Process study of biogeochemical cycling of dissolved inorganic arsenic during spring phytoplankton bloom, southern Yellow Sea

Science of the Total Environment 593–594 (2017) 430–438

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Process study of biogeochemical cycling of dissolved inorganic arsenic during spring phytoplankton bloom, southern Yellow Sea Lei Li a,b, Jing-Ling Ren a,b,⁎, Xiu-Hong Cao a, Su-Mei Liu a,b, Qiang Hao c, Feng Zhou c, Jing Zhang d a

Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Ocean University of China, 238 Songling Road, Qingdao 266100, PR China Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, PR China State Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography, State Oceanic Administration, 36 Baochu North Road, Hangzhou 310012, PR China d State Key Laboratory of Estuarine and Coastal Research, East China Normal University, 3663 Zhongshan Road North, Shanghai 200062, PR China b c

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• As cycling in the Yellow Sea, an important fishery, was studied. • Dissolved inorganic As behaved nonconservatively during a phytoplankton bloom • ~15.1% As(5+) in the euphotic zone was converted to As (3+) at 0.53 nmol/L/d. • Dissolved As (7.1%) was scavenged from the water column by uptake of phytoplankton. • As conversion efficiency per unit of diatom was N 5-fold higher than dinoflagellates.

a r t i c l e

i n f o

Article history: Received 14 November 2016 Received in revised form 11 March 2017 Accepted 11 March 2017 Available online xxxx Editor: D. Barcelo Keywords: Arsenate Arsenite Dinoflagellates Diatoms Chlorophyll-a

a b s t r a c t Previous studies in the southern Yellow Sea (SYS) suggest that large spring phytoplankton blooms (SPBs) have occurred in recent decades. Elevated primary production in the water column can lead to the accumulation and transformation of trace elements. Two field study cruises (including two drifting anchor surveys) were conducted on 12–19 February and from 24 March to 15 April 2009, to investigate the impact of different SPB development periods on the concentrations of total dissolved inorganic arsenic (TDIAs: [TDIAs] = [As(V)] + [As(III)]) and As(III) (arsenite) in the SYS. The distribution of TDIAs in the study area was similar between the two field studies, with concentrations increasing from coastal to offshore areas. High arsenite concentrations and As(III)/TDIAs ratios were found in areas having high concentrations of chlorophyll-a, particularly in the subsurface waters of the central SYS during the drifting surveys, where a significant SPB occurred. Results show that the integrated arsenite concentrations increased at an average transformation rate of 0.53 ± 0.24 nmol/L/d within the 15 days during the bloom, and data from the anchor drifting surveys indicated that approximately 15.1% of the arsenate in the euphotic zone (~30 m depth) was converted to arsenite. In addition, 7.1% of TDIAs was scavenged from the water column by phytoplankton forming the blooms (a factor of 5 higher than expected). A preliminary box model was established to estimate the budget for TDIAs in the SYS in early spring (February to April). This showed that biological scavenging is an important sink for TDIAs, which may promote the transformation and migration of inorganic arsenic species, and thus have a substantial impact on the biogeochemical cycling of this element in the SYS. Depletion of arsenate in the upper waters could lead to arsenate stress, potentially damaging fisheries and the ecosystem. © 2017 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Ocean University of China, 238 Songling Road, Qingdao 266100, PR China. E-mail address: [email protected] (J.-L. Ren).

http://dx.doi.org/10.1016/j.scitotenv.2017.03.113 0048-9697/© 2017 Elsevier B.V. All rights reserved.

L. Li et al. / Science of the Total Environment 593–594 (2017) 430–438

1. Introduction The southern Yellow Sea (SYS) is a semi-enclosed marginal sea bordered by China and the Korean Peninsula, in the western Pacific Ocean. It has an area of approximately 3.09 × 105 km2 and an average depth of 45.3 m, and is an important fishing ground for many species of fishes and prawns (Su and Yuan, 2005; Lu et al., 2013; Shan et al., 2013). The fisheries and mariculture in the SYS make a significant contribution to the development of adjacent coastal economies, providing annual production equivalent to nearly 300 billion dollars (Yu et al., 2012; Zhang et al., 2014). However, the SYS has been negatively impacted by natural and anthropogenic factors (e.g. climate change and eutrophication), and the structure and function of its ecosystem have changed markedly; the

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changes in recent years have the potential to restrict economic development, and affect human health (Lin et al., 2005; Zhang et al., 2008; Fu et al., 2009; Sun et al., 2015; Wu et al., 2015). The SYS is influenced by complex shelf circulation systems, involving several major hydrological features (Fig. 1a, b) including: the Yellow Sea Warm Current (YSWC), which transports warm and relatively high salinity water from the open ocean into the SYS; the cold and low salinity Yellow Sea Coastal Current (YSCC) and the Korea Coastal Current (KCC), which move along the coasts of China and Korea, respectively (Su, 1998; Naimie et al., 2001; Xu et al., 2009); and the moderate temperature and salinity Yellow Sea Central Water (YSCW), which mainly occurs in the broad shelf region of the SYS and has hydrographic properties that are related to distinctive source water masses (Zhou et al., 2013). Although

Fig. 1. Sampling locations in the southern Yellow Sea. (a) 12–19 February 2009; (b) 24 March to 15 April 2009; (c) and (d) drifting anchor sampling trajectory conducted at stations Z11 (tracing time 102 h, tracing distance 53.7 km) and Z4 (tracing time 126 h, tracing distance 119.2 km), respectively. The shadowed region in Fig. 1(b) is the estimated high frequency bloom region; ★ drifting anchor stations; ○ SPB stations.

