Seasonal variability in dissolved oxygen in the Bohai Sea,China*

Yaozu CHEN , Fangguo ZHAI , Yanzhen GU ,**, Jing CAO , Cong LIU ,Xingchuan LIU , Zizhou LIU , Peiliang LI ,5

1 School of Marine Sciences, Sun Yat-Sen University, Zhuhai 519082, China

2 College of Oceanic and Atmospheric Sciences, Ocean University of China, Qingdao 266100, China

3 North China Sea Environmental Monitoring Center, State Oceanic Administration, Qingdao 266000, China

4 Institute of Physical Oceanography and Remote Sensing, Ocean College, Zhejiang University, Zhoushan 316021, China

5 Hainan Institute of Zhejiang University, Sanya 572024, China

Abstract Deoxygenation has frequently appeared in coastal ecosystems over the past century due to the joint inf luence of increasing anthropogenically induced nutrient inputs and global warming. The semi-enclosed Bohai Sea is a typical system that is prone to deoxygenation, with regular hypoxia events consistently recorded in recent decades. Based on in-situ observation data collected in large-scale voyage surveys in the Bohai Sea during 2008-2017, the seasonal variability in dissolved oxygen (DO) and its controlling mechanisms were studied. The results indicated that in spring and autumn, the DO distributions exhibited similar spatial patterns in the surface and bottom layers, while in summer, its spatial distribution was characterized by large-scale oxygen-poor zones distributed off the Qinhuangdao Coast and the central southern Bohai Sea in the bottom layer. The controlling mechanisms of the DO distribution varied from season to season. Spring and autumn DO distributions were dominated by the seawater temperature. Under the combined eff ects of stratif ication and decomposition, the summer bottom DO exhibited dual-core distribution. On the one hand, stratif ication could greatly impede vertical mixing, resulting in reduced bottom DO replenishment. On the other hand, the increased bottom organic matter intensif ied the decomposition processes, inducing massive DO consumption and elevated dissolved inorganic nitrogen concentrations. In addition, the stronger stratif ication might be the reason for the more severe deoxygenation in the southern oxygen-poor zones in summer. Our study provides guidance for an in-depth understanding of the DO seasonality in the Bohai Sea and the mechanisms that modulate it and for the improvement of hypoxia forecasts in ocean models.

Keyword: dissolved oxygen; seasonal variability; mechanism; the Bohai Sea

1 INTRODUCTION

Dissolved oxygen (DO) is an important factor inf luencing the stability of riverine and marine ecosystems. Hypoxia, which is characterized as the DO decreasing to a certain level that is unable to meet the DO demand, may lead to mass mortality,biodiversity reduction, and alterations of the community structure and the whole ecosystem (Diaz and Rosenberg, 1995; Rabalais and Turner, 2001).Nixon (1995) def ined the threshold of hypoxia as 2 mg/L, which has been widely used in many studies.Since the onset of the observation history of DO,hypoxia has been frequently detected in the world’s major coastal and estuarine ecosystems, together with a negative secular trend of DO (Diaz, 2001), which is likely to be caused by increasing nutrient inputs from land due to human activities (Anderson et al., 2002;Zhang et al., 2007; Danielsson et al., 2008; Diaz and Rosenberg, 2008; Halpern et al., 2008; Rabalais,2015). It has been suggested that global warming driven by greenhouse gases also reduces DO in seawater (Stramma et al., 2008; Solomon et al., 2009).On the other hand, a series of reactions such as denitrif ication or metal oxide reduction could occur in hypoxic water (Middelburg and Levin, 2009), which might generate greenhouse gases and promote global warming (Naqvi et al., 2010).

The Bohai Sea is a marine system vulnerable to bottom deoxygenation (Jiang et al., 2016). The Bohai Sea is a semi-enclosed shallow sea in northern China with an average depth of 18 m, and the Bohai Strait is the only channel through which it can exchange water with the northern Yellow Sea. The topography of the Bohai Sea is characterized by a shallow central ridge and a deep channel (Laotieshan Channel) in the northern Bohai Strait. Due to the inf luence of the East Asian monsoon, the prevailing surface wind direction is southeasterly wind in summer and northwesterly wind in winter, while the winter monsoon has a signif icantly larger magnitude. With increasing human activities, in recent years the Bohai Sea has become more vulnerable to marine environmental problems such as eutrophication and red tides (Song et al., 2016). According to Lin et al. (2008) and Zhang et al. (2016), red tides are likely to occur from May to September, with the highest frequency in June. Thus,our study is of great importance due to it further revealing the characteristics and intrinsic mechanisms of DO in the Bohai Sea.

Using discrete observation data, the mechanism of DO variations in the Bohai Sea has been discussed in previous studies (Jiang et al., 2016; Zhang et al.,2016; Zhao et al., 2017). However, these data rarely satisfy both temporal and spatial continuity. Only a small proportion of the data have both long-term time series and comprehensive spatial coverage.Nevertheless, previous studies have found that the bottom layer of the Bohai Sea is prone to deoxygenation in summer (Jiang et al., 2016; Zhao et al., 2017; Wei et al., 2019a), and there is some consensus on its mechanisms. Zhang et al. (2016) indicated that the blocking eff ect of stratif ication was the key mechanism for the generation of oxygen-poor zones, and the decomposition of organic matter was an important reason for the development of oxygen-poor zones and bottom acidif ication. Zhao et al. (2017) studied the DO distributions in the Bohai Sea in August 2014,suggesting that the DO distribution at the bottom was correlated with the water depth and the stratif ication and decomposition of organic matter. Wei et al.(2019a) proposed that in summer, the bottom layer of the Bohai Sea tended to form two oxygen-poor zones corresponding to cold pools, indicating that vertical stratif ication had a signif icant inf luence on the distributions of DO. In summary, the occurrence of summer oxygen-poor zones in the Bohai Sea is probably due to seasonal stratif ication, and the decomposition of bottom organic matter contributes to the development of bottom deoxygenation. In addition, some studies have suggested that the ocean circulation and the residence time of water column also inf luence the oxygen-poor zones of the Bohai Sea (Wang, 2009; Zhai et al., 2012). Ocean circulation transports water masses with diff erent properties,inf luencing the spatial distributions of temperature,salinity, or DO (Zhou et al., 2017). Moreover,circulation may indirectly aff ect DO by modulating the deposition of marine systems by inducing the aggregation and sedimentation of organic matter (Hu et al., 2011, 2013). Water columns with long residence times more easily suff er from hypoxia (Zhang et al.,2019).

