Metal concentrations in various fish organs of different fish species from Poyang Lake, China

Ecotoxicology and Environmental Safety 104 (2014) 182–188

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Metal concentrations in various fish organs of different fish species from Poyang Lake, China YiHua Wei, JinYan Zhang, DaWen Zhang, TianHua Tu, LinGuang Luo n Institute for Quality & Safety and Standards of Agricultural Products Research, Jiangxi Academy of Agricultural Sciences, Nanchang 330200, PR China

art ic l e i nf o

a b s t r a c t

Article history: Received 13 August 2013 Received in revised form 29 January 2014 Accepted 1 March 2014

Concentrations of As, Cd, Cr, Cu, Hg, Ni, Pb, and Zn in the muscle of eleven fish species (bighead carp, bream, catfish, carp, crucian, Culter alburnus, grass carp, mandarin fish, white semiknife carp, silver carp, and yellow catfish) from Poyang Lake were analysed using inductive coupling plasma mass spectrometry. Metal levels in other organs (e.g., bladder, gill, kidney, liver, and spleen) of bighead carp, carp, grass carp, and silver carp were also determined. The results showed that metal concentrations in the muscle of all fish species were significantly lower than the proposed limits. Heavy metal concentrations were found to be substantially higher in benthic fish than in pelagic fish. Higher Hg contents were observed in predatory fish. In addition, various metals showed different affinity to fish organs. Hg was the most abundant in muscle, while Ni and Pb concentrations were highest in gills, Cd and Zn concentrations were highest in kidneys, and Cu was most commonly found in livers. Estimations of health risks revealed no evidence of potential threats to consumers. & 2014 Elsevier Inc. All rights reserved.

Keywords: Fish Heavy metal Risk assessment Poyang Lake

1. Introduction Toxic heavy metals, such as mercury (Hg), cadmium (Cd), and lead (Pb), are harmful to eco-environments and human beings. Hg can affect the reproductive health of fish. It enters the human body through the food chain and is a potential human carcinogen (Crump and Trudeau, 2009). Cd and Pb are non-essential metals that exhibit extreme toxicity, even at trace levels (Merian, 1991). Arsenic (As) is one of the most toxic elements for human and animal health, which can cause toxic and detrimental biological effects such as liver, skin, and bladder cancer (Kapaj et al., 2006). Although copper (Cu) and zinc (Zn) are essential minerals for humans, overdosing on these beneficial elements can also cause health problems (Gale et al., 2004). Heavy metals cannot degrade, and they are continuously deposited and incorporated into water, sediments, and aquatic organisms (Linnik and Zubenko, 2000). Heavy metal pollution has begun to grow at an alarming rate and now constitutes a significant global problem (Malik et al., 2010). Anthropogenic activities, such as increased population, urbanisation, industrialisation, and agricultural practices, have further aggravated this problem (Gupta et al., 2009). Fish are an important source of protein for humans. Additionally, they are low in cholesterol and contain beneficial poly-unsaturated fatty acids (Ersoy and Celik, 2010). However, contaminant levels in fish

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Corresponding author. Fax: þ86 791 87090291. E-mail address: [email protected] (L. Luo).

http://dx.doi.org/10.1016/j.ecoenv.2014.03.001 0147-6513/& 2014 Elsevier Inc. All rights reserved.

present a considerable concern. Heavy metals, particularly Hg, are known to accumulate in various aquatic organisms and can be bioaccumulated via the food chain to levels that are hazardous to health (Mathews and Fisher, 2009). The general population is most commonly exposed to Hg through the consumption of fish (CastroGonzáleza and Méndez-Armenta, 2008). Methyl-mercury (Me-Hg) concentrations, in particular, are typically high in some fish species and account for most of the total Hg found in fish. Me-Hg is known to cause adverse health effects in people who consume large quantities of fish (Hites et al., 2004). It is therefore important to determine the metal concentrations in fish and evaluate the possible risks to human health following the consumption of fish. Not surprisingly, numerous previous studies have focused on metal accumulation in various fish species (e.g., Cheung et al., 2008; Qiu et al., 2011; Cai et al., 2012; Medeiros et al., 2012). Poyang Lake is regarded as the largest freshwater lake in China. It has significant ecological, social, economic, and recreational value. Five major rivers, including the Ganjiang, Fuhe, Xinjiang, Raohe, and Xiushui rivers, flow into the lake. In the northern portion of Poyang Lake, there is an outfall to the Yangtze River. These rivers are the greatest contributors of industrial wastewater and domestic sewage to the lake. The Dexing and Yongping copper mines, as well as the Guixi metallurgical refinery, are located next to the lake, and large amounts of metals are transferred into the lake, primarily via the Raohe and Xinjiang rivers. Over the past twenty years, Jiangxi Province has achieved rapid economic development, causing increasingly intense environmental pressures on Poyang Lake. For instance, Cu, Pb, and Zn levels in sediments from Poyang Lake averaged

