Chemosphere 254 (2020) 126846

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Water conservancy project on the Yellow River modifies the seasonal variation of Chlorophyll-a in the

Xiaokun Ding a, b, Xinyu Guo a, b, Chao Zhang a, Xiaohong Yao a, c, Sumei Liu c, d, Jie Shi a, c, * Chongxin Luo a, Xiaojie Yu a, Yang Yu a, Huiwang Gao a, c, a Frontiers Science Center for Deep Ocean Multispheres and Earth System, and Key Laboratory of Marine Environment and Ecology, Ministry of Education of , Ocean University of China, 238 Songling Road, Qingdao, 266100, China b Center for Marine Environmental Studies, Ehime University, 2-5 Bunkyo-Cho, Matsuyama, 790-8577, Japan c Laboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China d Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education of China, Ocean University of China, 238 Songling Road, Qingdao, 266100, China highlights graphical abstract

We discussed Chl-a dynamics in the BHS using historical observations and a model. Chl-a exhibited two peaks in spring and autumn until 2002. Chl-a has exhibited one peak in spring-summer since 2002. Concentrations of Chl-a in spring- summer have increased by 56% since 2002. Water conservancy project on river induces the seasonal shift of Chl-a. article info abstract

Article history: The Water Sediment Regulation Scheme (WSRS) is a unique engineering measure that has been regularly Received 11 March 2020 performed to reduce reservoir sedimentation and increase the flood capacity of the Yellow River in China Received in revised form since 2002. As a side effect, the WSRS greatly increases the monthly input flux of nutrients to the Bohai 17 April 2020 Sea (BHS) in summer, potentially exacerbating eutrophication levels therein and subsequently affecting Accepted 18 April 2020 the growth of phytoplankton. However, its influence on the Chlorophyll-a (Chl-a) dynamics over the BHS Available online 23 April 2020 is still poorly understood. In this study, two approaches were adopted to investigate it: 1) long-term in- Handling Editor: Derek Muir situ observations and satellite-derived data of surface Chl-a were used to study its seasonal variations before and since 2002, and 2) one 1D physical-biological coupled model was developed to evaluate the Keywords: impact of WSRS on seasonal Chl-a. The results showed that the surface Chl-a exhibited two peaks in Chlorophyll-a spring and autumn until 2002, but has exhibited only one peak in spring-summer since 2002. Satellite- Seasonal variation derived Chl-a concentrations in spring-summer since 2002 have increased by 56% compared to those Water Sediment Regulation Scheme until 2002. The simulated results showed that the change in Yellow River discharge induced by the WSRS Yellow River has resulted in the appearance of high concentrations of Chl-a in summer over the Central Bohai Sea Bohai Sea since 2002. The WSRS increased the ratio of added Chl-a owing to the riverine nutrients to total Chl-a by 19% compared to that until 2002. Overall, WSRS greatly affects the seasonal cycling of Chl-a in the Bohai Sea, and the side effect needs to be considered. © 2020 Elsevier Ltd. All rights reserved.

* Corresponding author. Frontiers Science Center for Deep Ocean Multispheres and Earth System, and Key Laboratory of Marine Environment and Ecology, Ministry of Education of China, Ocean University of China, 238 Songling Road, Qingdao, 266100. China. E-mail address: [email protected] (H. Gao). https://doi.org/10.1016/j.chemosphere.2020.126846 0045-6535/© 2020 Elsevier Ltd. All rights reserved. 2 X. Ding et al. / Chemosphere 254 (2020) 126846

