Biological pumps of carbon, nitrogen, and phosphorus in the northern South China Sea

This paper presents the measured biological pumps (BPs) of carbon (C), nitrogen (N), and phosphorus (P) and their response to seasonal and event-driven oceanographic changes in the northern South China Sea (NSCS). The BP is defined as the sum of active and passive fluxes of biogenic carbon in the surface layer, which may be considered as the central part of marine carbon cycle. These active and passive fluxes of N and P were also considered to understand stoichiometric flux patterns and the 10 roles of nutrients involved in the BP. The magnitudes of total C, N, and P fluxes were respectively estimated to be 71.9347 (mean: 163) mg C m d, 13.030.5 (mean: 21.6) mg N m d, and 1.022.97 (mean: 1.94) mg P m d, which were higher than most previously reported BPs in open oceans, likely because a quarter of the BPs was contributed from active fluxes that were unaccounted for in BPs previously. Moreover, the passive fluxes dominated the BPs and were estimated as 65.3255 (mean: 125) mg C m d (76.7% of total C flux), 11.923.2 (mean: 17.6) mg N m d (83.0% of total N flux), and 0.891.98 (mean: 15 1.44) mg P m d (74.2% of total P flux). Vertical fluxes of dissolved organic C, N, and P generally contributed to less than 5% of passive fluxes. The contrasting patterns of active and passive fluxes found between summer and winter could mainly be attributed to surface warming and stratification in summer and cooling and wind-induced turbulence for pumping nutrients into the euphotic zone in winter. In addition to seasonal variations, the impacts of anticyclonic eddies and internal-wave events on BP enhancement was apparent in the NSCS. Both active and passive fluxes were likely driven by nutrient availability within the 20 euphotic zone, which was ultimately controlled by the changes in internal and external forcings. The nutrient availability also determined the inventory of chlorophyll a and new production, thereby allowing the prediction of active and passive fluxes for unmeasured events. To a first approximation, the SCS may effectively transfer 0.208 Gt C yr into the ocean’s interior, accounting for approximately 1.89% of the global C flux. The internal forcing and climatic conditions are likely critical factors in determining the seasonal and event-driven variability of BP in the NSCS. 25

4 (Wyrtki 1961, Shaw andChao 1994;Hu et al. 2000). As a result, the physical and biogeochemical conditions of NSCS were profoundly influenced by seasonal changes of climatic forcing and terrestrial inputs (Shaw and Chao 1994;Dai et al. 2013). The 80 NSCS is also a hot spot of internal waves generated in the Luzon Strait and transport westward from the Luzon Strait to the Dongsha-Atoll (DA) continental shelf, causing significant impacts on the DA-associated environments following internal-waves dissipation and shoaling events (Wang et al. 2007, Li andFarmer 2011;Alford et al. 2015). Therefore, the vertical transfers of C, N, and P may vary temporally and spatially under the impacts of atmospheric and oceanic forcings in the NSCS. Despite many reports have shown a balance or a tiny physical pump of carbon dioxide in most oligotrophic regimes (Zhai et al. 2005, 85 2012; Dai et al. 2013), the study of BPs is essential and urgent because the limited data have been published so far in realizing the states and involved processes of BPs in the NSCS. Our ultimate goals focus primarily on understanding the current strengths of BPs and their controlling mechanisms in the oligotrophic NSCS.

Study area and sampling locations 90
Figure 1 depicts the study area and sampling stations which are located on various regimes in the NSCS. Except for stations located on the Dongsha-Atoll (DA) associated shelf and upper slope under the influence of internal-wave events, most sampling stations were located on lower slope and basin regions. To avoid confusion for different names on the same location in different expeditions, the sampling stations were re-named numerically (Sts. 111) to clearly identify them among locations and expeditions ( Table 1). The Station #11 is the Southeast Asian Time-series Study (SEATS) station in the NSCS. 95

