Long-term investigation of spatial–temporal variations, risk assessments, and controlling factors of persistent organic pollutants (HCHs, DDTs, and PAHs) and heavy metals in coastal regions along the Chinese Bohai Sea

Persistent organic pollutants (POPs) and heavy metals in marine systems have been given more and more attention due to their high toxicity and bioaccumulation capacity. After discharging into the marine systems, large proportions of POPs and heavy metals are likely to remain in coastal seas, causing serious contamination and high ecological risks. However, the lack of systematic studies restricts our understanding of POP and heavy metal cycling in coastal regions. Herein, the coastal regions along the Chinese Bohai Sea (an important fishing and typically polluted area) were chosen to establish a study model for investigating long-term spatial–temporal variations, risk assessments, and controlling factors of hexachlorocyclohexanes (HCHs), dichlorodiphenyltrichloroethanes (DDTs), polycyclic aromatic hydrocarbons (PAHs), and heavy metals in coastal regions. The results showed that concentrations of HCHs, DDTs, and PAHs in sediment, and contents of heavy metals in seawater and sediment were higher than those in other coastal regions during 2015–2018 and that concentrations of As and Cu in approximately 95% and 20% of sampled organisms exceeded maximum permissible levels recommended by China and the WHO, respectively. The significantly temporal variations in HCH and PAH concentrations were indicative of increasing POP pollution, and no significantly temporal variations in most heavy metal concentrations were found. Meanwhile, the higher concentrations of POPs and heavy metals were mainly located in estuaries and other nearshore areas. The geo-accumulation index (I_geo), potential ecological risk index (PERI), and provisional tolerable daily intake (PTDI) showed that As, Cd and Hg should be listed as the primary heavy metal pollutants in sediment; higher dietary risk was posed by As through seafood consumption; the dietary risks posed by HCHs, DDTs, and PAHs were lower. Finally, the results of multiple regression, Pearson’s, and cluster analyses indicated that anthropogenic activities (e.g., industrial and agricultural discharges, and riverine input) played important roles in controlling HCH, DDT, PAH, and heavy metal distributions in coastal regions along the Chinese Bohai Sea. The outcomes of this study are expected to shed new light on an improved understanding of POP and heavy metal cycling and provide a scientific basis for contamination control in coastal systems.

1 Introduction

Persistent toxic substances (PTS), including persistent organic pollutants (POPs) and heavy metals, have been given more and more attention due to their high toxicity and bioaccumulation capacity, especially through the aquatic food chain (Ali et al., 2019; Sreedevi and Harikumar, 2023). The POPs, for instance, organochlorine pesticides (OCPs) including hexachlorocyclohexanes (HCHs) and dichlorodiphenyltrichloroethanes (DDTs), and polycyclic aromatic hydrocarbons (PAHs) [listed in the Stockholm Convention (UNEP, 2019)], in aquatic environments originate from anthropogenic sources (e.g., domestic sewage discharge and industrial and agricultural activities) (Schwarzenbach et al., 2010). Heavy metals in aquatic environments originate from both natural (e.g., geological activities) and anthropogenic sources (e.g., mining, industrial and agricultural activities, and atmospheric deposition) (Kennsih, 1997). Compared with natural sources, the increase in anthropogenic discharge is deemed to be the major cause of intensified PTS pollution in aquatic environments in the past several decades, posing a serious threat to human health, especially through the consumption of aquatic products (Kennsih, 1997; Schwarzenbach et al., 2010; Pan and Wang, 2012). The POPs and heavy metals released from these anthropogenic and natural sources then enter the aquatic environments via a variety of pathways, e.g., river input, atmospheric deposition, wastewater discharge, and coastal erosion.

The oceanic ecosystem, as the largest aquatic environment, plays important roles in controlling the biogeochemical cycling of PTS. After discharging into the marine systems, large proportions of POPs and heavy metals are likely to remain in coastal seas through settling to sediment bounding with suspended particulate matter and then release through resuspending/diffusing from sediment into the water column, resulting in long-term environmental risks (Palm et al., 2004; Zeng et al., 2019). The subsequent bioaccumulation by marine organisms in these areas makes coastal systems the “hot spots” for ecosystem risks of POPs and heavy metals (Harmesa et al., 2022). The toxicity and fate of PTS in coastal regions depend not only on the gross concentrations but also on its cycling processes and bioavailability. The POPs and heavy metals in marine systems are controlled by a variety of environmental factors, such as temperature, salinity, pH, suspended particulate matter (SPM), nutrients, organic matter, and redox condition (Hoffmann et al., 2012; Sunda, 2012; Yao et al., 2016; Zhang et al., 2018; Fernandes et al., 2019; Wu et al., 2020; Harmesa et al., 2022; Lu et al., 2022; Wang et al., 2024). These important factors have significant effects on the major biogeochemical processes, chemical speciation, and bioavailability of POP and heavy metal cycling, e.g., adsorption/desorption, diffusion at the sediment–water interface, sedimentation/resuspension, and exchange with nearby oceans (Aparicio-González et al., 2012). Elucidating the controlling factors and processes is crucial for understanding the cycling of POPs and heavy metals in coastal environments.

