Trace elements in fish from Taihu Lake, China: Levels, associated risks, and trophic transfer

Ecotoxicology and Environmental Safety 90 (2013) 89–97

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Trace elements in fish from Taihu Lake, China: Levels, associated risks, and trophic transfer Ying Hao b, Liang Chen a, Xiaolan Zhang a, Dongping Zhang a, Xinyu Zhang a, Yingxin Yu a,n, Jiamo Fu a,c a

Institute of Environmental Pollution and Health, School of Environmental and Chemical Engineering, Shanghai University, Shanghai 200444, PR China Department of Environmental Science and Engineering, School of Environmental and Chemical Engineering, Shanghai University, Shanghai 200444, PR China c State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, PR China b

a r t i c l e i n f o

abstract

Article history: Received 13 September 2012 Received in revised form 13 December 2012 Accepted 17 December 2012 Available online 12 January 2013

Concentrations of eight trace elements [iron (Fe), manganese (Mn), zinc (Zn), chromium (Cr), mercury (Hg), cadmium (Cd), lead (Pb), and arsenic (As)] were measured in a total of 198 samples covering 24 fish species collected from Taihu Lake, China, in September 2009. The trace elements were detected in all samples, and the total mean concentrations ranged from 18.2 to 215.8 mg/g dw (dry weight). The concentrations of the trace elements followed the sequence of Zn4 Fe 4Mn 4 Cr 4 As 4Hg 4 Pb 4Cd. The measured trace element concentrations in fish from Taihu Lake were similar to or lower than the reported values in fish around the world. The metal pollution index was used to compare the total trace element accumulation levels among various species. Toxabramis swinhonis (1.606) accumulated the highest level of the total trace elements, and Saurogobio dabryi (0.315) contained the lowest. The concentrations of human non-essential trace elements (Hg, Cd, Pb, and As) were lower than the allowable maximum levels in fish in China and the European Union. The relationships between the trace element concentrations and the d15N values of fish species were used to investigate the trophic transfer potential of the trace elements. Of the trace elements, Hg might be biomagnified through the food chain in Taihu Lake if the significant level of p-value was set at 0.1. No biomagnification and biodilution were observed for other trace elements. & 2012 Elsevier Inc. All rights reserved.

Keywords: Biomagnification Fish Taihu Lake Trace element Trophic transfer

1. Introduction Environmental pollution caused by trace elements has aroused widespread concern around the world (Cui et al., 2011). In biochemistry, trace elements generally can be classified as essential trace elements, such as zinc (Zn), iron (Fe), manganese (Mn), and chromium (Cr), and non-essential trace elements, such as mercury (Hg), arsenic (As), cadmium (Cd), and lead (Pb) (Fraga, 2005). Exposure to non-essential trace elements, even at low concentrations, over a long time period is harmful to organisms (Thomas et al., 2009; Zheng et al., 2011). Essential trace elements are necessary because they form an integral part of enzymes that are involved in metabolic or biochemical processes in organisms. The primary role of such elements is serving as catalysts, and only trace amounts are needed for cellular functions. Excess exposure

Abbreviations: AFS, atomic fluorescence spectrometry; GFAAS, Graphite furnace atomic absorption spectrometry; ICP-AES, inductively coupled plasma-atomic emission spectrometry; MDL, method detection limit; MeHg, methylmercury; MPI, metal pollution index; THg, total mercury n Corresponding author. Fax: þ86 21 6613 6928. E-mail address: [email protected] (Y. Yu). 0147-6513/$ - see front matter & 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ecoenv.2012.12.012

of organisms to such elements may result in toxic effects (Gopalani et al., 2007). Fish is an important part of the human diet because of its high nutritional quality (Sioen et al., 2007). However, non-essential trace elements in the edible tissues of fish have been detected due to the bioaccumulation in organisms and the highly persistent and non-biodegradable properties of these elements (Burger and Gochfeld, 2005; Zhang and Wang, 2012). In a freshwater system, fish is usually among the topper consumers. Some of these elements (such as Hg) have been reported to be biomagnified via food chains both in marine and freshwater systems (Campbell et al., 2005; Nfon et al., 2009; Wang et al., 2012). If the trace element levels are elevated enough, they can pose potential health risks to humans via fish consumption. There are very different conclusions on trophic transfer behaviors of these elements, such as Cd (Dietz et al., 2000; Nfon et al., 2009). Dietz et al. (2000) found that the concentration of Cd increased towards higher trophic levels, whereas Nfon et al. (2009) reported that the concentration of Cd showed statistically significant decreases with increased trophic levels and they concluded that Cd was tropically biodiluted in Baltic food chain. Many factors, such as environment conditions, contaminant levels, the length of food chains, and the physiochemical properties of contaminants, can

