Assessment of Heavy Metal Pollution in the Water, Sediment and Fish during a Complete Breeding Cycle in the Pond of the Pearl River Delta, China

The paper aimed to investigate the concentration variations and evaluate the bioaccumulation as well as the health risk of Cr, Ni, Cu, Zn, As, Cd and Pb in the aquaculture pond ecosystem during a complete breeding cycle. The samples of water, sediment and aquatic organisms were collected from the pond of gull island in the Pearl River Delta, China. In the breeding cycle, the results revealed the metal concentration in the water increased, while the sediment metal concentration showed no significant difference. The heavy metal concentrations in the water were higher than the background values (December 2017) which related to the input of feeds. Sediment metal concentrations (Cr, Ni, Cu, Zn, As and Cd) in the sediment were higher than the background values of Guangdong Province, China, indicating these metal pollutions came from anthropogenic activities. While the concentration of Pb was comparable to the background value, implying that the Pb was mainly from the earth crust. In addition, various metals showed different affinity to fish organs (muscle, skin, bladder, gill, heart, kidney and liver). Zinc was abundant in skin, while As and Cd concentrations were highest in kidneys; Cu was accumulated highest in liver; Cr concentrations was highest in hearts; and Ni was mainly found in bladders, and the Pb was most commonly found in gills. The distribution of heavy metals in the tissues organs was in the sequence of: Zn > Cu > Cr > Ni > Pb > As > Cd. As the fish ages, the Cu and Zn concentration How to cite this paper: Mao, B.J., Huang, Z.W., Zeng, F.T., Du, H.W., Fang, H.Y., Lin, S., Zhang, Y.Y. and Shi, L. (2020) Assessment of Heavy Metal Pollution in the Water, Sediment and Fish during a Complete Breeding Cycle in the Pond of the Pearl River Delta, China. Journal of Environmental Protection, 11, 509-530. https://doi.org/10.4236/jep.2020.116030 Received: May 2, 2020 Accepted: June 25, 2020 Published: June 28, 2020 Copyright © 2020 by author(s) and Scientific Research Publishing Inc. This work is licensed under the Creative Commons Attribution International License (CC BY 4.0). http://creativecommons.org/licenses/by/4.0/ Open Access


Introduction
In recent decades, with the increase of significant population and rapid industrialization, the Pearl River Delta (PRD) has undergone rapid economic development. Heavy metals pollution caused by anthropogenic activities has been reported in various studies [1] [2] [3]. In PRD region, river water is still used to fill up the fish ponds by most of the fish farmers [4]. Heavy metals may enter fish ponds through the sewage outfalls, industrial runoff and atmospheric deposition. Moreover, the fish feeds have been regarded as the main sources of some metals to aquaculture environment [5]. Metal contamination in water, sediment and aquatic organisms has attracted widely attention due to their toxicity, persistence, bioaccumulation and biomagnification [6]. If the concentration of the metal accumulating in fish tissues was higher than the permissible maximum value, an adverse health risk will generate.
Metals contamination in the PRD is focused on offshore aquaculture [7] [8], but little information about fresh water fishs pond environments [1]. In addition, muscle was the major organs analyzed in most studies [9] [10] comparatively; there is less research on other fish organs. This is the first study to analyze the variations of metals concentration in the water, sediments and tissue organs (muscle, skin, bladder, gill, heart, kidney and liver) during a complete breeding cycle. To investigate the transformation and bioaccumulation of metals in those tissue organs in the breeding time, this information will be helpful for fisheries management in freshwater fish pond environment. Therefore, this study was presented to address the above-mentioned issue, and the objective was to: 1) investigate the 7 metal levels in water, sediments and various fish tissue organs during a complete breeding cycle; 2) assess the pollution levels and potential ecological risk of heavy meals in sediments; 3) estimate the transfer, bioaccumulation and human health risk.

Field Sampling
A total of 108 surface water, feeds and sediment samples were collected in triplicate, as well as 46 fish samples were obtained from the pond in gull island, China

Data Analysis
The concentrations of heavy metals were presented on a dry weight (dw) as mg·kg −1 . For comparison, the wet weight (ww) converted to dw with a conversion rate of 20% (assuming water content of 80%) [14]. Statistical analysis was performed using SPSS 22.0 software and EXCEL 2007. The sampling map was drawn by ArcMap 10.2. The Geoaccumulation index (I geo ), metal pollution index (MPI), bioaccumulation factor (BCF), biota-sediment accumulation factor (BSAF) and the metal concentrations in tissues were performed using SigmaPlot 10.0.