The Chinese Bohai Sea, a semi-closed coastal sea and a part of the Northwest Pacific Ocean, is an important fishing area in China with approximately 10⁶ tons of fishery catch yield per year (Bureau of Fisheries and Administration, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, 2019). The Chinese Bohai Sea abuts the northeastern terrestrial areas of China, which are among the three most populated and industrialized areas in China (Bohai Sea Economic Rim) (Figure 1) (Chen et al., 2022). With the economic development, pollutants including POPs and heavy metals are discharging into the Chinese Bohai Sea, especially the coastal areas of Bohai Bay and Laizhou Bay with several rivers including the Yellow River (the second largest river in China) discharging, causing serious contamination and subsequently posing potential risks to the ecosystem and human health (Gao et al., 2014; Zhang et al., 2016; Chen et al., 2022). Great efforts were exerted to investigate concentrations, distributions, and risk assessments of POPs and heavy metals in seawater, sediment, and organisms of the Chinese Bohai Sea (Wang et al., 2005; Wang and Wang, 2007; Gao and Chen, 2012; Hu et al., 2017; Li et al., 2017; Liu et al., 2018; Wang et al., 2020; Gong et al., 2021; Chen et al., 2022). However, a systematic study on POPs and heavy metals in seawater, sediment, and organisms in coastal regions along the Chinese Bohai Sea is lacking, and the magnitude of PTS contamination in this ecosystem remains unknown. Additionally, the long-term monitoring of POPs and heavy metals and relevant parameters in various matrixes present in coastal regions along the Chinese Bohai Sea is scarce. The lack of such important information restricts our understanding of long-term spatial–temporal variations, proper risk assessments, and controlling factors of POPs and heavy metals in coastal regions along the Chinese Bohai Sea.

Figure 1

Figure 1 Study area and sampling sites.

The aims of this study were to 1) analyze long-term spatial–temporal variations of POPs (HCHs, DDTs, and PAHs) and heavy metals (As, Cd, Cu, Hg, Pb, and Zn) in seawater, sediment, and organisms in coastal regions along the Chinese Bohai Sea; 2) assess ecological risks posed by HCHs, DDTs, PAHs, and heavy metals; and 3) identify major factors controlling HCHs, DDTs, PAHs, and heavy metals in these regions. The outcomes of this study are expected to shed new light on an improved understanding of POP and heavy metal cycling and provide a scientific basis for PTS contamination control in coastal systems.

2 Materials and methods

2.1 Study area and sample collection

The Chinese Bohai Sea consists of three bays, namely, Bohai Bay, Laizhou Bay, and Liaodong Bay. Western Laizhou Bay and southern Bohai Bay are located in the southern region of the Chinese Bohai Sea, abutting the northeastern terrestrial areas, which are among the most industrialized areas in China. More than 10 rivers, including the Yellow Sea, which is the second largest river in China, carry pollutants including POPs and heavy metals, causing serious contamination in this coastal system. To evaluate spatial–temporal variations and environmental risk of HCHs, DDTs, PAHs, and heavy metals, a total of 538 seawater, 76 sediment, and 120 organism (Oratosquilla oratoria, Meretrix meretrix L., Scapharca subcrenata, Mactra veneriformis, Sinonovacula constricta, Sphyraenus, and Ruditapes philippinarum) samples were collected from the coastal regions along the Chinese Bohai Sea in spring, summer, autumn, and winter of 2015–2018 (Figure 1). Seawaters were collected using 4-L Niskin samplers at surface layers. Seawater with a volume of 500 mL was transported in a high-density polyethylene (HDPE) bottle, and HNO₃ (trace metal grade, Fisher Inc., Waltham, MA, USA) was added to adjust to pH ~ 2. The acidized seawater sample was stored at 4°C for heavy metal analysis. Surface sediment (0–5 cm) was collected using a grab sampler, one aliquot of sample was transported into a plastic bag and stored at −20°C for heavy metal analysis, and another aliquot of sample was wrapped with aluminum foil and stored at −20°C for analyses of HCHs, DDTs, and PAHs. Fish muscle, mollusk, or arthropod soft tissue was sampled using a ceramic knife, washed with deionized water (DIW), and stored at −20°C for analyses of POPs and heavy metals.

2.2 Determinations of HCHs, DDTs, PAHs, and heavy metals in seawater, sediment, and organisms

The surface sediment was treated according to the United States Environmental Protection Agency (USEPA) Methods 3540C and 3630C (USEPA, 1996a, 1996b) for analyses of HCHs, DDTs, and PAHs. Briefly, 10 g of freeze-dried and sieved (180-μm) surface sediment and 10 g of Na₂SO₄ (Merck, Darmstadt, Germany) were mixed, followed by Soxhlet extraction in 300 mL of hexane (Merck, Germany) and acetone (Merck, Germany) solution (1:1 v/v) for 24 h at 6 cycles/h. The extract was cooled and concentrated using hexane by a rotary evaporator and then further concentrated to approximately 2 mL using N₂. The solid-phase extraction tube including 1 g of SiO₂ sorbent was pre-eluted with 4 mL hexane. After adding the extract, 10 mL of n-hexane (Merck, Germany) and diethyl ether (Merck, Germany) (1:1, v/v) were used for eluting the column. These two fractions were mixed and concentrated to approximately 1 mL using N₂. The organism sample (fish muscle, mollusk, or arthropod soft tissue) was treated according to previous studies for analyses of HCHs, DDTs, and PAHs (Carro et al., 2002; Vives and Grimalt, 2002). Briefly, approximately 2 g of freeze-dried and homogenized soft tissue was extracted using 35 mL of n-hexane and acetone solution (4:1, v/v) and 5 mL KOH (1%). The samples were spiked with a mix of internal standards, including tetrabromobenzene (TBB) (Aldrich-Chemie, Germany) for the OCPs, and perylene-d₁₂ and pyrene-d₁₀ (Sigma-Aldrich, St. Louis, MO, USA) and anthracene-d₁₀ and naphthalene-d₈ (Acros Organics, Geel, Belgium) for PAHs. The extract was fractionated by adsorption chromatography with glass columns containing 5 g of Al₂O₃ (Sigma-Aldrich, USA) deactivated with DIW and 1 g of Na₂SO₄ (Merck, Germany). Two fractions were collected: F1, non-polar OCPs, eluting 8 mL of n-hexane-dichloromethane (19:1, v/v) and 2.5 mL of n-hexane-dichloromethane (1:2, v/v); and F2, polar OCPs and PAHs, adding 10 mL of n-hexane-CH₂Cl₂ (1:2, v/v). The OCPs and PAHs in samples were measured using gas chromatography–mass spectrometry (Agilent 7890A GC coupled with Agilent 5975C MS, Agilent, Santa Clara, CA, USA).