Y. Wei et al. / Ecotoxicology and Environmental Safety 104 (2014) 182–188

30.20 mg/kg (ranging from 12.40 to 112.08 mg/kg), 68.18 mg/kg (31.75–118.14 mg/kg), and 75.56 mg/kg (51.21–118.15 mg/kg), respectively, values that are significantly higher than their background concentrations of 4.75, 17.57, and 45.75 mg/kg, respectively (Zhang et al., 2012). The study of heavy metals in water and sediments in the Poyang Lake region has gained considerable interest recently (Luo et al., 2008; Yuan et al., 2011, Zhang et al., 2012). However, few reports have focused on heavy metal concentrations in the fish found in the lake. The possible accumulation of heavy metals in fish is an important indicator of contamination of the Poyang Lake's water system. The main objectives of this study are as follows: (1) to determine the As, Cd, Cr, Cu, Hg, Ni, Pb, and Zn concentrations in several organs of various fish species from Poyang Lake and (2) to conduct a health risk assessment of heavy metals attributed to the consumption of fish.

183

the rainy season and 1000 km2 in the dry season. Its average depth is 8.4 m, while the maximum depth is 25.1 m. The total water volume of the lake is 2.95 km3.

2.2. Sample collection A total of eleven fish species (bighead carp, bream, carp, catfish, C. alburnus, crucian, grass carp, mandarin fish, white semiknife carp, silver carp, and yellow catfish) were caught from Poyang Lake by fisherman in the spring of 2011. The scientific and common names, feeding modes, and related parameters of the sampled fish species are listed in Table 1. Samples were wrapped in plastic bags, placed in polyethylene bags, and stored in an ice box for further treatment. The fish were dissected, and the muscle, bladder, gill, kidney, liver, and spleen were separated. All organs were lyophilised using a FD-1A-50 freeze dryer (Beijing Boyikang Lab Instrument Co, Ltd., Beijing, China) and then homogenised and stored in a desiccator before metal analysis. Concentrations of As, Cd, Cr, Cu, Hg, Ni, Pb, and Zn were determined using an inductive coupling plasma mass spectrometry (ICP-MS) (Elan DRC-e, PerkinElmer SCIEX, USA).

2.3. Reagents

2. Materials and methods 2.1. Study area Poyang Lake is located in the northern part of Jiangxi Province to the south of the Yangtze River (Fig. 1). Poyang Lake depends on surface runoff and rainfall for its water supply. The lake occupies an area of 162,225 km2, with a maximum length of 170 km and a maximum width of 17 km. It accounts for 97 per cent of the total catchment of the watershed of Jiangxi Province. Its surface area is 4400 km2 during

All reagents used, including nitric acid (67 per cent) and hydrogen peroxide (30 per cent), were of ultra-pure grade (Suzhou Crystal Clear Chemical Co., Ltd., China). All laboratory wares used for storage, handling, or sample decontamination were immersed overnight in a 20 per cent v/v HNO3 solution, rinsed with ultrapure water, and finally dried on a clean bench. The standard solutions for the calibration curves (National Centre of Analysis and Testing for Nonferrous Metals and Electronic Materials, China) were prepared from a 1000 mg/L standard by dilution with acidified ultrapure water (5 per cent v/v HNO3).

Fig. 1. Map of Poyang Lake.

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Table 1 Fish species obtained from Poyang Lake. Common name

Scientific name

Feeding mode

n

Body length/cm (mean7 SD)

Weight/g (mean7 SD)

Bighead carp Bream Carp Catfish Crucian Culter alburnus Grass carp Mandarin fish Silver carp White semiknife carp Yellow catfish

Hypophthalmichthys nobilis Parabramis pekinensis Cyprinus carpio carpio Siluriformes Carassius auratus Culter alburnus Ctenopharyngodon idellus Siniperca chuatsi Hypophthalmichthys molitrix Hemicculter Leuciclus Pelteobagrus fulvidraco

Filter feeder Herbivorous Omnivorous Carnivorous Omnivorous Carnivorous Herbivorous Carnivorous Filter feeder Omnivorous Carnivorous

6 6 8 8 8 6 10 4 10 6 5

45.0 7 15.3 23.5 7 2.9 27.9 7 5.0 31.6 7 7.0 15.4 7 6.0 26.2 7 6.3 41.17 6.5 27.5 7 1.8 43.4 7 6.9 13.0 7 0.9 13.4 7 2.9

24587 1648 3017 160 6117 358 3577 242 1587 162 222 7 115 14717 503 6357 102 1480 7 498 26.3 7 6.9 50.6 7 42.6

