Regional variations in trace element concentrations in tissues of black tiger shrimp Penaeus monodon (Decapoda: Penaeidae) from South Vietnam

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Marine Pollution Bulletin 57 (2008) 858–866 www.elsevier.com/locate/marpolbul

Regional variations in trace element concentrations in tissues of black tiger shrimp Penaeus monodon (Decapoda: Penaeidae) from South Vietnam Nguyen Phuc Cam Tu a, Nguyen Ngoc Ha b, Tokutaka Ikemoto b, Bui Cach Tuyen c, Shinsuke Tanabe b, Ichiro Takeuchi a,* b

a Faculty of Agriculture, Ehime University, Tarumi 3-5-7, Matsuyama 790-8566, Japan Center for Marine Environmental Studies, Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japan c Nong Lam University, Linh Trung Ward, Thu Duc District, Ho Chi Minh City, Vietnam

Abstract The goal of the present study was to examine the specific bioaccumulation of 22 trace elements in muscle, exoskeleton and hepatopancreas of black tiger shrimp Penaeus monodon from the Mekong River Delta (MRD), and the South Key Economic Zone (SKEZ), South Vietnam. The general tendency in most trace element concentrations among different tissues were hepatopancreas > exoskeleton > muscle. Comparisons of trace element levels in tissues between the two regions showed that concentrations of Se in muscle and As in all three tissues were higher in SKEZ; whereas in MRD, the higher concentrations of most elements such as Mn, Cu, Cd, Ba, Hg, were observed in tissues. These geographical variations in trace element levels may reflect the differences in human activities between the two regions of South Vietnam. The target hazard quotient (THQ) values for trace elements (<1) indicate that local residents are not exposed to potential health risks via the consumption of shrimp. Ó 2008 Elsevier Ltd. All rights reserved. Keywords: Trace elements; Black tiger shrimp; Penaeus monodon; South Vietnam; Health risk

1. Introduction Vietnam has a high potential for aquaculture development and fisheries which are recognized as a key economic sector with an annual contribution of 9–10% of export turnover, presenting a value of over US $2.7 billion in 2005. Accounting for an export value of US $1.2 billion, black tiger shrimp farming has received the greatest attention of all types of mariculture in Vietnam. Notably, shrimp culture is well developed in South Vietnam, particularly in the Mekong River Delta (MRD) region, which accounted for up to 70% of shrimp culture area (Ruckes and Dang, 2004; MOFI, 2006; Phuong et al., 2006).

*

Corresponding author. Tel./fax: +81 89 946 9899. E-mail address: [email protected] (I. Takeuchi).

0025-326X/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2008.02.016

The South Key Economic Zone (SKEZ) encompasses eight cities and provinces including Ho Chi Minh City, Binh Phuoc, Dong Nai, Binh Duong, Ba Ria Vung Tau, Tien Giang, Long An and Tay Ninh. The zone accounts for more than 50% of Vietnam’s GDP (Gross Domestic Product), attracts more than US $15 billion of investment capital since 1997 and often boasts its economic growth rate of more than 12%, almost double that of the whole country. The zone also houses approximately 60 industrial parks and export processing zones which play a critical role in Vietnam’s industrialization (SHTP, 2007). While, contributing to half of the rice production, making the MRD the most important rice granary of Vietnam (Ninh et al., 2007). However, unprecedented economic and industrial growth has caused negative impacts on the environmental quality of South Vietnam, particularly the release of trace elements into aquatic ecosystems. Trace elements therefore

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may pose a health risk to humans who consume contaminated aquatic food. For non-carcinogenic effects of trace elements, the risk is expressed as a THQ, the ratio between exposure and the reference dose (RfD). If the THQ is <1, there is no obvious risk. Conversely, an exposed population of concern will experience health risks if the THQ is P1 (Han et al., 1998, 2000). Method for the determination of THQ was from the US EPA Region III risk-based concentration (RBC) table (US EPA, 2000, 2007). In the present study, contamination status of 22 trace elements was analyzed in abdominal muscle, abdominal exoskeleton (hereafter called muscle and exoskeleton, respectively), and hepatopancreas of Penaeus monodon collected from South Vietnam. Another objective of this study was to evaluate the human health risks of trace elements via consumption of shrimp to people from South Vietnam using estimations of THQ. 2. Materials and methods 2.1. Sampling Pre-adults of the black tiger shrimp (P. monodon) were collected from local aquaculture farms and local small markets in the SKEZ (Ho Chi Minh City, Ba Ria – Vung Tau and Long An) and from the MRD (Bac Lieu, Ben Tre, Kien Giang, Soc Trang and Tra Vinh) zones between September 2003 and April 2005. Farmers and salesmen were not informed ahead of time that collections would be made. Shrimp were placed in polyethylene bags, transported to Japan, and stored in a deep freezer at 20 °C until chemical analysis. All shrimps were analyzed individually rather than as composites. Body weight was measured prior to dissection. To analyze tissue-specific concentrations of trace elements, shrimps were dissected and muscle, exoskeleton, and the hepatopancreas were carefully