The analyses of six heavy metals (As, Cd, Cu, Hg, Pb, and Zn) in seawater and sediment were conducted according to the Specification for marine monitoring—Part 4: Seawater analysis (GB 17378.4–2007) (General Administration of Quality Supervision, Inspection, and Quarantine and Standardization Administration of the People’s Republic of China, 2008a) and Part 5: Sediment analysis (GB 17378.5–2007) (General Administration of Quality Supervision, Inspection, and Quarantine and Standardization Administration of the People’s Republic of China, 2008b). Briefly, the concentrations of Cd, Cu, Pb, and Zn in seawater were determined by anodic stripping voltammetry (797 VA Computrace, Wantong Inc., Switzerland); the concentrations of Hg and As were analyzed by atomic fluorescence spectrometry (AFS; AFS-820, Beijing Jitian Instrument Inc., Beijing, China). Approximately 0.2 g of freeze-dried and sieved (180-μm) surface sediment was weighed in a polytetrafluoroethylene (PTFE) tube followed by the addition of 2 mL HNO₃ (trace metal grade) and 6 mL HCl (trace metal grade). The sample was digested by microwave (Master, Sineo, Shanghai, China) at 105°C for 10 min and 180°C for 25 min. The digestion was evaporated to 1 mL and then diluted to 50 mL with DIW for analysis of heavy metals. The concentrations of Cd, Cu, Pb, and Zn were determined by atomic absorption spectrometry (ZEENIT^® 700P, Jena, Germany), and the concentrations of Hg and As were determined by AFS. Approximately 0.2 g of freeze-dried and homogenized soft tissue and 6 mL of 65% HNO₃ (v/v) were added into a 50-mL PTFE tube for pre-digestion overnight. Subsequently, 1 mL of 30% H₂O₂ (v/v) was added to the tube, followed by microwave digestion for 1.5 h. After cooling, the digestion was diluted with DIW, and 5 mL of the solution was transferred to a centrifuge tube. Finally, concentrations of As, Cd, Cu, Pb, and Zn were measured using inductively coupled plasma–mass spectrometry (ICP-MS; iCAP RQ, Thermo Fisher, Waltham, MA, USA) (Chen et al., 2022). The concentration of Hg in organisms was digested by 10 mL HNO₃ and 1 mL HClO₄, then reduced using KHB₄, and measured via AFS (GB 17378.6–2007) (General Administration of Quality Supervision, Inspection, and Quarantine and Standardization Administration of the People’s Republic of China, 2008c).

2.3 Measurements of other ancillary parameters

Temperature (T), salinity (S), pH, and redox potential (Eh) were in situ determined using a portable multi-parameter analytical instrument (SG98-FK2, Mettler-Toledo, Columbia, MD, USA). The dissolved oxygen (DO) was measured using the Winkler titration method (Zhang et al., 2015). The concentrations of total phosphorus (TP), total nitrogen (TN), nitrate (NO₃⁻), nitrite (NO₂⁻), ammonia nitrogen (NH₄⁺–N), and silicate (SiO₄³⁻) were determined following the Specification for marine monitoring—Part 4: Seawater analysis (GB 17378.4–2007). Chl-a was extracted with 90% acetone (v/v) in the dark for 24 h and measured according to a previous study (Parsons et al., 1984). Water with a volume of 500 mL was vigorously blended and then filtered through a pre-weighed 0.45-μm glass fiber filter to measure the SPM. Total organic carbon (TOC) in the sediment was measured using a TOC analyzer (SSM-5000A, Shimadzu, Kyoto, Japan) (Chen et al., 2021). The sulfide in the sediment was analyzed using the methylene blue spectrophotometric method according to Specification for marine monitoring—Part 5: Sediment analysis (GB 17378.5–2007).

2.4 QA/QC

Quality assurance and control procedures were conducted during the analyses of HCHs, DDTs, PAHs, and heavy metals. For each of the 20 samples, three method blanks, three certified reference materials or three matrix spikes in water samples, and triplicates of one randomly chosen sample were included. The recoveries of PAHs and OCPs in the spiked samples ranged from 87% to 103% and 78% to 101%, respectively. Relative standard deviations (RSDs) of triplicates were less than 16% and 13% for the PAHs and OCPs, respectively. The limits of detections (LODs) of OCPs and PAHs were 0.01 μg/kg to 1.46 μg/kg and 0.04 μg/kg to 0.40 μg/kg, respectively. The recoveries of heavy metals in seawater (87%–110%), sediment (93%–107%), and organisms (88%–112%) were within the acceptable ranges. The RSD of triplicates ranged from 3.6% to 13.2%, which were also within the acceptable RSD. The LODs were 0.5 μg/L for As, 0.01 μg/L for Cd, 0.6 μg/L for Cu, 0.007 μg/L Hg, 0.1 μg/L for Pb, and 1.2 μg/L for Zn in seawater. The LODs were 0.06 mg/kg for As, 0.04 mg/kg for Cd, 2.0 mg/kg for Cu, 0.002 mg/kg Hg, 1.0 mg/kg for Pb, and 6.0 mg/kg for Zn in sediment. The LODs were 0.27 mg/kg for As, 0.01 mg/kg for Cd, 0.08 mg/kg for Cu, 0.002 mg/kg Hg, 0.01 mg/kg for Pb, and 1.60 mg/kg for Zn in organisms. The DIW was used throughout the sample collection and analysis. All HDPE bottles were soaked in 30% HNO₃ for at least 96 h and then cleaned and filled with DIW until sampling heavy metals. Field and method blanks using the DIW were conducted during the sampling and analysis procedure. The concentrations of HCHs, DDTs, PAHs, and heavy metals in field and method blanks were comparable or lower than those of the LODs.

