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Heavy metal concentrations in water, sediment, and tissues of two fish species from the Yellow River


Environ Monit Assess DOI 10.1007/s10661-009-0929-2

Heavy metal concentrations in water, sediment, and tissues of two fish species (Triplohysa pappenheimi, Gobio hwanghensis) from the Lanzhou section of the Yellow River, China
Yimin Wang · Peng Chen · Ruina Cui · Wantong Si · Yingmei Zhang · Weihong Ji

Received: 15 January 2009 / Accepted: 18 April 2009 ? Springer Science + Business Media B.V. 2009

Abstract In order to assess the condition of heavy metal pollution in the Yellow River, Lanzhou section, China, and to quantify heavy metal (copper, lead, zinc, and cadmium) contents in tissues (liver, kidney, gills, and muscles) of two ?sh species (Triplophysa pappenheimi and Gobio hwanghensis), levels of these four metals in the water body, sediment, and tissues of the two ?sh were measured using inductively coupled plasmaatomic emission spectrometry. The metal levels from this study were compared with the threshold values in the guidelines of water, sediment, and food given by the National Environmental Protection Agency of China, the National Oceanic and Atmospheric Administration of America, and the National Standards Management Department of China. We found the mean concentrations of Cu, Pb, Zn, and Cd in THE water body, sediment, and muscles of two ?sh species were far below the values in guidelines. We also found that the type of metals present and their concentrations varied in different tissues and species. The results suggested that (1) Cu, Pb, Zn, and Cd did not contaminate the aquatic ecosystem severely and did not threaten the safety of human consumption

in the Yellow River, Lanzhou section, and (2) organs that are sensitive to accumulating heavy metals may be useful to develop bioindicators for monitoring metal contamination. Considering environmental variables, further study is necessary before deciding which ?sh species or tissue could be the ideal bioindicators for aquatic pollution. Keywords Heavy metal · Pollution · Concentration · Fish · Risk assessment

Introduction Heavy metals are natural trace components of the aquatic environment, but background levels have increased due to industrial wastes, agricultural and mining activities (Kalay and Canli 2000). Fluvial environments, which commonly act as dumping systems for pollutants, often receive a variety of contaminants containing heavy metals. Cu, Pb, Zn, and Cd are the most common contaminants in the aquatic environment, and their levels in water, sediment, and organisms are usually monitored. Cu and Zn are essential elements required by a wide variety of enzymes and other cell components and have vital functions in all life. However, over intake of Zn and Cu would cause health problem (Gale et al. 2004). Cd and Pb exhibit

Y. Wang · P. Chen · R. Cui · W. Si · Y. Zhang (B) · W. Ji School of Life Sciences, Lanzhou University, Lanzhou 730000, Gansu, China e-mail: ymzhang@lzu.edu.cn

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extreme toxicity even at trace levels (Fianko et al. 2007; Merian 1991). The Yellow River, one of the largest freshwater ecosystems, is the most important resource of water supply in northern China. It has a length of 5,464 km and a total watershed area of 7.52 × 105 km2 . More than one hundred million people rely on it directly or indirectly. However, the Yellow River has been polluted in the past few decades, even in the upper stream in the Lanzhou region. Recently, people have become increasingly aware of the environmental problems such as the harmful effects of water pollution in the Yellow River. Investigation, routine monitoring, and pollutant management have been performed by the government to improve and maintain the water quality. Many studies have been carried out to evaluate the ecological risks of the polluted water (Huang et al. 2006; Zhang and Zhang 2008). However, so far, in the Lanzhou section, an attempt has not yet been made to evaluate the concentrations of heavy metals in tissues of ?sh species. Fish of higher trophic levels are prone to accumulate metals in their tissues and can cause chronic and acute diseases in humans through the food chain (Terra et al. 2008; Al-Yousuf et al. 2000; Has-Sch?n et al. 2006). Monitoring heavy metal contamination in ?sh tissues may help to assess the health of aquatic ecosystems (Adams 2002). Two dominant endemic ?sh species, Triplophysa pappenheimi and Gobio hwanghensis, both common in the Lanzhou section of the Yellow River, were chosen as a target species for determining the metal levels in tissues of liver, kidney, gill, and muscle. Among these tissues, muscles are usually included in the diet of some local people. Understanding metal accumulation in muscle tissues of these ?sh would contribute to better risk assessment of such food consumption. In the present study, we used the heavy metal threshold values in water quality standard for ?sheries (National Environmental Protection Agency 1989) as a guideline to evaluate Cu, Pb, Zn, and Cd contamination in water. Because sediment quality standards have not been de?ned in the mainland of China so far, the standards of the National Oceanic and Atmospheric Administration (NOAA) of America (Long and Morgan 1990)

