while Proteobacteria was the major phylum in S. carteriand made up 60% of the community (Lee et al., 2010). Such specificdifference in the microbial community structure may also beresponsible for the different accumulation patterns of Zn, As, andHg between the two species. Sponges are ecologically diverse hot-spots of unexplored microbial communities. Bacteria, unicellularalgae, cyanobacteria, dinoflagellates, zoochlorellae and domainArchaea have been found to attach themselves to the sponges inthe extra- and intra-cellular spaces (Lee et al., 2009). The presenceof sponge-associated bacteria can have significant impact on themetal concentrations in marine sponges, because they can accountfor up to 40–50% of a sponge’s biomass (Hentschel et al., 2002;Selvin et al., 2009). On the one hand, bacteria are efficient metalbioaccumulators that either adsorb or absorb metals because oftheir high surface-volume ratio (Dixon et al., 2006; Chen et al.,2008). It has been shown that the accumulation of metals is alsospecies-specific for bacteria (Vogel and Fisher, 2010). On the otherhand, bacteria can facilitate metal uptake in the organisms they areattached to. For example, Sayler et al. (1975) found that mercuryconcentrations were 200 times greater in tissue fractions of theoyster Crassostrea virginica dosed with the mercury-metabolizingbacteria Pseudomonas compared with oysters not dosed with thebacteria in the control. Therefore, it is reasonable to think thatthe specific bacterial communities attached to the sponges canaffect the interspecies metal accumulation patterns of their hosts.

Currently there are about 240 known species of sponge in theRed Sea, with many species uninvestigated (Ilan et al., 2004;Radwan et al., 2010). Because of their abundant resources andstrong capacities for metal accumulation, sponges appear to bepromising biomonitors for the Red Sea coastal environment.Sponges show a wide distribution in coastal environments, andare available all year round, are abundant in sublittoral areas,and are easy to transplant (Cebrian et al., 2007). They are sedentarybenthic invertebrates which means that the accumulated contam-inants detected are representative of the ones found in the area.The concentrated metals in sponge tissues allow more simple mea-surements of metals to be carried out than the critical techniquesrequired for the typical water analysis. Our results show thatsponges had species-specific affinities for metals, which suggeststhat biomonitoring data for a certain contaminant should be com-pared intraspecifically. Attention should be given to the accumula-tion strategy when employing sponges as biomonitors. A strongnet accumulator is better than a weak one for monitoring pro-grammes. For example, it may be more appropriate to use S. incon-stans and Chalinula sp. to monitor Cd and Zn contamination,respectively, because they can accumulate the respective metalsreadily. Employing multiple species of sponges may generate com-plementary results.

A biomonitor should be able to accumulate a considerable con-centration of contaminant in relation to the average contaminantconcentration in its ambient environment. Cebrian et al. (2007)found significant positive relationships between the metals accu-mulated in the sediments and in the sponges found in Mediterra-nean coasts. Such relationships were not found in our studypossibly because only a limited number of sponge samples wereavailable from each sampling site, and the metal exposures amongdifferent sites in which sponges were collected were similarly low.However, it is noted that the accumulation of metals in sponges oc-curs both directly from dissolved metals via water filtration, aswell as from particulate metals when food particles are retainedby the sponges (Roberts et al., 2008). Metal concentrations in thesediment provide valuable information about metal contaminationin the ambient environment but do not supply comparative infor-mation about the metals’ bioavailability to sponges. Beside metalconcentrations in ambient environments, geographical featuressuch as water currents may also affect the accumulation of metals

Cu0

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etal

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cent

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n in

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arte

ri (µ

g g-1

)

0

15

30

45

60y=0.47x+2.0

r2=0.99 p <0.01

Pb

Metal concentration in H.erectus (µg g-1)

0.0

0.2

0.4

0.6

0.8

Hg

0 10 20 30 400 30 60 90 120

0.0 0.2 0.4 0.6 0.8 0.1 0.2 0.3 0.4 0.5

0.00

0.05

0.10

0.15

0.20

y=1.4x-13.6

r2=0.80 p <0.05

Fig. 3. Relationship between the metal concentrations in the sponges H. erectus and S. carteri collected concurrently from four different sites (n = 3).

K. Pan et al. / Marine Pollution Bulletin 62 (2011) 1140–1146 1145

in sponges. Bargagli et al. (1996) suggested that intense upwellingcurrents were responsible for a high accumulation of cadmium byAntarctic sponges grown in the pristine Antarctic areas. Uncertain-ties remain about the contribution of dissolved metals and the ef-fects of other geographical factors on the overall metalaccumulation in sponges in our study. Interestingly, significantrelationships were found between the Zn and Cu accumulated inH. erectus and S. carteri collected from different sites (Fig. 3), imply-ing that there was a positive relationship between the metal con-centrations in the sponges and the bioavailability of Zn and Cu atthese sites. The results also suggest the feasibility of employingmulti-species of sponges in biomonitoring to provide more reliableand consistent results.

The metal concentrations in sediments collected from the ninesampling sites were low. Both the total concentration and the geo-chemical speciation of metals showed that metal contaminationwas not significant in most of the studied areas. Only the fish mar-ket and its adjacent areas were moderately metal contaminated.Sponges accumulated much higher metal contents than thesediments although the metal exposure was low in the ambientenvironment. Significant interspecies variations in the metalaccumulation patterns were found in the sponges. Sponges in theRed Sea appear to be promising biomonitors of metal contamina-tion because of their excellent ability to accumulate specificmetals.

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