2.5 Statistical analysis

Distribution patterns of HCHs, DDTs, PAHs, and heavy metals in seawater and sediment were drawn using Ocean Data View (AWI, Bremerhaven, Germany). The temporal and spatial variations in concentrations of HCHs, DDTs, PAHs, and heavy metals were evaluated using the Mann–Whitney U-test by SPSS 19.0 (SPSS Inc., Armonk, NY, USA). A p-value of <0.05 indicates a significant difference. The cluster analysis and Pearson’s analysis were conducted to discover the relationships among HCHs, DDTs, PAHs, and heavy metals in seawater and sediment. The relationships between HCHs, DDTs, PAHs, heavy metals, and other ancillary parameters were detected by conducting Spearman’s analysis and multiple regression analyses to identify the controlling factors. The multicollinearity test was conducted before the multiple regression analyses, and the variance inflation factor (VIF) and condition index were calculated to detect the possible existence of collinearity among the input parameters (VIF < 10 and condition index <30). All of the above statistical analyses were performed using SPSS 19.0. The environmental risks posed by heavy metals in sediment and provisional tolerable daily intake of HCHs, DDTs, PAHs, and heavy metals through seafood consumption were calculated by the following methods.

2.5.1 I_geo

The geo-accumulation index (I_geo) was calculated to assess the pollution status of heavy metals in sediment of the coastal regions along the Chinese Bohai Sea (Equation 1).

$\begin{array}{ll}{\text{I}}_{geo}{\text{=log}}_2(\frac{{\text{C}}_{\text{i}}}{1.5{ \times \text{B}}_{\text{i}}})& (1)\end{array}$

where C_i is the concentration of each heavy metal in the sediment of the coastal regions along the Chinese Bohai Sea (mg/kg). B_i is the background value of each heavy metal in sediment (mg/kg). The values of 6.26 mg/kg, 0.032 mg/kg, 15.34 mg/kg, 0.019 mg/kg, 13.43 mg/kg, and 69.12 mg/kg were adopted for background concentrations of As, Cd, Cu, Hg, Pb, and Zn, respectively (Xiao et al., 2017).

2.5.2 PERI

The potential ecological risk index (PERI) was also calculated to assess the potential ecological risk posed by heavy metals following Equations 2 and 3 (Yu et al., 2023):

$\begin{array}{ll}\text{PERI=}\sum _{\text{i}=1}^{\text{n}}{E}_r^i& (2)\end{array}$

$\begin{array}{ll}{E}_r^i=T_r^i{C}_f^i=T_r^i\frac{{\text{C}}_{\text{i}}}{{\text{B}}_{\text{i}}}& (3)\end{array}$

where PERI is the potential ecological risk index posed by all heavy metals; $E_r^i$ is the potential risk of each heavy metal; $T_r^i$ is the toxic response factor for each heavy metal (As = 10, Cd = 30, Cu = Pb = 5, Hg = 40, and Zn = 1) (Hilton et al., 1985); $C_f^i$ is the contamination factor (the ratio between present and background concentrations in sediment). The background values of 6.26 mg/kg, 0.032 mg/kg, 15.34 mg/kg, 0.019 mg/kg, 13.43 mg/kg, and 69.12 mg/kg were adopted for As, Cd, Cu, Hg, Pb, and Zn, respectively (Xiao et al., 2017).

2.5.3 PTDI

Provisional tolerable daily intake (PTDI) values of HCHs, DDTs, PAHs, and heavy metals by residents were calculated by Equation 4.

$\begin{array}{ll}\text{PTDI=}\frac{{\text{C}}_{\text{i}}\times m_v}{\text{bw}}& (4)\end{array}$

where PTDI is the provisional tolerable daily intake of HCHs, DDTs, PAHs, and heavy metals (μg kg⁻¹ bw d⁻¹); C_i is the concentrations of HCHs, DDTs, PAHs, and heavy metals in aquatic product (mg/kg); m_v is the average consumption amount of aquatic products by adults in Shandong Province (32.6 g/d) (National Bureau of Statistics of China, 2022); bw is the average body weight of adults in Shandong Province (61.4 kg) (Health Commission of Shandong Province, 2015).

3 Results

3.1 Heavy metals in seawater

The concentrations of As, Cd, Cu, Hg, Pb, and Zn were 2.72 ± 1.01 μg/L, 0.25 ± 0.11 μg/L, 3.32 ± 0.80 μg/L, 0.06 ± 0.02 μg/L, 1.09 ± 0.83 μg/L, and 19.41 ± 10.78 μg/L in all seawater samples collected during 2015–2018, respectively. In comparison to those of other coastal systems, the concentrations of heavy metals in seawater of the coastal regions along the Chinese Bohai Sea were approximately 2–10 times higher than the background values of natural surface seawater (Wu and Zeng, 1983) and higher than those in the river estuaries, coastal bays, and open oceans in China and other countries (Supplementary Table 1). In general, the concentrations of heavy metals in seawater of the coastal regions along the Chinese Bohai Sea were at the highest rank among the reported coastal regions (at the higher 10th percentile) (Supplementary Table 1), suggesting the serious pollution status of heavy metals in this region.