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influence the trophic transfer behavior. The trophic transfer behavior of trace elements in aquatic biota is complex and needs more field research. Taihu Lake, the second largest freshwater lake in China, is located in the Yangtze delta plain on the border of the Jiangsu and Zhejiang provinces of eastern China. It plays an important role in flood control, water supply, and fisheries (Yunkai et al., 2009). Rapid industrial and economic development has occurred around the lake since the 1980s. Yuan et al. (2011) reported that Taihu Lake was moderately polluted by trace elements based on their study of sediments. Fish is the main aquatic product of Taihu Lake, and trace element pollution will affect their quality (Chi et al., 2007). Wang et al. (2012) reported that the MeHg and total mercury (THg) showed obvious biomagnification along the food web in the lake, although the bioaccumulation factor of MeHg was relatively low compared to that of other aquatic ecosystems. T. Yu et al. (2012) observed that some heavy metal concentrations tended to be higher in predatory fish such as C. ectenes and E. ilishaeformis than in herbivorous fish from Taihu Lake. However, in the two studies (Wang et al., 2012; T. Yu et al., 2012), the authors did not quantitatively investigate the trophic transfer of the heavy metals except for Hg. Trace elements may accumulate in fish and be biomagnified to toxic levels, thus raising public health concern. The trophic transfer of trace elements could represent the increase or decrease of human exposure to the elements, as a function of fish trophic levels, due to fish consumption. Therefore, knowledge of trophic transfer behavior of trace elements in fish from the lake is important, both with respect to aquatic ecosystems and human consumption. In September 2009, as a part of the program of the Water Environmental Quality Evolution and Water Quality Criteria in Lakes (the National Basic Research Program of China), we collected a total of 198 samples of 24 fish species from Taihu Lake. Previously, we measured the concentrations of polybrominated diphenyl ethers, polychlorinated biphenyl, organochlorine pesticides, polycyclic aromatic hydrocarbons, and synthetic musks in the samples and investigated the trophic transfer behaviors of the organic pollutants along the food chain in the lake (Y.X. Yu et al., 2012; Wang et al., 2012; Zhang et al., 2012). In the present study, the main objectives were (1) to measure the concentrations of eight trace elements, including Fe, Mn, Zn, Cr, Hg (as total mercury, THg), As, Cd, and Pb in the fish species collected; (2) to estimate the associated risks of the trace elements; (3) to investigate the trophic transfer behavior of the trace elements through the food chain.

2. Materials and methods 2.1. Sampling and sample preparation Fish normally used for consumption were purchased from fishermen or caught for us by commercial fishermen from Taihu Lake in September 2009. They were the same samples used in our previous study (Y.X. Yu et al., 2012). In the present study, two Coilia ectenes taihuensis samples were not used, and a total of 198 samples including 24 fish species were analyzed. The species included three types of herbivorous fish: Ctenopharyngodon idellus, Megalobrama amblycephala, and Parabramis pekinensis; ten types of omnivorous fish: Carassius carassius, Cyprinus carpio, Hypophthalmichthys molitrix, Hemiculter leucisculus, Acheilognathus macropterus, Hypophthalmichthys nobilis, Saurogobio dabryi, Hyporhamphus intermedius, Pelteobagrus fulvidraco, and Toxabramis swinhonis; and eleven types of carnivorous fish: Coilia ectenes taihuensis, Hemibarbus maculates, Cultrichthys erythropterus, Culter alburnus, Protosalanx hyalocranius, Neosalanx taihuensis Chen, Chanodichthys mongolicus, Chanodichthys dabryi, Paracanthobrama guichenoti, Silurus asotus, and Acheilognathus rhombeus. The collected fish were stored in ice and transported to the laboratory immediately. After the length and weight were recorded, they were dissected, homogenized and lyophilized, ground into powder, and stored in clean amber glass containers at  18 1C until use. For more detailed sample information, we have listed them in Table S1 (Supplementary Material).

2.2. Analyses of trace elements A wet digestion method with some modifications was used (Turkmen and Ciminli, 2007) to measure the concentrations of Cd, Pb, Fe, Mn, and Zn. Briefly, for each analysis, 2 g of dry sample powder was added to a 100 mL Erlenmeyer flask, 30 mL of concentrated HNO3 was added slowly, and the sample was soaked overnight. Thereafter, 4 mL of 30% H2O2 was added to the flask and the sample was soaked again for 4–6 h. Then, the flask containing the sample solution was heated at 250 1C to evaporate the solution slowly to near dryness. Next, 10 mL of concentrated HNO3 was added to the residue and the solution was evaporated slowly to near dryness again. The digestion process using HNO3 was repeated until all organic materials in the sample were completely digested. After cooling down, the residue was transferred to a 25 mL volumetric flask containing deionized water filtered through a 0.45 mm nitrocellulose membrane filter. The resulting sample solution was stored at 4 1C until analysis. For the measurement of Hg, As, and Cr concentrations, the samples of a given fish species were pooled, and the same amount of sample was used for each species (corresponding to 24 samples for 24 fish species). A microwave digestion method was used (Cui et al., 2011). Briefly, 0.2 g of dry sample was digested using a microwave system with 4 mL of 65% HNO3 and 3 mL of 30% H2O2 in a Teflonlined vessel under controlled pressure. The sample was heated to 70 1C and held for 5 min, to 100 1C and held for 5 min and to 120 1C and held for 5 min. All digested samples were cooled down to room temperature. The samples then were filtered through 0.45 mm nitrocellulose membrane filters and diluted to 25 mL in volumetric flasks with deionized water. The sample solutions were stored at 4 1C until analysis. Quantifications of Fe, Mn, and Zn concentrations were performed using an inductively coupled plasma-atomic emission spectrometry (ICP-AES) (LEEMAN Prodigy, USA). The concentrations of Pb, Cd, and Cr were determined using Graphite furnace atomic absorption spectrometry (GFAAS) (ZEEnit600/650, Germany), and Hg and As concentrations were measured using atomic fluorescence spectrometry (AFS) (AFS-9130, USA).

2.3. Calculations To estimate the accumulation levels of the trace elements in different fish species, the metal pollution index (MPI) was used to compare the total trace element accumulation levels in various fish species. The MPI value can be calculated using the following equation (Sharma et al., 2008): MPI ¼ C 1  C 2      C f


1=f

,

where Cf is the concentration of an element f in the sample.

2.4. Quality assurance and quality control A procedural blank was run for each batch of 12 samples to monitor any interference during the sample treatment. The values obtained from the blanks were subtracted from the sample values. For every 24 samples, one was chosen randomly and re-run to examine the reproducibility of the results. The accuracy of the method was tested using trace element-spiked samples. The recovery rates of the spiked trace elements ranged from 92.6% to 121.3%, with a mean of (105.77 8.1)%. The mean relative standard deviations of replicate samples were generally less than 20%. The method detection limits (MDLs) for the trace elements were as follows: Hg 0.000005 mg/mL, As 0.00005 mg/mL, Cd 0.000015 mg/mL, Pb 0.0009 mg/mL, Cr 0.0001 mg/mL, Fe 0.08 mg/mL, Mn 0.016 mg/mL, and Zn 0.02 mg/mL. To prevent contamination of the samples, all laboratory-wares were soaked in 5%–10% HNO3 solution for at least 48 h and rinsed five times with water and then five times with deionized water prior to use.

