Nutrient dynamics and coupling with phytoplankton species composition during the spring blooms in the Yellow Sea

Deep-Sea Research II 97 (2013) 16–32

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Nutrient dynamics and coupling with phytoplankton species composition during the spring blooms in the Yellow Sea Jie Jin a, Su Mei Liu a,n, Jing Ling Ren a, Cheng Gang Liu b, Jing Zhang c, Guo Ling Zhang a, Da Ji Huang b a Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, College of Chemistry and Chemical Engineering, Ocean University of China, 238 Songling Road, Qingdao 266100, PR China b State Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography, State Oceanic Administration, 36 Baochubei Road, Hangzhou 310012, PR China c State Key Laboratory of Estuarine and Coastal Research, East China Normal University, 3663 Zhongshan Road North, Shanghai 200062, PR China

art ic l e i nf o

a b s t r a c t

Available online 20 May 2013

Nutrient dynamics during spring phytoplankton bloom period in the Yellow Sea (YS) was discussed based on field observations performed in February, March–April and June 2009. Abundant nutrients and optimal molar ratios among dissolved inorganic nitrogen, phosphorus and Silicic acid in early spring provided favorable conditions for blooming phytoplankton. Depletion of phosphorus and nitrogen in the euphotic zone terminated the spring bloom in the central YS in early summer. Continuous observations in every 3 h for about 4–5 days were conducted to investigate supply, consumption and other characteristics of nutrients during phytoplankton bloom period at two drift stations. The major sources of nutrients are Yellow Sea Warm Current water (in winter and early spring) and Changjiang Diluted Water (in early summer). The upward nutrient fluxes from deep water to the euphotic zone (upper 30 m depth) by means of diffusion and turbulent entrainment were important nutrient sources to sustain the bloom, and they appeared to account 56% of N, 56% of P and 69% of Si for phytoplankton growth demand. 57–76% of DIN and 46–68% of PO43− in the upper 10–20 m water were utilized by phytoplankton in about one week to produce a bloom. & 2013 Elsevier Ltd. All rights reserved.

Keywords: Nutrients Diffusion Turbulent entrainment Spring phytoplankton bloom Yellow Sea

1. Introduction Nutrient availability is essential for phytoplankton growth and biomass accumulation (Paytan and McLaughlin, 2007; Struyf et al., 2009). So the temporal and spatial variations of nutrient concentrations affect the phytoplankton community structure and the primary production in marine ecosystem (Tilman et al., 1982; Gong et al., 2003; Maranon et al., 2007; Glé et al., 2008; Zhu et al., 2010). The semi-enclosed Yellow Sea (YS), located between China and Korea, is a continental shelf sea of the Northwest Pacific with an average water depth of 44 m. A deep trough with depths of 60– 80 m exists in the central YS and extends northwestward into the Bohai Sea. The general circulation of the YS presents obvious seasonal variability (Fig. 1). In winter, the Yellow Sea Warm Current (YSWC) penetrates northward through the deep trough; the coastal currents including the Yellow Sea Coastal Current (YSCC) and Korea Coastal Current (KCC), flow southward along

n

Corresponding author. Tel.: +86 532 6678 2100; fax: +86 532 6678 2100. E-mail address: [email protected] (S.M. Liu).

0967-0645/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dsr2.2013.05.002

the coasts of China and Korea. In summer, the YSWC becomes weak and turns eastward into the Cheju Strait between Cheju Island and the Korea Peninsula. The Changjiang Diluted Water (CDW) driven by summer monsoon flows northeastward into the southern Yellow Sea. Under the seasonal thermocline, the Yellow Sea Cold Water (YSCW) is isolated in the central area of the YS (Naimie et al., 2001; Lie et al., 2003; Zang, et al., 2003; Pang et al., 2005; Zhang et al., 2008; Chen, 2009; Xu et al., 2009). Spring phytoplankton blooms are a common phenomenon in temperate and sub-polar aquatic systems such as the Oyashio region (Saito et al., 2002; Nakayama et al., 2010; Sugie et al., 2010), the Patagonia shelf-break region (Garcia et al., 2008), the Celtic Sea shelf edge (Rees et al., 1999). It can influence dynamic of higher trophic levels' production and cycling of biogenic elements. The distribution of Chlorophyll a in the YS showed a wide range of spatial and temporal variation. High chlorophyll a was observed due to the onset of phytoplankton bloom in spring (Hyun and Kim, 2003; Fu et al., 2009; Zheng and Wei, 2010). During the past several decades, structural and functional changes of the YS ecosystem were documented, such as changes in fish community structure and species diversity, which were probably caused by anthropogenic forcing (i.e. over-exploitation, pollutants from

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Fig. 1. Maps of field observation stations in the Yellow Sea in 2009 ((A) February cruise; (B) March–April cruise; (C) June cruise; (D) float trajectory at drift station Z11b (The extent of the drift experiment was 13.78 km east and 20.98 km north); (E) float trajectory at drift station Z4d (The extent of the drift experiment was 3.29 km east and 14.01 km north). Circles are grid stations and pentacles are drift stations.). The circulation regimes and main water mass are also sketched, including Yellow Sea Warm Current (YSWC), Yellow Sea Coastal Current (YSCC), Korean Coastal Current (KCC), Changjiang Diluted Water (CDW) and Yellow Sea Cold Water (YSCW).

industrial, agricultural wastes through run-off and atmospheric deposition into the sea) and climate change (Lin et al., 2005; Tang, 2009). Many studies have reported nutrient dynamics in the YS. The nutrient characteristics in different seasons were described (Lin et al., 2002; Wang et al., 1998, 2003; Wei et al., 2010), the nutrient limiting for phytoplankton growth was studied by in-situ extra nutrients addition incubation experiments (Zou et al., 2001; Li et al., 2002) and the nutrient budgets were calculated based on a simple one-box model (Chung et al., 2002; Liu et al., 2003b). But the coupling between the nutrient condition and phytoplankton bloom in the YS is rarely reported. In this study, we describe nutrient dynamics during a spring phytoplankton bloom period in the YS. Furthermore, the nutrient supply and consumption during a bloom and their influence on phytoplankton biomass are

discussed, to provide better understanding of the mechanism of the spring phytoplankton bloom in the YS.

