Exposure assessment for trace elements from consumption of marine fish in Southeast Asia

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Environmental Pollution 145 (2007) 766e777www.elsevier.com/locate/envpol

Exposure assessment for trace elements from consumptionof marine fish in Southeast Asia

Tetsuro Agusa a, Takashi Kunito b, Agus Sudaryanto a, In Monirith a, Supawat Kan-Atireklap a,Hisato Iwata a, Ahmad Ismail c, Joompol Sanguansin d, Muswerry Muchtar e,

Touch Seang Tana f, Shinsuke Tanabe a,*

a Center for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japanb Department of Environmental Sciences, Faculty of Science, Shinshu University, 3-1-1 Asahi, Matsumoto 390-8621, Japan

c Department of Biology, Faculty of Science and Environmental Studies, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysiad Eastern Marine Fisheries Development Center, Ban Phe, Muang, Rayong 21160, Thailand

e Research and Development Center for Oceanology Indonesia Institute of Sciences, Jl. Pasir Putih 1, Ancol Timur, Jakarta 11048, Indonesiaf Social and Cultural Observation Unit (OBSES), Office of the Council of Ministers, Phnom Penh, Cambodia

Received 15 February 2006; received in revised form 3 April 2006; accepted 4 April 2006

Intake of mercury through consumption of some marine fish species might be hazardous to the people in Southeast Asia.

Abstract

Concentrations of 20 trace elements were determined in muscle and liver of 34 species of marine fish collected from coastal areas ofCambodia, Indonesia, Malaysia and Thailand. Large regional difference was observed in the levels of trace elements in liver of one fish family(Carangidae): the highest mean concentration was observed in fish from the Malaysian coastal waters for V, Cr, Zn, Pb and Bi and those from theJava Sea side of Indonesia for Sn and Hg. To assess the health risk to the Southeast Asian populations from consumption of fish, intake rates oftrace elements were estimated. Some marine fish showed Hg levels higher than the guideline values by U.S. Environmental Protection Agency andJoint FAO/WHO Expert Committee on Food Additives (JECFA). This suggests that consumption of these fish may be hazardous to the people.� 2006 Elsevier Ltd. All rights reserved.

Keywords: Trace elements; Fish; Risk assessment; Southeast Asia

1. Introduction

Anthropogenically-derived trace elements are widely re-leased into the marine environment (Nriagu and Pacyna,1988). It is known that global anthropogenic emissions arelarger than or comparable to natural emissions for the mostof trace elements (Pacyna and Pacyna, 2001). Large emissionand contamination of trace elements are of concern at presentin Asian developing countries because of the rapid economicgrowth and increasing population in recent years.

* Corresponding author. Tel./fax: þ81 89 927 8171.

E-mail address: shinsuke@agr.ehime-u.ac.jp (S. Tanabe).

0269-7491/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.

doi:10.1016/j.envpol.2006.04.034

Seafood is an important source of protein and income forpeople in Southeastern Asia. However, harmful substances in-cluding toxic elements (e.g., Hg, Cd and Pb) released by hu-man activities have contaminated the marine environment.For instance, the Straits of Malacca, an important fishingground (Eng et al., 1989), is seriously contaminated by inter-national shipping activity, heavy industrialization and urbani-zation, and oil spills (Eng et al., 1989; Abdullah et al.,1999). Trace elements released from anthropogenic sourcesmay be accumulated in marine organisms through the foodweb. Hence, human health risks may occur through the con-sumption of seafood contaminated by trace elements. How-ever, available studies on trace elements (heavy metal)concentrations in marine organisms from Southeast Asia

767T. Agusa et al. / Environmental Pollution 145 (2007) 766e777

(Law and Singh, 1991; Sin et al., 1991; Ismail et al., 1995;Kambey et al., 2001; Yap et al., 2002, 2004; Agusa et al.,2005) are limited. Moreover, there are few studies on the as-sessment of the human health risk by trace elements throughseafood consumption in Southeast Asian countries (Agusaet al., 2005).

In the present study, concentrations of 20 trace elements (V,Cr, Mn, Co, Cu, Zn, Se, Rb, Sr, Mo, Ag, Cd, Sn, Sb, Cs, Ba,Hg, Tl, Pb and Bi) were determined in 235 specimens of ma-rine fish collected from coastal areas in Cambodia, Indonesia,Malaysia and Thailand. Human dietary exposure of trace ele-ments from consumption of marine fish and risk assessmentwere also estimated.

2. Materials and methods

2.1. Samples and sampling locations

A total of 235 fish samples representing 34 species (Table 1) were col-

lected in several locations from Cambodia (C1, Koh Kong; C2, Sihanouk

Ville; and C3, Kampot); Indonesia (I1, Kamal; I2, Lada Bay; and I3, Bondet);

Malaysia (M1, Cabang Tiga; M2, Kuala Terengganu; M3, Mersing; M4, Parit

Jawa; M5, Port Dickson and M6, Langkawi) and Thailand (T1, Rayong; T2,

Trat; T3, Prachuap Khiri Khan; T4, Khlong Yai; T5, Pak Namkra Dae; T6, Pat-

tani; T7, Song Khla; T8, Krabi; T9, Trang; T10, Phang Nga; T11, Ranong;

T12, Smaut Sakorn; and T13, Smaut Parkarn) from 1995 to 1999. The sample

details and sampling locations are shown in Table 1 and Fig. 1, respectively.

Fish samples were put into clean polyethylene bags and stored at �20 �C until

chemical analyses.

2.2. Analytical procedures

Analytical procedure of trace elements in fish samples followed the previ-

ous study (Anan et al., 2001). Livers (n ¼ 226) and muscles (n ¼ 235) of fish

were oven-dried at 80 �C for 12 h and were homogenized. About 0.1 g of pow-

dered sample was digested in a microwave oven with 1.5 ml of nitric acid.

Eighteen trace elements (V, Cr, Mn, Co, Cu, Zn, Rb, Sr, Mo, Ag, Cd, Sn,

Sb, Cs, Ba, Tl, Pb and Bi) were determined with an inductively coupled

plasma-mass spectrometer (ICP-MS) (HP-4500; Hewlett-Packard, Avondale,

PA, USA) with Y as the internal standard. Mercury and Se were detected by

a cold vapor atomic absorption spectrometer (model HG-3000; Sanso,

Tsukuba, Japan) and a hydride generation atomic absorption spectrometer

(HVG-1 hydride system; Shimadzu, Kyoto, Japan), respectively. Standard

reference materials, SRM1577b (bovine liver; National Institute of Standards

and Technology, Gaithersburg, MD, USA) and DORM2 (dogfish muscle;

National Research Council Canada, Ottawa, ON, Canada) were used to assess

the accuracy of the analysis. Recoveries of all the elements ranged from 88%

to 130% of the certified value.

2.3. Statistics

Statistical analyses were executed by the programs StatView (version 5.0,

SAS� Institute, Cary, NC, USA) and SPSS (version 12.0J, SPSS Inc.,

Chicago, IL, USA). Half the value of the respective limit of detection was

substituted for those values below the limit of detection for use in statistical

analysis. All data were tested for fitness to a normal distribution by the Kol-

mogoroveSmirnov one-sample test. Because most of variables were not nor-

mally distributed, they were logarithmically transformed before parametric

analysis. Pearson’s correlation coefficient was used to measure the strength

of the association between trace element concentration in liver and muscle.

To compare concentrations of trace elements between liver and muscle,

a two-group t-test was used. Regional and species differences in trace element

concentrations of liver were tested by two-factor analysis of variance (AN-

OVA). Because species difference and interaction between region and species

on trace element concentrations were observed, TukeyeKramer method,

along with one-factor ANOVA was conducted using one fish family (Carangi-

dae) for the detection of site-specific accumulation of trace elements. A p

value of less than 0.05 was considered to indicate statistical significance in

this study. The three levels of significance were set at p < 0.05, p < 0.01

and p < 0.001.

3. Results and discussion

3.1. Concentrations of trace elements in liver and muscleof marine fish

Concentrations of trace elements in liver and muscle of ma-rine fish are shown in Tables 2 and 3, respectively. Among allthe species of marine fish, Zn (geometric mean (GM); 102 mg/gdry wt.) showed the highest concentration in liver, followedby Cu (11.8 mg/g dry wt.) and Sr (10.6 mg/g dry wt.).Extremely high concentration of Zn (GM; 953 mg/g dry wt.,max; 1,720 mg/g dry wt.) was observed in liver of Kawakawas,suggesting specific accumulation of Zn in this species. In themuscle, Zn (22.7 mg/g dry wt.), Sr (3.71 mg/g dry wt.) andRb (3.21 mg/g dry wt.) were relatively higher among the ele-ments examined. On the other hand, concentrations of Sb, Tland Bi were below detection limit in both tissues in most ofsamples. Thus, these elements were excluded in the furtherdiscussion.

