Bioaccumulation of trace metals in farmed fish from South China and potential risk assessment

Ecotoxicology and Environmental Safety 74 (2011) 284–293

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Bioaccumulation of trace metals in farmed fish from South China and potential risk assessment Yao-Wen Qiu a,b, Duan Lin c, Jing-Qin Liu c, Eddy Y. Zeng b,n a

Key Laboratory of Tropic Marine Environmental Dynamics, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China c South China Sea Branch, State Oceanic Administration of China, Guangzhou 510300, China b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 2 April 2010 Received in revised form 9 September 2010 Accepted 3 October 2010 Available online 18 October 2010

Concentrations of trace metals were determined in water, sediment, fish feed and two species of farmed fish, pompano and snapper, collected from Daya Bay and Hailing Bay of South China in July 2007 and January 2008. Total average concentrations of Cu, Pb, Zn, Cd, Cr, Hg and As were 1.6, 2.7, 27.3, 0.025, 0.62, 0.18 and 0.59 mg/g dry wt in pompano and 1.5, 2.6, 23.6, 0.020, 0.55, 0.22 and 0.53 mg/g dry wt in snapper. In general, the concentrations of all target metals except Hg were positively correlated with lipid contents whereas negative correlations were observed between the metal concentrations and fish body weights. Model calculation indicated that dietary uptake of Zn and Cd predominate their accumulation in snapper, accounting for 99.9% and 98.2% of the total inputs. Risk assessments suggested that potential ecological and human health risk may be present due to elevated Pb concentrations in sediment and farmed fish. & 2010 Elsevier Inc. All rights reserved.

Keywords: Fish Trace metals Bioaccumulation Risk assessment South China

1. Introduction Fish are one of the important sources of proteins with omega-3 polyunsaturated fatty acids, which are renowned globally for greatly reducing cholesterol levels and maintaining healthy human hearts, brains, joints and immune systems (Daviglus et al., 2002). The fishery culture has been growing rapidly worldwide due to the increasing demand for fish as a food source. At present, Guangdong Province (South China) is one of the most important fish-culturing bases in China. Previous studies demonstrated that the mean and upper-bound concentrations of organochlorine pesticides, polychlorinated biphenyls and polybrominated diphenyl ethers in fish collected from the coast of South China were lower than the action and tolerance levels developed by the United States Food and Drug Administration, but the concentrations of organochlorine pesticides in fish feed were at the upper levels of the global range (Meng et al., 2007; Guo et al., 2009a; 2009b). On the other hand, the state of trace metal pollution in farmed fish and fish feed has yet to be thoroughly examined. Widespread industrial activities due to rapid economic growth over the last few decades have led to trace metal contamination in the environment of China (Chen et al., 2000; Streets et al., 2005). These highly persistent and non-biodegradable contaminants have been

n

Corresponding author. Fax: + 86 20 85290706. E-mail address: [email protected] (E.Y. Zeng).

0147-6513/$ - see front matter & 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ecoenv.2010.10.008

reported to cause toxic effects in fish and may be bioaccumulated via food web to hazardous levels, thus posing potential health risk to human fish consumers (Foran et al., 2005; Tsuchiya et al., 2008; Mathews and Fisher, 2009), though some metals are essential elements with important physiological roles at low levels. For example, mercury in the aquatic environment can impact the reproductive health of fish (Crump and Trudeau, 2009). Methylmercury was shown to counteract cardioprotective effects and to damage developing fetuses and young children (2000). Moderate exposure to Pb and Cd can also significantly reduce human semen quality and is related to many diseases in adults and children alike (e.g., damage to DNA or impairment of the reproductive function) (Teliˇsman et al., 2000). Therefore, there is an urgent need to understand the processes of bioaccumulation and biomagnification of these toxic metals in farmed fish. Elevated levels of trace metals in the marine environments around the world have been well documented in the last century as coastal areas act as dumping sites for waste chemicals, where these pollutants were pooled up in huge quantities (Fowler, 1990; Furness and Rainbow, 1990; Chen et al., 2000; van der Oost et al., 2003). Many previous studies on the occurrence of trace metals in the coast of South China have mainly focused on sediments (Li et al., 2000), water (Ho and Hui, 2001) and wild organisms (Wong et al., 2000; Ip et al., 2005; Qiu et al., 2005a). To our knowledge, few monitoring programs have been conducted to survey the state of pollution and bioaccumulation of trace metals in farmed fish. Thus further research work is needed to fill the knowledge gap. Furthermore, a lot of fish cultured in the coast of

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285

Fig. 1. Sampling locations in Daya Bay and Hailing Bay, South China.