2.4. Analytical procedure Approximately 0.5 g of the sample was weighed into a polytetrafluoroethylene (PTFE) vessel containing 5 mL HNO3 and 2 mL H2O2 and then kept for 30 min at room temperature. The sample was digested in a Mars X-press Microwave Digestion System (CEM, USA). The microwave digestion process was as follows: the temperature was first brought to 120 1C for 6 min, that temperature was maintained for 3 min, the sample was brought to 150 1C for 3 min, kept at 150 1C for 3 min, and finally it was brought to 190 1C over a 4 min period and held at 190 1C for 30 min. After digestion, the solution was diluted to a total volume of 50 mL with ultra-pure water, followed by adding 1 mL of 500 μg/L Rh as an internal standard. Further analyses were conducted using ICP-MS. 2.5. Certified reference material for quality control Certified reference material GBW08573 (yellow croaker) was used to validate the method for determining the concentrations of metals. Relative standard deviations among sample replicates were o 10 per cent, the recovery rates for metals ranged from 85 per cent to 110 per cent, and the data showed good agreement between measurement values and certified values. Metal concentrations were expressed on a dry weight (dw) basis as mg/kg. However, metal concentrations in muscle were converted to wet weight (ww) for comparison, assuming water content of 80 per cent. 2.6. Health-risk assessment for fish consumption Daily heavy metal intake (EDI) was estimated based on the average concentrations of all fish muscle and daily fish consumption rates. The risks for fish consumption were assessed based on target hazard quotients (THQs). THQs assume a level of exposure below which it is unlikely for even sensitive populations to experience adverse health effects. If the EDI exceeds this threshold, there may be concern for potential non-carcinogenic effects. Higher THQ values mean a higher probability of experiencing long-term non-carcinogenic effects. In general, if the THQ value is less than 1, toxic effects are not expected to occur (Chien et al., 2002). EDI ¼

C  FIR  EDtot  EFr  10  3 BWa  Atn

THQ ¼

C  FIR  EDtot  EFr  10  3 Rf D  BWa  Atn

where C is the average concentration of heavy elements in fish (mg/kg wet weight); FIR is the rate of fish consumption (71 g/day/person) as recorded by the Food and Agricultural Organisation (2008); EDtot is the exposure duration (70 years, average lifetime); EFr is the exposure frequency (365 days/year); BWa is the average Chinese adult body weight (58.1 kg) (Gu et al., 2006); and Atn is the average exposure time for non-carcinogens (365 days/year  number of exposure years, assuming 70 years). Current metal intakes were compared with the respective provisional tolerable weekly intakes (PTWIs). PTWIs were established by the Joint Food and Agriculture Organization/ World Health Organization Expert Committee on Food Additives (1993). ADI was calculated from PTWIs set by JECFA (1993). Reference doses (RfDs) of individual heavy elements were obtained from the United States Environmental Protection Agency (2010).

3. Results and discussion 3.1. Metal concentrations in the muscle of eleven fish species Metal concentrations in the muscle of eleven fish species from Poyang Lake are shown in Table 2.

3.1.1. As The highest concentration of As in fish muscle found was 0.084 mg/kg in carp, the lowest concentration found was 0.010 mg/kg in grass crap, and the average concentration in all sampled fish was 0.040 mg/kg. The concentrations of As in fish species can be sequenced as follows: carp4white semiknife carp4C. alburnus4crucian4yellow catfish4silver carp4bighead carp4bream4catfish4grass carp. The literature reports As levels to be 0.42–3.44 mg/kg in four farmed fish species from fish ponds in the Pearl River Delta of China (Cheung et al., 2008), 0.88–4.48 mg/kg in two cultured marine fish species in the Fujian Province of China (Onsanit et al., 2010), 0.156–0.834 mg/kg in fifteen fish species in the Persian Gulf (Saei-Dehkordi et al., 2010), and 0.43–5.91 mg/kg in four fish species in the Adriatic Sea (Bilandžić et al., 2011). Compared with the values from these previous studies, As levels in this study were found to be far lower. However, As levels in this study were slightly higher than reported by Yi et al. (2008) for 28 fish species (0.012–0.029 mg/kg) in the Yangtze River of China. According to the United States Food and Drug Administration (1993), inorganic arsenic can be estimated as 10 per cent of total arsenic. Based on this parameter, concentrations of inorganic arsenic for muscles of all fish species do not exceed the safety limit set by the China National Standards Management Department. 3.1.2. Cd The highest Cd level in muscle was 0.009 mg/kg for bream, while the lowest level was 0.0009 mg/kg for mandarin fish. The mean level was 0.004 mg/kg with the following decreasing order: bream 4catfish4white semiknife carp 4crucian 4carp 4yellow catfish4 grass carp4C. alburnus 4 bighead carp4mandarin fish. These values are in agreement with much of the literature, which reports Cd concentrations of 0.0011–0.0088 mg/kg for fish from the Yangtze River (Yi et al., 2008), 0.003–0.021 mg/kg (dw) in four fish species from Taihu Lake of China (Chi et al., 2007), 0.002– 0.006 mg/kg in fish from the Adriatic Sea (Bilandžić et al., 2011), and 0.001–0.009 mg/kg in eleven fish species from Rio de Janeiro State in Brazil (Medeiros et al., 2012). However, the Cd levels in the present study were lower than those reported in other studies, including Cd ranging from 0.03 to 1.57 mg/kg in fish from the Pearl River Delta (Cheung et al., 2008), 0.01 to 0.04 mg/kg in fish from Fujian Province (Onsanit et al., 2010), and 0.024 to 0.030 mg/kg in fish from the Yellow River of China (Wang et al., 2010). 3.1.3. Cr The highest Cr content in muscle was detected in white semiknife carp (0.291 mg/kg). The lowest content was detected in bighead carp (0.186 mg/kg). The average content was 0.238 mg/ kg. The decreasing order of Cr was as follows: white semiknife carp4C. alburnus 4grass carp 4carp4 bream 4crucian 4catfish 4silver carp4mandarin fish4yellow catfish4 bighead carp.

