Activity Levels of 210Po, 210Pb and Other Radionuclides (134Cs, 137Cs, 90Sr, 110mAg, 238U, 226Ra and 40K) in Marine Organisms From Coastal Waters Adjacent to Fuqing and Ningde Nuclear Power Plants (China) and Radiation Dose Assessment

With the rapid development of nuclear power, the radiation impacts on edible marine organisms, and the potential radiation risks to humans have become of considerable concern to public health. In this study, the activities of ²¹⁰Po and ²¹⁰Pb as well as those of other radionuclides in fishes (Mugil cephalus, Konosirus punctatus, Largehead hairtail, and Larimichthys polyactis), crustaceans (Mantis shrimp, Parapenaeopsis hardwickii, and Portunus trituberculatus), bivalves (Crassostrea gigas, Sinonovacula conzcta), and macroalgae (Gracilaria, Porphyra) collected in the coastal area adjacent to the Fuqing and Ningde nuclear power plants (NPPs) were determined. The activity range of ²¹⁰Po and ²¹⁰Pb was 0.60–48.09 and 0.07–2.76 Bq/kg _freshweight, respectively, with ²¹⁰Po/²¹⁰Pb activity ratios of 1.1–189.7. The ranking of ²¹⁰Po activity levels in marine organisms was bivalve mollusks > crustaceans > fishes > macroalgae. The calculated bioconcentration factors of ²¹⁰Po and ²¹⁰Pb were 636–44,944 and 3–1,226 L/kg, respectively. These values provide a new supplement to the IAEA reference database. The radiation dose rates for these marine organisms ranged from 0.037 to 1.531 μSv/h, which was much lower than the ERICA ecosystem screening benchmark of 10 μGy/h. The calculated committed effective dose received by humans from ingestion of these marine organisms was 0.06–2.99 mSv. Overall, ²¹⁰Po was the dominant radiation dose contributor in marine organisms and humans, whereas the dose contributions from the artificial nuclides ⁹⁰Sr and ¹³⁷Cs were negligible.

Introduction

The polonium isotope ²¹⁰Po (half-life, T_1/2 = 138.4 d) and its grandparent ²¹⁰Pb (T_1/2 = 22.26 y) are nonconservative, naturally occurring radionuclides within the uranium ²³⁸U decay chain, which is ubiquitous in the environment of the earth. The isotopes ²¹⁰Po and ²¹⁰Pb in the atmosphere mainly originated from the release of ²²²Rn from the ground and its subsequent decay. Due to their strong particle reactivity, they are firmly attached to the aerosol soon after they are produced. With the dry and wet depositions, they are subsequently discharged into the terrestrial and marine environment via dry and wet deposition (Seiler and Wiemels, 2012). Due to their unique geochemical properties, ²¹⁰Po and ²¹⁰Pb are used as a tracer pair to study the dynamic processes of aerosols in the atmosphere and estimate the residence times of aerosols (Aba et al., 2020). They are also used to study particle scavenging processes in the sea, particularly in assessing the export of particulate organic carbon (POC) fluxes from the euphotic zone (Zhang et al., 2020; Bam and Maiti, 2021), as well as specific marine food chain processes (Strady et al., 2015). Indeed, beyond the oceanographic application of ²¹⁰Po and ²¹⁰Pb, their accumulation in marine organisms and transfer to human consumers of seafood, and the resulting radiation doses to marine organisms or committed effective doses to humans are also issues of public concern. This is especially true for ²¹⁰Po, as it is one of the most radiotoxic nuclides that emit high-energy (~5.3 MeV) alpha rays and is the main contributor of the radiation dose received by marine organisms and humans (UNSCEAR, 2000; Sivakumar, 2014; Men et al., 2020a,b).