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many rivers enter the SYS from China and Korea, most terrestrial materials and pollutants are derived from dry atmospheric deposition associated with Asian dust storms that occur frequently in winter and spring (Zhang et al., 2001; Zhang and Gao, 2007; Ren et al., 2011). The central SYS is beyond the direct influence of rivers, and atmospheric deposition is thought to be a major source of nutrients and trace metals that stimulate the spring phytoplankton bloom (SPB), which typically occurs in April in this area (Zhang and Liu, 1994; Chung et al., 1998; Zhang et al., 2002, 2004, 2007a; Xuan et al., 2012). The SPB is one of the most important biological processes in the SYS, and plays a key role in the marine food web (Xuan et al., 2012; Li et al., 2013a). It is a crucial event in the dynamics of carbon flux, producing high levels of new production and biomass accumulation, and often high sedimentation rates (Falkowski et al., 2003; Lin et al., 2013). The primary production during the SPB leads to the release of high concentrations of dissolved organic matter (DOM) from phytoplankton into the water column, and typically the accumulation or transformation of trace elements (e.g. As) (Nagata, 2008; Almroth et al., 2009). This process may have negative impacts on fisheries, mariculture, and potentially the ecosystem, and should receive more intensive scientific investigation (Millward et al., 1993; Francesconi and Edmonds, 1997; Mandal and Suzuki, 2002; Lin et al., 2005; Zhang et al., 2008; Fu et al., 2009; Sun et al., 2015; Wu et al., 2015). Arsenic is a toxic metalloid element, and its biogeochemical behavior in marine environments is complex, because it occurs in various oxidation states (+5, +3, 0, −3) and a variety of organic compounds (Cutter et al., 2001; Ellwood and Maher, 2002). As(III) (arsenite) is generally considered to be more toxic than As(V) (arsenate) and most of the organic species (Francesconi and Edmonds, 1997; Hu and Cai, 2009). Based on thermodynamics, arsenate is more stable than arsenite, and has an important role in most oceans (Sánchez-Rodas et al., 2005; Romić et al., 2011). However, the concentration of arsenite can increase when reducing conditions occur in the environment, through biologically mediated phytoplankton production, as a result of bacterial dissimilatory reduction, or by photochemical generation (Neff, 1997; Cutter and Cutter, 1998; Mandal and Suzuki, 2002; Li et al., 2014). As a consequence of its chemical structural similarity to phosphate, arsenate can be transformed into arsenite or organic arsenic species (e.g. monomethylarsenic or dimethylarsenic), then released back into the water column from phytoplankton, when surface water phosphate concentrations are extremely low (b 0.05 μmol/L) (Beceiro-Gonzaèlez et al., 2000; Cutter et al., 2001). In addition, methylated arsenicals can be produced through phytoplankton detoxification, microbial action, or bioaccumulation and release (Sanders and Riedel, 1993; Hellweger et al., 2003). Some of the high molecular weight organic arsenic compounds formed in the water column are buried in the sediment along with other biological detritus and particles, while some is decomposed to inorganic arsenic and released back into the near bottom waters, through DOM decomposition by microorganism during particle deposition (Masscheleyn et al., 1991; Millward et al., 1993; Legeleux et al., 1994). The study of biogeochemical cycles of dissolved arsenic have been extensive in the Pacific (Andreae, 1979; Cutter and Cutter, 2006), Atlantic (Cutter and Cutter, 1995, 1998; Cutter et al., 2001), and Southern Oceans (Featherstone et al., 2001), coastal Australia (Munksgaard and Parry, 2001), the North Sea (Millward et al., 1996), the Baltic Sea (Andreae and Froelich, 1984), and in many rivers (Schaeffer et al., 2006) and estuaries (Gieter et al., 2005; Li et al., 2014) worldwide. However, there are limited data on the concentrations and distribution of arsenic in the SYS (Ren et al., 2010; Liu et al., 2011; Sun et al., 2015; Wu et al., 2015). The impacts of SPB development on the biogeochemical cycles of arsenic species are unknown, and understanding of the efficiency of utilization of arsenic by different phytoplankton species is also at a preliminary stage. Thus, the aims of this study were to: (1) provide more extensive data on the occurrence of arsenic in the SYS; (2) study arsenic dynamics during the SPB, and the response of phytoplankton species; and (3) develop a budget for dissolved inorganic arsenic in