2.5. Statistical analysis The statistical analyses of data were carried out using SPSS 11.5 for Windows. When the amount of an element was lower than its MDL, its concentration was reported as one-half of its MDL; when it was not detected, the concentration was reported as zero. The differences of concentrations of the trace elements among the herbivorous, omnivorous, and carnivorous fish were analyzed using Kruskal– Wallis test. The relationship between the trace element concentrations and the d15N values of fish species were analyzed using linear regression. Statistically significance level was set at p ¼ 0.05.

Table 1 Concentrations of trace elements (mg/g dw) in fish from Taihu Lake, China. Species

4 (4) 6 (8) 4 (5)

Hgb

Asb

Crb

Cd

Pb

Fe

Mn

Mean

Median

Range

Mean

Median

Range

Mean

Median

Range

Mean

48.1 39.8 62.5

0.075 0.040 0.131

0.141 0.259 0.144

0.495 0.308 0.351

0.005 0.018 0.022

0.003 0.013 0.008

MDL–0.013 0.006–0.048 MDL–0.069

0.036 0.175 0.038

0.036 0.166 0.036

ND-MDL 0.137–218 ND–0.081

14.95 12.3 27.6

2.64 12.5 31.3

MDL–23.2 8.68–17.6 MDL–44.0

1.94 1.36 2.27

Zn Median

Range

1.78 1.19 2.17

1.26–2.94 0.94–2.34 MDL–4.42

Mean

30.5 25.2 31.9

Median

Range

31.8 24.1 37.6

22.4–35.9 23.5–29.8 10.1–42.3

Omnivorous fish C. carassius C. carpio H. molitrix H. leucisculus A. macropterus H. nobilis S. dabryi H. intermedius P. fulvidraco T. swinhonis

18 11 12 6 8 10 2 7 12 4

(54) (12) (12) (44) (4100) (10) (10) (4200) (88) (4100)

152.5 87.9 42.9 87.4 120.2 32.2 18.2 215.8 76.0 203.5

0.102 0.118 0.073 0.166 0.077 0.092 0.042 0.088 0.102 0.304

0.102 0.228 0.166 0.126 0.368 0.135 0.126 0.944 0.198 0.258

0.286 0.324 0.400 0.375 0.285 0.320 0.299 0.363 0.334 0.329

0.017 0.014 0.011 0.039 0.03 0.02 0.021 0.109 0.014 0.151

0.008 0.01 0.005 0.039 0.034 0.019 0.021 0.107 0.014 0.15

MDL–0.057 MDL–0.058 MDL–0.039 0.028–0.045 0.011–0.041 0.008–0.045 0.013–0.029 0.095–0.137 0.006–0.023 0.149–0.152

0.036 0.031 0.047 0.046 0.087 0.043 0.061 0.242 0.045 0.153

0.036 0.036 0.036 0.036 0.093 0.036 0.061 0.239 0.036 0.144

ND-MDL ND–0.123 ND–0.141 MDL–0.098 MDL–0.104 MDL–0.083 MDL–0.086 0.224–0.265 ND–0.104 0.073–0.250

21.9 24.1 15.9 9.83 6.49 8.97 1.86 29.7 24.5 39.6

8.09 9.75 4.91 39.3 34.0 18.7 21.3 107.4 13.9 150.4

MDL–40.7 14.2–38.5 MDL–28.9 MDL–16.8 MDL–10.5 MDL–12.3 ND–3.72 25.2–36.8 14.4–40.6 28.7–49.0

1.48 2.50 1.95 2.62 10.2 1.14 1.82 8.63 1.43 12.5

1.47 2.01 2.06 2.44 8.63 0.946 1.82 8.6 1.33 12.0

0.943–2.69 1.23–4.35 1.04–2.88 1.86–3.86 7.2–16.7 0.515–2.75 1.48–2.51 7.80–9.58 MDL–5.42 10.9–15.18

128.5 60.6 24.4 74.3 102.7 21.5 14.0 175.7 49.3 150.2

130.0 65.0 27.7 71.4 101.7 21.1 14.0 175.7 46.3 148.8

77.7–212.0 31.7–70.6 12.1–33.7 62.9–88.4 93.9–121.1 17.2–25.1 12.6–15.5 168.9–183.4 40.9–72.2 138.9–164.4

Carnivorous fish C. taihuensis H. maculates C. erythropterus C. alburnus P. hyalocranius N. taihuensis Chen C. mongolicus C. dabryi P. guichenoti S. asotus A. rhombeus

27 9 14 11 9 9 7 3 2 2 1

(4100) (25) (68) (20) (4200) (4200) (9) (34) (6) (2) (35)