Risk Assessment Methods
The geoaccumulation index (I geo ) was applied to assess the concentrations of heavy metals in sediments [15] and expressed as Equation (1): where C n is the measured content of metal n in sediments, B n is the background value of metal n in sediments. The constant 1.5 performs the potential variation about the baseline date caused by lithogenic effects [15]. for Cd and 36 mg·kg −1 for Pb [16]. The lists of 7 grades of I geo are shown in Table   S2.
The Potential ecological risk index was established by [17] to assess the heavy metals ecological risks in sediment (E i ) and comprehensive heavy metals ecological risks in sediment (RI), which could be calculated with the following Equa- where C i and S i are the measured and background concentrations of metal i, as well as T i is the toxicity factor of metal i (Cr = 2, Ni = Cu = Pb = 5, Zn = 1, As = 10 and Cd = 30) [18]. The E i and RI classification are presented in Table S3.
The metal pollution index (MPI) was used to compare the metal concentration in different tissues [19] and Equation (4) was: where C i are the average concentrations of metal i in tissues (dw, mg·kg −1 ).
Bioaccumulation factor (BCF) is to assess by the ratio between metal concentration in the fish organs and those in the water, while the biota-sediment accumulation (BSAF) is to assess by the ratio between metal concentration in the fish organs and those in the sediment [10]. The calculated Equations (5)-(6) are: where C fish , C water and C sediment are the metal concentration in the fish tissue, water and sediment. The grades of BCF values are: less probability of accumulation (BCF < 1000); bioaccumulative (1000 < BCF <5000); highly bioaccumulative (5000 < BCF). As for BASF, if the value > 1, it suggests metal in fish tissue can accumulate from the sediment.
Health risk of metal in fishes was assessed by estimation of daily intake (EDI), target hazard quotient (THQ), hazard index (HI) and carcinogenic risk (CR), which were calculated with the following Equations (7)

Metal Concentrations in the Water
The heavy metal concentrations in the pond water during a complete breeding cycle are given in Table S4. The mean metals concentrations were in the order of Zn > Cu > As > Ni > Pb > Cr > Cd. The concentration of Zn (48.7 ± 21.9 μg·L −1 ) and Cu (5.72 ± 4.71 μg·L −1 ) in the water were relatively high, which was consistent with the result from Wen-Rui Tang River [26]. Additionally, the Zn and Cu concentrations in this pond water were higher than the Pearl River [27], which might due to the input of enriched Zn and Cu feeds (Table S5). The concentrations of heavy metals in the pond water were increased in June 2018 than in December 2017, which could be explained that the fish feeds were the major sources of metals to aquaculture [5]. The higher metal concentrations were observed in March 2018, which might be related to the increased feed remains in the water. In comparison to the fisheries standard of China [28], concentrations of metals in the pond water did not exceed the permissible values. The result indicated that the pond water quality was suitable for farming. According to the classification criteria of contamination degree (CD) [29] which was used to assess the heavy metal pollution in water, the calculated results showed that heavy metals in the water showed low pollution (CD < 6).

Sediment Metals Concentrations
The metals concentrations analyzed in the fish pond sediments are presented in Table S6. There were no significant differences (P > 0.05) among the heavy metals during the complete breeding cycle. The average metals concentrations in the pond sediments decreased in the order of Zn > Cr > Pb > As > Cu > Ni > Cd.