the early spring in the SYS. The study contributes to knowledge of the role of biological processes in the biogeochemical cycle of dissolved arsenic, and the potential hazards of this to the SYS ecosystem. 2. Materials and methods 2.1. Sample locations and sampling Two field study cruises were conducted aboard the R/V Bei Dou in the SYS (approximately 32–37° N and 121–125° E) during 12–19 February and 24 March to 15 April 2009, respectively (Fig. 1a, b). The first cruise (February 2009) occurred in the absence of a SPB, and was used to provide baseline information on the biogeochemical behavior of arsenic in the study area. The second cruise involved a general survey based on grid stations (24–30 March), and two anchor drifting experiments (the vessel was anchored at SPB stations) from 30 March to 15 April. Based on historical long-term ocean color chlorophyll data available from SeaWiFS, a potential high frequency bloom region (HFBR) having an area of approximately 19,600–21,200 km2 was identified as likely to develop a SPB (Fig. 1b; Lin et al., 2013; Zhou et al., 2013). Within this region, in-situ chlorophyll-a (Chl-a) concentrations were measured using in-vivo fluorescence to monitor for the formation of a SPB (Chla N 4 μg/L, Xuan et al., 2011; Li et al., 2013a; Zhou et al., 2013). When a bloom was detected, a surface drifter was released to identify the movement of the water mass containing bloom patches. The research vessel followed buoys launched at 03:30 h on 4 April from station (St.) Z11 (located near St. B20: 35°59.761′ N, 123°00.356′ E, 72 m depth) and at 13:42 h on 9 April from St. Z4 (located near St. B23: 35°30.123′ N, 124°00.289′ E, 83 m depth) to trace the development of the bloom (Fig. 1b). Samples for Chl-a and dissolved arsenic analysis were collected every 3 h and 6 h, respectively, until the bloom had almost disappeared. In total, the buoy tracking for stations Z11 and Z4 involved 102 h and 126 h of drifting anchor measurements, respectively (Fig. 1c, d). A CTD profiler rosette assembly (Sea-Bird 911plus) containing Niskin bottles was used to obtain depth profiles of temperature, salinity, turbidity, and fluorescence in the water column at the grid stations and the drifting stations. Discrete water samples were collected for analysis of Chl-a, nutrients, and arsenic species at depths determined from the CTD readings. Following collection the samples were filtered through pre-cleaned 0.45 μm pore-size cellulose filters. Prior to use the filters were soaked in HCl solution (pH = 2) for 24 h in a Class-100 clean station, and then in Milli-Q water (Millipore, USA) until a neutral pH was reached. The filtrates were stored in Nalgene LDPE bottles and then acidified to pH 2 using purified HCl in first cruise (February 2009) and frozen at −20 °C in second (March to April 2009) because of logistical problems occurred in the February. Blanks were also prepared at sea by filtering a known volume of Milli-Q water using methods identical to those for seawater samples. 2.2. Analytical methods In the laboratory, the concentrations of total dissolved inorganic arsenic (TDIAs: [TDIAs] = [As(V)] + [As(III)]) and dissolved As(III) (arsenite) were measured using hydride generation atomic fluorescence spectrometry (HG-AFS). TDIAs was determined by hydride generation at the acidity of 1 mol/L HCl, after arsenate had been reduced to As(III) using a mixed thiourea–ascorbic acid solution. The As(III) concentrations were determined by generating hydride at pH 5.3–5.5 using a buffered sodium citrate–HCl solution; under these conditions arsenate is unable to be reduced to As(III). Consequently, arsine (AsH3) generation by the reduction of potassium borohydride was limited to the As(III) initially present in the sample. The concentration of arsenate was calculated from the difference between the TDIAs and As(III) concentrations. In this process it was assumed that arsenic species other than arsenate and As(III) were present in negligible amounts. The detection limits for

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TDIAs and As(III) using HG-AFS were 0.12 nmol/L and 0.02 nmol/L, respectively. The precision in the TDIAs analysis was better than 3% at a concentration of 20 nmol/L and for As(III) was better than 4.2% at a concentration of 2 nmol/L. To access the accuracy of the method we included the national reference standard sample GSBZ50004-883610116 (Institute for Environmental Reference Materials of Ministry of Environmental Protection), and international standard reference samples NASS-6 and North Sea samples in the analyses. In our analysis of these samples the measurements were within 2% of stated values, indicating that our HG-AFS measurement method was accurate. Values for the hydrographic parameters and the Chl-a and phosphorus concentrations were those previously reported for these field studies (Fig. S1; Jin et al., 2013; Li et al., 2013a; Zhou et al., 2013). Significance tests (independent sample tests) were performed using Statistical Product and Service Solutions (SPSS) software (version 19.0). 3. Results and discussion 3.1. Arsenic regimes in the SYS Ranges and average values for temperature, salinity, Chl-a, phosphate, and arsenic species in the SYS during the two field studies in 2009 are shown in Table 1. Concentrations of Chl-a in February were generally b3 μg/L; they increased slightly with the exception of two stations, where sporadic blooms of very short duration were detected in March (Table 1; Fig. S2). In early April with the solar radiation levels and water temperature increased moderately, the Chl-a concentration increased significantly to N 4 μg/L in the subsurface layer (8–22 m) in the central SYS (Table 1). As a consequence, the concentrations of TDIAs and As(III) showed significant differences between April and February or March (t-test; p = 0.05), particularly in the subsurface layer. The mean concentration of TDIAs (20.7 ± 3.6 nmol/L) in the SYS were higher than in the open ocean (~ 15 nmol/L, e.g. Atlantic Ocean and Pacific Ocean), consistent with most of the marginal seas (~20 nmol/L, e.g. East China Sea, Baltic Sea, North Sea), but lower than the results which have been reported in the rivers, coastal bays, and estuaries polluted by anthropogenic activities (N 30 nmol/L, e.g. Scheldt Estuary, Changjiang Estuary and Laizhou Bay, Table S1). The concentration was within nature levels, but was somewhat higher than reported in previous studies conducted in May 2001 (mean TDIAs concentration = 16.9 nmol/L) and April 2007 (mean TDIAs concentration = 17.8 nmol/L) at times when the SPB was much larger than in 2009 (Ren et al., 2010; Sun et al., 2015). However, previous data on nutrient levels in the SYS have suggested that phosphorus deficiency occurs during the SPB period, based on the fact that at this time the N/P ratio is higher than the Redfield ratio (Zhang and Liu, 1994; Liu et al., 2003; Zhang et al., 2007a; Jin et al., 2013). Extremely low concentrations of phosphorus contribute to the absorption and transformation of arsenic species in the SYS (Sanders and Riedel, 1993; Gregory et al., 2001; Cutter and Cutter, 2006). The As/P molar ratio in the euphotic zone (approximately 30 m: Jin et al., 2013; Zhou et al., 2013) during the bloom period in the SYS was 0.05 ± 0.02, which is a factor of 20 higher than that in the open ocean (Cutter and Cutter, 1995, 2006), and a factor of 2 higher than in