95.4 64.5 57.7 46.5 104.6 84.8 41.4 139.8 56.3 60.9 131.0

0.071 0.071 0.143 0.186 0.055 0.037 0.075 0.069 0.067 0.521 0.049

0.120 0.112 0.126 0.135 0.342 0.569 0.846 0.289 0.248 0.040 0.198

0.518 0.358 0.288 0.330 0.373 0.430 0.340 0.370 0.331 0.315 0.439

0.034 0.024 0.013 0.003 0.063 0.038 0.013 0.028 0.014 0.015 0.016

0.033 0.027 0.012 0.002 0.062 0.038 0.012 0.026 0.014 0.015 –

0.009–0.069 0.003–0.039 MDL–0.030 MDL–0.005 0.040–0.080 0.028–0.046 0.009–0.019 0.022–0.032 0.008–0.019 ND–MDL –

0.127 0.044 0.113 0.032 0.04 0.083 0.077 0.128 0.036 0.132 0.131

0.11 0.036 0.105 0.036 0.036 0.102 0.036 0.124 0.036 0.132 –

0.035–0.310 ND–0.111 MDL–0.323 ND–0.072 MDL–0.072 MDL–0.119 MDL–0.161 0.118–0.145 MDL MDL–0.228 –

16.4 27.0 12.9 12.8 1.93 7.52 11.4 53.1 16.8 27.7 11.9

32.9 26.8 12.2 1.58 62.1 37.9 9.13 26.1 13.5 14.8 –

MDL–92.2 22.8–30.3 10.2–18.0 7.55–21.0 ND–9.9 ND–16.0 MDL–19.4 46.9–64.7 16.6–17.1 MDL–51.7 –

6.92 2.41 1.92 1.43 12.1 9.53 1.53 7.45 2.65 1.11 17.8

4.52 2.05 1.17 0.967 11.8 7.81 1.63 7.95 2.65 1.11 –

2.67–17.1 1.76–4.14 0.954–7.17 MDL–3.07 7.55–17.1 5.12–12.7 0.798–1.76 6.54–8.76 2.42–2.89 1.09–1.13 –

71.2 34.5 42.2 31.6 89.7 66.6 27.2 78.4 36.1 31.1 100.4

41.9 32.1 32.6 31.4 91.8 69.2 27.0 80.3 36.1 31.1 –

24.7–183.0 28.6–45.0 27.4–93.0 27.6–36.2 59.6–104.6 28.9–83.0 24.7–30.7 73.3–86.6 32.7–39.6 21.4–40.6 –

Y. Hao et al. / Ecotoxicology and Environmental Safety 90 (2013) 89–97

Herbivorous fish C. idellus M. amblycephala P. pekinensis

Totala

n

n is the number of the samples, the number in bracket is the individual samples for each species, and the sample was pooled according to fish size. ND: not detected; MDL: method detection limit. a b

Total mean concentrations of the eight trace elements. the samples of a given fish species were pooled, and the same amount of sample was used for each species (corresponding to 24 samples for 24 fish species).

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3. Results

4. Discussion

3.1. Concentrations of trace elements

4.1. Accumulation levels of trace elements in fish considering feeding habits

Table 1 shows the concentrations of the trace elements in the fish species. Because of the investigation of the trophic transfer behavior of these elements, the element concentrations based on dry weight are listed. For comparison purpose, when the wet weight concentration of a trace element was available in the literature, its concentration was given as dry weight based on a wet/dry weight conversion factor of 4 if there was no special explanation (Onsanit et al., 2010). The total mean concentrations of the eight trace elements ranged from 18.2 to 215.8 mg/g dw in the fish species investigated (Table 1). The highest total mean concentration was observed in H. intermedius, followed by T. swinhonis, and S. dabryi had the lowest total concentration. The concentrations of essential trace elements (Zn, Fe, Mn, and Cr) were higher than those of nonessential trace elements (Hg, As, Cd, and Pb), and the sequence of Zn4Fe 4Mn4Cr 4As4Hg 4Pb4Cd was observed. The essential trace elements were generally the most abundant in the samples. Of the eight trace elements analyzed, Zn was the predominant one. The highest mean concentration of Zn was observed in H. intermedius (175.7 mg/g dw) and the lowest found in S. dabryi (14.0 mg/g dw). The contribution of Zn accounted for 51.0%–85.8% of the total trace element concentrations in the species tested. Fe was the second most abundant in the samples. The mean concentrations of Fe ranged from 1.86 (S. dabryi) to 53.1 mg/g dw (C. dabryi), with a mean value of 18.2 mg/g dw. Manganese was detected in all samples, and its mean concentrations ranged from 1.1 (S. asotuss) to 17.8 mg/g dw (A. rhombeus). Of the essential trace elements, Cr was the lowest one. Its mean concentrations ranged from 0.285 (A. macropterus) to 0.518 (C. taihuensis) mg/g dw, which were approximately 1–2 order of magnitude lower than those other essential trace elements. Compared with the essential trace elements, concentrations of the non-essential trace elements were lower. Of the four nonessential trace elements, As was the predominant one, followed by Hg. The concentrations of As ranged between 0.04 (S. asotus) and 0.944 (H. intermedius) mg/g dw. Mercury contamination in lakes, reservoirs, and other water bodies is a worldwide problem. The mean concentrations of THg in the fish species tested herein ranged from 0.037 (N. taihuensis Chen) to 0.521 (S. asotus.) mg/g dw. For Pb, the concentrations were between 0.031 (C. carpio) and 0.242 (H. intermedius) mg/g. Regarded as one of the most toxic metals to aquatic organisms, Cd was found at the lowest concentrations with values ranging between 0.003 (C. alburnus) and 0.151 (T. swinhonis) mg/g dw; it accounted for only 0.01%–0.12% of the total, with a mean value of less than 0.04%.