Overall, studies concerning DO in the Bohai Sea have obtained considerable results and reached a consensus to some extent. However, the seasonal variability in DO and the controlling mechanisms in diff erent seasons are still unclear. Previous studies seldom involve long-term and large-scale DO variations. Due to the limited possible survey times,many studies have focused only on the summer of one year. Generally, the data of those studies were discrete,with poor tempo-spatial coverage. Studies concerning long-term observations have mainly focused on the Huanghe (Yellow) River estuary-Liaodong Bay transection, which has diffi culty displaying spatial variations. In addition, DO variations in spring and autumn are less studied and comprehensive studies should be performed to further uncover the seasonality of DO. Our study illustrates the spatial distributions of DO in each season in recent years (2008-2017).The observation data used in our study, which is introduced in Section 2.1, have high tempo-spatial continuity, meeting the need for a study of DO seasonality. This study aimed to display the seasonal variations in DO and to explore the potential mechanisms that modulate the variations to provide appropriate guidance for the development of marine activities in the Bohai Sea. In addition, this work will help optimize relevant ecological models, achieve more reliable hypoxia forecasting, and reduce the extent and number of disasters induced by hypoxia.

Fig.1 Topography of the Bohai Sea

2 MATERIAL AND METHOD

2.1 In-situ observation

In-situ observation data were collected by the North China Sea Environmental Monitoring Center,State Oceanic Administration. Large-scale voyage surveys were conducted in the spring (May), summer(August), and autumn (October) every year during 2008-2017. The survey stations were encompassed by our study area (Fig.1), covering the whole Bohai Sea. Notably, the spatial coverage of the stations was similar in each survey, with a minimum number of 37 stations (Table 1). The distributions of the stations in each survey are shown in Supplementary Figs.S1 &S2. The observed variables included the temperature,salinity, DO, and dissolved inorganic nitrogen (DIN).These variables were recorded in two layers, with the surface layer recorded 1 m under the free surface and the bottom layer recorded 2 m above the seabed.Water samples were taken by a multi-bottle CTD-type water sampler at the surface and bottom. The temperature and salinity were recorded by corresponding sensors, while DO and DIN were determined onboard by iodometric titration and spectrophotometry, respectively, using the collected water samples. In addition, DIN was used in our study since it occupies a high proportion of the total concentration of nutrients in the Bohai Sea. The DIN concentration was considered the sum of the NO3-N,NO2-N, and NH4-N concentrations, following Shi et al. (2009).

Table 1 The number of the stations during 2008-2017

2.2 Chlorophyll- a concentration

Monthly mean sea surface chlorophyll-aconcentration data used in this study were derived using the Moderate-Resolution Imaging Spectroradiometer(MODIS) from January 2008 to December 2017. The Level-3 Equidistant Cylindrical Mapped Image with a spatial resolution of 4.64 km×4.64 km was acquired from the U.S. National Aeronautics and Space Administration (NASA) website at https://oceandata.sci.gsfc.nasa.gov. The spatial range of the chlorophyllaconcentration data f its our study area, and the May,August, and October mean data were used when determining the climatological seasonal mean chlorophyll-aconcentration f ield.

2.3 Method

Due to the varying number of stations with high spatial coverage (Table 1) in each survey, it is necessary and reasonable to interpolate the in-situ observations to our study area. By applying convergent weighted-averaging interpolation (Barnes, 1964), all the observation data are interpolated to a 56×41 regular grid. The interpolation method is based on the Fourier integral, which can be applied in the practical form of

whereg(x,y) is the interpolated f ield determined by a reasonablervalue (radius of inf luence) and allMnumber of observations circled by it, andfjis thejthobservation within the radius of inf luence. The weight factorηcan be expressed asη=exp(-r2/4k), which is inf luenced by the distance between a data point and the grid point.kis a parameter determining the shape of the weight factor, which is calculated usingk=r2/16.We choose a wide range ofrvalues and calculated several two-dimensional f ields, e.g., temperature, as well as the corresponding mean absolute error (MAE)between the raw observations and the interpolated values. Then, the f ield with the minimum MAE(Supplementary Fig.S3) was selected as the best f ield for further analysis. Additionally, near-shore interpolations were removed to eliminate the marginal values with relatively high errors caused by the method.

Table 2 Statistical characteristics of the climatological seasonal mean DO f ield (mg/L)

According to García and Gordon (1992), the DO solubility equation can be represented as:

Ts=ln[(298.15-t)(273.15+t)-1],

whereO2Sis DO solubility,tis temperature andSis salinity. The rest of the parameters are constants(Supplementary Table S1) listed by García and Gordon (1992). Apparent oxygen utilization (AOU)is calculated using the observed temperature, salinity and DO, which can be expressed as:

whereO2Sis the DO solubility at equilibrium with the atmosphere.O2Orepresents the observed DO.