3.2 HCHs, DDTs, PAHs, and heavy metals in sediment

The average concentrations of ∑HCHs, ∑DDTs, and ∑PAHs were 0.023 ± 0.032 mg/kg, 0.003 ± 0.002 mg/kg, and 0.26 ± 0.10 mg/kg in surface sediment collected from coastal regions of the Chinese Bohai Sea during 2015–2018, respectively. As shown in Figure 2, the compositions of HCHs showed a decreasing order of δ-HCH (41.8%) > α-HCH (32.4%) > γ-HCH (16.1%) > β-HCH (9.7%); compositions of DDTs were in order of OP′-DDT (44.5%) > PP′-DDE (28.3%) > PP′-DDT (14.9%) > PP′-DDD (12.3%); the dominant compositions of PAHs were FLU (25.3%), PHE (19.1%), NAP (11.1%), FLT (9.1%), ANT (7.8%), PYR (5.8%), and ANA (5.5%). Concentrations of As, Cd, Cu, Hg, Pb, and Zn were 10.38 ± 4.41 mg/kg, 0.20 ± 0.08 mg/kg, 14.35 ± 4.37 mg/kg, 0.02 ± 0.02 mg/kg, 16.70 ± 6.20 mg/kg, and 39.93 ± 11.51 mg/kg in all surface sediment samples collected during 2015–2018, respectively. Compared with those of other coastal regions, the concentrations of ∑HCHs, ∑DDTs, and ∑PAHs in surface sediment of the coastal regions along the Chinese Bohai Sea were at the highest rank; notably, the ∑HCHs and ∑DDTs levels were 3–20 times higher (Supplementary Table 2). The concentrations of As (at the higher 10th percentile) and Cd (at the higher 40th percentile) in surface sediment of the coastal regions along the Chinese Bohai Sea were higher, and comparable or lower concentrations of other measured heavy metals were observed (Supplementary Table 3). These results indicated that the sediment of the coastal regions along the Chinese Bohai Sea was seriously polluted by HCHs, DDTs, PAHs, As, and Cd.

Figure 2

Figure 2 Compositions of HCHs, DDTs, and PAHs (%) in surface sediment of the coastal regions along the Chinese Bohai Sea. HCHs, hexachlorocyclohexanes; DDTs, dichlorodiphenyltrichloroethanes; PAHs, polycyclic aromatic hydrocarbons.

3.3 HCHs, DDTs, PAHs, and heavy metals in organisms

The average concentrations of HCHs, DDTs, and PAHs were respectively 0.62 ± 0.23 μg/kg, 6.81 ± 2.90 μg/kg, and 6.14 ± 1.60 μg/kg in arthropods and 1.98 ± 0.57 μg/kg, 2.17 ± 0.39 μg/kg, and 11.30 ± 9.91 μg/kg in mollusks. The average concentrations of As, Cd, Cu, Hg, Pb, and Zn were respectively 2.69 ± 0.62 mg/kg, 0.15 ± 0.03 mg/kg, 10.16 ± 1.41 mg/kg, 0.01 ± 0.002 mg/kg, 0.30 ± 0.04 mg/kg, and 18.58 ± 0.77 mg/kg in arthropods; 1.82 ± 0.61 mg/kg, 0.19 ± 0.16 mg/kg, 4.61 ± 3.61 mg/kg, 0.01 ± 0.006 mg/kg, 0.33 ± 0.09 mg/kg, and 12.36 ± 3.20 mg/kg in mollusks; and 1.52 ± 1.51 mg/kg, 0.07 ± 0.003 mg/kg, 0.31 ± 0.20 mg/kg, 0.02 ± 0.005 mg/kg, 0.20 ± 0.03 mg/kg, and 4.01 ± 1.99 mg/kg in fish. In comparison to those of other coastal regions, the concentrations of HCHs, DDTs, and PAHs were comparable or lower; however, the heavy metal levels in organisms collected from the coastal regions along the Chinese Bohai Sea were higher (Supplementary Table 4). Meanwhile, the levels of HCHs, DDTs, and PAHs in organisms collected from the coastal regions along the Chinese Bohai Sea were lower than the maximum permissible levels (MPLs) recommended in China (0.1 mg/kg for HCHs, 0.5 mg/kg for DDTs, and 5 μg/kg for PAHs) (National Health Commission, Ministry of Agriculture and Rural Affairs, State Administration of Market Regulation of the People's Republic of China, 2021; National Health Commission, State Administration of Market Regulation of the People's Republic of China, 2022). The concentrations of As in approximately 95% of the sampled organisms exceeded MPLs of 0.5 mg/kg recommended in China (National Health and Family Planning Commission, National Food and Drug Administration of the People’s Republic of China, 2017). Meanwhile, the concentrations of Cu in 20% of the sampled organisms exceeded MPLs of 10 mg/kg according to the guideline of the World Health Organization (Joint FAO/WHO Expert Committee on Food Additives, 1982), suggesting that organisms in the coastal regions along the Chinese Bohai Sea were contaminated with different levels of As and Cu.

4 Discussion

4.1 Spatial–temporal distributions and variations of HCHs, DDTs, PAHs, and heavy metals in coastal regions along the Chinese Bohai Sea

4.1.1 Spatial distributions of HCHs, DDTs, PAHs, and heavy metals in seawater and sediment

As shown in Figure 3, the concentrations of As, Pb, and Zn in seawater sampled from western Laizhou Bay were higher than those from southern Bohai Bay (Mann–Whitney U-test, p < 0.05), suggesting that pollution of these heavy metals in the former system was more serious than in the latter, while opposite variations were found in Cd and Cu concentrations (Mann–Whitney U-test, p < 0.05). No significant trend of Hg concentrations was found in these two regions. Generally, the concentrations of heavy metals displayed decreasing trends from nearshore to offshore. Several “hot spots” were located at the river estuaries, e.g., Yellow River and Xiaoqiang River (Figure 3), indicative of the effect of riverine input on heavy metal distributions. Moreover, some higher concentrations of heavy metals also were observed in offshore areas due to oceanic current transport, resuspension and diffusion from sediment, atmospheric deposition, and other processes.

Figure 3

Figure 3 Spatial distributions of heavy metals in seawater (μg/L) of the coastal regions along the Chinese Bohai Sea.