There were no significant differences (p ¼0.954) in Fe concentrations among the herbivorous (mean: 18.3 mg/g dw), omnivorous (mean: 18.3 mg/g dw), and carnivorous (mean: 18.1 mg/g dw) fish as analyzed using Kruskal–Wallis test. Similar results were observed for other essential trace elements (p ¼0.252–0.503) among the three type of fish species, although there were obvious differences in the mean concentrations of Zn and Mn. The mean concentrations of Zn in herbivorous, omnivorous, and carnivorous fish were 29.2, 80.1, and 55.4 mg/g dw, and those of Mn were 1.86, 4.43, and 5.90 mg/g dw, respectively. The large deviations of these trace element concentrations in omnivorous and carnivorous fish might be one of the reasons for the observation. For the non-essential trace elements, As concentrations in the species on the basis of species increased in the following order: herbivorous fish (0.181 mg/g dw) oomnivorous fish (0.265 mg/ g dw) ocarnivorous fish (0.275 mg/g dw). However, the differences in the As concentrations among the three types of fish species (p ¼0.990) were not statistically significant as analyzed using Kruskal–Wallis test, although the above sequence suggested an increase in the As concentration with trophic level. This result was similar to that for Mn. Similar result was also observed for Hg, whose concentrations increased from herbivorous fish (0.082 mg/g dw) to omnivorous fish (0.116 mg/g dw) to carnivorous fish (0.122 mg/g dw), suggesting that biomagnification of Hg might occur through the food chain. The trophic transfer behavior of Hg through the food chain might be mainly attributed to methylmercury (MeHg). The proportion of MeHg in fish from Taihu Lake ranged from 20% to 97%, with a mean value of 62717% (Wang et al., 2012). It is generally believed that MeHg constitutes about 90% of the total mercury in fish muscles (Campbell et al., 2008). For other two non-essential trace elements, there were also no significant differences (p ¼0.577– 0.861) in their concentrations among the herbivorous, omnivorous, and carnivorous fish. To estimate the accumulation levels of the trace elements in different fish species, the MPI was calculated to compare the total trace element accumulation levels in various fish species (Sharma et al., 2008). The results showed that T. swinhonis (1.606) accumulated the highest total trace elements and S. dabryi (0.315) contained the lowest (Fig. 1). Considering the feeding habits of the species, the MPI values in the species tested followed the order of omnivorous fish (mean: 0.744), carnivorous fish (mean: 0.649), and herbivorous fish (mean: 0.496). This pattern

1.8

3.2. Trophic transfer of trace elements

Herbivious fish

Omnivious fish

Carnivious fish

1.6 1.4

MPI

1.2 1.0 0.8 0.6 0.4 0.2 .a C m .i b d P. lyce ellu pe ph s ki al ne a ns is C. ca ra s s C. iu c s H H.m arp . A leu oli io . m ci tr ac scu ix ro lu H pter s .n u H S obi s .in . d li te a s P. rm bry fu edi i T. lv us sw idr in aco ho ni C. s ta ih H C. .m ue er a ns yt cu is hr la o t C p es N P. h .al teru . t y bu s ai alo rn hu c u s C. ens rani m is C us on h go en P. C.sd licu gu a s ic bry he i A S.a noti . r so ho tu m s be us

0.0

M

The trophic transfer potentials of the trace elements were estimated using relationships between the trace element concentrations and the d15N values of the fish species. Generally, a significant positive correlation between them indicates that the substance is biomagnified through a food chain, whereas a negative correlation suggests that biodilution has occurred. In the present study, the relationships between the concentrations of the trace elements (Hg, As, Cd, Pb, Cr, Fe, Mn, and Zn) and the d15N values of the fish species were investigated. Although there were a positive slope for THg (p ¼0.128) and negative slopes for other seven trace elements (p ¼0.269–0.96), there were no statistical significance.

Fig. 1. Metal pollution indices of the total trace elements.

Y. Hao et al. / Ecotoxicology and Environmental Safety 90 (2013) 89–97

might be a result of different ecological needs, metabolisms, and feeding patterns. 4.2. Comparison of trace elements in fish from Taihu Lake with other studies There have been several studies on trace element concentrations in fish conducted in the same lake. In the present study, Zn was the most abundant element. Our results were consistent with previous reports in which the Zn concentrations ranged between 16 and 130 mg/g dw in fish from the same lake (Chi et al., 2007; T. Yu et al., 2012; Yang et al., 2009). The high levels of Zn are likely attributed to the high Zn levels in the local habitat, as industrial discharge into the lake has occurred during the past three decades because of the rapid economic and social development around the lake (T. Yu et al., 2012). For Fe, our data were comparable to those in mandarin fish (6.7–16.8 mg/g dw) from South Taihu Lake (Cheng et al., 2010). Similar results were observed for Cr. Chi et al. (2007) and T. Yu et al. (2012) observed that Cr concentrations ranged from non-detected to 0.387 mg/g dw, and from 0.24 to 0.72 mg/g dw, respectively. The concentrations of Mn in P. hyalocranius in the present study (7.6–17.1 mg/g dw) were comparable to those (7.3–11.6 mg/g dw) in the same species in the study by Yang et al. (2009). However, its concentration in mandarin fish in our study (mean: 4.78 mg/g dw) was much higher than the values (0.74–1.96 mg/g dw) in the same species reported in a previous study (Cheng et al., 2010). One possible reason for the different results was the sampling sites. In the study by Cheng et al. (2010), the samples were collected from Southwestern Taihu Lake, which generally is regarded as having relatively better water quality compared to other parts of the lake. For the non-essential trace elements, our data were comparable with the previous results in fish from the same lake. The mean concentration of As in P. hyalocranius was 0.499 mg/g dw as reported by Yang et al. (2009). For Hg, our data was comparable to the results (0.12–0.56 mg/g dw) in fish collected from the same lake in 2009, except for the large largemouth bass, which had a mean concentration of 1.24 mg/g dw as reported by Wang et al. (2012). The concentrations of Pb were 0.177–0.287 and 0.32–1.72 mg/g dw in fish from Taihu Lake in the studies conducted by Chi et al. (2007) and T. Yu et al. (2012), respectively. The concentrations of Cd were 0.003–0.021 mg/g dw as measured in the mid-2000s (Chi et al., 2007), and 0.04–0.28 mg/g dw in another study conducted by T. Yu et al. (2012). These results indicated that the non-essential trace element concentrations in fish from Taihu Lake kept unchanged in recent years. There are many studies monitoring the contamination levels of trace elements in fish from other water bodies. To explore the contamination status of fish from Taihu Lake, we listed some data published in recent years from other water bodies in Asia, Africa, Europe, and America (Table 2). Compared our data with the published results, the trace element concentrations in fish from Taihu Lake were similar to or lower than the values reported, demonstrating that the contamination levels in fish from Taihu Lake were low. 4.3. Potential health risk implications posed via fish consumption Excessive exposure of organisms to essential trace elements may result in toxic effects. There are no reports of accidental Fe poisoning. However, Fe deficiency in humans is frequently associated with anemia, and thus with reduced working capacity and impaired intellectual development (Medeiros et al., 2012). Hence, Fe supplementation is usually suggested for humans. Zinc has many important metabolic functions, and most organisms have

