Bioaccumulation of Heavy Metals in the Water, Sediment, and Organisms from The Sea Ranching Areas of Haizhou Bay in China

: Heavy metals (HMs) have the characteristics of high toxicity, long residual time, and difﬁcult degradation, which pose a potential threat to aquatic ecosystems. The distribution and migration of HMs in different media can reﬂect their potential impact on aquatic ecosystem health. In this study, we analyzed the distribution characteristics of seven HMs (Zn, Cu, Cr, Ni, Hg, As, and Pb) in the water and sediment and ﬁve groups of organisms (ﬁsh, Crustacean, cephalopod, bivalvia, and gastropoda) in the sea ranching area of Haizhou Bay and explored the regularity of HM accumulation from water and sediments to organisms. The results showed that in the water, Zn and Hg had the smallest concentrations in the nearshore area, Cr had the lowest concentrations in the offshore area, and As, Cu, Pb, and Ni had the lowest concentrations in the central area. In the sediment, Hg had the smallest concentrations in the nearshore area and As, Pb, Cr, Cu, Ni, and Zn had the lowest concentrations in the offshore area; the average contents of seven heavy metals all meet the Class I standard of sediments in China. The concentrations of Cu and Zn in crustaceans were signiﬁcantly higher than those in ﬁshes ( p < 0.05), and As showed a higher enrichment effect in cephalopods. Under the inﬂuence of feeding habits and habitat environment, the BAF value of benthic crustaceans and bivalvia accumulated HMs from sediments is high, and the BAF value of ﬁsh accumulated HMs from water and sediments is low. Overall, the concentration of HMs in water is high, and HMs in sediments are in good condition, crustaceans and bivalviaa have a strong ability to accumulate HMs from water and sediments, while ﬁsh are weak. Therefore, in order to ensure the safety of biological quality, it is necessary to focus on the discharge of heavy metal pollutants near the coast in the future.


Introduction
Heavy metals (HMs) are environmental pollutants characterized by high toxicity, long detention time, and resistant degradation that are crucial in regulating aquatic ecosystems and are potentially hazardous to animals [1][2][3][4][5][6].In recent years, HM pollution within the marine ecosystem generated by human activities and industries has continuously entered the ocean by atmospheric deposition, surface runoff, etc., causing a severe threat to the offshore environment [7][8][9].These HMs adsorb and settle into sediments through a series of physical and chemical reactions and then return to the water column in the form of a dissolved state through complex hydrodynamic action, thereby causing persistent pollution to the marine environment and great harm to marine organisms [5,10,11].Moreover, the strong fat solubility of HMs makes them not decompose and transform once they enter the tissues or organs of aquatic organisms [10,12,13].This effect will also constantly be retained in environmental media and accumulate in aquatic organisms, and, consequently, the HMs will be transmitted to humans through the food chain [3,14,15].Even though the analysis of HMs in aquatic environment is essential for assessment, it is often necessary to combine HMs in organisms to determine the pollution degree of a sea area more comprehensively and systematically [14][15][16].Recently, HM bioaccumulation and biomagnification in marine organisms has been considered a major issue and aroused the interest of a large number of researchers [10,[17][18][19][20].In contaminated marine ecosystems, high-concentration exposure to metals will force marine organisms to absorb some HMs from the immediate environment [16,21].HMs can be excreted via the gills, bile (via faeces), kidneys, and skin of organisms [22], which not only affects organ functioning but also changes their taste and smell [15].In addition, specific environmental and biological factors are responsive to the uptake of HMs, which also results in varied bioaccumulation between organisms, seasons, and locations [10,23].
Haizhou Bay is located on the coast of the Yellow Sea northeast of Lianyungang city, Jiangsu Province, with a coastline of more than 170 km.Since 2003, the marine protected areas (MPAs) dominated by artificial reefs were constructed by local government, with a total scale of 291,161.2m 3 and an area of 178.25 km 2 , for the purpose of ecological restoration and resource conservation [24][25][26].Most of the earlier studies concentrated on the quantification and characterization of HMs in the water column and sediment in this region [27][28][29], while studies of HM bioaccumulation and biomagnification are scarce and could not provide better feedback.
Therefore, the characteristics of HM concentrations and distributions in the water, sediment, and commercial organisms in the sea ranching areas of Haizhou Bay were determined in this study, and basic information on the HMs accumulated in the organisms from the water and sediment was established.Our research will provide some scientific points and a theoretical reference for offshore ecological restoration projects to further assess the potential risk of HMs in this region.