Marine organisms usually concentrate ²¹⁰Po and ²¹⁰Pb from the marine environment. Although the activity levels of ²¹⁰Po and ²¹⁰Pb in the marine environment are relatively low compared with those in the terrestrial environment, different marine organisms can concentrate these two radionuclides to relatively high levels with high concentration factors (CFs) (~10² to ~10⁵) (IAEA, 2004). Therefore, ²¹⁰Po and ²¹⁰Pb provide the main radiation source for marine organisms. In seawater, there are relatively higher levels of other naturally occurring nuclides, such as uranium ²³⁸U (12.2–215.4 Bq/m³), radium ²²⁶Ra (0.22–7.20 Bq/m³), and potassium ⁴⁰K (~12,000 Bq/m³), and artificial radionuclides, such as cesium ¹³⁷Cs (<3.2 Bq/m³) and strontium ⁹⁰Sr (<2.2 Bq/m³) (IAEA, 2005; Liu, 2010). Marine organisms also concentrate these nuclides in their body, which thus also produce self-radiation. Since the 1980s, the concept of human-centered environmental protection has gradually evolved into the concept of ecological protection in which the whole ecosystem is the protection target within the field of radiation protection. Many international organizations and government departments have been studying the effects of ionizing radiation on nonhuman species, including the International Commission on Radiation Protection (ICRP), the International Atomic Energy Agency (IAEA), the United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR), and the European Commission (EC). Additionally, after the 2011 Fukushima Dai-ichi Nuclear Power Plant (FDNPP) accident, the rapid development of nuclear power has raised increasing attention to the radiation impacts on marine organisms and the potential radiation risks to public health (Yu et al., 2018; Men et al., 2020a,b).

At present, the Fuqing and Ningde Nuclear Power Plants (NPPs), located on the coast of Fujian province (Figure 1), are in operation. The marine organisms living in the area adjacent to these two NPPs provide ideal experimental test subjects to study the concentrations of radionuclides in the marine environment as well as to undertake radiation dose assessment. In this study, data are provided on the activity levels of naturally occurring and artificial radionuclides in marine organisms used as bio-monitors of nuclear power plant operations. Activity levels of ²¹⁰Po, ²¹⁰Pb, and other naturally occurring or artificial radionuclides were investigated in fish, crustaceans, bivalve mollusks, and macroalgae in the areas surrounding Fuqing and Ningde NPPs, and the resulting radiation doses to both marine organisms and humans were assessed.

FIGURE 1

Figure 1. Sediment and water sampling stations (green symbols) near the Fuqing and Ningde nuclear power plants along the coast of China.

Materials and Methods

Sample Collection

Samples of marine organisms were obtained by hired fishermen in areas adjacent to Fuqing and Ningde NPPs (i.e., within 10 km) in July 2020 (Figure 1). Twelve samples with a fresh weight of ~2.2–10.6 kg each were collected. They were refrigerated and immediately sent to the laboratory (within 24 h). Marine organisms include fishes (the mullet Mugil cephalus, Konosirus punctatus, Largehead hairtail, and Larimichthys polyactis), crustaceans (Mantis shrimp, Parapenaeopsis hardwickii, and crab Portunus trituberculatus), bivalves (soft tissues of the Pacific oyster Crassostrea gigas, and razor clam Sinonovacula conzcta), macroalgae [the red algae Gracilaria spp. (Gracilariaceae) and Porphyra spp. (Bangiaceae)] (Figure 2). Seawater and sediment samples were also collected at each of 10 stations near Fuqing NPP and Ningde NPP (Figure 1).

FIGURE 2

Figure 2. Specimens of the marine organism sampled in this study.

Sample Processing and Analysis

The weighed marine organism samples were dried to constant weight for 48–96 h at 60°C in a drum dryer. Dried samples were pulverized, using agate mortar and pestle sets in preparation for the radioactive analysis. About 1 g of these pulverized dry samples was used for the measurement of ²¹⁰Po, using α spectrometer (Canberra 7200) (Štrok and Smodiš, 2011). The rest was transferred into crucibles and ashed in a muffle furnace at 450°C for 24–40 h. The ashes were ground and weighed at room temperature, stored in sealed boxes (~100 g per sample) for 20 days until analysis. Canberra BE6530 and GR4021 HPGe spectrometers were used to determine the activities of ²¹⁰Pb, ¹³⁴Cs, ¹³⁷Cs, ^110mAg, ²³⁸U, ²²⁶Ra, and ⁴⁰K (Men et al., 2017). The di (2-ethylhexyl) phosphoric acid (HDEHP) extraction-β counting method and the Ortec MPC-9604 α/β counter were employed for ⁹⁰Sr analysis (Men et al., 2017), using ~10 g of the ashes. Seawater and sediment samples were also analyzed according to the Technical Specification for Marine Radioactivity Monitoring (State Oceanic Administration of China, 2011). All marine organisms were analyzed whole, except for the bivalves whose shells were removed. Parallel sample analysis was implemented for Konosirus punctatus and Mantis shrimp; the results were in good agreement within an error <3%.

