Contrasting Behaviors of 210Pb and 210Po in the Productive Shelf Water Versus the Oligotrophic Water

We measured the total, truly dissolved (<10 kDa), colloidal (10 kDa–0.2 μm), and particulate phases (>0.2 μm) of 210Pb and 210Po in the East China Sea (ECS) shelf water and the East Sea (Japan Sea). In order to examine the behaviors of 210Pb and 210Po in different marine environments, we compiled our results with previously reported data in the same region and in the northwestern Pacific Ocean (NWPO). The proportions of the truly dissolved, colloidal, and particulate phases in the shelf water were 32, 27, and 41% for 210Pb and 49, 32, and 19% for 210Po, respectively. Based on a steady-state scavenging model, 210Pb and 210Po showed higher (3.0 ± 0.6 year–1) and lower (0.3 ± 0.2 year–1) scavenging rates, respectively, in the shelf water than those in the NWPO and the East Sea. A non-steady-state model, accounting for the residence time of the shelf water, also showed twice more efficient removal rate of 210Pb in the shelf water than that in the NWPO and the East Sea. In contrast, there was the net input of 210Po in the shelf water relative to the large removal in the NWPO and the East Sea. The large proportions of total dissolved (truly dissolved + colloidal) 210Po (>80%) in the shelf water indicate active regeneration of 210Po from the sinking particles and the surface sediments. Our results suggest that the ECS shelf is the source for Po in the northwestern Pacific marginal seas, a proxy for sulfur group elements (S, Se, and Te), whereas it is the efficient sink for Pb, together with other particle-reactive trace elements.


INTRODUCTION
Naturally occurring .3 years) is produced from 222 Rn (half-life = 3.8 days), belonging to the 238 U decay series, and it produces . In oceanic environments, 210 Pb originates mainly from the atmospheric deposition in the upper ocean and in situ production from 226 Ra (half-life = 1,600 years) decay, via 222 Rn, in the deep ocean. Since the production of 210 Po from 210 Pb is negligible in the atmosphere, most 210 Po in the ocean is assumed to be produced from 210 Pb decay. Both 210 Pb and 210 Po are known to be particle reactive in aqueous systems, but 210 Po tends to be preferentially assimilated by marine biota (Fisher et al., 1983;Wei and Murray, 1994;Hung and Chung, 1998;Stewart and Fisher, 2003;Carvalho, 2011). This efficient biological removal of 210 Po results in disequilibria between 210 Pb and 210 Po in the upper ocean, and this principle has been used to determine particulate organic carbon export (Bacon et al., 1976;Friedrich and van der Loeff, 2002;Stewart et al., 2007;Tang and Stewart, 2019).
Although the removal of 210 Po is known to be related to marine productivity, previous studies have reported a large deficiency of 210 Po in oligotrophic oceans (Nozaki et al., 1990a;Kim, 2001;Chung and Wu, 2005). Nozaki et al. (1990a) attributed such a distinct deficiency to the significant atmospheric input of 210 Pb. However, Kim (2001) suggested that an unusually large deficiency in the oligotrophic ocean could be due to the efficient uptake of 210 Po by cyanobacteria and then transfer to higher trophic levels along marine food chains rather than downward settling. On the contrary, in the eutrophic ocean, 210 Po may reside for a much longer time in the non-settling organic pool as it is taken up by free-living bacteria (Kim, 2001). This hypothesis was further supported by Chung and Wu (2005) in the South China Sea.
The East China Sea (ECS) shelf, including the Yellow Sea and the southern sea of Korea, is one of the largest continental shelves in the world. It has a total area of 3.6 × 10 5 km 2 with a mean depth of 70 m (Fang et al., 2009;Dong et al., 2011). This sea receives great amounts of nutrients from the Changjiang (e.g., 1.1 × 10 11 mol year −1 for dissolved inorganic nitrogen; Dai et al., 2011) and also shows high primary productivity (510-580 mg C m −2 day −1 ), which is 2.7 times higher than that in the adjacent Kuroshio water (Hama et al., 1997;Gong et al., 2000). As very oligotrophic Kuroshio water in the northwestern Pacific Ocean (NWPO) flows into the East Sea (Japan Sea) through this ECS shelf, significant biogeochemical alterations occur in the shelf water (Kim et al., 2018;Cho et al., 2019). The East Sea is a semienclosed marginal sea that has a total area of 1.0 × 10 6 km 2 with a maximum depth of over 3,500 m. This interconnected system (the NWPO-the ECS shelf water-the East Sea) may provide an ideal opportunity to study how chemical species behave in different biogeochemical conditions. However, only a few studies have examined the behaviors of 210 Pb and 210 Po according to the change in environmental conditions in this region. Thus, in this study, we aim to (1) investigate the behaviors of 210 Pb and 210 Po in different oceanic settings (productive shelf water versus oligotrophic water) and (2) understand the scavenging mechanisms of both radionuclides in association with colloids.