Description of the Study Area
Haizhou Bay, which is located on the west coast of China Lianyungang city, Jiangsu Province, is an open bay with an area of approximately 877 km 2 and mainly composed of sandy and muddy habitats [30,31].The tides in the coastal waters of Haizhou Bay belong to regular semi-diurnal tides, and the high tide velocity is higher than the low tide velocity.The rising tide flow direction is southwest, and the ebb tide flow is northeast.The coastal waters are dominated by a circulating current, and the coastal waters are dominated by a counterclockwise rotating current [32].In recent years, as the development of coastal areas in Jiangsu Province becomes a national strategy, Ganyu Port Area has been built in an all-round way, and traditional industries such as marine fishery, marine transportation, and marine salt industry have developed rapidly.At the same time, the construction of several port-adjacent industrial parks has made the manufacturing industry, energy development, biopharmaceuticals, and other emerging industries continue to grow [27,33].A large amount of domestic sewage, agricultural and fishery wastewater, and industrial wastewater containing heavy metals is discharged into Haizhou Bay through Linhong River, which has caused serious coastal environmental pressure in this area [28,29,34].

Sample Collection
The survey was conducted (34  1).A plastic hydrophore was used to collect 2 L of surface water samples, and a dredger was used for the surface sediment samples.The organisms were trawled using single-ship winged bottom trawl (specification 40 m × 94 m/49.3 m), with an average towing speed of 3.0 kn and towing time of nearly 1 h.The organism samples were identified as species (species that could not be identified were listed) and sent back to the laboratory for further measurement (Table 1).
search Institute, and in accordance with the Marine Monitoring Code (State Oceanic Administration, 2007) (Figure 1).A plastic hydrophore was used to collect 2 L of surface water samples, and a dredger was used for the surface sediment samples.The organisms were trawled using single-ship winged bottom trawl (specification 40 m × 94 m/49.3 m), with an average towing speed of 3.0 kn and towing time of nearly 1 h.The organism samples were identified as species (species that could not be identified were listed) and sent back to the laboratory for further measurement (Table 1).

Sample Treatment and Analysis
Water samples: 50 mL water sample was filtered using a 0.45 µm fiber filter and stored in 50 mL polypropylene bottles.The filtered water samples were analyzed using inductively coupled plasma mass spectrometry (PerkinElmer, Elan DRC-e, Waltham, MA, USA) for determining HMs.According to the standard of 26 metal element mixed solutions (GNM-M261674-2013, Zhongchangyanbiao technology, Wuhan, China), a total of 7 HMs (zinc (Zn), copper (Cu), chromium (Cr), nickel (Ni), mercury (Hg), lead (Pb), and arsenic (As)) were detected.
Sediment sample: After being freeze-dried, the sediment samples were grounded to 100 mesh powder using agate mortar.First, 0.5 g (dry weight) of sample was weighed into the digestion tank with 20 mL HNO 3 (ultra-pure, Merck, Germany) and 5 mL HCl (ultra-pure, Merck, Darmstadt, Germany) added.An MDS-6 (CEM Mars 6, Matthews, NC, USA) microwave digestion system was used for digestion (the digestion temperature was set to 120 • C for 10 min and kept at 180 • C for 10 min).The digestion solution was placed on a constant temperature electric heating plate to drive acid for clarification and transferred to a 50 mL volumetric flask.Then, the digestion tank was washed using ultrapure water (18.2MΩ cm −2 ) which was filtered using a 0.45 µm fiber filter.Finally, the filtered solution was analyzed using inductively coupled plasma mass spectrometry (PerkinElmer, Elan DRC-e, Waltham, MA, USA) for HM concentration analysis.
Organism sample: ultrapure water (18.2MΩ cm −2 Milli-Q water, Millipore) was repeatedly used to remove impurities, and the species were identified and dissected.A total of 2 g (dry weight) of muscle tissue freeze-dried in the lyophilizer was collected for HM analysis.The muscles below the first dorsal fin of fish, the abdominal muscles of shrimp, the first cheliped of crabs, the mantle of cephalopods, the abdominal foot of Gastropodas, and the adductor muscle of bivalvia were taken.First, 0.1 g of sample was weighed into the digestion tank with 4 mL HNO 3 (ultra-pure, Merck, Darmstadt, Germany) and 1 mL H 2 O 2 (ultra-pure, Merck, Darmstadt, Germany) added.An MDS-6 (CEM Mars 6, Matthews, NC, USA) microwave digestion system was used for digestion (the digestion temperature was set to 120 • C for 10 min and kept at 180 • C for 10 min).The next process is the same as the sediment sample.