2. Material and methods 2.1. Sampling Three cruises were carried out on board “R/V Bei Dou” in February (winter), March–April (spring), June (early summer) 2009 in the Yellow Sea (YS). Grid stations were set during all of the three cruises (Fig. 1A–C). In addition, two drift observations, which lasted 102 h (from 3:00 am 4th April to 9:00 am 8th April) and 126 h (from 3:00 am 9th April to 9:00 am 14th April) respectively (Fig. 1D–E) were carried out at stations Z11b

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with an average of 7.971.6 1C in March. The mean temperature in March was lower than that in February mainly due to obviously cold and windy weather during the March cruise. The salinity varied from 31.5 to 34.2 in February and from 31.4 to 33.8 in March (Figs. 2 and 3). The water column was vertically well mixed in winter. In early spring, the water in the shallow area with low temperature and low salinity was still vertically mixed, while in the central YS, it became weakly stratified. Furthermore, the warm (T49.0 1C) and saline (S433.0) water tongue of the YSWC was stronger in early spring than in winter. It flowed toward the north and could reach to 351N (Fig. 3). In June, the seasonal thermocline had formed. The temperature in the surface water reached to 20.2–23.3 1C and decreased with depth, cold water (To10.0 1C) (Figs. 2 and 3) occupied the bottom layer in the northeast part of the study area. Fig. 2. T–S diagram for all the water samples collected in February, March–April and June 2009 in the Yellow Sea (Circles stand for February cruise; squares stand for March–April cruise; triangles stand for June cruise).

3.2. Chlorophyll a distribution

(123.01E, 36.01N) and Z4d (124.01E, 35.51N). Seawater temperature and salinity were measured with a CTD (Model: Seabird19 Plus) probe. Discrete water samples for nutrients and chlorophyll a analysis were collected with 5-l Niskin bottles attached to the CTD rosette at different depths from the surface to near bottom waters depending on the fine structure of CTD profiles and water depth. At drift stations, water samples were collected every 3 h. After collection, water samples for nutrients were filtered with acid precleaned 0.45 μm pore-size acetate cellulose filters (Development Center of Water Treatment Technology, Hangzhou, China). The filtrates were poisoned by addition of saturated HgCl2 (ca. 1.5
10−3 v/v), preserved in low-density polyethylene (LDPE) bottles at room temperature and then analyzed in the laboratory. Water samples for chlorophyll a concentration were filtered onto Whatman GF/F filters (0.7 μm pore-size), and analyzed immediately on board.

The chlorophyll a concentration in the upper layer water was low in both February and March, with averages of 0.9170.84 mg m−3 and 1.1670.88 mg m−3, respectively. The distribution of chlorophyll a showed patchy characteristics (Fig. 4A and B). The remote sensing images (Fig. 5A and B) showed that the chlorophyll a concentration in the central YS was lower than the coastal area near Shandong Peninsula in both February and March. In early April, the chlorophyll a concentration in the central YS increased (Fig. 5C), and phytoplankton blooms (chlorophyll a 44 mg m−3) (Ning, X., unpublished data; Xuan et al., 2011) were observed at the drift stations, which were diatom dominated at station Z11b and dinoflagellate dominated at station Z4d. At the drift stations, the peak chlorophyll a concentration even reached to ∼30 mg m−3 in the subsurface layer (Fig. 4D and E). In late June, the chlorophyll a of the whole study area decreased by ca. 26% compared with that in March, especially in the coastal and central region, with an average of 0.56 mg m−3 (Fig. 5D). Higher chlorophyll a (42 mg m−3) were found in the upper 10 m waters at some stations in the south of 33.51N (Fig. 4C).

2.2. Determination of nutrients

3.3. Nutrients in February 2009

Nutrients including NO3−, NO2−, SiO32− were determined photometrically using an autoanalyzer (Model: SKALAR SANplus), while NH4+ and PO43− were determined by manual method (Parsons et al., 1984). Total dissolved nitrogen (TDN) and total dissolved phosphorus (TDP) were decomposed to NO3− and PO43− with a boracic acid-persulfate oxidation solution and then measured (Grasshoff et al., 1999). The precision of nutrients analysis in this study was ≤3% (Liu et al., 2005). The concentration of dissolved inorganic nitrogen (DIN) is the sum of NO3−, NO2− and NH4+. The concentrations of dissolved organic nitrogen (DON) and dissolved organic phosphorus (DOP) are the differences between TDN and DIN, TDP and PO43−, respectively.

The nutrients distributions in the surface water are shown in Fig. 6. The concentrations of NO3−, DIN, PO43−, TDP and SiO32− increased gradually from the northwest to the southeast of the study area. The lower values appeared in shallow water area near the Shandong Peninsula. Relative high levels of DON, TDN and DOP were found in the nearshore area and the southern part of the study area. High values of NO2− and NH4+ existed in the east part of the study area. Due to strong vertical mixing of water in winter, both the concentrations and the horizontal distributions of nutrients in near bottom water were almost the same as that in the surface water (data not shown). For nitrogen compounds, NO3− contributed to 65–97% of DIN at offshore stations, then followed by NH4+, which contributed to 3–27%; NO2− occupied the smallest proportion, which was just 1–8% of DIN. While at coastal stations where water depth was less than 50 m, NH4+ became the dominant species of DIN, which accounted for 50–81% of DIN. In TDN, DON accounted for ca. 63% and DIN accounted for ca. 37% in the whole study area. For phosphorus compounds, PO43− and DOP represented 26–48% and 52–74% of TDP at nearshore stations, respectively. At offshore stations, PO43− was the dominant species of TDP, which contributed ca. 81% of TDP on average.

2.3. Determination of chlorophyll a concentration The chlorophyll a was extracted from the particles trapped by filters in 10 ml 90% (v/v) acetone in the dark at 4 1C for 14–24 h, and then the fluorescence was measured both before and after acidification with 5% (v/v) HCl using a Turner Designs Trilogy Laboratory fluorometer (Parsons et al., 1984).