Specifically, ca. 1 ml of 0.12848 Bq/ml ²⁰⁹Po was added to 1 g of a dry biological sample, and then the spiked sample was digested with a mixture of concentrated nitric acid and hydrogen peroxide. After steaming until nearly dry, 2 mL of concentrated hydrochloric acid (HCl) was added and steaming carried out again, and the residue was dissolved with 2-M HCl. After filtration, the filtrate was placed in an α spectrometer for measurement over 24 h. The chemical yield for ²⁰⁹Po ranged from 52 to 89%, averaging 72 ± 12% (SD, n = 14) after adding 1 ml of 0.12848 Bq/ml of ²⁰⁹Po standard solution.

Seawater (5 L) was taken from each station for analysis. A known amount of ²⁰⁹Po (~1 g) was added to the seawater samples to determine the yield. The spiked samples were co-precipitated with ferric hydroxide by adding ~50 mg of Fe³⁺ and adjusting the pH to ~8, with the addition of concentrated ammonium hydroxide (NH₄OH). The precipitate was then dissolved in concentrated HCl, and auto-deposition was carried out. The analysis of other radionuclides in seawater is described in detail by Men et al. (2017).

Radiation Dose for Marine Organisms

The ERICA assessment tool (version 1.3, Tier 2) was used to evaluate the dose rates for marine organisms (Beresford et al., 2007; Men et al., 2020a,b). The average biological parameters of the specimens sampled, including length, width, and height, as well as weight, are listed in Table 1, and were used to calculate the radiation doses listed (the biological parameters were determined for all individuals of each species in the sample). The average nuclide activities in seawater and sediment were used to estimate the external dose rates. The activity levels of these nuclides in the marine organism were used to estimate the internal dose rates. The low beta, beta/gamma, and alpha weighing factors were taken to be 3, 1, and 10, respectively. The other parameters were set to their default values.

TABLE 1

Table 1. Average biological parameters of the sampled marine organisms.

Committed Effective Dose for Humans Consuming Various Marine Organisms

After ingestion or inhalation by humans, some radionuclides persist in the body and irradiate various tissues for many years. The resulting total effective dose over a lifetime (70 years or number of years up to reaching age, 70 for infants, 50 years for adults) is the committed effective dose (ICRP, 2007; Men et al., 2017). This dose received by a human per unit intake (1 Bq) of a given radionuclide is the radionuclide-specific dose coefficient (DC) for ingestion (Fisher et al., 2013), which converts the energy emitted from the ingested radionuclide into a radionuclide-specific, committed effective dose for human adults (Sv). For calculation of the committed effective dose for ingestion of marine organisms in this study, the ingestion rate was assumed as exact ingestion rates were not available. Here, the mean per capita consumption rate of aquatic products in China (50.97 kg/year) in 2018 was used to estimate the committed effective dose (FAOSTAT, 2018). This was calculated by multiplying the radionuclide activity in the marine organism (Bq/kg _freshweight) by the ingested mass (kg) and the DC (Sv/Bq) (ICRP, 2012).

Results and Discussion

Activity Levels of ²¹⁰Po and ²¹⁰Pb and Other Radionuclides in Marine Organisms

The activities of ²¹⁰Po and ²¹⁰Pb as well as other radionuclides in marine organisms from the coastal area adjacent to Fuqing and Ningde NPPs are listed in Table 2; ²¹⁰Po and ²¹⁰Pb activities ranged from 0.60 to 48.09 Bq/kg _freshweight and 0.07 to 2.76 Bq/kg _freshweight, respectively. These values are within the reported ranges of ²¹⁰Po and ²¹⁰Pb in marine organisms in China (²¹⁰Po: 0.117–65.8 Bq/kg _freshweight; ²¹⁰Pb: 0.02–6.88 Bq/kg _freshweight) (Li et al., 2016, 2018; Lin et al., 2016; Dong et al., 2018; Lin, 2018). The limit of ²¹⁰Po activity recommended in fish, meat, and shrimp by the Chinese National Standard on limited concentrations of radioactive materials in foods (GB 14882-94) is 15 Bq/kg _freshweight (Ministry of Health of the People's Republic of China, 1994). About 50% of ²¹⁰Po activities in marine organisms reported in the present study exceeded this value. Most ²¹⁰Po activities were higher than the UNSCEAR representative ²¹⁰Po activities in marine fish, crustaceans, and mollusks (2.4, 6, and 15 Bq/kg _freshweight) (UNSCEAR, 2000). The activity levels of ²¹⁰Po varied greatly among the different marine species. For example, the highest and lowest ²¹⁰Pb activities were measured in Crassostrea gigas and Porphyra, respectively. In general, ²¹⁰Po activities in marine organisms ranked in the order bivalves > crustaceans > fishes > macroalgae.