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the East China Sea (Ren et al., 2015). This phenomenon may have negative ecological consequences, and could give rise to food safety problems. Elevated arsenite concentrations in the SYS in early spring will increase the arsenic toxicity, and potentially have negative impacts on the ecosystem and economic sustainability. As shown in Fig. S2, a relatively high TDIAs concentration (N20 nmol/L), was found in the near bottom waters in the south of the SYS, where incursion by the YSWC occurs; this was correlated with high salinity (Fig. S1) and low levels of suspended particulate matter (SPM: Li et al., 2013b). The YSWC brings substantial amounts of TDIAs into the SYS, and is thought to be one of the major sources of TDIAs at the southeastern boundary of the study area. In contrast, the TDIAs concentrations were predominantly low (b 18 nmol/L) in the coastal area during the study period, incorporation of relatively high concentrations of Chl-a confirm that the lower TDIAs values are typical of the long-term occurrence and relatively high efficiency of biological scavenging. In addition, the vertical profiles of temperature, salinity, Chl-a, phosphate, TDIAs, and As(III) at St. B28 (located in the bloom area) and St. B14 (located out of the bloom area) in March 2009 showed that relatively low concentrations of TDIAs (b20 nmol/L) were present in the subsurface layer of the central SYS, where the SPB occurred (Fig. S3). In contrast, high As(III) concentrations (N2 nmol/L) occurred in those areas in February and March, particularly with high levels of Chl-a, even in bottom waters near the shore. This may be related to terrestrial inputs and biological transformation. The As(III)/TDIAs ratios were N 0.15 in the bloom areas, particularly in the subsurface layer, where the ratio was a factor of 3–10 higher than in the other regions. The arsenate consumed in the coastal area can not readily be rapidly replaced because of the low levels of riverine input (Yang et al., 2003; Yang and Youn, 2007) and relatively stable hydrological environment (Xuan et al., 2011; Zhou et al., 2013) in the SYS in winter and early spring. The correlation between TDIAs and salinity in all samples collected in the study area (r b 0.3) indicated a non-conservative behavior of TDIAs in the SYS, because of removal processes (e.g. scavenging by phytoplankton) that occurred; these are discussed in detail below. 3.2. Impact of biological activities on the transformation of inorganic arsenic species in the SYS Large-scale blooms occurred in the subsurface layer (approximately 2–5 m in thickness) in the central SYS from 30 March to 15 April 2009. The species Detonula pumila (a diatom) and Heterocapsa sp. (a dinoflagellate) dominated the blooms at St. Z11 and St. Z4, respectively (Li et al., 2013a). The time series variations of density (sigma-t), Chl-a, TDIAs, and As(III) at St. Z11 and St. Z4 are shown in Fig. S4. The drifting anchor data showed that strong stratification occurred in the water column, with a pycnocline at approximately 20 m and 10 m at St. Z11 and St. Z4, respectively. Elevated concentrations of Chl-a were detected in the subsurface waters (8–20 m at St. Z11, and 15–22 m at St. Z4), and reached maximum values of 5.61 μg/L and 29.54 μg/L at approximately 60 h, respectively, followed by a decline after 80 h. The TDIAs concentrations ranged from 15.4 to 21.7 nmol/L at St. Z11 and 17.8 to 23.1 nmol/L

Table 1 The concentration ranges of temperature, salinity, Chl-a, phosphate, TDIAs, As (III) and As (III)/TDIAs ratios in the SYS (mean values are given in the parenthesis). Time

Layer

Temperature (°C)

Salinity

Chl-a (μg/L)

Phosphate (μmol/L)

TDIAs (nmol/L)

As (III) (nmol/L)

As (III)/TDIAs

2009-02

Surface Bottom Surface Bottom Surface Subsurface Bottom

5.3–13.8 (8.4) 5.2–13.5 (8.7) 3.9–10.5 (7.8) 3.9–11.0 (8.0) 7.5–12.7 (9.6) 7.4–9.2 (8.5) 7.3–9.1 (8.2)

31.50–34.22 (32.81) 31.52–34.24 (32.84) 31.43–33.71 (32.62) 31.44–33.82 (32.74) 32.03–32.71 (32.44) 32.17–33.11 (32.65) 32.71–33.29 (32.82)

0.28–3.61 (0.86) 0.32–2.99 (0.78) 0.23–4.24 (1.56) 0.10–3.36 (1.32) 0.36–3.42 (1.86) 0.82–29.54 (4.71) 0.32–0.76 (0.48)

0.12–0.61 (0.49) 0.07–0.70 (0.52) 0.02–0.66 (0.27) 0.13–0.81 (0.35) 0.01–0.47 (0.18) 0.02–0.57 (0.22) 0.52–1.34 (0.66)

