Illustrated in Figure 1 , the sampling region is situated in the South China Sea, China. The study comprised 20 sites, with the Qiongzhou Strait acting as a natural boundary, assigning 10 sampling sites to both its eastern and western sectors. At each site, marine fish samples were gathered and promptly frozen at –20°C before being transported to the laboratory for subsequent processing. Our research entailed the sampling of 351 wild fish, representing a variety of 31 distinct species.

Each frozen fish sample was dissected and subsequently freeze-dried at –80°C for 96 hours. The moderately dried muscle tissue was then transferred into a 15 mL tube (Corning, USA), with the addition of HNO₃ (Fisher Scientific, Geel, Belgium) to each muscle sample. After digestion, the sample was diluted with ultrapure water to achieve the appropriate concentration for testing. Metal analysis was conducted using inductively coupled plasma-mass spectroscopy (ICP-MS), NexION350X, PerkinElmer, USA. The certified reference material for mussels (GBW08571, China) was chosen as the standard material and analyzed every 20 samples to ensure the reliability of the testing method. The Ar flow rate was set at 0.8 L/min, with identified potential interferences being ArCl, Sm²⁺, Nd²⁺, and Eu²⁺. The detected concentration levels ranged from 0.4 to 50 μg/L to prevent any interference with the equipment. Specific internal standard metal elements were selected to ensure the accuracy of the testing process: ⁷²Ge for As, Se, and Zn; ⁴⁵Sc for Cr, Cu, and Ni; ¹¹⁵In for Cd; and ²⁰⁹Bi for Pb, and the rate of recovery was between 70–130%. Finally, the metal concentration in marine fish muscle was calculated and reported in μg/g dry weight. In further analysis, a wet/dry weight conversion factor of 4 was utilized in the risk assessment. The proportion of inorganic As to total As was estimated as 10%, as per the guidelines provided by the United States Food and Drug Administration in 1993, for the assessment of As’s carcinogenic risk (Zhang and Wang, 2012).

In evaluating the potential risks associated with marine fish consumption, the metal pollution index (MPI), THQ, and total target hazard quotient (TTHQ) were chosen as non-CR indices for heavy metal pollution assessment. The MPI was chosen to characterize the specific levels of various metal pollutants (Hao et al., 2013). The formula was presented as following:

Where, the MPI is the pollution index of heavy metal, C_i is the concentration of heavy metal.

The estimated daily intake (EDI) was chosen to quantify the average metal intake. Both the THQ and TTHQ were utilized to assess non-cancer risks and total non-cancer risks, respectively (Iaquinta et al., 2021; Zhang et al., 2023). The formula was presented as following:

Where, C_i is the concentration of heavy metal; C_consumption is the daily fish consumption in average, assuming that the daily fish consumption being 59.91 g (Biswas et al., 2023); B_w is the body weight of consumer (the average body weight of Chinese people is 61.2 kg) (Zhang et al., 2023). RfD_i is the oral reference dose of heavy metal U. S. Environmental Protection Agency (USEPA, 2024), the Oral RfD_i values are 0.005 mg/kg/day for As, 0.001 mg/kg/day for Cd, 0.003 mg/kg/day for Cr, 0.04 mg/kg/day for Cu, 0.02 mg/kg/day for Ni, 0.0035 mg/kg/day for Pb, 0.005 mg/kg/day for Se, and 0.25 mg/kg/day for Zn.

The CR was chosen to assess the potential risk of carcinogenic exposure when an individual is exposed to carcinogenic heavy metals over a lifetime (Liu et al., 2022). The formula was presented as following:

Where, Cancer Slope Factor (CSF) represents the carcinogenic slope factor for As, Cd, and Pb as provided by USEPA and Office of Environmental Health Hazard Assessment (OEHHA). Specifically, the CSF for inorganic As is determined to be 1.5, estimated from total As detailed in Section 2.2 on Sample Pretreatment and Metal Analysis, 0.38 for Cd, and 0.0085 for Pb, respectively; EDI_i is the estimated intake of As, Cd and Pb mentioned before.