93

biochemical mechanisms to regulate the amount of Zn in the cells. A Zn deficiency in humans can lead to several disorders, but an excessive Zn intake can cause acute adverse effects (Kirchhoff and Scherz, 2006). Mn is recognized as an essential trace element for humans, and several metabolic roles have been identified (Hurley et al., 1984; Tinggi et al., 1997). Chromium is an essential trace element because trace amount of trivalent Cr(III) plays an essential role in glucose and lipid metabolism. However, high concentrations of Zn, Mn, and Cr may have toxic effects for humans. To date there are no regulations in China regarding the maximum allowable residue limits of Zn and Mn in fish for human consumption. In order to evaluate the potential health risk posed by fish consumption via Mn and Zn, we defined a maximum allowable concentration of the elements considering non-carcinogenic risk on the basis of the reference dose (RfD) of the elements and the maximum allowable fish consumption rate considering the non-carcinogenic effect of a contaminant (USEPA (United States Environmental Protection Agency), 2000). The maximum allowable concentration (mg/g ww) was calculated as C max ¼

ðBW  RfDÞ  1000, Rfish

where Rfish is the fish consumption rate; BW is the consumer body weight; and 1000 is the conversion factor of unit. In the present study, the Rfish and BW were set at 227 g/day and 70 kg, respectively (USEPA (United States Environmental Protection Agency), 2000). The RfD values of Mn and Zn are 0.14 and 0.3 mg/kg-day, respectively (IRIS/http://www.epa.gov/IRIS/S). As a result, the Cmax of Mn and Zn are 43.2 and 92.5 mg/g ww (i.e., 172.8 and 370 mg/g dw), respectively. If the concentrations of Mn and Zn are lower than the Cmax, it means that there is no obvious non-carcinogenic risk in consuming the fish species, and vice versa. In the fish species tested, the concentrations of Mn and Zn were much lower than the Cmax of the elements, indicating that Mn and Zn would not pose obvious human health risk via fish consumption considering non-carcinogenic effect endpoints of Mn and Zn. For Cr, the present concentrations were lower than the maximum allowable residue limit in China (Table 3). Nonetheless, the maximum allowable concentrations of Cr was calculated on basis on the RfD value of 0.003 mg/kg-day for Cr(VI) (Table 3). The concentrations of Cr did not exceed the maximum allowable concentration. In humans, a Cr deficiency can result in disturbances of the metabolism of glucose and lipids. The average human requires an estimated 1 mg/day of Cr (Joksimovic et al., 2011). Based on the results in the present study, approximately 5 g of dry fish (20 g wet weight) would provide the required Cr intake per day, even when consuming the fish species with the lowest Cr concentration. For the non-essential trace elements, there are maximum allowable residue limits in fish in China and the European Union. Arsenic is a potent toxicant and carcinogen, and its toxicity depends on the speciation (Devesa et al., 2008). Trivalent As(III) has the highest toxicity. Due to logistical constraints, only total As concentrations were measured in this study. With the exception of H. intermedius, N. taihuensis Chen, and C. mongolicus, the As levels measured in the species were lower than the maximum allowable residue limit of inorganic As in China (Table 3). However, all of our values were much lower than the maximum allowable residue limit of total As in freshwater fish established by the General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China (AQSIQ (General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China), 2001). For Hg, generally, the predominant species in fish is MeHg, which can be biomagnified through food chains, thus

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Y. Hao et al. / Ecotoxicology and Environmental Safety 90 (2013) 89–97

Table 2 Comparison of the concentrations of the trace elements in this study with those of wild fish from other water bodiesa. Country

Area

Year of collection (number of species)

China

Taihu Lake, Jiangsu In September 2009 (24)

China

Taihu Lake, Jiangsu – (4)

China

Taihu Lake, Jiangsu In September 2010 (8) China South Taihu Lake, In 2009 (1) Jiangsu China Taihu Lake, Jiangsu In April, May, June, and August, 2007 (1) China The Yangtze River In 2007(41) basin China Seven main coastal April and May cities and the Pearl 2010 (29) River Estuary China The Yellow River In August Delta 2008 (6) China The Yangtze River In 2006 and basin 2007 (31) China The East China Sea In November 2001 and 2002 (42) Vietnam The Mekong Delta In April 2004 (15) India Agatti Island In July– August, 2010 (20) – (5) Turkey Is-ıklı Dam Lake ¨ andKaracaoren Dam Lake Turkey The Black and In 2005 (9) Aegean Seas Turkey The Black Sea During 2008 (10) – (Asia) The Sulu Sea, the In November– December, Celebes Sea, and the Philippine Sea 2002 The Neretva river In October and Bosnia November, and 2003 (6) Herzegovina Sweden The Baltic Sea During 1991– 1993 (1) Slovenia In 2006 (10) ˇ The Salek lakes Brazil Egypt

Canada

Range (mg/g)