Sampling procedures and analytical methods in seawater
Seawater samplings and electronic data retrieval were carried out on board R/V Ocean Researcher I (ORI-1039, ORI-1059, ORI-1074, ORI-1082), and R/V Ocean Researcher III (ORIII-1073, ORIII-1184 and ORIII-1214) ( Table 1). Seawater samples were collected using cleaned Niskin bottle (20 L) mounted on a CTD/Rosette from six light penetration depths (100%, 46%, 38%, 13%, 5% and 0.6%) in the euphotic zone, and from various depths in the aphotic zone in each station to determine 130 hydrological and biogeochemical parameters. Seawater temperature (T), salinity (S), depth, and fluorescence were recorded with CTD and attached probes. Surface and subsurface irradiances were measured with a PAR sensor (OSP2001, Biospherical Instrument, San Diego, USA). The scientific echo sounder (Simrad EK60) including 38 kHz and 120 kHz was used for recording the signals of diel migrators located at different depths throughout expeditions. The euphotic zone was recorded as the depth at which light intensity was 0.6% of surface irradiation (Chen, 2005). The mixed layer depth was estimated from a difference of 135 potential density (<0.125) between that of the ocean surface and the bottom of the mixed layer (Monterey and Levitus 1997).
The stratification index (SI) was defined as the averaged density difference (kg m -4 ) between the surface and a depth of 150 m (Chen et al., 2014).
The concentration of dissolved oxygen (DO) in retrieved seawater was determined immediately by following a method of direct spectrophotometry of total iodine (Pai et al. 1993). The content of chlorophyll a (Chl-a) was determined with a fluorometer 140 (Turner Designs, according to the method of Welschmeyer (1994) (Grasshoff et al. 1983) with a UV-Vis spectrophotometer (Hitachi U-3310) equipped with a module of flow injection analysis for subsurface and deep water samples. DIN and DIP in oligotrophic surface samples were determined by the chemiluminescent method (Garside 1982;Hung et al. 2007) and modified MAGIC method (Thomson-Bulldis and Karl 1998;Hung et al. 2007), respectively. The averaged concentrations and inventories of Chl-a, DIN and DIP in the euphotic zone were estimated from the mean value and trapezoidal integration of all determinants through the euphotic zone, respectively. DOC 150 was measured using a method of high-temperature catalytic oxidation via the Shimadzu TOC-5000A analyzer following the established procedures (Hung et al. 2007(Hung et al. , 2008. The quality of DOC data was regularly monitored using reference materials (41-44 M C) provided by Dr. D. A. Hansell from the University of Miami. DON was determined from the difference between dissolved inorganic nitrogen (DIN = NO2  + NO3  ) and total dissolved nitrogen (TDN) that was measured with the chemiluminescence method using an instrument of Anteck Models 771/720 (Hung et al. 2007(Hung et al. , 2008. DOP was determined from 155 the difference between DIP and total dissolved phosphorus (TDP) that was measured with UV-persulfate oxidation and colorimetric method (Ridal and Moore 1990).The precision of TDN and TDP analyses was better than ±7% and ±5%, respectively [Hung et al., 2007[Hung et al., , 2008.
POC and particulate organic nitrogen (PON) in filtered particulates were determined with an elemental analyzer (Thermo Scientific Flash 2000) after removal of carbonate from particulates with 2 M HCl (Hung et al. 2007(Hung et al. , 2008. The analytical 160 precisions of POC and PON were generally < 0.3 M C(N) ( 1), as evaluated from eight replica samples collected from the same depth. Each biogeochemical parameter was measured in triplicate ensuring the data quality of analyses in the laboratory (Hung et al. 2007(Hung et al. , 2008.

Estimates of active fluxes of carbon, nitrogen and phosphorus
The active flux was determined by collecting diel migrators with a zooplankton net (NORPAC net,200 m mesh,165 L: 180 cm) coupled with a flow meter (Hydrobios, German) during three day-time (10:00~13:00) and night-time (22:00 ~ 01:00) plankton tows. The difference of integrated biomass profiles in the upper 200-m layer between night and day was regarded as an estimate of the zooplankton and micronekton migrant biomass. The zooplankton net was towed obliquely under 1.52.5 knots through the upper layer of 200 m in each sampling time. After collection, the collecting time and water volume were recorded and the zooplankton and micronekton samples were cleaned with in-situ seawater followed by Milli-Q water and stored in sealed 170 https://doi.org/10.5194/bg-2021-17 Preprint. Discussion started: 21 April 2021 c Author(s) 2021. CC BY 4.0 License. 9 plastic bags. The samples were frozen immediately with liquid nitrogen and stored at -20 ℃ until further treatment and analyses in the land-based laboratory. In the laboratory, the migrators were size fractionated according to the previously reported methods (Hannides et al., 2009;Al-Mutairi and Landry, 2001) by passing through 0.2, 0.5, 1.0, 2.0, and 5.0-mm sieves. The each size sample was equally split into two parts for experimental purposes. One part was used for immediate analyses of Chl-a and phaeopigment contents and the remainder was used for species identification (data not reported here) and numeration. The 175 zooplankton and micronekton abundance (A, inds m 3 ) of each class was estimated from total individuals (inds) divided by the flowed water volume (V). The other part was filtered through pre-weighed Nucleopore PC filter (5 m, 47 mm) to determine the dry-weight (DW) biomass (mg m 3 ) of various planktonic sizes after drying filtered samples in an oven at 60 C for 3 days. The total migrant biomass was defined by the sum of various sized migrant biomass derived from the difference of sized zooplanktonmicronekton biomass between night-time and day-time tows. The body contents of organic C, N, and P were determined by 180 measuring a specific amount of homogenized dried biomass with same analytical procedures described in the next section for settling materials.
The total active flux reported here includes gut, excretory, respiratory, and mortality fluxes by zooplankton and micronekton (Hannides et al. 2009;Hernández-León et al. 2019). The gut carbon flux was converted from gut Chl-a flux (carbon/Chl-a = 30, Vidal 1980), and the gut Chl-a flux was estimated from gut contents (gut contents = Chl-a + 1.5  [phaeopigment]) and gut 185 clearance rate constants (k, h 1 ) according to the methods of Dagg and Wyman (1983) and Dam and Peterson (1988). The Chla and phaeopigment contents in zooplankton and micronekton were determined by following the acidification method of Strickland and Parsons (1972). The excretory fluxes of C, N and P were defined as the fluxes of DOC, (DIN+DON), and (DIP+DOP), where DOC, DIN, DON, DIP and DOP fluxes were estimated from migrant DW biomass using empirical allometric relationships reported by Al-Mutairi and Landry (2001). The excretory rates of ammonia (EDIN, gN ind 1 h 1 ) and phosphate 190 (EDIP, gP ind -1 h -1 ) were estimated according to Eq. 1 and Eq. 2 ln EDIN =  2.8900 + 0.7616ln DW + 0.0511T (T is mean temperature at 300500 m daytime seawater) (1) ln EDIP =  4.3489 + 0.7983ln DW + 0.0285T (T is mean temperature at 300500 m daytime seawater) The magnitude of organic excretion by l migrators was estimated by assuming organic products represent a constant fraction of the total amount of waste by-products released by migrators at depths (Hannides et al. 2009). The fraction was 0.24 for organic 195 https://doi.org/10.5194/bg-2021-17 Preprint. Discussion started: 21 April 2021 c Author(s) 2021. CC BY 4.0 License.