Bioaccumulation Factor
The bioaccumulation factor (BAF) was used to standardize the variability contributed by the capture site and thus to compare the levels of metal accumulation among all the species collected.The BAF values are calculated as the ratio between the element concentration in organisms at a steady state (µg/g, dry weight) and the element concentration in the water (µg/L) or sediments (mg/kg) [35,36]; the dry weight of sediment and organism samples is 80% of the original weight.It was calculated according to the following equation: BAF = Metal conc. in the organism Metal conc. in the water or sediments "Metal concentration in the organism" means the average concentration of a metallic element in a given aquatic species; "metal concentration in the water or sediment" means the concentration of a metallic element in a given site of the study area.

Quality Control and Statistical Analysis
The quality of sample processing and analysis were controlled by reagent blank for the duplicate sample and standard reference sample.Ultra-pure water is used as reagent blank, and standard reference material (GBW080040 for water, GBW07456 for sediment, GBW10050 for Organism) from the Center of National Standard Reference Material of China was used to verify the accuracy of the analysis using the same procedures as that for the samples.The recoveries of all elements were between 90% and 110%, ensuring the reliability and consistency of the measurement.To examine the repeatability of the metal concentration, 10% of the sample was analyzed three times, with relative standard deviation (RSD) between 0.05% and 2.5%; moreover, the quality control analysis was performed with 10 samples as intervals.The concentrations of HMs in all samples were higher than the detection limit of the method (Table 2).
The one-sample Kolmogorov-Wallis (KeS) test was used to assess the data normality.All the values meet the assumptions of normality and homogeneity of variance.Analysis of variance (ANOVA) and Kruskal-Wallis tests were used to analyze HM accumulation, as well as BAF values, in different groups with statistical significance at p < 0.05.All the data were analyzed using Excel 2021 and SPSS 26.0.

The Distribution of HMs in the Water and Sediments
The distribution of HMs in the water and sediments is shown in Figure 2. In the water, the concentrations of Zn and Hg were higher in the coastal area and lower in the near shore, and the concentrations of Cr showed the opposite trend.The concentrations of As and Pb in the central area were higher and in the surrounding area were lower.The concentrations of Cu and Ni in the central area were lower.The concentrations of As are (12.2µg/L), Cr (11.4 µg/L), Cu (12.0 µg/L), Hg (0.054 µg/L), Pb (11.4 µg/L), Ni (5.2 µg/L), and Zn (57.2 µg/L) for water.In the sediments, the distribution patterns of these HMs were different to some extent.The concentrations of As, Pb, Cr, Cu, Ni, and Zn in the sediment were higher in the coastal area and lower in the near shore.The distribution of the Hg concentration was rather the opposite and totally different compared to other HMs.The concentrations of As are (17.45mg/kg), Cr (52.36 mg/kg), Cu (24.93 mg/kg), Hg (0.0156 mg/kg), Pb (33.63 mg/kg), Ni (31.16 mg/kg), and Zn (78.53 mg/kg) for sediment.