TABLE 2

Table 2. Activities of ²¹⁰Po and ²¹⁰Pb and other radionuclides in marine organisms sampled in this study.

The accumulation of ²¹⁰Po in marine organisms is related to food type, life cycle stage, trophic level, and body size (Carvalho, 2018). Firstly, suspension-feeding bivalves are primary consumers that mainly ingest phytoplankton and detrital particulate organic matter. Crustaceans are opportunistic secondary consumers that mainly ingest benthic organisms. Biomagnification can significantly enhance the ²¹⁰Po activity level in bivalves (Fowler, 2011; Dong et al., 2018). Secondly, bivalves that usually live on the bottom showed higher ²¹⁰Po activities due to rapid bottom deposition and biological adsorption. The higher ²¹⁰Po level in their bodies has been attributed to bioconcentration (Sirelkhatim et al., 2008; Lin, 2018). Finally, ²¹⁰Po is typically more concentrated in the digestive tract and hepatopancreas or in the gonads (Carvalho, 2018; Dong et al., 2018; Hurtado-Bermudez et al., 2019). The ²¹⁰Po/²¹⁰Pb activity ratios in the present study ranged from 1.1 to 189.7 (Table 2). It is reported that both ²¹⁰Po and ²¹⁰Pb bind strongly to organisms, and that ²¹⁰Pb is preferably associated with the mineral fractions of bones and shells. Compared with ²¹⁰Pb, ²¹⁰Po is primarily associated with proteins in organisms and can penetrate the cell cytoplasm. Therefore, ²¹⁰Po can be more effectively assimilated in marine organisms than ²¹⁰Pb, resulting in ²¹⁰Po/²¹⁰Pb activity ratios >1 in most marine organisms (Stewart et al., 2008).

As shown in Table 2, the activities of ¹³⁷Cs, ⁹⁰Sr, ²³⁸U, ²²⁶Ra, and ⁴⁰K ranged from undetectable to 0.08,0.03–0.75,0.04–2.66,0.02–1.61, and 51.−174.9 Bq/kg _freshweight, respectively. The activity levels ranked in the order ⁴⁰K > ²¹⁰Po > ²¹⁰Pb > ²³⁸U > ²²⁶ Ra > ⁹⁰Sr > ¹³⁷Cs. The activity levels of ⁹⁰Sr and ¹³⁷Cs in marine organisms were ~10⁻² to ~10⁻¹ Bq/kg _freshweight, which is within background levels (Liu and Zhou, 2000; Chen et al., 2003; Zhang, 2015; Lou et al., 2018). Those of ⁹⁰Sr and ¹³⁷Cs activities in fish, meat, and shrimp established by the Chinese National Standard on limited concentrations of radioactive materials in foods are 290 and 800 Bq/kg _freshweight, respectively (Ministry of Health of the People's Republic of China, 1994). The radioisotope ²¹⁰Po is the major natural decay product from the uranium series and provides the largest radiation dose to the human body via consumption of marine organisms (UNSCEAR, 2000; Carvalho, 2011; Khot et al., 2021; Kong et al., 2021). Indeed, the scavenging rate of ²¹⁰Po is higher than that of other radionuclides in the atmospheric environment (Alam and Mohamed, 2011), resulting in high ²¹⁰Po deposition in the marine environment. In turn, marine organisms show a stronger affinity for ²¹⁰Po than for other radionuclides (Bogdan, 1997; Lin, 2018), resulting in a higher activity level of ²¹⁰Po than that of other radionuclides. The activity levels of ⁹⁰Sr and ¹³⁷Cs in marine organisms in the present study are far below these values. The average activities of ²¹⁰Po and ²¹⁰Pb as well as other radionuclides in seawater and sediment in the sea area adjacent to Fuqing and Ningde NPPs are listed in Table 3. The data in Tables 2, 3 were used to estimate the radiation doses for the corresponding marine organisms.