Experiments on passive fluxes of organic carbon, nitrogen and phosphorus
As an exclusive part of passive flux, the vertical fluxes of settling POC, PON, and particulate organic phosphorus (POP) 210 were determined by using floating sediment traps for particle collection followed by elemental analyses. The traps were deployed generally for three depths (50m, 100m, 150m) in a planned station for approximately 13 days, depending on the oceanic condition and ship time availability, to collect sinking particles from upper layers. The sediment-trap array modified from Knauer et al. (1979) consists of two trap sets made from eight Plexiglass tubes (aspect ratio of 9.53) attached to a polypropylene cross frame, similar to those described by Wei et al. (1994), for the depth of 50 m and 100 m, and a commercial sediment trap 215 (PARFLUX Mark8-13, McLane, USA) for a depth of 150 m. All sample tubes were filled with saline seawater to minimize the loss of collected sinking particles. However, no poisons were added to retard bacterial growth and decomposition. In the particular area of DA associated shelf, the PARFLUX trap was attached to the thermistic-fluoroscence string moored at the planned location. After collection, the particulate matter was removed from the PC filter (Polycarbonate, 90 mm, pore size 0.4 µm), washed with Q-water to remove sea salts. After removing swimmers, the particulate matter was freeze-dried to determine 220 https://doi.org/10.5194/bg-2021-17 Preprint. Discussion started: 21 April 2021 c Author(s) 2021. CC BY 4.0 License. settling fluxes of sinking particles and POC, PON, and POP. In an earlier experiment, vertical fluxes of POC at a depth of 120 m were measured through summer and winter by a deep-moored time-series trap (TECNICAP P.P.S. 3/3) deployed near the SEATS station following the deployed method described in Hung et al (1999) and Chung and Hung (2000).
POC and PON were analyzed by placing collected particulate matter in a silver cup and a few drops of 2 M HCl was added to remove carbonate. The acidified sample was dried in an oven and then determined with an elemental analyzer (Thermo 225 Scientific Flash 2000). Another fraction of particulate matter without treating acid was used for total carbon (TC) analyses.
Particulate inorganic carbon (PIC) was the difference between TC and POC. Organic matter content was estimated from POC content by a factor of 2 (Gordon 1970;Monaco et al.1990). Particulate organic phosphorus (POP) was determined from the difference between total particulate phosphorus (PP) and particulate inorganic phosphorus (PIP). PIP was determined by the extraction of particulate matter with 1 M HCl (wt/vol = 50) for 24 hr and the extracted solution was determined by the DIP 230 method described above (Aspila et al. 1976). The concentration of PP was determined by combusting particulate matter at 550 C for 6 hr followed by extraction and measurement as the same procedures for PIP (Aspila et al. 1976). Analytical uncertainty was < 6% (n = 6) evaluated from repeated analyses for a coastal sediment. Vertical fluxes of particulate matter, POC, PON, and POP were determined by dividing the collected mass and elements at a specific depth with the trapping area and time period of deployed trap. 235 Despite of playing minor role in passive fluxes, the downward fluxes of DOC, DON and DOP through a depth of 100 m were estimated from Fick's Law of diffusion (Eq. 7) Where F(100) is the flux of DOC (N, P) through a depth of 100 m, Kz is vertical turbulent coefficient, and dC/dz is the gradient of measured parameter concentrations across the boundary. The concentration gradient (dC/dz) of DOC (N, P) was calculated from 240 the difference of mean concentrations ( 1 2) divided by the mean depth interval ( 2 -1) between two 100-m layers that were above and below the considered boundary (Hung et al., 2007). The Kz was derived from the dissipation rate (), the Richardson number (Rf) and the square of the Brunt-Väisälä frequency (N  ((-g/p)(dp/dz)) 1/2 ) at the pycnocline. Therefore, the https://doi.org/10.5194/bg-2021-17 Preprint. Discussion started: 21 April 2021 c Author(s) 2021. CC BY 4.0 License.