3. Results

3.4. Nutrients in March–April 2009

3.1. Hydrographic properties

The nutrients distributions at the sea surface in March are shown in Fig. 7A. The concentrations of NO3−, DIN, TDN, PO43−, TDP and SiO32− were low in the western part, while high in the southern part of the study area. The concentrations of DIN, PO43−

The temperature in the study area ranged from 5.2 1C to 13.5 1C, with an average of 8.772.4 1C in February and from 3.9 1C to 11.0 1C,

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Fig. 3. Horizontal distributions of temperature (1C) and salinity in the surface and near bottom water of the Yellow Sea in February, March and June, 2009. The isolines of T ¼ 9.0 1C and S¼ 33.0 indicating the extension of the YSWC (Zang et al., 2003; Pang et al., 2005).

and SiO32− were ca. 4 folds higher in the central YS than in the coastal region. The inorganic nutrients concentrations in the area east of 122.51E had good negative correlations with chlorophyll a (NO3− ¼−1.4422 chl a+8.5593, R¼ 0.75; PO43− ¼−0.1005 chl a +0.6299, R¼ 0.78; SiO32− ¼−2.1151 chl a+14.29, R¼0.67), indicating the distributions of NO3−, PO43− and SiO32− might be affected by phytoplankton activity in the central YS. The concentrations of NH4+, DON and DOP decreased from near shore to offshore at the surface. Higher NO2− concentration was found in the central part of the study area. The nutrients distributions in the near bottom water were similar to those in the surface water (Fig. 7B). On average, concentrations of NO3−, NH4+, DIN, DOP and SiO32− in the near bottom water were 1.1–1.5 times higher as those at the surface. PO43 − , TDP, DON and TDN concentrations were vertically uniform. NO2− concentration in the near bottom water was just 90% of that at the surface.

With respect to nitrogen compounds, at the stations in the east of 122.51E, NO3− contributed to 60–95% of DIN, NH4+ contributed to 4–33% of DIN. At the stations in the west of 122.51E where DIN was low (o2 μmol L−1), NO3– only contributed to less than 30% of DIN. NH4+ became the dominant species of DIN, which contributed to 66–98% of DIN. DON accounted for 60–96% of TDN in the whole study area. For phosphorus compounds, PO43− and DOP represented ca. 80%, ca. 20% of TDP in the central YS and ca. 45% and ca. 55% of TDP in the coastal area respectively. 3.5. Nutrients distributions in June 2009 In June, the nutrients distributions were quite different from that in February and March–April 2009 (Fig. 8A). Low concentrations of NO3− (o0.5 μmol L−1), NO2− (o0.05 μmol L−1), DIN (o1.0 μmol L−1) and SiO32− (o2.5 μmol L−1) were found in the surface water of most

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Fig. 4. Horizontal distribution of depth integrated chlorophyll a concentration (mg m−3) in the upper layer water of the Yellow Sea in February (A), March (B) and June (C) and changes of chlorophyll a concentration (mg m−3) at drift stations Z11b (D) and Z4d (E) in April, 2009.

Fig. 5. SeaWiFS remote sensing images of monthly average chlorophyll a concentration (mg m−3) in February (A), March (B), April (C) and June (D), 2009 in the Yellow Sea. http://gdata1.sci.gsfc.nasa.gov/daac-bin/G3/gui.cgi?instance_id=ocean_month.

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Fig. 6. Horizontal distributions of dissolved nutrients (all in μmol L−1) in the surface water of the Yellow Sea in February, 2009 (The figures of dissolved nutrients distributions in the near bottom water are not shown because they were similar to that in the surface water.).

parts of the study area, while in the southern parts of the study area, the concentrations increased rapidly, with the maximum values of 13.6, 0.1, 15.3 and 16.6 μmol L−1, respectively. The concentrations of DIN and SiO32− showed remarkable negative relationships with salinity in the surface water (DIN¼−3.1076S+101.74, R¼ 0.85, p¼0.001; SiO32− ¼−2.6891S+90.496, R¼0.80, p¼0.001), which indicated the influence of the Changjiang Diluted Water (Wang, 1998). The surface water of the whole study area was depleted of PO43− (i.e. not detected—0.05 μmol L−1) and DOP (i.e. 0.13–0.18 μmol L−1). Relative high concentration of NH4+ existed in the southwest part. DON had a higher concentration in the northwest part. In the near bottom water, the concentrations of NO3−, DIN, TDN, PO43−, TDP and SiO32− increased by 6–20 folds from west to east of the study area (Fig. 8B). NO2−, NH4+, DON and DOP concentrations were relatively low in the

central part of the study area. As for the vertical distributions, the concentrations of NO3−, DIN, TDN, PO43−, TDP and SiO32− in the central YS were low in the upper layer waters, then increased remarkable in the deep water, which were 2–8 folds higher than that in the upper layer waters. Contrarily, the concentrations of NO2−, NH4+ and DON were lower in the deep water, which were 70–80% of that in the upper layer water. DOP was almost uniform in the water column. 3.6. Variations of nutrients at two drift stations At drift station Z11b, during the 102 h observation, the temperature increased with depth, with the mean value of 8.270.5 1C at the surface and 9.470.1 1C in the near bottom water. Salinity showed

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At drift station Z4d, during the 126 h observation, the temperature decreased from 11.371.0 1C at the surface to 7.470.0 1C in the near bottom water. The salinity was vertically uniform. In the surface and near-bottom water, the salinity was 32.6870.02 and 32.7370.01, respectively. The concentrations of DIN, PO43− increased with depth and varied dramatically during the observation time in the subsurface water layer (10–20 m) (Fig. 10). The average concentrations of DIN and PO43− were 0.93, 0.10 μmol L−1, respectively in the surface water and 8.65, 0.58 μmol L−1, respectively in the near bottom water. The average concentration of NH4+ decreased apparently from 1.50 μmol L−1 to 0.50 μmol L−1 after 48 h observation. The SiO32− concentration increased slightly with observation time, with low value of ∼10.5 μmol L−1 in the upper 20 m during 18–54 h and high value of ∼13.0 μmol L−1 below the 50 m depth during 72–108 h.