18.9–22.3 (20.8) 18.5–23.0 (20.5) 10.4–24.6 (19.6) 15.8–27.5 (21.6) 17.6–21.8 (20.2) 15.4–21.7 (19.4) 18.9–23.1 (21.2)

– – 0.19–1.97 (0.86) ~0–3.81 (1.25) 0.16–3.61 (1.42) 0.37–7.42 (2.88) 0.12–1.67 (0.78)

– – 0.01–0.18 (0.04) ~0–0.24 (0.06) 0.01–0.19 (0.07) 0.02–0.36 (0.15) 0.01–0.08 (0.04)

2009-03 2009-04 (drifting surveys)

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at St. Z4 during the observation period, with the minimum concentration at both stations occurring in the subsurface waters at approximately 60 h, which corresponded to the maximum Chl-a and As(III) concentrations. As(III) concentrations were higher in the upper water column at both stations, and subsequently decreased to b2 nmol/L below 30 m, following the patterns of Chl-a. After 80 h the vertical profiles of As(III) indicated the water column was well mixed, and the concentration remained extremely low. To assess the impact of the SPB on the biogeochemical behavior of arsenic in the SYS, the bloom development was divided into three successive periods. These included: (i) the incubation period, covering approximately the first 30 h immediately prior to the outbreak of the bloom; (ii) the occurrence period, from approximately 30 to 70 h at St. Z11, and 30 to 80 h at St. Z4, during which times the SPB was growing rapidly; and (iii) the decline period, immediately following the occurrence period, when the SPB began to decline (Xuan et al., 2011; Lin et al., 2013; Zhou et al., 2013; Li et al., 2013b). The concentrations found during the general survey in March, prior to the occurrence of the SPB, were used as the background value. Fig. 2 shows the variations in the integrated concentrations (every 20 h, including 3–4 sampling sites) for Chl-a, TDIAs, and As(III) in the euphotic zone at St. Z11 (Fig. 2a) and St. Z4 (Fig. 2b) during the three bloom periods. The concentrations of Chl-a were approximately 1 μg/L at both stations in March, and increased slightly to 2–3 μg/L during the incubation period. With onset of the bloom the Chl-a concentrations rose rapidly to N4 μg/L, especially at St. Z4 where a maximum concentration of N10 μg/L was found. After 70–80 h the concentration gradually returned to natural levels. The background concentrations of As(III) were b1 nmol/L, but increased significantly to N 3 nmol/L when the SPB occurred. During the decline period the concentration of As(III) began to decrease slightly, to approximately 1 nmol/L. The maximum As(III)/ TDIAs ratio (0.36) was found at 60 h at St. Z11, and was 3 to 5 fold higher

than in any other period. In addition, the As(III)/TDIAs ratio showed a negative correlation with dissolved inorganic phosphate (DIP) in the euphotic zone during the drifting surveys (r = 0.85, p b 0.05, Fig. 3), which infers that during the SPB, when the concentration of phosphate is depleted, the phytoplankton absorb arsenate and release arsenite, because arsenate and phosphate have similar chemical structures. The biological conversion of arsenate also explains why the maximum ratios of As(III)/TDIAs usually occurred at 40–60 h during the drift surveys, when the phytoplankton were growing rapidly. Based on the average change in the integrated As(III) concentration in the euphotic zone and the time of the bloom incubation and occurrence period (0–60 h), we estimated the maximum As(III) formation rate was 2.24 ± 1.07 nmol/L/d and 0.69 ± 0.28 nmol/L/d at St. Z11 and St. Z4, respectively. The average As(III) formation rate was estimated to be 0.53 ± 0.24 nmol/L/d throughout the entire drifting survey period, based on the difference in As(III) concentrations prior to and following the bloom. Based on the values above we use the product of the average arsenite formation rate, the volume of the euphotic zone in the HFBR, and the duration of the bloom to estimate the internal transformation between arsenate and arsenite, based quantitatively on the law of conservation of mass. We assumed that every bloom lasted 5 days, and that 4–5 blooms occurred during the early spring period in the SYS (Hu et al., 2004; Fu et al., 2009; Xuan et al., 2011, 2012). Based on the above we estimated that 7.3 ± 2.9 × 106 mol arsenate was converted into arsenite during the SPB, which accounted for 15.1 ± 6.0% of the arsenate in the euphotic zone of the HFBR. These values are similar to those reported in previous studies of coastal areas, which have found that As(III)/TDIAs ratios of approximately 10% are usual background, but during blooms the ratio can reach 30% or more (Cullen and Reimer, 1989; Cutter, 1991; Ren et al., 2007; Li et al., 2014; Ren et al., 2015). It is notable that the diatom bloom (St. Z11) had a greater impact on the internal transformation of arsenic species than did the dinoflagellate

Fig. 2. Comparison of the integrated concentrations of Chl-a, TDIAs, and As(III) in the euphotic zone at St. Z11 (a) and St. Z4 (b) during the time series investigation. Note that the values for St. B20 and St. B23, from the grid survey in March, were used as the background concentrations. The three dashed rectangles indicate the bloom incubation, occurrence, and decline stages. (c) and (d) shows the difference of integrated TDIAs and As(III) concentrations calibrated using the concentrations of Chl-a between the subsequent time periods in the euphotic zone at St. Z11 (c) and St. Z4 (d).