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separated from other body organs. Sample details and sampling location are shown in Table 1 and Fig. 1, respectively. 2.2. Chemical analyses The procedure used for measuring concentrations trace elements has been described previously (Kubota et al., 2002; Nam et al., 2005). Tissue samples were dried for 12 h at 80 °C and ground to a fine powder using mortar and pestle before analysis. Approximately 0.2 g of the sample was digested in 5 mL of concentrated HNO3 in a microwave system (MILESTONE, ETHOS D), using a digestion protocol of seven steps: 2, 3, 5, 5, 5, and 10 min under 250, 0, 250, 400, 500 and 400 W, respectively, and ventilation for 5 min. Levels of 19 trace elements (V, Cr, Mn, Co, Cu, Zn, Rb, Sr, Mo, Ag, Cd, In, Sn, Sb, Cs, Ba, Tl, Pb and Bi) were analyzed with an inductively coupled plasma-mass spectrometer (ICP-MS) (HP-4500, HewlettPackard, Avondale, PA, USA) with yttrium as the internal standard. Mercury and Se were determined using a cold vapor atomic absorption spectrometer (AAS) (AA680, Shimadzu Corporation, Kyoto, Japan; Model HG-3000 cold vapor system, Sanso, Tsukuba, Japan) and a hydride generation (HG) AAS (Model HFS-3 hydride system, Hitachi, Ltd., Tokyo, Japan), respectively. For As analysis, samples were digested with an acid mixture (HNO3:H2SO4:HClO4 = 1:1:2) and determined by a HGAAS (HVG-1 hydride system, Shimadzu Corporation, Kyoto, Japan). Accuracies of the methods were assessed using certified reference material DORM-2 (National Research Council of Canada) in triplicate, and recoveries of all the elements ranged from 87% to 111% of the certified values. All data were expressed on a dry weight basis (lg/g dry wt.). Moisture content of muscle and hepatopancreas samples were 74.7 ± 1.4% and 73.7 ± 8.0%, respectively. In order to compare with other shrimp and evaluate human health risk on a wet wt. basis, our data was converted to wet wt. using

Table 1 Sample information of black tiger shrimp Penaeus monodon from South Vietnam

SKEZ BRVT

HCMC LA MRD BL BT KG ST

TV a

Location

Date

Latitude

Longitude

Remarks

na

Weight (g)

Ba Ria – Vung Tau 1 Ba Ria – Vung Tau 2 Ba Ria – Vung Tau 3 Ho Chi Minh City Long An

2004/09/02 2004/09/02 2005/04/10 2003//09/16 2004/09/01

10°310 95900 10°310 20300 10°310 95900 10°230 24600 10°310 35900

106°240 76000 107°030 74000 106°240 76000 106°550 17500 106°240 76200

Aquaculture shrimp Wild shrimp Aquaculture shrimp Wild shrimp Wild shrimp

6 3 8 3 3

43.5 ± 4.6 36.1 ± 6.7 30.3 ± 2.7 61.9 ± 11.7 20.3 ± 1.3

Bac Lieu Ben Tre Kien Giang Soc Trang 1 Soc Trang 2 Soc Trang 3 Tra Vinh 1 Tra Vinh 2

2004/04/23 2004/08/27 2003/09/14 2003/09/10 2003/09/13 2004/08/30 2005/04/21 2005/04/21

09°150 87000 10°090 05300 10°010 84300 09°330 10700 09°330 10700 09°320 78700 09°470 51000 09°400 92400

105°470 77700 106°430 03600 105°450 90400 105°0590 3300 105°0590 3300 105°0590 8600 106°270 17700 106°300 57600

Aquaculture shrimp Aquaculture shrimp Wild shrimp Aquaculture shrimp Aquaculture shrimp Aquaculture shrimp Wild shrimp Wild shrimp

3 3 3 3 3 3 3 3

16.4 ± 4.4 19.4 ± 2.0 70.9 ± 17.3 35.2 ± 15.0 26.0 ± 8.6 32.6 ± 3.1 18.9 ± 10.8 27.2 ± 4.1

Number of individual (non-composited) specimens.

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Fig. 1. Study area showing the sampling locations of black tiger shrimp Penaeus monodon (Abbreviations refer to Table 1).

conversion factors of 3.96 for muscle and 4.15 for hepatopancreas. The mean wet wt. of muscle and hepatopancreas corresponded to 55.5% and 2.38% of whole body wt., respectively. 2.3. Health risk estimation Since it is customary for South Vietnamese people to consume both muscle and hepatopancreas, the health risks were estimated for these two tissues. To evaluate the health risks, THQ was estimated by the concentrations (wet wt. basis) of trace elements in muscle and hepatopancreas of shrimp. According to Han et al. (1998), the following equation for estimating THQ is: THQ ¼