The statistical analysis and graphic presentation of data were conducted using R, which involved the utilization of packages such as xlsx, car, plyr, reshape2, and ggplot2. Specifically, Wilcoxon rank sum test was employed to analyze the variations in heavy metal concentrations among tissues and locations, as well as differences in THQ and CR values. The data were represented as mean ± standard error.

Figure 2 illustrates the concentrations of heavy metals, such as As, Cd, Cr, Cu, Ni, Pb, Se, and Zn in various tissues (gill, intestine, liver, and muscle) of wild marine fish. The average concentrations of all detected heavy metal were notably higher in the gill, intestine, and liver compared to the muscle tissue. These results align with prior studies indicating a tendency for heavy metals to accumulate more prominently in organs like the gill and liver rather than in muscle tissue (Bilgin et al., 2023). The gill and intestine play crucial roles in pollutant influx for marine fish, with the gill serving as the primary site for ion and micro-molecule exchange with seawater, and the intestine responsible for food digestion and nutrient absorption. In Mugilogobius chulae, Cd absorption is primarily mediated through gill and intestine tissues, with gill absorption accounting for 77.2% to 89.4% of waterborne Cd absorption and intestinal absorption contributing to 81.3% to 98.7% of dietary Cd absorption, leading to Cd storage in the fish of 22.8% to 51.6% and 47.1% to 80.4%, respectively (Guo et al., 2019). In addition to Cd, the gill and intestine play crucial roles in the bioaccumulation and distribution of As and Zn in marine fish. These organs serve as key pathways through which marine fish efficiently acquire heavy metals from the marine environment and food chain, utilizing both waterborne and dietary routes (Zhang and Wang, 2006; Zhang et al., 2011). The liver is considered the primary organ for detoxification in marine fish. Metallothionein, a crucial macromolecule found in the liver, plays a key role in binding metals and mitigating the adverse effects of heavy metals (Magnuson and Sandheinrich, 2023; Paylar et al., 2023). The liver exhibited the highest accumulation of heavy metals, with concentrations of Cu and Zn significantly surpassing those found in muscle tissue. This phenomenon may function as a protective mechanism for the organism (Jayasinghe et al., 2024). Therefore, the muscle tissue consistently displayed markedly lower concentrations of heavy metals compared to gill, intestine, and liver tissues.

Muscle tissue is commonly selected as an indicator of metal contamination levels in marine fish due to its role in metal distribution and storage. In our investigation, heavy metal concentrations in the muscle of marine fish were as follows: 6.56 ± 0.628 μg/g for As, 0.170 ± 0.0352 μg/g for Cd, 0.847 ± 0.0681 μg/g for Cr, 3.56 ± 0.222 μg/g for Cu, 5.08 ± 0.494 μg/g for Ni, 0.0700 ± 0.0170 μg/g for Pb, 1.78 ± 0.140 μg/g for Se, and 39.5 ± 1.71 μg/g for Zn ( Table 1 ). The heavy metals were ranked by concentration in the following order: Zn > Ni > As > Cu > Se > Cr > Cd > Pb. Among these, Zn emerged as the predominant heavy metal in marine fish muscle, surpassing Pb by nearly 567-fold. Consistently, Zn concentrations in marine fish muscle were consistently the highest, reaching levels up to 10³ times greater than those of Pb (Zhang and Wang, 2012), aligning with our research findings.

To evaluate geographical variations in pollutant levels within marine fish muscle, the average concentrations of heavy metals were compared between the eastern waters (Wenchang) and the western waters (Wushi), as depicted in Figure 3 . The various heavy metal elements exhibited distinct contamination levels, leading to their classification into two groups based on the observed average concentration differences across the sampling sites. This categorization enables the provision of specific health risk recommendations for the populations residing in these areas. In this study, metals with significant carcinogenic potential, namely As, Cd and Pb, were categorized into group 2, which also encompassed Se due to its association with As. Group 1, composed of the heavy metals Cr, Cu, Ni, and Zn, exhibited higher average levels in Wushi, whereas group 2, consisting of As, Cd, Pb, and Se, displayed elevated concentrations in Wenchang.