To quantify the stratif ication in the Bohai Sea in Section 4.2, the bottom-surface density gradient(Δρ/z)is calculated as an indicator of the stratif ication intensity following Wei et al. (2019a), which is determined by

whereΔρdenotes the diff erence between the bottom density (ρb) and surface density (ρs).zrepresents the depth. In fact, the density gradient here might be smaller than that in the stratif ied layers because the calculatedΔρ/zonly ref lects the mean state of stratif ication intensity between the surface and the bottom.

3 RESULT

3.1 Seasonality

Obviously, both the surface and bottom DO displayed strong seasonal variability (Fig.2). The concentrations of spring surface DO (Fig.2a) were higher in the northwestern Bohai Strait and the southeastern Liaodong Bay, displaying a tongue structure spreading from the northern Bohai Strait to Bohai Bay. For the bottom layer (Fig.2b) in spring, the bottom DO displayed nearly the same distribution as that of the surface, although it did not show an extended tongue structure, unlike the surface DO. The diff erence was clearly captured in Fig.2c, with a high-diff erence region (＞0.5 mg/L) located in the northeastern Huanghe River estuary. Additionally, some of the domains were covered by negative diff erences, such as the southern Bohai Strait, southern Liaodong Bay, and east of the Luanhe River estuary, although their absolute values were much lower (＜0.3 mg/L).

Surface and bottom DO distributions showed signif icant diff erences in summertime (Fig.2d-e). For the surface layer, there were three high-DO regions located in the northeastern Huanghe River estuary,the northwestern Bohai Strait, and the southeastern Liaodong Bay, which were similar to the distributions in the summer of 2014 presented by Zhao et al.(2017). Since these high-DO regions coincided well with the spring surface DO (Fig.2a), we assumed that the surface DO retained its spring structure until summer, accompanied by overall decreased magnitudes and weak spatial variability (note the smaller summertime statistical parameters relative to spring in Table 2). On the other hand, the summer bottom DO has been widely studied (Jiang et al.,2016; Zhang et al., 2016; Zhao et al., 2017; Wei et al.,2019a) because hypoxia is most likely to occur at the bottom in this season. Our results showed that summer bottom DO distributions (Fig.2e) presented a dualcore spatial pattern, with two distinct low-DO cores in the south and north. The low-DO regions spread from the southern trough to the northern trough,bypassing the central shoal. These distributions were also similar to those detected by Zhang et al. (2016),Zhao et al. (2017), and Wei et al. (2019a), suggesting that the summer bottom of the Bohai Sea was vulnerable to deoxygenation from 2008 to 2017.

Fig.2 Spatial distributions of DO in spring (a, b), summer (d, e), autumn (g, h), and corresponding surface-bottom diff erences(c, f, i)

Autumn DO (Fig.2g-h) showed the minimum spatial variability compared to the other seasons, with the smallest standard deviations (SDs) of 0.19 mg/L and 0.21 mg/L at the surface and bottom, respectively(Table 2). The surface DO in autumn was lower in the southwestern Bohai Strait and northeastern Huanghe River estuary, while it was higher in Liaodong Bay.By comparing Fig.2g-h, it could be found that the distributions of the surface and bottom DO in autumn were slightly diff erent. Specif ically, the DO values in the northwestern Bohai Strait were slightly lower at the bottom than at the surface, which is clearly depicted in Fig.2i as well (with diff erences larger than 0.3 mg/L). Nevertheless, the surface-bottom DO diff erences were small (＜0.1 mg/L) in most areas of the domain. The seawater was highly vertically homogeneous, indicating the strong vertical mixing in this season.

By computing the spatial mean values of each climatological seasonal mean DO f ield, the statistical characteristics of DO are given in Table 2 to show its general variations. From Table 2, obviously all statistical values (maximum, minimum, and mean)except the SD were the largest in the spring and smallest in the summer. By combining Table 2 with Fig.2, we found that the DO generally peaked in spring, and then decreased rapidly to its minimum in summer, and then, it f inally recovered in autumn.

3.2 Oxygen-poor zones

Fig.3 Frequency of the years when the summer bottom DO was less than 5 mg/L (a) and climatological summer bottom AOU (b)

The summer dual-core distributions in previous studies and our work both indicated that the summer bottom Bohai Sea deserves more attention because of its potential to experience hypoxia. We counted the years when the summer bottom DO was lower than 5 mg/L from 2008 to 2017. The resultant frequency distributions are shown in Fig.3, as well as the summer bottom AOU distributions. Obviously, the regions with high frequencies were coincident with the summer bottom DO (black isolines, also refer to Fig.2e). Simultaneously, these regions were covered by high AOU values, as well, suggesting drastic DO consumption in these regions. This phenomenon further demonstrated the high possibility of these regions suff ering from bottom deoxygenation. As shown in Fig.3, we considered the regions encompassed by the black isoline of 5.5 mg/L as the dual-core region in the subsequent analysis.