EF  ED  F IR  C  103 RfD  W AB  T A

where EF is exposure frequency (365 days/year); ED is the exposure duration (70 years), equivalent to the average lifetime (Bennett et al., 1999); FIR is the food ingestion rate (g/person/day); C is the metal concentration in food (lg/ g wet wt.); RfD is the oral reference dose (mg/kg body wt./day) (US EPA, 2007); WAB is the average body weight (50 kg for adults); and TA is the averaging of exposure time (365 days/year  number of exposure years, assuming 70 years in this study). It was further assumed that cooking has no effect on the toxicity of trace elements

in shrimp (e.g., Chien et al., 2002). Based on an annual fishery product consumption of 30 kg/person/year in South Vietnam, of which shrimp consumption accounted for 17% of the total quantity consumed (Ruckes and Dang, 2004; FAO, 2005), the shrimp consumption rate was estimated to be about 14 g/person/day. Based on the mean wet wt. value of tissues/whole body wt., FIR of 7.77 g muscle/person/day and 0.33 g hepatopancreas/person/day were used for these estimations. Among the trace elements analyzed in this study, the US EPA developed a RfD for V, Cr, Mn, Co, Cu, Zn, As, Se, Sr, Mo, Ag, Cd, Sn, Sb, Ba, Tl, and methyl mercury (MeHg) (US EPA, 2007). Because the majority of Hg is present as MeHg in the edible portions of fish (US EPA, 2000), we assumed that the concentration of total Hg was equal to that of MeHg in the two tissues. Lead was not available on the RBC table, but a provisional tolerable weekly intake of 25 lg/kg body wt./week (=3.57 lg/kg body wt./day) was used (EC, 2004). For the calculation of THQ of As, we assumed inorganic As accounted for 10% of the total As (MacIntosh et al., 1996; Han et al., 1998, 2000).

2.4. Statistical analyses For values below the limit of detection, half of the respective limit of detection was substituted to use in statis-

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tical analysis. All data were tested for goodness of fit to a normal distribution with a Kolmogorov–Smirnov’s one sample test. When concentration data failed to meet a normal distribution, a non-parametric test was alternatively used to compare between groups. A Wilcoxon signed ranks test was used to detect between-tissue differences in trace element concentrations. The strength of the association between body weight and trace element concentration was examined using a Spearman’s rank correlation coefficient. For testing geographical differences, data were transformed by applying neperian logarithms and were analyzed using one-way analysis of covariance with body weight as the covariate. A p-value <0.05 was considered to indicate statistical significance. All statistical analyses were performed using the program SPSS (version 10.05, SPSS, Chicago, IL, USA). 3. Results and discussion 3.1. Tissue-specific variations of trace elements A total of 47 individuals of shrimp from South Vietnam were examined in this study. Of these specimens, measurements of hepatopancreas were not available for two individuals of BRVT and two individuals of ST. Among the elements analyzed, mean concentrations of Cu (590 lg/g), Zn (142 lg/g), As (12 lg/g), Se (4.1 lg/g), Ag (3.0 lg/g) and Cd (2.15 lg/g) in hepatopancreas, Mn (99.9 lg/g), Sr (1,780 lg/g) and Ba (35 lg/g) in exoskeleton and Rb (5.74 lg/g) in muscle were relatively high (Table 2). In contrast, concentrations of In were not detected in most of samples; therefore, this element was not considered in the further discussion. In this study, the general tendency in most trace element concentrations among different tissues were hepatopancreas > exoskeleton > muscle. Concentrations of V, Cr, Co, Cu, Zn, As, Se, Mo, Ag, Cd, Sb and Bi (Wilcoxon signed ranks test, p < 0.001) were highest in hepatopancreas; whereas Mn, Sr, Ba and Pb in exoskeleton (p < 0.001), and Rb and Cs in muscle (p < 0.001). Furthermore, Hg levels in muscle and hepatopancreas were not significantly different, but higher than those in exoskeleton. For Sn concentration, exoskeletal and hepatopancreatic tissues were one order of magnitude higher than muscle. No significant difference of Tl (p > 0.05) was found among tissues. The hepatopancreas is the main regulatory organ in crustaceans and, as such, is the prime site for metal storage and detoxification in these animals. Crustaceans (e.g., shrimp) respond to metal exposure by producing metallothionein (MTs), particularly in hepatopancreas. These MTs play an important role in the regulation of essential elements and detoxification of the unusual entry of essential and non-essential ones (Bainy, 2000; Legras et al., 2000; Wu and Chen, 2005). The high concentrations of Mn, Sr, Ba and Pb in the exoskeleton are likely due to their chemical similarity to Ca. Manganese is known to be able to substitute Ca in CaCO3