Measurements of primary productivity and new production
Primary productivity (PP) and nitrate-uptake new production (NP) were measured through deck incubation by adding NaH 13 CO3 and Na 15 NO3 into seawater respectively, following the methods of Chen et al. (2008a). Briefly, water samples were collected from the same six depths in the euphotic zone.. The collected seawater was transferred immediately into two sets of three transparent polycarbonate bottles (2.3 L), one set for primary production measurement and the other for new production 250 measurement. Each set included two light bottles and one dark bottle. The bottles were covered with layers of neutral density screen to simulate irradiances at the sampling depths and incubated on deck under natural light in incubators circulated with flow-through surface seawater, starting at approximately 08:00-09:00 h and lasting for 3 h. After incubation, the concentrations of particulate organic carbon, particulate nitrogen, and the isotopic ratios of 13 C : 12 C and 15 N : 14 N were measured by an automatic carbon-nitrogen elemental analyser (ANCA) 20-20 mass spectrometer (Europa Scientific). Details of calculation for PP and NP 255 can be referred to Chen et al. (2008a).

Hydrographic characteristics
The oceanographic conditions in the coast-excluded NSCS domains were likely dominated by monsoon-mediated surface circulation and Kuroshio intrusion (Chen et al., 2005;Dai et al., 2013;Hung et al., 2007Hung et al., , 2020Liu et al., 2002;Zhai et al., 2005Zhai et al., , 260 2013). In general, a strong northeast monsoon prevails between November and April and a weak southwest monsoon prevails between June and September leading to a basin-wide cyclonic circulation being dominant in winter and an anticyclonic circulation being dominant in summer (Shaw and Chao, 1994;Liu et al., 2002;Wong et al., 2007). Thus, Stations 1 and 2 sampled in summer (July, 2013) exhibited similar distribution (0300 m) of high surface temperature (T), low surface salinity (S), and low surface Chl-a concentration with a subsurface maximum (Fig. 2). The mixed layer was shallow (2027 m) and the TS 265 diagram reveals that their characteristics were similar to the typical pattern in South China Sea Water (SCSW; Fig. 3a). Stations 3a), influenced apparently by the intrusion of KW. Stations 3 and 4 were located inside and outside the anticyclonic eddy (Chen et al., 2015), respectively, with a pronounced deeper mixed layer (160 m vs. 85 m) and higher Chl-a at Station 3 than at Station 270 4. Stations 5 and 6 sampled in later spring (May, 2014) displayed similar patterns with those (T, S, and Chl-a) in summer (Stations 1 and 2; Fig. 2). The T-S features belong to certain extents between summer and winter (Fig. 3a).
Station 7 sampled at the location close to the Dongsha Atoll in summer (June, 2014) was influenced by the internal-wave (IW) shoaling activity, and exhibited low surface T and high surface S and Chl-a, attributed apparently to the upwelling events   ). Higher mesozooplankton biomass and abundance were observed in night tows than in day tows for all size classes; the 305 occurrence of small mesozooplankton (0.22.0 mm) was generally higher than that of large mesozooplankton (2.05.0 mm), except for the highest occurrence of large (0.25.0 mm) mesozooplankton in winter (Table 2). However, the magnitude of migrant biomass (night minus day) was usually the largest for the 2.05.0 mm class, except during an internal-wave event in summer ( Table 2). The total migrant biomass (sum of all sizes) was 474 mg m 2 in late spring, ranged from 235 to 418 (mean: 327) mg m 2 in summer, was 635 mg m 2 in winter with an anticyclonic event, and ranged from 158 to 189 (mean: 174 ) mg m 2 310 https://doi.org/10.5194/bg-2021-17 Preprint. Discussion started: 21 April 2021 c Author(s) 2021. CC BY 4.0 License. during fall at SEATS station (Table 2). An elevated biomass of 997 mg m 2 was observed in the internal-wave influencing fields in summer ( Table 2). The night/day ratio of migrant biomass was higher for large mesozooplankton (2.153.12 for size 2.05.0 mm) than for small mesozooplankton (1.212.09 for size 0.20.51.0 mm), coincident with the size distribution of migrant biomass ( Table 2). This implied that larger migrators might play crucial roles than smaller migrators in determining the vertical transport of materials and elements. 315
Resolving spatial and seasonal variations in active fluxes in the NSCS is difficult because of unsuccessful sampling at certain stations and cruises. Nevertheless, for the first-order approximation, the active fluxes that could not be measured were estimated using the empirical relationship established from the experimental data of active fluxes and Chl-a inventories (Fig. 5).
Thus, the compiled active fluxes of C, N, and P were 7.6993.4 mg C m 2 d 1 , 1.067.26 mg N m 2 d 1 , 0.130.99 mg P m 2 d 1 , 355 respectively (Fig. 6). The flux distribution was the highest in summer due to the impact of internal-wave upwelling, followed by in winter with an anticyclonic eddy, and finally, in summer with a calm oceanic condition. The smallest values were found in the fall season under relatively calm condition (Fig. 3)  in summer with the internal-wave upwelling field and to 1753.5 mg C m 2 d 1 in winter within the anticyclonic eddy (Table 3, Fig. 7). At the SEATS station located in the central basin, the POC fluxes ranged from 51.4 mg C m 2 d 1 during fall to 100 mg 385 C m 2 d 1 during winter (Table 3). Additional data obtained from previous sequentially moored traps at the SEATS station at a depth of 120 m revealed extremely high fluxes (199254 mg C m 2 d 1 ) in winter (SEATS-W2, SEATS-W3; Fig. 7). Although data on PON and POP fluxes were limited, the data predicted after the addition of POC:PON and POC:POP ratios the seasonal and event-effected patterns followed apparently with the variability of POC fluxes (Table 3).
The molar ratios of POC:PON ranged from 5.650.20 (at 50 m) to 8.000.15 (at 100 m), with an overall value of 390 approximately 6.840.60 (data not shown). The C:N ratio increased slightly from 50 to 150 m, likely attributed to the rapid decay of PON over POC with increasing depth. The mean ratio was close to the Redfield ratio (6.6; Redfield, 1958), indicating a relatively low contribution of lithogenic POC sources. The molar ratios of POC:POP ranged from 1521.57 (at 50 m) to 24315.3 (at 150 m), with an overall value of approximately 1949.5. The increase in C:P ratios with increasing depth was more pronounced than that of C:N ratios, indicating that POP was more labile PON in settling organic matter. The C:N and C:P ratios 395 were applied to the estimation of the PON and POP fluxes not obtained from the measured POC fluxes presented in Table 3.