4 DISCUSSION

In general, previous studies of DO are based on discrete observations or ocean models, in which potential factors that aff ect DO variations are extensively discussed (Jiang et al., 2016; Zhang et al.,2016; Zhao et al., 2017). There are a series of factors aff ecting DO distributions in seawater, which can be approximately classif ied as physical and biochemical factors. The physical factors include seawater temperature, salinity, and stratif ication. Specif ically, a rise in temperature and salinity would reduce the solubility of DO in seawater, resulting in a decrease in DO (Carstensen et al., 2014; Schmidtko et al., 2017).In contrast to temperature, salinity exerts a weak inf luence on DO solubility (García and Gordon,1992). Additionally, the stratif ication and mixing process can also aff ect DO distributions by restraining/stimulating vertical water exchange (Obenour et al.,2012). On the other hand, biochemical factors mainly consist of photosynthesis, air-sea interactions, and the decomposition of organic matter. These factors are also considered the main sources or sinks of DO in seawater (Diaz, 2001; Zhao et al., 2017). In particular,the natural balance between the DO supply and consumption can be disequilibrated by eutrophication,which stimulates primary production and brings a large amount of organic matter to the subsurface,resulting in an increasing DO demand for the decomposition of organisms (Carstensen et al., 2014;Rabalais et al., 2014). The traditional view of the circulation pattern in the Bohai Sea is mainly based on discrete observations and does not have a consensus, causing diffi culties in researching the circulation and its impact on DO. Based on the study of Guan (1994), two cyclonic circulations are located in the northern and southern trough, and a basin-scale cyclonic circulation constitutes the summer circulation pattern of the Bohai Sea. Furthermore, since more than 80% of sedimentary organic matter in the central Bohai Sea comes from algae (Liu et al., 2015), these cyclonic circulations could induce the aggregation and sedimentation of organic matter, which would cause intensif ied decomposition at the bottom (Hu et al., 2011, 2013). Nevertheless, more observations are needed to accurately determine the real circulation patterns in the Bohai Sea and the resulting variable transport.

Based on in-situ observations and ocean models,previous studies have revealed that DO is inf luencedby diff erent factors, including temperature, salinity,stratif ication, circulation, wind, and biochemical processes (García and Gordon, 1992; Babin et al.,2004; Obenour et al., 2012; Zhao et al., 2017; Wei et al., 2019b). Furthermore, the dominant factors are variable among diff erent marine systems (Levin,2018). For the Bohai Sea, the modulation of DO is hard to explain by any single factor. In the following subsections, we focus on the main factors which include temperature, stratif ication, and biochemical factors, to explore the relationships between DO and these factors.

Table 3 The relative contributions of temperature and salinity on DO solubility

4.1 Sea water temperature

The temperature controls DO by physically aff ecting the DO solubility in seawater (Schmidtko et al., 2017). With increasing temperatures, the DO solubility drops, resulting in a reduced DO concentration. Based on a previous study, salinity has a much lower inf luence on DO than temperature(García and Gordon, 1992). We examined the relative contributions of temperature and salinity on DO solubility in the Bohai Sea. For the given mean temperature/salinity and the salinity/temperature change climatological seasonal f ield, we calculated the correlation coeffi cients between the raw DO solubility f ield (according to the equation of García and Gordon (1992)) and the solubility f ield computed with a f ixed temperature or salinity. Moreover, their SD ratios were calculated as well, which are shown in Table 3. Obviously, both the correlations and SD ratios are signif icantly higher with a f ixed salinity and varying temperature, further demonstrating that salinity has an almost negligible inf luence on DO solubility in the Bohai Sea. Thus, the salinity will not be subsequently discussed.

The correlation coeffi cients between the temperature and DO f ield (Fig.2) were calculated and are shown in Table 4 to evaluate the similarity of their distributions. By comparing the surface and bottom temperatures in the spring, we see that the bottom cold pool has formed in this season, and the dual-coreregion displays high temperature diff erences (Fig.4c),especially in the northern trough. In summer, previous studies have demonstrated that there are cold pools at the bottom of the Bohai Sea. Using observational data from large-scale surveys in diff erent years, Lin et al.(2006), Zhang et al. (2016), Zhao et al. (2017), and Wei et al. (2019a) captured nearly the same summer temperature spatial pattern, which is well reproduced in our work (Fig.4e). The summer surface-bottom temperature diff erences are strengthened compared to the spring temperature and display dual-core distributions. The similarity may imply the importance of the thermocline (or stratif ication), which will be discussed later. The autumn temperature distributions are similar at the surface and bottom, which reveal the smallest vertical diff erences, indicating that the seawater is vertically homogeneous in autumn.

Table 4 Correlation coeffi cients ( R) between climatological seasonal mean temperature and DO distributions

By comparing Fig.2 with Fig.4, we f ind that the DO distributions coincide well with the temperature in spring and autumn (note the highRvalues in Table 4). Specif ically, low (high)-DO regions correspond to high (low)-temperature regions,indicating that they are negatively correlated in spring and autumn. However, the summer temperature and DO distributions are not spatially correlated, withR=-0.32 andR=0.43 at the surface and bottom respectively, suggesting a decreased dominance of the temperature and, probably, other factors, such as stratif ication or biochemical processes, that modulate DO distributions. The strong connections in spring and autumn are also captured by the temperature-DO diagram (Fig.5), with signif icantly higher negative slopes in spring and autumn relative to those in summer. The slopes are comparable in these two seasons, with a minimum value of -0.16 mg/(L·℃).Although the summer temperature and DO did not display a close relationship, their corresponding surface-bottom diff erences showed similar spatial patterns (comparing Fig.4f with Fig.2f), withR=0.82.Consequently, by physically regulating DO solubility in seawater, the temperature dominates the seasonal cycle of DO in spring and autumn. The summer DO is probably mainly controlled by other processes, which will be discussed later.

