Radiocesium in the Taiwan Strait and the Kuroshio east of Taiwan from 2018 to 2019

The release of anthropogenic radiocesium to the North Pacific Ocean (NPO) has occurred in the past 60 years. Factors controlling 137Cs (half-life, 30.2 year) and 134Cs (half-life, 2.06 year) activity concentrations in the Kuroshio east of Taiwan and the Taiwan Strait (latitude 20° N–27° N, longitude 116° E–123° E) remain unclear. This study collected seawater samples throughout this region and analyzed 134Cs and 137Cs activity concentrations between 2018 and 2019. A principal component analysis (PCA) was performed to analyze the controlling factors of radiocesium. Results of all 134Cs activity concentrations were below the detection limit (0.5 Bq m−3). Analyses of water column 137Cs profiles revealed a primary concentration peak (2.1–2.2 Bq m−3) at a depth range of 200–400 m (potential density σθ: 25.3 to 26.1 kg m−3). The PCA result suggests that this primary peak was related to density layers in the water column. A secondary 137Cs peak (1.90 Bq m−3) was observed in the near-surface waters (σθ = 18.8 to 21.4 kg m−3) and was possibly related to upwelling and river-to-sea mixing on the shelf. In the Taiwan Strait, 137Cs activity concentrations in the near-surface waters were higher in the summer than in the winter. We suggest that upwelling facilitates the vertical transport of 137Cs at the shelf break of the western NPO.

The global fallout from the atmospheric nuclear weapons tests during the late 1950s to early 1960s is the main source of artificial radiocesium to the world ocean 1,2 and can still be discerned in the surface water, the subsurface, and deep waters (up to 600-1000 m) in the western North Pacific Ocean (NPO) 3 . After the Fukushima Daiichi nuclear power plant (FDNPP) accident on March 11th, 2011, additional anthropogenic radiocesium with long half-life 137 Cs (30.2 year) and short half-life 134 Cs (2.06 year) was released into the NPO [4][5][6][7][8][9][10][11] . Previous studies have estimated that the total amount of 137 Cs released by the FDNPP accident ranged between 15 and 27 PBq, of which a very significant portion found its way to the atmosphere and ocean 5,12,13 . Traceable, FDNPP-derived 137 Cs (latitude 37.42° N, longitude 141.03° E) follows the pathway of the North Pacific circulation toward the eastern NPO 6,9,14 . Thus 60 years after the first nuclear tests in the Pacific region, the fate of long-lives radionuclides on the western NPO and adjacent marginal seas still raises social concerns about potential health risks, e.g. associated with seafood consumption and fishing industry.
Recent studies have observed that 137 Cs can disperse through the Subtropical Mode Water (STMW) and Central Mode Water (CMW) in the western NPO 9,15 . STMW is formed right south of the Kuroshio Current and Extension (between 132° E and near the dateline) by deep vertical convection in winter [16][17][18] . CMW forms north of the Kuroshio Extension (around 36-41° N, 160° E-165° W), hence is characterised by colder temperatures and a deeper layer (250-500 m) 19 . These two water masses (i.e., STMW and CMW) circulate clockwise beneath the surface of the western NPO 20 . When plotted against depth, the vertical profiles of 137 Cs activity concentrations recorded at 20° N, 165° E in 2002 exhibited two distinct peaks: the first one at a potential density (σ θ ) of 25.5 kg m −3 (corresponding to the σ θ range of STMW) and the second one at a σ θ of 26.0 kg m −3 (corresponding to the σ θ range of CMW) 3 . The subsequent injection of FDNPP-derived radionuclides resulted in a contamination plume spreading eastward and merging with the Oyashio Current; hence the incorporation of radiocesium in the formation of STMW and CMW and its current value as a tracer of ocean circulation 4  Subtropical marginal seas of the western NPO are characterized by a monsoon cycle and seasonal coastal currents. For instance, the Taiwan Strait is affected by the northeasterly monsoon in the winter and the southwesterly monsoon in the summer 22,23 . As a result, the northern half of the Taiwan Strait is characterized by a southwardflowing coastal current in the winter while the southern half of the Taiwan Strait is characterized by a warm, northward-flowing current reinforced by the Kuroshio intrusion branch in the summer [24][25][26][27] . Furthermore, there are well documented upwelling regions in the study area, such as the waters off northeastern Taiwan 28,29 , several regions in the Taiwan Strait 30,31 , and regions in the northern SCS [32][33][34] . However, to the best of our knowledge, the effects of seasonality and upwelling on the fate of radiocesium in seawater in this study area remain unclear.
