Changes in concentrations of biogenic sulfur compounds in coastal waters off Qingdao, China during an Ulva prolifera bloom

Marine Pollution Bulletin 152 (2020) 110940

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Changes in concentrations of biogenic sulfur compounds in coastal waters off Qingdao, China during an Ulva prolifera bloom

T

Chun-Ying Liua,b, Gao-Bin Xua,b, Xue Denga,b, Hong-Hai Zhanga,b, Tao Liuc, Gui-Peng Yanga,b,

⁎

a

Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Qingdao 266100, PR China Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, PR China c College of Marine Life Sciences, Ocean University of China, Qingdao 266100, PR China b

ARTICLE INFO

ABSTRACT

Keywords: Ulva prolifera bloom Sulfur cycle Biogenic sulfur compounds Qingdao coastal waters Sea-to-air flux The Yellow Sea

Distributions and variations of biogenic sulfur compounds including dimethylsulfide (DMS), dissolved and total dimethylsulfoniopropionate (DMSPd and DMSPt) and acrylic acid (AA) were investigated in coastal waters off Qingdao, China during the late-bloom and after-bloom periods of the Ulva prolifera bloom of 2015. DMSPd, DMS and AA concentrations after the bloom were significantly higher than during the late-bloom, but DMSPt concentrations in surface waters began to decrease. High concentrations of these compounds in the surface layer were associated with the bloom, with the exception of increased concentrations of DMSPt in the middle layer as decaying U. prolifera debris settled. The sea-to-air fluxes of DMS were estimated to be 18.08 and 24.24 μmol m−2 d−1 during the late-bloom and after-bloom, and about three times higher than the reported average fluxes of the Yellow Sea, which highlighted the impacts of U. prolifera blooms on DMS emissions.

1. Introduction Green tides are massive accumulations of unattached green algae that have been recognized as one type of harmful algal blooms, which can occur when there are favorable hydrographic conditions in eutrophic areas (Fletcher, 1996; Nelson et al., 2003). The number of green tide outbreaks has increased significantly in the last few decades alongside global environmental change (Largo et al., 2004). Their increasing frequency has caused severe economic and ecological impacts, which is why their origin, expansion, and biogeochemical processes have attracted worldwide attention. Since 2007, green tides of the macroalga Ulva prolifera have recurred annually in the Yellow Sea (YS) in China (Liang et al., 2008; Sun et al., 2008). Of special note, an extensive U. prolifera bloom occurred between May and July in 2008, which has been regarded as one of the largest blooms in recorded history (Hu and He, 2008). According to satellite observations, the algae originated from the Subei shoal of Jiangsu Province, accumulated while moving into the middle of the YS in the dominant northward currents, developed into a bloom under suitable sunlight and hydrological conditions, and then drifted to the Shandong Peninsula caught in the southeast monsoon and summer ocean surface currents (Hu et al., 2010; Keesing et al., 2011; Miao et al., 2018). Previous studies have focused on the species composition of green tide populations (Liu et al., 2009,

2013a; Miao et al., 2018), the origin of green tides (Lee et al., 2011; Zhang et al., 2014a; Wang et al., 2015), the breaking out mechanisms, and potential control methods (Wang et al., 2012; Zhou et al., 2015; Gao et al., 2016; Li et al., 2016b). However, relatively little is known about the migration and transformation of substances within continuous large green tides in the YS. Even less was known about the longterm environmental and ecological impacts caused by green tides in blooming regions, especially along the downstream coastline cities, such as Qingdao. When a green algal bloom occurs, the chemical environment in seawater can be greatly changed (Van Alstyne et al., 2015). For example, the quick uptake of nutrients from seawater causes nutrient limitation for other photosynthetic organisms in the blooming area. Photosynthesis during the day combined with respiration at night brings about marked pH and dissolved oxygen (DO) fluctuations which can affect other marine organisms (Van Alstyne et al., 2015). Furthermore, seaweeds that form green tides can usually produce allelopathic compounds, such as dimethylsulfoniopropionate (DMSP), reactive oxygen species (ROS), dopamine and their breakdown products, which can have negative effects on the germination of seaweed zygotes and the growth of other seaweed species (Nelson et al., 2003; Wang et al., 2011; Xu et al., 2013). Further effects can be found in both benthic (Nelson et al., 2003) and planktonic ecosystems (Tang and Gobler,

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

https://doi.org/10.1016/j.marpolbul.2020.110940 Received 5 October 2019; Received in revised form 20 January 2020; Accepted 23 January 2020 0025-326X/ © 2020 Elsevier Ltd. All rights reserved.