Fig.4 Spatial distributions of the temperature in the spring (a, b), summer (d, e), autumn (g, h), and corresponding surfacebottom diff erences (c, f, i)

4.2 Stratif ication

It has been illustrated in Section 4.1 that the temperature has a poor correlation with DO in summer. However, the summer surface-bottom temperature diff erences display a close relationship with the summer bottom DO (or surface-bottom DO diff erences). Thus, we speculate that the thermocline inf luences summer bottom DO distributions by impeding vertical mixing of seawater. With the intensif ication of the thermocline, the vertical exchange of seawater will be further restrained,resulting in a reduced supply of DO from the surface to the bottom and thus aff ecting the bottom DO distributions. To conf irm whether the summer stratif ication in the Bohai Sea is dominated by temperature or salinity, the temperature/salinity is f ixed as its spatial mean value, while the salinity/temperature retains the original value. On this basis,the stratif ication intensity is computed and compared(Supplementary Figs.S4-S5). Using the algorithm(Δρ/z) explained in Section 2.3, the distributions of the stratif ication intensity are depicted in Fig.6. Upon comparing Supplementary Figs.S4-S5 with Fig.6b, it is obvious that the contributions of the temperature are signif icantly higher than those of the salinity,especially in dual-core regions. Consequently, the stratif ication is actually dominated by the temperature in the Bohai Sea.

Fig.5 Temperature-DO diagram of each season

The dual-core regions are much deeper than the Liaodong Bay, Bohai Bay, and Laizhou Bay, as well as the central shoal. Vertical water mixing in these regions is weaker due to its greater depth. With this background, as depicted in Fig.6, stratif ication begins to develop in dual-core regions because of intensifying solar radiation, although it is weak in this phase(＜0.07 kg/m4). Almost no stratif ication exists in shallow regions because of strong mixing. As summer arrives, the stratif ication has been highly strengthened in the dual-core region due to the strong solar radiation and weak summer monsoon, with a maximum of 0.11 kg/m4. Notably, the summer bottom DO (black isolines in Fig.6b) has almost the same spatial pattern as that of the stratif ication (R=-0.86 in Table 5),demonstrating the importance of stratif ication in the formation and development of summer bottom deoxygenation. As the stratif ication corrupts in autumn, the dual-core pattern disappears due to strong vertical mixing. Additionally, the correlation coeffi cient between the summer surface-bottom DO diff erences and stratif ication reaches 0.85, indicating that the spatial distributions of the summer bottom DO are probably dominated by stratif ication, i.e., the summer bottom DO decreases with the strengthening of stratif ication.

Concerning the relationship between the stratif ication and bottom DO (or surface-bottom DO diff erences), their scatter diagram is shown in Fig.6d.Obviously, high correlations are also revealed as shown in Fig.6b and Table 5. Specif ically, the linear regression shows that the bottom DO decreases with the strengthening of stratif ication, while the correlation between the stratif ication and surfacebottom DO diff erences is reversed, with relatively close absolute slopes of -21.57 and 23.22 (mg·m4)/(L·kg), respectively.

Fig.6 Distributions of the climatological seasonal mean stratif ication intensity (a, b, c) and diagrams of stratif ication-bottom DO and stratif ication-DO diff erence (d)

4.3 Biochemical processes

The biochemical processes that control DO variations mainly include photosynthesis and the decomposition of organic matter, which are considered important sources or sinks of DO in summer (Diaz,2001; Zhao et al., 2017). Generally, in the Bohai Sea,phytoplankton blooms appear in spring and the concentration of chlorophyllareaches its maximum in summer due to the strengthening of solar radiation and the rising seawater temperature. Moreover, spring blooms can provide a large amount of organic matter,resulting in intensif ied decomposition and consequent hypoxia in summer (e.g. Malone, 1987; Pomeroy et al., 2006). On the other hand, eutrophication also aff ects the decomposition of bottom organic matter in summer by intensifying photosynthesis in the euphotic zone, as Carstensen et al. (2014) and Rabalais et al. (2014) presented. Thus, in this section,we analyze the seasonal variations in the chlorophyllaand DIN concentrations and their impact on DO variations.

Table 5 Correlation coeffi cients ( R) between the distributions of the climatological seasonal mean stratif ication and DO f ield

4.3.1 Chlorophylla

Fig.7 Distributions of the climatological seasonal mean surface chlorophyll-a concentration derived from MODIS (a, b, c)and the saturation of DO (d, e, f)

The spatial distributions of chlorophyllashow distinct seasonal variability (Fig.7a-c). The spatial mean values of the chlorophyll-aconcentration are 4.71, 5.22, and 3.88 mg/m3in spring, summer, and autumn respectively. Consequently, the surface chlorophyll-aconcentration in the Bohai Sea is highest in summer, which is coincident with previous studies. Spring chlorophyllais relatively higher on the eastern Qinhuangdao Coast. The newly produced organic matter from spring is continually deposited on the bottom. As summer arrives, the regions with higher chlorophyll-aconcentrations expand to the whole dual-core region. By comparing the surface chlorophyll-aconcentration (Fig.7a-c) with the surface saturation of DO (Fig.7d-f), it is determined that the regions east of Bohai Bay are slightly oversaturated in spring and summer, only covering the southern part of the dual-core regions. In addition,the surface DO is also higher in the southern regions(note the black isolines of 9.5 mg/L in Fig.7a and 7.5 mg/L in Fig.7b). This phenomenon implies that as a source of DO, photosynthesis mainly inf luences the southern dual-core regions. On the other hand,considering the bottom DO distributions in summer,the growth and f lourishing of phytoplankton in the southern dual-core regions may provide more organic matter for the bottom, intensifying bottom decomposition. Under the combined eff ects of stratif ication and decomposition, deoxygenation appears at the bottom in summer. Notably, the chlorophyll-aconcentration is generally high in coastal regions in each season, where the seawater is vertically homogeneous. The concentration is also not spatially variable, with standard deviations of 0.83,1.04, and 0.48 mg/m3in spring, summer, and autumn,respectively. Nevertheless, further studies should be performed with accurate observations or models to quantify the relationship between chlorophyllaand DO.