This study reports the activity concentration of 134 Cs and 137 Cs over the shelf break of the western NPO and examines the fates of these radionuclides on the shallow continental shelf. The 134 Cs and 137 Cs activity concentrations were measured on samples collected in near-surface, subsurface or deeper waters in the Kuroshio region east of Taiwan and the Taiwan Strait between 2018 and 2019. The origin of the 137 Cs maximum in the subsurface/ deep waters and the factors controlling seasonal variations in 137 Cs activity concentration in the near-surface waters are discussed.

Methods
From 2018 to 2019, surface (< 5 m), subsurface (5-200 m), and deep seawater (200-1000 m) samples were collected at sites in the Kuroshio east of Taiwan and the Taiwan Strait ( Fig. 1). Surface seawater samples (40 or 60 L) were collected mostly from fishing boats by using cleaned 20-L tanks. Subsurface samples were taken by using Niskin bottles mounted on a Conductivity-Temperature-Depth (CTD) rosette, which recorded temperature, salinity (from conductivity), and water depth (from pressure) onboard R/Vs Ocean Researcher I, II, and III. Sampling locations are shown in Fig. 1. Each 20-L sample was acidified using hydrochloric acid (11 M HCl, 100 mL) and was kept at room temperature (~ 15-30 °C) until it was transported to the Radian Monitor Center, Atomic Energy Council, Kaohsiung, Taiwan. Radiocesium was pre-concentrated by adsorption onto ammonium molybdophosphate (AMP) 35,36 and counted using a high-purity germanium (HPGe) detector with lead shielding. Each 40-L or 60-L sample was counted for 200,000 s or 120,000 s, respectively. The detection limits of both 134 Cs and 137 Cs were 0.5 Bq m −3 . In this study, we corrected all 137 Cs activity concentrations to January 1st, 2020. This date was also applied to data in earlier studies for comparison purposes.
Total alkalinity (TA) samples were collected together with nearly 61% of radiocesium samples (92% of 49 subsurface and deep waters, and 55% of 242 near-surface waters). TA water samples were taken into 250-mL borosilicate glass bottles and poisoned immediately with 100-µL saturated HgCl 2 solution to eliminate biological activities. We followed the open-cell Gran titration method with a temperature-controlled, semi-automated titrator (AS-ALK2 Apollo Scitech) to determine TA value of each sample. TA measurements were referenced against certified reference materials from A. G. Dickson's laboratory at Scripps Institution of Oceanography with a precision of 0.1% 37 . TA is usually treated as a conservative tracer. We used it to determine the water sources and possible mixing processes between fresh water and seawater by normalizing TA values to salinity 35 (NTA = (TA/S) × 35) 38 .
As variables can be collectively controlled by major oceanographic mechanisms, principal component analysis (PCA) 39,40 serves as a multivariate analysis tool to catch the major features of a dataset. PCA can analyze intercorrelations among these variables and reduces the dimension of a dataset. The major factors affecting this dataset is thus obtained. The result is displayed as a subset of new, independent (orthogonal) variables which are referred to as dimensions. The higher the coordinates of a dimension are, the greater the amount of co-variability among the original variables this dimension explains. The results were presented graphically as plots with each dimension and length represented the relationship and weight to the principal components, correspondingly. We applied PCA using R software 41 on our data set for which four variables had been determined: salinity, temperature, σ θ , and 137 Cs activity concentrations from the surface layer to a depth of 400 m. The oceanographic context is then used to interpret the meaning of each dimension.

Results
Surface water properties and the distribution of 134 Cs and 137 Cs. Surface water samples were obtained from depths of less than 5 m, with temperatures of 9.7-34.9 °C and salinities of 21.8-34.2 psu (Figs. 2 and 3a). Salinity, TA, and σ θ displayed large variations in surface waters (Fig. 3). Salinities were comprised between 35 and 21 psu and σ θ was usually lower than 24 kg m −3 (Fig. 3a,b), indicating mixing between seawater and fresh water. The average TA in surface waters was 2243 ± 38 μmol kg −1 . NTA values associated with low σ θ values, i.e., surface waters, deviated significantly from the average value determined in subsurface and deep waters (2309 μmol kg −1 ) (Fig. 3d), implying that TA values in surface waters were likely to be affected by additional river TA sources.
In our samples, 134 Cs activity concentrations were under the detection limit (0.5 Bq m −3 ), and 137 Cs activity concentrations ranged from 0.5 to 2.0 Bq m −3 (Fig. 3e,f), with an average of 1.2 ± 0.3 Bq m −3 in the surface water ( Supplementary Fig. S1). We also noticed a peak in the surface water 137 Cs vertical profile (Fig. 3f)  www.nature.com/scientificreports/ In the surface waters, the 137 Cs values binned in one-degree latitude bands were higher between 25 to 26° N than the ones between 21 to 22° N in the Kuroshio and its adjacent waters (approximately to the east of 121° E in our study area) (Fig. 4a). Binned 137 Cs activity concentrations were close to each other to the west of 121° E (Fig. 4b).