For all the specimens used in the present study, concentra-tions of V ( p < 0.001), Cr ( p < 0.001), Mn ( p < 0.001), Co( p < 0.001), Cu ( p < 0.001), Zn ( p < 0.001), Sr ( p < 0.001),Mo ( p < 0.001), Ag ( p < 0.001), Cd ( p < 0.001), Sn( p < 0.001), Ba ( p < 0.001), Pb ( p < 0.001) and Hg( p < 0.05) in liver were higher than those in muscle, whereasRb ( p < 0.001) and Cs ( p < 0.001) concentrations showed anopposite trend (Fig. 2). Especially, Cd concentration in liverwas about 100 times higher than that in muscle. High accumu-lation of trace elements in liver of fish has also been reported inother studies (Honda et al., 1983; Agusa et al., 2005), suggestingthat liver plays an important role for metabolism of trace ele-ments in fish. High concentrations of Rb and Cs have alsobeen observed in muscle of fish (Yamazaki et al., 1996; Agusaet al., 2005). Similarly, other wild animals such as pinnipeds(Ikemoto et al., 2004) and waterfowls (Nam et al., 2005) alsohave shown high accumulation of Rb and Cs in muscletissue. For all the specimens used, concentrations of V( p < 0.001), Cr ( p < 0.001), Mn ( p < 0.001), Co( p < 0.001), Se ( p < 0.001), Rb ( p < 0.001), Sr ( p < 0.001),Mo ( p < 0.001), Ag ( p < 0.001), Cd ( p < 0.001), Ba( p < 0.001), Hg ( p < 0.001), Pb ( p < 0.001) and Zn( p < 0.05) in liver were positively correlated with those in mus-cle, whereas no correlations were found between liver and mus-cle for Cu and Sn. These trends were similar to those ofa previous study (Agusa et al., 2005). Concentrations of almostall the elements in liver were correlated with those in muscle andwere higher than those in muscle as described above. So, onlythe data on liver were used for further discussion of their speciesor site-specific differences; but the data of muscle were used forevaluating risk assessment.

768 T. Agusa et al. / Environmental Pollution 145 (2007) 766e777

Table 1

Sample information on marine fish from Southeast Asia

Location Common name Scientific name n Total length (cm) Total weight (g)

Cambodia

C1 (GT-C) Koh Kong Bluespot mullet Valamugil seheli 3 21.0e22.5 95e124

Brownstripe red snapper Lutjanus vitta 3 22.8e26.0 171e255

Narrow-barred Spanish mackerel Scomberomorus commerson 3 41.0e43.0 500e600

C2 (GT-C) Sihanouk Ville Bluespot mullet Valamugil seheli 3 20.8e21.6 99e116

Obtuse barracuda Sphyraena obtusata 3 44.0e49.7 55e600

Russell’s snapper Lutjanus russellii 3 20.8e26.0 99e116

Sharptooth jobfish Pristipomoides typus 3 22.2e23.0 134e145

Short mackerel Rastrelliger brachysoma 3 21.0e22.0 121e127

Torpedo scad Megalaspis cordyla 3 22.3e24.0 132e145

C3 (GT-C) Kampot Bluespot mullet Valamugil seheli 3 22.0e23.5 117e153

Frigate tuna Auxis thazard thazard 3 36.0e44.0 265e600

Obtuse barracuda Sphyraena obtusata 3 33.0e49.3 106e282

Indonesia

I1 (JS) Kamal Talang queenfish Scomberoides commersonnianus 3 26.0e30.6 163e246

White-spotted spinefoot Siganus canaliculatus 3 11.5e13.1 24e34

Unknown Sconberomorus sp. 3 28.1e29.0 228e251

I2 (JS) Lada Bay, Panimbang Chacunda gizzard shad Anodontostoma chacunda 3 15.0e15.2 46e55

Indian mackerel Rastrelliger kanagurta 3 22.0e23.2 121e156

Japanese threadfin bream Nemipterus japonicus 3 17.0e17.2 74e81

Red bigeye Priacanthus macracanthus 3 24.5e28.0 199e400

Small-scaled terapon Terapon puta 3 16.1e18.1 70e86

I3 (JS) Bondet, Cirebon Bluetail mullet Valamugil buchanani 3 15.0e17.5 36e59

Chacunda gizzard shad Anodontostoma chacunda 3 13.4e14.2 37e44

Fourfinger threadfin Eleutheronema tetradactylum 3 21.0e23.5 102e115

Sharpnose hammer croaker Johnius borneensis 3 16.0e17.0 49e53

Malaysia

M1 (SCS) Cabang Tiga, Kelantan Fork-tailed threadfin bream Nemipterus furcosus 5 20.0e20.8 85e107

Kawakawa Euthynnus affinis 5 38.5e41.2 700e1000

Torpedo scad Megalaspis cordyla 6 24.0e26.0 157e214

M2 (SCS) Kuala Terengganu, Terengganu Bigeye scad Selar crumenophthalmus 4 20.5e22.5 98e103

Redtail scad Decapterus kurroides 5 24.0e25.5 185e209

M3 (SCS) Mersing, Johor Bigeye scad Selar crumenophthalmus 5 21.0e23.0 114e145

Indian mackerel Rastrelliger kanagurta 5 19.6e21.2 91e108

Javelin grunter Pomadasys kaakan 7 18.7e21.0 90e153

M4 (SM-M) Parit Jawa, Johor Bigeye scad Selar crumenophthalmus 5 20.5e22.0 98e116

Doublespotted queenfish Scomberoides lysan 5 27.5e31.3 130e181

M5 (SM-M) Port Dickson, Johor Bigeye scad Selar crumenophthalmus 11 17.0e19.2 60e81

Black pomfret Parastromateus niger 5 20.8e24.0 192e300

Torpedo scad Megalaspis cordyla 5 25.0e28.5 169e239

M6 (SM-M) Langkawi Bigeye scad Selar crumenophthalmus 6 15.0e26.5 38e57

Doublelined tonguesole Paraplagusia bilineata 5 23.0e26.2 42e76

Redtail scad Decapterus kurroides 9 15.0e19.0 29e65

Shortfin scad Decapterus macrosoma 3 17.0e19.8 42e55

Torpedo scad Megalaspis cordyla 5 17.5e28.0 188e203

Yellowfin seabream Acanthopagrus latus 1 22.0 233

Thailand

T1 (GT-T) Rayong Bigeye scad Selar crumenophthalmus 3 20.0e21.4 112e118

Malabar blood snapper Lutjanus malabaricus 3 19.0e21.3 79e107

T2 (GT-T) Trat Bluespot mullet Valamugil seheli 1 20.0 78

Torpedo scad Megalaspis cordyla 1 19.0 66

Whipfin silverbiddy Gerres filamentosus 1 35.5 650

T3 (GT-T) Prachuap Khiri Khan Torpedo scad Megalaspis cordyla 3 19.2e21.0 68e102

T4 (GT-T) Khlong Yai Bluespot mullet Valamugil seheli 3 14.8e18.5 35e59

Tiger-toothed croaker Otolithes ruber 2 23.0e24.5 151e174

Torpedo scad Megalaspis cordyla 2 20.0e20.1 88e106

T5 (GT-T) Pak Namkra Dae Bluespot mullet Valamugil seheli 3 18.2e21.5 61e80

T6 (GT-T) Pattani Bluespot mullet Valamugil seheli 3 16.0e19.4 43e79

T7 (SM-T) Song Khla Bluespot mullet Valamugil seheli 3 21.0e23.5 104e116

Indian mackerel Rastrelliger kanagurta 3 18.9e20.0 64e72

769T. Agusa et al. / Environmental Pollution 145 (2007) 766e777

Table 1 (continued )

Location Common name Scientific name n Total length (cm) Total weight (g)

T8 (SM-T) Krabi Torpedo scad Megalaspis cordyla 3 22.5e24.5 143e185

T9 (SM-T) Trang Torpedo scad Megalaspis cordyla 3 20.9e22.3 88e119

T10 (SM-T) Phang Nga Bluespot mullet Valamugil seheli 3 15.2e17.0 46e54

T11 (GT-T) Ranong Barramundi Lates calcarifer 2 26.5e26.7 242e264

Indian mackerel Rastrelliger kanagurta 3 20.5e23.2 105e154

T12 (GT-T) Smaut Sakorn Barramundi Lates calcarifer 2 27.5e29.0 280e350

Bluespot mullet Valamugil seheli 3 22.3e24.5 111e140

Torpedo scad Megalaspis cordyla 3 19.6e21.0 95e109

T13 (GT-T) Smaut Parkarn Barramundi Lates calcarifer 2 27.0e27.6 321e325

Bluespot mullet Valamugil seheli 3 23.4e25.3 138e161

Torpedo scad Megalaspis cordyla 3 20.0e20.6 91e104

Unknown means that species was not identified.