4.3.2 DIN

Eutrophication may stimulate the primary production of phytoplankton in the spring, causing superabundant organic matter to be transported to the bottom in summer and resulting in an increased need for DO for the decomposition of those organic matter types (Carstensen et al., 2014; Rabalais et al., 2014).With the impedance of strong stratif ication in summer,the DO consumed at the bottom can barely be replenished by surface water, inducing hypoxia (Wei et al., 2019a). In the Bohai Sea, the spring DIN(Fig.8a-b) has similar distributions at the surface and bottom, with a higher DIN in Liaodong Bay, Bohai Bay, and Laizhou Bay. The summer bottom DIN distributions are noticeably diff erent compared to those of the surface. Although the summer bottom DIN (Fig.8e) does not seem higher in the dual-core regions, it does increase signif icantly in the regions relative to the surface DIN. The distributions of surface-bottom DIN diff erences (Fig.8f) are coincident with the dual-core region (the correlation coeffi cient between the surface-bottom DIN diff erences and the summer bottom DO reaches 0.85),as well as the distributions of the summer bottom AOU (R=-0.89, note the black isolines in Fig.8f). This phenomenon indicates that the bottom DIN may increase in summer due to the impedance of strong stratif ication and the strengthened decomposition of organic matter. In autumn, with the disappearance of stratif ication, the increased bottom DIN might rise to the surface through strong vertical mixing. Thus, the surface and bottom DIN (Fig.8g-h) in autumn are approximately equal, with little surface-bottom diff erences (Fig.8i).

Fig.8 Distributions of the climatological seasonal mean DIN in the spring (a, b), summer (d, e), autumn (g, h), and corresponding surface-bottom DIN diff erences (c, f, i)

To combine chlorophylla, DIN, and DO, Fig.9 shows the distributions of the climatological mean surface chlorophyll-aconcentration, surface-bottom diff erence of DIN, and bottom AOU in summer, with the distributions of the summer bottom DO superimposed (note the black isolines). As a result,we found that the surface chlorophyll-aconcentration(Fig.9a) was slightly higher in the dual-core regions,while the surface-bottom diff erences in DIN and AOU were signif icantly high in these regions. This spatial pattern in Fig.9b-c is also similar to the distributions of dissolved inorganic carbon (DIC)presented by Zhao et al. (2017). The signif icantly increased DIN and AOU in the dual-core regions suggest strong decomposition of organic matter and DO consumption. On the one hand, the organic matter newly produced by phytoplankton since spring is continually transported to the bottom layer,intensifying bottom decomposition. The process consumes more DO and generates more DIN. On the other hand, as summer arrives, the vertical exchange of water is blocked by strengthened stratif ication. As a result, the bottom DO is irreversibly consumed and high-DIN water is retained at the bottom.

In addition, to discover the diff erent mechanisms of the two oxygen-poor zones in summer, we separated the dual-core regions into two parts. The dual-core regions to the north and south of 39°N are def ined as the northern and southern cores, respectively. By computing the statistical mean values of the bottom DO, stratif ication intensity, bottom DO saturation,and bottom DIN in the two oxygen-poor zones in summer (Table 6), we f ind that DO in the southern core is slightly lower, with a diff erence of 0.063 mg/L.Meanwhile, the stratif ication seems stronger in the southern core, accompanied by a lower DO saturation and a higher DIN concentration. These results indicate that the southern oxygen-poor zone probably experiences more severe deoxygenation than the northern oxygen-poor zone under the combined eff ect of stronger stratif ication and bottom decomposition of organic matter. The stronger stratif ication further hinders vertical mixing, resulting in the greater consumption of DO and an increase in DIN concentration induced by bottom decomposition.

Fig.9 Distributions of the climatological mean surface chlorophyll- a concentration (a), surface-bottom diff erence of DIN (b),and bottom AOU (c) in summer

5 CONCLUSION

Using in-situ observation data collected in largescale voyage surveys, the seasonal variation in DO and its controlling mechanisms were studied. The results show that the surface and bottom DO distributions are similar in spring and autumn, with overall small surface-bottom diff erences. Temperature dominates DO variations in the two seasons but has a minimal eff ect in summer. The situation is diff erent at the bottom in summer, where the DO displays a dualcore spatial pattern, with two oxygen-poor zones located in the north and south of the Bohai Sea. This dual-core region has been demonstrated to be vulnerable to bottom deoxygenation. The analysis of the mechanisms showed that the summer bottom DO distributions are controlled by both stratif ication and bottom decomposition. On the one hand, stratif ication impedes vertical water exchange, restraining the replenishment of the bottom DO and the upward movement of high-DIN waters. On the other hand, the growth and f lourishing of phytoplankton may provide more organic matter for the bottom, resulting in strengthened bottom decomposition, a reduced DO and elevated DIN concentrations. Furthermore, the diff erences between the two oxygen-poor zones in the dual-core regions in summer were studied. The stronger stratif ication in the southern part of the dual-core regions might be the key factor that induces more severe bottom deoxygenation in the south.

Table 6 Statistical mean values of the variables in two oxygen-poor zones in summer

6 DATA AVAILABILITY STATEMENT

The in-situ observation data that support the f indings of this study are available from the North China Sea Environmental Monitoring Center, but restrictions are applied to the availability of these data, which were used under license for the current study and so are not publicly available. However, the data are available from the authors upon reasonable request and with permission from the North China Sea Environmental Monitoring Center.

The chlorophyll-aconcentration data that supports the f indings of this study is available from MODIS.The hyperlink of the data is: https://oceandata.sci.gsfc.nasa.gov.

7 ACKNOWLEDGMENT

We thank the anonymous reviewers and the editor for their valuable comments that helped greatly improve the manuscript.

ReferencesAnderson D M, Glibert P M, Burkholder J M. 2002. Harmful algal blooms and eutrophication: nutrient sources,composition, and consequences.Estuaries, 25(4): 704-726, https://doi.org/10.1007/BF02804901.