Occurrence of Heavy Meals in Fish
The concentrations of heavy metals in tissue organs during a complete breeding cycle are depicted in Table S7 and Figure 2. Average values of heavy metals in the muscle are shown in Table 1. Zinc had the highest concentration in tissue organs, followed by Cu, Cr, Ni, Pb, As and Cd.  Zinc is the essential metal to promote metabolism and its shortage can result in some adverse influences, i.e. retarded growth, dysfunction of the immune system and appetite loss [30]. The Zn concentration was the highest compared to target metals analyzed in different tissue. During the breeding cycle, the highest Zn concentration (259 ± 20.5 mg·kg −1 , dw) was observed in the skin (May 2018) and the lowest Zn value (18.6 ± 3.79 mg·kg −1 , dw) was found in the muscle (January 2018). The accumulation sequence of mean Zn concentrations in all the organs with an order is skin > kidney > gill > heart > liver > bladder > muscle.
The skin is the main organ which accumulated higher Zn concentration com- age Zn concentration in this study was higher than those reported studies [19] [32]- [38], but lower than this reported study [10].
Copper is the essential metal to form the hemoglobin and some requisite enzymes, but excess intake of Cu can alter the liver and kidney function [39]. in the sequence of: liver > heart > kidney > gill > bladder > muscle > skin. The highest Cu value was found in the liver which was in agreement with the study [40]. The acceptable limit of 8 mg·kg −1 dw for Cu was developed by European Commission [41]. It was worth noting that the mean Cu concentration in the muscle was far higher than those recorded values [19] [32]- [38], but lower than the accorded value [10].
Chromium is regarded as being involved in the metabolism of carbohydrates and lipids [42]. If the intake of Cr is not enough, the risks of cardiovascular diseases and diabetes will be increased [43]. Lead is a non-essential element and can cause adverse health effects (neurotoxicity and nephrotoxicity) [47]. The highest Pb content was detected in the gill (1.40 ± 0.14 mg·kg −1 , dw) in December 2017, while the lowest content was detected in the liver (0.003 ± 0.001 mg·kg −1 , dw) in June 2018. There were significant differences in Pb concentrations among different fish organs (P < 0.05). No Pb concentrations were detected in the muscle. The following decreasing order of mean Pb content in organs was found: gill > kidney > heart ≈ bladder ≈ skin > liver. The average Pb concentration in the muscle did not exceed the maximum levels set by [45], as well as lower than those reported studies [10] [32]- [38].
Arsenic is an ubiquitous in the environment and may be potentially a toxic metal. The highest concentration of As was detected in the kidney (0.13 ± 0.01 mg·kg −1 , dw) in June 2018, whereas the lowest concentration was detected in the bladder (0.02 ± 0.01 mg·kg −1 , dw) in April 2018. The As concentrations were not detected in all the target organs from December 2017 to January 2018. In addition, the distribution of As in each organ is relatively balanced compared to other target metals. The mean As concentrations in organs could be sequenced as follows: gill ≈ kidney > muscle ≈ skin ≈ heart ≈ liver > bladder. The mean As concentration in the muscle was far lower than the regulated value by [41].  centrations were observed in the order of kidney > liver > gill > heart ≈ bladder > skin. The average Cd concentration was lower than the maximum level set by [45], as well as those reported studies [10] [19] [32]- [38].

Metal Pollution Index
The MPI can be visually used to indicate the degree of metal pollution in fish tissues. The calculated MPI results in different tissues during a complete breeding cycle are shown in Figure 3. The highest MPI value was observed in the gill (1.00), while the lowest value found in the liver (0.004). It was worth noting that the highest and lowest MPI values in all the tissues occurred in March 2018 and December 2017, except that the muscle showed the highest MPI value in May 2018 and the skin found the lowest MPI value in January 2018. The average MPI value in tissues was as follows: gill (0.39) > kidney (0.34) > heart (0.15) > bladder (0.13) > skin (0.11) > liver (0.10) > muscle (0.03). The gill and kidney had higher metal pollution compared with other target tissues, which was consistent with the previous study [25]. One way for the metal to enter the fish is through the breath of the gill, and the mucus in the gill can easily absorb metal ions or metal-containing suspensions, etc., and the kidney is the detoxification center of active metabolism of the organism, so the MPI values of the gill and kidney will be higher than other tissues.

Bioaccumulation Factor and Biota-Sediment Accumulation of Heavy Metals in Organisms
The BCF is used to assess the ability of the aquatic organism to accumulate metals from the water. If BCF > 1000, it implies that the organism has a potential to accumulate the metals, and vice versa. The calculated BCF values are presented in Figure 4(a). The highest BCF value was found for Cd (in the kidney), while the lowest value was observed for As (in the bladder). The BCF values of metals in the grasp carp were generally in the order of Zn > Cu > Cd > Cr > Ni > Pb > As. The BCF values of Cu and Zn (essential metals) were higher than Cr, Ni, As, Cd and Pb (non-essential elements), implying that a more important transfer of essential elements than non-essential elements which was inconsistent with previous research [48]. The BSAF is depicted to evaluate the ability of the aquatic organism to accumulate metals from the sediment and the results are shown in Figure 4(b). If BASF > 1, it reflects that the organisms can probably accumulate metals. Among all the metals, only Zn had the value of BASF > 1 in the skin, this result indicated that the skin could accumulate Zn from the sediment. Probably because grass carp mainly live in the lower layer of the water environment enriched with a higher Zn concentration.

Health Risk Assessment
The values of EDI for target metals are shown in Table S9. The EDI of all the metals during the breeding cycle was far less than the PTDI, indicating that the exposure risk of heavy metals through the fish consumption within the safe range.   The calculated values of THQ, HI and CR are given in that there was non-carcinogenic risk associated with intake of multiple metals through the consumption of grasp carps. In general, when the CR value is less than 10 −6 , it is considered that the carcinogenic risk can be negligible; when the CR value is higher than 10 −4 , the carcinogenic risk is unacceptable; when the value of CR is between 10 −6 and 10 −4 , the carcinogenic risk is considered to be acceptable [49]. In Table S10

Conclusion
The  Chinese water quality standard for fisheries (GB11607-89) [28]. b Means data are not detected.