3.2. Regional differences in concentrations of traceelements in liver of marine fish

Because many fish from geographically dispersed locationswere used in the present study (25 locations and 34 fishspecies; Table 1), it is difficult to clearly assess the regionaldifferences of contamination by trace elements using all thefish samples: the sample size in each sampling point wassmall, and the same species could not be collected in all thelocations (Table 1). Migration of fish species for feeding andreproduction may also affect the geographical differences.Hence, 25 sites were divided into six areas: Gulf of Thailandside of Cambodia (GT-C; C1, C2 and C3), Gulf of Thailandside of Thailand (GT-T; T1 to T6 and T11 to T13), SouthChina Sea side of Malaysia (SCS; M1, M2 and M3), Straightof Malacca side of Malaysia (SM-M; M4, M5 and M6),Straight of Malacca side of Thailand (SM-T; T7 to T10) and

Java Sea side of Indonesia (JS; I1, I2 and I3). At first, weused three fish families (Carangidae, Mugilidae and Scombri-dae) with relatively large number of specimens to determinewhether the pooled data of the three fish families can beused to assess the regional difference in trace element contam-ination or each fish family should be separated from one an-other to avoid effects of species-specific accumulation oftrace elements on the evaluation of regional contamination.

Two-way ANOVA showed significant fish-family specificdifference in trace element accumulation ( p < 0.05) and inter-actions of trace element accumulations between fish familiesand areas ( p < 0.05) for almost all the trace elements. There-fore, one family (Carangidae: torpedo scads, talang queen-fishes, bigeye scads, redtail scads, doublespotted queenfishes,black pomfrets and shortfin scads) was selected to assess theregional difference of contamination by trace elements be-cause they were collected from all the six divided sampling

M5

M6

M4

M3

I3

I2

M2

M1

T5T6

T4

T7

T8

T9

T10

T11

T13 T1

T2

T12

T3 C1

C3

C2

South China Sea

Java Sea

Indian Ocean

I1

Gulf of

Thailand

Thailand

Cambodia

Indonesia

St. of M

alacca Malaysia

Fig. 1. Sampling locations of marine fish in coastal waters of Cambodia, Indonesia, Malaysia and Thailand. The site codes of sampling locations refer to those in

Table 1.

Table 2

Trace element concentrations (geometric mean (n > 1) and individual value (n ¼ 1), mg/g dry wt.) in liver of marine fish from Southeast Asia

Cs Ba Hg Tl Pb Bi

0.02 0.10 <0.05 0.002 0.277 0.001

0.05 0.058 0.35 0.001 0.065 <0.001

0.06 0.050 0.18 0.001 0.047 0.001

0.02 0.029 0.08 <0.001 0.208 <0.001

0.08 0.053 0.90 <0.001 0.229 0.010

0.04 0.14 0.32 0.001 0.069 <0.001

0.06 0.074 1.8 0.004 0.509 0.004

0.02 0.68 0.09 0.017 0.686 <0.001

0.06 0.11 0.15 0.002 0.020 <0.001

0.02 0.061 0.11 <0.001 0.417 0.011

0.06 0.040 0.56 <0.001 0.051 0.013

0.05 0.072 0.35 <0.001 0.050 0.002

0.06 0.022 0.46 <0.001 0.020 <0.001

0.06 0.036 0.47 <0.001 0.022 0.002

0.01 0.082 0.11 0.007 0.116 <0.001

0.06 0.21 1.4 0.029 1.58 0.024

<0.01 0.12 0.28 0.003 0.750 <0.001

0.02 0.075 0.23 0.002 0.391 0.025

0.02 0.033 0.21 <0.001 0.041 <0.001

0.02 0.045 0.34 <0.001 0.043 <0.001

0.01 0.15 0.07 0.005 0.087 <0.001

0.01 0.11 0.29 0.001 0.106 0.019

0.04 0.082 0.14 0.003 0.020 0.004

0.02 0.13 0.25 0.003 0.113 0.034

0.05 0.14 2.4 0.001 0.198 0.048

0.07 0.045 0.10 <0.001 0.041 0.001

0.06 0.18 0.15 <0.001 0.052 0.001

0.02 1.3 0.12 0.016 0.360 0.006

0.04 0.13 0.15 <0.001 0.090 0.007

0.04 0.17 0.26 <0.001 0.240 0.012

0.02 0.27 0.12 0.009 0.380 0.003

<0.01 0.24 0.06 <0.001 0.115 0.018

0.05 0.14 0.12 <0.001 0.068 0.003

0.05 0.039 0.36 <0.001 0.079 0.003

<0.01 0.21 <0.05 0.009 0.670 0.004

0.02 0.34 0.21 <0.001 0.085 0.002

0.05 0.063 0.18 0.001 0.043 0.009

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Location Common name V Cr Mn Co Cu Zn Se Rb Sr Mo Ag Cd Sn Sb

Cambodia

C1 (GT-C) Bluespot mullet (n ¼ 3) 0.70 0.55 2.83 0.31 6.35 50.3 1.1 5.35 6.60 1.17 0.102 0.170 0.001 0.03

Brownstripe red snapper (n ¼ 3) 0.55 0.38 4.24 0.71 26.6 234 4.6 3.29 24.4 0.987 0.084 0.230 <0.001 <0.01

Narrow-barred Spanish

mackerel (n ¼ 3)

0.043 0.50 4.51 0.059 12.0 112 9.7 3.21 3.95 0.400 0.063 0.927 0.090 <0.01

C2 (GT-C) Bluespot mullet (n ¼ 3) 1.1 0.44 17.7 0.35 9.39 64.6 2.1 4.20 4.55 1.42 0.131 0.291 <0.001 <0.01

Obtuse barracuda (n ¼ 3) 0.11 0.43 6.74 0.28 28.0 362 5.3 2.40 4.42 0.485 0.139 5.45 0.024 <0.01

Russell’s snapper (n ¼ 3) 0.049 0.47 3.63 0.13 12.3 106 4.5 2.16 15.7 0.820 0.063 1.32 0.062 <0.01

Sharptooth jobfish (n ¼ 3) 0.49 0.39 4.25 0.20 11.0 115 10 2.36 9.25 0.593 0.032 13.2 0.023 <0.01

Short mackerel (n ¼ 3) 0.31 0.54 3.43 0.18 11.7 148 14 1.92 14.8 0.575 0.144 11.3 0.042 <0.01

Torpedo scad (n ¼ 3) 0.12 0.47 3.46 0.22 27.4 102 13 2.40 8.26 1.02 0.171 9.28 0.087 <0.01

C3 (GT-C) Bluespot mullet (n ¼ 3) 3.1 0.91 2.97 0.37 8.44 73.2 2.1 4.18 6.90 1.19 0.071 0.225 0.037 <0.01

Frigate tuna (n ¼ 3) 0.045 0.34 3.22 0.070 9.02 119 7.1 2.43 2.79 0.424 0.020 1.30 0.186 <0.01

Obtuse barracuda (n ¼ 2) 0.051 0.33 6.09 0.10 29.7 165 4.3 2.04 4.39 0.603 0.085 2.35 0.004 <0.01

Indonesia

I1 (JS) Unknown (n ¼ 3) 0.11 0.43 5.06 0.38 17.0 75.1 6.9 2.47 2.77 0.893 0.080 12.4 0.286 <0.01

Talang queenfish (n ¼ 3) 0.053 0.40 4.62 0.092 11.1 89.3 6.2 2.11 2.80 0.679 0.023 0.261 0.930 <0.01

White-spotted spinefoot (n ¼ 2) 0.66 0.64 42.1 0.90 9.65 82.2 2.1 2.56 9.72 0.821 0.041 0.111 0.271 0.01

I2 (JS) Chacunda gizzard

shad (n ¼ 3)

0.64 0.79 9.28 0.14 25.6 200 5.6 3.95 9.99 0.707 0.103 0.653 0.013 0.02

Indian mackerel (n ¼ 3) 1.2 0.50 2.30 0.40 9.31 96.3 20 1.23 8.05 0.701 0.079 2.62 0.122 0.01

Japanese threadfin

bream (n ¼ 3)