1. Introduction influence of WSRS on the growth of phytoplankton over the BHS. With regard to the main pigment of phytoplankton, The coastal seas are one of the most important areas of the Chlorophyll-a (Chl-a) is considered an essential indicator or index world’s oceans from a human perspective (Jickells, 1998). Although of phytoplankton biomass (Cullen, 1982), and hence reflects the they account for only ~7% of the surface area and ~0.5% of the oceanic primary production (Bierman et al., 2011). In the BHS, the volume of the global oceans, coastal seas play a disproportionately Chl-a concentration in the surface seawater has shown an large role in the marine primary production, remineralization, and increasing trend in recent decades as extra eutrophication (Fu et al., sedimentation of organic matter (Walsh, 1991; Gattuso et al., 1998; 2016; Zhang et al., 2017), but there is no consensus among the Muller-Karger et al., 2005; Chen et al., 2013). High nutrient loads, seasonal variations of Chl-a. Many early observations in the BHS especially from rivers, have an important impact on the ecosystem exhibited peaks of Chl-a in spring and autumn (e.g., Sun et al., 2003; dynamics in coastal seas (Zweifel et al., 1995; Lenhart et al., 1997; Li Wei et al., 2004). Previous studies demonstrated that the spring et al., 2007). bloom and secondary autumn bloom, which regularly occur in River discharge rich in nutrients has long been known to play a temperate coastal systems, resulted from the favorable light con- key role in coastal ecosystems, and is particularly important in ditions and high nutrients availability in spring and sufficient nu- closed areas (e.g., Cloern et al., 1983; Harding et al., 2016). Large- trients produced by the vertical mixing in autumn, respectively scale water conservancy projects on rivers such as dam building (Weisse et al., 1990; Zhang et al., 2006; Jakobsen and Markager, and river diverting may further influence the coastal ecosystem 2016). However, a higher Chl-a concentration in summer than in (e.g., Vitousek et al., 1997; Domingues et al., 2012). In the Black Sea, other seasons was frequently observed in recent years in the BHS damming on the Danube River caused a concomitant decrease in (Liu and Wang, 2013; Fu et al., 2016). We therefore expect that the the wintertime silicate concentration by more than 60% in central large amounts of nutrients loads owing to WSRS may contribute surface waters, thereby altering the phytoplankton composition significantly to the sharp increase in Chl-a during recent summers, from a diatom-based community to nonsiliceous forms (Humborg and consequently induce the seasonal shift over the BHS. et al., 1997). Similarly, damming on rivers resulted in decreased In this study, we specifically introduced the seasonal variation of phytoplankton biomass and the disappearance of cyanobacteria Chl-a over the BHS from 1998 to 2017 using in-situ observations blooms in the Mediterranean Sea (Ludwig et al., 2009; Domingues and satellite-derived data. In addition, we discussed the influence et al., 2012). With the construction of the Three-Gorges Dam on the of WSRS on the seasonal shift of Chl-a and evaluated the contri- Changjiang River, which is the largest dam in the world, the bution of riverine nutrients to the increase in Chl-a in the BHS using nutrient ratios and phytoplankton community in the East China Sea a physical-biological coupled model. This work emphasizes the changed owing to a sharp decrease in silicate in diluted water, important impact of a special human activity working on rivers simultaneously leading to a massive decrease in summer Chl-a and (WSRS) on the coastal ecosystem. primary production by ~76% and ~86%, respectively, in the broad coastal