Guangdong Province are exported to many other countries in recent years, and fish quality will certainly affect human health around the world. The present work aimed to (1) examine the current pollution status of trace metals (Cu, Pb, Zn, Cd, Cr and Hg) and As (designated as trace metals thereafter) in seawater, sediment and farmed fish collected from Daya Bay and Hailing Bay, South China (Fig. 1), two areas with extensive fish culturing activities; (2) study the bioaccumulation of trace metals in farmed fish; (3) assess the potential ecological risk of trace metals and consequently the health risk to human fish consumers.

2. Materials and methods 2.1. Study area Daya Bay is a subtropical semi-enclosed bay adjacent to Hong Kong, with a coastal line of 92 km and an area of 600 km2. There are a few small seasonal streams flowing into the bay, and a nuclear power station is located on the bank. The annual average values of water color, transparency, turbidity, temperature, salinity, pH and dissolved oxygen in the past 20 years were 8.0, 3.0 m, 2.53, 23.81 1C, 31.52%, 8.23 and 7.06 mg/L, respectively, which were obtained by a long-term monitoring program (Qiu et al., 2005b). Impaired water quality as characterized by frequent occurrence of red tides has resulted in a drastic decline of phytoplankton and zooplankton biomass, severely depressing the fish population (Qiu et al., 2005b). On the other hand, Hailing Bay, located in the western Guangdong Province where agriculture has traditionally been a dominant economic driving force, is relatively

less impaired by industrial activities compared to Daya Bay, and was therefore selected as a reference site. In addition, Hailing Bay is also an important marine aquaculture base and appropriate for conducting metal bioaccumulation studies.

2.2. Sample collection and processing Seawater, surface sediment and farmed fish samples from seven sites in Daya Bay (S1, S2, S3 and Sc) and Hailing Bay (Y1, Y2 and Y3) (Fig. 1 and Table 1) were collected in July 2007. Sediment samples were collected from the upper 2 cm layer using a box grab sampler and placed in acid-rinsed polypropylene bag. Three sediment samples at each site (triangle sampling method) were collected. Meanwhile, 2 L surface water (0.5 m under the sea level) and bottom water (0.5 m above the sea floor) samples were also collected using a glass water sampler. The samples were stored at  4 1C immediately after collection until laboratory analysis. A total of 69 pompano (Trachinotus blochii) and 64 snapper (Lutjanus malabaricus) individuals of different sizes, with a median body weight of 621.8 g (ranging between 160 and 3500 g) for pompano and a median body weight of 513.4 g (ranging between 185 and 1578 g) for snapper, were collected in July 2007 and January 2008. Fish feed samples including compound feed and trash fish were simultaneously collected. All farmed fish and fish feed samples were stored in polyethylene bags with ice immediately after collection and frozen at  20 1C until analysis. Because all fish individuals were purchased dead from local fishermen working at the two culturing bases, the present study did not involve any ethical issues. Fish individuals were thawed at room temperature and dissected carefully to obtain muscles and whole body samples. Muscle is the most important organ in terms of human exposure, while whole body burden is a critical parameter for ecological risk assessment. Portions of the fish samples were freeze-dried and homogenized for determination of Cu, Pb, Zn, Cd and Cr, while the concentrations of