The sea surface temperature (SST) distribution in 2018 displayed a general pattern, where SST values of less than 25 °C were found in the southern ECS and the northern Taiwan Strait while SST values over 27 °C were common for the Kuroshio and the Luzon Strait (Fig. 5). The SST in the northern Taiwan Strait and southern ECS showed strong seasonal variations, displaying SST over 25 °C during the summer-like months (i.e., July-September) and less than 25 °C during winter-like months (i.e., January-March) (Supplementary Fig. S2). The SST in shelf waters of the northern Taiwan Strait displayed stronger seasonal variations than those in the pelagic Kuroshio waters east of Taiwan.
In the shelf waters, including the Taiwan Strait and the waters off northern Taiwan, the average 137 Cs activity concentration was statistically higher in August than in February (two-tailed t-test, p < 0.05) (Fig. 6a). A statistically significant relationship was observed between monthly variations of 137 Cs and temperature (Fig. 6b). Monthly values of 137 Cs (Fig. 6a)  . TA values in the subsurface and deep waters varied in a narrow range (Fig. 3c). The average and standard deviation of NTA value for waters between 5 to 400 m was 2309 ± 5 μmol kg −1 (Fig. 3d).
At station NTU2 in the Kuroshio region, 134 Cs activities were below the detection limit (0.5 Bq m −3 ), and 137 Cs activities were lower than 2.5 Bq m −3 from the surface to a depth of 1000 m (Fig. 3e). Moreover, two layers of elevated 137 Cs activities were observed: 137 Cs activities were mostly higher than 1 Bq m −3 from 0 to 400 m and also higher than 2 Bq m −3 from 200 to 400 m. By contrast, they were lower than 1 Bq m −3 from 600 to 1000 m (Fig. 3f). A synthesis of these results showed that low 137 Cs activity concentrations (1.5 to 0.6 Bq m −3 ) corresponded to the high σ θ (> 25 kg m −3 ) waters between 400 and 1000 m (Fig. 3e,f).

Discussion
The first three dimensions of the PCA results explained 91% of all variations, including sample temperature, salinity, and σ θ , and 137 Cs activity concentration above the depth of 400 m. Dimension 1 explained 54% of the variations (Fig. 7a,b) and was dominated by σ θ , temperature, and salinity ( Table 2). σ θ , salinity, and 137 Cs were positively correlated with Dimension 1 while the temperature was negatively correlated (Fig. 7a). We suggest that Dimension 1 represents density-induced water layer distributions and explains the primary peak of 137 Cs in the deep waters. This suggestion is consistent with the fact that σ θ is positively correlated with the variables that have a high loading on Dimension 1 (Fig. 7c) and is a marker for the two layers of elevated 137 Cs in the top 400 m of the water column.
The highest coordinate of Dimension 2 corresponds to the secondary peak of 137 Cs in the surface waters (Fig. 7d), implying that Dimension 2 represents a factor that led to the secondary 137 Cs peak. The plot of Dimension 2 coordinates against σ θ (Fig. 7d) can be divided into a high σ θ (> 22 kg m −3 ) arm and a low σ θ (< 22 kg m −3 ) www.nature.com/scientificreports/ arm. As both temperature and salinity were positively correlated with Dimension 2 (Fig. 7a, Table 2), we hypothesize that the high σ θ arm was caused by upwelling which transports high salinity water toward the surface and reduces the thickness of the lens of warm surface water in this study area. Upwelling near the coast of Taiwan and in the Taiwan Strait is known to transport subsurface waters (as deep as 80 m to 100 m) to the near-surface layer. The vertical velocity of upwelling off northeastern Taiwan (Fig. 1) [42][43][44][45] has been estimated to be 15 m day −1 on the shelf and over 40 m day −1 at the shelf edge 29,46 . The σ θ of water with salinity = 34.3 psu, temperature = 18.3 °C, and σ θ = 25.0 kg m −3 at a depth of 200 m, can decrease to less than 22 kg m −3 if the water temperature increases to 28 °C at 1 m during the upwelling process (Fig. 2a). This annual upwelling to the northeastern Taiwan may lead to the higher binned 137 Cs between 25 and 26° N than the others to the east of 121°E in the near-surface waters (Fig. 4a). Another driving force of annual upwelling is internal tide, which can induce upwelling in the waters off northeastern Taiwan 47 and off southern Taiwan [48][49][50] . Moreover, this transition σ θ of 22 kg m −3 in Fig. 7d was also consistent with the transition range of σ θ where NTA positively deviated from 2309 ± 5 μmol kg −1 in the near-surface water (Fig. 3d). This deviation of NTA in low σ θ waters indicates freshwater inputs from terrestrial runoff. To sum up, we suggest that mixing between riverine freshwater and seawater is responsible for the lower σ θ arm while upwelling drives the higher σ θ arm in Fig. 7d. Dimension 3 accounted for no more of the variance than 137 Cs itself ( Table 2, Fig. 7b), suggesting that it was controlled by the chemical characteristics of 137 Cs. MacKenzie et al. 51 have argued that high freshwater discharge from land can remobilize 137 Cs from surface sediments (< 10 cm). Future work should be conducted towards a dynamic representation of radionuclide transfer among freshwater, seawater, sediment, and the biological compartments 11 .