The Concentration of HMs in Different Groups
The distribution of HMs in different aquatic biota (fish, crustaceans, cephalopods, Bivalvia, and gastropodas) in the sea ranching area of Haizhou Bay is shown in Figure 3 and Appendix C. As, Hg, and Zn were detected in all organisms, while Cu, Ni, and Pb were not detected in Lateolabrax japonicus.Pb was not detected in Larimichthys polyactis, Engraulis japonicus, and L. japonicus of fish, A. chinensis of crustaceans, Sepiella maindroni of cephalopods, and Rapana venosa of gastropodas.
The average As concentration of cephalopods and gastropoda was significantly higher than that of fish (p < 0.05) (Figure 3), and the concentration of As was the highest in Neptunea cumingi (151.33 µg/g) and lowest in L. polyactis (1.10 µg/g).The average Cu concentrations of bivalvia, cephalopods, and gastropoda were significantly higher than that of fish (p < 0.05), with the highest concentration of Cu (257.63 µg/g) found in O. denselamellosa.The average Zn concentration of bivalvia and crustaceans was significantly higher than that of fish (p < 0.05), with the highest concentration (2529.50µg/g) observed in O. denselamellosa and the lowest concentration (24.80 µg/g) in Sebastes schlegelii.Additionally, there were no significant differences in the Cr, Hg, Ni, and Pb concentrations between groups (p > 0.05), among which the highest concentration of Cr (7.93 µg/g) was observed in O. denselamellosa, the highest Hg concentration (1.389 µg/g) was observed in Octopus ocellatus, and the highest Ni concentration was observed in both O. ocellatus (2.13 µg/g) and O. denselamellosa (2.13 µg/g).

Bio-Water and Bio-Sediment Accumulation Factors
The bio-water accumulation factors (BAFs) of different aquatic groups for six HMs are shown in Figure 4.In terms of As, the average BAF of cephalopods and gastropoda was significantly higher than that of fish (p < 0.05).The average BAF for Cu of bivalvia, cephalopods, and gastropoda was significantly higher than that of fish (p < 0.05).Cephalopods and gastropoda can accumulate more As and Cu from water, whereas bivalvia can accumulate more Cu from water.The average BAF values for Hg of several groups were higher, ranging from 10,000 to 25,000, but there was no significant difference between groups (p > 0.05).Similarly, there was no significant difference in the average BAF of Ni and Pb among the different groups (p > 0.05).For Zn, the BAF of bivalvia and crustaceans was significantly higher than that of fish (p < 0.05).

Bio-Water and Bio-Sediment Accumulation Factors
The bio-water accumulation factors (BAFs) of different aquatic groups for six HMs are shown in Figure 4.In terms of As, the average BAF of cephalopods and gastropoda was significantly higher than that of fish (p < 0.05).The average BAF for Cu of bivalvia, cephalopods, and gastropoda was significantly higher than that of fish (p < 0.05).Cephalopods and gastropoda can accumulate more As and Cu from water, whereas bivalvia can accumulate more Cu from water.The average BAF values for Hg of several groups were higher, ranging from 10,000 to 25,000, but there was no significant difference between groups (p > 0.05).Similarly, there was no significant difference in the average BAF of Ni was significantly higher than that of fish (p < 0.05).The average BAF for Cu of bivalvia, cephalopods, and gastropoda was significantly higher than that of fish (p < 0.05).Cephalopods and gastropoda can accumulate more As and Cu from water, whereas bivalvia can accumulate more Cu from water.The average BAF values for Hg of several groups were higher, ranging from 10,000 to 25,000, but there was no significant difference between groups (p > 0.05).Similarly, there was no significant difference in the average BAF of Ni and Pb among the different groups (p > 0.05).For Zn, the BAF of bivalvia and crustaceans was significantly higher than that of fish (p < 0.05).The bio-sediment accumulation factors (BAF) of different aquatic groups for seven HMs are shown in Figure 5.In terms of As, the average BAF in fish was significantly lower than that in cephalopods and gastropoda (p < 0.05).The average BAF for Cu of bivalvia, cephalopods, and gastropoda was significantly higher than that of fish (p < 0.05).Compared with other HMs, the average BAF for Hg, Cr, Ni, and Pb showed no significant difference between the different groups (p > 0.05), even though they appeared to vary widely, as shown in Figure 5.For Zn, the average BAF of bivalvia was the highest (17,959), The bio-sediment accumulation factors (BAF) of different aquatic groups for seven HMs are shown in Figure 5.In terms of As, the average BAF in fish was significantly lower than that in cephalopods and gastropoda (p < 0.05).The average BAF for Cu of bivalvia, cephalopods, and gastropoda was significantly higher than that of fish (p < 0.05).Compared with other HMs, the average BAF for Hg, Cr, Ni, and Pb showed no significant difference between the different groups (p > 0.05), even though they appeared to vary widely, as shown in Figure 5.For Zn, the average BAF of bivalvia was the highest (17,959), which was significantly higher than that of the other groups (p < 0.05).Cephalopods and gastropoda can accumulate more As and Cu from sediment, whereas bivalvia can accumulation more Cu and Zn from sediment.