waters (Gong et al., 2006; Jiang et al., 2014; Zhou et al., 2. Materials and methods 2017a; Ding et al., 2019; Liu et al., 2019). In another manipulation, the large-scale river diversions on the lower Mississippi River 2.1. Study area induced a high Chl-a level and changes in the distribution and fi composition of sh during spillway opening in the deltaic Louisiana The BHS, located in the northwest Pacific, is a shallow shelf sea (Das et al., 2012; Roy et al., 2013; Riekenberg et al., 2015). with an average depth of 18 m and a total area of 7:7 104 km2 There is growing concern about the ecological response over (Fig. 1). It is connected to the through the Bohai Strait. coastal seas with regard to water conservancy projects on rivers. The sea can be divided into five subregions based on geographical The Yellow River, which is the second largest river in China, location: Liaodong Bay, , , Coast, provides an ideal case for investigating the coastal ecological and the Central Bohai Sea. response to variations in the riverine input associated with human activity. The Yellow River accounts for more than 75% of the total river discharge to the Bohai Sea (BHS), which is a typical semi- 2.2. In-situ and satellite data enclosed sea in the northwest Pacific(Liu and Yin, 2010). Since 2002, the Yellow River Conservancy Commission has carried out Lots of in-situ observations in recent decades were collected the Water Sediment Regulation Scheme (WSRS) at the beginning of from historical materials, including monthly Chl-a, dissolved inor- every flood season (generally in June or July). Different from ganic phosphorus (DIP), and river discharge (see Text S1 for details damming and diverting, WSRS has been regularly performed to of data source). Comparisons of the in-situ Chl-a over recent de- reduce reservoir sedimentation and increase the flood capacity of cades were fairly rough owing to the inconsistent observation times the Yellow River by artificially altering the river flow with several and stations. We further analyzed the seasonal variation of Chl-a large reservoirs (Yu et al., 2013). WSRS causes high monthly water over the BHS using satellite-derived data from 1998 to 2017 (see discharge and sediment load that occur at least two months prior to Text S2 in detail of data source). the normal high flow month (Liu, 2015) and accounts for ~40% of the annual nutrients flux into the sea (Wu et al., 2017a). WSRS af- 2.3. Physical-biological coupled model fects the nutrients balance and the seasonal variability of phyto- plankton distribution within the Yellow River estuary, and also A vertical 1D physical-biological coupled model was imple- promotes the spread of nutrients to the south Central Bohai Sea (Liu mented to analyze the impact of the Yellow River input on Chl-a in et al., 2012; Wang et al., 2017). Many other studies about the long- the Central Bohai Sea (Fig. 1), with a total area of 2.9 104 km2 and term and proximate influence of WSRS on the BHS have also been an average depth of 22.5 m. The model is composed of a hydro- conducted, including the impacts on morphology and hydrody- dynamic module and a biological module, which were described in namics (Bi et al., 2014a; Xu et al., 2016), the shift in the salinity detail by Text S3. To understand the influence of WSRS on the distribution pattern (Mao et al., 2008; Wang et al., 2011), and the Central Bohai Sea, the nutrients carried by the Yellow River to the distribution and transport of trace elements (Bi et al., 2014b; Hu sea were considered as the only exogenous nutrients source in the et al., 2015). However, there is no specific research about the model. As shown in Fig. 2, the nutrients fluxes exhibited X. Ding et al. / Chemosphere 254 (2020) 126846 3