Summer-IWs denotes the internal-wave event in summer; Winter-In denotes values inside the anticyclonic eddy in winter; 400
Winter-out denotes values outside the anticyclonic eddy in winter. SEATS-W1, S1, S2, F1, F2, F3, W2, and W3 represent various samplings at winter (W), summer (S) and fall (F) seasons at the SEATS station.SEATS-W2 and W3 data were obtained from the bottom-moored traps at a depth of 120 m (see Fig. 11). Other SEATS data were derived from integrating data of the new production and Chl-a (see Figs. 9 and 10) except for data of SEATS-F1, which were obtained from the  # POC fluxes were derived from integrated new production (see Fig. 9); @ POC fluxes were derived from Chl-a inventories in the euphotic zone (see Fig. 9a); PON and POP fluxes in parentheses were estimated from POC fluxes and C:N and C:P ratios.  Table S1). Moreover, the larger migrators, particularly those of sizes 25 mm, appeared to be dominant in transporting C, N, and P into mesopelagic zones (Table 2) The NSCS experiences contrasting atmospheric and oceanic forcings between the winter and summer including most of the time during spring and fall (Liu et al., 2002;Hung et al., 2020). In general, the upper-ocean stratification progressed from spring to summer (SI, 0.0250.04 kg m 4 ) with an increase in temperature and weak southwesterly monsoon winds, after which the stratification began to erode from fall to winter (SI, < 0.01 kg m 4 ) due to surface-water cooling and the prevailing northeasterly monsoon winds. The subsurface nutrient pumping through the eutrophic base may intensify the entry into the winter season. 460 Thus, the discrete contents and inventories of nutrients and Chl-a in the euphotic zone were considerably higher in winter than in summer in the NSCS, excluding the coastal and shelf zones reported in our previous studies (Hung et al., 2007;Chen et al., 2008Chen et al., , 2014 and in the current experiments. To obtain a complete data set of active fluxes for seasonal comparison, the flux data that could not be collected were derived from the data of Chl-a and DIN inventories using appropriate correlations between active carbon fluxes and Chl-a inventories (r = 0.9247, p <0.002; Fig. 5a) and between active carbon fluxes and DIN 465 inventories (r = 0.9641, p <0.0001; Fig. 5b) constructed from the successfully collected data in the current study. These empirical relationships may also indicate that the active fluxes were driven by the availability of nutrients (DIN) in the euphotic zone, which in turn determined Chl-a inventories because of a significant correlation between integrated DIN and integrated Chl-a (r = 0.9479, p < 0.0001).
In the northern regime, active fluxes were generally higher in winter than in spring and summer, likely due to the increase 470 of nutrient pumping in winter. In addition, the active flux was slightly higher in the region within the anticyclonic eddy (St. 3) than the in the region located outside the eddy (St. 4; Fig. 5), as a result of the eddy-enhanced nutrient pumping to the euphotic zone. Chen et al. (2015) demonstrated that this anticyclonic eddy occurring during winter was characterized by a deep mixed layer of up to 140180 m and the concentration of nitrate and Chl-a increased in the top water column (0200 m), resulting in an increase in primary productivity and new production. Thus, the nutrient pumping in the euphotic zone appears to be the major 475 driver enhancing the active carbon fluxes in winter and in anticyclonic eddy-driven events. The extremely high active carbon flux that occurred in the internal-wave influencing field near the Dongsha Atoll was also attributed to the strong nutrient upwelling caused by the elevation of waves despite of the summer season conditions (Hung et al., 2021). At the SEATS station located on the central basin, the active carbon fluxes were not necessarily lower than those found in respective seasons in the northern regime, although the lowest fluxes were noted during the fall season (Fig. 6). Similarly, the carbon fluxes were 480 considerably higher in winter than in other seasons at the SEATS station, likely attributable to the abovementioned mechanism.
Data on active nitrogen and phosphorus fluxes in the NSCS are limited. To a first approximation, active nitrogen and phosphorus fluxes were derived from excretory and mortality fluxes; they respectively ranged from 1.06 mg N m 2 d 1 and 0.13 mg P m 2 d 1 during fall at SEATS station to 3.21 mg N m 2 d 1 and 0.40 mg P m 2 d 1 during spring, 1.77 mg N m 2 d 1 and 0.33 mg P m 2 d 1 during summer, 3.51 mg N m 2 d 1 and 0.57 mg P m 2 d 1 during the winter-eddy event, and 7.26 mg N m 2 d 1 and 485 1.08 mg P m 2 d 1 during the summer-IWs event. In general, the distribution of active nitrogen and phosphorus fluxes followed the seasonal patterns of active carbon fluxes. The C:N ratios of active fluxes ranged from 6.9 (fall) to 14.2 (winter; mean: 10.6) and the C:P ratio ranged from 55.7 (fall) to 87.7 (winter; mean: 72.9). The C:N and C:P ratios appeared to increase with an increase in active fluxes, likely caused by the increased contribution of respiration and gut fluxes to active fluxes, and the respiration and gut fluxes did not include nitrogen and phosphorus fluxes. Moreover, higher respiration and gut fluxes occurred 490 in winter than in summer. The C:N and C:P ratios of active fluxes were respectively higher and lower than the C:N and C:P ratios of particulate vertical fluxes, the major component of passive fluxes.