were recommended for evaluating the sediment quality in waters (Liu et al. 2005). Safety quali?cations for agricultural products for nonenvironmental pollution aquatic products (National Standards Management Department 2001) de?ned the maximum permitted levels of Cu, Pb, and Cd in the edible parts of ?sh (muscle); we used these levels as standard guidelines to evaluate the quality of ?sh muscle contaminated by heavy metals. The aims of our study were (1) to assess the effect of Cu, Pb, Zn, and Cd on the health of the aquatic ecosystem and (2) to explore the current levels of these metals in ?sh tissues so as to conduct biomonitoring in the future.

Materials and methods Study area and ?sh samples The Lanzhou region, with a population of about three million people, has many pollutantproducing industries, such as oil re?neries and chemical mills. The Lanzhou section of the Yellow River, with a length of 358 km at the upper stream and a total watershed area of 85,369 km2 , acts as the main ef?uence channel of waste water and receives a great amount of contaminants every year. The pollutants include phenols, polycyclic aromatic hydrocarbons (PAHs), oils, and unionized ammonia (NH3 ), and they usually contain heavy metals such as Cu, Pb, Zn, Cd, As, Hg, Cr, and other toxic compounds. Of heavy metals, Cu, Pb, Zn, and Cd could usually be detected in the water body. Because the river has been polluted for a long period of time, since the 1970s, the organisms living in it have inevitably been affected (Huang et al. 2007). The sampling sites were chosen at a mixed polluted area located downstream of the Lanzhou region (35? 54 39 N, 103? 40 26 E). Triplophysa pappenheimi and G. hwanghensis used in the study were caught with ?shing net in the year 2008. Sample preparation The investigation of metal concentration in water and sediment were performed in July, August, and September, 2008. In view of protecting the

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biological resource, ?sh samples were collected only at the end of September. Samples were immediately brought to the Biological Laboratory of Lanzhou University. After anesthetizing with clove oil (in accordance with institutional guidelines for animal welfare), biometric measurements were taken and ?shes were dissected. Tissues of liver, kidney, gill, and muscle were separately weighted and stored at ?20? C. Distilled water was used throughout the procedure to clean the samples. In order to minimize the differences in metal accumulation caused by the age of the individuals, the body weight and length were con?ned at 34.0– 38.3 g and 15.94–17.31 cm for T. pappenheimi and 42.1–46.3 g and 15.19–17.35 cm for G. hwanghensis. Samples used in this analysis were identi?ed as 4–6 years old according to the number of rings on the articular surface of the ?rst vertebral body.

solutions were prepared from stock solutions. Standard reference material mussel (GBW 08571) was used to check the accuracy and precision. The recovery rates were Cu 92.47%, Pb 97.76%, Zn 92.55%, and Cd 90.22%, respectively. The results showed good agreement between the certi?ed and the analytical values. Statistical analyses Heavy metal concentrations were showed in milligrams per liter for water, micrograms per gram of dry weight for sediment, and micrograms per gram of wet weight for ?sh tissues. The statistical analyses were carried out using SPSS 13.0. The results were offered as mean value ± standard deviation. One-way ANOVA and Duncan tests were used to compare the data by species and by tissue. p < 0.05 was considered as statistically signi?cant; p < 0.01 was considered as extremely signi?cant.