Babin S M, Carton J A, Dickey T D, Wiggert J D. 2004.Satellite evidence of hurricane-induced phytoplankton blooms in an oceanic desert.JournalofGeophysical Research:Oceans, 109(C3): C03043, https://doi.org/10.1029/2003jc001938.

Barnes S L. 1964. A technique for maximizing details in numerical weather map analysis.JournalofAppliedMeteorologyand Climatology, 3(4): 396-409, https://doi.org/10.1175/1520-0450(1964)003＜0396:ATFMDI＞2.0.CO;2.

Carstensen J, Andersen J H, Gustafsson B G, Conley D J.2014. Deoxygenation of the Baltic Sea during the last century.ProceedingsoftheNationalAcademyofSciences oftheUnitedStatesofAmerica, 111(15): 5628-5633,https://doi.org/10.1073/pnas.1323156111.

Danielsson Å, Papush L, Rahm L. 2008. Alterations in nutrient limitations—Scenarios of a changing Baltic Sea.Journal ofMarineSystems, 73(3-4): 263-283, https://doi.org/10.1016/j.jmarsys.2007.10.015.

Diaz R J, Rosenberg R. 1995. Marine benthic hypoxia: a review of its ecological eff ects and the behavioural response of benthic macrofauna.Oceanographyand MarineBiology, 33: 245-303.

Diaz R J, Rosenberg R. 2008. Spreading dead zones and consequences for marine ecosystems.Science, 321(5891):926-929, https://doi.org/10.1126/science.1156401.

Diaz R J. 2001. Overview of hypoxia around the world.JournalofEnvironmentalQuality, 30(2): 275-281, https://doi.org/10.2134/jeq2001.302275x.

García H E, Gordon L I. 1992. Oxygen solubility in seawater:better f itting equations.LimnologyandOceanography,37(6): 1307-1312, https://doi.org/10.4319/lo.1992.37.6.1307.

Guan B X. 1994. Patterns and structures of the currents in Bohai, Huanghai and East China Seas.In: Oceanology of China Seas. Springer, Dordrecht. p.17-26, https://doi.org/10.1007/978-94-011-0862-1_3.

Halpern B S, Walbridge S, Selkoe K A, Kappel C V, Micheli F,D'Agrosa C, Bruno J F, Casey K S, Ebert C, Fox H E,Fujita R, Heinemann D, Lenihan H S, Madin E M P, Perry M T, Selig E R, Spalding M, Steneck R, Watson R. 2008.A global map of human impact on marine ecosystems.Science, 319(5865): 948-952, https://doi.org/10.1126/science.1149345.

Hu L M, Lin T, Shi X F, Yang Z S, Wang H J, Zhang G, Guo Z G. 2011. The role of shelf mud depositional process and large river inputs on the fate of organochlorine pesticides in sediments of the Yellow and East China seas.GeophysicalResearchLetters, 38(3): L03602, https://doi.org/10.1029/2010GL045723.

Hu L M, Shi X F, Guo Z G, Wang H J, Yang Z S. 2013. Sources,dispersal and preservation of sedimentary organic matter in the Yellow Sea: the importance of depositional hydrodynamic forcing.MarineGeology, 335: 52-63,https://doi.org/10.1016/j.margeo.2012.10.008.

Jiang T, Xu Y, Liu C X, Zhang Y, Ding D S, Sun X M, Chen J F, Chen B J, Zhao J, Qu K M. 2016. Report on the occurrence of hypoxia in the Central Bohai Sea.ProgressinFisherySciences, 37(4): 1-6, https://doi.org/10.11758/yykxjz.20150618002. (in Chinese with English abstract)

Levin L A. 2018. Manifestation, drivers, and emergence of open ocean deoxygenation.AnnualReviewofMarine Science, 10: 229-260, https://doi.org/10.1146/annurevmarine-121916-063359.

Lin F A, Lu X W, Luo H, Ma M H. 2008. History, status and characteristics of red tide in Bohai Sea.Marine EnvironmentalScience, 27(S2): 1-5, https://doi.org/10.3969/j.issn.1007-6336.2008.z2.001. (in Chinese with English abstract)

Lin X P, Xie S P, Chen X P, Xu L L. 2006. A well-mixed warm water column in the central Bohai Sea in summer: eff ects of tidal and surface wave mixing.JournalofGeophysical Research:Oceans, 111(C11): C11017, https://doi.org/10.1029/2006jc003504.

Liu D Y, Li X, Emeis K C, Wang Y J, Richard P. 2015.Distribution and sources of organic matter in surface sediments of Bohai Sea near the Yellow River Estuary,China.Estuarine,CoastalandShelfScience, 165: 128-136, https://doi.org/10.1016/j.ecss.2015.09.007.

Malone T C. 1987. Seasonal oxygen depletion and phytoplankton production in Chesapeake Bay: preliminary results of 1985-86 f ield studies.In: MacKiernan G ed.Dissolved Oxygen in the Chesapeake Bay. College Park:Maryland Sea Grant, Maryland, US. p.54-60.

Middelburg J J, Levin L A. 2009. Coastal hypoxia and sediment biogeochemistry.Biogeosciences, 6(7): 1273-1293, http://doi.org/10.5194/bg-6-1273-2009.

Naqvi S W A, Bange H W, Farías L, Monteiro P M S, Scranton M I, Zhang J. 2010. Marine hypoxia/anoxia as a source of CH4and N2O.Biogeosciences, 7(7): 2159-2190.

Nixon S W. 1995. Coastal marine eutrophication: a def inition,social causes, and future concerns.Ophelia, 41(1): 199-219, https://doi.org/10.1080/00785236.1995.10422044.