As shown in Figure 4, the concentrations of PAHs in sediment sampled from the southern of Bohai Bay were higher than those in western Laizhou Bay (Mann–Whitney U-test, p < 0.05), indicative of more serious PAH pollution. The concentrations of As and Zn in sediment collected from western Laizhou Bay were higher than those in southern Bohai Bay (Mann–Whitney U-test, p < 0.05), also indicative of serious pollution in Laizhou Bay than in Bohai Bay. There were no significant spatial variations in concentrations of HCHs, DDTs, and other heavy metals between these two bays. The highest concentrations of HCHs, DDTs, PAHs, and heavy metals in sediment were mainly measured at river estuaries around the coastal regions along the Chinese Bohai Sea (Figure 4). The riverine water carries pollutants including POP and heavy metal discharges into the marine systems, and large proportions of pollutants remain in coastal regions with the settlement of suspended particulate matter.

Figure 4

Figure 4 Spatial distributions of HCHs, DDTs, PAHs, and heavy metals in sediment (mg/kg) of the coastal regions along the Chinese Bohai Sea. HCHs, hexachlorocyclohexanes; DDTs, dichlorodiphenyltrichloroethanes; PAHs, polycyclic aromatic hydrocarbons.

4.1.2 Temporal variations of HCHs, DDTs, PAHs, and heavy metals in seawater and sediment

As shown in Figure 5A, the concentrations of HCHs were 0.004 ± 0.003 mg/kg, 0.011 ± 0.006 mg/kg, 0.027 ± 0.026 mg/kg, and 0.042 ± 0.047 mg/kg in surface sediment collected in 2015, 2016, 2017, and 2018, respectively (Supplementary Table 5), which showed significantly increasing trends (Mann–Whitney U-test, p < 0.01). The concentrations of PAHs in surface sediment increased from 0.15 ± 0.08 mg/kg in 2015 to 0.30 ± 0.07 mg/kg (Mann–Whitney U-test, p < 0.05), and no significantly temporal variations in DDT concentrations were found during the sampling period (Mann–Whitney U-test, p > 0.05) (Supplementary Table 5). These results suggested that the POP pollution, especially the HCHs and PAH, is becoming more and more serious in the coastal regions of the Chinese Bohai Sea. The temporal variations in heavy metal concentrations in seawater and surface sediment (Figures 5B, C) and results of the Mann–Whitney U-test showed that the concentrations of Zn in seawater in 2018 (14.53 ± 2.74 μg/L) were lower than those during the other years (p < 0.05) (Supplementary Table 5). The highest average concentrations of As, Cd, Cu, Hg, and Pb in seawater were 2.89 ± 0.39 μg/L, 0.32 ± 0.10 μg/L, 3.40 ± 0.79 μg/L, 0.06 ± 0.02 μg/L, and 1.23 ± 0.85 μg/L in 2015, 2018, 2016, 2015, and 2018, respectively. Except for slight fluctuations, no significantly temporal variations were found in the concentrations of these metals in seawater (Mann–Whitney U-test, p > 0.05) (Supplementary Table 5), indicating a relatively stable status of heavy metals in seawater of the coastal regions along the Chinese Bohai Sea during the sampling periods (Figure 5B). The highest average concentration of As in surface sediment was 16.78 ± 4.57 mg/kg in 2015 and showed a decreasing trend to 8.26 ± 1.42 mg/kg during 2018 (Mann–Whitney U-test, p < 0.05) (Figure 5C and Supplementary Table 5). The highest average concentration of Hg in surface sediment was 0.03 ± 0.03 mg/kg measured in 2017, and the highest average concentrations of other heavy metals (Cd, 0.22 ± 0.10 mg/kg; Cu, 17.26 ± 5.65 mg/kg; Pb, 21.34 ± 5.76 mg/kg; Zn, 44.84 ± 3.71 mg/kg) were measured during 2015, and no significantly temporal variations were found (Mann–Whitney U-test, p > 0.05) (Figure 5C and Supplementary Table 5).

Figure 5

Figure 5 Temporal variations of HCHs, DDTs, and PAHs in sediment (A), heavy metals in seawater (B), and sediment (C) of the coastal regions along the Chinese Bohai Sea. HCHs, hexachlorocyclohexanes; DDTs, dichlorodiphenyltrichloroethanes; PAHs, polycyclic aromatic hydrocarbons.

4.2 Risk assessments of HCHs, DDTs, PAHs, and heavy metals in coastal regions along the Chinese Bohai Sea

4.2.1 Pollution status and ecological risks of heavy metals in sediment

The geo-accumulation index (I_geo) was calculated by Equation 1 and can be divided into seven grades: 1) unpolluted, I_geo ≤ 0; 2) unpolluted to moderately polluted, 0 < I_geo < 1; 3) moderately polluted, 1 < I_geo < 2; 4) moderately to strongly polluted, 2 < I_geo < 3; 5) strongly polluted, 3 < I_geo < 4; 6) strongly to extremely polluted, 4 < I_geo < 5); and 7) extremely polluted, I_geo > 5 (Wang et al., 2018). The average I_geo values of heavy metals in sediment of the coastal regions along the Chinese Bohai Sea were in order of As (2.65 ± 11.73) > Cd (0.61 ± 0.35) > Hg (−0.24 ± 2.82) > Zn (−0.76 ± 0.23) > Pb (−2.64 ± 9.08) > Cu (−3.97 ± 18.81) (Supplementary Table 6). These results suggested that the sediment in coastal regions along the Chinese Bohai Sea was moderately to strongly polluted by Cd and As, which was consistent with previous studies (Xiao et al., 2017; Liu et al., 2023).