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Table 1 The average concentrations of trace metals in fish samples collected from around the world, along with the standards for trace metals in fish recommended by the Food and Agricultural Organization (FAO). Species

n

Pb

Zn

Cd

Ref.*

0.18

0.17

In present

0.23

0.10

Cu

Daya Bay, South China (muscle) Pompano 26 Snapper 20

mg/g dw mg/g dw

1.3

3.8

26.9

0.013

0.55

0.9

2.2

18.9

0.011

0.36

Hailing Bay, South China (muscle) Pompano 30 Snapper 23

mg/g dw mg/g dw

1.2 1.3

2.1 2.6

23.5 16.0

0.011 0.010

0.44 0.43

0.22 0.29

0.23 0.14

In present

Daya Bay, South China Benthonic fish

0.051

1.24

[1]

mg/g ww

1.08

0.24

13.1

0.069

Pearl River estuary, south China Benthonic fish 35

mg/g ww

1.81

2.2

18.4

0.049

Gulf and Gulf of Omen Grouper

10

mg/g dw

0.44

0.11

21.8

0.002

Catalonia, Spain Sardine Tuna Salmon

2 2 2

mg/g ww mg/g ww mg/g ww

0.05 0.02 0.13

0.006 0.015 0.010

New Jersey, US Blue fish Flounder Yellowfin tuna

51 55 50

mg/g ww mg/g ww mg/g ww

0.06 0.06 0.04

0.006 0.01 0.03

20

Coastal waters of Victoria, Australia Abalone 50 Snapper 50 Flathead 1 40 Flathead 2 20

mg/g dw mg/g dw mg/g dw mg/g dw

2.6 0.3 0.2 0.1

0.05 0.05 0.05 0.05

11.30 5.20 3.40 6.10

0.12 0.02 0.02 0.02

Standard of assessment Fish

mg/g ww

20

2

50

0.3

Cr

As

Unit

Hg

[2] 0.034

0.25 0.31 0.20

1

1.04

3.6

[3]

0.08 0.48 0.05

3.74 1.12 1.99

[4]

0.26 0.05 0.65

0.26 3.3 1.0

[5]

0.01 0.17 0.08 0.14

7.7 4.7 1.4 10.9

[6]

0.5

1.4

[5]

ww: wet weight; dw: dry weight. * [1] Qiu et al. (2005b), [2] Ip et al. (2005), [3] de Mora et al. (2004), [4] Falco´ et al. (2006), [5] Burger and Gochfeld (2005), [6] Fabris et al. (2006).

Hg and As were determined with wet samples. Sediment samples for analysis of Cu, Pb, Zn, Cd and Cr were oven-dried at 105 1C, disaggregated and ground in an agate mill to pass a screen with a nominal size of 100 mesh, while wet sediment samples were used to determine the concentrations of Hg and As. Water samples were filtered using GF/F filters (nominal pore size 0.7 mm; Whatman International, Maidstone, England) to separate suspended particulate matter and filtrates. All glassware was cleaned by soaking in 10% HNO3 (v/v) for at least 2 days, followed by soaking and rinsing with deionized water. 2.3. Chemical analysis Measurements of trace metals in seawater, sediment and fish largely followed the procedures described previously (Qiu et al., 2005a). Sediment samples at 0.5 g and fish samples at 0.5  1.0 g were accurately weighed to determine the concentrations of trace metals. Concentrations of Cu, Pb, Zn, Cd and Cr in sediment and fish samples were determined using atomic adsorption spectrometry (SOLAAR M6, UK), while those of Hg and As were determined with atomic fluorescence spectrometry (AFS-8130, Beijing, China). Polarography (HY-1E, Qingdao, China) was used to determine the concentrations of the target trace metals in water. In addition, subsamples of sediment, feed and fish were dried to constant weight to determine the water contents; total organic carbon (TOC) contents in water and sediment samples were determined by Carbon Analyzer (Sunset Laboratory, USA), and fish lipid was determined gravimetrically after sample being Soxhlet extracted with a 1:1 (v/v) acetone and hexane mixture for 48 h. 2.4. Quality assurance and quality control Reagent blanks, the Chinese national standard samples of GBW07314 (reference materials for offshore sediment) and GBW08571 (reference materials for mussel) were used to monitor the analytical quality. The results were consistent with the reference values with relative differences within 10% (mostly within 5%). Blank determinations were carried out for each set of analysis. The limits of determination of Cu, Pb, Zn, Cd, Hg and As in seawater were 0.8, 1.8, 0.3, 0.20, 0.007 and 0.5 mg/L. The detection limits of Cu, Pb, Zn, Cd, Cr, Hg and As in sediment were 0.1, 0.1, 0.2, 0.02, 0.2, 0.002 and 0.06 mg/g dry wt, and in fish were 0.2, 0.1, 0.2, 0.01, 0.20, 0.010 and 0.20 mg/g dry wt, respectively.