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2011). The changes in seawater chemistry have been investigated during green tides in the YS, and have included DO and carbonate parameters (Hu et al., 2015; Zhang and Wang, 2017; Deng et al., 2018), and nitrogen and phosphate (Gao et al., 2013; Shi et al., 2015; Li et al., 2017), among others. However, variations of DMSP and its degradation products dimethylsulfide (DMS) and acrylic acid (AA), caused by U. prolifera blooms have not been examined, despite being one of the most abundantly produced metabolites in most species of Ulva algae (Van Alstyne and Puglisi, 2007; Van Alstyne, 2008). DMSP, DMS, and AA act as activated defenses in marine macroalgae (Van Alstyne et al., 2001). Moreover, DMS released into the atmosphere oxidizes to form compounds that function as cloud condensation nuclei (CCN), leading to an increase in the albedo of the atmosphere and a decrease of local temperatures, although other sources also contributed to changes in CCN (Quinn and Bates, 2011). DMS can also contribute to the formation of acid rain (Nguyen et al., 1992). We see from the literature that DMSP and its degradation products released by the green tide event can affect the climate and environment, and therefore, an in depth quantitative study of the sulfur cycle is required. In this work, we examined the spatial-temporal patterns of DMS, DMSP, and AA in the coastal waters off of Qingdao during the latebloom period (when U. prolifera was decaying but still present) and after the bloom (when U. prolifera was no longer present) in summer, 2015. The field investigation data were analyzed to illustrate the links between the large-scale floating U. prolifera biomass, environmental parameters, and the phase of the green tide bloom and the production of biogenic sulfur compounds. Using this information, we attempted to understand the influence of U. prolifera green tides on the local ecological environment and climate. 2. Materials and methods 2.1. Study area The breakout of green tides has become an annual event during spring-summer in the YS (Liu et al., 2013a). The drift path and distribution of the bloom were obtained from the North China Sea Branch of the State Oceanic Administration (SOA) in 2015 (www.ncsb.gov.cn/ n1/n127/n139/n39/index_5.html) (Fig. 1). A large proportion of U. prolifera was transported to the coast of Qingdao by surface ocean currents and the southeast monsoon during early summer, before slowly decaying and disappearing in mid to late August (Hu et al., 2010; Keesing et al., 2011; Xu et al., 2016; Hu et al., 2017). Qingdao coastal waters are located in the western YS and surrounded by the Shandong Peninsula. The increasing anthropogenic activities, inorganic fertilizer application, and effluents from aquaculture enterprises have greatly increased sewage input into the sea in this area (Zhang et al., 2012), which is dominated by semi-diurnal tidal currents (Zhao et al., 2011). As one of the main final destinations of U. prolifera green tides in the YS, the change of the chemical environment in Qingdao coastal waters deserves attention. 2.2. Sampling Distributions of U. prolifera on 16 July (representing the late bloom stage) and 5 August (when the U. prolifera began to disappear) in 2015 are shown in Fig. 1. Two cruises were carried out on the R/V ‘Haidiao 235’, during the late bloom (16–17 July) and after the bloom (28–29 August). Here the late bloom and after the bloom refer to the times when U. prolifera had begun to decay and when it had disappeared from the coastal waters of Qingdao, respectively. The study region and sampling stations are shown in Fig. 2. Samples were collected from the surface, middle, and bottom layers using 8 L Niskin bottles, which corresponded to depths of 0.5 m and 10 m from the surface, and 2 m from the bottom, respectively. Temperature and salinity were recorded in situ with a Conductivity-Temperature-Depth sensor (Manta2, Eureka

Fig. 1. Distributions of Ulva prolifera on 16th July and 5th August in 2015. (Cited from the North China Sea Branch of State Oceanic Administration (http://www.ncsb.gov.cn/n1/n127/n139/n39/index_5.html). 2

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Fig. 2. Topography of the southern Yellow Sea and sampling stations in the study area.

Water Probes, Austin, USA). Two milliliter aliquots for dissolved DMS measurements were filtered through Whatman glass fiber filters (GF/F) and directly injected into glass bubbling chambers, sealed quickly, immersed in ambient seawater in darkness, and analyzed after return to the laboratory within 12 h of collection. For dissolved DMSP (DMSPd) analysis, 4 mL aliquots of seawater were filtered under gravity through a 0.7 μm-pore GF/F filter (Kiene and Slezak, 2006). Samples for total DMSP (DMSPt) and DMSPd analyses were immediately fixed with 40 μL of 50% sulfuric acid in 10 mL glass vials for storage. The addition of sulfuric acid keeps DMSP stable and causes the oxidation of endogenous DMS (Shooter and Brimblecombe, 1989). Samples for AA analysis were collected directly from the Niskin bottles and filtered under gravity through a precleaned 0.2 μm AS 75 Polycap filter capsule (a nylon membrane with a glass microfiber prefilter enclosed in a polypropylene housing; Whatman Corporation, USA; Wu et al., 2015). The filtrates were transferred to 40 mL glass vials with Teflon™-lined caps and stored in the dark at 4 °C. Samples for DO determination were collected using 125 mL glass bottles and immediately treated with the Winkler reagents, sealed, immersed in ambient seawater, and analyzed after returning to the home laboratory. For dissolved organic carbon (DOC), a 30 mL aliquot of each sample was filtered through a 0.7 μm-pore GF/F filter, frozen, and stored in glass bottles at −20 °C. Chlorophyll a (Chl-a) samples were collected by filtering 300 mL seawater through 0.7 μm-pore GF/F filters under low pressure (< 15 kPa) after removing the U. prolifera; the filter membranes were then frozen until analysis. All samples were analyzed after return to the laboratory, within several days of collection.