0.32 0.49 8.43 0.36 10.3 84.4 7.9 2.11 7.94 0.815 0.028 1.66 0.204 0.04

Red bigeye (n ¼ 3) 0.086 0.45 3.05 0.056 5.17 93.9 3.5 1.36 2.50 0.205 0.012 1.15 0.116 <0.01

Small-scaled terapon (n ¼ 2) 0.047 0.45 2.01 0.089 6.31 79.2 3.2 1.28 4.42 0.241 0.042 0.330 0.364 <0.01

I3 (JS) Bluetail mullet (n ¼ 3) 1.8 0.64 6.59 0.83 11.1 83.7 4.5 2.89 4.83 0.564 0.029 0.357 0.238 <0.01

Chacunda gizzard

shad (n ¼ 3)

0.39 0.62 6.82 0.28 8.83 62.4 3.4 2.72 3.39 0.558 0.038 0.238 0.136 0.02

Fourfinger threadfin (n ¼ 3) 0.14 0.71 4.21 0.19 11.8 91.1 6.5 2.42 5.22 0.982 0.029 0.184 1.04 0.01

Sharpnose hammer

croaker (n ¼ 2)

0.77 0.55 12.7 1.7 9.90 108 5.4 2.76 8.40 0.389 0.012 0.569 0.146 <0.01

Malaysia

M1 (SCS) Fork-tailed threadfin

bream (n ¼ 5)

0.75 0.98 4.98 0.53 17.8 117 9.4 2.10 10.2 0.660 0.057 8.88 0.412 <0.01

Kawakawa (n ¼ 5) 0.13 0.80 2.21 0.074 17.2 953 8.5 2.45 7.90 0.642 0.325 5.87 0.437 <0.01

Torpedo scad (n ¼ 5) 0.27 0.79 3.22 0.23 29.0 126 8.4 2.77 12.3 0.695 0.033 20.2 0.062 <0.01

M2 (SCS) Bigeye scad (n ¼ 4) 0.26 0.77 1.86 0.12 9.64 151 12 2.56 16.7 0.763 0.074 3.43 1.06 <0.01

Redtail scad (n ¼ 5) 0.21 1.1 1.76 0.14 17.1 119 13 2.25 17.2 0.490 0.266 12.6 0.497 <0.01

M3 (SCS) Bigeye scad (n ¼ 5) 0.41 1.3 3.78 0.40 23.8 158 10 1.78 19.2 1.26 0.098 4.82 0.866 <0.01

Indian mackerel (n ¼ 5) 0.39 0.92 2.43 0.20 17.7 157 10 2.25 9.95 1.18 0.171 3.53 0.575 <0.01

Javelin grunter (n ¼ 5) 0.091 0.97 0.687 0.085 2.62 27.1 1.9 0.667 7.74 0.091 0.012 0.194 0.441 <0.01

M4 (SM-M) Bigeye scad (n ¼ 5) 0.16 0.99 3.48 0.27 13.2 81.9 6.3 1.90 6.30 0.630 0.037 0.865 0.842 <0.01

Doublespotted queenfish (n ¼ 5) 0.10 0.83 5.24 0.11 13.3 162 9.0 2.32 4.16 0.821 0.045 0.245 NA <0.01

M5 (SM-M) Bigeye scad (n ¼ 11) 0.73 1.2 1.52 0.19 7.60 108 7.3 1.54 17.2 0.947 0.033 0.873 0.143 <0.01

Black pomfret (n ¼ 5) 0.33 1.0 5.27 1.6 25.3 179 9.0 3.53 11.2 1.38 0.479 11.3 1.30 <0.01

Torpedo scad (n ¼ 5) 0.11 0.88 5.13 0.27 12.8 86.5 5.6 1.76 3.67 0.926 0.021 1.57 1.69 <0.01

M6 (SM-M) Bigeye scad (n ¼ 6) 2.2 1.2 4.70 0.41 7.68 109 7.4 2.21 47.2 6.86 0.020 1.01 NA <0.01 0.02 4.3 <0.05 0.032 0.792 0.008

0.414 0.044 2.79 0.587 0.04 0.04 0.58 0.24 0.002 0.784 0.097

0.433 0.041 3.59 NA <0.01 0.04 0.50 <0.05 <0.001 0.080 0.004

0.320 0.029 3.74 0.587 <0.01 0.02 0.090 <0.05 <0.001 0.041 0.004

0.564 0.152 33.8 0.552 <0.01 0.05 0.034 0.09 <0.001 0.044 0.001

0.562 0.078 10.8 NA 0.03 0.03 0.30 0.35 <0.001 0.877 0.022

0.569 0.077 11.0 0.217 0.05 0.06 0.38 0.10 0.024 0.153 0.023

0.443 0.019 1.55 0.369 0.01 0.07 0.19 0.44 0.005 0.122 0.020

0.799 0.013 0.098 0.097 <0.01 0.01 0.10 0.13 0.003 0.073 <0.001

0.349 0.007 1.39 0.097 0.01 0.04 0.17 0.43 0.001 0.065 0.006

0.323 0.015 0.492 0.293 <0.01 0.07 0.033 0.44 0.001 0.032 0.009

0.431 0.054 3.67 0.104 <0.01 0.03 0.36 <0.05 0.004 0.025 <0.001

0.744 0.031 0.131 0.221 <0.01 <0.01 0.49 0.07 <0.001 0.198 0.021

0.119 0.011 0.732 0.058 <0.01 0.02 0.23 0.29 0.001 0.074 <0.001

0.233 0.037 1.39 0.171 0.02 0.02 0.15 0.06 0.017 0.045 0.010

1.30 0.118 0.588 0.153 0.03 0.04 0.44 0.14 0.009 0.911 0.078

0.690 0.067 0.131 0.085 <0.01 0.03 0.37 0.08 0.004 0.489 0.060

1.09 0.189 0.413 1.09 0.04 0.11 1.3 0.12 0.017 1.92 0.078

1.61 0.060 2.90 0.138 0.04 0.02 1.2 0.16 0.038 0.864 0.008

0.867 0.167 8.26 0.063 <0.01 0.07 0.81 0.11 0.006 0.027 0.005

0.580 0.240 7.42 0.331 <0.01 0.05 0.42 0.09 0.004 0.050 <0.001

0.424 0.067 0.173 0.135 <0.01 0.10 0.46 0.08 0.005 0.749 0.016

0.194 0.050 0.034 0.088 <0.01 0.09 0.79 0.17 0.011 0.044 0.009

1.20 0.054 2.39 0.012 <0.01 0.02 0.95 <0.05 0.021 0.214 0.002

0.154 0.033 0.084 0.103 <0.01 0.02 0.085 0.05 <0.001 0.003 <0.001

2.42 0.143 0.282 0.389 0.03 0.02 0.32 <0.05 0.007 0.394 0.023

0.639 0.105 7.77 0.184 <0.01 0.04 0.26 0.12 0.001 0.042 0.001

0.226 0.036 0.056 0.143 <0.01 0.01 0.083 <0.05 <0.001 <0.001 <0.001

2.50 0.109 0.268 0.112 <0.01 <0.01 0.21 0.16 <0.001 0.322 0.031

0.466 0.082 4.18 0.090 <0.01 0.03 0.25 <0.05 <0.001 0.003 <0.001

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Doublelined tonguesole (n ¼ 5) 1.3 1.8 8.68 0.14 6.93 105 5.6 2.88 36.5

Redtail scad (n ¼ 9) 0.16 1.1 1.11 0.12 9.91 83.7 6.2 1.94 15.9

Shortfin scad (n ¼ 3) 0.058 0.79 0.861 0.11 8.36 65.3 6.6 1.18 6.27

Torpedo scad (n ¼ 5) 0.12 0.92 3.92 0.17 20.9 107 5.3 2.10 5.50

Yellowfin seabream (n ¼ 1) 2.3 1.4 12.3 0.39 12.7 193 6.4 2.52 19.4

Thailand

T1 (GT-T) Bigeye scad (n ¼ 3) 0.17 0.74 1.40 0.11 10.9 103 14 2.19 21.6

Malabar blood

snapper (n ¼ 3)