Characteristics of HMs in the Water and Sediments
Under the influence of various complex factors (e.g., seasonal variation, geograp location, environmental conditions, and hydrodynamics), the distribution pattern HMs in different regions show great differences [37].Compared with five kinds of h metals in the water of the study area investigated in 2009 [38], it was found that th content showed a decreasing trend, while the Pb, Cu, Zn, and Cr content showed a creasing trend.Compared with other typical sea areas in China during the same pe the Hg concentration in Haizhou Bay was lower compared to that in Bohai Bay and River Estuary, and the concentrations of Pb, Cu, Zn, Cr, As, and Ni were higher comp to those in Bohai Bay, Yangtze River Estuary, and Pearl River Estuary, which indicates the HM concentration in the study area was high (Table 3).

Characteristics of HMs in the Water and Sediments
Under the influence of various complex factors (e.g., seasonal variation, geographical location, environmental conditions, and hydrodynamics), the distribution patterns of HMs in different regions show great differences [37].Compared with five kinds of heavy metals in the water of the study area investigated in 2009 [38], it was found that the Hg content showed a decreasing trend, while the Pb, Cu, Zn, and Cr content showed an increasing trend.Compared with other typical sea areas in China during the same period, the Hg concentration in Haizhou Bay was lower compared to that in Bohai Bay and Pearl River Estuary, and the concentrations of Pb, Cu, Zn, Cr, As, and Ni were higher compared to those in Bohai Bay, Yangtze River Estuary, and Pearl River Estuary, which indicates that the HM concentration in the study area was high (Table 3).In this study, the concentrations of Cr were much lower offshore and high nearshore in the water.With rapid economic development, human activities such as waterway construction and river discharge have become the main sources for the increase in HMs in the offshore environment [42], which may be the main reasons for the distribution characteristics.Because the distribution of Zn and Hg are doubly affected by atmospheric precipitation and the rerelease of sediments [43].The concentrations of Zn and Hg were much lower nearshore and high offshore in the water.The distribution trend of As and Pb in the water was higher in the central area and lower in the surrounding area, which is related to marine engineering activities.The vertical flow velocity of the artificial reef area increases [44], which accelerates the release of HMs from sediments.The implementation of these activities may release HMs to the water column by intervening in the sediments, leading to higher HM concentrations in the water [45].The distribution trend of Cu and Ni in the water was lower in the central area and higher in the surrounding area, which may be due to the existence of artificial reefs, and the fishing activities in the central part of the country are limited [43][44][45][46].Compared with other sea areas, the content of heavy metals in the water in the study area is relatively high, and bioremediation technologies such as seaweed can be used to improve its environmental conditions in the future.On the one hand, algae can enrich heavy metals in water, reduce their concentration, and improve the offshore environment [47].On the other hand, algae have an important impact on species diversity and suspended sediment migration in marine ecosystems [48,49].
For the HMs in the sediment, the average contents of seven heavy metals all meet the Class I standard of sediments in China.Compared with the six kinds of heavy metals in the sediments of the study area investigated in 2009 [50], it was found that the contents of Cu, Zn, and Cr are decreasing, while the contents of Pb, Cd, and As are increasing.Compared with other typical sea areas in China during the same period, the concentrations of As in Haizhou Bay were higher compared to those in Bohai Bay, the concentrations of Cr were higher compared to those in Pearl River Estuary, and the concentrations of seven HMs were lower compared to those in Yangtze River Estuary, which indicates that the HMs in the sediments are maintained at a relatively stable level (Table 4).The concentrations of As, Pb, Cr, Cu, Ni, and Zn in the sediments showed a decreasing trend from nearshore to offshore, which may be the result of the interaction of marine hydrodynamic forces, sediment particle size, and terrestrial input [53,54].On the one hand, it has been recognized that the discharge of domestic sewage and industrial wastewater leads to high HM concentrations in nearshore sediments [44].On the other hand, the tidal current in Haizhou Bay is a regular semidiurnal tide, and the flow rate at high tide is higher than that at low tide, which is conducive to the transfer of fine grain-size sediments that are more inclined to attach HMs from offshore to nearshore [54,55], resulting in the distribution pattern of high HM concentrations near the shore and low HM concentrations offshore.Additionally, during the migration of fine particles from the offshore area where artificial reefs exist to the nearshore area, some of the particles may be stagnant in the artificial reef area, leading to the migration of some HMs.In the sediments, the distribution of Hg showed an opposite trend compared to other HMs.Some studies have shown that the concentration of organic matter is the main factor for Hg distribution in seawater and sediments, while coarse particles usually contain more organic matter, resulting in a good adsorption effect on Hg [45,56,57].