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Table 2 Metal concentrations in the muscle (mg/kg, wet weight converted by dry weight assuming water content of 80 per cent) of fish species from Poyang Lake (mean7 SD). Fish species

As

Cd

Cr

Cu

Hg

Ni

Pb

Zn

Bighead carp Bream Carp Catfish Crucian Culter alburnus Grass carp Mandarin fish Silver carp White semiknife carp Yellow catfish Chinaa EUb

0.026 70.001 0.023 70.007 0.084 70.019 0.014 70.002 0.0457 0.006 0.055 70.007 0.010 70.001 0.0637 0.003 0.029 70.002 0.062 7 0.002 0.030 70.004 0.1 (inorganic As) –

0.002 70.0005 0.009 70.0011 0.005 70.0010 0.0077 0.0008 0.0067 0.0009 0.002 70.0006 0.003 70.0007 0.00097 0.0002 0.0017 0.0003 0.0077 0.0001 0.003 70.0007 0.1 0.05

0.1867 0.019 0.252 7 0.043 0.254 7 0.042 0.241 70.046 0.2477 0.024 0.265 7 0.057 0.255 7 0.040 0.208 7 0.041 0.2177 0.026 0.2917 0.140 0.20770.029 1.0 –

0.325 7 0.093 0.7037 0.101 0.476 70.144 0.2217 0.034 0.505 7 0.044 0.2007 0.027 0.328 7 0.081 0.096 7 0.015 0.205 7 0.043 0.6187 0.079 0.363 7 0.062 – –

0.0467 0.017 0.0357 0.011 0.036 7 0.011 0.086 7 0.024 0.030 7 0.006 0.1167 0.024 0.008 7 0.003 0.168 7 0.023 0.038 7 0.009 0.054 7 0.004 0.082 7 0.025 0.5 (Me-Hg)c 0.5

0.021 70.006 0.0407 0.012 0.0247 0.010 0.0757 0.036 0.114 70.044 0.0187 0.010 0.0357 0.013 0.0177 0.007 0.028 70.021 0.056 70.023 0.034 70.009 – –

0.0167 0.004 0.021 70.005 0.026 7 0.008 0.028 7 0.010 0.084 7 0.027 0.0147 0.005 0.0177 0.006 0.029 7 0.010 0.0197 0.007 0.0707 0.013 0.022 7 0.004 1.0 0.3

3.46 7 0.66 4.55 7 0.40 14.5 7 4.57 5.69 7 1.05 11.6 71.80 4.127 0.57 3.977 0.84 5.007 0.77 2.99 7 0.80 11.17 0.65 12.5 74.39 – –

a b c

China National Standards Management Department (2012). European Union (2006). Non-predatory fish.