The ecological risk of heavy metals in sediment based on the PERI values can be divided into five grades: 1) low risk, PERI < 150; 2) moderate risk, 150 < PERI < 300; 3) high risk, 300 < PERI < 600; and 4) significantly high risk, PERI > 600 (Ferreira et al., 2022). The average PERI value calculated by Equation 2 was 254.96 ± 89.92 (ranging from 106.04 to 494.94), suggesting that the ecological risk posed by heavy metals was moderate. As shown in Figure 6A, the higher PERI values were mainly located at the Yellow River estuary and western nearshore areas of Laizhou Bay, indicative of the effects of anthropogenic discharge on heavy metal risks in the sediment. According to Equation 3, the ecological risk ($E_i^r$) of As, Cd, Cu, Hg, Pb, and Zn were 16.58 ± 7.04, 185.12 ± 76.17, 4.68 ± 1.42, 41.79 ± 40.53, 6.22 ± 2.31, and 0.58 ± 0.17, respectively (Supplementary Table 6), indicating that the ecological risks posed by Cd and Hg were high (160≤ ${\text{E}}_r^{\text{i}}$<320) and moderate (40≤${\text{E}}_r^{\text{i}}$<80) in sediment of the coastal regions along the Chinese Bohai Sea. Meanwhile, the ${\text{E}}_r^{\text{i}}$ indicated that the contribution of each heavy metal on the total PERI was in the order of Cd (71.92%) > Hg (16.09%) > As (7.18%) > Pb (2.56%) ≈ Cu (1.99%) > Zn (0.26%) (Figure 6B and Supplementary Table 6). To summarize, based on the PERI and I_geo methods, As, Cd, and Hg should be listed as the primary heavy metal pollutants in the sediment of the coastal regions along the Chinese Bohai Sea, while the ecological risks posed by Cd and Hg are worthy of attention. Additionally, the concentrations of ∑HCHs, ∑DDTs, and ∑PAHs in surface sediment of this study were at the highest rank in comparison to those of other coastal systems (Supplementary Table 2), suggesting that POP pollution in coastal regions along the Chinese Bohai Sea is serious, especially HCHs and DDTs.

Figure 6

Figure 6 The distribution of potential ecological risk index (PERI) of all heavy metals (A) and contribution of each heavy metal (B).

4.2.2 Dietary risks of HCHs, DDTs, PAHs, and heavy metals in organisms

As shown in Table 1, the average PTDI values of HCHs, DDTs, and PAHs in arthropods sampled from the coastal regions along the Chinese Bohai Sea were respectively (3.3 ± 1.2) × 10⁻⁴ μg kg⁻¹ bw d⁻¹, (3.6 ± 1.5) × 10⁻³ μg kg⁻¹ bw d⁻¹, and (3.0 ± 0.8) × 10⁻³ μg kg⁻¹ bw d⁻¹. Higher PTDI values of (1.0 ± 0.3) × 10⁻³ μg kg⁻¹ bw d⁻¹, (5.1 ± 0.2) × 10⁻³ μg kg⁻¹ bw d⁻¹, and 0.12 ± 0.05 μg kg⁻¹ bw d⁻¹ by HCHs, DDTs, and PAHs, respectively, in mollusks were estimated. The calculated PTDI values were lower than the RfD recommended by the USEPA (Table 1), suggesting lower dietary risk posed by HCHs, DDTs, and PAHs in aquatic products sampled from the coastal regions along the Chinese Bohai Sea. The average PTDI values of As, Cd, Cu, Hg, Pb, and Zn in arthropods were 1.43 ± 0.33 μg kg⁻¹ bw d⁻¹, 0.08 ± 0.02 μg kg⁻¹ bw d⁻¹, 5.39 ± 0.75 μg kg⁻¹ bw d⁻¹, 0.007 ± 0.001 μg kg⁻¹ bw d⁻¹, 0.16 ± 0.02 μg kg⁻¹ bw d⁻¹, and 9.86 ± 0.41 μg kg⁻¹ bw d⁻¹; 0.97 ± 0.33 μg kg⁻¹ bw d⁻¹, 0.10 ± 0.09 μg kg⁻¹ bw d⁻¹, 2.45 ± 1.92 μg kg⁻¹ bw d⁻¹, 0.005 ± 0.003 μg kg⁻¹ bw d⁻¹, 0.17 ± 0.05 μg kg⁻¹ bw d⁻¹, and 6.56 ± 1.70 μg kg⁻¹ bw d⁻¹ in mollusks; and 0.81 ± 0.80 μg kg⁻¹ bw d⁻¹, 0.04 ± 0.002 μg kg⁻¹ bw d⁻¹, 0.16 ± 0.11 μg kg⁻¹ bw d⁻¹, 0.01 ± 0.02 μg kg⁻¹ bw d⁻¹, 0.10 ± 0.02 μg kg⁻¹ bw d⁻¹, and 2.13 ± 1.06 μg kg⁻¹ bw d⁻¹ in fish, respectively. Generally, the dietary risks posed by heavy metals in organisms displayed an order of anthropod > mollusk > fish for most heavy metals except for Hg and Pb (Table 1). As shown in Table 1, the PTDI by As in arthropods, mollusks, and fish exceeded the RfD, and others were below the recommended values by USEPA, indicative of high dietary risks posed by As in organisms from the coastal regions along the Chinese Bohai Sea. Although As has no biological functions in living organisms (Siegel, 2003), both inorganic and organic As are absorbed by living organisms in the gastrointestinal tract. The concentrations of As in tissues of aquatic organisms vary widely, with particularly high concentrations in lipids, liver, and muscles, posing high health risks to humans through the consumption of aquatic products (Sloth and Julshamn, 2008).

Table 1

Table 1 Dietary risks posed by HCHs, DDTs, PAHs, and heavy metals in organisms collected from the coastal regions along the Chinese Bohai Sea.