weak stratification, which were 32.2470.12 at the surface and 33.2370.06 in the near bottom water. The vertical distributions of inorganic nutrients showed the similar tendencies as salinity (Fig. 9). The concentrations of DIN, PO43− and SiO32− increased from the surface to the near bottom water, with averages of 0.79, 0.10, 2.40 μmol L−1, respectively in the surface water and 16.0, 0.62, 13.3 μmol L−1, respectively in the near bottom water. Low levels of inorganic nutrients in the surface water were probably due to phytoplankton uptake and lack of supply from the deep water where nutrients were regenerated. The concentrations of inorganic nutrients changed dramatically in the subsurface water layer (10–20 m). As for organic nutrients, the average concentrations of DON and DOP were 13.9 and 0.17 μmol L−1, respectively in the upper 30 m water and 15.0 and 0.13 μmol L−1, respectively in the deep water.

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Fig. 7. Horizontal distributions of dissolved nutrients (all in μmol L−1) in the surface (A) and near bottom (B) water of the Yellow Sea in March, 2009.

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High value of DON (16.3–21.8 μmol L ) was observed during 12–36 h, and then deceased to ca. 12.7 μmol L−1 after 36 h observation. The DOP concentration was high (0.18–0.30 μmol L−1) at the ∼20 m depth and was 0.15 μmol L−1 on average in the deep water. 4. Discussion 4.1. Nutrient composition Nutrient molar ratios have been used to infer potential nutrient limitation, as well as changes in the phytoplankton community assemblage (Justic, et al., 1995; Wang, et al., 2003; Ramírez et al., 2005; Sylvan et al., 2006). On the other hand, they could also to

some extent reflect the nutrient regeneration and transportation mechanism in the seawater. The DIN/DIP ratio varied from winter to early summer. In winter, the ratio of DIN/DIP ranged from 4.5 to 19.2. DIN/DIP increased from nearshore to offshore. Low values of DIN/DIP (o10) were just found in the shallow region near the Shandong Peninsula such as at stations B1, B19 and B31a. At stations where the water depth was deeper than 50 m, the mean ratio of DIN/DIP was 16.0 7 1.9. In late March before bloom, both the higher and the lower values of DIN/DIP were found in the coastal area. Low values of DIN/DIP (2.5–6.5) were found at stations B2, B3, B18 and B19 where the DIN concentration was less than 0.8 μmol L−1. High values of DIN/DIP (20.7–32.7) were found at stations B31, B32 near

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the Shandong Peninsula. The mean ratio of DIN/DIP in the central YS was 14.5 71.4, just slightly decreasing from winter. The DIN/ DIP ratio was very close to the typical Redfield ratio (N/P¼ 16) suggesting that N/P ratio was optimal for phytoplankton growth in the central YS in spring. In April when the blooms took place, the mean ratios of DIN/DIP in the euphotic zone (upper 30 m) decreased to 10.3 74.8 at station Z11b and 8.8 75.9 at station Z4d. Both of them were much smaller than the Redfield ratio (N/P¼ 16), suggesting nitrogen potentially limited phytoplankton growth during the bloom. Relatively high phosphate concentration compared with DIN in the euphotic zone might result from the faster regeneration of phosphorus relative to nitrogen (Li et al., 2002). Besides, the average concentrations of DIN and phosphate

at the surface were 0.717 0.22, 0.107 0.03 μmol L−1, respectively at station Z11b and 0.917 0.72, 0.11 70.04 μmol L−1, respectively at station Z4d. Studies about the nutrient uptake kinetics showed that the threshold values for phytoplankton growth were DIN¼1.0 μmol L−1 and dissolved P ¼0.1 μmol L−1, respectively (Justic et al., 1995). Low levels of DIN and phosphate at the surface could not meet phytoplankton's requirement, thus, the maximum chlorophyll a concentrations layer (4–30 mg m−3) existed not at the surface but at the subsurface (10–20 m) where nutrient concentrations were relatively high. In early summer, the ratio of DIN/DIP had a wide range, from 4.0 to 509. Higher values of DIN/DIP ( 450) were mainly found in the upper 20 m layer waters where phosphate concentration was low (o 0.02–0.12 μmol L−1).

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Fig. 8. Horizontal distributions of dissolved nutrients (all in μmol L−1) in the surface (A) and near bottom (B) water of the Yellow Sea in June, 2009.

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38° N 37°

36°

36°

35°

35°

34°

34°

38° N 37° <0.10

Nitrite_bottom

32° 120°

122°

124° E

35°

33°

Nitrate_bottom 32°

36°

34°

33°

33°

120°

122°

124° E

120°

38° N 37°

38° N 37°

36°

36°

36°

35°

35°

35°

34°

34°

34°

33° DIN_bottom

32° 120°

122°

120°

122°

TDN_bottom

124° E

120°

38° N 37°

36°

36°

35°

35°

35°

34°

34°

34°

32° 120°

122°

124° E

122°

124° E

38° N 37° >0.15

33° Phosphate_bottom

124° E

32°

38° N 37°

33°

122°

33° DON_bottom

32°

124° E

Ammonium_bottom

32°

38° N 37°

33°

25

36°

33° DOP_bottom

32° 120°

122°

124° E

TDP_bottom

32° 120°

122°

124° E

38° N 37° 36° 35° 34° 33° Silicate_bottom

32° 120°

122°

124° E Fig. 8. (continued)