It is noteworthy that the heavy metals posing CR (As, Cd, and Pb) were significantly higher in the Wenchang region. The concentrations of metal elements in group 1 were as follows: 1.01 ± 0.101 μg/g in Wushi and 0.712 ± 0.0908 μg/g in Wenchang for Cr, 5.62 ± 0.377 μg/g in Wushi and 1.71 ± 0.154 μg/g in Wenchang for Cu, 10.4 ± 0.873 μg/g in Wushi and 0.333 ± 0.0717 μg/g in Wenchang for Ni, and 58.3 ± 2.55 μg/g in Wushi and 22.6 ± 1.44 μg/g in Wenchang for Zn ( Figure 3 ). Residents in the vicinity of Wushi should exercise increased vigilance regarding these non-carcinogenic heavy metals. Conversely, the concentrations of metal elements in group 2 were 12.2 ± 1.02 μg/g in Wenchang and 0.248 ± 0.00361 μg/g in Wushi for As, 0.277 ± 0.0656 μg/g in Wenchang and 0.0497 ± 0.00504 μg/g in Wushi for Cd, 0.337 ± 0.00202 μg/g in Wenchang and 0.114 ± 0.0373 μg/g in Wushi for Pb, and 3.29 ± 0.211 μg/g in Wenchang and 0.0990 ± 0.00934 μg/g in Wushi for Se ( Figure 3 ). The carcinogenic heavy metals As, Cd, and Pb exhibited similar geographical trends, with higher concentrations in the eastern waters. The As pollution level showed a significant disparity, with marine fish in Wenchang waters accumulating nearly 49 times more As than those in Wushi waters, underscoring the necessity for increased health risk awareness among Wenchang residents. The Pb pollution level also revealed a substantial difference, with the concentration in Wenchang at 0.337 μg/g compared to 0.114 μg/g in Wushi, nearly three times higher. While Cd and Pb displayed similar bioaccumulation patterns to As geographically, the health risks may not differ as significantly as with As. As is particularly concerning due to its potential to impair neuropsychological development and memory, along with its significant CR, particularly for skin and lung carcinoma. It is crucial for residents to refrain from consuming foods contaminated with As (Zhang and Wang, 2012; Zhang et al., 2016; Soler-Blasco et al., 2023; Hua et al., 2024). Therefore, individuals should prioritize monitoring of carcinogenic heavy metals such as As, Cd, and Pb in marine fish in Wenchang.

The variations in heavy metal bioaccumulation among different marine fish muscle are elaborated in Table 1 . As stands out as a critical hazardous metal necessitating immediate and rigorous monitoring. As concentrations in fish muscle spanned from 0.174 to 70.1 μg/g across all species. The highest concentration was not found in the dominant fish species Nemipterus bathybius, Johnius belangerii, and Priacanthus macracanthus, with their respective As concentrations at 6.21 μg/g, 0.234 μg/g, and 18.5 μg/g. Pampus argenteus exhibited the lowest As accumulation, while the benthic fish Uroconger lepturus displayed an exceptionally high As accumulation, approximately 402 times greater, reaching 70.1 μg/g. Remarkably, benthic marine fish like U. lepturus inherently demonstrated a potential for higher As bioaccumulation, consistent with prior research findings. Benthic marine fish that feed on clams showed an increased rate of As biotransformation, likely attributed to the As content in their dietary supplementation (Zhang et al., 2013; Zhang et al., 2017). It is crucial to acknowledge that the bioaccumulation and biomagnification of As have been demonstrated to transfer and accumulate within wild ecosystems through the food chain. This occurrence has been documented in field studies and trophic level analyses, showcasing As magnification in Daya Bay during winter. Benthic invertebrates, in particular, displayed notably elevated concentrations, contributing significantly to As accumulation (Du et al., 2021). The bioaccumulation of As was linked to dietary sources. Studies have shown that the dietary habits of fish notably influenced As bioaccumulation, with carnivorous fish accessing higher levels of As when their diet included more marine animals (Zhang and Wang, 2012; Zhang et al., 2022). In this study, the species with the highest accumulation of As, U. lepturus, is a nearshore benthic warm-water fish that feeds on small fish, shellfish, and other organisms in its natural habitat. The combination of its diet and the environmental conditions of residing in bottom sediments likely contributes to the remarkably elevated As concentration found in its muscle tissue. The benthic carnivorous fish Trypauchen vagina has the ability to accumulate 133.7 μg/g dw of As in its muscle tissue (Zhang and Wang, 2012). Therefore, the public must carefully monitor the issue of As contamination in marine benthic fish.