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and this may explain why Mn concentrations are highest in these calcified parts (Pa´ez-Osuna et al., 1995; Pourang et al., 2004). Hockett et al. (1997) demonstrated that Sr and Mn are incorporated into barnacle shells in direct proportion to the levels of Sr and Mn in artificial sea water. In an exposure study of crayfish to Pb-contaminated sediment, Knowlton et al. (1983) observed that 80% of the Pb in intermolt crayfish was in the exoskeleton and the accumulation in the exoskeleton was mainly through adsorption. Uniquely, Cu values in the hepatopancreas varied widely over the different locations. Shrimp highly contaminated with Cu were observed in four locations of the MRD: ST (1,120 lg/g dry wt.), BL (816 lg/g), KG (716 lg/g), and TV (515 lg/g), followed by HCMC (483 lg/g), BT (448 lg/g), BRVT (422 lg/g), and LA (254 lg/g) (Table 2). The high levels of Cu may be related to the essential role of this element in the production of the respiratory protein haemocyanin (Brouwer et al., 2002; Lee and Shiau, 2002). Some crustaceans, particularly decapods, appear to have a relatively constant total body concentration of Cu over a wide range of dissolved Cu available in the environment. The caridean decapod Palaemon elegans appears to regulate the body concentration of Cu (ca. 130 lg/g dry wt.) over a wide range of dissolved Cu exposure until regulation ceases to occur at high Cu concentrations. Once regulation has stopped at high dissolved Cu, the metal concentration in P. elegans rise rapidly in direct proportion to the external Cu concentration, and reach a level of 600 lg/g dry wt. (White and Rainbow, 1982; Rainbow and White, 1989). Zinc levels in P. monodon were also present in large quantities in the hepatic material (83.5–164 lg/g dry wt.). Unlike caridean shrimps, penaeids do not show regulations of Zn body concentrations in proportion to the bioavailability of dissolved Zn by matching Zn excretion to Zn uptake. Therefore, penaeid shrimps inhabiting anthropogenically contaminated coastal waters with raised Zn bioavailabilities can be expected to contain raised body concentrations of Zn (Nun˜ez-Nogueira and Rainbow, 2005). In the black tiger shrimp, As was present in higher concentrations in the hepatopancreas (12 ± 8 lg/g) and muscle (9.0 ± 7.0 lg/g) than in the exoskeleton (2.7 ± 2.4 lg/g). A significant level of variation in Cd concentrations among tissues was observed in the shrimp. Cadmium levels in muscle, exoskeleton and hepatopancreas were 0.009 ± 0.011, 0.013 ± 0.009 and 2.15 ± 2.58 lg/g, respectively. For Ag, the highest concentrations of Ag (8.4 ± 4.6 lg/g, from KG) were found in hepatopancreas. In particular, exoskeleton contained the highest Sr and Ba levels (1,780 ± 440 and 35 ± 31 lg/g, respectively) among the tissues, which was higher than those of muscle with the lowest concentrations (7.18 ± 3.09 and 0.078 ± 0.063 lg/g, respectively). 3.2. Size-dependent variations of trace element accumulation Size-dependent variation was observed in concentrations of several trace elements in tissues of shrimp. Hepatopancreatic

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Table 2 Trace element concentrations (mean ± standard deviation of lg/g dry wt.) in tissues of the black tiger shrimp Penaeus monodon from South Vietnam Cr

Mn

Co

Cu

Zn

As

Se

Rb

Sr

Mo

Muscle BRVT HCMC LA BL BT KG ST TV

0.014 ± 0.012 0.017 ± 0.002 0.036 ± 0.004 0.063 ± 0.058 0.015 ± 0.014 0.021 ± 0.007 0.029 ± 0.007 0.015 ± 0.012

0.24 ± 0.09 0.27 ± 0.06 0.16 ± 0.05 0.40 ± 0.19 0.33 ± 0.17 0.35 ± 0.03 0.35 ± 0.25 0.18 ± 0.03

0.419 ± 0.068 0.746 ± 0.166 0.564 ± 0.063 2.32 ± 0.62 0.895 ± 0.086 0.683 ± 0.233 1.23 ± 0.48 0.967 ± 0.376

0.020 ± 0.006 0.021 ± 0.005 0.021 ± 0.002 0.015 ± 0.005 0.077 ± 0.018 0.014 ± 0.003 0.019 ± 0.013 0.024 ± 0.011

13.5 ± 2.9 14.9 ± 3.0 16.2 ± 2.2 19.9 ± 2.5 28.2 ± 2.4 9.21 ± 2.22 24.6 ± 6.8 20.4 ± 5.7

51.0 ± 3.4 48.8 ± 4.7 51.1 ± 0.4 49.2 ± 5.1 49.7 ± 2.0 50.0 ± 2.0 52.3 ± 2.0 45.9 ± 1.6

14 ± 5 15 ± 5 5.5 ± 1.9 0.83 ± 0.72 18 ± 2 10 ± 9 2.0 ± 1.5 3.5 ± 1.8

1.2 ± 0.3 1.5 ± 0.1 1.2 ± 0.1 0.80 ± 0.03 0.72 ± 0.08 1.5 ± 0.5 0.78 ± 0.26 0.63 ± 0.27

4.69 ± 0.24 4.55 ± 0.52 12.2 ± 0.4 1.55 ± 0.12 3.74 ± 0.13 7.42 ± 4.84 8.19 ± 1.56 4.68 ± 0.45

7.73 ± 2.69 9.09 ± 7.19 3.06 ± 0.51 5.13 ± 1.59 8.72 ± 1.63 9.34 ± 4.67 5.44 ± 0.75 8.46 ± 2.16

0.040 ± 0.022 0.052 ± 0.023 0.036 ± 0.005 0.020 ± 0.004 0.043 ± 0.008 0.055 ± 0.030 0.047 ± 0.030 0.035 ± 0.008