Low level of phosphate concentration indicated phosphorus limited the phytoplankton growth after spring bloom. As for organic nutrients, the molar ratio of DON to DOP varied between 22 and 331 from winter to early summer, which was much higher than the typical Redfield ratio (N/P ¼16). Diatoms are the dominant species of phytoplankton community in the YS (Fu et al., 2012). The mean ratios of Si to DIN were 1.670.7 in both winter and early spring and then increased to 4.17 2.5 in early summer. In April, a diatom bloom was observed at station Z11b, with the average Si/DIN ratio of 2.9 71.0. All of the Si/DIN ratios were higher than 1, indicating that silicate was abundant compared with DIN. Thus, silicate would not restrict diatom's growth in the YS, in agreement with previous studies (Sun et al., 2008; Wang et al., 2003). Furthermore, decreasing

trends of SiO32− concentration from winter to early summer in the YS (Table 1) might induce the proportion of diatoms in phytoplankton cell abundance decreasing from 98.9% in winter, 77.9% in early spring to 61.2% in early summer 2009 (Tian, 2011). In the course of the spring phytoplankton bloom period, the nutrients concentrations in the YS had dramatically changed (Table 1). In the upper water layer, the concentrations of DIN, PO43− and SiO32− decreased slightly from winter to early spring before phytoplankton bloom onset. While in early summer, due to phytoplankton's rapid consumption during the spring bloom period, the average nutrient concentrations were almost depleted, especially the concentration of PO43− was found around and even below detection limit (0.02–0.03 μmol L−1) at about 80% stations. The concentration of DON in early summer was less than 60%

J. Jin et al. / Deep-Sea Research II 97 (2013) 16–32

0

0

-10

-10

-20

-20

Depth (m)

Depth (m)

26

-30 -40

Nitrate

-60 12

24

36

48

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84

96

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DON

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-60 0

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TDP

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48

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96

Time (hr)

Silicate

-60 0

12

24

36

48

60

72

84

96

Time (hr)

Fig. 9. Changes of dissolved nutrients (all in μmol L−1) at station Z11b in April, 2009.

of that in winter and early spring, which may be attributed to phytoplankton utilization or mineralization to inorganic pools (Bronk et al., 2007). DOP level kept almost steady from winter to early summer. In the deep water, average concentrations of PO43−,

DOP and SiO32− did not change much from winter to early summer. DIN had a maximum value in early summer, which was 1.3 times higher than that in the early spring. DON had a minimum value in early summer, which was just 44% of that in early spring. For the

0

0

-10

-10

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Depth (m)

J. Jin et al. / Deep-Sea Research II 97 (2013) 16–32

-30 -40 -50 -60

-50

12

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84

96 108 120 0

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-70 0

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-60

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0

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0

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-60

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-70 0

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96 108 120

Silicate

-70

Time (hr)

Time (hr) −1

Fig. 10. Changes of dissolved nutrients (all in μmol L ) at station Z4d in April, 2009.

nitrogen composition, the molar ratio of NO3−/(NO3−+DON) was 0.01–1.2 in both winter and early spring. In early summer, the NO3−/(NO3−+DON) ratio increased to 1.7–3.7 in the deep water in the central YS. For phosphorus compounds, the molar ratio of DIP/DOP was 0.2–0.9 in the shallow area and 1.1–11.2 in the central YS in both winter and early spring. In early summer, because of the

depletion of PO43− by phytoplankton utilization, the DIP/DOP ratio dropped to 0.01–0.9 in the upper layer water, while in the deep water, the DIP/DOP ratio remained higher than 1 (1.5–9.9). During the recent 10 years, the nutrient concentrations in the YS have a great change. The concentrations of nitrate, phosphate and silicate were 2.87 71.70, 0.33 70.24, 9.51 74.62 μmol L−1,

28

J. Jin et al. / Deep-Sea Research II 97 (2013) 16–32

Table1 Nutrient concentrations (μmol L−1) in different cruises in the YS. Cruise

February

March

June

The upper layer water

Deep water

The upper layer water

Deep water

The upper layer water

Deep water

DIN Average Range

7.26 0.54–11.5

7.75 0.52–12.5

5.60 0.51–9.55

7.00 0.65–10.9

2.40 0.48–18.4

9.08 0.44–20.3

DON Average Range

14.2 6.02–22.1

12.9 5.17–23.6

14.8 12.1–22.6

14.5 11.8–20.6

8.19 5.02–9.76

6.33 2.91–10.2

PO43− Average Range

0.47 0.11–0.69

0.48 0.07–0.72

0.38 0.06–0.64

0.49 0.04–0.81

0.03 ND–0.13

0.51 ND–0.99

DOP Average Range

0.13 ND–0.27

0.13 ND–0.27

0.14 0.08–0.21

0.13 ND–0.20

0.15 ND–0.19

0.16 0.10–0.51

SiO32− Average Range

10.1 1.11–15.2

10.5 1.07–16.4

8.74 1.02–14.9

10.8 1.14–15.6

4.37 0.87–16.6

11.2 1.39–20.2

ND：Not detected.

respectively in 1998 (Liu et al., 2003b) and 5.9172.39, 0.4570.15, 10.673.73 μmol L−1, respectively in 2009. On average, NO3− concentration increased 2.1 folds and PO43− concentration increased 1.4 folds from 1998 to 2009 in spring, whereas there was no significant difference of SiO32− concentrations between 1998 and 2009 in spring. Studies on 361N transect in the YS showed that annual average NO3– concentration exhibited an increasing trend, while PO43− and SiO32− concentrations exhibited decreasing trends during the past 25 years between 1976 and 2000 (Lin et al., 2005). Increasing trend of NO3– concentration and decreasing trend of SiO32− concentration were also observed in the central Bohai Sea (Zhang et al., 2004) and western area of East China Sea (Gao and Li, 2009) from 1960s to 1990s. With the development of industry and agriculture, the industrial sewage and fertilizer usage with abundant nitrogen discharged into the sea caused the DIN concentration increasing and damming reduced the silicate flux from the river to the sea (Zhou et al., 2008; Fu et al., 2012). The increasing DIN concentration and DIN/DIP molar ratio had an important impact on phytoplankton community in the YS. A reduction of 64.6% in phytoplankton abundance and 72.3% in Bacillariophyta abundance were found from 1986 to 1998 in spring in the YS, and Pyrrophyta abundance showed no difference between 1986 and 1998. Furthermore, the percentage of Bacillariophyta in the total phytoplankton abundance in spring dropped from 88.9% in 1986 to 69.5% in 1998, then 50.9% in 2005, probably attributed to anthropogenic impact (Wang, 2001; Fu et al., 2012). 4.2. Nutrient status before spring bloom The YSWC is a prominent feature of the YS circulation in winter and early spring (Huang et al., 2005; Xu et al., 2009). Plotting nutrient concentrations versus both salinity and temperature showed that dissolved inorganic nutrients (NO3-, PO43- and SiO32-) concentrations increased as salinity (or temperature) increased (Fig. 11). The linear correlations are significant at the 99% confidence level, and the correlation coefficients range from 0.40 to 0.59 (n ¼99). Furthermore, ca. 30% of the study area was affected by YSWC during the February cruise. The mean depth integrated concentrations of DIN, PO43− and SiO32− in the YSWC area were 658.97 175.6, 40.4 77.2, 840.37132.9 mmol m−2, respectively, which were 1.5 times as high as that in the nonYSYC area. The nutrients in the area affected by the YSWC contributed to 40% of DIN, 39% of PO43− and 38% of SiO32− of the total nutrient inventory in our study area. Meanwhile, the