4.3 Controlling factors and potential sources of HCHs, DDTs, PAHs, and heavy metals in coastal regions along the Chinese Bohai Sea

4.3.1 Controlling factors of heavy metals in seawater

To investigate the factors controlling the distributions of heavy metals in seawater of the coastal regions along the Chinese Bohai Sea, multiple regression analyses of heavy metal concentrations in seawater against physicochemical parameters were performed. Spearman’s correlation analysis was first conducted to choose the parameters significantly correlated to heavy metal concentrations (Supplementary Table 7), and these parameters were adopted in subsequent multiple regression analyses. As shown in Table 2, the results of multiple regression analyses showed that SPM, TN, chemical oxygen demand (COD), and TP were parameters controlling distributions of Cd, Cu, Pb, and Zn in seawater of the coastal regions along the Chinese Bohai Sea, respectively; T, COD, TP, SiO₄³⁻, T, and SPM dominated distributions of As and Hg. Nutrients, phosphorus, and silicate in coastal systems are mainly discharged into riverine water, industrial and sewage wastewaters, and groundwater (Slomp and Van Cappellen, 2004; Archana et al., 2018); moreover, the chemical oxygen demand generally reveals the content of organic pollutants (Kamarudin et al., 2020). The significantly positive relationships between these parameters and heavy metals in seawater observed in this study suggested that anthropogenic discharge plays important roles in controlling the distributions of heavy metals in coastal regions along the Chinese Bohai Sea. The significantly positive correlations between As, Hg, and T may be due to more riverine input and wet deposition of pollutants in the warm season (Peng, 2015), also indicative of the important effects of anthropogenic discharge on heavy metal distributions. The high affinity to be absorbed and transported with the suspended particulate matter may result in positive correlations of Hg and Cd with SPM, which was consistent with previous studies (Zhang et al., 2018; Lao et al., 2019).

Table 2

Table 2 Factors controlling heavy metals in seawater of the coastal regions along the Chinese Bohai Sea.

4.3.2 Potential sources of HCHs, DDTs, PAHs, and heavy metals in sediment

As shown in Supplementary Table 8, the results of Pearson’s analysis showed that HCHs, DDTs, PAHs, and heavy metals were significantly positive with organic matter (p < 0.01). Previous studies reported that the terrestrial organic matter and pollutants were transported by the rivers, discharged, and retained in the sediment of the coastal regions (Gao and Chen, 2012; Gao et al., 2012). These results also indicated that anthropogenic discharge plays important roles in controlling the distributions of POPs and heavy metals in coastal regions along the Chinese Bohai Sea. Moreover, the cluster analysis and Pearson’s analysis can be used to identify similar sources or environmental behavior of pollutants (Li et al., 2013). The cluster analysis on the concentrations of HCHs, DDTs, PAHs, and heavy metals in surface sediment of the coastal regions along the Chinese Bohai Sea is presented in Figure 7. Three clusters were identified from HCHs, DDTs, PAHs, and heavy metal enrichment dendrograms. The first cluster contains HCHs, DDTs, PAHs, Hg, and Cd; Pb, Cu, and As were identified in the second cluster; Zn was identified in the third cluster. The results of Pearson’s correlation analysis (Supplementary Table 8) showed significantly positive relationships (p < 0.01) among Hg-DDTs (0.41), DDTs-HCHs (0.49), HCHs-Cd (0.39), and Cd-PAHs (0.37) in the sediment of the coastal regions along the Chinese Bohai Sea (Supplementary Table 8). Agricultural fertilizers and pesticides, domestic and industrial sewage, and river water carrying pollutants may be the most important sources of POPs and heavy metals in coastal regions along the Chinese Bohai Sea. Except for the point source, the atmospheric deposition also contributed input of Hg and Cd into these regions. Moreover, the same cluster of Cd and Hg in sediment and the significant correlations between them and SPM in seawater (Table 2) indicated that anthropogenic discharge dominated Cd and Hg and that SPM plays important roles in their biogeochemical cycling in coastal regions along the Chinese Bohai Sea.

Figure 7

Figure 7 Cluster analyses of HCHs, DDTs, PAHs, and heavy metal concentrations in surface sediment of the coastal regions along the Chinese Bohai Sea. HCHs, hexachlorocyclohexanes; DDTs, dichlorodiphenyltrichloroethanes; PAHs, polycyclic aromatic hydrocarbons.

5 Conclusions

HCHs, DDTs, PAHs, and heavy metals in seawater, surface sediment, and organisms in coastal regions along the Chinese Bohai Sea were measured during 2015–2018. The results showed that the concentrations of HCHs, DDTs, and PAHs in surface sediment and concentrations of heavy metals in seawater and surface sediment were higher than the background values and the other coastal regions and that concentrations of As and Cu in approximately 95% and 20% of the sampled organisms exceeded MPLs recommended in China and the WHO, respectively, indicative of serious heavy metal pollution in coastal regions along the Chinese Bohai Sea. Significantly temporal variations in HCH and PAH concentrations and no variations in most heavy metal concentrations were found, and the higher concentrations were mainly located at estuaries and other nearshore areas, suggesting the important effects of anthropogenic discharges on POPs and heavy metal distributions in this coastal system. As, Cd and Hg were identified to be the primary heavy metal pollutants in sediment using I_geo and PERI methods, and the dietary risk posed by As in organisms is worthy of attention according to higher PTDI values. Finally, anthropogenic activities (e.g., industrial and agricultural discharges, and riverine and sewage inputs) played important roles in controlling HCHs, DDTs, PAHs, and heavy metal distributions in coastal regions along the Chinese Bohai Sea by multiple regression, Pearson’s, and cluster analyses.

Data availability statement

The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding authors.

Ethics statement

The manuscript presents research on animals that do not require ethical approval for their study.

Author contributions

YS: Writing – original draft, Writing – review & editing, Formal analysis, Data curation, Methodology. WW: Writing – original draft, Investigation, Formal analysis. YYS: Writing – original draft, Investigation. XW: Writing – original draft, Investigation. HZ: Writing – original draft, Investigation. ZL: Writing – review & editing, Writing – original draft, Visualization, Supervision, Resources, Conceptualization. YY: Writing – review & editing, Visualization, Supervision, Resources, Project administration, Methodology, Conceptualization.

Funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the Hubei University of Science and Technology Program (BK202416) and the National Natural Science Foundation of China (32000906, 42307332).

Acknowledgments

We thank the editor and reviewer for their valuable comments and suggestions. We are also thankful to our lab fellow and all those who assisted during this study.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2024.1450208/full#supplementary-material

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