The Cd concentrations in the muscle tissue of various marine fish species ranged from 0.00556 to 4.86 μg/g ( Table 1 ). Among the key fish species, N. bathybius, J. belangerii, and P. macracanthus exhibited Cd concentrations of 0.0462 μg/g, 0.0368 μg/g, and 0.305 μg/g, respectively. Lutjanus russellii displayed the highest Cd accumulation, while Dendrophysa russelii exhibited the lowest, with a difference of approximately 7 times. The diverse habitats of marine fish play a significant role in their uptake of heavy metals (Guo et al., 2018). Cd has been demonstrated to be absorbed through waterborne sources, diet, and sediment in marine fish. The feeding strategies employed significantly influence the bioaccumulation of Cd (Guo et al., 2015; Guo et al., 2017; Guo et al., 2018). Caution should be exercised in consuming L. russellii to minimize exposure to Cd.

Pb concentrations in fish muscle varied from 0.00909 to 0.358 μg/g across all species ( Table 1 ). In the largest fish group, N. bathybius, J. belangerii, and P. macracanthus, Pb concentrations measured 0.0480 μg/g, 0.0472 μg/g, and 0.201 μg/g, respectively. The highest and lowest Pb concentrations were found in L. russellii and Plectorhinchus argenteus, respectively, exhibiting a 39-fold difference. Human activities, particularly the use of leaded gasoline, influenced the Pb concentration in the marine environment (Nriagu, 2023). It was noted that the Pb concentration in Setipinna tenuifilis in Liaodong Bay, China, could reach up to 0.76 μg/g, whereas the Pb concentration observed in this study was slightly lower (Gao et al., 2021). The discrepancies observed can be attributed to various factors, including geographical variations, specific environmental conditions, and differences in the species under study.

Zn concentrations in fish muscle exhibited significant variability across all species, ranging from 14.1 to 128 μg/g ( Table 1 ). In the predominant fish species group comprising N. bathybius, J. belangerii, and P. macracanthus, Zn concentrations were recorded at 14.1 μg/g, 51.4 μg/g, and 20.9 μg/g, respectively ( Table 1 ). The highest and lowest Zn concentrations were found in Caranx kalla and N. bathybius, respectively, representing a 7-fold difference. Zn pollution in wild marine organisms was most severe in Laizhou Bay, China, with subsequent rankings of Cu, As, Cd, Cr, Ni, and Pb, suggesting that Zn may have a higher tendency for accumulation (Liu et al., 2015). The levels of Zn concentrations in the South China Sea area also warrant significant concern.

Various fish species exhibited differing levels of heavy metal contamination. In addition to marine species, attention should be directed towards species with substantial populations. Among all the species examined, N. bathybius had the largest population, followed by J. belangerii and P. macracanthus, indicating that N. bathybius and J. belangerii were the predominant catches in this study. Notably, the most abundant species, N. bathybius, J. belangerii, and P. macracanthus, did not show significantly high levels of heavy metal bioaccumulation in their muscle tissues, implying that commonly caught species may have lower contamination levels and be safer for consumption. Intriguingly, species with the highest metal accumulation, such as L. russellii for Cd and Pb, U. lepturus for As, and C. kalla for Zn, displayed a similar trend among carnivorous fish. This aligns with previous research indicating the bioaccumulation of heavy metals along the food chain (Lee et al., 2016; Wang and Wang, 2019; Xia et al., 2019). Carnivorous fish, typically consuming diets rich in crustaceans, fish, and zooplankton, are predisposed to accumulating pollutants. For instance, U. lepturus, a predator, tends to favor a diet that enhances trophic richness in marine ecosystems, potentially elucidating its elevated accumulation of specific heavy metals (Chaudhuri et al., 2014). Within this study area, species with substantial populations exhibited lower pollution levels, whereas benthic and carnivorous species showed higher contaminant concentrations.