replenishment of nutrients to the surface water occurred due to strong vertical mixing by wind in winter. Despite nutrients were abundant (DIN ¼8.23 72.20 μmol L−1; PO43− ¼0.51 70.12 μmol L−1; SiO32− ¼11.272.22 μmol L−1) in the upper water layer, low phytoplankton biomass was found in winter, probably caused by some physical factors such as low temperature, instability of water column (Fu et al., 2009; Xuan et al., 2011) or low light availability (Varela, 1996). In late March, the water was more stable than in February, thus phytoplankton could gradually accumulate in the euphotic zone, on average, chlorophyll a concentration was ca. 30% higher than in February. Accordingly, the integrated nutrient concentrations in the upper 30 m water decreased from 217.7799.9 mmol m−2 of DIN, 13.775.3 mmol m−2 of phosphate, 298.17120.7 mmol m−2 of silicate in February to 168.2792.4 mmol m−2 of DIN, 11.875.9 mmol m−2 of phosphate, 261.97148.9 mmol m−2 of silicate in late March. The YSWC in early spring was stronger than in winter. The average concentration of DIN, PO43− and SiO32− were 8.6870.73, 0.5670.10, 13.171.28 μmol L−1, respectively in the YSWC surface water. The mean depth integrated concentrations of DIN, PO43− and SiO32− in the YSWC area were 1.6–1.8 folds as high as that in the non-YSWC area. And the nutrient stock in the area affected by the YSWC accounted for 47% of DIN, 45% of PO43− and 45% of SiO32− of the whole study area. Furthermore, there were still good positive relationships between inorganic nutrients concentrations and temperature (or salinity), with coefficients range from 0.56 to 0.85 (n¼105) at the 99% confidence level (Fig. 11). Higher chlorophyll a concentration was found in the central YS in late March. Compared with the integrated chlorophyll a concentrations in winter, about 56% of phytoplankton biomass increased in the central YS, only 9.9% of DIN decreased, phosphate concentration kept stable and silicate increased by 6%. These results illustrate that the conditions in central YS were favoring the occurrence of the bloom. 4.3. Nutrient dynamics during the spring bloom in the central YS The onset of the spring phytoplankton bloom in the central YS is usually in April (Hu et al., 2004; Xuan et al., 2011). The nutrient supply and consumption during the bloom are discussed below. In April, weak stratification existed at some stations in the central YS (data not shown). The upward nutrient fluxes from deep water to the euphotic zone by means of diffusion (Cai et al., 2002; Chung, et al., 2002) and turbulent entrainment (Wei et al., 2002)

J. Jin et al. / Deep-Sea Research II 97 (2013) 16–32

29

Fig. 11. The relationships between nutrients concentrations and temperature (or salinity) during the February cruise (triangles) and March cruise (squares). The solid lines are obtained by the least-square regression.

could be considered as an important nutrient source to support the phytoplankton bloom. Cai et al. (2002) estimated the upward flux of nitrate into the euphotic zone by the coupled 228Ra–nitrate approach. Fick's first law of diffusion for dissolved species is adopted to evaluate the diffusion fluxes (Fd) of NO3−, PO43− and SiO32−. F d ¼ −K z


dC dz

ð1Þ

where Kz is the vertical diffusion coefficient and dC/dz is the nutrient concentration gradient. Based on the vertical profile of 224 Ra and 223Ra in the southern Yellow Sea, Su et al. (2013) calculated the mean vertical diffusion coefficient Kz as 1.0– 12.7 cm2 s−1. The nutrient concentration gradients were calculated according to the vertical profiles of nutrients, which were 0.0036– 0.21 mmol m−4 of NO3−, 0.00046–0.0095 mmol m−4 of PO43− and 0.0043–0.20 mmol m−4 of SiO32−. Based on Eq. (1), the upward diffusion fluxes of NO3−, PO43− and SiO32− into the euphotic zone ( 30 m) in early spring were 1.55 mmol N m−2 d−1, 0.090 mmol P m−2 d−1 and 1.49 mmol Si m−2 d−1 on average (Table 2). It is reported that the average primary productivity in the water column of the YS was 505 7 190 mg C m−2 d−1 in spring (Zhu et al., 1993; Lin et al., 2005; Tian et al., 2005). Based on Redfield ratios (C:N:P:Si ¼106:16:1:16), the assimilated nutrient fluxes are 6.35 mmol N m−2 d−1, 0.40 mmol P m−2 d−1 and

6.35 mmol S m−2 d−1 for supporting phytoplankton growth. Comparison with our estimation reveals that the nutrients upward diffusion to the euphotic zone could match 24% of N requirement, 23% of P and Si requirement for phytoplankton growth in spring. Besides upward diffusion, nutrients can be transported across the thermocline by means of turbulent entrainment. The nutrients vertical fluxes by turbulent entrainment (Ft) could be estimated as follows: F t ¼ W e
C deep