Controlling mechanisms of passive fluxes of C, N, and P
Vertical POC fluxes varied with seasons and locations (Fig. 7), likely because of a pronounced difference in hydrographic and biogeochemical conditions between summer and winter. The upper water column has been widely reported to undergo 495 stratification and experience restricted nutrient availability in summer; however, in winter surface stratification was eroded and nutrient availability increased, leading to enhanced primary productivity and new production (Figs. 2&4; Chen, 2005;Chen et al., 2008a;Dai et al., 2013;Zhai et al., 2013: Hung et al., 2020. By combining the previous and current measurements, https://doi.org/10.5194/bg-2021-17 Preprint. Discussion started: 21 April 2021 c Author(s) 2021. CC BY 4.0 License. particularly our coauthor's (Chen, Y.-L.) new-production data, we found a striking relationship (r = 0.8502, p < 0.02) between integrated new productions and vertical POC fluxes through a depth of 100 m (Fig. 9). Vertical POC fluxes have also been 500 efficiently predicted from primary production (R 2 = 0.690.97) in various regimes of the ocean (Baltzer et al., 1984;Pace et al., 1987). However, Karl et al. (1996) later found an inverse correlation between POC fluxes and primary production during the ENSO period at ALOHA station. Under the oceanographic paradigm, new production is a significant contributor of primary productivity and the export production; therefore, a strong correlation between vertical POC fluxes and new productions is expected. By using this empirical relationship, the data of vertical POC fluxes that could not be collected in this study can be 505 predicted on the basis of the new production data and the more efficient data set of vertical fluxes can be used for spatial and seasonal comparisons. of 100 m at the SEATS station, except for a datum (star symbol) derived from the station near the Dongsha Atoll (Hung 510 et al., 2021). INP data were adapted from Chen et al. (2007Chen et al. ( , 2008aChen et al. ( , 2014 except for a datum derived from Hung et al. https://doi.org/10.5194/bg-2021-17 Preprint. Discussion started: 21 April 2021 c Author(s) 2021. CC BY 4.0 License.
Nutrient availability in the euphotic zone appeared to drive the variability of vertical POC fluxes in the NSCS. Based on previous results that the primary productivity and new production were determined by the availability of nutrients in the euphotic 515 zone of the NSCS (Chen et al., 2005(Chen et al., , 2008b(Chen et al., , 2014, the vertical POC fluxes through a depth of 100 m should be dependent of nutrient availability, particularly the availability of N+N in the euphotic zone because of the remarkable nitrogen limitation ([N+N]/[DIP] << 16) in the NSCS (Chen et al., 2008b(Chen et al., , 2014Hung et al., 2020}. The nutrient supply and availability were in turn determined mainly using climatic and oceanic forcing (e.g., the winter intensification of wind-driven turbulence and vertical convection). Therefore, vertical POC fluxes were largely determined using integrated Chl-a (r = 0.8367, p < 0.01) which was 520 determined by the availability of DIN (r = 0.9151, p <0.01) derived from the data collected in this experiment (Fig. 10). As a result, vertical POC fluxes were likely to vary with the varying hydrographic and nutrient conditions.  By combing the experimental and predicted data, we found that the seasonal, geographic, and ocean events affect the vertical POC fluxes (Fig. 7). Vertical POC fluxes were higher in winter than in other seasons in both the northern regime and central basin (SEATS). The flux was also slightly higher in the case influenced by an anticyclonic eddy than the one unaffected by an eddy in winter in the northern regime. An exception to this pattern in POC fluxes occurred in summer; the POC fluxes were 530 expected to be low, but were highly elevated due to the impact of the upwelling of internal waves. Although POC fluxes were largely predicted using empirical relationships between POC fluxes and integrated new production and Chl-a, the overall data indicated that the highest POC fluxes were noted in winter, followed by summer and fall. Notably, for vertical POC fluxes through a depth of 120 m collected sequentially by moored traps covering summer and winter periods, extremely low POC fluxes were observed in summer and fall but extremely high POC fluxes were observed in winter (Fig. 11c). The exceptionally high 535 POC fluxes in winter may be caused by the more effective trapping in catching pulsed winter blooming through the sequential and continuous collection by traps with larger trapping area (TECNICAP P.P.S. 3/3) than that through the short-term (13 days) collection with floating traps with smaller trapping areas in each event. The highest POC fluxes correspond to the highest POC contents (wt. %) in settling mass (Fig. 11c), indicating major biological origins of the total settling materials (%POM = %POC  2) in winter. The highest POC fluxes were also attributable to the prevailing northeast monsoon wind (Fig. 11a) and lowest 540 surface temperature (Fig. 11b), which enhanced surface mixing and nutrient pumping. 11544.103'E) close to the SEATS station. All data were adapted from unpublished data in Tsai's thesis (Tsai, 2007). 545 Vertical PON and POP fluxes were relatively incomplete compared with POC fluxes that elucidated the seasonal and geographic variations because of the lack of predicted data for evaluation. However, PON and POP fluxes at a depth of 100 m https://doi.org/10.5194/bg-2021-17 Preprint. season. The POC:PON ratios ranged from 5.650.20 at a depth of 50 m to 8.560.20 at a depth of 150 m, which is not quite different from the Redfield ratio (6.6). The POC:POP ratios ranged from 1521.57 at a depth of 50 m to 24315.3 at a depth of 150 m, which is higher than the Redfield ratio (106) and may reflect the dominant distribution of small-size phytoplankton (Chen et al., 2008b(Chen et al., , 2014). The C:N and C:P ratios generally increased from a depth of 50 m to a depth of 150 m, implying the preferential decay of POP and PON over POC. 555 Vertical fluxes of DOC and DON through a depth of 100 m were relatively low compared with POC and PON fluxes because of the small vertical gradient of concentrations in surface waters. Vertical DOP fluxes were negligible because of the insignificant concentration gradient. Despite the lack of winter data, DOC and DON fluxes were expected to increase from summer to winter because of the summer surface accumulation caused by stratification, and the increase of downward fluxes in winter due to the erosion of stratification. 560