Pb and Po Analysis
The analytical methods for 210 Pb and 210 Po were adapted from Kim and Kim (2012). Briefly, the 209 Po spike (1 dpm), Pb 2+ carrier (20 mg), and Fe 3+ carrier (50 mg) were added to the seawater samples. After the equilibration, the pH was raised to 8 using NH 4 OH to precipitate Fe(OH) 3 , together with 210 Pb and 210 Po. The precipitates were allowed to settle for 4 h. After the supernatants were siphoned off, the precipitates were filtered using Whatman 41 grade paper. The precipitates and any organic matters in the sample were fully digested with the mixed solution of concentrated HNO 3 , HCl, and HF and then converted to 0.5 M HCl. The samples were heated to 80 • C after adding ascorbic acid (0.5 g) to reduce Fe 3+ to Fe 2+ . Po from the heated samples was simultaneously plated onto a silver disk while rotating the disk for 3 h using a magnetic stirrer. The 210 Po sources were counted using alpha spectrometry with a passivated implanted planar silicon detector (Alpha Analyst, Canberra, Australia). The remaining solution was further purified for 210 Pb analysis. Concentrated HNO 3 was added to the solution and heated to oxidize the ascorbic acid. After the solution was converted to 9 M HCl, it was loaded onto the pre-conditioned anion exchange column (AG 1 × 8 resin, Bio-Rad Laboratories, Hercules, CA, United States) to separate Pb. The eluents (Pb) were stored for more than 6 months for the ingrowth of 210 Po. The 210 Pb activity was determined via the ingrown 210 Po activity using the same Po plating and alpha counting procedures. The recovery of 210 Pb was obtained by measuring stable Pb in 210 Pb solutions using a magnetic sector field inductively coupled plasma mass spectrometer (ICP-MS; Element 2, Thermo Scientific, Waltham, MA, United States).