Exoskeleton BRVT HCMC LA BL BT KG ST TV

0.091 ± 0.035 0.034 ± 0.008 0.26 ± 0.12 0.80 ± 0.09 0.25 ± 0.04 0.12 ± 0.03 0.18 ± 0.11 0.062 ± 0.017

0.32 ± 0.12 0.24 ± 0.03 0.26 ± 0.03 0.94 ± 0.06 0.58 ± 0.25 0.35 ± 0.06 0.46 ± 0.26 0.25 ± 0.06

22.7 ± 9.4 8.76 ± 3.21 21.8 ± 9.9 347 ± 20 58.7 ± 22.6 59.5 ± 63.2 251 ± 109 94.5 ± 47.0

0.14 ± 0.03 0.087 ± 0.009 0.18 ± 0.06 0.38 ± 0.08 0.24 ± 0.03 0.14 ± 0.01 0.11 ± 0.01 0.12 ± 0.02

27.9 ± 7.0 16.9 ± 1.5 33.6 ± 2.7 42.0 ± 7.2 41.3 ± 5.1 16.6 ± 7.4 33.4 ± 11.0 24.8 ± 8.7

14.1 ± 2.5 18.3 ± 1.0 18.2 ± 0.8 19.0 ± 3.4 18.0 ± 1.4 25.8 ± 15.6 17.8 ± 4.4 15.7 ± 3.1

4.0 ± 1.4 4.4 ± 1.4 1.4 ± 0.5 0.33 ± 0.34 7.7 ± 1.2 3.0 ± 2.2 0.70 ± 0.97 0.26 ± 0.28

0.28 ± 0.11 0.37 ± 0.06 0.34 ± 0.05 0.12 ± 0.10 0.10 ± 0.09 0.63 ± 0.53 0.22 ± 0.15 0.06 ± 0.13

1.37 ± 0.16 1.69 ± 0.16 4.84 ± 0.13 1.95 ± 0.24 2.12 ± 0.06 2.64 ± 1.46 3.20 ± 0.30 1.74 ± 0.43

2030 ± 143 2100 ± 136 676 ± 41 1400 ± 346 1250 ± 59 1630 ± 549 1730 ± 249 2060 ± 254

0.078 ± 0.027 0.053 ± 0.020 0.054 ± 0.004 0.084 ± 0.007 0.089 ± 0.012 0.059 ± 0.015 0.085 ± 0.018 0.052 ± 0.009

0.50 ± 0.18 0.53 ± 0.16 0.46 ± 0.41 0.45 ± 0.10 0.77 ± 0.16 0.79 ± 0.53 0.55 ± 0.26 0.57 ± 0.31

6.75 ± 5.40 6.86 ± 3.03 4.75 ± 2.33 15.6 ± 2.1 5.79 ± 0.79 15.5 ± 6.1 16.2 ± 8.1 20.0 ± 21.2

2.3 ± 1.3 1.1 ± 0.7 1.1 ± 0.2 0.84 ± 0.50 2.9 ± 0.7 2.3 ± 1.0 1.7 ± 1.5 2.1 ± 0.8

422 ± 318 483 ± 179 254 ± 10 816 ± 316 448 ± 36 716 ± 274 1120 ± 394 515 ± 362

152 ± 42 159 ± 22 86.6 ± 8.8 150 ± 23 83.5 ± 4.6 164 ± 67 159 ± 59 131 ± 42

19 ± 6 20 ± 1 5.6 ± 1.7 2.3 ± 0.2 19 ± 4 11 ± 8 4.6 ± 2.1 10 ± 4

3.4 ± 1.4 6.9 ± 2.2 1.8 ± 0.4 3.8 ± 1.2 2.0 ± 0.1 7.9 ± 4.1 2.9 ± 0.9 6.4 ± 2.7

4.17 ± 1.31 3.52 ± 0.16 8.43 ± 1.02 1.60 ± 0.10 4.01 ± 0.18 4.61 ± 0.97 5.39 ± 0.78 3.33 ± 1.07

81.7 ± 61.7 55.7 ± 26.8 10.8 ± 1.8 26.4 ± 5.5 45.1 ± 4.6 38.1 ± 5.7 28.2 ± 9.4 44.1 ± 27.0

2.58 ± 1.86 2.09 ± 2.31 0.582 ± 0.056 0.558 ± 0.024 0.687 ± 0.007 1.34 ± 0.44 1.27 ± 0.86 1.96 ± 0.83

Hepatopancreas BRVT 0.22 ± 0.11 HCMC 0.22 ± 0.08 LA 0.14 ± 0.01 BL 0.26 ± 0.13 BT 0.14 ± 0.05 KG 0.80 ± 0.53 ST 0.28 ± 0.12 TV 0.41 ± 0.42 Ag

Cd

Sn

Sb

Cs

Ba

Hg

Tl

Pb

Bi

Muscle BRVT HCMC LA BL BT KG ST TV

0.007 ± 0.005 0.011 ± 0.003 0.003 ± 0.001 0.002 ± 0.002 0.018 ± 0.012 0.014 ± 0.010 0.006 ± 0.003 0.023 ± 0.026