Obenour D R, Michalak A M, Zhou Y T, Scavia D. 2012.Quantifying the impacts of stratif ication and nutrient loading on hypoxia in the Northern Gulf of Mexico.EnvironmentalScienceandTechnology, 46(10): 5489-5496, https://doi.org/10.1021/es204481a.

Pomeroy L R, D’Elia C F, Schaff ner L C. 2006. Limits to topdown control of phytoplankton by oysters in Chesapeake Bay.MarineEcologyProgressSeries, 325: 301-309,https://doi.org/10.3354/meps325301.

Rabalais N N, Cai W J, Carstensen J, Conley D J, Fry B, Hu X P, Quiñones-Rivera Z, Rosenberg R, Slomp C P, Turner R E, Voss M, Wissel B, Zhang J. 2014. Eutrophicationdriven deoxygenation in the coastal ocean.Oceanography,27(1): 172-183, https://doi.org/10.5670/oceanog.2014.21.

Rabalais N N, Turner R E. 2001. Coastal Hypoxia:Consequences for Living Resources and Ecosystems.Coastal and Estuarine Studies. Vol. 58. American Geophysical Union, Washington, DC. 464p.

Rabalais N N. 2015. Human impacts on f isheries across the land-sea interface.ProceedingsoftheNationalAcademy ofSciencesoftheUnitedStatesofAmerica, 112(26):7892-7893, https://doi.org/10.1073/pnas.1508766112.

Schmidtko S, Stramma L, Visbeck M. 2017. Decline in global oceanic oxygen content during the past f vie decades.Nature, 542(7641): 335-339, https://doi.org/10.1038/nature21399.

Shi H M, Wang L S, Shi X Y. 2009. The seasonal composition and distribution characteristics of dissolved inorganic nitrogen of North Yellow Sea.PeriodicalofOcean UniversityofChina, 39(S1): 207-211, https://doi.org/10.16441/j.cnki.hdxb.2009.s1.040. (in Chinese with English abstract)

Solomon S, Plattner G K, Knutti R, Friedlingstein P. 2009.Irreversible climate change due to carbon dioxide emissions.ProceedingsoftheNationalAcademyof SciencesoftheUnitedStatesofAmerica, 106(6): 1704-1709, http://doi.org/10.1073/pnas.0812721106.

Song N Q, Wang N, Lu Y, Zhang J R. 2016. Temporal and spatial characteristics of harmful algal blooms in the Bohai Sea during 1952-2014.ContinentalShelfResearch,122: 77-84, https://doi.org/10.1016/j.csr.2016.04.006.

Stramma L, Johnson G C, Sprintall J, Mohrholz V. 2008.Expanding oxygen-minimum zones in the tropical oceans.Science, 320(5876): 655-658, https://doi.org/10.1126/science.1153847.

Wang B D. 2009. Hydromorphological mechanisms leading to hypoxia off the Changjiang estuary.Marine EnvironmentalResearch, 67(1): 53-58, https://doi.org/10.1016/j.marenvres.2008.11.001.

Wei Q S, Wang B D, Yao Q Z, Xue L, Sun J C, Xin M, Yu Z G.2019a. Spatiotemporal variations in the summer hypoxia in the Bohai Sea (China) and controlling mechanisms.MarinePollutionBulletin, 138: 125-134, https://doi.org/10.1016/j.marpolbul.2018.11.041.

Wei Q S, Yao Q Z, Wang B D, Xue L, Fu M Z, Sun J C, Liu X H, Yu Z G. 2019b. Deoxygenation and its controls in a semienclosed shelf ecosystem, northern Yellow Sea.JournalofGeophysicalResearch:Oceans, 124(12): 9004-9019, https://doi.org/10.1029/2019JC015399.

Zhai W D, Zhao H D, Zheng N, Xu Y. 2012. Coastal acidif ication in summer bottom oxygen-depleted waters in northwestern-northern Bohai Sea from June to August in 2011.ChineseScienceBulletin, 57(9): 1062-1068,https://doi.org/10.1007/s11434-011-4949-2.

Zhang H, Li Y F, Tang C, Zou T, Yu J, Guo K. 2016. Spatial characteristics and formation mechanisms of bottom hypoxia zone in the Bohai Sea during summer.Chinese ScienceBulletin, 61(14): 1612-1620, https://doi.org/10.1360/N972015-00915.

Zhang W X, Wu H, Hetland R D, Zhu Z Y. 2019. On mechanisms controlling the seasonal hypoxia hot spots off the Changjiang River Estuary.JournalofGeophysical Research:Oceans, 124(12): 8683-8700, https://doi.org/10.1029/2019JC015322.

Zhang Y Y, Zhang J, Wu Y, Zhu Z Y. 2007. Characteristics of dissolved oxygen and its aff ecting factors in the Yangtze Estuary.EnvironmentalScience, 28(8): 1649-1654,https://doi.org/10.13227/j.hjkx.2007.08.033. (in Chinese with English abstract)

Zhao H D, Kao S J, Zhai W D, Zang K P, Zheng N, Xu X M,Huo C, Wang J Y. 2017. Eff ects of stratif ication, organic matter remineralization and bathymetry on summertime oxygen distribution in the Bohai Sea, China.Continental ShelfResearch, 134: 15-25, https://doi.org/10.1016/j.csr.2016.12.004.

Zhou F, Huang D J, Xue H J, Xuan J L, Yan T, Ni X B, Zeng D Y, Li J. 2017. Circulations associated with cold pools in the Bohai Sea on the Chinese continental shelf.ContinentalShelfResearch, 137: 25-38, https://doi.org/10.1016/j.csr.2017.02.005.