Chemical analysis The surface water samples were acidi?ed with nitric acid (0.5%). The samples were then ?ltered through a 0.45-μm micropore membrane ?lter. The sediment samples were dried, passed through a 0.2-mm sieve, and digested with a hydrochloric– nitric acid mixture. Water and sediment samples were then analyzed for Cu, Pb, Zn, and Cd by inductively coupled plasma-atomic emission spectrometry (ICP-AES) (IRIS advantage, Thermo Electro, Waltham, MA, USA) followed the procedure of Wang et al. (2003). Approximately, a 0.2-g sample of muscle and entire liver, kidney, and gill from each ?sh sample was digested based on the procedure of Yang et al. (2007). All samples were analyzed three times for Cu, Pb, Zn, and Cd by ICP-AES. Standard

Results and discussion Heavy metals in ?sh tissues Heavy metals in the aquatic environment can accumulate in ?sh tissues even at very low concentrations; therefore, the measurement can re?ect the exposure effects. Our study showed that the concentrations of different metals varied with species and the type of tissues. Signi?cantly higher metal concentrations of T. pappenheimi occurred ( p < 0.01): Cu in the liver, Pb in liver and kidney, and Cd in kidney. In the case of G. hwanghensis, Cu was found in liver and gill, Pb in liver and

Table 1 The heavy metal concentrations (μg/g wet weight) in tissues of T. pappenheimi (the comparisons of the same metal were made among different tissues) Cu Liver Kidney Gill Muscle F value 22.543 ± 3.406a 1.285 ± 0.176b 1.832 ± 0.373b 1.280 ± 0.262b 300.382? Pb 0.088 ± 0.015a 0.104 ± 0.010a 0.046 ± 0.013b 0.061 ± 0.009b 37.474? Zn 4.734 ± 0.698a 4.882 ± 0.522a 4.645 ± 0.790a 4.327 ± 0.327a 1.183 Cd 0.031 ± 0.004b 0.063 ± 0.008a 0.024 ± 0.005b 0.024 ± 0.003b 109.560?

Different superscript letters mean differences between tissues ? Extremely signi?cant, p < 0.01

Environ Monit Assess Table 2 The heavy metal concentrations (μg/g wet weight) in tissues of G. hwanghensis (the comparisons of the same metal were made among different tissues) Cu Liver Kidney Gill Muscle F value 2.486 ± 0.330a 0.457 ± 0.110c 2.186 ± 0.371a 1.715 ± 0.079b 96.554? Pb 0.117 ± 0.025a 0.140 ± 0.011a 0.002 ± 0.001c 0.059 ± 0.011b 84.517? Zn 6.314 ± 0.535b 5.784 ± 1.275b 32.097 ± 4.949a 5.668 ± 0.372b 206.603? Cd 0.027 ± 0.005b 0.047 ± 0.016a 0.028 ± 0.006b 0.030 ± 0.001b 8.588?

Different superscript letters mean differences between tissues ? Extremely signi?cant, p < 0.01

kidney, and Cd in kidney. The highest concentration of Zn was found in gill of G. hwanghensis, whereas its concentration in the other tissues of both species had no signi?cant difference (Tables 1 and 2). In general, active metabolite organs, such as gill, liver, and kidney, often sensitively accumulate larger amounts of metals than muscle. Different tissues have varied accumulating capacities of metals, which may be due to the different metabolic roles of metals and functions of organs (Ashraf 2005). Moreover, heavy metal concentrations in different ?sh species might be a result of different ecological needs, metabolisms, and feeding patterns (Allen-Gil and Martynov 1995). Triplophysa pappenheimi lives in the torrents and feeds on shrimps, whereas G. hwanghensis lives in the slow-moving water area and feeds on benthic invertebrates. These differences may play an important role in causing the diversity of species and tissues on metal accumulation.