RESULTS
In order to examine the behaviors of 210 Pb and 210 Po in different oceanic settings, our results are compared with previously published data in the northwestern Pacific seas. The data are sorted into three regions: the NWPO (Tsunogai and Nozaki, 1971;Nozaki and Tsunogai, 1976;Nozaki et al., 1990a), the ECS shelf water Hong et al., 1999;Su et al., 2017; this study), and the East Sea ; this study; Figure 1). Data on the truly dissolved and colloidal phases of 210 Pb and 210 Po are only available in this study (ECS shelf water) and in Kim and Kim (2012;East Sea). Although the stations of Lee et al. (1996) and stations E1, S1, and S4 in this study are located in the southwestern part of the East Sea, they are included in the ECS shelf water data because they are located downstream of the ECS shelf water flows (Morimoto and Yanagi, 2001;Chang et al., 2004Chang et al., , 2016. Some data near the Changjiang (Hong et al., 1999;   Tsunogai and Nozaki, 1971;Nozaki and Tsunogai, 1976;Nozaki et al., 1990a), the East China Sea (ECS) shelf water Hong et al., 1999;Su et al., 2017;this study), and the East Sea ; this study).  Su et al., 2017) and the southern Yellow Sea (Hong et al., 1999), which show unusually high activities ( 210 Po/ 210 Pb ratios > 1), are excluded since they are considered to be significantly influenced by terrestrial sources. All the analytical results of our experiments are given in Supplementary Table 1.
In the surface layer (0-25 m), the activities of total 210 Pb were lower in the ECS shelf water (14 ± 3 dpm 100 L −1 ) relative to the NWPO (20 ± 6 dpm 100 L −1 ) and the East Sea (17 ± 4 dpm 100 L −1 ; Figure 2A). The distributions of total 210 Pb generally showed maximum values in the surface layer and decreased with depth in the three regions, as observed in other major oceans (e.g., Nozaki et al., 1980;Kim, 2001;Rigaud et al., 2015;Horowitz et al., 2020). For example, the activities of total 210 Pb decreased by approximately 50, 20, and 50% from 0 to 150 m in the ECS shelf water, the NWPO, and the East Sea, respectively. In the ECS shelf water, several stations showed maximum 210 Pb activities near the bottom sediments, which were 1.5-2.0 times higher than those in the surface layer. Of the total activities, the proportions of truly dissolved, colloidal, and particulate 210 Pb in the ECS shelf water were about 32 ± 13%, 27 ± 14%, and 41 ± 24%, whereas those in the East Sea were about 34 ± 7%, 51 ± 8%, and 16 ± 6%, respectively ( Figure 3A). There was no significant difference in the activities of truly dissolved and colloidal phases between the ECS shelf water and the East Sea. However, the activities of particulate 210 Pb in the ECS shelf water were about four times higher than those in the East Sea (Supplementary Table 1).
For total 210 Po activities, there was no distinct difference in the surface layer (0-25 m) among the ECS shelf water (11 ± 3 dpm 100 L −1 ), the NWPO (11 ± 5 dpm 100 L −1 ), and the East Sea (10 ± 2 dpm 100 L −1 ; Figure 2B). As such, there was no clear trend with depth. However, there was a significant difference in the deficiency of 210 Po ( 210 Pb-210 Po) in the three regions ( Figure 2C). The most oligotrophic NWPO showed a relatively larger deficiency (9 ± 4 dpm 100 L −1 ) in the upper ocean (0-25 m) compared with those in the East Sea (7 ± 3 dpm 100 L −1 ) and the ECS shelf water (3 ± 3 dpm 100 L −1 ). The largest deficiency of 210 Po in the NWPO was observed at 200 m, while it was observed in the surface layer and decreased with depth in the ECS shelf water and the East Sea. Of the total activities, the proportions of truly dissolved, colloidal, and particulate 210 Po in the ECS shelf water were about 48 ± 19%, 31 ± 8%, and 24 ± 21%, whereas those in the East Sea were about 21 ± 7%, 36 ± 6%, and 47 ± 8%, respectively ( Figure 3B). The activities of 210 Po in the ECS shelf water were approximately 3.8, 1.7, and 1.8 times higher than those in the East Sea for the truly dissolved, colloidal, and particulate phases, respectively (Supplementary Table 1).

Steady-State and Non-steady-State Scavenging Models for 210 Pb and 210 Po
A steady-state (SS) scavenging model is used to estimate the scavenging rates of 210 Pb and 210 Po in this study, as utilized by previous studies in open ocean (e.g., Bacon et al., 1976;Obata et al., 2004;Murray et al., 2005). At steady state (∂A/∂t = 0), if advection and diffusion are neglected, the scavenging rate constants of 210 Pb and 210 Po can be calculated using the following equations: For 210 Pb: For 210 Po: where λ, A, F Atm , and k are the decay constant (day −1 ), inventory of element (dpm m −2 ), atmospheric depositional flux of 210 Pb (55 dpm m −2 day −1 ; Nozaki et al., 1973;Turekian et al., 1977), and the scavenging rate constant (year −1 ), respectively. t, td, c, and p represent the total, truly dissolved, colloidal, and particulate phases, respectively. To obtain the activities of 226 Ra in the ECS shelf water, the empirical relationship with salinity is used for the southern sea of Korea (Stn. C-1, C-2, C-3, and C-4; Yang et al., 1992Yang et al., , 1996, and the data from Wang et al. (2018c) are used for the other ECS shelf regions. The activities of 226 Ra in the NWPO and the East Sea are from previously published results (Nozaki and Tsunogai, 1976;Chung and Craig, 1980;Harada and Tsunogai, 1986;Nozaki et al., 1990b). The riverine inputs are neglected because 210 Pb is almost completely trapped in the Changjiang estuary (Wang et al., 2018b). The atmospheric input of 210 Po is also neglected since the 210 Po/ 210 Pb ratios in precipitation in this study region are lower than 0.2 (Kim et al., 2005a;Yan et al., 2012). The hydrological conditions and biogeochemical processes in the ECS shelf water are significantly affected by the intrusion of the NWPO (Wang et al., 2018a;Zuo et al., 2019;Liu et al., 2021). The chemical properties of the intruded water undergo rapid changes during the water residence times in the ECS shelf. Therefore, the removal fluxes of 210 Pb and 210 Po in the ECS shelf water can be calculated using the non-steady-state (NSS) model, accounting for the residence times of the shelf water. The removal fluxes of 210 Pb and 210 Po in the ECS shelf water are expressed by the following equations: (10) where R and F lateral are the removal flux (in disintegrations per minute per square meter per day) and the lateral transport of the radionuclide by current, respectively. Assuming that A Ra , F Atm , R, and F lateral are constant during a given time interval, the solutions for Eqs 9, 10 are expressed as follows (based on the work by Friedrich and van der Loeff, 2002): In this calculation, we assume that the water of the NWPO enters the ECS shelf at time t 1 and stays for an amount of time t (t 2t 1 ). Therefore, t is the residence time of the ECS shelf water. A t1 Frontiers in Marine Science | www.frontiersin.org and A t2 are the activities of radionuclides in the NWPO and the ECS shelf water, respectively. The lateral transport term (F lateral ) is calculated by multiplying the current velocity of ∼20 cm s −1 (Ichikawa and Beardsley, 2002;Lee et al., 2014) by the activity gradient between the NWPO and the ECS shelf water along the 400-km distance (Yangtze River mouth-Jeju Island). The calculated results using Eqs 11, 12 according to the change in residence times of the ECS shelf water are shown in Figure 4. The SS model, which accounts for the advection of water, is given for comparison.