Fig. 1. (a) Location of the Bohai Sea, and (b) map of study area and bathymetry (contour lines, units in meters). The sea is divided into five subregions by white dashed lines: Liaodong Bay (LDB), Qinhuangdao Coast (QHD), Bohai Bay (BHB), Laizhou Bay (LZB), and Central Bohai Sea (CBS). Blue solid lines represent three largest rivers into the sea. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Fig. 2. (a) Monthly mean fresh water discharge from Yellow River during 1998e2017. Green, red, and blue circles represent June, July, and August, respectively. (b) Monthly nu- trients flux carried by Yellow River into the sea. Four nutrients are dissolved organic phosphorus (DOP), dissolved inorganic phosphorus (DIP), dissolved inorganic nitrogen (DIN), and particulate phosphorus (PP). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) 4 X. Ding et al. / Chemosphere 254 (2020) 126846

autumn, and winter were 1.02, 0.71, 1.11, and 0.83 mg,m3, respectively. Since 2006, Chl-a has seen an obvious increase in spring and summer with multiyear mean values of 3.02 and 3.39 mg,m3, respectively. Further, Chl-a in autumn and winter has somewhat increased with multiyear mean values of 1.89 and 1.18 mg,m3, respectively. The Chl-a concentration in the summer of 2016 over the Central Bohai Sea was also at a high level with the mean value of ~2.5 mg,m3 (Wang et al., 2018a). Additionally, the limited observations in the BHS indicated that Chl-a in the summer of 2002 had also been at a high level (~2.1 mg,m3) and exhibited higher concentrations than all seasonal values until 2001 (Fig. 3). Moreover, coastal observations indicated that the mean concen- tration of Chl-a in the spring of 2002 was ~1.88 mg,m3 (Li et al., 2003, 2006; Cao et al., 2006), which was lower than that in sum- mer over the entire BHS (~2.1 mg,m3). Since previous studies showed a higher Chl-a in coastal areas than in offshore areas in the BHS (Fu et al., 2016; Zhang et al., 2017), we cannot expect high Chl-a in offshore areas in the spring of 2002. Consequently, Chl-a over the Fig. 3. Seasonal variations of Chl-a from in-situ observations (see Table 1 for details of data sources). entire BHS had a peak value in summer rather than in other seasons in 2002. Therefore, a shift in the seasonal pattern of Chl-a from the two peaks in spring and autumn to one peak in spring-summer has presumably occurred in the BHS since 2002. synchronous variation with the Yellow River discharge during Satellite-derived data with high temporal resolution were used e fl 1998 2017, and the monthly uxes of dissolved inorganic nitrogen to further analyze interannual and seasonal variations in Chl-a from (DIN) and particulate phosphorus (PP) were both two orders of 1998 to 2017. In this study, February, May, August, and November magnitude higher than the DIP and dissolved organic phosphorus are defined loosely as winter, spring, summer, and autumn, (DOP). For a spin-up, the model was integrated for 5 years as forced respectively. As shown in Fig. 4, Chl-a in four seasons exhibited no e by climatological surface forcing (1998 2017) and monthly nutri- obvious differences from 1998 to 2001, with all values around 2 ents input in 1998. Then, the model was integrated for 20 years mg,m3. This was inconsistent with the two peaks in spring and from 1998 to 2017 using the same surface forcing as in the spin-up autumn from in-situ observations. The relatively high concentra- and monthly nutrients input for these 20 years. tion of satellite-derived Chl-a in summer during 1998e2001 may be attributed to the higher Chl-a along the coastal areas compared 3. Results to that in spring (Fig. 5bec). Since 2002, Chl-a in spring and sum- mer has increased to 2.91 and 3.71 mg,m3 (on average), whereas 3.1. Seasonal trends of Chl-a in recent decades those in the other two seasons exhibited a slight decrease compared to those until 2002. The Chl-a concentrations in spring- From in-situ observations (Fig. 3) in the BHS, the concentrations summer have obviously declined after 2013, although they have of Chl-a exhibited higher values in spring and autumn than in remained higher compared to those in autumn and winter (Fig. 4). summer and winter until 2001 except in 1992e1993, when Chl-a In addition, the strength of seasonal fluctuation in Chl-a changed was at a low level with no obvious seasonal variation. Until 2001, with the seasonal shift. Here, we define one variable, the seasonal the multiyear mean concentrations of Chl-a in spring, summer, range of Chl-a (SRC), expressed as

Fig. 4. Seasonal variations of satellite-derived Chl-a from 1998 to 2017. Solid lines in different colors represent the four seasons, orange dashed line represents mean values of Chl-a in spring and summer, and magenta dashed line represents seasonal range of Chl-a (see equation (1) in text). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) X. Ding et al. / Chemosphere 254 (2020) 126846 5

Fig. 5. Spatial distribution of seasonal mean Chl-a from satellite-derived data. (a, e, i): winter, (b, f, j): spring, (c, g, k): summer, and (d, h, l): autumn. (aed): 1998e2001, (eeh): 2002e2017, (iel): Chl-a from 2002 to 2017 minus that in 1998e2001. (unit: mg,m3).