0.073 1.0 2.17 0.085 8.55 101 5.1 2.55 19.7

T2 (GT-T) Bluespot mullet (n ¼ 1) 1.3 0.54 2.30 2.9 11.0 68.0 3.3 3.96 6.85

Torpedo scad (n ¼ 1) 0.14 0.54 0.929 0.14 4.96 53.0 4.0 2.48 11.3

Whipfin silverbiddy (n ¼ 1) 0.094 0.57 3.07 0.059 9.01 81.0 5.4 2.75 5.40

T3 (GT-T) Torpedo scad (n ¼ 3) 0.073 0.60 4.33 0.13 9.83 72.7 7.1 2.39 33.5

T4 (GT-T) Bluespot mullet (n ¼ 3) 0.23 0.65 4.68 0.15 6.96 47.1 2.1 1.47 20.6

Tiger-toothed croaker (n ¼ 1) 0.099 0.61 6.74 0.10 4.07 54.9 2.7 1.35 40.4

Torpedo scad (n ¼ 2) 0.054 0.81 1.54 0.052 6.31 40.0 3.2 0.779 10.1

T5 (GT-T) Bluespot mullet (n ¼ 3) 1.2 0.93 13.2 0.25 13.6 126 3.9 4.42 12.9

T6 (GT-T) Bluespot mullet (n ¼ 3) 0.32 0.72 2.07 0.32 8.24 109 3.1 3.04 18.1

T7 (SM-T) Bluespot mullet (n ¼ 3) 1.9 0.69 5.14 0.34 9.24 97.6 2.2 5.58 11.0

Indian mackerel (n ¼ 3) 1.8 0.91 10.8 0.35 7.62 106 10 2.42 24.7

T8 (SM-T) Torpedo scad (n ¼ 3) 0.17 0.74 3.33 0.18 26.2 116 7.1 1.89 35.1

T9 (SM-T) Torpedo scad (n ¼ 3) 0.082 0.59 2.07 0.11 18.0 92.9 6.5 2.41 24.6

T10 (SM-T) Bluespot mullet (n ¼ 3) 0.65 1.5 11.0 0.38 6.77 40.1 2.3 3.82 23.5

T11 (GT-T) Barramundi (n ¼ 2) 0.11 0.64 2.00 0.063 12.0 43.2 2.2 2.13 47.9

Indian mackerel (n ¼ 3) 0.92 0.63 1.29 0.25 7.54 66.4 3.8 2.22 38.6

T12 (GT-T) Barramundi (n ¼ 2) 0.025 0.69 1.05 0.030 15.3 36.6 3.0 1.95 5.48

Bluespot mullet (n ¼ 3) 4.0 0.57 8.66 0.23 16.9 92.9 3.2 3.79 14.0

Torpedo scad (n ¼ 2) 0.10 0.56 3.39 0.13 19.2 115 8.0 2.08 17.3

T13 (GT-T) Barramundi (n ¼ 2) 0.032 0.64 4.24 0.027 17.6 47.9 3.3 1.37 2.61

Bluespot mullet (n ¼ 3) 3.0 0.62 30.3 0.39 13.9 95.9 3.4 3.68 6.40

Torpedo scad (n ¼ 3) 0.094 0.73 1.75 0.15 14.2 60.1 6.1 2.25 12.3

NA; not analyzed.

Table 3

Trace element concentrations (geometric mean (n > 1) and individual value (n ¼ 1), mg/g dry wt.) in muscle of marine fish from Southeast Asia

Cs Ba Hg Tl Pb Bi

0.03 0.034 <0.05 <0.001 0.010 <0.001

0.06 0.042 0.18 <0.001 0.027 0.003

0.05 0.073 0.07 <0.001 0.002 0.001

0.02 0.032 <0.05 <0.001 0.020 0.004

0.10 0.032 0.23 <0.001 0.021 0.005

0.04 0.037 0.20 <0.001 0.017 0.002

0.08 0.052 1.4 <0.001 0.032 0.010

0.02 0.19 <0.05 0.002 0.031 <0.001

0.08 0.037 0.10 <0.001 0.014 <0.001

0.02 0.021 <0.05 <0.001 0.036 <0.001

0.07 0.045 0.23 <0.001 0.016 0.001

0.08 0.082 0.45 <0.001 0.017 0.005

0.15 0.033 0.65 0.004 0.007 0.011

0.10 0.018 0.68 <0.001 0.003 <0.001

0.02 0.040 <0.05 <0.001 0.005 <0.001

0.03 0.33 0.31 0.002 0.094 0.007

0.05 0.16 0.12 0.005 0.017 0.002

0.06 0.029 0.11 <0.001 0.003 0.009

0.07 0.018 0.29 <0.001 0.004 <0.001

0.05 0.033 0.22 0.001 <0.001 <0.001

0.02 0.18 <0.05 0.001 <0.001 0.001

0.03 0.46 0.11 <0.001 0.040 0.005

0.06 0.031 0.18 <0.001 0.012 0.002

0.05 0.033 0.17 <0.001 0.001 0.012

0.10 0.031 0.67 <0.001 0.027 0.018

0.09 0.069 0.09 <0.001 0.036 <0.001

0.07 0.071 0.21 <0.001 0.054 <0.001

0.03 0.30 0.10 0.003 0.046 <0.001

0.05 0.054 0.16 <0.001 0.032 <0.001

0.08 0.051 0.36 <0.001 0.023 0.002

0.04 0.12 <0.05 <0.001 0.029 <0.001

0.04 0.052 0.09 <0.001 0.018 0.038

0.12 0.085 0.11 <0.001 0.048 0.001

0.13 0.011 0.09 <0.001 0.014 <0.001

0.04 0.16 <0.05 0.004 0.054 0.001

0.05 0.59 <0.05 <0.001 0.027 <0.001

0.17 0.028 0.27 <0.001 0.049 0.003

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Location Common name V Cr Mn Co Cu Zn Se Rb Sr Mo Ag Cd Sn Sb

Cambodia

C1 (GT-C) Bluespot mullet (n ¼ 3) 0.036 0.43 0.305 0.040 1.09 13.0 0.60 7.75 2.54 0.008 0.002 <0.001 0.058 <0.01

Brownstripe red snapper (n ¼ 3) 0.022 0.48 0.516 0.009 0.846 16.9 2.3 5.33 1.05 0.007 0.001 <0.001 0.187 <0.01

Narrow-barred Spanish

mackerel (n ¼ 3)

0.014 0.37 0.448 0.005 1.33 17.5 2.1 4.19 1.07 0.008 0.002 0.003 0.158 <0.01

C2 (GT-C) Bluespot mullet (n ¼ 3) 0.036 0.50 0.498 0.026 1.24 17.7 0.91 7.07 1.85 0.010 0.002 0.003 0.172 <0.01

Obtuse barracuda (n ¼ 3) 0.024 0.42 0.343 0.006 1.22 22.6 2.9 3.72 1.34 0.007 <0.001 0.016 0.152 <0.01

Russell’s snapper (n ¼ 3) 0.013 0.39 0.411 0.006 0.867 14.4 2.3 4.15 1.15 0.006 <0.001 0.005 0.150 <0.01

Sharptooth jobfish (n ¼ 3) 0.041 0.40 0.511 0.012 1.11 13.4 3.0 4.00 3.91 0.008 0.002 0.030 0.028 <0.01

Short mackerel (n ¼ 3) 0.051 0.40 0.367 0.027 1.80 17.4 3.8 2.76 3.49 0.015 0.004 0.098 0.039 <0.01

Torpedo scad (n ¼ 3) 0.017 0.41 0.482 0.013 2.48 27.9 2.6 3.94 1.57 0.008 0.002 0.034 0.156 <0.01

C3 (GT-C) Bluespot mullet (n ¼ 3) 0.096 0.46 0.328 0.021 1.36 15.3 0.69 6.12 1.76 0.008 0.002 0.002 0.058 <0.01

Frigate tuna (n ¼ 3) 0.019 0.40 0.342 0.008 1.33 18.1 2.0 4.59 1.12 0.016 0.003 0.004 0.153 <0.01

Obtuse barracuda (n ¼ 3) 0.027 0.58 0.656 0.006 1.28 18.7 2.9 3.70 3.19 0.016 <0.001 0.008 0.172 <0.01

Indonesia

I1 (JS) Unknown (n ¼ 3) 0.013 0.31 0.639 0.026 2.22 15.3 1.7 4.22 1.95 0.029 0.007 0.031 0.083 0.01

Talang queenfish (n ¼ 3) 0.009 0.26 0.436 0.007 1.47 13.5 1.5 3.58 0.927 0.008 <0.001 <0.001 0.125 <0.01

White-spotted spinefoot (n ¼ 3) 0.10 0.43 2.77 0.17 1.58 20.2 1.0 5.53 3.77 0.013 <0.001 0.001 0.041 <0.01

I2 (JS) Chacunda gizzard

shad (n ¼ 3)

0.18 0.54 1.98 0.021 1.74 28.0 2.4 5.51 12.3 0.015 0.001 0.021 0.032 <0.01

Indian mackerel (n ¼ 3) 0.051 0.33 0.736 0.038 1.09 15.0 2.1 3.63 4.38 0.022 0.005 0.013 0.056 <0.01