The seasonal variation of the 137 Cs activity concentration in the Taiwan Strait (Fig. 6a) reflects the seasonal intrusions of waters from Kuroshio intrusion, ECS, and SCS. Wu et al. 19 corrected their 137 Cs activity concentrations to the same date as this study, leading to a mean of 0.71 ± 0.27 Bq m −3 in the surface ECS and an average of 0.92 ± 0.28 Bq m −3 in the surface SCS. These results are consistent with our observation that southward-flowing cold waters with low 137 Cs values intruded into the northern half of the shallow Taiwan Strait during the winter while the reverse took place during the summer (Fig. 6a) 22,24,25 . In addition to the Kuroshio offshoot transporting warm waters with higher 137 Cs values in the summer, the Pearl river plume can also intrude into the southern Taiwan Strait during the summer 52 . It follows that the slightly lower 137 Cs activity concentration during July  www.nature.com/scientificreports/ indicates that the effect of the intrusion of Kuroshio is more than offset by the amount of warm water with lower 137 Cs activity originating from the SCS. The maximum in 137 Cs activity concentration was observed in a specific range of σ θ in the subsurface and deep waters (Fig. 3e,f), implying a lateral transport along the 125-400 m depth horizon in addition to local atmospheric fallout. Local and modern atmospheric 137 Cs fallout can only affect the average 137 Cs values in the surface waters (Table 1). 137 Cs activity concentrations in the subsurface water of the study area displayed characteristics (σ θ = 25.2 and 26.1 kg m −3 ) which were similar to those of STMW and CMW (σ θ = 25.3 to 26.3 kg m −3 ) in NPO 4 (Fig. 3). Some surface NTA values and also the average NTA value in subsurface waters (2309 ± 5 μmol kg −1 ) of this study were consistent with NTA values previously reported in the surface western NPO (2301 ± 9 to 2299 ± 5.4 μmol kg −1 ) 53,54 . The maximum 137 Cs activity concentration at a depth of 300 to 400 m at 165° E before the FDNPP event should be 1.65 Bq m −3 (corrected to January 1st, 2020) 3 . After the FDNPP event in June/July 2012, 137 Cs activity concentrations at depths of between 0 and 600 m in the western NPO (25 to 45° N, 165° E) were between 2.1 and higher than 8.4 Bq m −3 (corrected to January 1st, 2020) 4 . As the half-life of 134 Cs is shorter than that of 137 Cs, 134 Cs/ 137 Cs is assumed to be 1.000 at 165° E; it became 0.095 after 7.5 year (July 2012 to December 2020). Since 137 Cs activity concentration is already low (< 2.1 Bq m −3 ) in this study area, 134 Cs is expected to be < 0.2 Bq m −3 which is lower than the detection limit (0.5 Bq m −3 ) in this study.  (a) 137 Cs activity concentration and corresponding seawater temperature were measured at the study sites on both sides of the Taiwan Strait and the waters off northern Taiwan (refer to Fig. 1b). Both parameters displayed seasonal variations: low in winter and high in summer. (b) The monthly 137 Cs activity concentration was statistically correlated to its corresponding seawater temperature.  55 reported that approximately 43% of FDNPP-derived 137 Cs could be delivered to below the mixed layer through eddy processes. In  www.nature.com/scientificreports/ addition, 137 Cs in STMW and CMW appears to be transported clockwise toward the western boundary of the NPO 3,56-59 . This subsurface or deep-water layer corresponding to σ θ = 26.7 kg m −3 can further rise westward and reach the shelf break surrounding Taiwan [60][61][62][63][64][65][66] . East of Taiwan, the Kuroshio is a swift and powerful current that can reach as deep as 400-600 m 67 . While the primary 137 Cs maximum centered around σ θ of 25.3 to 26.1 kg m −3 is suspected to be from lateral transportation from the NPO, there is still a research gap between pelagic studies in the NPO and shelf break data in this study area. For example, impacts of interleaving 68 and meso-scale eddies 69 on the cross-Kuroshio transport mechanism of 137 Cs are still unclear. Direct evidence to constrain the origin and evolution of the 137 Cs maxima along 165° E to this study area is needed in the future. We suggest integrating multiple chemical tracers to study the complex circulation across the pelagic NPO to its western shelf boundary in the future.