Risk assessment The threshold values given by guidelines mentioned in the “Introduction” and the mean concentrations from this study were summarized in Table 3. In the water body of the Yellow River, the concentrations of metals varied within a range of 0.0015–0.0050 mg/L for Cu, 0.0001–0.02 mg/L for Pb, 0.001–0.022 mg/L for Zn, and 0.0002– 0.0011 mg/L for Cd. The mean concentrations of all metals investigated were under the threshold values given by the guidelines, but the highest levels of Cu and Cd exceeded the threshold values of water quality standards for ?sheries (National Environmental Protection Agency 1989). In the sediment, the highest levels were 19.78 μg/g for Cu, 16.13 μg/g for Pb, 124.79 μg/g for Zn, and 0.586 μg/g for Cd, which were below the threshold values given by the NOAA (Long and Morgan 1990). Metal levels in muscles of ?sh were found

Table 3 Metal concentrations in water, sediment, muscles of two ?sh species and guidelines Cu Guidelines Water Sediment Food This study Water Sediment Muscle of T. pappenheimi Muscle of G. hwanghensis NEPA NOAA ERL NOAA ERM NSMD 0.01 34 270 50 0.0029 ± 0.0014 18.485 ± 0.823 1.280 ± 0.262 1.715 ± 0.079 Pb 0.05 46.7 218 0.5 0.0081 ± 0.0097 16.125 ± 1.437 0.061 ± 0.009 0.085 ± 0.011 Zn 0.1 150 410 Cd 0.005 1.2 9.6 0.1 0.0083 ± 0.0097 0.00045 ± 0.0038 78.531 ± 16.110 0.586 ± 0.198 4.327 ± 0.327 0.024 ± 0.003 5.668 ± 0.372 0.030 ± 0.001

Metal content units are expressed as milligrams per liter of water, micrograms per gram of dry weight of sediment, and micrograms per gram of wet weight of food and ?sh muscles NEPA National Environmental Protection Agency, China (1989); NOAA National Oceanic and Atmospheric Administration, America (Long and Morgan 1990); ERL effects range—low value; ERM effects range—median value; NSMD National Standards Management Department, China (2001)

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to be well below the maximum levels in foods given by the National Standards Management Department of China (2001). The results demonstrated that the Lanzhou section of the Yellow River was not signi?cantly contaminated by Cu, Pb, Zn, and Cd. This assessment, according to our detection of metal levels in the water body, sediment, and tissues, was consistent with the assessment based on a longterm water quality monitoring program (Zhang and Zhang 2008). Nevertheless, the accumulation of heavy metals in liver, kidney, and gill of the two species may result in harmful effects for the ?sh, especially with toxic metals, such as Pb and Cd. Exogenous pesticides, heavy metals, chemical mutagens, radiations, and various stress factors can cause an increase of free radicals and oxidative stress. As a result of increasing these stresses, lipid peroxidation, protein denaturation, and DNA damages may occur in the cells of living organisms. These changes could be a great risk for their life and productivity (Fidan et al. 2008). At the same sampling site, previous studies in our laboratory documented that the toxic pollutants such as PAHs and heavy metals in the polluted water body of the Yellow River could induce obvious oxidative damage (Huang et al. 2006) and cause DNA fragmentation (Long et al. 2006) in the carp Cyprinus carpio. Therefore, it is highly possible that such damages could also have occurred in T. pappenheimi and G. hwanghensis and are worth further investigation.

bioindicators for monitoring metal pollution. However, long-term investigation is necessary before suggesting which ?sh species or tissues could be used as bioindicators for monitoring aquatic contamination.
Acknowledgements The project was supported by the National Natural Science Foundation of China (No. 30770390) and Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, China (No. XJDX02012007-01). The analyses were carried out in the Instrumental Analysis and Research Center of Lanzhou University. The ?sh sample collection was approved by the Fishery Administration Bureau of Gansu Province. We especially thank Pingsheng Wang and Yibing Su for helping us with sample collection and analyses of metal elements in the laboratory.

References
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Conclusions At the Lanzhou section of the Yellow River, the aquatic ecosystem have not been signi?cantly contaminated by Cu, Pb, Zn, and Cd, and metal levels in ?sh muscles were all under the threshold values of the guidelines of the National Standards Management Department. However, the organic contaminants have not been determined in ?sh muscles, so further study is necessary to determine safety for human consumption. The highest Cu, Pb, Zn, and Cd accumulations were found in liver of T. pappenheimi, kidney of G. hwanghensis, gill of G. hwanghensis, and kidney of T. pappenheimi, respectively, which may be useful to develop

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