Japanese threadfin

bream (n ¼ 3)

0.019 0.29 0.475 0.026 1.13 12.3 2.1 3.98 1.46 0.006 0.001 0.003 0.035 <0.01

Red bigeye (n ¼ 3) 0.008 0.27 0.364 0.006 0.888 12.4 2.2 4.38 1.17 0.005 <0.001 0.003 0.042 <0.01

Small-scaled terapon (n ¼ 3) 0.016 0.32 0.405 0.014 1.41 29.0 1.4 3.33 4.24 0.008 0.001 0.006 0.033 <0.01

I3 (JS) Bluetail mullet (n ¼ 3) 0.12 0.64 0.615 0.064 1.50 37.5 1.8 6.03 2.14 0.005 <0.001 0.003 0.032 <0.01

Chacunda gizzard

shad (n ¼ 3)

0.19 0.28 3.23 0.039 1.47 27.1 1.3 5.29 9.80 0.016 0.002 0.008 0.033 <0.01

Fourfinger threadfin (n ¼ 3) 0.038 0.30 0.517 0.013 1.33 18.9 1.3 3.89 1.22 0.006 <0.001 0.001 0.105 <0.01

Sharpnose hammer

croaker (n ¼ 3)

0.038 0.30 0.583 0.12 1.03 23.5 1.3 5.07 2.45 0.005 <0.001 0.002 0.043 <0.01

Malaysia

M1 (SCS) Fork-tailed threadfin

bream (n ¼ 5)

0.033 0.38 0.386 0.012 0.862 15.4 2.3 2.98 2.95 0.007 0.001 0.013 0.015 <0.01

Kawakawa (n ¼ 5) 0.039 0.44 0.612 0.017 3.02 60.1 2.9 2.08 2.61 0.025 0.007 0.148 0.153 <0.01

Torpedo scad (n ¼ 6) 0.037 0.37 0.345 0.016 2.53 28.3 1.7 2.05 3.16 0.008 0.002 0.133 0.021 <0.01

M2 (SCS) Bigeye scad (n ¼ 4) 0.062 0.51 0.466 0.025 2.16 28.0 3.8 2.56 10.5 0.029 0.003 0.064 0.060 <0.01

Redtail scad (n ¼ 5) 0.066 0.53 0.346 0.019 1.83 32.4 2.4 2.14 6.50 0.010 0.004 0.081 0.022 <0.01

M3 (SCS) Bigeye scad (n ¼ 5) 0.091 0.63 0.374 0.016 2.94 39.2 2.5 2.21 8.41 0.015 0.001 0.025 0.153 <0.01

Indian mackerel (n ¼ 5) 0.091 0.57 0.334 0.019 1.94 23.2 2.5 3.07 5.08 0.035 0.003 0.029 0.069 <0.01

Javelin grunter (n ¼ 7) 0.046 0.46 0.214 0.013 1.59 22.8 1.5 2.16 3.72 0.010 0.003 0.005 0.008 <0.01

M4 (SM-M) Bigeye scad (n ¼ 5) 0.054 0.49 0.460 0.016 2.23 25.5 1.8 3.19 3.61 0.007 <0.001 0.004 0.141 <0.01

Doublespotted queenfish (n ¼ 5) 0.052 0.46 0.250 0.006 1.37 26.8 1.8 4.00 1.54 0.008 <0.001 <0.001 0.581 <0.01

M5 (SM-M) Bigeye scad (n ¼ 11) 0.087 0.46 0.343 0.032 2.06 29.7 1.8 2.71 5.85 0.023 0.003 0.020 0.024 <0.01

Black pomfret (n ¼ 5) 0.040 0.39 0.659 0.024 1.05 17.1 2.4 5.52 7.50 0.007 0.002 0.023 0.084 <0.01

Torpedo scad (n ¼ 5) 0.051 0.49 0.536 0.023 2.87 27.1 2.0 3.78 3.05 0.022 0.001 0.013 0.265 <0.01

M6 (SM-M) Bigeye scad (n ¼ 6) 0.18 0.49 0.460 0.085 1.91 27.0 1.7 2.83 19.7 0.562 0.002 0.029 0.003 <0.01 0.03 0.79 <0.05 0.003 0.066 <0.001

0.010 0.001 0.019 0.041 <0.01 0.04 0.037 0.09 <0.001 0.030 0.036

0.012 0.003 0.098 0.041 <0.01 0.05 0.089 0.05 <0.001 0.026 <0.001

0.014 0.001 0.162 0.107 <0.01 0.04 0.15 0.06 <0.001 0.051 <0.001

0.007 0.002 0.203 0.007 <0.01 0.10 0.028 0.10 <0.001 0.026 <0.001

0.022 <0.001 0.059 <0.001 <0.01 0.05 0.64 0.31 <0.001 0.072 0.009

0.007 0.004 0.127 0.037 <0.01 0.06 0.058 <0.05 0.004 0.008 0.001

0.002 <0.001 0.011 0.019 <0.01 0.06 0.043 0.23 <0.001 0.005 0.006

0.003 <0.001 <0.001 0.021 <0.01 0.14 0.021 0.86 <0.001 0.083 0.009

0.006 <0.001 0.006 0.013 <0.01 0.07 0.042 0.50 <0.001 0.003 0.001

0.002 <0.001 <0.001 0.009 <0.01 0.04 0.022 0.66 <0.001 <0.001 <0.001

0.012 <0.001 0.166 0.024 <0.01 0.06 0.053 <0.05 <0.001 <0.001 <0.001

0.023 <0.001 0.003 0.024 <0.01 0.01 0.11 0.09 <0.001 0.021 0.004

0.001 <0.001 0.056 0.017 <0.01 0.03 0.025 0.30 <0.001 0.021 0.008

0.024 0.009 0.073 0.041 <0.01 0.03 0.061 0.09 0.005 0.017 0.007

0.025 0.007 0.008 0.018 <0.01 0.02 0.080 0.06 0.002 0.030 0.016

0.022 0.010 0.005 0.029 <0.01 0.03 0.048 0.08 0.004 0.031 0.027

0.012 0.006 0.002 0.022 <0.01 0.06 0.030 <0.05 0.002 0.002 0.030

0.150 0.005 0.093 0.021 <0.01 0.02 0.31 0.08 0.004 0.053 0.001

0.006 <0.001 0.069 0.008 <0.01 0.06 0.046 0.22 <0.001 0.008 <0.001

0.010 0.003 0.100 0.033 <0.01 0.06 0.061 0.09 <0.001 0.005 <0.001

0.022 0.001 0.003 0.020 <0.01 0.03 0.11 <0.05 0.001 0.003 0.005

0.004 <0.001 <0.001 0.030 <0.01 0.17 0.032 0.48 <0.001 <0.001 0.010

0.107 0.011 0.069 0.037 <0.01 0.04 0.10 <0.05 0.014 0.015 0.009

0.004 0.001 0.002 0.030 <0.01 0.04 0.028 0.14 0.001 0.002 0.003

0.012 0.005 0.003 0.022 <0.01 0.03 0.076 <0.05 0.003 0.003 0.007

0.004 <0.001 0.057 0.023 <0.01 0.06 0.053 0.05 <0.001 <0.001 0.001

0.002 <0.001 <0.001 0.046 <0.01 0.05 0.025 0.12 <0.001 <0.001 0.002

0.007 0.002 <0.001 0.020 <0.01 0.02 0.065 <0.05 <0.001 0.011 0.009

0.007 <0.001 0.043 0.024 <0.01 0.07 0.13 <0.05 <0.001 <0.001 <0.001

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Doublelined tonguesole (n ¼ 5) 0.096 0.62 0.398 0.012 1.35 18.9 1.6 2.83 6.44

Redtail scad (n ¼ 9) 0.043 0.39 0.323 0.019 3.32 33.1 2.2 1.95 4.85

Shortfin scad (n ¼ 3) 0.083 0.63 0.539 0.027 3.48 29.1 2.3 1.80 7.43

Torpedo scad (n ¼ 5) 0.038 0.41 0.383 0.018 2.21 17.9 1.8 2.40 2.86

Yellowfin seabream (n ¼ 1) 0.069 0.48 0.588 0.016 1.31 33.6 1.4 2.62 20.8

Thailand

T1 (GT-T) Bigeye scad (n ¼ 3) 0.032 0.42 0.485 0.015 2.46 35.4 3.1 3.07 2.76

Malabar blood

snapper (n ¼ 3)