ð2Þ

where We is the entrainment velocity from deep water to upper water and Cdeep is the nutrient concentration in the deep water. Wei et al. (2002) estimated the entrainment velocity in the central YS in spring was 2.71
10–6 m s−1 based on a mixing layer model. The concentrations of NO3−, NH4+, PO43− and SiO32− in the deep water were 3.76– 9.49, 0.24–3.43, 0.29–0.65 and 6.89–14.3 μmol L−1, respectively in spring. Based on Eq. (2), the average turbulence fluxes from deep water to the euphotic zone were 1.79 mmol m−2 d−1 of NO3−, 0.19 mmol m−2 d−1 of NH4+, 0.13 mmol m−2 d−1 of PO43− and 2.92 mmol m−2 d−1 of SiO32− (Table 2), which could match 31% of N requirement, 33% of P requirement and 46% of Si requirement for phytoplankton growth in spring. Atmospheric deposition is also considered as a nutrient source to the euphotic zone. The total atmospheric fluxes to the YS were 0.094 mmol m−2 d−1 of NO3–, 0.12 mmol m−2 d−1 of NH4+, 0.0017 mmol m−2 d−1 of PO43− and 0.0039 mmol m−2 d−1 of SiO32−

30

J. Jin et al. / Deep-Sea Research II 97 (2013) 16–32

Table 2 Nutrients fluxes (mmol m−2 d−1) to the euphotic zone in the YS. Nutrients Fluxes

NO3 

NH4 þ

PO43 

SiO32 

References

Diffusion Turbulence entrainment Total atmospheric deposition

0.15–8.65 (1.55)a 0.88–2.22 (1.79)a 0.094

– 0.056–0.80 (0.19)a 0.12

0.020–0.40 (0.090)a 0.068–0.15 (0.13)a 0.0017

0.18–8.52 (1.49)a 1.61–3.36 (2.92)a 0.0039

This study This study Zhang et al. (2007)

a

Average value.

(Zhang et al., 2007). The upward nutrients fluxes from the deep water to the euphotic zone were higher than the atmospheric deposition by one to three orders of magnitude, except NH4+. The NH4+ fluxes were comparable between atmospheric input and turbulent entrainment from deep water, indicating atmospheric input was an important source for NH4+. The nutrient supply from the deep water by both diffusion and entrainment could support ca. 48% of N and P requirement indicating it was an important nutrient source to sustain the bloom. Furthermore, as organic nutrients were the major nutrients species (i.e., DOP/TDP¼ca. 51%; DON/TDN¼ ca. 87%) in the upper 20 m where higher chlorophyll a existed during the bloom period, the bioavailability of organic nutrients in the euphotic zone should not be ignored. Some species of phytoplankton could also utilize DON (such as urea) (Bronk et al., 2007) and/or DOP (such as phosphomonoesters and nucleotides) (Wang et al., 2011) as nutrient source in the case that inorganic nutrients were depleted. Besides, the residence time of P in the dissolved pools was very short (3–4 d) in the YS (Zhang and Yin, 2007). However, the nutrient supply by the bioavailability of organic nutrients and nutrients regeneration during the bloom should be studied further. In the course of the bloom at the two drift stations, the inorganic nutrient concentrations fluctuated dramatically at the subsurface chlorophyll a maximum layer (10–20 m). The inorganic nutrients concentrations (DIN, PO43− and SiO32−) had negative correlations with chlorophyll a, and the correlation coefficients at the 95% confidence level ranged between 0.41–0.46 (n¼ 31) at Z11b and 0.34–0.55 (n¼39) at Z4d. This suggests that the inorganic nutrient concentrations at the subsurface chlorophyll a maximum layer were mainly controlled by the phytoplankton utilization. To roughly estimate the nutrient consumption characteristics during the blooms, we defined nutrient variation (Δnutrient) within the subsurface chlorophyll a maximum layer by the nutrient concentration at tn+1 time minus the nutrient concentration at tn time. The slope of the regression line (Fig. 12) could reflect the nutrient assimilation ratio by phytoplankton to some extent. At station Z11b, the ratio of ΔDIN/ΔP was 18.3 and ΔSi/ΔDIN was 1.3. At station Z4d, the ratio of ΔDIN/ΔP was 16.4 and ΔSi/ΔDIN was 0.1. The difference of nutrient ratios between two stations could reflect different nutrients utilization characteristics by different phytoplankton species. Diatoms (Detonula pumila and Guinardia delicatul) were the dominant species at Station Z11b and dinoflagelltes (Hetercapsa sp.) were the dominant species at station Z4d (Tian, 2011). As a dinoflagelltes bloom took place at station Z4d, the phytoplankton assimilation of silicate was only 10% of DIN at the subsurface chlorophyll a maximum layer. Before the bloom occurred, the concentrations of DIN and phosphate in the upper 10–20 m waters at two drift stations were 6.58–7.46 and 0.44–0.50 μmol L−1. After about 1 week, the chlorophyll a concentration increased from ca.1 mg m−3 to 3–4 mg m−3, correspondingly, the concentrations of DIN and phosphate decreased to 1.59–3.21 and 0.14–0.27 μmol L−1, respectively. The nutrients decrease suggested ca. 57–76% of DIN and 46–68% of phosphate in the upper 10–20 m waters were utilized by phytoplankton in about one week to make a bloom break out. Meanwhile, during the occurrence period of these two blooms, 0.5–0.7 mmol m−2 d−1 for phosphorus, 5.3–11.8 mmol m−2 d−1 for nitrogen and 21.1 mmol m−2 d−1 for silicon (at station Z11b) in the