Ocean-wide comparisons of active fluxes, passive fluxes, and biological pumps
Overall, the active fluxes of C, N, and P were 7.5693.4 (mean: 37.9) mg C m 2 d 1, 1.06-7.26 (mean: 3.64) mg N m 2 d 1 , and from 0.130.99 (mean: 0.5) mg P m 2 d 1 , in the NSCS (Table 4). Although most previous reports lacked data on active N and P fluxes, our magnitudes of active fluxes of C, N, and P were considerably higher than those reported in the North Pacific Subtropical Gyre (Hamides et al., 2009;  Canary Island (Yebra et al., 2005; Table 4), subtropical-tropical Atlantic (Longhurst, 1990; Table 4), and Northwest Pacific (Kobari et al., 2013; Table 4 oceanic regime (most from the SEATS station) during various periods (Chen, et al., 2008a;Ho et al., 2010;Wei et al., 2011, Cai et al., 2015Table 4), although the passive fluxes of N and P have not been recorded. Our data are strikingly close to the fluxes 575 of C, N, and P reported from the Costa-Rica-Dome upwelling system (Stukel et al., 2016; Table 4). However, our data are apparently higher than those reported from the Northeast Pacific (Knauer et al., 1979; Table 4). This may imply that the NSCS effectively mediates carbon transfer from the surface to the interior of the ocean.
The total export of carbon from the surface into the interior of the ocean in the South China Sea (3.510 6 km 2 ) may be 580 extrapolated from the total BP measured in the NSCS. To a first approximation, the total export was preliminarily projected to be 0.208 Gt C yr 1 [(163 mg C m 2 d 1 )  (3.510 6 km 2 )  (365 d/yr)], which is approximately 1.89% of the global annual flux (11 Gt C yr 1 ) reported by Sanders et al. (2014). This value is expected to change if more BP data are available for the SCS.