The 31 fish species displayed varying MPI values, a metric used to compare heavy metal accumulation across different fish species. L. russellii exhibited the highest MPI at 111, followed by Gymnothorax reevesii and Trachurus japonicus with MPIs of 40.6 and 28.2, respectively. These elevated MPI values indicate potential contamination in these species, suggesting a heightened risk of contamination for L. russellii, G. reevesii, and T. japonicus. Apart from these species with exceptionally high MPIs, most species had MPIs below 1. The MPI serves as a direct indicator of heavy metal presence in marine fish, with prior research indicating that demersal fish tend to have higher MPIs than pelagic and mesopelagic fish, and omnivorous fish exhibit higher MPIs compared to carnivorous and herbivorous species (Liu et al., 2022). In this study, the highest MPI was recorded in L. russellii, a species that exhibits characteristics of both a demersal and carnivorous fish.

Figure 4 illustrates the non-CR associated with various heavy metals. Typically, if the THQ is less than 1, there is a low risk of dietary exposure to specific metals; however, if the THQ exceeds 1, there is a high risk of exposure. The average THQ values for metals ranked as follows: THQ_As > THQ_Se > THQ_Cd > THQ_Ni > THQ_Cr > THQ_Zn > THQ_Cu > THQ_Pb. Notably, the average THQ for As was notably high at 0.308, indicating a significant non-CR associated with this metal. Specifically, U. lepturus exhibited an exceptionally high THQ_As of 3.43 ( Figure 5 ), indicating a significant bioaccumulation of As as mentioned earlier. The average THQ values for other metals were below 0.1, suggesting a lower non-CR compared to As. While previous studies have shown minimal health risks associated with the consumption of marine fish species and deemed them generally safe (Zhang and Wang, 2012; Zhang et al., 2016). Therefore, the significant health risk associated with U. lepturus warrants attention.

Figure 5 presents the TTHQ for each species. U. lepturus exhibited the highest TTHQ value of 3.64, with the THQ of As accounting for 94.3% of this elevated TTHQ. Conversely, D. russelii, Rastrelliger kanagurta, and Pennahia pawak exhibited the lowest TTHQ values, measuring 0.196, 0.242, and 0.257, respectively. It is recommended that local consumers prioritize D. russelii, P. argenteus, and R. kanagurta for their daily fish protein intake because of their lower TTHQ values. Figure 6 illustrates the varying contributions of TTHQ by different heavy metals and fish species. As accounted for 44.4% of the TTHQ, while the contributions of other metals were all below 13%. This observation highlights As as the primary potential health risk in Qiongzhou Strait. In the TTHQ calculation, U. lepturus, L. russellii, and Upeneus bensasi accounted for 17.0%, 7.67%, and 6.20% of the total, respectively. Overall, the consumption of fish presents a limited non-carcinogenic health threat to local residents. However, consumers should be cautious in avoiding As pollutants and fish species with elevated TTHQ values mentioned like U. lepturus and U. bensasi.

Considering the carcinogenic properties of heavy metals such as As, Cd, and Pb, the potential CR associated with fish consumption emerges as a paramount concern in this context. As depicted in Figure 7 , the CR for Pb, as indicated by CR_Pb values ranging from 1.89 × 10^–8 to 7.44 × 10^–7, suggests a relatively low risk associated with the consumption of marine fish. Most CR_Cd values fell between 10^–6 and 10^–4, except for one outlier at 4.52 × 10^–4. However, CR_As values ranged from 6.40 × 10^–6 to 2.57×10^–3, emphasizing the need for consumers to be cautious in selecting marine fish species with lower risk profiles. The average CR values were ranked as CR_As > CR_Cd > CR_Pb, highlighting the significantly higher CR of As compared to Cd and Pb. Traditionally, a CR below 10^–6 is considered safe, while a CR between 10^–4 and 10^–6 is deemed acceptable with limited damage; anything above 10^–3 is considered unacceptable (Aendo et al., 2019; Liu et al., 2022). In this study, the CR_Pb was the lowest, indicating safety, while the CR_Cd suggested limited damage from Cd. However, the high CR_As values, especially exemplified by U. lepturus with a CR_As of 2.57×10^–3 due to its elevated As contamination, underscore the need for caution when consuming certain fish species. Local residents should avoid consuming U. lepturus and consider P. argenteus as a seafood source due to its lowest CR_As and CR_Pb values among all marine species.