other areas during the four seasons (Fig. 5aed). Since 2002, peak ¼ SRC Chlmax Chlmin (1) Chl-a in the four seasons has been identified in summer over most areas, especially in Qinhuangdao Coast and Liaodong Bay, followed where Chlmax and Chlmin represent the maximum and minimum of by spring (Fig. 5eeh). Comparisons of Chl-a during the two periods the seasonal mean Chl-a, respectively. As shown in Fig. 4, the SRC exhibited a significantly increased Chl-a in summer, followed by fi · 3 has increased signi cantly with a mean value of ~2.2 mg m since spring, and a slight decrease in autumn and winter over the entire 2002 compared to that until 2002 (~0.4 mg·m 3). The increasing BHS (Fig. 5iel). This directly resulted in a shift in the seasonal trend of the SRC is similar to the trend of Chl-a during summer, pattern of Chl-a. Meanwhile, the SRC for the multiyear average was indicating that the high Chl-a during summer is directly respon- lower than 1 mg,m3 in the entire BHS until 2002, but has since sible for the large SRC. exhibited an obvious increase with values higher than 2 mg,m3 (Fig. S6). 3.2. Spatial distribution of Chl-a in four seasons 3.3. Correlations between Chl-a and river discharge during summer Spatial variations of Chl-a often exist as a common phenomenon in the BHS (Fu et al., 2016; Zhang et al., 2017). Here, the spatial There are more than 40 rivers flowing into the BHS (Liu and Yin, distributions of Chl-a in four seasons before and since 2002 were 2010) that add large amounts of nutrients, thereby promoting the analyzed using the satellite-derived data. As shown in Fig. 5, the growth of phytoplankton. We chose the three largest rivers (Yellow coastal Chl-a exhibited higher concentrations compared to those in River, Haihe River, and Liaohe River) to analyze the correlation central areas. Until 2002, there was a weak bloom during spring in between the mean river discharge during summer (from June to the southwest of the Central Bohai Sea, where Chl-a in other sea- August) and the mean Chl-a concentration in August over the BHS sons were all at a low level (Fig. 5aed). In addition, Chl-a in the from 1998 to 2017. As shown in Table 1, there was a good correlation coastal areas of the BHS exhibited relatively high values than the between Chl-a in the Central Bohai Sea and the Yellow River 6 X. Ding et al. / Chemosphere 254 (2020) 126846

Table 1 agreement with the interannual trend of Yellow River discharge Correlation coefficients (r) between Chl-a (satellite-derived data) and river during summer (Fig. 2a), implying that WSRS shifted the seasonal discharge during summer in the Bohai Sea from 1998 to 2017. Five subregions: pattern of Chl-a in the Central Bohai Sea by loading a large amount Central Bohai Sea (CBS), Bohai Bay (BHB), Laizhou Bay (LZB), Qinhuangdao Coast (QHD), and Liaodong Bay (LDB). of nutrients in summer. The response of Chl-a and primary pro- duction in the Central Bohai Sea to the monthly river discharge CBS BHB LZB QHD LDB Bohai Sea from June to August were quantitatively estimated using linear Yellow River 0.82* 0.54* 0.26 0.71* 0.63* 0.76* regression (Fig. 6b-6c). As represented by the slope of linear Haihe River 0.11 0.02 0.18 0.05 0.21 0.10 * * * * * regression, the monthly concentrations of Chl-a and primary pro- Liaohe River 0.58 0.21 0.53 0.59 0.71 0.65 3 Total 0.80* 0.40 0.39 0.69* 0.63* 0.75* duction can respectively increase by 0.04 mg Chl-a m and 3.19 mg C m 2 d 1 per 108 m3 of freshwater into the BHS. Using *p < 0.05. such regression relations, the contributions of Yellow River