References

Hg

As

Cr

Cd

Pb

Fe

Mn

Zn

0.040– 0.521 dw 0.005– 0.122 ww –

0.040– 0.944 dw 0.009– 0.178 ww –

–

–

–

–

–

0.015– 7.8 ww

0.0005– 0.005 ww

0.0023– 0.037 ww

6.70– 16.8 ww –

0.74– 1.96 ww –

14.0– 175.7 dw 3.75– 62.4 ww 16– 130 dw 8.82– 17.6 ww 25.2– 73.1 ww 3.1– 4.4 ww

The present study

–

0.024– 0.242 dw 0.006– 0.045 ww 0.177– 0.287 dw 0.08– 0.43 ww –

1.11– 17.8 dw 0.215– 3.63 ww –

–

0.003– 0.151 dw 0.001– 0.034 ww 0.003– 0.021 dw 0.01– 0.07 ww –

1.86– 51.6 dw 0.275– 12.3 ww –

–

0.285– 0.518 dw 0.054– 0.102 ww ND– 0.387 dw 0.06– 0.18 ww –

ND– 0.054 ww –

ND– 0.039 ww 0.002– 0.133 dw

ND– 0.805 ww 0.017– 0.121 dw

ND–2.0 ww 0.009– 10.1 ww 0.003– 0.005– 0.06 dw 0.29 dw

–

–

0.79– 50.8 ww 10.4– 79.0 dw

Yi et al. (2011) Zhang and Wang (2012)

0.03– 0.59 dw 0.011– 0.048 ww ND–8.7 dw

ND– 8.97 dw 0.009– 0.039 ww 4.1–100 dw

3.6– 49.15 dw 0.005– 0.033 ww 0.33– 3.6 dw

ND– 0.05 dw 0.001– 1.21 ww 0.037– 5.52 dw

ND– 3.60 dw 0.009– 0.12 ww 0.032– 1.69 dw

–

2.41– 43.3 dw –

21.6– 713.1 dw 2.74– 27.5 ww 21.2– 134 dw

Cui et al. (2011) Yi et al. (2008) Asante et al. (2008)

0.11– 0.22 dw –

0.38– 2.3 dw –

2.7–13 dw

0.007– 0.061 dw Mean: 0.14 dw

0.078– 0.358 dw Mean: 0.24 dw

– Mean: 5.14 dw

8.76– 47.9 dw Mean: 0.31 dw

54.9– 117 dw Mean: 5.36 dw

Ikemoto et al. (2008) Dhaneesh et al. (2012)

–

–

12.12– 32.08 dw

1.95– 2.27 dw

1.24– 2.37 dw

0.37– 12.3 dw

8.85– 9.94 dw

2.64– 24.5 dw

Kalyoncu et al. (2012)

–

– 0.11– 0.32 ww 40–66 dwb

0.45– 0.9 dw 0.1– 0.35 ww –

0.33– 0.93 dw 0.28– 0.87 ww –

68.6– 163 dw 36.2– 145 ww –

–

–

0.95– 1.98 dw 0.63– 1.74 ww 0.66– 3.1 dwb

Uluozlu et al. (2007) Tuzen (2009)

3.96– 13.7 dwb

35.4– 106 dw 38.8– 93.4 ww 41.8– 55.2 dwb

–

–

473.6– – 11788 dw

2.17– 24.24 ww – 1.03– 172 dw

–

Chi et al. (2007) T. Yu et al. (2012) Cheng et al. (2010) Liu et al. (2009)

Asante et al. (2010)

0.05– 0.401 ww

–

–

0.013– 0.055 ww

0.055– 0.703 ww

–

–

–

Djedjibegovic et al. (2012)

0.01– 0.04 ww 0.03– 0.16 ww –

0.37– 0.79 ww 0.02– 0.08 ww 0.002– 5.5 ww –

0.23– 0.37 ww –

0.02– 0.04 ww ND– 0.02 ww 0.001– 0.3 ww 0.011– 2.69 ww

ND– 0.02 ww 0.01– 0.04 ww 0.01– 1.7 ww 1.07– 2.67 ww

5.85– 14.3 ww –

0.49– 1.23 ww –

9.61– 19.5 ww 6.71– 16.5 ww 0.06– 39.3 ww 3.35– 41.9 ww

Nfon et al. (2009) Petkovsek et al. (2012) Medeiros et al. (2012) Malhat (2011)

0.11– 1.4 ww

–

0.005– 0.03 ww

0.005– 0.47 ww

_

3.4– 53.4 ww

Benoit et al. (2011)

The Rio de Janeiro In April and State Coast, July 2009 (11) – The River Nile During June 2007– September 2008 (1) The Grand Lake In August 0.02– and The East River 2007 (7) 0.5 ww

– –

0.4– 0.07– 26.1 ww 7.3 ww 34.97– – 165.3 ww

0.19– 24.3 ww

ND: not detected. a In order to obtain the initial data in the literature, we listed the wet weighted concentrations of the trace elements, and the data in the table listed as wet weighted concentrations were not converted into dry weight based concentrations. b Range of geometric mean concentrations of the trace element in the sea.

leading to high levels in top predators. Mercury accumulation in fish has received much attention internationally, and many countries have fish consumption advisories related to Hg. The present concentrations of THg in the fish species tested herein were much lower than the maximum allowable residue limits in China, the European Union, and the maximum allowable concentration (Table 3). Lead is an environmental contaminant that can cause serious damage to human health. It competes with

calcium (Ca2 þ ) at enzymatic locations in organisms. The main exposure route of non-occupationally exposed individuals is food consumption (Liu et al., 2010). Like Pb, Cd is also a nonessential element that competes with calcium (Ca2 þ ) at enzymatic locations in organisms. Excessive Cd exposure may give rise to renal-, pulmonary-, hepatic-, skeletal-, and reproductivetoxicity effects and cancer. The Pb and Cd levels in all samples tested in our study were lower than the maximum allowable

Y. Hao et al. / Ecotoxicology and Environmental Safety 90 (2013) 89–97

95

Table 3 Maximum allowable residue limits (mg/g dw) of some toxic trace elements in fish in China and the European Union, and the maximum allowable concentrations (mg/g dw) of the elements considering non-carcinogenic risk calculated in the present study.