Behaviors of 210 Pb and 210 Po
The scavenging rate constant of total 210 Pb in the ECS shelf water (3.0 ± 0.6 year −1 ) was relatively higher than that in the NWPO (2.2 ± 0.4 year −1 ) and the East Sea (2.6 ± 0.4 year −1 ) based on the SS model ( Table 1). The corresponding values of truly dissolved and colloidal 210 Pb in the ECS shelf water were also 1.2-2.0 times higher than those in the East Sea. However, the scavenging rate constant of particulate 210 Pb in the ECS shelf water was approximately 3.8 times lower than that in the East Sea, perhaps associated with the higher activities of particulate 210 Pb in the ECS shelf water. Given that the maximum activities of particulate 210 Pb were observed in the surface layer at C3 and the bottom layer at C4, respectively, such high activities of particulate 210 Pb might be attributed to the lateral input from land or the resuspension from the bottom sediments. This could occur due to the shallow water depth and by episodic storm events (Choi et al., 2004(Choi et al., , 2010. In both cases, the SS model is not appropriate for calculating the scavenging rate constant and removal flux in the ECS shelf water. Based on the NSS model, total 210 Pb was more effectively removed in the ECS shelf water (128-137 dpm m −2 day −1 ) relative to the NWPO (55 dpm m −2 day −1 ) and the East Sea (55 dpm m −2 day −1 ; Figure 5). The removal flux of total 210 Pb showed differences from 1 to 9% between the NSS and SS models within the previously reported residence times of the ECS shelf water (0.5-3.1 years; Figure 4A; Nozaki et al., 1989;Chen, 1996;Tsunogai et al., 1997;Wang et al., 2018c). These high scavenging rate and removal flux of 210 Pb in the ECS shelf water might be due to the higher concentrations of the suspended particulate matters in the ECS shelf water (6.8-15.0 mg L −1 ; Bi et al., 2020) compared with those in the NWPO (0.1-0.3 mg L −1 ; Hung and Chan, 1998) and the East Sea (0.2-0.6 mg L −1 ; Chen et al., 1996;Hong et al., 2008).
For 210 Po, the scavenging rate constant of total 210 Po in the ECS shelf water (0.3 ± 0.2 year −1 ) was much lower than that in  the NWPO (1.3 ± 0.5 year −1 ) and the East Sea (1.8 ± 0.3 year −1 ), which is opposite to the 210 Pb trend (Table 1). Especially, the truly dissolved and colloidal 210 Po in the ECS shelf water approached equilibrium with 210 Pb. The calculated results of the NSS model showed the net input of 210 Po in the ECS shelf water (7-10 dpm m −2 day −1 ), opposite to the net removal in the NWPO (20 dpm m −2 day −1 ) and the East Sea (18 dpm m −2 day −1 ; Figure 5). The net input flux of 210 Po increased with the residence times of the ECS shelf water and showed a difference from 13 to 35% between the NSS and SS models ( Figure 4B). These distinctively low scavenging rate constant and net input flux of 210 Po have been reported in the ECS (Nozaki et al., 1991), Gulf of Lion (Radakovitch et al., 1998), and northwestern Mediterranean Sea (Masqué et al., 2002). Nozaki et al. (1991) and Radakovitch et al. (1998) argued that this trend might be due to the extensive inputs of suspended particulate matters from river discharges with 210 Po/ 210 Pb ratios of ∼1. On the other hand, Masqué et al. (2002) suggested that the incorporation of 210 Po into the organic matter following the uptake by buoyant particles resulted in the low scavenging rate constant of 210 Po. In this study, we discount the riverine sources as the main reason for the low scavenging rate constant of 210 Po because the influence of river discharge with high 210 Po/ 210 Pb ratios was excluded in the comparison. In addition, the 210 Po/ 210 Pb ratios were ∼0.5 for the particulate phase and ∼1 for the total dissolved (truly dissolved + colloidal) phases in the ECS shelf water.
In general, low contents of organic carbon (0.2-1.0%) were observed in the sinking particles and the bottom sediments in the ECS shelf, associated with rapid organic carbon remineralization (Lin et al., 2000(Lin et al., , 2002Iseki et al., 2003). The results of sediment core incubation also showed that the organic carbon remineralization rate in the bottom sediments accounted for 12-24% of the primary productivity in this highly eutrophic ECS shelf water (Song et al., 2016), indicating the efficient regeneration of organic matter in the bottom sediments. In addition, hypoxia occurred intermittently in the bottom of ECS shelf water (dissolved oxygen concentrations <2-3 mg L −1 ; Chen et al., 2007), which can also increase the net input flux of 210 Po as insoluble Po(IV) can be reduced to soluble Po(II) (Balistrieri et al., 1995;Kim et al., 2005b;Kim and Kim, 2014). Considering the relatively higher proportions of the total dissolved (truly dissolved + colloidal) 210 Po in the ECS shelf water (>80%), the colloidal matter might be associated with the net input of 210 Po due to regeneration from the sinking particles and in the bottom sediments.
Thus, our results suggest that 210 Po, a proxy for sulfur group elements (S, Se, and Te), may reside longer in the water column because of active regeneration, while 210 Pb and other particlereactive elements would be removed in association with the large population of the sinking particles in the shelf water.