discharge to Chl-a (Chl AEi) and primary production (PP AEi) in the discharge (r ¼ 0.82). In addition, a good correlation between Chl-a Central Bohai Sea were estimated as follows: in the Liaodong Bay (Qinhuangdao Coast) and Liaohe River (Yellow : ¼ 0 04 Ri; River) discharge was exhibited. However, Chl-a in Laizhou Bay Chl AEi (2) exhibited little correlation with the Yellow River discharge, which Chli was probably affected by the numerously small rivers nearby and : nonpoint sources (Guo et al., 2017; Jiang et al., 2018). The significant ¼ 3 19 Ri; PP AEi (3) correlation of Chl-a in Laizhou Bay with the discharge of the Liaohe PPi River, which was far from Laizhou Bay, might result from the similar trends between the Liaohe River discharge and the terrestrial input where i represents the year from 1998 to 2017, Ri is the monthly around Laizhou Bay in summer. mean Yellow River discharge from June to August, and Chli and PPi represent the simulated monthly mean Chl-a and primary pro- duction from June to August in the Central Bohai Sea, respectively. 4. Discussion The calculated results indicated that WSRS had increased the contribution of Yellow River discharge to Chl-a (primary produc- Our results indicated that a sharp increase in Chl-a in summer tion) during summer in the Central Bohai Sea from 18±7% (14±6%) has been found since 2002, as well as a slight increase in spring, until 2002 to 37±15% (23±12%) since 2002. Consequently, WSRS which directly led to the seasonal shift (Figs. 3 and 4). Here, we plays an important role in the seasonal variation of Chl-a by directly mainly discuss the reason for the significant increase in the con- promoting the growth of phytoplankton during summer in the centration of Chl-a during summer in recent decades. Central Bohai Sea.

4.1. Direct influence of Yellow River discharge on Chl-a in summer 4.2. Long-term effect of Yellow River discharge on seasonal Since 2002, WSRS on the Yellow River has caused a high variation in Chl-a monthly water discharge and sediment load at least two months prior to the normal high-flow season (Liu, 2015). As shown in On the interannual scale, Chl-a in spring and summer display a Fig. 2a, the annual maximum water discharge began to appear in significant increasing trend in the BHS with p < 0.05 (Fig. 4). The summer instead of autumn since 2002. The low summer discharge percentage increases in spring and summer since 2002 have in 2003 occurred because WSRS was carried out in September of reached 42% and 69% (on average), respectively, leading to an that year (Wu et al., 2015). The decreased discharge after 2013 overall annual average of Chl-a increasing by 30%. As shown in might be attributed to the reduced days of WSRS, which was even Fig. 7, the Yellow River discharge during summer has been signifi- interrupted in 2016e2017 owing to the significant reduction of the cantly affecting the surface Chl-a within three months after total amount of sediment in the Yellow River (Wu et al., 2015; Chen entering the sea (lag 3 months, r > 0.44). The discharge in et al., 2019). Many studies have shown that the Yellow River summer of one year may also significantly affect Chl-a in the next freshwater flows northeastward during summer owing to the spring-summer period (lag ¼ 10e14 months, r > 0.44) and even the southeasterly wind (e.g., Wang et al., 2008; Wang et al., 2011). The third year (lag ¼ 20e26 months). The accumulation of nutrients nutrients carried by the river freshwater may promote the growth over time, which often exists as a common phenomenon in coastal of phytoplankton in the Central Bohai Sea, thereby exhibiting a seas (Nielsen et al., 2004; Neumann et al., 2018), might be good correlation between Chl-a and Yellow River discharge during responsible for the increasing trends of Chl-a. Since there is only summer (Table 1). Since the phytoplankton biomass in the Central one outlet (the Bohai Strait) connected to another water body (the Bohai Sea accounts for nearly half that in the BHS (Fig. S7), WSRS Yellow Sea), the water exchange is very weak with a renewal time likely plays an important role in the seasonal shift of Chl-a by of several years (1.1e5.2 years) in the BHS (Cai, 2013; Li et al., 2015; promoting the growth of phytoplankton during summer over the Li, 2017). Moreover, many studies emphasized that a significant Central Bohai Sea. fraction of the organic matter entering the coastal systems is A 1D physical-biological model was applied to examine the in- mineralized by the benthos, and only a small fraction is perma- fluence of Yellow River discharge on the seasonal variability of Chl- nently buried (Nixon and Pilson, 1983; Fennel et al., 2006). Hence, a in the Central Bohai Sea from 1998 to 2017. With the Yellow River the large amounts of nutrients carried by the Yellow River input as the only exogenous nutrients source, the model can suc- discharge in summer are difficult to remove completely from the cessfully reproduce the seasonal variation of the water temperature BHS in a short time. They may be stored as dissolved nutrients or and biological variables (see Text S4 on model validation). As particulate organic matter, thereby promoting the growth of shown in Fig. 6a, the simulated surface Chl-a exhibited two peaks in phytoplankton in a few weeks to several months and even longer. spring and autumn until 2002, but has since exhibited one peak in The relatively high Chl-a in spring-summer compared to that in spring-summer, indicating a shift in the seasonal pattern of Chl-a. other seasons in 2016e2017, when WSRS was interrupted, also The interannual variation of summer Chl-a was in good indicated nutrients accumulation in the BHS. X. Ding et al. / Chemosphere 254 (2020) 126846 7