Relative contributions of active fluxes and passive fluxes to biological pumps 605
Contributions of active fluxes of C, N, and P to total fluxes of C, N, and P accounted for 23.3%, 17.2%, and 25.8%, respectively (Table 4). Despite the limited data available for other oceans, in our study, the magnitude of contribution of active C flux was lower, but that of contributions of active N and P fluxes was higher than the corresponding findings by Hannides et al. (2009) in the North Pacific Subtropical Gyre (Table 4). However, the magnitude of contribution of active flux in our study was apparently lower than the range reported by Hernández-León et al. (2019;Table 4) in the subtropical-tropical Atlantic. 610 Overall, the range of difference in total fluxes (BP) was reasonable, which may imply that our findings are reliable. The C:N and C:P ratios in the BP were 7.69 and 84.0, respectively, indicating higher C and P enrichment compared with the Redfield ratio. This may be attributed to the more pronounced enrichment in C and P in active fluxes (C:N = 10.4; C:P = 75.8) because the ratios in passive fluxes (C:N = 7.1; C:P =86.8) are close to the Redfield ratio. DVM-mediated transport may play a crucial role in the transfer of P from the surface to the mesopelagic zone. 615

Conclusions
To understand the strength of carbon removal from the surface to the interior of the ocean, the study of BPs is essential.
Elucidating the BPs of C, N, and P in the SCS is a high research priority not only because of the limited existing data on the regimes but also for increasing the knowledges of the BP responses to changing tropical oceans. Overall, the collected and predicted data indicated that the passive fluxes of C, N, and P were seasonally variable and particularly higher in winter than in 620 other seasons in the NSCS. The strengths of passive fluxes were estimated as 66.3255 (mean: 125) mg C m 2 d 1 , 11.923.2 (mean: 17.6) mg N m 2 d 1 , and 0.891.98 (mean: 1.44) mg P m 2 d 1 , of which the fluxes of DOC, DON, and DOP accounted for generally less than 5%. Active fluxes varied largely in coincidence with the seasonal variations of passive fluxes, ranging from 7.56 to 93.4 (mean: 37.9) mg C m 2 d 1 , from 1.06 to 7.26 (mean: 3.64) mg N m 2 d 1 , and from 0.13 to 0.99 (mean: 0.5) mg P m 2 d 1 in the NSCS. They usually account for less than one-third of the total fluxes (BPs). Both active and passive fluxes 625 exhibited contrasting patterns between summer and winter, resulting mainly from surface warming and stratification in summer and cooling and wind-induced turbulence in pumping nutrients into the euphotic zone in winter. The increase in nutrient availability appeared to increase the primary and secondary production in tropical winter when the temperature remained sufficiently high for biological activity. In addition, the impact of anticyclonic eddy and internal-wave events on BP enhancement was pronounced in the NSCS. Overall, the active and passive fluxes were driven by nutrient availability within 630 the euphotic layer, which was ultimately controlled by the change in internal and external forcings. To a first approximation, the SCS may effectively transfer 0.208 Gt C yr 1 into the ocean's interior, accounting for approximately 1.89% of the global C flux.

Data availability
The data published in this contribution are largely included in this article and its supplementary materials. Additional data can 635 be accessed through email request to the corresponding author.

Author contribution
In this work, JJH planned and conducted the experiments and wrote the article; CHT, ZYL, SHP, LST, and YHL performed experiments including collection and analyses of hydrographic and biological pump data; YLC performed new-production experiments and supervision. 640

Competing interests:
The authors declare that they have no conflict of interests