CONCLUSION
The scavenging rate constant and removal flux of 210 Pb and 210 Po were estimated using a geochemical scavenging model in the productive shelf system connected to the oligotrophic NWPO. The scavenging rate constant of 210 Pb was relatively higher (3.0 ± 0.6 year −1 ) in the ECS shelf water, whereas that of 210 Po was lower (0.3 ± 0.2 year −1 ) than that in the NWPO and the East Sea. In addition, a NSS model accounting for the ocean currents showed the effective removal of 210 Pb in the ECS shelf water (128-137 dpm m −2 day −1 ), whereas 210 Po showed the net input from the sinking particles and the bottom sediments (7-10 dpm m −2 day −1 ). Given that the largest proportions of 210 Pb and 210 Po were particulate and total dissolved (truly dissolved + colloidal) phases, respectively, these opposite behaviors could be due to the efficient scavenging of 210 Pb versus the efficient regeneration of 210 Po from organic matter in the ECS shelf water. Thus, our results suggest that particle-reactive elements would be effectively removed in the shelf water, whereas sulfur group elements (S, Se, and Te) might be supplied from the sinking particles and the bottom sediments by efficient regeneration.

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.

AUTHOR CONTRIBUTIONS
GK contributed to the conceptualization of the study. HS and DJ performed field sampling and analyses. HS and GK were involved in the data interpretation and writing of the manuscript. All authors contributed to the final version of the manuscript.

ACKNOWLEDGMENTS
We thank the crew members of the R/V Tamgu and R/V Isabu for their help with field sampling. We also thank all lab members for their assistance with sampling and analyses.