Characteristics of HMs in the Tissues of Organisms
The differences in metal elements in different organisms are related to their habitats, physiological characteristics, and specific metal accumulation modes [57][58][59][60].In this study, the concentrations of HMs in bivalvia, gastropoda, and crustaceans were relatively high.For example, the highest concentrations of Cu (257.6 µg/g), Ni (2.13 µg/g), Pb (4.6 µg/g), and Zn (2529.5 µg/g) were found in Ostrea denselamellosa.O. denselamellosa are sessile organisms that mainly live on the surfaces of reefs or rocks and can accumulate high concentrations of HMs by filtering seawater [57].Previous studies have shown that oxygen and nitrogen complexes in O. denselamello can combine excess Cu and Zn, thereby facilitating the absorption of other toxic metals (e.g., Hg, Cd) [61,62].This interaction between HMs may be responsible for the higher concentrations of Cu, Ni, Pb, and Zn in O. denselamellosa.The concentrations of HMs (especially As (151.33 µg/g)) were higher in gastropoda, represented by Neptunea cumingi.N. cumingi mainly inhabit deep sandy and muddy seabeds in the subtidal zone and are carnivorous or saprophytic animals that feed on bivalvia and dead fish [62].This pathway of HM enrichment through the food chain may be the reason for the relatively high HMs in N. cumingi.The average concentrations of Cu and Zn in crustaceans represented by Charybdis japonica and Oratosquilla oratoria were significantly high, which may be due to the interactions between several metals [63,64].Studies have shown that essential metals such as Zn and Cu play a key role in the expression of metallothioneins, which can combine a variety of toxic HMs as receptors, making it positively correlated with the concentration of some HMs [63][64][65].The average concentration of As in cephalopods was significantly higher, especially in Sepiella maindroni (109.78 µg/g).A high concentration of As in nekton (e.g., cephalopods and crustaceans) is a common phenomenon, and As is also considered an essential element of cephalopods [66][67][68].In the experiment of HM transfer between cephalopod tissues, As in the gonads of cephalopods is transferred to their progeny through reproduction, thus showing a higher concentration of As in the progeny.The Zn concentration of fishes is significantly lower than that of crustaceans and bivalvia (p < 0.05).On the one hand, compared with some filter-feeding benthic bivalvia and crustaceans, fishes are less likely to absorb and accumulate HMs from sediments [69].On the other hand, the rapid growth and metabolism of fish will dilute the concentration of HMs in their body to a certain extent [70].