Cr levels found in this study were higher than those reported by Yi et al. (2008), who found Cr ranging from 0.0051 to 0.053 mg/kg in fish from the Yangtze River. In other studies, Cr contents were found to be 0.95–1.98 mg/kg in fish from the Black and Aegean seas of Turkey (Uluozlu et al., 2007), 0.04–1.75 mg/kg in twelve fish species from the Marmara, Aegean and Mediterranean seas (Türkmen et al., 2008), and 0.08–2.63 mg/kg in fish from the Pearl River Delta (Cheung et al., 2008). Compared with these values, the Cr contents found in fish muscle from Poyang Lake were low. 3.1.4. Cu Concentrations of Cu in muscle ranged from 0.096 mg/kg for mandarin fish to 0.703 mg/kg for bream, with a mean concentration of 0.367 mg/kg. The order of Cu concentration was as follows: bream4white semiknife carp4crucian4carp4yellow catfish4 grass carp4bighead carp4catfish4silver carp4C. alburnus4mandarin fish. In the literature, higher levels of Cu were reported as 0.73– 1.83 mg/kg in nine fish species from the Black and Aegean seas of Turkey (Uluozlu et al., 2007), 0.32–6.48 mg/kg in fish from the Marmara, Aegean and Mediterranean seas (Türkmen et al., 2008), 0.4–3.41 mg/kg in fish from the Yangtze River (Yi et al., 2008), 0.23– 1.47 mg/kg in fish from the Adriatic Sea (Bilandžić et al., 2011), and 1.2–2.9 mg/kg in fish from Rio de Janeiro State (Medeiros et al., 2012). 3.1.5. Hg The highest Hg content in muscle was observed in mandarin fish, with a concentration of 0.168 mg/kg, followed by C. alburnus (0.116 mg/kg) and catfish (0.086 mg/kg). The lowest content was observed in crucian, which had 0.008 mg/kg Hg. The average content of Hg was 0.064 mg/kg, with an average of 0.113 mg/kg for predatory fish (0.082–0.168 mg/kg) and an average of 0.035 mg/kg for nonpredatory fish (0.008–0.054 mg/kg). The following decreasing order of Hg content was found: mandarin fish4C. alburnus4catfish4yellow fish4white semiknife carp4bighead carp4silver carp4carp4 bream4grass carp. Hg contents found in this study were consistent with those previously reported in the literature, including 0.01– 0.17 mg/kg for fish from Victoria, Australia (Fabris et al., 2006), 0.01– 0.22 mg/kg for fish from the Pearl River Delta (Cheung et al., 2008), and 0.04–0.08 mg/kg for fish from the Adriatic Sea (Bilandžić et al., 2011). The Hg concentrations found were lower than those reported by Yi et al. (2008) for fish from the Yangtze River (0.0011–0.048 mg/ kg). Higher levels of Hg (0.120–0.527 mg/kg) have also been reported in fish from the Persian Gulf (Saei-Dehkordi et al., 2010). According to Bloom (1992), Me-Hg accounts for more than 95 per cent of the total mercury in the edible muscle of fish. Even if

the concentration of Me-Hg was estimated using a value of 100 per cent of total Hg, none of the fish exceeded the safety limits set by China and the European Union. 3.1.6. Ni The highest Ni concentration in the edible parts of eleven fish species was 0.114 mg/kg for crucian, while the lowest concentration was 0.017 mg/kg for mandarin fish. The average Ni concentration was 0.042 mg/kg. The order of Ni concentration from large to small was as follows: crucian4 catfish4 catfish4 oil article 4 bream 4grass carp4silver carp4carp4bighead carp4C. alburnus4mandarin fish. In other studies, Ni concentrations ranged from 1.92 to 5.68 mg/kg in fish from the Black and Aegean seas (Uluozlu et al., 2007) and 0.02 to 3.97 mg/kg in fish from the Marmara, Aegean and Mediterranean seas (Türkmen et al., 2008). Compared with these previous studies, Ni concentrations found in this study were lower. 3.1.7. Pb The highest Pb content in muscle was 0.084 mg/kg for crucian, and the lowest content was 0.014 mg/kg for C. alburnus. The mean Pb content was 0.030 mg/kg. The decreasing order of Pb content was as follows: crucian4white semiknife carp4mandarin fish4catfish4 carp4yellow catfish4bream4silver carp4grass carp4bighead carp4C. alburnus. Bilandžić et al. (2011) found lower values, with concentrations ranging from 0.01 to 0.02 mg/kg in fish from the Adriatic Sea. Pb contents in this study agreed with the literature, which reported Pb ranging from 0.177 to 0.287 mg/kg (dw) in fish from Taihu Lake (Chi et al., 2007), 0.009 to 0.066 mg/kg in fish from the Yangtze River (Yi et al., 2008), and 0.061 to 0.085 mg/kg in fish from the Yellow River (Wang et al., 2010). Whereas higher Pb levels were described by other authors, including concentrations ranging from 0.33 to 0.93 mg/kg in fish of the Black and Aegean seas (Uluozlu et al., 2007), 0.33 to 0.86 mg/kg in fish from the Marmara, Aegean and Mediterranean seas (Türkmen et al., 2008), 0.33 to 7.74 mg/kg in fish from the Pearl River Delta (Cheung et al., 2008), and 0.04 to 0.3 mg/kg in fish from Rio de Janeiro State (Medeiros et al., 2012). 3.1.8. Zn Zn levels in muscle ranged from 2.99 mg/kg for silver carp to 14.5 mg/kg for carp, with a mean concentration of 7.23 mg/kg. The fish species can be ordered from the highest to the lowest levels of Zn as follows: carp4yellow catfish4crucian4white semiknife carp4catfish4mandarin fish4bream4C. alburnus4grass carp4bighead carp4silver carp. Zn levels in this study were similar to the literature, which reported ranges from 4.49 to 11.2 mg/kg for fish from the

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Y. Wei et al. / Ecotoxicology and Environmental Safety 104 (2014) 182–188