2.5. Data analysis Metal bioaccumulation in fish can be calculated by equation (Wang and Fisher, 1999; Wang and Rainbow, 2008): Css ¼

ku  Cw AE  IR  Cf þ kew þ g kef þ g

the

following

ð1Þ

where Css is the total metal concentration in fish (mg/g), ku is the uptake rate constant from the dissolved phase (L/g d), Cw is the metal concentration in the dissolved phase (mg/L), kew is the efflux rate constant following uptake from the dissolved phase (d  1), AE is the metal assimilation efficiency from the dietary phase, IR is the weight-specific ingestion rate of the fish (g/g d), Cf is the metal concentration in the dietary phase (mg/g), kef is the efflux rate constant following uptake from food (d  1) and g is the growth rate constant of the fish (d  1). To determine whether accumulation via the dissolved phase or dietary uptake was the more important source of trace metals in farmed fish, the relative contribution of dietary metal intake can be inferred from Eq. (1) as %dietary uptake ¼

ðAE  IR  Cf Þ=ðkef þ gÞ  100 Css

ð2Þ

2.6. Statistical analysis In the present study, Pearson Correlation was conducted using SPSS for Windows Release 10.0. In order to study the general characteristics of trace metals in the estuarine bays of South China, the concentrations of trace metals in sediment and fish and the TOC content in sediment as well as the lipid content in fish were used as the input data in the PC. Meanwhile, t-test was applied to assess the differences of the concentrations of trace metals in various compartments.

3. Results and discussion Chemical parameters including water depth, pH, total organic carbon (TOC) and nutrients concentrations in waters of Daya and Hailing Bays of South China are summarized in Table S1.

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3.1. Occurrence of trace metals in seawater and sediment The average concentrations of Cu, Pb, Zn, Cd, Hg and As in seawater from Daya Bay were 2.4, 0.7, 10.4, 0.20, 0.49 and 1.4 mg/L, while those from Hailing Bay were 2.4, 0.7, 11.4, 0.29, 0.12 and 1.3 mg/L, respectively. There was no obvious difference between the trace metal concentrations in seawater from the two bays except for Hg concentrations which were higher in Daya Bay than in Hailing Bay (Fig. 2a). Compared with historical data (Qiu et al., 2005a), the concentrations of Cu, Pb, Zn and As at Daya Bay from the present study declined while the concentrations of Hg and Cd increased. Seawater trace metal concentrations in the two bays were relatively lower than those observed in six estuaries in Texas of the United States (Cu: 100–3200; Pb: 16–305; Zn: 300–18000 mg/L) (Benoit et al., 1994) and coastal and estuarine seawater in North Australia (Cu: 308; Pb: 7.7; Zn: 126; Cd: 4.1 mg/L) (Munksgaard and Parry, 2001), but were comparable to those from Deep Bay, South China (Cu: 5.8; Pb: o1; Zn: 39.5; Cd: o1; and Cr: o1 mg/L) (Cheung et al., 2003). The average concentrations of Cu, Pb, Zn, Cd, Cr and Hg in sediment of Daya Bay were 24.6, 589, 117.0, 0.32, 48.6 and 0.089 mg/g dry wt, while those at Hailing Bay were 21.9, 1088, 79.9, 0.36, 34.6 and 0.078 mg/g dry wt, respectively. The sediment trace metal concentrations were also not significantly different between the two bays (Fig. 2b). Intensified agriculture is universal around Hailing Bay leading to the use of large quantities of fertilizers and pesticides with metals, resulting in high levels of trace metals in the local environment. Antifouling paint with metals might have contributed to the elevated levels of metals