10 mol L−1 KOH and stored in the dark at 4 °C for at least 24 h to allow the complete conversion of DMSP into DMS before analysis. DMSP was quantified using the method described above according to a 1:1 stoichiometry (Dacey and Blough, 1987). AA was determined using a high-performance liquid chromatography system (L-2000, Hitachi Ltd., Japan) according to Gibson et al. (1996). An Agilent SB-Aq-C18 column with an 0.35% H3PO4 (pH = 2.0) eluent at a flow rate of 0.5 mL min−1 was used to separate AA. The column eluate was measured by a UV detector at 210 nm. The analytical precision was generally in the range of 1.3–1.6%, and the detection limit was 4 nmol L−1 (Liu et al., 2013b). DOC samples were analyzed using a high-temperature combustion method in a total organic carbon analyzer with a platinum catalyst at 680 °C (Shimadzu TOC-VCPH; Japan). DOC concentrations were quantified based on a calibration curve made from potassium hydrogen phthalate. The analytical precision was < 2.0% (Yang et al., 2010). Chl-a on the membrane was measured with a Model F-4500 fluorescence spectrophotometer (Hitachi, Japan) after extraction in 90% acetone according to Parsons et al. (1984). In this study, because samples were filtered through Whatman GF/F membranes after U. prolifera had been removed, the concentration of Chl-a measured here represented the biomass of micro-phytoplankton. In addition, the concentrations of dissolved inorganic nitrogen (DIN, including nitrate, nitrite, and ammonium) were determined using the Technicon AutoAnalyser AA II (Seal Analytical, UK) based on the procedure described by Strickland and Parsons (1972). The detection limits were 0.14 μmol L−1 for nitrate, nitrite and ammonium, with precisions better than 3%.

2.3. Analytical methods

2.4. Sea-air DMS flux estimation

All DMS samples were analyzed using a modified purge and trap method described by Wu et al. (2017). DMS dissolved seawater sample was extracted with high purity nitrogen for 3 min at a flow rate of 40 mL min−1. Then, the gas was dried through a Nafion gas sample dryer and trapped in a loop of Teflon tubing immersed in liquid nitrogen. The trapped gas was desorbed with boiling water and introduced into a GC-14B gas chromatograph (Shimadzu, Japan) equipped with a flame photometric detector and a 3 m × 3 mm glass chromatographic column packed with 10% DEGS on Chromosorb WAW-DMCS. The analytical precision was generally < 10% and the detection limit was approximately 0.4 nmol L−1 DMS. DMSPd and DMSPt samples were injected with 300 μL of

The sea-to-air fluxes of DMS during the late bloom and after the bloom were estimated using a gas exchange model (Liss and Merlivat, 1986):

FDMS = kDMS C = kDMS [DMS]; where FDMS is the sea-to-air flux of DMS (μmol m−2 d−1), kDMS represents the gas exchange coefficient (cm h−1), and ΔC is the difference between the concentration of DMS in the water (CW) and in the air (CA) divided by the Henry's Law constant for DMS. Considering that atmospheric DMS concentrations are generally negligible compared to dissolved DMS levels, we set CA to zero, resulting in ΔC = CW = [DMS], where [DMS] is the concentration of DMS at the sea surface (nmol L−1). 3

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kDMS was calculated from the wind speed u (m s−1) multiplied by the dimensionless Schmidt number Sc (Saltzman et al., 1993). The parameterization advanced by Nightingale et al. (2000) (N2000) is a reasonable intermediate method commonly used for DMS sea-to-air flux calculations and was hence adopted in this study. The mean wind speeds from July and August (i.e. 3.73 and 3.65 m s−1, respectively) in Qingdao coastal waters (Saha et al., 2014) were used to calculate the wind speed-dependent gas transfer coefficient of N2000 (Nightingale et al., 2000):

kDMS = (0.22u2 + 0.33u) (Sc/660) Sc = 2674.0

during the late bloom and after the bloom (P > 0.05, n = 14), while temperatures in the middle and bottom layers of the late-bloom cruise were a little higher than those of the after-bloom cruise. Salinity had a very slight increasing trend from the surface to the bottom layers. The average values of salinity were 31.14 and 31.25‰ in the surface waters during the first and second cruises, respectively, with no significant difference between the two cruises (P > 0.05, n = 14). In the horizontal distribution, the temperature generally exhibited a slight decreasing trend from the coast towards offshore (Fig. 3a), while salinity had the opposite trend (Fig. 3b). The concentration of Chl-a was very low during the late bloom stage, ranging from 0.01 to 0.21 μg L−1 in the surface seawater, with a mean of 0.10 μg L−1. When the bloom was over, an obvious increase in Chl-a was observed (P < 0.05, n = 14), rising to the range of 0.35–0.64 μg L−1. Furthermore, the concentrations of Chl-a in the middle and bottom layers also showed a similar change. The concentration of Chl-a in the surface layer was lower than the concentrations in the middle and bottom layers during the late bloom, however, it was higher after the bloom. The average DOC concentrations were 131 and 130 μmol kg−1 in the surface waters during the first and second cruises, respectively. DOC concentrations during the late bloom were a little higher than those after the bloom in the upper waters, while the opposite was true in the boom layer with the concentration of DOC during the late-bloom period being lower than that after the bloom. Distribution of DOC in surface waters generally showed a decreasing trend from inshore to offshore waters during the late-bloom period. After the bloom, concentrations of DOC generally increased from south to north in the surface layer (Fig. 3c). The pH values in surface water varied from 7.99 to 8.11 and 7.99 to 8.24, with the average values of 8.04 and 8.10 during the late- and postbloom cruises, respectively. The vertical distribution of pH was characterized by a gradual decreasing trend with depth. The pH value in the surface water increased in a northeast to southwest direction during the first cruise, however, it generally decreased from inshore to offshore waters and was generally higher along the coastline during the second cruise (Fig. 3d). The average DO concentrations were 6.69 and 7.16 mg L−1 in the