Marmara, Aegean and Mediterranean seas (Türkmen et al., 2008), 2.74 to 11.57 mg/kg in fish from the Yangtze River (Yi et al., 2008), 4.327 to 5.668 mg/kg in fish from the Yellow River (Wang et al., 2010), and 2.7 to 9.3 mg/kg in fish from Rio de Janeiro State (Medeiros et al., 2012). Higher Zn levels were found by Uluozlu et al. (2007), with Zn concentrations ranging from 35.4 to 106 mg/kg in fish from the Black and Aegean seas. Metal concentrations in the muscle of all fish species from Poyang Lake were significantly lower than the limits proposed by China and the European Union. Based on the results of this study, metal concentrations in fish muscle from the lake were found in the following descending order: Zn4Cu4Cr4Hg4Ni4As4Pb4Cd. We found that carp had the highest As and Zn concentrations, bream had the highest Cd and Cu concentrations, crucian had the highest Ni and Pb concentrations, and mandarin fish had the highest Hg concentration. Different fish species from the same area contained different metal levels in muscle tissue. It is noted that the same fish did not have the highest values of more than two metals. The differences may be due to trophic level, geography, size, age, foraging method/location, and the propensity of metals to undergo biomagnification in the food chain. Fish living near the lake bed and feeding on benthic invertebrates (e.g., bream, carp, crucian, and mandarin fish) exhibited significantly higher metal levels when compared to those living in the upper or middle zones of the water column (e.g., bighead carp and grass carp). Benthic fish, which are in contact with the sediment, accumulate relatively high heavy metal concentrations and reliably reflect the contamination state of the aquatic environment. Mandarin fish, C. alburnus, and catfish, which are relatively high on the food chain, have much higher Hg concentrations than those found in non-predatory fish. Marrugo-Negrete et al. (2008) also noted the presence of higher Hg concentrations in predatory fish species. Unlike the Hg concentration, Pb and Cd concentrations did not show any increase among fish species in water ecosystems. Interestingly, several elements (e.g., Cr, Cu, Pb, and Zn) were found at lower concentrations in predatory fish than in non-predatory fish. The metals showed high correlation coefficients between the concentrations in fish, sediment and water (Usero et al., 2003). A comparison has been made between metal concentrations in fish muscle from Poyang Lake and in polluted water ecosystems of the world (Table 3). In polluted areas, high metal levels in the edible

parts of fish were reported to be 1.98–3.96 mg/kg for As, 0.028– 0.050 mg/kg for Cd, and 0.4–1.5 mg/kg for Cu in the Odiel reservoirs from the southern Atlantic coast of Spain (Usero et al., 2003); 16–130 mg/kg for Zn (dw) in Taihu Lake of China (Chi et al., 2007); 0.42–3.44 mg/kg for As, 0.03–1.57 mg/kg for Cd, 0.08– 2.63 mg/kg for Cr, and 0.33–7.74 mg/kg for Pb in the Pearl River Delta of China (Cheung et al., 2008); 10.36 mg/kg for Cd, 48.84 mg/ kg for Cu, 10.1 mg/kg for Pb, and 212.44 mg/kg for Zn (dw) in the Manzala Lake of Egypt (Seed and Shaker, 2008); and 0.71–1.77 mg/ kg for Cd, 0.12–1.75 mg/kg for Ni, and 1.42–4.48 mg/kg for Pb (dw) in the Athi-Galana-Sabaki tributaries of Kenya (Muiruri et al., 2013). We can see that metal concentrations in the fish, sediment, and water of Poyang Lake were at comparatively low levels in comparison with those observed in more polluted areas. 3.2. Risk assessment The estimated EDI values and THQ values are given in Table 4. The estimated EDI values were far below the recommended values. The THQ values were significantly lower than 1. Therefore, it can be concluded that the metals monitored in the edible parts of fish species from Poyang Lake pose no health problems for consumers. 3.3. Metal levels in various organs of different fish species Metals show different affinity to fish organs, which may be due to the different metabolic roles of metals and functions of organs (Asharf, 2005). Metal levels in fish organs not only reflect exposure to elements but also the elemental excretion from various organs by metabolic processes. The gill is the first organ to be exposed to re-suspended sediment particles. Thus, significant levels of interaction with metal ions occur in fish gills (Pawert et al., 1998). Metal levels in the liver represent metal storage from the waters and sediments where the fish species live (Karadede et al., 2004). Thus, the liver is recommended as an environmental indicator of external medium pollution more often than other fish organs (Jezierska and Witeska, 2006). As presented in Table 5, Cu levels in the liver of silver carp were 400 times higher than in muscle; Cd levels in the kidney of carp were 370 times higher than in muscle; Zn levels in gills of carp were 43 times higher than in muscle; and Ni levels in gills of bighead carp were twenty times higher than in muscle. As levels

Table 3 Metal concentrations in the muscle of fish species (mg/kg), sediments (mg/kg), and water (μg/L) from Poyang Lake and polluted water ecosystems of the world. As Poyang Lake

a

Zhang et al. (2012). Usero et al. (2003). Chi et al. (2007). d Cheung et al. (2008). e Seed and Shaker (2008). f Muiruri et al. (2013). b c

Cr

Fish 0.010–0.084 0.0009–0.009 0.186–0.291 Sedimentsa 8.35–23.18 0.13–1.49 – a Water 0.83–2.18 0.01–0.36 –

Polluted water ecosystems Fish Odiel reservoirs of the southern Atlantic coast, Spainb Sediments Water Taihu Lake, Chinac Fish (dw) Fish ponds of Pearl Fish d River Delta, China Sediments Manzala Lake, Egypte Fish (dw) Sediments Water Athi-Galana-Sabaki Fish (dw) tributaries, Kenyaf Water ND, not detected.