TABLE 3

Table 3. Average activities of ²¹⁰Po and ²¹⁰Pb and other radionuclides in seawater/sediment.

Bioaccumulation of ²¹⁰Po and ²¹⁰Pb and Other Radionuclides in Marine Organisms

The bioconcentration factor is defined as the activity ratio of a radionuclide in the marine organism or biota to that in ambient seawater (L/kg) and is an indicator of the accumulation capacity of a given organism for a particular nuclide (Arnot and Gobas, 2006; Alava and Gobas, 2016; Ishii et al., 2020). Bioconcentration factors in different radionuclides vary widely due to their different biochemical properties, while bioconcentration factors (BCFs) in different marine organisms differ greatly due to their different bioaccumulation capacities. Even within the same species, BCFs vary among individuals due to differences in physiology, microhabitat, etc. For the sake of convenience and standardization, a set of values for different radionuclides and different kinds of marine organisms was recommended by the IAEA (Table 4) (IAEA, 2004). Using the data for seawater and marine organism samples in the present study, the BCFs of ²¹⁰Po and ²¹⁰Pb as well as those of other radionuclides can be estimated (Table 4). The BCFs for ²¹⁰Po and ²¹⁰Pb were in the ranges 636–44,944 and 3–1,226, respectively. BCFs of ¹³⁷Cs, ⁹⁰Sr, ²³⁸U, ²²⁶Ra, and ⁴⁰K were in the range 5–55, 41–1,014, 1–79, 7–479, and 4–15 L/g _freshweight, respectively. The BCF data reported in this study provide a useful supplement of information for the IAEA database.

TABLE 4

Table 4. Bioconcentration factors of ²¹⁰Po and ²¹⁰Pb and other radionuclides in marine organisms sampled in this study.

Radiation Dose Assessment

The radiation doses for nonhuman species have become an issue of increasing public health concern. The ERICA tools downloaded freely from the internet are widely used for radiation assessment (Garnier-Laplace et al., 2011; Johansen et al., 2015; Men et al., 2017, 2020a,b). As shown in Tables 1–4, the radiation doses received by marine organisms in the studied area were assessed, using the ERICA tools. The internal and external dose rates derived for each radionuclide and the total radiation dose rates are listed in Table 5. The total dose rates ranged from 0.037 to 1.531 μSv/h. Around the Ningde NPP, the highest and lowest radiation doses were observed in Crassostrea gigas and Porphyra, respectively. Overall, these values are markedly lower than the ERICA ecosystem screening benchmark of 10 μGy/h (Beresford et al., 2007) and the most conservative safety benchmark, which is one to two orders of magnitude lower than the International Commission on Radiological Protection (ICRP)-derived reference levels for corresponding reference animals or plants (ICRP, 2008; Fisher et al., 2013; Men et al., 2017). This suggested that there are no irradiation effects on marine organisms in the area adjacent to Fuqing and Ningde NPPs.

TABLE 5

Table 5. Internal and external radiation dose rates derived for each radionuclide for the different marine species sampled in this study (in μSv/h).

The dose contributions of different nuclides in different species were plotted in Figure 3 and show that ²¹⁰Po was the dominant dose contributor except for Mugil cephalus and Porphyra (Fuqing NPP) (47–97%), while ²²⁶Ra and ⁴⁰K were the main dose contributors for Mugil cephalus and Porphyra (Fuqing NPP), respectively. The contribution from external and internal doses for each nuclide (Table 5) suggests that the internal doses were much greater than the external doses. In general, the greatest internal dose should be from ²¹⁰Po sources because of its alpha emissions. Additional main contributors should be ²²⁶Ra and ²³⁸U, which produced intermediate internal doses because of alpha emissions. Due to high-activity levels in seawater (~11,500 Bq/m³) and marine organisms (51−174.9 Bq/kg _freshweight) as well as emitted high-energy γ-rays (1,460 keV), ⁴⁰K generated much higher internal and external dose rates than ²¹⁰Pb, ¹³⁷Cs, and ⁹⁰Sr (EI-Arabi, 2007). Indeed, the dose contribution from ¹³⁷Cs and ⁹⁰Sr was <0.13%, which was extremely low compared to that of naturally occurring radionuclides.