1/2

147.12 T + 3.726 T 2

0.038T 3

2.5. Statistical analyses Statistical analyses were performed using either Origin 7.5 software (OriginLab Corporation, Northampton, MA, USA) or SPSS 19.0 software (IBM, NY, USA). The differences of biogenic sulfur compounds and related parameters between the late-bloom and after-bloom or between water layers were analyzed using a one-way ANOVA followed by the least significant difference test at α = 0.05. All sample sets were tested for normality with a Shapiro–Wilk test prior to correlation analyses with a Pearson's product moment correlation. The DMSP, DMS and AA concentration data were calculated from two parallel samples in the tables. 3. Results 3.1. Background data The ranges and mean values of temperature, salinity, DO, Chl-a concentration, DOC concentration, and pH are presented in Table 1, and the distributions of temperature, salinity, DOC concentration, pH, and DO are shown in Fig. 3. Seawater temperature on both of the two cruises decreased with the depth. The average temperatures were 24.39 and 24.37 °C in the surface waters during the first and second cruises, respectively. There was no significant difference between the surface water temperatures

Table 1 Ranges and means (in brackets, n = 14) of hydrographic data during the Ulva prolifera late bloom and after the bloom in the coastal waters of Qingdao. Parameters

Cruises

Surface layer

Middle layer

Bottom layer

Temperature (°C)

July

23.74–25.49 (Average:24.39) 22.67–26.38 (Average:24.37) 30.74–31.51 (Average:31.14) 30.82–31.57 (Average:31.25) 6.44–6.88 (Average:6.69) 6.55–7.57 (Average:7.16) 61–183 (Average:131) 67–154 (Average:130) 0.01–0.21 (Average:0.10) 0.35–0.64 (Average:0.45) 7.99–8.11 (Average: 8.04) 7.99–8.24 (Average: 8.10)

21.13–24.32 (Average:22.86) 18.85–24.53 (Average:21.53) 31.02–31.51 (Average:31.26) 30.98–31.46 (Average:31.22) 6.26–7.13 (Average:6.74) 6.23–8.24 (Average:7.08) 61–240 (Average:138) 72–157 (Average:127) 0.06–0.55 (Average:0.25) 0.23–0.35 (Average:0.28) 7.90–8.06 (Average: 7.99) 7.98–8.18 (Average: 8.09)

15.34–22.80 (Average:19.93) 15.34–21.54 (Average:19.28) 31.11–31.57 (Average:31.34) 31.02–31.38 (Average:31.26) 5.33–7.13 (Average:6.44) 6.42–11.82 (Average:8.97) 80–190 (Average:118) 92–156 (Average:129) 0.05–0.32 (Average:0.18) 0.23–0.42 (Average:0.34) 7.84–8.02 (Average: 7.90) 7.78–8.09 (Average: 7.88)

Salinity (‰) DO

(mg L−1)

DOC (μmol kg−1)

August July August July August July August

Chl-a (μg L−1)

July

pH

July

August

August

4

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surface layer during the late bloom and after the bloom, respectively. Notably, at both times the DO was oversaturated. DO concentrations in the surface and middle layers were higher than the bottom layer during the late-bloom period, however, the opposite was true after the bloom.

Comparing the two cruises, it was observed that the DO concentrations of every layer during the late bloom were lower than those after the bloom (Fig. 3e).

a Fig. 3. Horizontal distributions of temperature (°C) (a), salinity (b), DOC (μmol kg−1) (c), pH (d) and DO (mg L−1) (e) in the surface layer (S), the middle layer (M) and the bottom layer (B) in July and August.

5

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b Fig. 3. (continued)

3.2. Distributions of biogenic sulfur compounds in coastal waters of Qingdao

During the late bloom stage, the concentrations of DMSPt in the surface waters ranged from 34.43 to 110.89 nmol L−1, with an average of 67.83 nmol L−1, which was relatively high compared to global seawater averages. Concentrations of DMSPt showed a decreasing trend with depth. Under conditions without U. prolifera, concentrations of DMSPt in the surface layer dropped to the range of

The ranges and mean values of DMSPt, DMSPd, DMS, and AA, which showed significant spatial and temporal variations, are shown in Table 2 and Fig. 4. 6

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c Fig. 3. (continued)

10.36–113.09 nmol L−1, with a mean of 49.79 nmol L−1. The highest concentration of DMSPt appeared in the middle layer after the bloom. The lowest concentrations were measured in the bottom layers for both cruises. During the first cruise the DMSPt concentrations in different layers generally decreased in the north to south direction, however, during the second cruise the highest DMSPt values appeared in the

southern range of our observation area (Fig. 4a). Concentrations of DMSPd in the surface water varied from 3.66 to 21.70 and 7.74 to 73.16 nmol L−1 in July and August, respectively, with averages of 10.48 and 22.89 nmol L−1. During both of these two cruises, the concentrations of DMSPd decreased with depth. Furthermore, the DMSPd concentrations at all three depths during the 7

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d Fig. 3. (continued)

second cruise were far higher than those from the first cruise. During the late-bloom period, the concentrations of DMSPd in the surface layer were generally higher in inshore waters than offshore waters. The higher concentrations appeared in the southern region after the bloom (Fig. 4b).