Fig. 6. (a) Simulated monthly Chl-a in the Central Bohai Sea from 1998 to 2017, (unit: mg,m3); (b) Linear regression between the monthly Yellow River discharge and simulated Chl-a, and (c) primary production in the Central Bohai Sea during June, July, and August. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

(Song et al., 2016), exhibiting high Chl-a in these two areas (Fig. 5g). This is caused by the inputs of large amounts of nutrients from coastal runoffs, mariculture, shipping operations, and other human activities (Yuan et al., 2008; Wang et al., 2016; Cao et al., 2017). Seemingly, the quick-growing phytoplankton during summer in the Qinhuangdao Coast and Liaodong Bay, where abundant nutrients and phytoplankton may be transported into the other subregions by offshore current, have an important influence on Chl-a in the BHS. However, an extremely poor water exchange over the Qin- huangdao Coast and Liaodong Bay was found in comparison with other subregions (Li, 2014, 2017). There is an isolated cyclonic cir- culation around the cold pool in Liaodong Bay during summer (Fig. S5a) that can block the transport of nutrients and phyto- plankton to central areas as a retention system (Wei et al., 2003; Fig. 7. Correlation coefficients (r) between the Yellow River discharge during summer and the satellite-derived Chl-a concentration of different month delays after August of Zhou et al., 2017b). In addition, the slowly flowing southwestward that year in the Bohai Sea during 1998e2017. All data points represent values with water along the Qinhuangdao Coast has little offshore transport (Li, p < 0.05. Five subregions: the Central Bohai Sea (CBS), Bohai Bay (BHB), Laizhou Bay 2014). Therefore, the particularly high Chl-a during summer in (LZB), Qinhuangdao Coast (QHD), and Liaodong Bay (LDB). (For interpretation of the Liaodong Bay and Qinhuangdao Coast may have a weaker effect on references to color in this figure legend, the reader is referred to the Web version of this article.) the other subregions than the Yellow River diluted water, which can be transported to the Central Bohai Sea and even to the Qin- huangdao Coast by the northeastward flow (Wu et al., 2017b; Zhou et al., 2017b). In addition, many other factors such as light, tem- 4.3. Impact of other relevant factors on Chl-a in summer perature, atmospheric deposition, groundwater discharge, and mariculture may also affect the Chl-a concentrations as reported in In recent years, harmful algal blooms (HABs) have become more literatures (Thomas et al., 2012; Sempere et al., 2015; Andersen frequent over the Liaodong Bay and Qinhuangdao Coast in summer 8 X. Ding et al. / Chemosphere 254 (2020) 126846 et al., 2017; Liu et al., 2017; Shou et al., 2018; Wang et al., 2018b; summer owing to WSRS played a key role in the seasonal shift and Wang et al., 2019). Nevertheless, our results showed that they had fluctuations of Chl-a, whereas other factors might have little little effect on the increased Chl-a during summer in the BHS (see impact. The 1D physical-biological modeling results for the past 20 Text S5 in detail). years generally reproduced the observations in the Central Bohai Sea, where the phytoplankton biomass accounted for nearly half 4.4. Uncertainties in results that in the BHS. The modeling results show that the larger Yellow River discharge has resulted in the peak value of Chl-a in summer The greatest challenge in the analysis of interannual variability since 2002. The contribution of the river input to summer Chl-a using satellite data is the missing data owing to cloud coverage (He over the Central Bohai Sea increased by 19% (on average) fi