0.037 0.49 0.360 0.008 1.31 13.4 1.7 2.81 3.19

T2 (GT-T) Bluespot mullet (n ¼ 1) 0.030 0.45 0.374 0.002 1.09 17.0 1.5 3.43 1.57

Torpedo scad (n ¼ 1) 0.047 0.51 0.278 0.016 2.67 35.2 1.7 4.30 4.51

Whipfin silverbiddy (n ¼ 1) 0.081 0.33 0.148 0.28 1.52 21.6 0.58 5.97 3.94

T3 (GT-T) Torpedo scad (n ¼ 3) 0.027 0.41 0.402 0.020 2.96 29.3 3.6 2.73 4.04

T4 (GT-T) Bluespot mullet (n ¼ 3) 0.057 0.38 1.59 0.040 1.88 25.0 0.59 1.92 9.58

Tiger-toothed croaker (n ¼ 2) 0.043 0.57 0.307 0.013 1.94 23.9 1.8 1.47 4.01

Torpedo scad (n ¼ 2) 0.047 0.43 0.656 0.031 4.06 23.6 2.4 1.21 4.60

T5 (GT-T) Bluespot mullet (n ¼ 3) 0.12 0.36 0.951 0.030 1.68 18.7 0.84 4.66 7.31

T6 (GT-T) Bluespot mullet (n ¼ 3) 0.038 0.35 0.213 0.055 2.03 23.2 0.61 3.33 4.95

T7 (SM-T) Bluespot mullet (n ¼ 3) 0.069 0.38 0.311 0.014 1.14 16.4 0.96 6.80 3.03

Indian mackerel (n ¼ 3) 0.20 0.38 0.419 0.084 2.69 50.7 2.7 2.85 7.50

T8 (SM-T) Torpedo scad (n ¼ 3) 0.033 0.55 0.553 0.019 3.57 20.4 1.5 1.94 4.33

T9 (SM-T) Torpedo scad (n ¼ 3) 0.042 0.49 0.417 0.018 2.81 22.7 1.9 2.29 4.24

T10 (SM-T) Bluespot mullet (n ¼ 3) 0.061 0.42 0.597 0.062 1.44 19.2 0.73 3.00 6.63

T11 (GT-T) Barramundi (n ¼ 2) 0.013 0.27 0.213 0.006 1.09 17.1 1.3 2.80 2.69

Indian mackerel (n ¼ 3) 0.095 0.52 0.217 0.059 1.65 21.1 1.1 2.19 6.80

T12 (GT-T) Barramundi (n ¼ 2) 0.013 0.30 0.310 0.003 0.819 15.5 1.9 3.60 1.87

Bluespot mullet (n ¼ 3) 0.060 0.39 0.323 0.009 1.48 23.6 0.59 4.94 2.83

Torpedo scad (n ¼ 3) 0.042 0.43 0.401 0.017 4.39 21.3 2.2 2.05 3.78

T13 (GT-T) Barramundi (n ¼ 2) 0.034 0.49 0.560 <0.001 1.21 15.6 1.3 3.64 1.09

Bluespot mullet (n ¼ 3) 0.063 0.40 0.969 0.018 1.15 16.9 0.41 4.99 4.48

Torpedo scad (n ¼ 3) 0.047 0.60 0.611 0.018 3.60 22.0 2.3 2.72 7.10

774 T. Agusa et al. / Environmental Pollution 145 (2007) 766e777

areas mentioned above and also their sample size was the larg-est in this study. Significant regional differences in concentra-tions of all elements ( p < 0.05) except for Mn, Rb and Bawere observed by one-way ANOVA. Thus, multiple compari-sons were performed with Turkey-Kramer test. Concentrationsof V, Cr, Co, Cu, Zn, Sr, Mo, Ag, Cd, Sn, Pb and Bi in liver ofmarine fish showed significant difference among the six areas( p < 0.05; Fig. 3). Higher levels of V, Cr, Pb and Bi were ob-served around the Malaysian coastal region (SCS and SM-M).Especially, Zn concentration in fish from the SCS was higherthan those of the other areas. Although human activity is

Cd

Mo

Ag

Co

Mn

Cu

Pb

V

Zn

Sn

Se

Sr

Ba

Cr

Hg

Rb

Cs

-0.5 0 0.5 1.0 1.5 2.0 2.5

Log10

concentration ratio (liver/muscle)

Fig. 2. Comparison of trace element concentrations between liver and muscle

of marine fish from coastal waters of Cambodia, Indonesia, Malaysia and

Thailand. All the trace elements represented in this figure showed a significant

difference ( p < 0.001 for all elements except for Hg and p < 0.05 for Hg)

between liver and muscle.

concentrated in the west coast of the Malay Peninsula (SM-M)compared with the east side (SCS), concentrations of Zn,Cu, Se, Cd and Hg in the Carangidaes from the SCS were sig-nificantly higher than those from the SM-M. These results maysuggest that some point sources of trace element contamina-tion are present in the east side of the Peninsular in spite ofthe relatively lower human activity. Similar trend has alsobeen reported in a previous study (Agusa et al., 2005). Rela-tively high concentration of Hg was found in marine fishfrom the JS. Recently, Kambey et al. (2001) reported thatfishes in the Minahasa Peninsula, North Sulawaesi in Indone-sia were exposed to Hg in run-off from illegal gold mining.However, illegal usage of Hg for extraction of gold may notinfluence our results, because sampling locations in Indonesiain the present study were far from the Minahasa Peninsula.Further study to identify the source of Hg in the Java Sea isrequired. Tin concentrations were high in fish from the JS, fol-lowed by the SM-M. Butyltin (BT), one of organic Sn com-pounds, has been used for industry (e.g., stabilizers ofpolyvinyl chloride) and agriculture (e.g., biocides). AmongBT compounds, tributyltin (TBT) has been used as an effectiveantifouling paint for ships, vessels, harbor structures and aqua-culture nets (Blunden and Evans, 1990). The study regardingAsiaePacific Mussel Watch Program (APMW) has reportedthat relatively high concentrations of BT compounds were ob-served in mussel from the Straights of Malacca among Asiandeveloping countries (Sudaryanto et al., 2002). Sudaryantoet al. (2004) also found a significant positive correlation be-tween concentrations of BT compounds and total Sn in musseland fish from Malaysian marine environment and suggestedthat anthropogenic sources of BT compounds influence the to-tal Sn accumulation in marine organisms. Therefore, high

10-2

10-1

100

101

100

101

102

10-2

10-1

100

101

10-1

100

101

100

101

102

103

10-2

10-1

100

101

10-2

10-1

100

101

10-1

100

101

102

10-3

10-2

10-1

100

101

101

102

103

10-1

100

101

102

100

101

102

10-3

10-2

10-1

100

10-3

10-2

10-1

AgSr CdMoSe

Sn Hg BiPb

ZnCr CuCoV

GT

-C

GT

-T

SC

S

SM

-M

SM

-T

JS

GT

-C

GT

-T

SC

S

SM

-M

SM

-T

JS

GT

-C

GT

-T

SC

S

SM

-M

SM

-T

JS

GT

-C

GT

-T

SC

S

SM

-M

SM

-T

JS

GT

-C

GT

-T

SC

S

SM

-M

SM

-T

JS

a

a

ab

a a

bc

bbc

c

ab

a

abb ab

ab

a

ba

b

a

ab

a b

abcc abc

abc

b ab

a b

abab ab

c

ab b

ab

ab

a

ba ab

ab

a

a

b

ab

a

abb

abab

a

ba b

b ab

a

a

b

ab

ab ab

ab

c

abc

bc

abc

a

a

a

ab

b

abab

aa

b

bb

a

b

Co

ncen

tratio

n (µ

g/g

d

ry w

t.)

Fig. 3. Concentrations of trace elements in liver of marine fish at the six areas (Gulf of Thailand in Cambodia, GT-C; Gulf of Thailand in Thailand, GT-T; South

China Sea in Malaysia, SCS; Strait of Malacca in Malaysia, SM-M; Strait of Malacca in Thailand, SM-T; Java Sea, JS). Concentrations with the same letter are not

significantly different at p < 0.05. Each point and vertical bar represents the individual value and geometric mean, respectively.

775T. Agusa et al. / Environmental Pollution 145 (2007) 766e777

concentrations of Sn in fish from the SM-M may be the resultof usage of anthropogenic Sn such as BT compounds in thearea. The highest concentration of Sn in fish from the JS mightalso be due to the contamination by BTs in the Java Sea.However, relatively low concentration of BT in mussel fromIndonesian coastal waters has been reported by APMWstudy (Sudaryanto et al., 2002). Because the sample numberof Carangidaes collected from the Indonesian waters waslimited (n ¼ 3) in the present study, further evaluation isrequired.