Cd

1.98–3.96 81–328 43–60 – 0.42–3.44 55.4–62.7 – – – – –

0.028–0.050 9–19 0.4–3.4 0.003–0.021 0.03–1.57 1.07–2.34 10.36 33.00–110.00 10–90 0.71–1.77 ND-10

0.032–0.050 61–67 0.4 ND-1.890 0.08–2.63 17.6–94.7 – – – ND-0.2 ND-68

Cu

Hg

Ni

0.096–0.703 16.01–112.08 0.10–2.14

0.008–0.168 0.017–0.114 0.014–0.084 – 17.26–32.08 31.75–118.14 – 0.67–1.53 0.13–0.66

2.99–14.5 51.21–118.15 0.71–5.24

0.4–1.5 221–757 3.7–11 – – – 48.84 106.00–412.00 360–680 – –

0.011–0.023 0.7–1.6 o 0.1 – 0.01–0.22 0.07–0.23 – – – – –

6.07–11.4 1000–3450 33–57 16–130 – – 212.44 202.00–576.00 320–660 28.00–76.33 2–695

0.015–0.070 43–46 3.3–3.8 – – – – – – 0.12–1.75 7–62

Pb

0.03–0.09 116–285 0.8–0.9 0.177–0.287 0.33–7.74 57.1–82.4 10.1 78.00–174.00 12–220 1.42–4.48 4–47

Zn

Y. Wei et al. / Ecotoxicology and Environmental Safety 104 (2014) 182–188

were the highest in the gills of silver carp. Cd levels were the highest in the kidneys of carp. Cr levels were the highest in the bladders of silver carp. Cu levels were highest in the livers of silver carp. Ni levels were the highest in the gills of bighead carp. Pb levels were the highest in the gills of silver carp. Zn levels were the highest in the gills of carp. Based on these results, it was concluded that the liver is the primary organ for Cu deposition, the kidney is the primary organ for Cd and Zn deposition, and the gills are the ideal organs for Ni and Pb deposition. Similar results were demonstrated in previous studies (e.g., Čelechovská et al., 2007; Tepe et al., 2008; Has-Schön et al., 2008). Compared with the gill, kidney, and liver, muscle typically contains low metal concentrations. Alcorlo et al. (2006) suggested that muscle was not an active tissue for metal bioaccumulation. Consistent with this hypothesis, the lowest Cd and Pb concentrations were found in muscle tissue. However, the highest level of Hg was also discovered in muscle tissue, which suggests that Hg can accumulate more easily in muscle than in other organs. Similar results have been described in previous reports (Čelechovská et al., 2007; Has-Schön et al., 2008).

187

In conclusion, fish organs, such as the gill, liver, and kidney, accumulate greater amounts of heavy metals in benthic fish species, and Hg accumulates in the muscle tissue of predatory fish species, making these organs and muscle suitable as environmental monitors.

4. Conclusions This study provides new information on heavy metal and As concentrations in eleven fish species from Poyang Lake. Our results reveal that the metal concentrations in all analysed fish species from the Poyang Lake were generally low and safe for consumption. Metal accumulation in fish depends primarily on the concentrations found in ambient water and prey or commercial feed and on biological and ecological factors such as the feeding habits and habitat of the fish (Sankar et al., 2006; Kojadinovic et al., 2007). We found that the concentrations of metals varied significantly depending on the type of the organ and fish species sampled.

Table 4 Daily intakes of metals (EDIs) and the target hazard quotients (THQs) through fish from Poyang Lake. Metals

Average concentration (mg kg  1 wet weight)

EDIs (mg kg  1 day  1)

ADIs (mg kg  1 day  1)

Ratio of EDIs to ADIs (per cent)

Rfds (mg kg  1 day  1)

THQs

Inorganic Asa Cd Cr Cu Me-Hgb Ni Pb Zn

4.01E-03 4.17E-03 2.38E-01 3.67E-01 6.35E-02 4.20E-02 3.15E-02 7.23E þ00

4.90E-06 5.10E-06 2.91E-04 4.48E-04 7.77E-05 5.13E-05 3.84E-05 8.84E-03

2.14E-03 1.00E-03 2.17E-03 5.00E-01 2.30E-04 1.17E-02 3.60E-03 1.33E-01

2.29E-01 5.10E-01 1.34E þ01 8.97E-02 3.38Eþ 01 4.39E-01 1.07Eþ 00 6.64E þ00

3.00E-04 1.00E-03 1.50E þ 00 4.00E-02 1.00E-04 2.00E-02 2.00E-02 3.00E-01

1.63E-02 5.10E-03 1.94E-04 1.12E-02 7.77E-01 2.57E-03 1.92E-03 2.95E-02

a Average concentration of inorganic As was estimated by using a value of 10 per cent of total As in accordance with the United States Food and Drug Administration (USFDA) (1993). b Average concentration of Me-Hg was estimated by using a value of 100 per cent of total Hg (Bloom, 1992).