The DMS concentrations in the surface waters ranged from 8.38 to 25.82 nmol L−1 in the first cruise, with an average of 15.43 nmol L−1. In the second cruise, the DMS concentrations were in the range of 8.00 to 41.03 nmol L−1 with an average of 21.63 nmol L−1. The vertical distributions of DMS decreased gradually with depth, and the DMS 8

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e Fig. 3. (continued)

after the bloom, respectively, averaging 34.08 and 147.03 nmol L−1. The vertical distribution of AA showed a gradual decrease with depth, and the AA concentrations in all layers from the second cruise were far higher than those from the first cruise, which reflected the patterns observed in the DMS and DMSPd concentrations. While, the horizontal distributions of AA were different in all three layers during the late bloom, after the bloom, the high values appeared in the southern range of the investigation area in all water layers, which corresponded to the observed DMSPt and DMSPd distributions (Fig. 4d).

concentrations in all layers from the second cruise were higher than those from the first, which reflected the pattern of DMSPd concentrations. Horizontal distributions of DMS in the surface water revealed high concentrations in the coastal waters and the western region. Relatively high DMS concentrations were also observed in the southwest range of the investigation area in both the middle and bottom layers (Fig. 4c). The AA concentrations in the surface water had ranges of 5.09–264.76 and 24.38–465.79 nmol L−1 during the late bloom and 9

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Table 2 Ranges and means (in brackets, n = 14) of biogenic sulfur productions during the Ulva prolifera late bloom and after the bloom in the coastal waters of Qingdao. Parameters

Cruises

Surface layer

Middle layer

Bottom layer

DMS (nmol L−1)

July

DMSPt (nmol L−1)

July

DMSPd (nmol L−1)

July

AA

July

8.38–25.82 (Average: 15.43) 8.00–41.03 (Average:21.63) 34.43–110.89 (Average: 67.83) 10.36–113.09 (Average:49.79) 3.66–21.70 (Average:10.48) 7.74–73.16 (Average:22.89) 5.09–264.76 (Average:34.08) 24.38–465.79 (Average:147.03)

3.67–34.78 (Average:12.47) 2.52–41.52 (Average: 17.96) 28.27–72.75 (Average:47.39) 15.64–116.72 (Average:54.78) 2.87–18.93 (Average:7.88) 3.00–39.90 (Average:19.20) 0.80–66.15 (Average: 15.43) 19.46–176.88 (Average:92.90)

1.86–15.26 (Average:5.15) 2.15–24.49 (Average:9.61) 8.58–45.97 (Average:28.40) 7.00–75.92 (Average:22.70) 3.55–15.89 (Average:7.57) 3.79–35.05 (Average:18.18) 0.46–34.59 (Average:14.26) 11.36–118.50 (Average:36.80)

(nmol L−1)

August

August

August

August

4. Discussion

influenced by terrestrial inputs (Liu et al., 2016). The dissolved AA concentrations in this study had a similar range to the Phaeocystis pouchetii bloom (Yang et al., 1994) and the Cryptomonas sp. bloom (Gibson et al., 1996) in the Antarctic, which ranged from 0.001 to 0.51 μmol L−1 and from not detectable to 1.20 μmol L−1, respectively. After the bloom, the concentration of DMSPt in the surface water began to decrease, which was consistent with the observations of Yang et al. (1994) during the Phaeocystis pouchetii bloom in the summer of 1988 and Gibson et al. (1996) during the Cryptomonas sp. bloom in the Antarctic in the summer of 1994 to 1995. However, DMSPd, DMS and AA concentrations after the bloom became obviously higher than those during the late-bloom period (P < 0.05, n = 14). Our results show that DMS and AA concentrations were different from those observed during the Antarctic bloom (Gibson et al., 1996), which might be attributed to the different algal species. The microalga Cryptomonas sp. and Phaeocystis pouchetii were important producers of DMSP in the Antarctic bloom, while the macroalga U. prolifera was the main contributor to the high concentrations of dimethylated sulfur compounds in Qingdao coastal waters. Because DMSPd was released by the decaying U. prolifera, and then it was degraded into DMS and AA, the concentrations of DMS and AA remained high after the bloom and persisted for a while. However, concentrations of DMSPt were still higher than those of DMSPd and DMS, which implied that the U. prolifera also released a large amount of particulate DMSP in the process of decline and decay. The vertical profiles of all the sulfur compound concentrations during these two cruises exhibited decreasing trends with depth except the concentration of DMSPt, which was in accordance with the fact that U. prolifera mainly floated on the surface and biogenic sulfur compounds were released into the surface water. The DMSPt concentration in the middle layer after the bloom was higher than that during the late bloom, which was related to the decaying U. prolifera debris sinking during senescence, releasing more DMSP into the middle water layer. Gibson et al. (1996) also reported an increase in DMSPd and AA concentrations at 10 m depth during the Cryptomonas sp. bloom in the Antarctic.