FIGURE 3

Figure 3. Dose contributions of each radionuclide for the different marine organisms sampled in this study.

Radiation Dose Assessment for Humans

The calculated committed effective dose for humans from ingestion of marine organisms in the area adjacent to Fuqing and Ningde NPPs was 60.74–2,990.41 μSv (Table 6). Results show that a maximum committed dose of 2.99 mSv will be received over the following 50 years based on assumed consumption of 50.97 kg of these marine organisms in 1 year. In terms of species, Porphyra had the lowest committed effective dose to humans (<100 μSv), while Portunus trituberculatus, Sinonovacula constrzcta, Largehead hairtail, Crassostrea gigas, and Mantis shrimp had committed effective doses exceeding 1,000 μSv. Crassostrea gigas produced radiation doses close to 3,000 Sv. The contribution of ²¹⁰Po to these committed effective doses was 43–99%. Based on this assumed consumption, the committed effective dose in 1 year (~0.06 mSv) was far below the 1-m Sv standard (Ministry of Environmental Protection of China, 2002). It is, therefore, safe to consume these marine organisms. The contributions of different nuclides ranked in the order ²¹⁰Po > ²¹⁰Pb/⁴⁰K > ²²⁶Ra > ²³⁸U > ⁹⁰Sr > ¹³⁷Cs, where ²¹⁰Po was the dominant contributor to the committed effective dose at 43–99%. In contrast, the artificial nuclides ⁹⁰Sr and ¹³⁷Cs contributed only 0.03–2.2%, and thus made the lowest contribution. This suggests that the committed effective dose from anthropogenic nuclides ⁹⁰Sr and ¹³⁷Cs is negligible when the NPPs are in operation.

TABLE 6

Table 6. Committed effective dose^a to humans (in μSv) from the ingestion of various marine organisms (annual consumption).

Conclusions

The activity levels of ²¹⁰Po and ²¹⁰Pb in fishes (Mugil cephalus, Konosirus punctatus, Largehead hairtail, Larimichthys polyactis), crustaceans (Mantis shrimp, Parapenaeopsis hardwickii, Portunus trituberculatus), bivalve mollusks (Crassostrea gigas, Sinonovacula conzcta), and macroalgae (Gracilaria, Porphyra) collected in coastal waters adjacent to Fuqing and Ningde NPPs were in the range 0.60–48.09 Bq/kg _freshweight and 0.07–2.76 Bq/kg _freshweight, respectively. The activity ratios of ²¹⁰Po/²¹⁰Pb were in the range 1.1–189.7; calculated BCFs of ²¹⁰Po and ²¹⁰Pb in marine organisms were 636–44,944 and 3–1,226 L/kg, respectively. The radiation dose rates in the studied marine organisms, ranging from 0.037 to 1.531 μSv/h, were markedly lower than the ERICA ecosystem screening benchmark of 10 μGy/h, suggesting that there were no detectable irradiation effects on the marine organisms studied. The committed effective dose to humans from ingestion of these marine organisms was in the range of 0.06–2.99 mSv. Overall, when the Fuqing and Ningde NPPs are in operation, ²¹⁰Po is the dominant radiation dose contributor to both marine organisms and humans, and the dose contributions from artificial nuclides ⁹⁰Sr and ¹³⁷Cs can be considered negligible.

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 author/s.

Ethics Statement

The animal study was reviewed and approved by Third Institute of Oceanography.

Author Contributions

WM designed this work and performed the data analysis. JS performed the sample analysis and radiation assessment. JS and WM wrote the manuscript together. FW and JW edited this manuscript. All authors contributed to the article and approved the submitted version.

Funding

This work was supported by the guided project of the Department of Science and Technology of Fujian Province (2018Y0058), the National Natural Science Foundation of China (41776091, 42076038), Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0606), the Natural Science Foundation of Guangdong Province (2021A1515011886), STU Scientific Research Foundation for Talents (NTF18011), and the Open Fund of the Laboratory for Ocean Dynamics and Climate, the Pilot Qingdao National Laboratory for Marine Science and Technology (No. OCFL-201801).

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

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