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Fig. 3. Relationship between the As(III)/TDIAs ratio and DIP in the euphotic zone in the SYS during the drift surveys.

bloom (St. Z4). Fig. 2c and d show the differences in the integrated concentrations of TDIAs and As(III), which was calibrated using the concentrations of Chl-a between subsequent time periods in the euphotic zone at stations Z11 and Z4. The conversion efficiency of arsenic species per unit of diatom Chl-a was N 5–fold higher than that for dinoflagellates throughout the entire drift surveys, even though their original TDIAs and As(III) concentrations were very similar. This finding may be related to different nutrient utilization characteristics between diatom and dinoflagellate blooms because of their different cell metabolic mechanism (Ou et al., 2006; Tian, 2011). The results of studies of the phosphate dynamics, undertaken during the same field studies reported here, confirms the potential phosphate limitation occurred during the diatom bloom (DIN:DIP = 18.3) instead of the dinoflagellate bloom (DIN:DIP = 16.2) based on the Redfield ratio (Jin et al., 2013). The phosphate deficiency could accelerate the absorption and transformation of arsenate during diatom blooms, based on the similar chemical structure of phosphate and arsenate. However, as we lack direct evidence, our understanding of the mechanism remains very limited; this should be the subject of further study. 3.3. Scavenging of TDIAs during the spring phytoplankton bloom Because of the absence of dissolved organic arsenic data, the differences in the TDIAs concentration (ΔcTDIAs, ΔcTDIAs = cMar. − cFeb.) in the euphotic zone at the same stations in February and March were used to approximate the biological scavenging of TDIAs in the SYS over this period. Negative values suggested scavenging of TDIAs from the water column, whereas positive values suggested TDIAs regeneration through diagenesis (Belzile and Tessier, 1990; Li et al., 2014), regardless of the variations in riverine input and incursion of the YSWC because of the similar hydrographic properties over this period (Zhou et al., 2013). Fig. 4 shows the negative correlation between the differences in the Chl-a (ΔcChl-a) values and the TDIAs (ΔcTDIAs) concentrations in the euphotic zone of the SYS (r = 0.70, p b 0.05), and confirms the impact of biological activities, even though no bloom was detected during this period. To aid quantitative comparisons of TDIAs scavenging between the bloom and no bloom periods, we further assessed differences in the TDIAs concentration detected at grid stations between February and March, and integrated the rate of removal of TDIAs at two drifting stations in April to estimate the amount of TDIAs removed in the euphotic zone of the HFBR. In making the calculations we assumed: (1) that the water column above 30 m in the HFBR was relatively stable; and (2) that differences in the contribution of atmospheric deposition between the two field studies were insignificant (Li et al., 2013b). Thus, we used the equation

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Fig. 4. Euphotic zone differences in Chl-a (ΔcChl-a = cMar − cFeb.) plotted against differences in TDIAs (ΔcTDIAs = cMar. − cFeb.) between the two field studies in the SYS.

below to estimate the amount of TDIAs (M) removed from February to March (Welz and Schlemmer, 1986; Barrera et al., 1995): n

M ¼ ∑i¼1 ci V i

ðn ¼ 42Þ

where ci represents the ΔCTDIAs values in different sampling layers between the two field studies; Vi represents the volume of the water column, which was calculated as the product of the area and the thickness of each layer; i represents the sampling numbers (2–4 at each station, 12 stations in total) above 30 m in the HFBR. These calculations indicated that the integrated amount of TDIAs removed from water column could reach 1.8 ± 0.8 × 105 mol from February to March, equating to approximately 1.5 ± 0.7% of the total amount of TDIAs in the euphotic zone in the area. We also assumed that: (1) the integrated rate of removal of TDIAs at the two drift stations represented the overall situation in the HFBR; (2) approximately 4–5 blooms occurred and every bloom in April lasted 5 days; and (3) the number of diatom and dinoflagellate blooms was equal. Based on the assumption above, we used the product of the integrated rate of removal of TDIAs above 30 m (approximately 0.42 nmol/ L/d, calculated as the difference in the TDIAs concentrations prior to and following the bloom), the time of the SPB, and the volume of the euphotic zone to calculate the average amount of TDIAs removed during the bloom period. The estimate for April was 8.5 ± 3.6 × 105 mol, which was approximately 5–fold higher than that removed from February to March, which suggests that approximately 7.1% of the TDIAs in the upper water were scavenged from the water column during the SPB outbreak in the SYS. This appears to be consistent with previous studies that have demonstrated that dissolved organic arsenic is biologically transformed by uptake of arsenate by phytoplankton, and its subsequent release in organic or other forms (Sanders and Riedel, 1993; Millward et al., 1996; Li et al., 2014). However, the process of removal of arsenate during the SPB remains secondary compared with the internal transformation of arsenate to arsenite, especially during the period of rapid phytoplankton growth. 3.4. Arsenic budget for the southern Yellow Sea in early spring The arsenic budget for the SYS is currently based on the LOICZ Biogeochemical Modelling Guidelines (Gordon et al., 1996), which relies on the concept of conservation of water and salt masses (Waslenchuk, 1978; Ren et al., 2010; Sun et al., 2015). We updated the estimates for the arsenic budget for early spring only (from February to April), instead of constructing budgets for yearly averages (Sun et al., 2015); this was because of the unique seasonal characteristics of hydrographic processes, dust storms, and SPBs in this region (Zhang and Su, 2006; Ren et al., 2011; Zhou et al., 2013). Because of the absence of available data, contributions from groundwater and waste drainage were not included.