et al., 2013). We calculated the daily rate of spatial coverage (Ratesc) compared to that until 2002. The signi cant correlations between during 1998e2017, which was expressed as the Yellow River discharge during summer and the Chl-a concen- trations in the following different months implied that the in- Nvalid fluences of WSRS on Chl-a may extend from a few weeks to several Ratesc ¼ 100%; (4) Nsum months and even longer. Water conservancy projects on rivers, which are widely used around the world, have exhibited consid- where Nvalid is the number of pixels with valid data over the BHS erable influence on the ecosystem in coastal seas and need to from the satellite data, and Nsum is the total number of pixels. As receive more attention. shown in Table S3, the number of days with high Ratesc (>50%) in the BHS exhibited a very low value (<10 days) in each month, Declaration of competing interest especially in June and July. The missing data on the daily scale in the BHS brings great difficulties in accurately assessing the effect of The authors declare that they have no known competing WSRS on Chl-a over the BHS. This work proved that the Yellow financial interests or personal relationships that could have River discharge into the sea during summer has greatly promoted appeared to influence the work reported in this paper. the growth of phytoplankton in the BHS since 2002. However, some inconsistent changes were found in the Central Bohai Sea, such as CRediT authorship contribution statement the low Chl-a but high river discharge during summer in 2004, 2012, and 2013 (Figs. 2a and 4). The nutrients flux from the river not Xiaokun Ding: Writing - original draft. Xinyu Guo: Writing - only depended on the river water discharge but also on the con- review & editing. Chao Zhang: Data curation. Xiaohong Yao: centrations of nutrients, which were considered to be invariant Methodology. Sumei Liu: Methodology, Resources. Jie Shi: Re- over time in this study owing to a lack of observation data. In sources. Chongxin Luo: Software. Xiaojie Yu: Resources. Yang Yu: addition, the southeasterly winds played a crucial role in driving Visualization. Huiwang Gao: Writing - review & editing. the Yellow River plume to extend northeastward into the Central Bohai Sea in summer (Wang et al., 2008). Decreasing wind speed Acknowledgements and changes in wind direction can also impede the movement of diluted water toward the central area. For instance, the winds This study is funded by the National Nature Science Foundation prematurely turned from southerly to northeasterly in August 2004 of China (41876125) and the NSFC-Shandong Joint Fund (U1806211, and 2012 (Fig. S12), which probably accounted for the relatively low U1606404). X. Ding thanks the China Scholarship Council (CSC) for concentration of Chl-a despite the high river discharge during those supporting his stay in Japan and the Ministry of Education, Culture, years. The riverine organic nitrogen may also play an important role Sports, Science and Technology, Japan (MEXT) to a project on Joint in biogeochemical cycle in coastal waters (Lee et al., 2017; Huang Usage/Research Center, Leading Academia in Marine and Environ- et al., 2018). Liu et al. (2020) provided a useful method to esti- mental Research (LaMer) for supporting his study in Japan. mate riverine organic matters fluxes for Chinese rivers. However, the nutrients limiting phytoplankton growth in the Bohai Sea have Appendix A. Supplementary data changed to phosphorus owing to the excessive nitrogen input since the 1990s (Wang et al., 2009; Xu et al., 2011). 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