287

in Hailing Bay as a large number of fishing boats have visited the area in recent years. The levels of Cu, Zn and Hg in sediment acquired in the present study were not significantly different from those observed in the past decade, whereas the levels of Cd and Pb have increased significantly (Zheng et al., 1992; Qiu et al., 2005a; 2005c). It is worthwhile to note that continuously increased levels of Pb over the past 20 years have also been observed in the nearby water bodies, e.g., the Pearl River Estuary (Li et al., 2000). Coal burning at the power station and other industrial facilities in the region may be the major source of Pb in the sediments via surface runoff and atmospheric deposition (Li et al., 2000). Levels of trace metals except for Pb in the two bays were within the low to medium range of those reported in other areas of the world, e.g., Deep Bay of South China (Cheung et al., 2003), Pearl River Estuary (Li et al., 2000), the west coast of Peninsular Malaysia (Yap et al., 2002), Mediterranean Sea (Buccolieri et al., 2006) and the Pacific coast of the United States (Meador et al., 1998). The concentrations of trace metals in sediments of several major rivers (Minjiang, Beijiang and Pearl Rivers) in southern China have been influenced by the geological settings (e.g., widespread non-ferrous mineral deposits in this region) and strong weathering under the subtropical climate in southern China (Chen et al., 2000). The formation of marine sediment is primarily controlled by hydrologic forces (e.g., wave and tide), physico-chemical processes (e.g., flocculation, deposition and oxidation–reduction reactions) and biological processes (e.g., bioturbation). Higher TOC contents might stimulate more active microbial degradation of organic matter in sediment, resulting in various chemical compositions

Fig. 2. The average concentrations (7 SD) of trace metals in seawater (a) and sediment (b) from Daya Bay and Hailing Bay obtained in the present study and from the literature (Zheng et al., 1992; Qiu et al., 2005a; 2005c). dw ¼dry weight.

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in sediment. Fish excreta and excessive foodstuff deposited in sediments around the marine cultural area may interfere with the results. In the present study, TOC contents in sediment samples collected from the cultural area of Daya Bay and Hailing Bay were 14.171.4 and 7.5 72.6 mg/g, respectively. Our previous studies showed that surface sediments in Hailing Bay were dominated by clay silt and sand, with grain size ranging from 0.52 to 7.55+ (average: 4.6272.36+), and those in Daya Bay were dominated by silty sand (Qiu et al., 2005c). Positive correlations were observed between all target metals and TOC contents in sediment of Hailing Bay, while significant correlations were only found between Zn and Cd and TOC contents in sediment of Daya Bay (Table S2). The correlations between the concentrations of the target trace metals in sediments are also summarized in Table S2. Significant linear correlations were found among the concentrations of Cu, Zn, Cr and Hg in sediment of Hailing Bay and between the concentrations of

Cu and Cr in sediment of Daya Bay, probably indicating similar sources for these metals. 3.2. Occurrence of trace metals in farmed fish The distributions of trace metals in muscle and whole pompano and snapper are shown in Fig. 3, with average concentrations in fish muscle being summarized in Table 1. The total average concentrations of Cu, Pb, Zn, Cd, Cr, Hg and As in fish muscle and whole fish were 1.671.0, 2.773.5, 27.3711.9, 0.01570.017, 0.5470.34, 0.1870.11 and 0.2170.25 mg/g dry wt in pompano (n¼69) and 1.571.3, 2.673.4, 23.6711.8, 0.02070.010, 0.5570.43, 0.2270.14 and 0.5370.54 mg/g dry wt in snapper (n¼64). Lipid contents in the muscle and whole of pompano were 9.774.0 and 44.1716.6 mg/g, and those in snapper were 3.472.0 and 27.5715.9 mg/g, respectively. Generally, trace metals (except

Fig. 3. The distribution of trace metals in farmed fish from Daya Bay and Hailing Bay (horizontal bar represents average values, on dry weight basis).