0.003 ± 0.002 0.013 ± 0.004 0.009 ± 0.005 0.007 ± 0.002 0.043 ± 0.013 0.017 ± 0.012 0.005 ± 0.003 0.015 ± 0.009

0.007 ± 0.008 0.018 ± 0.005 0.007 ± 0.006 0.058 ± 0.033 0.173 ± 0.089 0.026 ± 0.019 0.107 ± 0.120 0.041 ± 0.027

<0.01 <0.01 <0.01 <0.01 <0.01 0.02 ± 0.01 0.03 ± 0.03 <0.01

0.03 ± 0.01 0.03 ± 0.01 0.04 ± 0.01 0.01 ± 0.01 0.03 ± 0.00 0.04 ± 0.02 0.02 ± 0.01 0.03 ± 0.00

0.025 ± 0.009 0.057 ± 0.034 0.11 ± 0.04 0.15 ± 0.05 0.084 ± 0.011 0.040 ± 0.012 0.094 ± 0.026 0.18 ± 0.08

<0.05 <0.05 <0.05 <0.05 <0.05 0.07 ± 0.05 0.06 ± 0.04 <0.05

<0.001 0.004 ± 0.001 0.003 ± 0.003 0.001 ± 0.001 <0.001 0.005 ± 0.005 0.002 ± 0.001 0.003 ± 0.001

0.024 ± 0.046 0.008 ± 0.001 0.009 ± 0.002 0.028 ± 0.016 0.015 ± 0.006 0.021 ± 0.016 0.014 ± 0.007 0.009 ± 0.005

0.002 ± 0.001 <0.001 <0.001 0.002 ± 0.001 <0.001 0.013 ± 0.017 0.023 ± 0.017 0.007 ± 0.006

Exoskeleton BRVT HCMC LA BL BT

0.018 ± 0.018 0.013 ± 0.004 0.004 ± 0.001 0.004 ± 0.001 0.006 ± 0.002

0.011 ± 0.009 0.016 ± 0.005 0.014 ± 0.002 0.016 ± 0.006 0.016 ± 0.005

0.019 ± 0.014 0.012 ± 0.004 0.008 ± 0.006 0.114 ± 0.060 0.184 ± 0.134

0.01 ± 0.03 <0.01 <0.01 0.03 ± 0.02 0.02 ± 0.00

0.01 ± 0.01 0.01 ± 0.00 0.03 ± 0.01 0.11 ± 0.01 0.04 ± 0.00

9.2 ± 3.0 16 ± 2 61 ± 17 47 ± 15 26 ± 2

<0.05 <0.05 <0.05 <0.05 <0.05

<0.001 0.005 ± 0.001 0.007 ± 0.006 0.007 ± 0.001 0.001 ± 0.001

0.158 ± 0.081 0.044 ± 0.006 0.142 ± 0.043 0.537 ± 0.151 0.403 ± 0.173

0.002 ± 0.001 <0.001 0.002 ± 0.001 0.006 ± 0.001 0.003 ± 0.001

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V

0.009 ± 0.005 0.006 ± 0.004 0.003 ± 0.001 0.005 ± 0.001 0.014 ± 0.005 0.025 ± 0.014 0.056 ± 0.038 0.021 ± 0.007 0.052 ± 0.028 0.090 ± 0.008 0.016 ± 0.003 0.087 ± 0.042 0.060 ± 0.034 0.337 ± 0.124 0.114 ± 0.072 0.118 ± 0.090 0.001 ± 0.002 0.003 ± 0.001 0.002 ± 0.003 0.002 ± 0.001 <0.001 0.010 ± 0.005 0.003 ± 0.001 0.005 ± 0.004 <0.05 0.09 ± 0.05 <0.05 0.06 ± 0.03 <0.05 <0.05 0.07 ± 0.05 <0.05 0.561 ± 0.342 3.51 ± 1.03 2.46 ± 0.49 1.78 ± 0.30 4.14 ± 0.23 8.37 ± 5.99 0.608 ± 0.377 3.19 ± 1.17 Hepatopancreas BRVT 2.9 ± 2.6 HCMC 4.1 ± 1.5 LA 0.86 ± 0.23 BL 0.42 ± 0.17 BT 1.2 ± 0.2 KG 8.4 ± 4.6 ST 1.7 ± 1.0 TV 5.0 ± 2.7

0.014 ± 0.015 0.104 ± 0.026 0.009 ± 0.004 0.210 ± 0.216 0.280 ± 0.017 0.054 ± 0.020 0.131 ± 0.192 0.057 ± 0.036

0.04 ± 0.02 0.05 ± 0.02 <0.01 0.03 ± 0.01 0.03 ± 0.00 0.07 ± 0.05 0.04 ± 0.03 0.04 ± 0.02

0.03 ± 0.01 0.02 ± 0.01 0.02 ± 0.01 0.02 ± 0.01 0.03 ± 0.01 0.09 ± 0.07 0.02 ± 0.01 0.03 ± 0.03

0.59 ± 0.35 0.94 ± 0.32 1.0 ± 0.5 1.2 ± 0.3 0.57 ± 0.16 1.5 ± 1.0 1.3 ± 0.6 2.6 ± 3.2