Characteristics of HMs Accumulated by Organisms from Water and Sediments
BAF is an indicator that reflects HM accumulation in organisms and is often used to evaluate the toxicity of pollutants in aquatic organisms, thus facilitating the formulation of relevant water environment monitoring standards and guidelines [71,72].HM concentrations in aquatic organisms are largely affected by HM pollutants in environmental media [8].In this study, the BAF values of Zn in bivalvia were significantly higher than those of other groups, which may be related to the habitat environment.Bivalvia with weak migration ability and small activity range generally inhabit the sea floor or the sediments.Once their living areas suffer from greater environmental pressure, they often cannot avoid it in time, leading to more HM accumulation from sediments [73][74][75].The BAF values of As in cephalopods were significantly higher than those in fishes (p < 0.05).Given that cephalopods mainly inhabit caves or crevices of rocky seafloors and move in the water column, they have a high probability of HMs directly from water and sediments [76,77].Generally, crustaceans can ingest HMs by filtering part of the seawater and sediments, and the HM concentrations in their tissues are greatly affected by habitats [18,19,59,78].However, we found that the BAF values of Cu and Zn in crustaceans were slightly lower than those in bivalvia and gastropoda (p < 0.05), which may be the result of the dilution of HM concentrations in crustaceans by internal factors such as shell molting [79,80].In addition, the BAF values of As, Cu, and Zn of fish are significantly lower than those of other groups (p < 0.05), which is due to the wide range and strong metabolic capacity activities of fish in the water [81,82].Owing to the different physiological mechanisms of each organism and the interaction between different HMs, more uncertainties have been added to the study of the accumulation rule of HMs.Therefore, future studies of HM bioaccumulation should be more detailed and in depth, and the collection and selection of samples should be standardized to make the results more scientific and accurate.

Conclusions
In this study, the bioaccumulation coefficient method was used for the first time to analyze the ability of different groups of organisms to accumulate HMs from different environmental media in the sea ranching area of Haizhou Bay.In the water, the concentrations of Zn and Hg were the smallest in the nearshore area, Cr was the smallest in the offshore area, Cu and Ni were the smallest in the central area, and As and Pb were the smallest in the nearshore area and offshore area.In the sediment, Hg had the smallest concentrations in the nearshore area, whereas As, Pb, Cr, Cu, Ni, and Zn had the lowest concentrations in the offshore area.The average contents of seven heavy metals all meet the Class I standard of sediments in China; the HMs in sediments are in good condition.The concentrations of Cu and Zn in crustaceans were significantly higher than those in fishes (p < 0.05), and As showed a high enrichment effect in cephalopods.The accumulation of HMs in the muscle tissues of different groups is largely affected by environmental media.The BAF value of benthic crustaceans and bivalvia accumulated HMs from sediments is high, and the BAF value of fish accumulated HMs from water and sediments is low.In this paper, the enrichment degree of heavy metals in different organisms is preliminarily explored, and the biomagnification phenomenon of heavy metals in the food chain still needs to be further studied.In the future, the absorption, storage, and metabolism of heavy metals by organisms of different trophic levels can be further studied.

Figure 1 .
Figure 1.The sampling sites.Note: The black dashed box is the sea ranching area.

Figure 1 .
Figure 1.The sampling sites.Note: The black dashed box is the sea ranching area.

Water 2023 , 17 Figure 2 .
Figure 2. Spatial distribution of HMs in the water and sediments.The bubble size indicates the concentration of HMs in the water, and the different colors indicate the concentration of HMs in the sediments (a): As; (b): Cr; (c): Cu; (d): Hg; (e): Pb; (f): Ni; (g): Zn.

Figure 2 .
Figure 2. Spatial distribution of HMs in the water and sediments.The bubble size indicates the concentration of HMs in the water, and the different colors indicate the concentration of HMs in the sediments (a): As; (b): Cr; (c): Cu; (d): Hg; (e): Pb; (f): Ni; (g): Zn.
• 52.849 -34 • 56.117 N, 119 • 13.641 -119 • 33.778 E) in May and August in 2017 under the marine survey plan by Jiangsu Marine Fisheries Research Institute, and in accordance with the Marine Monitoring Code (State Oceanic Administration, 2007) (Figure

Table 2 .
The detection limit of different elements measured by ICP-MS.

Table 3 .
Comparison of HM concentration (µg/L) in the surface water of Haizhou Bay and ty sea areas in China.

Table 3 .
Comparison of HM concentration (µg/L) in the surface water of Haizhou Bay and typical sea areas in China.

Table 4 .
Comparison of HM concentration (mg/kg) in the sediments in Haizhou Bay and typical sea areas in China.