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Hg) and lipid contents were higher in whole fish than in muscle tissue in pompano and snapper. The average concentrations of the target metals were comparable both in the two species and in two cultured bases. However, the concentrations of Hg in seawater were higher in Daya Bay than in Hailing Bay as mentioned above, which may suggest that seawater is not the major source of Hg accumulated in the farmed fish. In Daya Bay, the residual levels of trace metals in pompano were higher in Aotou (S1 of Fig. 1d) than in Dongshan (S3 of Fig. 1d), consistent with the higher trace metal concentrations in sediment of Aotou than in that of Dongshan. On the other hand, the concentrations of trace metals in snapper were not consistent with those in sediment. These observations indicate that pompano is more sensitive to the variation of trace metal concentrations in the environment than snapper. In Hailing Bay, the concentrations of trace metals in both pompano and snapper were higher in Hailing Harbor (Y3 of Fig. 1c) than in Fengtou Estuary (Y1 of Fig. 1c), consistent with the slightly higher concentrations in sediment of Hailing Harbor than that of Fengtou Estuary. Overall, the concentrations of trace metals except Pb in farmed fish were in the low to middle range of those recorded in biota around the world (Table 1), e.g., in the Pearl River Estuary of South China (Ip et al., 2005), Gulf and Gulf of Omen (de Mora et al., 2004), Catalonia of Spain (Falco´ et al., 2006), New Jersey of the United States (Burger and Gochfeld, 2005) and the coastal waters of Victoria, Australia (Fabris et al., 2006). Compared to historical data for wild fish acquired during 1996–1997 (Qiu et al., 2005a), Pb concentrations obtained in the present study were elevated, Hg concentrations were generally unchanged and Cu, Zn, Cd and As concentrations were lower (Table 1). There were significant correlations between the concentrations of Cu, Zn, Cd and Cr in pompano and between the concentrations of Cu, Zn and As in snapper (Table S3). Significant relationships were also observed between the concentrations of Cu, Zn and As and lipid contents in both pompano and snapper, indicating that lipid content may be an important factor regulating the bioaccumulation of these metals in farmed fish. However, negative correlations were found between Hg concentrations and lipid contents in the farmed fish, which is contrary to the fact that approximately 90% of Hg in fish tissue exist in lipophilic methylmercury (Burger and Gochfeld, 2005). The mechanics are unclear presently and need to be further studied in the future.

3.3. Factors influencing bioaccumulation Metal concentration in an organism is controlled by the balance between uptake and elimination (Wang and Rainbow, 2008). Accumulation of metals in the tissues of fish depends primarily on ambient water concentrations, levels in prey or commercial feed, and chemical uptake and elimination kinetics. Other factors, such as chemical speciation/bioavailability as well as fish growth cycle, age and trophic position, also can influence the extent of metal accumulation in fish (Kelly et al., 2008). Both laboratory and field investigations have confirmed that food can be a major source of trace metals bioaccumulated in fish (Spry et al., 1988; Mount et al., 1994), and fish feed is the major food for farmed fish cultured in the farming regions under investigation. In the present study, the average concentrations of Cu, Pb, Zn, Cd, Cr, Hg and As in fish feed were 2.7, 3.3, 80.2, 0.1, 1.2, 0.1 and 2.4 mg/g dry wt, respectively, which were slightly higher than the average concentrations of the target metals except Hg in the farmed fish. Food quality/quantity may significantly affect the dietary assimilation and ingestion rate of fish. For marine fish, dietary uptake (highly associated with trophic transfer) is the predominant pathway by which metals are