4.1. Response of the sulfur system to the U. prolifera bloom Historical data of DMSP and DMS in the surface layer of the U. prolifera bloom region and its adjacent waters during spring-summer are shown in Table 3. The averages of DMSPt, DMSPd, and DMS were in ranges of 17.70–32.36, 5.23–9.76 and 3.80–5.64 nmol L−1, respectively. Comparing the data from this study with those obtained before the bloom or from adjacent waters, we can see that the concentrations of DMSPt, DMSPd, and DMS during the late bloom period were significantly higher than the historical data. Zhang et al. (2009) found that concentrations of DMSPt, DMSPd, and DMS were in the ranges of 13.49–30.36 (average: 21.83), 6.28–12.17 (average: 9.76) and 2.61–4.71 (average: 3.80) nmol L−1, respectively, in the surface layer of the same investigation region in May 2006. Using the data of Zhang et al. (2009) to represent initial concentrations before the U. prolifera bloom, the concentrations of DMSPt, DMSPd, and DMS during the late bloom were 3.1, 1.1 and 4.1 times higher than those before the U. prolifera bloom, respectively. Since the average concentration of Chl-a (0.10 μg L−1, range: 0.01–0.21 μg L−1) during the late bloom was far lower than that (1.12 μg L−1, range:0.62–1.82 μg L−1) of Zhang et al. (2009) before the bloom, the increased dimethylated sulfur compounds can be attributed to the biosynthesis by the macroalga U. prolifera. Van Alstyne (2008) also proposed that one of the most abundant metabolites from algae that form green tides was DMSP, which occurs in most species of Ulva. Thus, the vast biomass of U. prolifera in the YS were likely the source of the high concentrations of dimethylated sulfur compounds, similar to the Phaeocystis pouchetii bloom (Yang et al., 1994) in the summer of 1988 and the Cryptomonas sp. bloom (Gibson et al., 1996) in the summer of 1994 to 1995 in the Antarctic. Yang et al. (1994) reported that DMS concentrations ranged from 0.003 to 0.588 μmol L−1 and Gibson et al. (1996) observed variations in DMSP concentrations from not detectable to 2.47 μmol L−1 in polar waters during algal blooms. In the present study, dissolved DMS concentrations in surface seawater obtained during the late-bloom period (15.43 nmol L−1) and after the bloom (21.63 nmol L−1) were far higher than the global mean DMS concentration (2.4 nmol L−1) for surface seawater between 30°–40° N (Simó and Dachs, 2002). Throughout the study, dissolved AA concentrations during the late bloom (34.08 nmol L−1) and after the bloom (147.03 nmol L−1) were both higher than those from the adjacent area reported by Wu et al. (2017), who reported that the AA concentrations in the surface water of the East China Sea were in the range of 23.42–29.16 nmol L−1 in summer, 2015. However, it was lower than those observed in the YS and the Bohai Sea in November 2013, which ranged from13.8 to 352.8 nmol L−1, with an average of 42.2 nmol L−1, and were

4.2. Relationship between environmental parameters and the green bloom and the sulfur system The temperature and salinity during these two cruises were both within suitable ranges for the growth of U. prolifera (temperature: 15 to 30 °C, salinity: 16 to 40; Gao et al., 2014). The similar spatial-temporal patterns of temperature and salinity during the late bloom and after the bloom showed that the change in the sulfur system was related to either the stage of the green tide or the life history of U. prolifera. DMSP has been proposed to function as a precursor in an activated defense system in numerous species of temperate marine macroalgae and may 10

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generally contribute to the widespread success of the Ulvophyceae (Van Alstyne et al., 2001). Steinke and Kirst (1996) demonstrated that the cleavage of DMSP within the cell of marine macroalga Enteromorpha clathrata (Ulvales, Chlorophyta) by algal DMSP lyase may have contributed to the production of oceanic and atmospheric DMS. Moreover,

high values of DMSPt, DMSPd and AA appeared in the southern region of the bloom which could be attributed to relatively high seawater temperatures. This is because, as a gas, DMS has a strong relationship with temperature. DO in seawater is an important indicator of the biological growth

a Fig. 4. Horizontal distributions of DMSPt (a), DMSPd (b), DMS (c) and AA (d) (nmol L−1) in the surface layer (S), the middle layer (M) and the bottom layer (B) in July and August. 11

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b Fig. 4. (continued)

and water pollution. The entire study area was found to be rich in oxygen due to the fact that the coastal waters were well mixed by tidal currents (Qu et al., 2015). However, a drop in DO appeared late in the U. prolifera bloom. This drop may be due to the decrease in photosynthesis by U. prolifera, the increase in oxygen-consuming organisms,

and/or the oxidation of organic compounds. DO concentrations in the surface and middle layers were lower than those in the bottom layer after the bloom, suggesting that strong oxygen-consuming processes continued in the upper waters even after U. prolifera had disappeared from the study area. Thus, it is likely that a large quantity of bacteria 12

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c Fig. 4. (continued)

that decompose DMSP also were present at this stage, leading to the high levels of DMS and AA (Van Boekel et al., 1992; Brussaard et al., 1995). The low concentrations of Chl-a in waters (after removal of U. prolifera) during the bloom could be ascribed to the competition of U.

prolifera with microalgae for nutrients, the secondary metabolites secreted by U. prolifera through allelopathy (Van Alstyne et al., 2015), and/or the inhibition of microalgal photosynthesis by the U. prolifera cover. The average content of NO3-N and NO2-N in the surface waters (2.87 μmol L−1) during the late bloom was significantly lower than that 13

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d Fig. 4. (continued)

(3.89 μmol L−1) after the bloom (P < 0.05, n = 14). However, the mean content of NH4-N (8.53 μmol L−1) during the late bloom was higher compared with that (6.63 μmol L−1) after the bloom. DMSP is one of the best-studied allelochemicals and can inhibit the growth of microalga (Liu et al., 2014). Furthermore, DMSP can be broken down

into DMS and AA by algae and bacteria. With a noxious odor, DMS produced by the enzymatic cleavage of DMSP can damage the microalgae, and the produced AA or acrylate have antibiotic properties (Seiburth, 1960). Thus, DMSP or its breakdown products may also prevent fouling by bacteria and microalgae, which in turn may increase 14

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Table 3 History data of DMS and DMSP in the surface layer of U. prolifera bloom region and adjacent waters during spring-summer. Regions