0.010 ± 0.009 0.004 ± 0.001 0.005 ± 0.004 0.028 ± 0.021 0.007 ± 0.002 0.019 ± 0.006 KG ST TV

0.021 ± 0.016 0.004 ± 0.002 0.018 ± 0.015

0.030 ± 0.014 0.1 ± 0.090 0.049 ± 0.015

0.02 ± 0.01 0.04 ± 0.02 <0.01

0.02 ± 0.01 0.03 ± 0.02 0.02 ± 0.01

19 ± 6 57 ± 11 76 ± 49

<0.05 <0.05 <0.05

0.332 ± 0.200 0.309 ± 0.143 0.084 ± 0.012

0.002 ± 0.001 0.005 ± 0.001 0.003 ± 0.002

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V, Zn, As, Se, Mo, Ag and Sb, muscular As, Se, Mo and Cs, and exoskeletal As, Se, Sr, and Ag levels increased with body weight (Spearman’s rank correlation, p < 0.05); whereas concentrations of Mn, Cu, Sn and Ba in muscle, and V, Mn, Cu, Sn, Cs, Ba and Bi in exoskeleton exhibited a significantly negative relationship (p < 0.05). The size-dependent variation, i.e. body weight and length dependence, in trace elements levels have been reported for many penaeid species. Pa´ez-Osuna and Ferna´ndez (1995b) found that the levels of Fe and Ni in muscle decreased with an increase in body length in the Mexican shrimp Penaeus vannamei; whereas the opposite tended to occur for Zn. The Fe, Mn, Ni and Co concentrations in muscle of Penaeus stylirostris were also negatively correlated with body size. In contrast, Cu levels were associated with size (Pa´ez-Osuna and Ferna´ndez, 1995a). A moderate decrease of Mn, Cu, Sn and Ba concentrations in muscle and exoskeleton may be explained by molting-related loss of the elements or an increase in shrimp size could ‘‘dilute” the metal content (Me´ndez et al., 1997). 3.3. Regional variation in trace element concentrations For testing regional differences, sampling sites were divided into two regions according to the Vietnamese economic areas: SKEZ including BRVT, HCMC, and LA, and MRD including BL, BT, KG, ST and TV (Table 1). One-way analysis-covariance showed significant regional differences in concentrations of most elements (p < 0.05), except for Co, Sr, Mo, and Ag. Levels of Mn, Cu, Cd, Sn, Sb, Ba, Hg, Tl and Bi in muscle, Cr, Mn, Zn, Rb, Sn, Sb, Cs, Ba, Tl, Pb and Bi in exoskeleton, and V, Mn, Cu, Cd, Sn, Ba, Tl, Pb and Bi in hepatopancreas were higher from MRD than from SKEZ (p < 0.05). In contrast, levels of Se in muscle and As in the three tissues (p < 0.001) were higher from SKEZ than from other one. The high concentration of most trace elements in shrimp from MRD suggests that sources of contamination of these elements may have originated from agricultural use of mineral fertilizers and pesticides. During the dry season in South Vietnam (November–May), particularly in MRD, there is an intrusion of seawater into lowland rice fields, and as a result, many farmers develop an alternating riceshrimp farming system within the same field, producing shrimp in the dry season and rice in the wet season. Some farmers have even abandoned the rice crop cycle and transformed their rice-shrimp fields into conventional shrimp ponds (Brennan et al., 2002). The development of the rice-shrimp farming system in the MRD has resulted in the increased accumulation of trace elements in shrimp. Copper sulfate is applied rice fields for the control of golden apple snails, which are an agricultural pest in Vietnam (Huan and Joshi, 2002; Ngoc, 2002). Phosphate fertilizers are a major source of Cd input to agricultural soils. The concentration of Cd in phosphate fertilizers in Vietnam ranges from 0.02 to 2.76 mg/kg (Hung et al., 2005). For Hg, about 15% of the total Hg is released to the soil

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from fertilizers, fungicides, and municipal solid waste (ATSDR, 1999). The same trend of high concentrations of Cd, Hg in Macrobrachium rosenbergii collected from MRD was also reported in our previous study (Tu et al., 2008). On the contrary, concentrations of As in all three tissues were significantly lower than SKEZ. Ai et al. (2001) reported that sedimentary As concentrations were higher in SKEZ coastal zone than in the Mekong River Delta, with levels of 26 ppm and 3–5 ppm, respectively. 3.4. Comparison of trace element levels in Vietnamese shrimp with those in other regions The Cu concentrations in muscles and exoskeleton of P. monodon were comparable to the Mexican shrimp P. stylirostris and P. vannamei. However, hepatopancreatic Cu levels in P. monodon were similar to those found in Penaeus semiculatus and Metapenaeus monocerus at Iskenderun, Turkey (an area polluted by factories), which exceeded the maximum in P. vannamei of given studies (Pa´ez-Osuna and Tron-Mayen, 1996; Kargin et al., 2001). Concentrations of Cr and Co in the muscle and Zn in all tissues of P. monodon were lower than in most other penaeid shrimps studied previously, such as P. stylirostris and P. vannamei (Pa´ez-Osuna and Ferna´ndez, 1995a,b). Mean concentrations of Mn in both muscle and hepatopancreas of the shrimp P. monodon were a similar order of magnitude to those reported from shrimp from coastal waters of Northwest Mexico (Pa´ez-Osuna and Ferna´ndez, 1995a,b; Pa´ezOsuna and Tron-Mayen, 1996); whereas Mn levels in the exoskeleton were extremely elevated. The average levels of