289

accumulated, primarily because of the very low dissolved uptake rate of metals (Xu and Wang, 2002; Wang and Rainbow, 2008). To somewhat quantitatively examine the sources of trace metals in farmed fish, the metal bioaccumulation model described in Eqs. (1) and (2) was utilized to analyze the data obtained in the present study. The values of the biokinetic parameters (ku, kew, kef and AE) derived from bioaccumulation experiments of Zn and Cd in snapper (Lutjanus argentimaculatus), i.e. the same fish family, were adopted (Xu and Wang, 2002). Combined with the data from the present study and assuming that the steady state was reached, the amounts of Zn and Cd accumulated in snapper (L. malabaricus), as well as the fractions derived from dietary uptake, were estimated (Table 2). The estimated levels of Zn (45.9 mg/ g dry wt) and Cd (0.020 mg/g dry wt) were comparable to the average measured levels in whole snapper fish (Zn: 36.4 mg/ g dry wt; Cd: 0.022 mg/g dry wt). In addition, dietary uptake predominated the accumulation of Zn and Cd in snapper, accounting for 99.9% and 98.2%, respectively, of the total inputs. A previous study (Mathews and Fisher, 2009) also reported that dietary intake accounted for 460%, often 490%, of the total body burdens of Cd and Zn in fish (teleost Psetta maxima and elasmobranch Scyliorhinus canicula). This result confirms the above observation that the trace metals concentrations in farmed fish were not significantly different between Daya Bay and Hailing Bay though there existed some differences for the trace metal concentrations in seawater and sediment, because the same fish feed was used in the two bases. It is well known that metals may be bioaccumulated in fish tissues (van der Oost et al., 2003). The magnitude of bioaccumulation is a function of age, species and trophic transfer (Spry and Wiener, 1991). Within the same species, the concentrations of metals may vary with the age and body weight. In the present study, the concentrations of Pb, Zn, Cd, Cr and As in snapper and those of Pb, Cd and As in pompano decreased with increase in the fish body weight (as a proxy of age), whereas the concentrations of Cu in snapper and those of Cu, Zn and Cr in pompano remained largely unchanged, and those of Hg in both fish species increased with increase in the body weight (Fig. 4). Similarly, the concentrations of Hg in finfish (Pagruss auratus, Platycephalus bassenssis and Neoplatycephalus richardsoni) from coastal waters of Victoria in Australia increased with increase in fish size (Fabris et al., 2006). Previous studies also demonstrated positive correlations between the concentrations of persistent halogenated compounds and lipid contents in various biota (Kiriluk et al., 1995). As shown in Fig. 5, positive correlations were generally observed between the concentrations of trace metals (Cu, Pb, Zn, Cd, Cr and As) and lipid contents in both fish species from Daya Bay and Hailing Bay, whereas negative correlations were found between the concentrations of Hg and lipid contents in both fish species. In addition, lipid contents also increased with decrease in the fish body weight in both fish species (Fig. 5). Fish age is generally proportional to the fish body weight for same fish species in the similar cultural environment. As the ‘‘growth dilution effect’’ suggests, bigger fish may contain lower concentrations of bioaccumulated trace metals compared to smaller ones. Therefore, there existed negative correlations between the concentrations of most target metals and fish body weights in the present study.

3.4. Risk assessment Marine sediment is often regarded as the ultimate sink for many pollutants including trace metals. Trace metals in sediment may pose hazard to aquatic biota upon release into overlaying water, or through direct digestion by bottom feeders. Many metals are biologically essential elements, but they also have potential toxicity to biota if their concentrations surpass certain thresholds.

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Table 2 The average biokinetic parameters for metal bioaccumulation, metal concentrations in water and diet and the estimated metal concentrations in fish and the fractions of metals derived from the dietary uptake.

n

Metal

ku (mL/g d)

kew (/d)

kef (/d)

AEn

IR (g/g d)

g (g/g d)

Cw ( mg/L)

Cf (mg/g dw)

Css (mg/g dw)

f (%)

Zn Cd

0.21 0.08

0.015 0.025

0.015 0.047

0.40 0.20

0.05 0.05

0.02 0.02

10.4 0.20

80.2 0.13

45.9 0.020

99.9 98.2

The biokinetic parameters (ku, kew, kef and AE) were derived from Xu and Wang (2002).

Fig. 4. Relationship between the residual levels of trace metals and body weights in farmed fish from Daya Bay and Hailing Bay (n¼ 69 of pompano and n¼ 64 of snapper). Circles and squares represent pompano and snapper, respectively; solid and dashed lines represent linear regressions for pompano and snapper, respectively. Confidence levels are 95%.