Time

DMS/nM

DMSP/nM

References

Range

Average

Range

Average

DMSPt 13.49–30.36, DMSPd 6.28–12.17 DMSPp 4.33–36.09, DMSPd 2.85–19.73

DMSPt 21.83 DMSPd 9.76 DMSPp 17.50 DMSPd 9.22 (DMSPt 26.72) DMSPt 25.2 DMSPp 27.13 DMSPd 5.23 (DMSPt 32.36) DMSPt 28.25 DMSPp10.6, DMSPd 7.10 (DMSPt 17.70)

Qingdao coast

May 2006

2.61–4.71

3.80

YS

April 2006

1.78–12.75

5.42

YS and ECS South YS and ECS

April–May 2009 July 2011

1.18–12.6 0.63–41.19

4.91 5.30

DMSPt 5.47–73.7 DMSPp 6.23–207.73, DMSPd 1.38–27.23

YS and ECS YS

June–July 2006 Spring, 2007

1.79–12.24 1.50–8.67

5.64 3.93

DMSPt 13.98–44.93 DMSPp 4.14–21.2, DMSPd 2.13–18.6

the productivity of the macroalgae themselves. The higher concentrations of DOC in the upper waters demonstrated that more organic compounds were released into the seawater during the late U. prolifera bloom, including DMSP, which was consistent with the higher concentrations of DMSPt found in the surface layer. The higher concentration of DMSPd, DMS, and AA appeared after the bloom owing to a lag in dissolution and decomposition of particulate DMSP (Scarratt et al., 2000; Steinke et al., 2002). The settlement of dead U. prolifera debris also contributed to the comparatively higher concentration of DOC in the bottom layer. Due to the strong respiration by floating U. prolifera, CO2 was continuously released. The lowest pH occurred in the upper waters in July, indicating that an oceanic acidification phenomenon occurred in the late bloom period. Ocean acidification can affect marine microalgae, which can accelerate the production of climate-active trace gases such as DMS and various halocarbons (Webb et al., 2016). However, the responses of trace gases to elevated pCO2 are compound-, and therefore, species-specific (Hopkins et al., 2010; Li et al., 2018). The influence of oceanic acidification on macroalgae including U. prolifera remains to be clarified.

Zhang et al., 2009 Zhang et al., 2008 Yang et al., 2012 Zhang et al., 2014b Yang et al., 2011 Li et al., 2016a

efficiency of the microbial community in converting DMSP to acrylate. This finding was in line with that reported by Gibson et al. (1996) for the Antarctic bloom (0.35). Compared with the surface layer, the ratios of AA/(DMSP+AA) in the middle layer were lower, at 0.25 in the late bloom period and 0.63 after the bloom. However, in the bottom layer, high AA/(DMSP+AA) values during the late bloom were also observed, at 0.33. Moreover, the ratios of AA/(DMSP+AA) during the green tide were lower than those after the bloom, which might be attributed to the consumption of AA by an abundance of microorganisms during the bloom (Seiburth, 1960; Liu et al., 2016). 4.4. Sea-to-air flux of DMS and its implications In this study, the ranges and average fluxes obtained by the N2000 method were 9.86–32.26 (average: 18.08) μmol m−2 d−1 in July and 8.73–47.77 (average: 24.24) μmol m−2 d−1 in August. The sea-to-air flux of DMS after the bloom was markedly higher than that during the late bloom (P < 0.05, n = 14), and during these two stages, the average flux was about three times higher than the previously reported average of 6.41 μmol m−2 d−1 from the YS (Zhang et al., 2008). The sea-to-air flux of DMS from coastal waters off Qingdao in the present study was also significantly higher than the global mean DMS sea-to-air flux of the 30°–40° N region (6.6 μmol m−2 d−1, Simó and Dachs, 2002). The total DMS released into the local atmosphere was somewhere between 204 and 274 kg S d−1 during the green tide bloom, based on the report that the green tide in coastal waters off Qingdao covered up to 182 km2 of the seawater surface on 16 July 2015 (www. ncsb.gov.cn/n1/n127/n139/n39/index_5.html). Thus, for the whole bloom area in the southern YS, the yearly contribution of DMS from the ocean to the atmosphere by U. prolifera was far higher than the flux value. Because more DMS was released into the atmosphere, the green tide may reduce the regional greenhouse effect by increasing the cloud cover via aerosol formation (Korhonen et al., 2008; Jarníková and Tortell, 2016). To better and more accurately understand the effect of green tides on the marine sulfur cycle, the temporal and spatial distributions of future green tide events need to be observed for the duration of the whole event. Besides floating U. prolifera, DMS release by U. prolifera that accumulates on beaches should also be investigated (Zhang and Wang, 2017).

4.3. Relationship among biogenic sulfur productions The ratios of DMS/(DMSP+DMS) were 0.19 and 0.30 in the surface water during the late bloom and after the bloom, respectively, suggesting that the cleavage of DMSP into DMS increased with time. In the middle layer, the ratio of DMS/(DMSP+DMS) during the late bloom (0.20) was similar to that of the surface water (0.19), moreover, the apparent degradation yields also increased from July (0.20) to August (0.25). These phenomena were consistent with the changes of DMS/ DMSP during a mesocosm experiment by Webb et al. (2016) and a laboratory-induced phytoplankton bloom by Zubkov et al. (2004). The ratios in the bottom layer were 0.15 and 0.30 during the late bloom and after the bloom, respectively, showing high production of DMS even after the bloom. As bacteria and phytoplankton may be significant contributors to DMS production from DMSPd during blooms in the field (Stefels and van Boekel, 1993; Scarratt et al., 2000), we also calculated the ratio of DMS/(DMSPd+DMS). The values were 0.61, 0.60, and 0.37 in the surface, middle and bottom layers in July, respectively, and they decreased to 0.49, 0.48, and 0.34 in August, which was consistent with decreasing amounts of bacteria or phytoplankton after the bloom. Furthermore, the apparent production yields of DMS from DMSPd were not obviously different between the surface and middle waters (P > 0.05, n = 14). The ratios of AA/(DMSP+AA) were 0.33 and 0.75 in the surface water during the late bloom and after the bloom, respectively, which were much higher than the ratios of DMS/(DMSP+DMS), reflecting the