Table 5 Metal levels (mg/kg, dry weight) in different organs of several fish species from Poyang Lake (mean7 SD). Fish species

As

Cd

Cr

Cu

Hg

Grass carp Muscle Bladder Gill Kidney Liver Spleen

0.050 7 0.005 0.057 7 0.007 0.155 7 0.020 0.127 7 0.044 0.158 7 0.069 0.070 7 0.018

0.007 70.004 0.011 70.004 0.044 70.019 2.86 71.60 1.92 71.01 0.089 70.031

1.28 7 0.20 1.81 7 0.37 1.30 7 0.16 1.377 0.27 1.157 0.10 1.29 7 0.19

1.647 0.40 1.917 0.23 2.377 0.26 7.84 7 1.33 2477 130 20.9 7 13.4

0.040 70.015 0.02470.033 0.025 70.013 0.105 70.077 0.074 70.033 0.015 70.005

Carp Muscle Bladder Gill Kidney Liver Spleen

0.419 7 0.095 0.404 7 0.122 0.310 7 0.076 0.589 7 0.903 0.3567 0.110 0.179 7 0.228

0.014 70.005 0.084 70.052 0.121 70.077 5.20 76.61 1.31 71.17 0.115 74.073

1.277 0.21 2.197 0.88 1.977 0.58 1.617 0.05 2.94 7 1.38 1.137 0.10

2.38 7 0.72 2.26 7 0.75 3.56 7 1.33 7.23 7 3.56 73.8 7 31.5 3.107 1.96

Silver carp Muscle Bladder Gill Kidney Liver Spleen

0.146 7 0.010 0.135 7 0.035 0.659 7 0.378 0.416 7 0.041 0.418 7 0.096 0.3597 0.047

0.003 70.002 0.104 70.102 0.097 70.045 3.01 71.09 1.19 70.48 0.217 70.034

1.08 7 0.013 2.95 7 0.77 2.137 0.64 1.357 0.07 1.247 0.21 2.34 7 0.14

Bighead carp Muscle Bladder Gill Kidney Liver Spleen

0.130 7 0.005 0.258 7 0.144 0.270 7 0.032 0.306 7 0.025 0.306 7 0.049 0.3547 0.026

0.004 70.003 0.02470.008 0.126 70.051 2.39 70.51 0.735 70.356 0.127 70.013

0.93 7 0.10 2.197 0.05 1.247 0.18 1.447 0.14 1.38 7 0.05 1.79 7 0.22

Ni

Pb

Zn

0.177 0.07 0.157 0.05 1.82 7 0.34 0.247 0.12 0.157 0.10 0.177 0.16

0.086 70.030 0.084 70.049 0.335 70.140 0.165 70.089 0.124 70.055 0.197 70.104

19.84 7 4.22 53.7 7 7.83 84.8 7 7.08 1007 12 3507 127 1347 39.2

0.180 70.015 0.017 70.005 0.041 70.010 0.090 70.006 0.044 70.015 0.015 70.019

0.127 0.05 0.55 7 0.33 1.647 0.46 0.157 0.04 0.09 7 0.04 0.22 7 0.17

0.128 70.040 0.133 70.055 0.70270.207 0.22470.153 0.123 70.047 0.174 70.097

72.6 7 22.9 436 7 157 31297 1331 21447 348 956 7 612 202 7 278

1.02 7 0.22 2.258 7 1.04 7.067 5.90 13.7 7 6.34 4127 142 19.8 7 6.37

0.189 70.045 0.030 70.018 0.083 70.090 0.045 70.017 0.103 70.024 0.056 70.025

0.147 0.10 0.217 0.08 2.20 7 0.71 0.667 0.34 0.137 0.11 0.137 0.07

0.097 70.035 0.112 70.041 0.941 70.450 0.136 70.014 0.219 70.112 0.316 70.031

15.0 7 4.04 68.27 51.8 1447 77 1147 40.2 3677 143 88.8 7 7.59

1.63 7 0.47 2.247 1.42 1.87 7 0.44 7.99 7 1.12 1147 58 9.487 1.04

0.228 70.085 0.065 70.005 0.026 70.003 0.051 70.017 0.117 70.055 0.021 70.014

0.117 0.03 0.26 7 0.02 2.217 0.65 0.337 0.10 0.096 7 0.06 1.32 7 0.08

0.085 70.020 0.107 70.050 0.518 70.258 0.129 70.060 0.423 70.088 0.268 70.053

17.3 7 3.31 1017 4.23 97.7 7 6.51 1207 6.57 1827 43.5 84.5 7 21.5

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