euphotic layer were consumed to support 35.3–78.3 mmol m−2 d−1 carbon based on the Redfield ratios of 106:16:1 for C:N:P. 4.4. Nutrient status after the spring bloom in the central YS In early summer, the vertically integrated chlorophyll a concentration in the central YS declined to only ca. 64% of that in early spring. And the higher chlorophyll a concentration has shifted from the central YS to the southern part of the study area. In the central YS, the average integrated concentrations of DIN, PO43− and SiO32− in the euphotic zone decreased to 64.0, 2.6 and 138.1 mmol m−2, respectively, decreasing to 32%, 19% and 42% of that in early spring, mainly due to the onset of bloom in April. Considering the hydrographic properties (Figs. 2–3), the seasonal thermocline had existed between 10–30 m, and beneath the thermocline, the YSCW (T o10 1C) existed (Zhang et al., 2008). The profiles of DIN, PO43− and SiO32− exhibited stratification where the YSCW existed. Although the YSCW was rich in nutrients (∼9.0 μmol L−1 of DIN, ∼0.5 μmol L−1 of PO43− and ∼11.0 μmol L−1 of SiO32−), the existence of the thermocline weakened the vertical transport of nutrients from bottom waters to the upper water layer, thus, high chlorophyll a concentration (i.e. 1–2 mg m−3) in the central YS was only observed at 30 m layer. Depletion of DIN (o1 μmol L−1) and phosphate (∼0.03 μmol L−1) in the upper 10 m waters constrained the phytoplankton growth, leading to the termination of the bloom in the central YS. On the other hand, the CDW affected the southern part of the study area (Wang et al., 2003). Changjiang River brought plenty of nutrients (74.1 μmol L−1 of DIN, 102 μmol L−1 of silicate and 0.83 μmol L−1 of phosphate) to the sea (Liu, et al., 2003a), induced high chlorophyll a concentration (i.e. 2–9 mg m−3). High phytoplankton cell abundance with dinoflagellates (Prorocentrum dentatum, Pseudo-nitzschia delicatissima) being dominant was found in the southern part of the study area (Tian and Sun, 2011). However, the surface water was enriched in DIN (10– 18 μmol L−1) and silicate (9–16 μmol L−1) but depleted in phosphate (∼0.08 μmol L−1). Low level of phosphate and extremely high molar ratio of DIN to DIP (100–500) implied phosphorus was the limiting factor for the phytoplankton growth in the southern part of the study area. Similarly, phytoplankton blooms in other shelf regions such as East China Sea (Wang et al., 2003) and Eastern Mediterranean Sea (Krom et al., 2010) are also known as phosphorus limited.

5. Conclusions The spring phytoplankton bloom is an important phenomenon in the YS. Both the concentrations and distributions of nutrients in the YS varied significantly during spring phytoplankton bloom. The nutrient concentrations had higher values in offshore area than in near shore area in winter and early spring. While in early summer, dissolved inorganic nutrients were almost exhausted in the surface water in the central YS. Abundant nutrients and fitting nutrients ratios in the central YS provided favorable conditions for phytoplankton bloom's onset in April. In early summer, depletion

DIN(µmol L-1)

DIN(µmol L-1)

J. Jin et al. / Deep-Sea Research II 97 (2013) 16–32

5.0 4.0 3.0 2.0

PO43-(µmol L-1)

0.0 -0.3

-0.2

-0.1

-1.0

8.0 6.0 4.0 2.0

1.0

PO 43-(µmol L-1)

31

0.0

0.1

0.2

0.3

-0.4

0.0

-0.2

0.0

0.2

0.4

-2.0

-2.0 -4.0

y = 18.282x + 0.0392 R2 = 0.9275 n=30, p<0.001

-3.0 -4.0

-8.0

SiO32-(µmol L-1)

SiO32-(µmol L-1)

-5.0

PO43-(µmol L-1)

4.0

6.0

3.0

4.0

2.0

2.0

1.0

PO43-(µmol L-1)

0.0 -0.3

-0.2

y = 16.422x -0.0862 R2 = 0.8717 n=38, p<0.001

-6.0

-0.1

0.0

0.1

0.2

0.0

0.3

-2.0

-0.6

-0.4

-0.2

0.0

0.2

0.4

0.6

-1.0 -4.0

-2.0

y = 24.967x + 0.0727 R2 = 0.9289 n=30, p<0.001

-6.0

-4.0

SiO32-(µmol L-1)

SiO32-(µmol L-1)

-8.0 6.0 4.0 2.0

DIN(µmol L-1) -4.0

4.0 3.0 2.0 1.0

DIN(µmol L-1) 0.0

0.0 -6.0

y = 2.4809x + 0.0204 R2 = 0.2570 n=38, p<0.05

-3.0

-2.0

0.0

2.0

4.0

6.0

-10.0

-5.0

-4.0

0.0

5.0

10.0

-1.0

-2.0

-2.0

y = 1.3257x + 0.0246 R2 = 0.9437 n=30, p<0.001

-3.0

y = 0.1343x + 0.0299 R2 = 0.2330 n=38, p<0.05

-4.0

-6.0

Fig. 12. The relationships between different nutrients concentrations variation in the sub-surface layer water (10–20 m) at station Z11b (A–C) and station Z4d (D–F) during ca. 100 h continuous observation. The solid lines are obtained by the least-square regression.

of both nitrogen and phosphorus led to the termination of bloom in the central YS, while in the southern part of the YS where the Changjiang Diluted Water affected, phosphorus would limit phytoplankton growth. The upward nutrient fluxes from deep water to the euphotic zone by means of diffusion and turbulent entrainment were important nutrient sources to sustain the bloom, which could match 56% of N, 56% of P and 69% of Si of phytoplankton growth demand. Besides, the bioavailability of organic nutrients and nutrients regeneration in the euphotic zone during the bloom should be studied further. Data from the two drift stations showed that 57–76% of DIN and 46–68% of phosphate in the upper water layer could be rapidly assimilated by phytoplankton to allow start of the bloom in about one week in the central YS if other physical factors (i.e. temperature, stability of water column, light availability) were optimal for phytoplankton growth.

Acknowledgments The authors are very grateful to colleagues from the Laboratory of Marine Biogeochemistry, Ocean University of China for their help in field work. This study was supported by the National Basic Research Program of China (Nos. 2006CB400601 and 2011CB409802) and the Natural Science Foundation of China

(Nos. 40925017 and 41221004). We also show our thanks to the anonymous reviewers, the captain and crews of R/V Bei Dou.

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