3.3. Human health risk assessment

Since seafood is one of the most important food sources inSoutheast Asia, intake of trace elements from seafood, espe-cially toxic elements, is of great concern for human healthrisk. To evaluate the health risk to people in Southeast Asiancountries through consumption of marine fish, daily intakeof trace elements was estimated on the basis of the concentra-tions (wet wt. basis) of trace elements in muscle of fish anddaily fish consumption. According to Bloom (1992), methylHg (MeHg) accounts for more than 95% of total mercury inedible muscle of freshwater and marine fish. Hence, we as-sumed that concentration of total Hg is equal to that of

MeHg in the muscle in the present study. Rates of fish con-sumption are 71 g/day for a Cambodian, 57 g/day for anIndonesian, 160 g/day for a Malaysian and 85 g/day fora Thailander (FAO, 2005). Reference doses (RfD) of V(1 mg/kg body wt./day), Cr (3 mg/kg body wt./day), Mn(140 mg/kg body wt./day), Co (20 mg/kg body wt./day), Cu(40 mg/kg body wt./day), Zn (300 mg/kg body wt./day), Se(5 mg/kg body wt./day), Sr (600 mg/kg body wt./day), Mo(5 mg/kg body wt./day), Ag (5 mg/kg body wt./day), Cd(1 mg/kg body wt./day), Sn (600 mg/kg body wt./day), Ba(70 mg/kg body wt./day) and MeHg (0.1 mg/kg body wt./day)and Tl (0.07 mg/kg body wt./day) were published by U.S. En-vironmental Protection Agency (EPA) (U.S. EPA, 2005). The61st meeting of the Joint FAO/WHO Expert Committee onFood Additives (JECFA) (JECFA, 2003) also established a pro-visional tolerable weekly intake (PTWI) of 1.6 mg/kg bodywt./week (0.23 mg/kg body wt./day) for MeHg. Since RfD ofPb was not established by EPA, PTWI of 25 mg/kg body wt/week (¼ 3.57 mg/kg body wt./day) established by the 41st re-port of the JECFA (JECFA, 1999) was used for risk assess-ment in the present study. Average body weight of SoutheastAsian people was assumed to be 50 kg, and the guidelinevalues for trace elements were calculated from the RfDs andPTWI and the body weight.

Table 4

Dietary intakes (mg/day) of trace elements through fish consumption for population in Southeast Asia

Location V Cr Mn Co Cu Zn Se Sr Mo Ag Cd Sn Ba Hg Pb

Cambodia

GT-C (n ¼ 36) GM 0.45 7.1 6.9 0.19 21 280 31 29 0.15 0.03 0.10 1.7 0.76 1.9 0.27

Min 0.12 4.6 4.0 0.07 12 180 8.6 12 0.08 0.01 0.01 0.21 0.27 0.35 0.01

Max 3.4 13 16 0.74 56 910 82 190 0.38 0.12 4.3 3.6 7.0 68 1.0

Indonesia

JS (n ¼ 36) GM 0.51 4.6 10 0.38 18 270 22 37 0.13 0.02 0.06 0.66 0.80 2.2 0.07

Min 0.08 2.7 3.6 0.05 10 130 12 9.4 0.05 0.01 0.01 0.25 0.17 0.34 0.01

Max 5.9 14 120 4.7 44 630 40 370 0.84 0.61 0.75 2.2 40 13 1.5

Malaysia

SCS (n ¼ 42) GM 2.18 19 15 0.67 80 1200 92 190 0.57 0.10 1.47 1.4 2.8 5.8 1.3

Min 0.89 11 4.6 0.33 32 550 48 64 0.19 0.02 0.06 0.02 0.48 1.0 0.41

Max 9.6 34 35 1.5 170 3500 190 610 3.6 0.62 13 36 18 41 6.7

SM-M (n ¼ 60) GM 2.6 19 16 0.89 83 1000 76 210 0.71 0.07 0.96 1.5 4.0 2.7 1.5

Min 0.94 10 7.0 0.19 35 480 38 46 0.15 0.01 0.02 0.01 0.29 0.94 0.19

Max 9.4 38 54 5.1 200 2200 140 1800 44 1.0 16 35 87 15 5.8

Thailand

GT-T (n ¼ 46) GM 0.94 9.0 9.5 0.33 41 460 28 86 0.18 0.04 0.22 0.53 1.2 1.8 0.10

Min 0.15 5.1 3.4 0.01 16 230 7.5 15 0.01 0.01 0.01 0.20 0.26 0.47 0.01

Max 3.6 19 150 6.3 100 1100 130 500 5.1 0.51 11 1.8 17 18 18

SM-T (n ¼ 15) GM 1.5 10 10 0.67 48 530 32 109 0.42 0.05 0.46 0.43 1.7 1.6 0.14

Min 0.48 5.4 4.6 0.25 22 250 16 54 0.11 0.01 0.01 0.06 0.47 0.50 0.01

Max 6.7 17 16 2.8 79 1400 69 240 4.8 0.16 3.0 1.0 15 8.5 1.5

Guideline valuea

U.S. EPA (2005) 50 150 7000 1000 2000 15,000 250 30,000 250 250 50 30,000 3500 5

JECFA (1999 and 2003) 11 179

a Guideline values were calculated from reference doses of each element and average body weight (50 kg). Reference doses for Hg and Pb were referred from

JECFA (2003) and JECFA (1999), respectively.

776 T. Agusa et al. / Environmental Pollution 145 (2007) 766e777

Table 4 shows estimated daily intakes and guideline valuefor trace elements. For all the elements examined, high intakeswere estimated in the SCS and the ST-M from Malaysia. Thiscould be due to the high consumption rate of seafood byMalaysian (160 g/day). All the estimated daily intakes of V, Cr,Mn, Co, Cu, Zn, Se, Sr, Mo, Ag, Cd, Sn and Ba were belowthe guideline values. Thus, for these elements, muscle tissueof the marine fish may not cause any serious health risk toSoutheast Asian people. However, 27% and 10% of fish sam-ples examined had Hg levels higher than the guideline valuesfor U.S. EPA (5 mg/day) and JECFA (11 mg/day), respectively(Fig. 4). The ratios of the fish which showed over the guidelinevalue for Hg of JECFA were 8%, 6%, 26%, 10% and 9% in theGT-C, JS, SCS, SM-M and GT-T, respectively. Especially, rel-atively high intake of Hg (GM; 5.85 mg/day) was observed inthe SCS, Malaysia. The estimated daily intakes (22.4e40.1 mg/day) from all the specimens of fork-tailed threadfin breams(GM; 0.67 mg/g dry wt.) in the SCS exceeded this guidelinevalues. Also, one of the sharptooth jobfishes (1.4 mg/g drywt.) in Cambodia showed the highest value (68 mg/day). Theseresults would indicate that consumption of these fish at thepresent rate might be hazardous to residents in SoutheastAsia, especially pregnant women because fetus is more sus-ceptible to Hg toxicity. Since the number of specimens ana-lyzed in each area was small and the contribution of eachspecies to dietary intake of seafood was not considered inour calculation, estimated intakes in the present study maybe only an approximation of actual intake. However, becausefew studies have been conducted on exposure to trace ele-ments through the marine fish consumption in these SoutheastAsian countries, these data would be valuable and providea useful information for assessment of the potential healthrisks of trace elements in residents of Southeast Asia.

0 20 40 60 80

Cambodia

Indonesia

Malaysia

Thailand

M1

M5

T1

T2

C1

I1

C2

C3

I2

I3

M2

M3

M4

T3

T4

T5

T6

T7

T8

T9

T10

T11

T12

T13

M6

RfD (EPA) PTWI (JECFA)

Intake of Hg (µg/day)

Fig. 4. Estimated daily intakes of Hg for residents at the 25 locations of

Cambodia, Indonesia, Malaysia and Thailand. The vertical bold and dashed

lines denote the guideline values of 5 mg/day and 11 mg/day calculated from

body weight (50 kg) and reference doses of 0.1 mg/kg body wt./day for U.S.

EPA (2005) and 0.23 mg/kg body wt./day for JECFA (2003), respectively.

Acknowledgments

The authors thank Professor Annamalai Subramanian,Ehime University, for critical reading of the manuscript.This research was supported by Grants-in-Aid for ScientificResearch (A) (No. 14254004) from Japan Society for thePromotion of Science, Research Revolution 2002 (RR 2002)Project for Sustainable Coexistence of Human, Nature andthe Earth (FY 2002) and ‘‘21st Century COE Program’’from the Ministry of Education, Culture, Sports, Science andTechnology, Japan.

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