Chinaa

European Uniona The present result

Mn

Zn

Cr

As

Hg

Pb

Cd

References

–

–

8

0.4 (inorganic As) 2 (total As)

2–4 (MeHg)

2

0.4

Chinese Food Health Criterion, 2005

–

–

2 (MeHg)

172.8 370 3.7 0.37 (inorganic 0.12 (MeHg)c As)b 3.7 (total As)e 0.2 (THg)f

1.2 0.2 –

AQSIQ (General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China) (2001) EC No 1881/2006, 2006

1.23d This study

a

The data in the table are dry weight based on wet/dry weight conversion factor of 4 (Onsanit et al., 2010). The data listed is calculated based on the RfD value (0.0003 mg/kg-day) of inorganic As. c The data listed is calculated based on the RfD value (0.0001 mg/kg-day) of MeHg. d The data listed is calculated based on the RfD value (0.003 mg/kg-day) of Cr(VI). e Assuming that inorganic As constitutes 10% of total arsenic in fish (Liao and Ling, 2003). f Assuming that the contents of MeHg in the fish species accounted for 62% of the total Hg (Wang et al., 2012). b

0.6

THg concentrations (μg/g)

y = 0.0177x - 0.1928 0.5

R2 = 0.102, p=0.128

0.4 0.3 0.2 0.1 0.0 10.0

13.0

16.0

δ15N

19.0

22.0

(‰)

Fig. 2. Relationships between THg concentrations and the d15N values the species.

residue limits in China, the European Union, and the maximum allowable concentration (Table 3). 4.4. Trophic transfer behavior of trace elements The relationship between Hg concentrations and the d15N values of fish species is shown in Fig. 2, which showed that Hg concentrations increased with the trophic level (k40). This result suggested that Hg was likely to be biomagnified through the food chain. Previous studies reported positive correlations between d15N or trophic levels and MeHg (and also THg) in various food webs, suggesting that Hg was biomagnified in organisms at higher trophic levels (Campbell et al., 2005; Ikemoto et al., 2008; Nfon et al., 2009; Tadiso et al., 2011). Our result was consistent with this observation. However, it needed to be noted that the p-value for our data was only 0.128. It was only a marginal significance even if the significant levels was set at p ¼0.10. Possible explanations for this result included (1) fish species from Taihu Lake were generally only 1 year old (Y.X. Yu et al., 2012), and this young age may mean that lower biomagnification of Hg had occurred, even at higher trophic levels; and (2) the proportion of MeHg in fish from Taihu Lake was much lower than that reported previously, thus leading to a lower biomagnification potential of Hg present in the system. Concentrations of other seven trace elements (i.e., As, Cr, Cd, Pb, Fe, Mn, and Zn) decreased towards higher trophic levels (ko0) (data

not shown). There were no correlations between the trace element concentrations and d15N values (p¼0.269–0.962), which indicated that the trace elements were not biomagnified or biodiluted through the food chain in Taihu Lake. Similar results could also be found in the literature. Some studies have reported no significant correlations between d15N or the trophic level and the concentrations of the trace elements, which suggested no biomagnification or biodilution (Asante et al., 2008; Ikemoto et al., 2008; Zhang and Wang, 2012). However, different results were observed in some aquatic ecosystems. For example, biodilution of Pb and Cd in freshwater and marine species has been reported (Dehn et al., 2006; Nfon et al., 2009; Ruangsomboon and Wongrat, 2006; Winterbourn et al., 2000). Laboratory studies suggested that low assimilation efficiencies and high efflux rates of Cd and Pb in marine organisms decrease their biomagnification potentials in food chains (Wang, 2002). In contrast, some field studies in freshwater and marine ecosystems have found evidence of Cd biomagnification in food chains (Dietz et al., 2000). For As, a previous study in shallow and deep-water organisms from the East China Sea reported that As concentrations decreased with the trophic level, suggesting that it was diluted by the trophic transfer along food chains (Asante et al., 2008). However, it was inconsistent with another study in Sulu Sea fish by the same group (Asante et al., 2010), in which the As level was positively correlated with d15N, indicating an As biomagnification. Trophic transfer of trace elements through aquatic food chains can be highly variable. Thus, it is not appropriate to make direct comparisons among results from different studies because intrinsic factors, such as the species compositions, the lengths of food chains, and the physiological conditions of the environment, vary among studies and habitats. In contrast to persistent organic pollutants that are mainly concentrated in lipid-rich tissues, trace elements are stored and detoxified by specific organs such as liver. Differences observed in the biomagnification profile might be attributed to differences in metal accumulation and detoxification abilities. Many factors control the trophic transfer of trace elements along food chains, which explain why different results often are observed in varied aquatic food chains.

5. Conclusions The levels and trophic transfer behavior of eight trace elements in 24 fish species from Taihu Lake were investigated. The trace elements were detected in all the samples. The total concentrations of the eight trace elements ranged from 18.2 (S.

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dabryi) to 215.8 (H. intermedius) mg/g dw, with the MPI values of 0.315 (S. dabryi)–1.606 (T. swinhonis). The concentrations of the essential trace elements were higher than those of the nonessential trace elements, with Zn concentrations being the highest. The levels of the non-essential trace elements in the fish species were lower than the maximum allowable residue limits in China. Mercury might be biomagnified through the food chain in Taihu Lake if the significant level of p-value was set at 0.1. No biomagnification and biodilution were observed for other trace elements.

Acknowledgment This research was financially supported by the National Basic Research Program of China (No. 2008CB418205), the National Nature Science Foundation of China (No. 21277086), and Shanghai Leading Academic Disciplines (No. S30109).

Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.ecoenv.2012. 12.012.

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