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Approximately 30 rivers discharge into the SYS, although in early spring, which is in the dry season, the runoff from each river accounts for only approximately 5–10% of the annual runoff (Liu et al., 2003). The TDIAs data for each river were derived from ongoing monitoring stations (e.g. the Changjiang) or because of the lack of available data, were calculated from the TDIAs/DIP ratios (e.g. the Han River) (Ren et al., 2011; Sun et al., 2015). The water exchange between the Bohai Sea and the Yellow Sea, and between the Yellow Sea and the East China Sea have been calculated and updated from previous studies, based on water and salt balances (Zhang et al., 2007a). In general, the flux of TDIAs from rivers and adjacent marginal seas can be estimated from the product of water discharges and the TDIAs concentration, and are listed in Table 2. Atmospheric deposition is one of the most important sources of TDIAs into surface waters; this is especially relevant for the SYS, which is affected by 3–4 dust storm events in early spring each year (Zhang et al., 2001; Zhang and Gao, 2007). The contribution of dry deposition to TDIAs concentrations is usually calculated from the product of geometric average dust deposition fluxes (75.3 ± 23.3 mg/m2/d: Ren et al., 2011), the average concentration of arsenic in atmospheric aerosols in Chinese coastal seas (39.1 ± 9.8 μg/g: Ren et al., 2007; Hsu et al., 2010; Li, 2014), and the average solubility of arsenic from the dust into the ocean (3.7 ± 2.2%: Ren et al., 2007). In addition, the contribution of arsenic from wet deposition onto the SYS shelf was estimated as the product of the average concentration of TDIAs in rainwater (Ren et al., 2007; Hsu et al., 2009; Li, 2014) and the rainfall amount (Zhou et al., 2004; Lin et al., 2007; Zhang et al., 2007b) in the early spring. Thus, the total atmospheric deposition of arsenic into the SYS in the early spring was 0.0145 mol/s; the uncertainty in this value is 60%, based on variations in the average solubility of arsenic, and rainfall levels, which show significantly seasonal and sporadic variability. Release from sediment may be another crucial source of arsenic into near bottom waters (Chaillou et al., 2003). However, as very limited reliable arsenic data are available on the exchange flux at the sediment–water interface in the SYS, we made estimates based on previous studies in the coastal area of the south SYS (near the Changjiang estuary) and the north SYS (near Sanggou Bay, Shandong Peninsula) (Li, 2014; Li et al., 2014). We assumed that the sediments in the SYS were under natural conditions not affected by arsenic pollution or extreme environmental conditions, such as hypoxia. We found that arsenic was released from silt and clay sediments into the overlying water with an average flux of 0.3477 ± 0.2086 nmol/m2/h and 0.0752 ± 0.0291 nmol/m2/h, respectively. The ratio of the area of silt sediments to clay sediments in the SYS is approximately 5.67:1 (Fan et al., 2002).

Thus, based on a 90-day period including early spring, the release of arsenic from the sediments was estimated to be 0.0176 ± 0.0119 mol/s. The scavenging of TDIAs during the period when large-scale blooms occur is worthy of consideration. As noted in section 3.3, the amount of TDIAs scavenged in the euphotic zone of the HFBR was calculated to be 1.8 ± 0.8 × 105 mol from February to March, and 8.5 ± 3.6 × 105 mol in April. However, most of the TDIAs (approximately 50–90%) scavenged in the upper water column will be released into deep water layers through decomposition and diagenesis (Andreae and Froelich, 1984; Millward et al., 1993; Riedel et al., 2003; Price et al., 2012; Li et al., 2014). Consequently, the scavenging of TDIAs over the full depth of the HFBR may be much less than that in the upper water column, and should be reevaluated. Based on the calculation described in section 3.3, we estimated that 1.4 ± 1.2 × 105 mol of TDIAs was scavenged from the full depth of the water column in the HFBR from February to March, and approximately 2.6 ± 2.2 × 105 mol of TDIAs was scavenged during the bloom period in April, based on the assumption that 50–90% of the scavenged TDIAs is regenerated and released back into deep waters. Thus, the total scavenging of TDIAs in the HFBR was estimated to be 0.0514 ± 0.0437 mol/s. Because of the absence of available data, the amount of TIDAs scavenged in other regions is not considered further here. Based on the average concentration of TDIAs (20.7 ± 3.6 nmol/L) in the SYS, the TDIAs inventory (the product of the TDIAs concentration, the area, and the average water depth) was estimated to be 2.9 ± 0.4 × 108 mol. From the sum of the fluxes listed in Table 2, the total input flux of TDIAs into the SYS in the early spring was approximately 0.1857 ± 0.0591 mol/s, and the total output flux was 0.1665 ± 0.0631 mol/s. The input and output fluxes for TDIAs differed by 10.3% in the SYS in the early spring, which indicates that some net sinks of TDIAs may not be known, and/or there are uncertainties in the estimates used for determination of the various components used in the calculations. The SPBs that occur in the upper water column of the central SYS may have a significant effect on the transformation and distribution of arsenic species, and thereby impact the biogeochemical cycling of arsenic in the early spring period. The increased concentration and residence time of toxic inorganic arsenic species during the SPB may have the potential to damage the marine ecosystem of the area, and should receive more scientific attention. 4. Conclusion Frequent dust inputs from East Asia and subsequent spring phytoplankton blooms significantly affect the behavior of dissolved trace elements in the marginal seas of China and the western Pacific Ocean