Se in muscles (0.16–0.38 lg/g wet wt.) were similar to those Mediterranean shrimps (Plessi et al., 2001). For Cd, the concentrations measured in muscle of the present study are lower than those found in other shrimp species; but, hepatopancreatic Cd levels were comparable to those in other species of shrimp. Total As concentrations in muscles found in this study were similar to those in black tiger shrimps from Pak Pa-Nang Estuary, Thailand (Rattanachongkiat et al., 2004). Levels of Hg in tissues of shrimp from South Vietnam were considered lower than those in other shrimp species. In Mediterranean shrimps, Hg levels in edible tissues ranged from 0.023 to 0.150 lg/g fresh wt. (Plessi et al., 2001). Mean concentrations of Hg in muscles, exoskeletons and hepatopancreas of penaeid shrimps from Altata-Ensenada del Pabello´n lagoon (Southeast Gulf of California, Mexico) were 0.19, 0.10 and 0.51 lg/g dry wt., respectively (RuelasInzunza et al., 2004). 3.5. Human health risks associated with trace element accumulation in shrimp The THQ values for all analyzed elements of both tissues were <1.0. Similarly, the total THQ of each element (i.e., the sum of muscle and hepatopancreas) due to the consumption of shrimp was <1. The total element THQ for ten elements (i.e., sum of individual element THQs for both tissues) via consuming shrimp in different areas is shown in Fig. 2 (THQs for other elements were too low and excluded). It has been reported that the exposure to two or more pollutants may result in additive and/or interactive effects (Chien et al., 2002). In this study, the

Fig. 2. The total metal THQ values via consuming tissues of black tiger shrimp Penaeus monodon.

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total element THQ is treated as the mathematical sum of each individual element THQ for both tissues derived by the method by Chien et al. (2002). Also, the total element THQ values for each population were <1. These results suggest that local residents are not exposed to non-carcinogenic risks by the consumption of shrimp. In conclusion, to our knowledge, this is one of the pioneer study on the accumulation profiles of trace elements in the tissues of the black tiger shrimp from South Vietnam, a species that is economically important to the regional economy. Our results provide clear evidence for the presence of contamination sources of Cu, Cd and Hg in the MRD, and As in the SKEZ. The geographical differences in contamination pattern of the trace elements likely reflect variations in agricultural and urban activities. All of THQ values were <1, suggesting that the consumption of shrimp from these areas is not harmful to consumers. Acknowledgements We express our sincere thanks to Dr. Todd Miller for critical review of the manuscript. The study was partially supported by a grant from Research Revolution 2002 (RR2002) of Project for Sustainable Coexistence of Human, Nature and the Earth (FY2002) from the Ministry of Education, Culture, Sports, Science and Technology, Japan and a Research Grants-in-Aid for Scientific Research from the Japan Society for Promotion of Science (No. 16310042). References Ai, D.V., Nhuan, M.T., Vinh, N.K., 2001. Arsenic distribution in nature and the environment pollution by arsenic in Vietnam. In: Current Situation of Arsenic Pollution in Vietnam. Department of Geology and Minerals of Vietnam, Ha Noi. ATSDR (Agency for Toxic Substances and Disease Registry), 1999. Toxicological profile for mercury. US Department of Health and Human Services. Bainy, A.C.D., 2000. Biochemical responses in penaeids caused by contaminants. Aquaculture 191, 163–168. Bennett, D.H., Kastenberg, W.E., McKone, T.E., 1999. A multimedia, multiple pathway risk assessment of atrazine: the impact of age differentiated exposure including joint uncertainty and variability. Reliability Engineering and System Safety 63, 185–198. Brennan, D., Preston, N., Clayton, H., Be, T.T., 2002. An evaluation of rice-shrimp farming systems in the Mekong Delta. Report of the World Bank/NACA/WWF/FAO Consortium Program on Shrimp Farming and the Environment. Brouwer, M., Syring, R., Brouwer, T.H., 2002. Role of a copper-specific metallothionein of the blue crab, Callinectes sapidus, in copper metabolism associated with degradation and synthesis of hemocyanin. Journal of Inorganic Biochemistry 88, 228–239. Chien, L.C., Hung, T.C., Choang, K.Y., Yeh, C.Y., Meng, P.J., Shieh, M.J., Han, B.C., 2002. Daily intake of TBT, Cu, Zn, Cd and As for fishermen in Taiwan. Science of the Total Environment 285, 177–185. EC (European Commission), 2004. Assessment of the dietary exposure to arsenic, cadmium, lead and mercury of the population of the EU Member States. Reports on Tasks for Scientific Cooperation, March 2004. FAO, 2005. Fishery country profile: The Socialist Republic of Vietnam. .

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