At low concentrations, Zn and Cu are essential for growth of organisms, whereas Cd and Pb are non-essential elements and are toxic even at low levels. In the present study, the guidelines (Table S4) for the estimated seawater and sediment safe levels of trace metals recommended by the National Oceanic and Atmospheric Administration (NOAA,

2009) of the United States were used to examine the potential ecological risk of trace metals in seawater and sediment. The concentrations of all the target metals in seawater of Daya Bay and Hailing Bay were below the chronic levels. In addition, the concentrations of Pb, Cu, Cr and Hg in 13, three, one and one out of 13 sediment samples exceeded the Effects Range-Low (ERL)

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291

Fig. 5. Relationship between the residue levels of trace metals and lipid contents in farmed fish from Daya Bay and Hailing Bay (n¼69 of pompano and n¼ 64 of snapper). Circles and squares represent pompano and snapper, respectively; solid and dashed lines represent linear regressions for pompano and snapper, respectively. Confidence levels are 95%.

values, respectively. The concentrations of Pb in 12 out of 13 sediment samples exceeded the Effects Range-Median values, while concentrations of other target metals were below the ERM values. These assessments suggested that Pb in sediment probably poses potential risk to the ecological system of Daya Bay and Hailing Bay, whereas other trace metals are mostly not hazardous to aquatic organisms. The assessment standards for trace metals (Cu, Pb, Zn, Cd, Cr, Hg and As) in fish (Table 1) recommended by the Food and Agricultural Organization (FAO) (Burger and Gochfeld, 2005) were used to examine whether farmed fish investigated in the present study may pose potential health risk to humans via fish consumption, though the amount of fish consumption is quite different depending on the food habits of each country or each ethnic group. The residual levels of Pb in six out of 69 pompano samples and five out of 64 snapper samples were higher than the standards; the residual level of

Cr in one out of 64 snapper samples was also higher than the standard. This indicates that farmed fish from the culturing bases of Daya and Hailing Bays generally pose no adverse health effects to fishconsuming humans in terms of the target trace metals except Pb (the concentrations of Pb in 8% of the fish samples exceeded the standard). As far as mercury is concerned, the levels of Hg in muscle of pompano and snapper were in the ranges of 0.02–0.14 (mean: 0.0670.03) and 0.01–0.16 (mean: 0.0670.04) mg/g wet wt, respectively. These levels were all below the human consumption guideline level of 0.5 mg/g wet wt for total mercury in commercial marine and freshwater fish established by Health Canada (Kelly et al., 2008) and a current ‘‘action level’’ for methylmercury in commercially sold fish of 1 mg/g dry wt recommended by the US Food and Drug Administration (Tsuchiya et al., 2008), suggesting that levels of mercury in farmed fish from two typical fish farming regions of South China are deemed safe for human consumption. Although

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methylmercury was not measured in the present study, many studies have shown that almost all of the mercury in fish tissue is methylmercury; therefore, 90% is a reasonable approximation of this proportion, which does vary somewhat among fish types and laboratories (Burger and Gochfeld, 2005). It should be pointed out that with rapid economic growth, concerns about fish pollution by metals are also increasing around the world. Very often, laws and regulations on environmental protection are not rigorously enforced in developing countries (Ni and Zeng, 2009), resulting in direct discharge of untreated industrial sewage into local water systems from time to time and unexpected damages to local ecosystems. For example, untreated sewage from a copper mine leaked into Ting River of Fujian Province of China in 2010, leading to more than 1890 tons of dead fish and toxicosis with a loss of approximately 1 billion yuan. Apparently, caution should be exercised in consuming fish which are cultured in potential metal polluted waters.

4. Conclusions The concentrations of trace metals (Cu, Zn, Cd, Cr, Hg and As) in various environmental compartments (seawater, sediment, fish and feed) of Daya Bay and Hailing Bay in South China were in the middle ranges of the global values, while Pb concentrations in sediment and fish were relatively high. The average concentrations of trace metals in feed were higher than in fish, suggesting that there was no obvious biomagnification of trace metals in farmed fish. In addition, the concentrations of Pb, Zn, Cd and As but not Hg increased with fish body weights. The concentrations of the target metals (except Hg) were also found to positively relate to lipid contents in farmed fish. Finally, levels of Pb in sediment and farmed fish were high enough to pose potential ecological and human health risk.

Acknowledgments This research was financially supported by the Joint Fund of the National Natural Science Foundation of China and the Government of Guangdong Province (No. U0633005) and the National Natural Science Foundation of China (Nos. 40573061 and 40821003). We thank Dr. Gan Zhang with the Guangzhou Institute of Geochemistry for his useful comments on the manuscript.

Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at doi:10.1016/j.ecoenv.2010.10.008.

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