5. Conclusions During the late U. prolifera bloom in the YS, high concentrations of DMSP, DMS, and AA in coastal waters off Qingdao were observed, which were released by a large number of decaying U. prolifera. The release continued for a period of time after the bloom and resulted in significantly higher DMSPd, DMS, and AA concentrations than those during the late bloom period, albeit, the concentration of DMSPt in the 15

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surface water began to decrease. High concentrations of DMSPd, DMS, and AA, but not DMSPt, emerged in the upper water column after the bloom as the decaying U. prolifera debris settled. The sea-to-air fluxes of DMS during the late bloom and after the bloom were about three times higher than the previously reported average for the YS. The considerable amounts of released DMS may diminish the regional greenhouse effect to some extent by forming cloud condensation nuclei. To better assess the impact of such U. prolifera blooms on the sulfur cycle, continuous in situ monitoring on larger spatial and temporal scales is needed.

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CRediT authorship contribution statement Chun-Ying Liu:Conceptualization, Methodology, Writing - original draft.Gao-Bin Xu:Data curation, Investigation.Xue Deng:Data curation, Investigation.Hong-Hai Zhang:Writing - review & editing, Supervision.Tao Liu:Conceptualization, Methodology.Gui-Peng Yang:Writing - review & editing, Validation. Declaration of competing interest We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product that could be construed as influencing the position presented in the manuscript entitled. Acknowledgements The authors thank the captain and crews of the R/V ‘Haidiao 235’ for their help during the in situ investigation. This work was financially supported by the National Natural Science Foundation of China (Grant No. 41676065), the Fundamental Research Funds for the Central Universities (No. 201762032), and the National Key Research and Development Program of China (Grants No. 2016YFA0601301 and 2016YFC1402101). This is MCTL contribution No. 224. We thank the editor and two reviewers for their thoughtful feedback on the manuscript. References Brussaard, C.P.D., Riegman, R., Noordeloos, A.A.M., Cadée, G.C., Witte, H., Kop, A.J., Nieuwland, G., van Duyl, F.C., Bak, R.P.M., 1995. Effects of grazing, sedimentation, and phytoplankton cell lysis on the structure of a coastal pelagic food web. Mar. Ecol. Prog. Ser. 123, 259–271. https://doi.org/10.3354/meps123259. Dacey, J.W., Blough, N.V., 1987. Hydroxide decomposition of dimethylsulfoniopropionate to form dimethylsulfide. Geophys. Res. Lett. 14, 1246–1249. https://doi.org/10. 1029/GL014i012p01246. Deng, X., Liu, T., Liu, C.Y., Liang, S.K., Hu, Y.B., Jin, Y.M., Wang, X.C., 2018. Effects of Ulva prolifera blooms on the carbonate system in the coastal waters of Qingdao. Mar. Ecol. Prog. Ser. 605, 73–86. https://doi.org/10.3354/meps12739. Fletcher, R.T., 1996. In: Schramm, W., Nienhuis, P.H. (Eds.), Marine Benthic Vegetation: Recent Changes and the Effects of Eutrophication. Springer, pp. 7–43. https://doi. org/10.2307/2960587. Gao, G., Zhong, Z.H., Zhou, X.H., Xu, J.T., 2016. Changes in morphological plasticity of Ulva prolifera under different environmental conditions: a laboratory experiment. Harmful Algae 59, 51–58. https://doi.org/10.1016/j.hal.2016.09.004. Gao, S., Shi, X.Y., Wang, T., 2013. Variation of nutrient concentrations at the inshore coastal area of northern Jiangsu province and the occurrence of green tide caused by Ulva prolifera. Environ. Sci. 33, 2204–2209 (in Chinese). Gao, S., Fan, S.L., Han, X.R., Yan, L.I., Wang, T., Shi, X.Y., 2014. Relations of Enteromorpha prolifera blooms with temperature, salinity, dissolved oxygen and pH in the southern Yellow Sea. China Environ. Sci. 34, 213–218 (in Chinese). Gibson, J.A.E., Swadling, K.M., Burton, H.R., 1996. Acrylate and dimenthylsulfoniopropionate (DMSP) concentrations during an Antarctic phytoplankton bloom. In: Kiene, R.P., Visscher, P.T., Keller, M.D., Kirst, G.O. (Eds.), Biological and environmental chemistry of DMSP and related sulfonium compounds. Springer, Boston, MA. https:// doi.org/10.1007/978-1-4613-0377-0_19. Hopkins, F.E., Turner, S.M., Nightingale, P.D., Steinke, M., Bakker, D., Liss, P.S., 2010. Ocean acidification and marine trace gas emissions. Proc. Natl. Acad. Sci. U. S. A. 107, 760. https://doi.org/10.1073/PNAS.0907163107. Hu, C.M., He, M.X., 2008. Origin and offshore extent of floating algae in Olympic sailing area. EOS Trans. Am. Geophys. Union 89, 302–303. https://doi.org/10.1029/

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