Table 2 Budget of TDIAs in early spring in the SYS. Transport Input Changjiang Huaihe Han River Yalujiang Bohai Atmospheric depositions Dry Wet Sediment release Output East China Sea Biological scavengingb

Salinity

Water fluxes (Sv)

TDIAs (nmol/L)

0 0 0 0 30.0–32.1

0.0008–0.0011 (0.0009) 0.0003–0.0004 (0.0003) 0.0003–0.0005 (0.0004) 0.0004–0.0006 (0.0005) 0.0029–0.0052 (0.0041)

40.3 24.7 43.2 17.3 20.4

± ± ± ± ±

4.3 3.0 14.6a 9.8 0.4

0.2

0.0036–0.0067 (0.0044)

2.1 ± 1.3

26.5–34.8

0.0048–0.0076 (0.0065)

17.7 ± 6.2

TDIAs flux (mol/s) 0.1857 ± 0.0591 0.0322–0.0443 (0.0363) 0.0074–0.0099 (0.0078) 0.0130–0.0216 (0.0173) 0.0069–0.0104 (0.0086) 0.0592–0.1061 (0.0836) 0.0145 ± 0.0087 0.0025–0.0101 (0.0052) 0.0050–0.0134 (0.0093) 0.0176 ± 0.0119 0.1665 ± 0.0631 0.0850–0.1345 (0.1151) 0.0514 ± 0.0437c

Reference Liu et al., 2003; unpublished Liu et al., 2003; Yan and Li, 2010 Hong et al., 1995; Ryu et al., 2008 Liu et al., 2003; unpublished Liu et al., 2003; unpublished Ren et al., 2007; Hsu et al., 2010; Ren et al., 2011 Lin et al., 2007; Hsu et al., 2009; Ren et al., 2007; Li, 2014 Li, 2014; Li et al., 2014

Zhang et al., 2007b; Ren et al., 2010 This study

a Due to the absence of available data for TDIAs concentrations in the Han River, the results were estimated through the As/P ratios on the assumption that the ratios here were similar to Changjiang. b This removal amount of TDIAs might include transformation into other organic and particulate forms of arsenic and scavenge from the water column, regardless of the influence of riverine input and YSWC incursion based on the negligible difference occurring in the euphotic zone of “HFBR” in early spring. c Due to the absence of available data, this result only includes the “HFBR” instead of the whole SYS.

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(Hung et al., 2009). Investigation of the arsenic species and their distribution in the SYS from February to April 2009 provided information linked to the dynamics and biological/chemical reactions taking place in the region. TDIAs concentrations in the SYS generally showed a gradient of increase from coastal waters to offshore areas during the study period, which reflects the effects of coastal blooms in the early spring, and incursion by the YSWC, based on correlations with Chl-a and salinity, respectively. In addition, a large-scale SPB occurred in the subsurface waters of the central SYS, where high As(III)/TDIAs ratios (N0.2) were also observed. Two drifting anchor experiments were conducted to investigate the impact of SPB on the behavior of TDIAs in the HFBR. These showed that the average internal rate of transformation between arsenate and arsenite during the bloom period was 0.53 ± 0.24 nmol/L/d. We calculated that approximately 15.1% of the arsenate in the euphotic zone (b 30 m) was converted to arsenite, based on the assumption that blooms are present in the SYS for 20–25 days in early spring. Approximately 7.1% of the TDIAs was scavenged from the water column in the euphotic zone of the HFBR during the bloom period in April, which is 5-fold higher than was found for the grid stations from February to March (1.5%). In addition, because of differences in nutrient demand, the conversion efficiency for arsenic species during diatom blooms was N 5-fold higher than that during dinoflagellate blooms having the same biomass. A simple box model was established to estimate the arsenic budget in the SYS in the early spring (90 days). Examination of data demonstrated that the major processes controlling arsenic geochemistry in the SYS are riverine input, atmospheric deposition, exchange with the Bohai Sea and East China Sea, release from sediments, and removal through the uptake by phytoplankton. A deficit of 10.3% was found for the outflow of arsenic from the SYS relative to the influx, indicating that there may be unknown net sinks of arsenic, and/or that there are uncertainties in the estimates used for determination of the arsenic fluxes. Based on previous studies the concentration of TDIAs (20.7 nmol/L) was at natural levels, but elevated As/P ratios during the bloom period contributed to the conversion of arsenate into arsenite. As arsenite is more toxic than arsenate, this process may have a detrimental effect on fisheries and sustainable development in that ecosystem; this possibility should receive more attention.

Acknowledgement This study was funded by the National Basic Research Program of Science and Technology of China (2011CB409801) and the National Natural Science Foundation of China (41676072 & 41530965). The Taishan Scholars Programme of Shandong Province (No. ts 201511014) and the Aoshan Talents Program (supported by the Qingdao National Laboratory for Marine Science and Technology: No. 2015ASTP-OS08) are also acknowledged. The authors thank the captain and crew of R/V Bei Dou for sample collection during the field studies. We are grateful to colleagues of the Marine Biogeochemistry Laboratory of the Ocean University of China for their assistance in field and laboratory work. Anonymous reviewers and English editor are especially acknowledged for their constructive suggestions, which greatly improved the manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2017.03.113.

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